L0017 Houck 1994 Mites Ecological and Evolutionary Analyses of Life-History

Ecological and Evolutionary
Analyses of Life-History
Patterns
Edited by
MarilynA. Houck
SPRINGER-SCIENCE+BUSINESS MEDIA, B.V

© 1994 Springer Science+Business Media Dordrecht
Originally published by Chapman & Hall in 1994
Softcover reprint of the hardcover Ist edition 1994
All rights reserved. No part of this book may be reprinted or reproduced or utilized in
any form or by any electronic, mechanical or other means, now known or hereafter in-
vented, including photocopying and recording, or by an information storage or re-
trieval system, without permission in writing from the publishers.
Library of Congress Cataloging in Publication Data

Mites : ecological & evolutionary analyses of life-history patterns /
editor, Marilyn A. Houck.
p. cm.
Includes bibliographical references and indexes.
ISBN 978-1-4613-6012-4 ISBN 978-1-4615-2389-5 (eBook)
DOI 10.1007/978-1-4615-2389-5
I. Mites. 2. Mites-Evolution. 3. Mites-Adaptation. I. Houck,
Marilyn A.
QL458.M58 1993
595.4'2-dc20 93-18439
CIP
British Library Cataloguing in Publication Data available

DEDICATED
TO
Dr. Edward W. Baker
and
Dr. George W. Wharton
In Recognition of their Creativity and Life-long

Dedication to the Study of Mites
Contents
Foreword IX
Evert E. Lindquist
Preface Xlll
Marilyn A. Houck
Contributors xxi
CHAPTER I: Poecilochirus carabi: Behavioral and Life-History

Adaptations to Different Hosts and the Consequences of Geographical
Shifts in Host Communities.
Jonathan M. Brown and David Sloan Wilson
CHAPTER 2: Life-History Patterns of Hummingbird Flower Mites in

Relation to Host Phenology and Morphology. 23
Robert K. Colwell and Shahid Naeem
CHAPTER 3: Mites as Potential Horizontal Transfer Vectors of

Eukaryotic Mobile Genes: Proctolaelaps regalis as a Model. 45
Marilyn A. Houck
CHAPTER 4: Evolution of Life-History Patterns in the Phytoseiidae. 70

Maurice W. Sabelis and Arne Janssen
CHAPTER 5: Evolutionary Aspects of Oribatid Mite Life Histories

and Consequences for the Origin of the Astigmata. 99
Roy A. Norton
CHAPTER 6: Life-History Modifications in Astigmatid Mites. 136

Barry M. OConnor
vii
viii / Contents
CHAPTER 7: Life-History Patterns of Astigmatid Inhabitants of

Water-Filled Treeholes. 160
Norman J. Fashing
CHAPTER 8: The Evolution of Parasitism and the Distribution of

Some Dennanyssoid Mites (Meso stigmata) on Vertebrate Hosts. 186
Frank 1. Radovsky
CHAPTER 9: Evolution and Life-History Patterns of Mites Associated

with Bees. 218
George C. Eickwort
CHAPTER 10: Adaptation and Transition into Parasitism from

Commensalism: A Phoretic Model. 252
Marilyn A. Houck
CHAPTER 11: Cytogenetics of Holokinetic Chromosomes

and Inverted Meiosis Keys to the Evolutionary Success of Mites,
with Generalizations on Eukaryotes. 282
Dana L. Wrensch, John B. Kethley and Roy A. Norton
Index 345
Foreword
During the past two decades, we have come to realize that the Acari (mites
and ticks) rival the insects in their global diversity, abundance, and ubiquity. But
what we have yet to realize fully is the potential that this group of metazoans,
which are so individually minute, has in providing fresh insights about general
biological phenomena and in serving as experimental animals for formulating
and testing biological concepts.
The very attribute-small size-that previously impeded research on mites
has, with recent technological advances, come to be recognized as advantageous
in studying and using them experimentally. The advent of molecular techniques
(such as polymerase chain reaction) has overcome the limitation of tiny amounts
of substance available for analysis of individual mites. Their smallness also
correlates with: short generation time, ease in experimental replication, rapid
results, and minimal demands on space. As put so eloquently by Asher Treat in
his 1975 book, Mites of Moths and Butterflies, modern technology now permits
us to share with mites "the strange and beautiful world where a meter amounts
to a mile and yesterday was years ago."
Ecological and evolutionary concepts have been based predominantly on stud-
ies of vertebrates, vascular plants, a few groups of insects (e.g. Drosophila), and
selected unicellular organisms. This has led to a somewhat limited and distorted
set of generalities on how multicellular organisms adapt and evolve. The Acari
are one of a few relatively untapped assemblages (major groups of fungi and
crustacea also come to mind) that have almost endless potential as study subjects,
to contribute to the overall picture of the complexity and diversity of life now on
earth.
This assemblage is remarkable in being very ancient (with extant families
represented in the geological record at least as early as the middle Devonian), as
well as very disparate. The early presence of acarines enabled them to interact
and co-evolve dynamically with subsequent major ecological and evolutionary
ix
x ! Foreword
radiations of vascular plants, insects, and terrestrial vertebrates, in ways that still
continue. Attributes of mites such as the intricacies of their life cycles, the genetic
and ecological mechanisms that regulate their abundance and adaptability, and
the diversity of their physiological and behavioral adaptations, all provide unique
opportunities for exploring fundamental biological processes.
The ancestral Acari was a conservative assemblage of omnivores (predators-
fungivores) that stemmed from a predatory class of arthropods, the Arachnida.
Through time, however, mite diversification led to habitat and trophic expansion
in all manner of niches on land and in fresh and ocean waters, and the assemblage
now includes: microorganism filter feeders; fungal and algal grazers; parasites of
plants, vertebrates and invertebrates; and parasitoids, commensals and mutualists
of invertebrates. What are the attributes that have enabled the Acari, unlike other
arachnids, to achieve such unparalleled biological diversity beyond predation?
The answers lie among the attributes and patterns that have evolved in their life
histories and reproduction.
Based on life history studies of disparate groups of mites living in a variety of
habitats, the chapters in this book offer new data synthesized with previous
knowledge, which in some cases lead to startling views with broad evolutionary
impact. In its breadth and major significance to biological themes, one chapter
is salient in challenging a widely held cytogenetic paradigm that does not account
for the long-term evolutionary success of major lineages of thelytokous and
haplodiploid mites. Among sarcoptiform mites, there is strong evidence for a
large, long existent, and diverse group of thelytokous mites. Stranger still, is the
evidence for an evolutionary reversal to sexuality in a major lineage derived from
this group. Among trombidiform mites, there is much evidence for repeated
independent success in highly inbred clades of arrhenotokous mites. This chap-
ter's phylogenetic perspective on the cytogenetic mechanisms which underlie
such diversity of life history patterns is elegant in its apparent simplicity not only
for mites but for the general lineage of eukaryotic organisms. The prospects
highlighted for further research in this area are exciting indeed.
Among other chapters, some consider life history and concomitant reproductive
patterns in diverse and speciose lineages of Acari, including the Oribatida and
the Astigmata in the suborder Sarcoptiformes, and the Dermanyssoidea and
Phytoseiidae in the suborder Parasitiformes. Another is of similar breadth, but
deals with symbiotic assemblages of mites co-adapted with a species group of
invertebrate hosts, bees in this case. Still other chapters deal in depth with specific
examples of hosts, such as fruit flies and carrion beetles, or with particular
examples of habitats such as hummingbird-pollinated flowers and water-filled
treeholes. The latter are tremendously fascinating because they shed light on
phenomena of general biological interest, such as horizontal-transfer vectors of
transposable genes between species, and the all-encompassing effects of host-
plant morphology and phenology on virtually every aspect of the lives of f1ower-
inhabiting mites.
Foreword / xi
If readers bear in mind that the included chapters are but tidbits of an almost
endless buffet of similarly fascinating associations of mites with other organ-
isms-be they bracket fungi, insectivorous plants, hawk moth-pollinated flowers,
subcortical nematodes, intertidal mollusks and crustaceans, sawyer beetles, hon-
eybees, midges, odoriferous glands of coreid bugs, or the bodies and nests of
birds and mammals-they will realize that similarly intriguing and biologically
significant studies are theirs for the choosing. Ecological and evolutionary analy-
ses of life history patterns, among the many families of protelean parasitic water
mites co-adapted with their aquatic invertebrate hosts, await investigators with a
bent for freshwater ecosystems. And what on earth do we know of such patterns
among the diversity of halacarid mites that have, unlike insects, successfully
invaded the sea, including its very depths? Or of the peculiar, vennifonn nemata-
lycid mites that somehow do well in soil depths to 10 meters?
The answers to these and similar questions are basic to an eventual understand-
ing of the biodiversity that exists in any of the earth's ecosystems. The Acari
offer unique opportunities for investigating other biological phenomena relevant
to life history patterns, such as: heterochrony and paedogenesis, demographic
polymorphism, adaptations to terrestrial and aquatic ways of life, exploitation
of patchy environments, vector and hypervector relationships, specialist versus
generalist predators, and resource tracking versus host tracking in co adaptations
with fungi, plants, nematodes, insects, and vertebrate animals. Once we have a
perspective on the life history patterns of a greater diversity of organisms (includ-
ing mites), based on ecological and evolutionary analyses superimposed on a
phylogenetic background, we will then be in a better position to predict the ways
of living and interacting of organisms representing a total array of biodiversity.
There is, moreover, an applied ecological side to these studies. Findings such
as the horizontal transfer of genes between species, the effect of prey densities
on the evolution of sex mechanisms in predatory mites, and the cytogenetic
mechanisms underlying the haplodiploid sex-detennining systems characteristic
of the most highly adapted groups of phytophagous and predatory mites, have
significant implication to the field of integrated control of animal and plant pests.
Further, studies of the interaction and co adaptation of mites and ticks with
closely associated microorganisms is critical to understanding how they, and other
invertebrates, transmit diseases to plants and animals, and how mites in tum may
be controlled by microbial pathogens.
As indicated by the diverse backgrounds of the authors of this book, these
subjects appeal to the more general students of evolutionary biology as well as
to the more specialized (and increasingly few) students of acarology. As well,
they appeal to both collaborative, multidisciplinary approaches and individual
investigations. And that is precisely the intent of this book: (1) to provide a
stimulating source of infonnation and ideas gleaned from the ways of life of
mites; (2) to have these ideas pursued further by general ecologists, geneticists,
parasitologists, and evolutionary biologists as well as by specialists; and (3) to
xii I Foreword
link generalists to the increasingly extensive and exciting acarologicalliterature

relevant to their areas of interest.
EVERT E. LINDQUIST
Ottawa, Canada
April, 1993
Preface
The work on this dedication volume was begun in December, 1989, when the
Acarological Society of America (ASA) chose to publicly recognize Dr. Edward
W. Baker and Dr. George W. Wharton for their life-long contributions to the
science of Acarology. A Formal Conference/Acarological Symposium, dedicated
to Ed Baker and George Wharton, was held on the afternoon of December 10,
1989, in conjunction with the national Entomological Society of America meeting
at the Convention Center, in San Antonio, Texas. The program was entitled
Acari: Life History and Reproductive Patterns, and the participants included (in
order of original presentation): D. E. Johnston, D. L. Wrensch, M. Sabelis,
M. J. Kaliszewski (co-moderator), R. A. Norton, B. M. OConnor, N. J. Fashing,
R. K. Colwell, G. C. Eickwort, J. M. Brown and D. S. Wilson, and M. A.
Houck (organizer and co-moderator).
Coauthors (A. Janssen, J. B. Kethley, S. Naeem) joined the efforts during the
process of constructing the volume and F. J. Radovsky graciously agreed to round
out the perspective by contributing an additional (and much needed) chapter on
mammal associates. Regretfully, due to unforeseen circumstances, two original
contributions are not recorded here. The chapter on heterochrony in mites is
absent, due to an unresolvable scheduling conflict, and the chapter on the Evolu-
tion of Polymorphism in the Tarsonemina was not sufficiently developed to bring
it to completion at the time of the premature death of M. Kaliszewski on October
14, 1992. We regret that Marek's chapter could not appear in this volume and
acknowledge his contribution and influence on modem acarology.
Following the Symposium, a reception dinner was held for the honorees and
appropriate comments and goodwill were public ally offered by many. Leis were
hand-carried by an ASA member, Ms. Sabina Swift, from Hawaii and presented
to the two honorees and an exuberant and happy evening was shared by all.
Preston Hunter compiled, for a special issue of the ASA Newsletter (published
in November 1989), the major accomplishments of E. W. Baker, and Donald
xiii
xiv I Preface
10hnston did the same for G. W. Wharton. The capsular account of the accom-
plishments of Ed Baker and George Wharton, which follows, is shamelessly
parasitized from the recollections of Preston Hunter and Don 10hnston published
in that issue of the ASA Newsletter.
On December 10th we did not know just how critical the timing of the celebra-
tion would tum out to be. George Wharton passed away just four months later
(4 April, 1990). In a Memorium statement in a subsequent ASA Newsletter, Don
10hnston was quoted as addressing George Wharton as "A Student's Professor,"
and that is how he is best remembered by those who knew him well.
Edward W. Baker
When Ed Baker, a Ph.D graduate from U.C. Berkeley in 1938, decided to devote
his life to an investigation of mites, there was essentially no organized literature
available on the identification or biology of the acarines. Preston Hunter described
the literature as "scattered and limited" and described the discipline of Acarology
as "non-existent." Thus, Ed Baker's degree was actually in entomology and plant
pathology but his dissertation focused on the fig mite Eriophyes ficus.
Soon after graduation, Ed joined the USDA and was sent to work at the Fruit
Fly Lab in Mexico City (1939-1944). His second position was also with the
USDA, at the Systematic Entomology Laboratory in Washington, D.C. (Insect
Identification and Beneficial Insect Introduction Institute). He held that position
for 43 years, earning the highest professional rank possible (ST -16). Ed "retired"
in February 1987, but when you want to reach him ... it is still best to try to
locate him in his small, slide- and illustration-filled office at the USDA.
There were so many accomplishments and so many "firsts" in Ed Baker's
singular career. He co-authored, with George Wharton, a book entitled An Intro-
duction to Acarology (later translated into Russian), a seminal work which birthed
and defined a new discipline, Acarology, as Americans know it. But that was
just a beginning of an effort to spread the excitement and joy available in the
world of the miniature. He expressed enthusiasm for his organism in the most
appropriate way possible ... he described over 700 species, 60 genera and 9
new families of mites, and according to Preston Hunter's account his work totals
over 4,200 published pages (over 130 original papers). Each illustration and each
interpretation was meticulously crafted by Ed. He did not have benefit of a large
support network of artists and technicians. At the same time he was responsible
for over 70,000 identifications of mites sent to the USDA from all over the world.
Ed Baker's work has had profound impact on American Acarology. His major
books include: A Revision of the Spider Mite Family Tetranychidae (Pritchard
and Baker, 1955), Guide to the Families of Mites (Baker, Camin, Cunliffe,
Woolley and Yunker, 1958), A Manual of Parasitic Mites (Baker. Evans, Gould,
Preface I xv
Hull and Keegan, 1956), Spider Mites of Southwestern United State and a
Revision of the Family Tetranychidae (Tuttle and Baker, 1968), An Illustrated
Guide to Plant Abnormalities Caused by Eriophyid Mites in North America
(Kiefer, Baker, Kono, Delfinado and Styer, 1982), and The False Spider Mites
of Mexico (Baker and Tuttle, 1987).
Ed Baker has also studied and lectured in Africa, Central America, Brazil,
Egypt, India, Iraq, Pakistan, the Philippines, Thailand and Venezuela. Along the
way he helped to establish Acarological programs in many of these locations, as
he did in the U. S. where he participated in the creation of the Institute of
Acarology. Professional accolades have been common in the life of one so
singular. He has earned the Distinguished Service Award from the Washington
National Academy of Science and was Vice-President and Plenary Speaker at the
First International Congress of Acarology (1963), President of the International
Congress in 1978, first recipient of the Berlese Award for Outstanding Achieve-
ment in Acarology by the International Journal of Acarology, recipient of the
USDA's Superior Service Award ... and the list goes on. Ed Baker has been,
from the beginning, a giant among his peers, a true "Father" (and obstetrician)
of a new discipline which has not been without some growing pains. His insight,
intellect, patience, dedication and nurturing of younger proselytes have been
unparalleled. My own fond memories of Ed begin with my first visit to his lab
where, like a kid in a candy shop, I sorted through boxes of reprints of his
publications on his floor shamefully and gleefully carrying out all I could carry.
They extend to later remembrances over beer, at the Cattleman's Steakhouse in
Tucson, Arizona, when Ed and his lovely wife Mercedes Delfinado-Baker visited
to talk about Varroa. The science stands as a deserved monument to the scientist
in Ed Baker, but our collective memories bear witness to his humanity, generosity,
and zest for life around him. His contributions are much more than the sum of
his publications.
George W. Wharton
George W. Wharton was born in the same year as Ed Baker (1914), but 11
months earlier. So perhaps his birth-order gives him some seniority in the role
of "Father of Acarology" which he shares with Ed Baker. However, while Ed
Baker was growing up on the sunny west coast, George Wharton was spending
his fonnative years in Belleville, New Jersey.
George Wharton received his Ph.D from Duke in 1939 and, like Ed Baker,
joined government service. He became a Biologist with the Norfolk Naval Ship-
yard and subsequently joined the Rockefeller group at NAMRU-l in the Pacific
war zone. Following World War II George returned to Duke, and in 1951 he and
Ed Baker decided to establish the Summer Teaching Program for acarologists.
George assumed the Departmental Headship at the University of Maryland in
xvi / Preface
1953, and moved the Summer Program to College Park, where it remained until
he accepted the Chairmanship of the Department of Zoology and Entomology at
Ohio State in 1961. According to Don Johnston, under whose able guidance the
Ohio State Acarology Program continues to flourish, it was at Ohio State where
the "Acarology Laboratory and the Summer Program have enjoyed their greatest
success." The Program trains students from all over the world and remains a
singularly valuable resource for material, reprints, and academic training concern-
ing mites.
In 1976 George "retired" as Director of the Acarology Laboratory but continued
his teaching and research until diminished eyesight and poor health prevented his
active participation. His enthusiasm and influence did not wane with his vision
and dexterity, however, and he continued to be a major force in acarology until
his untimely death in April, 1990.
Beside his collaborative publications with Ed Baker, mentioned above, George
also published A Manual of the Chiggers (with H. S. Fuller, 1952) and A Manual
of Mesostigmatid Mites Parasitic on Vertebrates (with R. W. Strandtmann,
1958). In addition to his life-long interest in mites, George Wharton had a broad
interest in biology and published on such topics as the physiology of respiratory
pigments in helminths and the ecology of littoral Crustacea. George brought
exceptional breadth as well as depth to the arena of Acarology. And, his experi-
ences and exploring curiosity for all of nature would make him most supportive
of the spirit of integration and extension which modem Acarology hopes to bring
to Biology.
Years of dedication to science have produced approximately 130 publications,
and have earned George much professional recognition. George chaired the
Tropical Medicine Study Section of the National Institute of Health (NIH), he
was President of the Society of Systematic Zoology, and the President of the First
International Congress of Acarology (1963). He was a Guggenheim Fellow
(1950-1951) and was elected to Honorary Life Membership in the International
Congress of Acarology in 1974.
George Wharton had a special dignity among men, was admired as a true
teacher, and was a scholar of the highest caliber. His perspective was that
acarologists should strive to synergize and respect equally both "basic" and
"applied" research for the sake of the wholeness of the discipline. He refused to
recognize the perceived dichotomy between them and enjoyed a joint appointment
with The Ohio Agricultural Experiment Station (Wooster, OH) during his chair-
manship at Ohio State.
George's guidance and his dedication to training quality acarologists has left
behind a legacy of equally gifted scholars, the most significant and fitting contribu-
tion one can make to one's discipline. He truly deserves the designation, "Father
of Acarology". I personally met George Wharton on only a few occasions, which
was sufficient for me to understand the influence one dedicated individual can
Preface / xvii
have on the people that enjoy the dividend of his time. His enthusiasm for the
Acari and his generosity with encouragement will stay with me as a remembrance.
Collectively, Ed Baker and George Wharton are a study in contrasts in terms
of temperament and personal history. Acarology has benefited greatly from their
individuality, perspectives, distinctions and uniqueness. What they shared was a
true passion for mites and a keen concern for the future of Acarology. It is this
commonality which created a whole far richer than either alone could have
contributed to the molding of a discipline. At a time when diminishing funding
and attrition in number of contributing acarologists threaten the future health of
Acarology, the authors of this volume feel a responsibility to reinforce and
continue the traditions established by Drs. Baker and Wharton. The challenge
will be to provide equal passion, vigor, and cooperation in order to
capture the imagination of the public with an understanding of the esthetic

values each of us derives from our intimate knowledge of the beauty and
symmetry of the form, function, and lifeways of the Acari
and acknowledge that the
intellectual values to be derived from the study of mites and ticks are yet to be
determined. That this is true is evident from the fact that no one yet has any
idea of how many kinds of Acari are living at the present time, let alone how
and where they live.
[Quotations extracted from the text of Dr. G. W. Wharton's Keynote Address to

the First International Congress of Acarology, Fort Collins, CO, 1963.]
As Acarology matures as an autonomous discipline, exciting ecological and
evolutionary patterns are emerging and hopefully these patterns will be woven
into the fabric of modem biology to give a more balanced interdisciplinary
understanding of ecology and evolution.
All of the contributors to this volume, and the 1989 symposium, have direct or
indirect gratitude to offer these two gentlemen. The work of all of the contributing
authors was possible because of the foundations established by these men. We
show them our respect and appreciation by offering to them this compilation of
papers on the ecological and evolutionary patterns in mites. In presenting this
compilation of papers, the intent is to strengthen an interdisciplinary discussion,
awareness, and curiosity about mites among ecologists, evolutionary biologists,
parasitologists, population biologists and naturalists. We hope especially to en-
courage students and researchers to see the excitement and possibilities in the
study of mites that we, the contributing authors, have enjoyed in our own work.
I hoped to have assembled a volume with a content and authorship representing
the most current and innovative studies focusing exclusively on mites. The authors
are individually recognized for the quality, depth, and creativity of their past
xviii I Preface
work, and each has contributed to this volume with previoulsy unpublished work
that will prove to be as well received. The authors have exploited their own
past successes, through capsular highlights of completed work, and offered a
projection of potential future directions. The authors offer a spectrum of topics
that showcase a diversity of acarological taxa, techniques, and perspectives. The
intent was not to be inclusive but rather to include innovative studies with the
broadest interest.
With absolutely no idea of what was involved in organizing such a volume, I
persuasively solicited publishing houses in the Spring of 1989, with the intent of
conceding the project to the "highest worthy bidder." Lesson one . . . general
enthusiasm for mites needs nurturing. Once Chapman and Hall was selected
(from among the two worthy bidders), I petitioned symposium speakers to deliver
manuscripts to me for editing at the end of the 1989 symposium session. Lesson
two ... being academicians, acarologists are overcommitted and overworked. I
extracted the final included chapter under duress in November, 1992.
While delayed publication became a disappointment, it provided authors with
the privilege to update revisions until as late as December 1992. Thus, while the
publication was belated, it is by no means outdated. The volume is very current
and timely in content-illustration, one diligent author was still updating citations
as late as Christmas, 1992.
This volume should prove to be very effective as a supplement for courses in
entomology, population biology, and general ecology and evolution, as well as
acarology. The level of comprehension is directed toward upper-level undergradu-
ates, graduate students and professional researchers. However, the diversity and
clarity of issues is appropriate for all who are interested in broadening their
general knowledge of organismal biology.
Modern acarology is beginning to flex its academic muscle, as it exits from a
time of maturation to a time of extension and integration. The expectation is that,
as mites become better appreciated, they will be relieved of the perception as
OTUs or miscellaneous "others" in field samples and become appreciated for
their uniqueness, their seductiveness and for the joy they offer to the exploring
mind. Mite-watcher's life lists of rare species, mite treks and expeditions led by
world-renowned experts, baited mite lures and traps of various sizes and shapes,
all are acarological contingency plans for the future.
This editorial experience has been a positive growth step in my learning curve,
with many necessary adjustments along the way. It taught me how to nag, how
to use an "N" dash, how to sprain sagacious egos without even trying, and most
of all how to compromise. With these reflections and facts in place, I wish to
thank: Greg Payne of Chapman and Hall for his patience, attention to detail and
appreciation of the smaller (acarine) things in life; James Geronimo, production
manager, for meticulous and careful handling of the final copy; Rich Strauss (my
husband) for fervent encouragement when teaching loads were getting me down;
and the dedicated authors who worked so hard to make this volume one that we
Preface / xix
could collectively be proud of (oh no, one last dangling participle !*). Special
thanks also to Ev Lindquist for taking time from his busy schedule the offer a
Foreword. They have been loyal conspirators to the end and deserve much credit
and no blame. Any existing errors are mine alone to cherish.
MARIL YN A. HOUCK
Texas Tech University, 1993
Contributors
Jonathan M. Brown John B. Kethley

Department of Biology Center for Evolutionary and
Bucknell University Environmental Biology
Lewisburg, PA 17837 Field Museum of Natural History
Roosevelt Rd. at Lake Shore Drive
Robert K. Colwell
Chicago, IL 60605
Department of Ecology and
Evolutionary Biology Evert E. Lindquist
University of Connecticut Bio-Systematics Research Institute
Storrs, CT 06269-3042 Agriculture Canada
George C. Eickwort K. W. Neatby Bldg.
Department of Entomology OOttawa, Ontario
Cornell University K 1AOC6 Canada
Ithaca, NY 14853 Shahid Naeem
Norman J. Fashing Centre for Population Biology
Department of Biology Imperial College at Silwood Park
College of William and Mary Ascot, Berks SL5 7PY
Williamsburg, VA 23185 United Kingdom
Marilyn A. Houck Roy A. Norton
Department of Biological Sciences Faculty of Environmental and
Texas Tech University Forestry Biology
Lubbock, TX 79409-3131 SUNY College of Environmental
Science and Forestry
Arne Janssen
Syracuse, NY 13210
Department of Pure and Applied
Ecology Barry M. OConnor
University of Amsterdam Museum of Zoology and Department
Kruislaan 302 of Biology
1098 SM Amsterdam The University of Michigan
The Netherlands Ann Arbor, MI 48109-1079
xxi
xxii / Contributors
Frank J. Radovsky David Sloan Wilson

North Carolina Department Division of Biological Sciences
of Agriculture SUNY, Binghamton, NY 13901
Raleigh, NC 27611
Dana L. Wrensch
Maurice W. Sabelis Department of Entomology
Department of Pure and Applied The Ohio State University
Ecology 1735 Neil Ave.
University of Amsterdam Columbus, OH 43210
Kruislaan 302
1098 SM Amsterdam
The Netherlands
1
Poecilochirus carabi: Behavioral and

Life-History Adaptations to Different Hosts
and the Consequences of Geographical Shifts
in Host Communities
Jonathan M. Brown and David Sloan Wilson
CONTENTS
1. INTRODUCTION
2. NATURAL HISTORY
2.1 The Beetles (Nicrophorus)
2.2 The Mites (Poecilochirus carabi)
3. THE STUDY
3.1 Carrier Preference of Poecilochirus carabi
3.2 Life-History Traits of Poecilochirus carabi
3.3 Morphological Analysis of Poecilochirus carabi
4. RESULTS
4. I I. Kellogg Biological Station (KBS)
4.2 II. University of Michigan Biological Station (UMBS)
4.3 III. The Region Between KBS and UMBS
5. DISCUSSION
5.1 Ecological Adaptation in Poecilochirus carabi
5.2 Specialization and Speciation in Poecilochirus carabi
1. Introduction
The concept of trade-offs is central to many aspects of evolutionary biology.

Life-history models, for example, routinely assume that some component of
fitness, such as fecundity, can only be increased at the expense of another
component, such as survival. Models of the evolution of specialization similarly
assume that efficiency at one task can be achieved only when an organism is
inefficient at others (e.g. Wilson and Turelli 1986). Life-history parameters
may themselves be important in the evolution of specialization if, for example,
different strategies result in maximum fitness in different habitats or in association
with certain hosts.
In its most abstract form, few people would question the basic concept of trade-
offs. Nevertheless, the nature of any trade-off is by no means obvious in any
1
2 I J. M. Brown and D. S. Wilson
particular ecological setting. Nor is its importance obvious in terms of the evolu-
tion of life-history traits and niche specialization. A growing number of empirical
studies have either failed to find trade-offs that initially appeared plausible, or
found them where they were unexpected (for investigations of longevity in
Drosophila see Service 1985; Luckinbill et al. 1989; see also Futuyma and
Moreno 1988). To proceed beyond abstract generalizations, the study of trade-
offs therefore requires a solid foundation in empirical studies.
In this chapter we present an overview of our research on host specialization
in a parasitid mite (Poecilochirus carahi) that is phoretic upon carrion beetles
(Silphidae; Nicrophorus [= Necrophorusl [Fig. 1.1]). Phoretic mites in general
are well suited for the study of specialization because they frequently have
access to a number of carrier species (= hosts) that transport them to different
environments, each potentially requiring a different set of adaptations for survival
and reproduction. Phoretic mites also span the full range from specialists on a
single carrier species, to generalists that utilize many carrier species.
P. carahi is particularly well suited to the study of the role of life-history
adaptations in the evolution of specialization, as populations vary in relative
breadth of host use. By investigating the interaction between mite life-history
parameters and their hosts' behavior and ecology, we are documenting the mite's
ability to adapt to local host communities. Our research demonstrates that host
specialization occurs where strong life-history trade-offs are found across hosts,
but also highlights the fact that the presence of trade-offs alone does not guarantee
that specialization will be found in any given community. Other factors (e.g.
population structure and the ability of organisms to select their hosts) interact
with trade-offs to affect the coexistence of specialist mites.
Figure 1.1. Poecilochirus species clinging to a flying Necrophorus beetle.

Poecilochirus carabi / 3
One subject of special interest to us is the role of trade-offs and the evolution
of specialization in the process of speciation. Is variation in life-history strategies
a response to selection for association with different host (carrier) species? In
particular, can a single species of mite become polymorphic for adaptations to
different carriers, and can the intraspecific morphs ultimately become separate
species? Our results, although not yet conclusive, suggest that such a process
might operate in P. carabi.
2. Natural History
2.1 The Beetles (Nicrophorus)
Most carrion beetles in the family Silphidae reproduce on large animal carcasses.
Beetles in the genus Nicrophorus, however, sequester small carcasses by burying
them underground and then using this resource to raise their brood. Typically a
small carcass is discovered by several Nicrophorus beetles, but ultimately the
carcass is monopolized by a single male and female which remain in the burial
chamber throughout most of their brood's development. The social and parental
behavior of Nicrophorus beetles is an active research area (Bartlett 1987, Muller
1987, Scott and Traniello 1987, Trumbo 1988, Muller and Eggert 1989).
Nicrophorus beetles are found at all geographic latitudes but reach their peak
of diversity in the north temperate zone. Some species live primarily in forested
habitats, others in grasslands (e.g . N. marginatus), and one species in North
America is restricted to bogs (N. vespilloides; Peck and Kaulbars 1987). Our
study focuses on four species that coexist in forested habitats: (1) N. sayi is a
large nocturnal species that overwinters as an adult and is reproductively active
only during the spring. During the early summer and fall N. sayi can be collected
in pitfall traps but will not subsequently breed in the laboratory, even when
provided with a mouse carcass; (2) N. orbicollis is also a large nocturnal species
that overwinters as an adult, but N. orbicollis is reproductively active during the
summer; (3) N. defodiens is a small crepuscular species that overwinters as an
adult and has a reproductive period that coincides with that of N. orbicollis; (4)
N. tomentosus is a medium-sized diurnal species that overwinters as a prepupa,
emerging in early summer. It is reproductively active only during the fall, after
N. orbicollis and N. defodiens have entered reproductive diapause.
Interactions among the four beetle species, and the mechanisms that allow
them to coexist on a single resource, are fairly well understood (Wilson et al.
1984). While small carcasses are required for reproduction of all four beetle
species, adults of Nicrophorus also frequent large carcasses to feed and to mate.
When co-occurring on large carcasses, the various species mingle nonaggres-
sively. On small carcasses, however, the species interact aggressively with the
outcome primarily determined by beetle body size.
The strongest interspecific aggression occurs between the two summer breed-
4 I 1. M. Brown and D. S. Wilson
ers, N. orbicollis and N. defodiens. A large proportion of carcasses initially found

by N. defodiens are subsequently discovered and appropriated by N. orbicollis
during the same or ensuing nights. N. defodiens can successfully coexist with N.
orbicollis primarily by being crepuscular, which allows them to fly during cool
periods when nighttime temperatures prohibit nocturnal N. orbicollis from search-
ing for carcasses (Wilson et at. 1984). Temperature-dependent competition be-
tween N. defodiens and N. orbicollis probably determines the geographical distri-
bution of N. defodiens, which is limited to northern latitudes and higher altitudes
(Peck and Kaulbars 1987).
The effect of competition on the reproductive phenology of the four species is
onl y partially understood. Adults of N. orbicollis and N. defodiens enter reproduc-
tive diapause in late summer, after which time any potential offspring would not
have sufficient time to develop into their overwintering (adult) stage. N. tomento-
sus overwinters in the prepupal stage and therefore can remain reproductively
active longer than N. orbicollis and N. defodiens. The onset of reproduction in
N. tomentosus is probably influenced by competition with N. orbicollis, although
this requires more documentation. It is tempting to think that N. sayi breeds only
in the spring because of competition with N. orbicollis, but pilot experiments
(Wilson, unpublished data) have failed to support this hypothesis, and the reason
that N. sayi foregoes reproduction throughout the summer remains a mystery.
The social behavior and community ecology of Nicrophorus beetles is a fasci-
nating subject in its own right. In this paper, however, we are viewing the beetle
community primarily as a complex environment inhabited by phoretic mites.
From this perspective it is obvious that the choice of a carrier species can have
profound consequences for mite fitness, particularly for those species whose
reproductive physiology is linked to carcass burial and reproduction by the beetles
(see below). A mite that remains attached to N. sayi in the summer, for example,
will not breed until the following spring. A mite that remains attached to N.
tomentosus may breed in the fall but its progeny will remain underground until
midsummer of the following year. More subtle, but equally important, conse-
quences of carrier choice will be documented below.
2.2 The Mites (Poecilochirus carabi)
Nicrophorus beetles collected from our study sites support an abundant commu-
nity of mites, comprising at least 14 species from four different families (Histiosto-
matidae, Macrochelidae, Parasitidae, Uropodidae). Our study focuses on a large
(1 mm in body length) parasitid species, Poecilochirus carabi (= P. necrophori
Vitzthum), that feeds on carrion fluids and small organisms associated with
carrion such as fly eggs and nematodes. The feeding activities of P. carabi tend
to have either a neutral or a beneficial effect on the fitness of their beetle carriers
(Springett 1968, Wilson 1983, Wilson and Knollenberg 1987).
The most widely accepted definition of phoresy in the Mesostigmata (Farish
and Axtell 1971) requires that the attached animal (the phoretic): (1) actively seek
a host; (2) neither feed nor develop while on the host; and (3) attach temporarily
and for the purposes of dispersal to an area more suitable for reproduction or
development. P. carabi satisfies this definition with one minor exception; they
sometimes feed while on the host, either on other phoretic associates such as
nematodes or on oral secretions of the beetle (Springett 1968). Since this mite is
so highly adapted to use Nicrophorus beetles as a transport agent and for no other
purpose, we describe the relationship as phoretic.
P. carabi is only phoretic in the deutonymphal stage. Unlike many other
species of phoretic mites which physically attach to their carrier until their final
destination is reached (e.g. members of the family Histiostomatidae), P. carabi
is extremely mobile and often leaves one carrier temporarily to feed or to perma-
nently switch to another nearby carrier. As outlined above, the natural history of
Nicrophorus beetles creates frequent opportunities for P. carabi to switch carriers
on large (and occasionally on small) carcasses.
When a Nicrophorus beetle arrives at a carcass that is suitable for its .own
reproduction, P. carabi disembarks and within 24-48 hours molts into the adult
stage. The next generation of deutonymphs can potentially: (1) disperse on the
parent beetles; (2) accompany the beetle offspring into their pupal chambers; or
(3) disperse on other insects that visit the abandoned burial chamber. From the
standpoint of the mite's preference, these options can usually be ranked 1 > 2
> 3. This is presumably because parent beetles will immediately search for new
carcasses, whereas their offspring require weeks of development before becoming
adults in need of a new resource. In addition, if both the male and the female-
beetle parents are present in the burial chamber, deutonymphs of P. carabi
preferentially embark on the males. Abandoned burial chambers probably are
seldom revisited by Nicrophorus beetles, since the carcass is usually completely
consumed by the brood.
It might seem that P. carabi could breed on large carcasses in addition to small
carcasses, since the former receive a constant traffic of Nicrophorus beetles who
visit to feed and to mate. It appears, however, that large carcasses are utilized
primarily by another species of Poecilochirus (described as P. silphaphila in an
unpublished Ph.D. thesis; Yoder 1972) that is phoretic both on Nicrophorus
beetles and other genera of silphids that specialize on large carcasses (Wilson,
unpublished data). While the specific cue is unknown, we have found that the
only predictable method to induce deutonymphs of P. carabi to molt into adults
is to place them on Nicrophorus pairs burying small carcasses.
The taxonomy of Poecilochirus in general, and of P. carabi in particular,
is unfortunately not helpful in understanding host specialization. The current
taxonomic trend is towards lumping previously named species into cosmopolitan,
morphologically variable species (for the latest treatments see Hyatt 1980 and
Wise et al. 1988). As most recently defined, P. carabi has been recorded most
often in association with Nicrophorus but also with other silphids and other
6 / J. M. Brown and D. S. Wilson
families of insects (Hyatt 1980). We will argue that, as currently defined, P.

carabi almost certainly includes several reproductively isolated and morphologi-
cally distinct species.
3. The Study
We have studied Poecilochirus carabi intensively at two sites in Michigan; the

University of Michigan Biological Station (UMBS) at Pellston, MI (latitude =
45° 34/) and Michigan State University's Kellogg Biological Station (KBS) at
Hickory Comers, MI (latitude = 42° 34/), 315 km south of UMBS. The general
habitat features of the two sites have been described elsewhere (Wilson et al.
1984). For our purposes the main difference concerns the occurrence of Nicropho-
rus defodiens, which (through the mechanism of temperature-dependent competi-
tion outlined above) is absent at KBS and abundant at UMBS. Based on our
results from KBS and UMBS, we have also taken more limited data from
additional sites to test specific hypotheses discussed below. This includes a
transect connecting KBS and UMBS, and scattered locations throughout North
America.
Our general goal has been to examine carrier-preference by the mite, mite life-
history traits, morphology, mating behavior, and natural patterns of association
in an integrated fashion. Methods are described in detail elsewhere (Brown 1989,
Brown and Wilson 1992) and will be summarized here.
3.J Carrier Preference of Poecilochirus carabi
The goal of these tests was to mimic situations that occur on or near large
carcasses, where mites have an opportunity to choose between different species
of beetles. Beetles and mites collected in baited pitfall traps were placed in
collection boxes for 24 hours. lndividual beetles with their attached mites were
then placed individually in small plastic tubs with moist paper towelling. Beetles
of a given species (e.g. N. orbicollis) were placed under a stream of CO 2 . P.
carabi were dislodged with a fine camel-hair brush and placed in a tub with
two beetles of different species (e.g. N. orbicollis and N. tomentosus) whose
Poecilochirus mites had been previously removed. The beetles tend to be nonag-
gressive in this situation, moving independently or resting side by side in the tub
as they do on large carcasses. Twenty-four hours later, the numbers of P. carabi
on each beetle were counted.
These experiments reveal whether mites found on a given beetle species at the
start of the experiment, actually prefer that species when given a choice. The
experiments do not reveal whether preferences are genetically based or the result
of prior experience. Therefore, we have conducted separate experiments in which
mites that are found on a given beetle species are forced to breed in association
with another beetle species. Choice experiments are then performed on their
offspring (Wilson 1982, Brown 1989).
The choice experiments have one problem that can be illustrated by the follow-
ing hypothetical example. Suppose that the majority of P. carabi in a population
are generalists that are indifferent to carrier species but that a small proportion
are specialists with strong preferences. The results of a choice experiment would
be dominated by the generalists and rare specialists might not be detected. We
therefore have conducted two-round choice experiments in which mites originally
taken from N. orbicollis (for example), that chose N. orbicollis during the first
round, are given a second choice between N. orbicollis and a second species. If
P. carabi consists of both generalists and specialists, then the proportion of
specialists on N. orbicollis should increase with each round of the choice experi-
ment, ultimately allowing them to be detected.
The choice experiments can be analyzed statistically in two ways. First, the
proportion of mites from beetle species i (i = 1, 2) that chose beetle species j (j
= I, 2) can be tested against the null hypothesis of no preference. This assumes
that each mite choice represents an independent event. It is possible, however,
that mites are influenced by the behavior of other mites or that all mites in a given
tub are influenced by factors unrelated to beetle species. A more conservative
test is, therefore, to score the number of tubs in which more than half of the mites
from beetle species i (i = 1, 2) chose beetle species j (j = I, 2). This is then
tested against the null hypothesis of an equal score for each beetle species (Chi-
square test).
3.2 Life-History Traits of Poecilochirus carabi
To measure differences in life-history traits that might correlate with carrier-

preference, P. carabi were bred in the laboratory with both their preferred and
non-preferred carrier species. The standard protocol involved placing beetles,
mites, and a dead mouse into soil-filled buckets fitted with lids that allowed the
beetles to exit into an emergence trap. In this fashion we recorded the total
fecundity of the mites and the distribution of their offspring on the departing
male-beetle parent, the departing female-beetle parent, and their emerging beetle
offspring. In a separate series of laboratory experiments, the developmental rate
of P. carabi was measured directly by dismantling burial chambers at periodic
intervals and extracting the mites with a sucrose solution.
3.3 Morphological Analysis of Poecilochirus carabi
The analysis of morphological variation in P. carabi was performed on both field-

caught specimens and on mites from the breeding experiments outlined above.
This controls for the effect of carrier-beetle species on mite morphology. Two
characters were then measured: (1) body size, measured as the length and width
of the sternal shield and/or dorsal shield; and (2) dorsal setal lengths.
8 / 1. M. Brown and D. S. Wilson
A principal components analysis (PCA) was performed on a set of log-trans-

formed lengths of the dorsal podonotal shield setae, using a covariance matrix
(SAS Institute Inc. 1985). The number of setae included in the analysis depended
on circumstances. Measurements of mites from the laboratory breeding experi-
ments included 19 podonotal shield setal lengths. Because smaller numbers of
mites were available from some field collections, and because setae tended to fall
off during preparation and mounting of the mites, it was necessary to use fewer
setal measurements per individual in these cases, in order to obtain a large enough
sample size. At a minimum, we chose to measure four setae (i3' i" Z2 and Z4)'
Previous studies demonstrated the least overlap in size of these setae between
KBS specialists (see below).
4. Results
Results will be presented first for the Kellogg Biological Station (KBS), then for
The University of Michigan Biological Station (UMBS), and finally for the other
sites for which we have limited data.
4.1 1. Kellogg Biological Station (KBS)
Figure 1.2A (KBS) shows the results of a two-round choice-experiment test

performed on August 8, 1981, using Poecilochirus carabi collected from Nicro-
phorus orbicollis andN. tomentosus. Starting from the left side of the top figure,
86 mites attached to N. orbicollis were divided into II tubs and provided a choice
between N. orbicollis (No) and N. tomentosus (Nt). Eighty-six percent chose N.
orbicollis. Stated more conservatively, the majority of mites chose N. orbicollis
in 10 out of the 11 tubs.
When these mites were provided a second choice, 95% of those choosing N.
orbicollis on the first trial, chose N. orbicollis on the second trial. When the
minority of the mites that chose N. tomentosus (Nt) during the first round were
provided a second choice, 70% again chose N. tomentosus. Proceeding to the
right side of Figure 1.2A, 92% of 108 mites originally on N. tomentosus chose
the same carrier during the first round, and 98% of these made the same choice
during the second round. Of the 8% that chose N. orbicollis during the first round,
88% made the same choice during the second round.
This experiment, which we have repeated several times at KBS, illustrates two
important points. First, virtually all P. carabi at KBS appear to have a strong
preference for one beetle species or the other. Second, having a preference for a
carrier species does not guarantee that a mite will be associated with that species.
Despite strong preferences, approximately 10% of P. carabi taken from beetles
in pitfall traps are found on the carrier species that they do not prefer.
It is important to emphasize that P. carabi will readily breed in association
with its non-preferred carrier species. Wilson (1982) showed that when P. carabi
Poecilochirus carabi I 9
< <
(A) KBS -- 8/8/81 No(.95) No(.SS)
No[S6]
< ... ~)'::<
10/11
6/6 "
N 1(.05)
17/20"" NI[10S]
N o(OS) [9]
12112"""
0/2 ns
N 1(.12)
21123
"""
No(.30) No(.02)
NI(.14) [10]< 1/3 ns N 1(.92) [92] < 9/9""
N 1(.70) N 1(.9S)
(B) UMBS -- 8/85

N 1(.37) N 1(.07)
"'' '< . . "'

Nt(.37) [51]< 113 ns N 1(.27) [40] < 2/2 ns
Nd(.63) Nd(.93)
7117 ns Nd [170]< 7110 ns 13/17
N 1(.65) N 1(.21)
Nd(.63) [SI]< 3/4 ns Nd(.73) [100]< 4/5 ns
Nd(.35) Nd(.79)
<
(C) UMBS -- 9/85
N 1(.77) NI(7S)
"'''lI' ::~<
6/8 ns <
N I( 55) [S9] N~/(52;>"
Nd (.23)
• <
N 1[214] 1011 0 1711 9 Nd [163] 4110 ns 9/20 ns
N 1(.94) NI(.21)
Nd(.10) [17]< 3/4 ns N d(.45) [77] < 4/5 ns
N d(.06) Nd(79)
Figure 1.2. Preference tests of Poecilochirus carabi for different beetle species. Each
pair of branches refers to a set of pairwise tests, with the number of pre-trial mites (found
on the beetle species) represented in brackets at each node of the bifurcation. The decimal
in parentheses at the end of each bifurcation is the proportion of all mites found on that
beetle species in that set of trials. The fraction given, located to the lower right of each
bifurcation, is the proportion of all trials "won" by the species at the node. A "win"
occurred when one species carried more mites at the end of the trial than the other species
(**p < 0.01, ***p < 0.001, for Chi-square test with the expectation of an equal number
of trials won by each species). Nd, Nt and No refer to the beetle species; Nicrophorus
defodiens, Nicrophorus tomentosus and Nicrophorus orbico/lis, respectively (From Brown
and Wilson 1992). A) Mites and beetles from KBS, tested on August 8,1981. B) Mites
and beetles from UMBS, tested on August II, 1985. C) Mites and beetles from UMBS,
tested on September 9, 1985.
from N. orbicollis are raised in association with N. tomentosus, their progeny

still prefer N. orbicollis (and vice versa), demonstrating that carrier preference
is genetically encoded. More recently, Brown and Wilson (1992) demonstrated
that the preference types will not interbreed. Finally, the preference types can be
discriminated morphologically based on both general body size and setal lengths
(Fig. 1.3). There seems to be little doubt that P. carabi at KBS consists of at
least two good biological species. We shall refer to the KBS mites as the orbicol-
lis-specialist and the tomentosus-specialist, after their preferred host species.
Why should two closely related species of Poecilochirus coexist on Nicropho-
0.4
0.3
0
0.2 0
0 0 T
o 00 0 0 TT
o 0 00
0.1 0
0
0 0 U '1I*r
(\J 0.0
?P *\)f'\'JUTTT
u
0
U U U UJU
a.. -0.1 0 T
T U UU
-0.2
* '* U
U
U
-0.3 * U
-0.4 U
-0.5
-0.8 -0.6 -0.4 -0.2 0.0 0.2 0.4
PC1
Figure 1.3. Principal components analysis of 19 log-transformed setal lengths of Poeci-
lochirus carabi from the Michigan study sites. PC2 is plotted against PCI for the KBS
mites, the orbicollis-specialist (0) and the tomentosus-specialist (n, and UMBS mites
found on several species (U). The few mites that were found on Nicrophorus orbicollis
beetles at UMBS are plotted with an "*,, (From Brown and Wilson 1992).
rus beetles at KBS? Presumably a trade-off exists such that breeding in association
with the different carrier species require different adaptations. Our reproductive
success experiments tend to confirm this intuition (Table 1.1). The tomentosus-
specialist produces almost twice as many offspring in association with its preferred
carrier (N. tomentosus) than with its nonpreferred carrier (N. orbicollis). The
orbicollis-specialist, in contrast, produces equal numbers of offspring in associa-
tion with either carrier and by this criterion alone should not exhibit a preference.
The pattern of dispersal of the offspring, however, depends greatly on carrier
species. In association with N. orbicollis, the orbicollis-specialist offspring dis-
perse on the male parent, the female parent, and the offspring in roughly equal
proportions. In association with N. tomentosus, virtually all of the offspring
attempt to disperse on the female parent. Since the female parent cannot possibly
carry all the P. carabi that emerge from the carcass (frequently in excess of 1000
mites), the majority will fall off the beetle when it takes flight. Thus, despite the
equal production of offspring on both carriers, the orbicollis-specialist more
effectively disperses its offspring in association with its preferred carrier. This
should result in total fitness differences across the two host species.
Although the differences between the two P. carabi species in Table 1.1
Table 1.1. Reproductive success experiments using KBS mites and beetles. Shown
are the means for each behavioral specialist raised on both beetle species at KBS.
Adaptedjrom Brown and Wilson (1992).
Orbicollis-specialist Tomentosus-specialist
Number of Offspring Number of Offspring
Beetle species N Mean N Mean
N. orbicollis
% on Males 0.21 0.46
% on Females 0.47 0.33
% on Offspring 0.33 0.21
Total (Per Capita) 15 27.10 14 27.10
N. tomentosus
% on Males 0.00 0.06
% on Females 1.00 0.84
% on Offspring 0.00 0.09
Total (Per Capita) 16 27.60 17 42.40
probably reflects a number of trade-offs, the one that we have documented most
thoroughly originates with the social behavior of the beetles. The male beetle
parent leaves the burial chamber slightly before the female in both species, but
for N. orbicollis the median leaving-times are 9 and 13 days respectively while
for N. tomentosus they are five and nine days (Fig. 7 in Brown and Wilson 1992).
In trials performed in isolation from beetle hosts, tomentosus-specialists were
shown to complete an entire generation (deutonymph to deutonymph) in six
days, while orbicollis-specialists took 8.3 days (Wilcoxon p < 0.001). The
developmental rates of the orbicollis-specialist and tomentosus-specialist are
synchronized with the male leaving-time of their preferred carrier. Since the male
represents the earliest dispersal agent to future carcasses, it is obviously important
for P. carabi to develop fast enough to catch the first ride.
Despite this striking synchrony between generation time and male dispersal,
what is the evidence that the differences in behavior between the two host species
represent a trade-off for mites? In other words, does lack of synchronization of
generation time with male dispersal result in a decrease in fitness? This is clearly
the case for orbicollis-specialist mites as we have argued above. These mites
suffer a loss in fitness when in association with N. tomentosus due to their long
generation times; lack of synchronization in generation time results in a dispersal
pattern that assures lower survivorship during dispersal.
The connection between synchrony and fitness is not as clear for the tomento-
sus-specialist; this specialist produces a lower number of offspring when in
association with its non-preferred host (Table 1.1), but this is not obviously
directly related to its short generation time. We do know that these mites are
ready to disperse after six days, but must then wait several days before dispersing
with N. orbicollis males. It is possible that this waiting period results in mortality
for mites embarked on a beetle that is still active in the burial chamber.
In summary, these results suggest that the two beetle species represent habitats
that differ in their optima for mite generation time. Synchronization of generation
time with male dispersal in one beetle species results in a fitness decrease in terms
of reproductive success or survivorship during dispersal when reproducing with
the other available beetle species (the non-preferred host). These types of trade-
offs are necessary if specialization is to evolve within a species, or if mUltiple
specialist species are to coexist in the community.
The reproductive success experiments provide some further information on the
behavioral sophistication of these mites. When the orbicollis-specialist is raised
on its non-preferred host, all offspring attempt to disperse on the female-parent
beetle. A slow developmental rate explains why the orbicollis-specialist does not
disperse on male N. tomentosus. But, why does it also fail to disperse on the
offspring? The most probable answer is that, by following a N. tomentosus
larva into its pupal chamber, the orbicollis-specialist foregoes any chance of
reproduction until mid-summer of the following year. By contrast, if the orbicoll-
is-specialist can successfully disperse on the female-parent beetle and transfer to
its preferred carrier, then reproduction can commence in mid-spring. Uncertain
dispersal and early reproduction may be more adaptive than certain dispersal and
delayed reproduction.
Our studies at KBS have focused on N. orbicollis and N. tomentosus. Our data
for N. sayi is more limited because this species is relatively uncommon at KBS.
N. sayi does not appear to have a third P. carabi morph, but rather is utilized
primarily by the orbicollis-specialist, as one would expect from the fact that N.
sayi parents remain even longer with their brood than do N. orbicollis parents
(Brown and Wilson 1992).
4.2 II. University of Michigan Biological Station (UMBS)
As previously stated, UMBS differs from KBS primarily in the addition of a

fourth Nicrophorus species, the competitively subordinate N. defodiens. This
species is almost identical to N. tomentosus in parental dispersal (average leaving-
times of the male and female parent are five and nine days for N. tomentosus and
six and nine days for N. defodiens; Fig. 7 in Brown and Wilson 1992), so it is
interesting to know if any other trade-offs allow a P. carabi "defodiens-specialist"
to coexist with the tomentosus-specialist at UMBS. Figure 1. 2B (UMBS -August)
shows the results of a two-round choice experiment performed at UMBS on
August 11, 1987, using P. carabi from N. tomentosus and N. defodiens.
Starting from the left side of Figure 1. 2B, 137 mites attached to N. tomentosus
were divided into 10 tubs and provided a choice between N. tomentosus and N.
defodiens. Only 37% chose N. tomentosus. When these were offered another
choice, again only 37% chose N. tomentosus. When the remaining 63% of the
mites that chose N. defodiens during the first round were tested again, only 35%
made the same choice. When analyzed conservatively at the tub level, mites
attached to N. tomentosus at the beginning of the experiment display little or no
preference for the two carrier species.
Proceeding to the right side of Figure 1.2B, 73% of 170 mites originally on
N. defodiens chose the same carrier during the first round, and 79% of these made
the same choice during the second round. Of the 27% that chose N. tomentosus
during the first round, only 21 % made the same choice during the second round.
These results suggest that mites attached to N. defodiens at the beginning of the
experiment display a moderate preference for N. defodiens that is significant at
the tub level.
Figure 1.2e (UMBS - September) shows that when the same experiment is
performed one month later at UMBS, the situation is reversed. Mites initially on
N. tomentosus exhibit a strong preference while mites initially on N. defodiens
are either indifferent or perhaps display a mix of preferences that segregate during
the second round of the experiment.
A seasonal change in a measure of preference can occur in two ways; individual
mites can change their preference, or the relative abundance of mites with fixed
preferences can change. Fortunately, these two explanations lead to very different
predictions. If individual mites had fixed preferences, we would expect the
proportion favoring N. defodiens to increase from August to September, since N.
defodiens breeds during this period while N. tomentosus does not. The fact that
P. carabi favors N. tomentosus at the beginning of its breeding period strongly
suggests that individual mites can adaptively change their preferences.
In summary, these experiments demonstrate a complex pattern in which overall
preference shifts from N. defodiens to N. tomentosus seasonally, but a spectrum
of preferences also exists at anyone time. There is no hint of the extreme
behavioral types associated with N. orbicollis and N. tomentosus at KBS, so we
provisionally conclude that N. tomentosus and N. defodiens at UMBS are shared
by a single P. carabi species.
Although the addition of N. defodiens to the Nicrophorus community at UMBS
has not resulted in a P. carabi "de,fodiens-specialist," it is associated with the
elimination of the orbicollis-specialist from the mite community, despite the
fact that N. orbicollis remains abundant and competitively dominant at UMBS.
Numerous preference experiments show that N. orbicollis is always rejected by
UMBS mites in favor of N. tomentosus and/or N. defodiens, regardless of the
season (Brown and Wilson 1992).
This result, although mystifying at first, can probably be explained by the
asymmetrical nature of competition among the beetles. A very large proportion
of the carcasses utilized by N. orbicollis at UMBS (up to 70%) have been
previously discovered by N. defodiens, many of whose mites have already disem-
barked. Thus, the first P. carabi to arrive at a carcass are usually carried by N.
defodiens, even when N. orbicollis is the ultimate beetIe victor. From the stand-
point of P. carabi, to prefer N. orbicollis is usually to be a latecomer. If arriving

first at a carcass provides a competitive advantage, it is adaptive for P. carabi to
prefer N. defodiens.
In addition, it can be shown theoretically that a competitively inferior species
can actually displace a competitively superior species if its numbers are supple-
mented by a sufficiently large influx of dispersers from another habitat (MacArthur
1972). Asymmetrical competition among the beetles provides just such an influx
of P. carabi from the N. defodiens into the N. orbicollis "habitat." I~ this fashion
the orbicollis-specialist could be excluded at UMBS by a morph that is better
adapted to N. defodiens, even while remaining competitively superior on N.
orbicollis. The importance of the presence of N. defodiens in the presence of the
orbicollis-specialist mite is indicated by data from sites between UMBS and KBS
(see below).
Finally, N. sayi at UMBS is avoided by all P. carabi throughout the late spring
and summer but becomes highly preferred in late fall (Brown and Wilson 1992).
This is obviously an appropriate response to a carrier species that is reproductively
inactive during the summer but the first to breed in spring, and provides another
example of adaptive behavioral flexibility in P. carabi.
Morphological analysis in general confirms the results of the behavioral experi-
ments. Figure 1.3 plots the PCA scores of 19 setal lengths for mites raised under
lab conditions. The two specialists from KBS segregate into two clouds; the
beetle species with which mites were raised has no significant effect on this
morphological measure (Brown and Wilson 1992). Mites from UMBS, even
those few found N. orbicollis at this site (indicated by H*"), are significantly
different from both KBS specialists, although they more closely resemble the
KBS tomentosus-specialist. The orbicollis-specialist is not found at this site. To
summarize, both behavioral and morphological data suggest that P. carabi at
UMBS is a single species with complex and seasonally changing patterns of
preference for carrier species.
4.3 1lI. The Region Between KBS and UMBS
To further document the relationship between the appearance of N. defodiens and

the disappearance of the orbicollis-specialist mite, beetles were trapped (on July
7, 1988) at six sites spanning the distance between KBS and UMBS. After
determining that site number three was close to the southern limit of N. defodiens,
beetles were trapped along a second transect spanning the distance between site
two and four of the original transect on August 8, 1988. This procedure was
repeated at three additional sites between UMBS and KBS in August, 1989. For
both transects the P. carabi on N. orbicollis were subject to morphological
analysis. Figure 1.4 shows quite clearly that the disappearance of the orbicollis-
specialist (here indicated by its larger body size) is not a peculiarity of UMBS,
but correlates with the rising abundance of N. defodiens along a north/south axis.
,
3 ".
". 1.0
o ".
".
".
'" '"
2 0
I
8 9
'" 0.8
o
c·
'" '" d
§ S ~
"j"' o 8 $>
0.6 Z
"-.
0 0
~
o
a.. -1
§ 0
0
0
0
0.4 "'C
0
j
T ~ 0
~ Z
-2 T @
§ 0 ~ ~
& 0
0 0.2
'" '"
-3
".
". 0
".
-4~~ __~~ __~________~________~________~~ 0.0
42 43 44 45 46
LATITUDE
Figure 1.4. Principal components analysis of the size of the sternal shield of mites found
on Nicrophorus orbicollis beetles across the transect from KBS (South) to UMBS (mites
captured in July, 1988 and August, 1989). Plotted at the left are scores for orbicollis-(O)
and tomentosus-specialists (D from KBS. Also plotted is the relative density of Nicropho-
rus defodiens (Nd) to Nicrophorus orbicollis (No) individuals in pitfall traps at three sites
in the transect in August 1989. The dotted lines connect these relative densities to those
reported at KBS and UMBS (Wilson et al. 1984).
5. Discussion
5.1 Ecological Adaptation in Poecilochirus carabi
Poecilochirus carabi is faced with a complex environment in the form of several

carrier species that differ in their reproductive phenology, social behavior and com-
petitive interactions. One way that P. carabi adapts to this environment is with
an impressive degree of behavioral sophistication. Single mites can discriminate
between carrier species and can alter their preferences seasonally in ways that en-
hance their own prospects for reproduction. The KBS orbicollis-specialist even
appears to distinguish between the immature stages of its carrier species, accepting
the pupating larvae of Nicrophorus orbicollis but not N. tomentosus.
In addition to the behavioral flexibility of individual mites, P. carabi also
appears to be behaviorally polymorphic, both at KBS and UMBS. In other words,
at anyone point in time individual mites differ in their preferences for carrier
species. At UMBS these differences take the form of some mites preferring a
given carrier while other mites remain neutral. At present, we do not know if the
behavioral polymorphisms at UMBS have a genetic basis or if carrier preference
correlates with any other traits that adapt mites to their preferred carrier. We only
know that the preferences themselves are seasonally labile.
At KBS the behavioral polymorphism takes the form of two specialists with
seasonally consistent preferences for N. orbicollis and N. tomentosus. Further-
more, the specialists are reproductively isolated, morphologically distinct, and
have correlated life-history traits that adapt them to their preferred carrier. Here,
strong life-history trade-offs across two hosts are associated with the coexistence
of two specialists.
Ecologically, the reason that P. carabi at KBS and UMBS are so different
from each other can be traced to a single beetle species, N. defodiens, that appears
to alter the complex environment in two ways. First, at UMBS most carcasses
found by N. orbicollis have been previously buried by N. defodiens individuals
that carry a large number of P. carabi. If they were present, orbicollis-specialists
at UMBS would have to compete with the large influx of mites that arrive with
N. defodiens.
Second, mites on N. orbicollis have the disadvantage of arriving several hours
to several days later than the first arrivals, which might offset the competitive
superiority that they otherwise would enjoy. The addition of a beetle species to
the community of available hosts has the paradoxical effect of collapsing a two-
niche environment into a one-niche environment as far as P. carabi is concerned.
This change in the mite community makes an important point about the role
of trade-offs in maintaining ecological diversity, namely that trade-offs alone are
not sufficient for specialization to evolve or be maintained in the community.
Along with natural selection for different trait values in different parts of the
environment (i.e. trade-offs), the ability of organisms to select habitats, and the
resulting population structure, can have profound influences on the degree of
ecological diversity that can evolve or be maintained (Rice 1987, Brown 1989,
Diehl and Bush 1989). Figure 1.5 summarizes the aspects of the host community
which highly determine these three central factors for these mites.
For example, the constituent beetle species and the local particulars of their
parental care behavior will determine whether different values of generation time
are selected in association with different hosts, i.e. whether trade-offs in life-
history characters across habitats are present. Another example was outlined
above in the case of N. orbicollis and N. defodiens at UMBS. Competitive
interactions between beetle species can result in the "involuntary" transfer of
mites from one selective environment to another. This weakens the ability of
mites to determine their host associations, a condition important in the evolution
of host or habitat specialization (Brown 1989). Inability to select habitats also
alters the structure of the mite populations, changing the nature of competitive
and mating interactions.
In summary, shifts in the host community can profoundly alter the factors that
ultimately determine the ecological diversity of the mite community, even to the
BEETLE COMMUNITY STRUCTURE
POPULATION
/ J, ~
LIFE HISTORY
STRUCTURE ~ HOST PREFERENCE
~ SELECTION
~ J, /
ECOLOGICAL DIVERSITY
OF THE MITE COMMUNITY
Figure 1.5. Conceptual model of the forces that influence the ecological diversity of a
local mite community.
point of eliminating a well-adapted specialist from a community in which its

preferred host species is abundant.
5.2 Specialization and Speciation in Poecilochirus carahi
Since P. carahi appears to consist of two species at KBS and one species at
UMBS, it is interesting to ask how the speciation event occurred. On the one
hand, the second species could have arisen allopatrically and then spread into
areas that ecologically constitute "two-niche" environments for P. carahi. On the
other hand, speciation could be the direct outcome of disruptive selection op-
erating within a two-niche environment (Wilson 1982).
We can hardly hope to answer such a complex question with our existing data.
Nevertheless, at least two features of P. carahi make it interesting from the
standpoint of speciation theory. First, some models of sympatric speciation can
be described as "microallopatric," in the sense that they require a near-total
disruption of gene flow for genetic divergence to occur. The disruption is merely
caused by small-scale isolation such as mating on different hosts or breeding at
different times of the year (Bush 1975, Rice 1987), rather than by large scale
isolation such as a geographical barrier.
The population structure of P. carahi clearly does not fit the requirements of
these models. Even in their current specialized state, approximately 10% of the
specialists at KBS occur on the "wrong" carrier species when taken from pitfall
traps (since these traps mimic large carcasses, it is likely that such transfer occurs
in nature). Thus, if speciation in P. carahi is a local process, it must have occurred
in the presence of significant gene flow.
Second, if we expand our scale to include a wider geographical region and
more species of Nicrophorus beetles, it is possible to envision P. carahi as
existing in a mosaic of "one-niche" and "multiple-niche" patches. If species arise

allopatrically and then fill the multiple-niche patches of the mosaic by dispersal,
we should expect a P. carabi species to be more closely related to ecologically
similar species from other patches than to coexisting species from the same patch.
If speciation is a local process, however, we should find a substantial number of
multiple-niche patches in which the coexisting species are most closely related
to each other.
To this end, we have initiated a study of Nicrophorus beetles and their mites
at locations throughout North America and South America. The initial survey
indicates a high degree of variation between sites in the local nature of host
specialization. Figures 1.6A and 1. 7 show one preliminary result from Farming-
dale, South Dakota. N. orbicollis and N. tomentosus were the only species
collected and on these grounds alone we might expect to find the two P. carabi
specialist species, as at KBS.
At the behavioral level, mites on N. tomentosus display a moderately strong
preference whereas mites on N. orbicollis are either indifferent or consist of a
mix of specialists (Fig. 1.6A). At the morphological level, mites from N. orbi-
collis that chose N. orbicollis are significantly different in setal lengths (though
not body size; Brown 1989) from those that chose N. tomentosus or those that
were originally on N. tomentosus (Fig. 1.7; Tables 1.2 and 1.3). Furthermore,
this provisional "orbicollis-specialist" bears no resemblance morphologically to
the orbicollis-specialist at KBS, but is similar to the KBS tomentosus-specialist
(Brown 1989). Although these measurements were performed on field caught
individuals with unknown histories, this is a tantalizing suggestion that morpho-
< <
(A)
Nt(.72) Nt(.49)
Nt[123] 12114" No[88] 5111 ns
No(.28) No(.51)
(B)
Nd[123]
Figure 1.6.
< Nt(.80)
Nd(.20)
919"" Nt [ 1 09] < Nt(.86)
Nd(.14)
015 "
Beetle species preference tests using Poecilochirus carabi captured in: A)

Farmingdale, South Dakota and B) Hill City. South Dakota in July 1988. See Figure 1.2
for an explanation of the symbols.
0.10
0.08
0.04
+
+ t t
N
U 0.00
~
-0.02
-0.04
No - No No - Nt Nt - No Nt - Nt
FROM - CHOSE
Figure 1.7. A plot of PC2 (from a principal components analysis of dorsal setal lengths
of mites from the Fanningdale, South Dakota preference tests) against the results of the
choice tests. The mean PC2 ± I S.D. is plotted for each behavioral phenotype, defined
by the beetle species on which the mite was found (FROM) and the beetle species
chosen in the preference trial (CHOSE). Nt and No refer to Nicrophorus tomentosus and
Nicrophorus orbicollis. respectively.
logical divergence can be a local process and can occur in the presence of
substantial gene flow.
Data from other sites outside of Michigan indicate extreme geographical vari-
ability in P. carabi carrier preference and morphology. In general, our samples
from numerous localities show that the P. carabi complex does not consist of
two morphologically stable species corresponding to the tomentosus-specialist
and orbicollis-specialist at KBS (Brown 1989). For example, at a site near Hill
City, South Dakota, members of two beetle species, N. tomentosus and N. defo-
diens, were captured in early July. Mites were found on both species, but signifi-
Table 1.2. Correlation of the scores of the first two PCA components (PC1 and PC2)
with the eight dorsal podonotal shield setae used in the analyses. and the percent
variance explained by the first two components. Analyses are of P. carabi from
Farmingdale. South Dakota.
Podonotal Shield Setae
i3 i5 i6 z2 z3 z4 s3 s4 % Variance
PCI 0.82 0.74 0.77 0.84 0.49 0.94 0.85 0.89 0.64
PC2 0.23 -0.40 -0.56 0.34 0.61 -0.04 0.28 0.25 0.16
Table 1.3. Analysis of variance of the scores of the first two principal components,
for the eight podonotal shield setae measured on P. carabi from Farmingdale, South
Dakota. P. carabi were divided into groups based upon their behavior in choice tests
(Fig. 1.6), i.e. the species of Nicrophorus upon which they were found (FROM effect)
and the species of Nicrophorus which they chose in the choice-test (CHOSE effect) (*p
< 0.05; **p < 0.01).
Source d.f. SS F
PCI FROM (F) 0.007 0.97

CHOSE (C) 0.0004 0.07
FxC 0.004 0.53
Error 28 0.188
PC2 FROM (F) 0.005 5.55*
CHOSE (Cl 0.003 3.59
FxC I 0.011 11.50**
Error 28 0.027
cantly preferredN. tomentosus over N. defodiens (Fig. 1. 6B). Since these tests were
run in early July, presumably whenN. defodiens are reproducing andN. tomentosus
are not, one might expect mites to prefer the reproducing beetle species, as they do
at UMBS. These results, along with the Farmingdale, South Dakota results, suggest
that the nature of mite host association is not predictable based solely on knowledge
of the species composition of the host community. The fact that KBS, Michigan
and Farmingdale, South Dakota share the same two dominant host species may
conceal significant differences in the selective regime associated with each beetle
species or the competitive interactions between beetle species.
As outlined above (Fig. 1.5), such aspects of the host community should highly
determine the outcome of evolution for specialization in the mites. If beetle
traits, such as degree of parental care or reproductive phenology, are themselves
geographically variable, the mosaic of "one-niche" and "multiple-niche" localities
may not be predictable based on species composition alone. The need for detailed
study of both mite and host communities is obvious.
Finally, Muller and Schwarz (1990) have documented a situation for P. carabi
on N. vespillo and N. vespilloides in Germany that is remarkably similar to the
situation at KBS. P. carabi exists as two reproductively isolated forms, with
differences in developmental times that match the leaving times of their preferred
carriers. In this case, however, the two beetle species are segregated primarily
by habitat preferences (forest and meadow, respectively), rather than seasonally.
It will be interesting to see if the two P. carabi species in Germany conform
morphologically to the species at KBS.
If morphological divergence and speciation in P. carabi are local processes
that depend on the underlying beetle community, we might expect the taxonomic
studies based on morphological variation (particularly size-related characters that
may co-vary with life-history variation) of this group to be problematic. This is

indeed the case. The more recent taxonomic treatments of the genus (e.g. Hyatt
1980) fault earlier workers for using characters to discriminate species that vary
"within samples" (a single "sample" potentially includes mites from several
sympatric beetle species). The result is a tendency to subsume many named
species in this genus into a single cosmopolitan species, P. carahi (Hyatt 1980).
Our studies suggest that "variation within a sample" may in fact reflect the
existence of closely related specialist species. However, these two species, along
with their typical morphological traits, may not be found everywhere, even when
the same host species is used. If divergence is in fact a local process that
relies on the conditions set up by the local host community, morphological
differentiation may proceed on different characters at different locations, or
intraspecific variation at one site might show up as interspecific variation at
another. It seems unlikely that any taxonomic treatment will succeed unless it
pays close attention to the complex environment in which P. carahi resides and
the ability of these mites to adapt to these local conditions.
Acknowledgments
The authors wish to thank the members of the KBS Ecology and Evolution
group for helpful advice and discussions of this work. D. Johnston and M. L.
Moraza first identified morphological variation between specialist mites. Thanks
to W. Knollenberg for assistance. This work was supported by NSF BSR
#8320457 and a NSF Graduate Fellowship awarded to 1MB. This is contribution
#704 of the Kellogg Biological Station.
References
Bartlett, 1. 1987. Filial cannibalism in burying beetles. Behav. Ecol. Sociobiol. 21: 179-
183.
Brown, J. M. 1989. Specialization in Poecilochirus carahi, a phoretic mite. Ph.D. thesis,
Michigan State Univ., East Lansing., MI.
Brown, J. M. and D. S. Wilson. 1992. Local specialization of phoretic mites on sympatric
carrion beetle hosts. Ecology 73:463-478.
Bush, G. L. 1975. Modes of animal speciation. Ann. Rev. Ecol. Syst. 6:339-364.
Diehl, S. R. and G. L. Bush. 1989. The role of habitat preference in adaptation and
speciation. In: Speciation and its Consequences (D. Otte and J. Endler eds.). Sinauer
Assoc., Sunderland, MA. Pp. 345-365.
Farish, D. J. and R. C. Axtell. 1971. Phoresy redefined and examined in Macrocheles
muscaedomesticae (Acarina: Macrochelidae). Acarologia 8: 16--29.
Futuyma, D. J. and G. Moreno. 1988. The evolution of ecological specialization. Ann.
Rev. Ecol. Syst. 19:207-33.
Hyatt, K. H. 1980. Mites of the subfamily Parasitinae (Mesostigmata: Parasitidae) in the

British Isles. Bull. Br. Mus. (Nat. Hist.) Zool. 38:237-378.
Luckinbill, L. S., T. A. Grudzien, S. Rhine. and G. Weisman. 1989. The genetic basis
of adaptation to selection for longevity in Drosophila melanogaster. Evol. Ecol. 3:31-
40.
MacArthur, M. L. 1972. Geographical Ecology. Harper and Row. NY. 269 pp.
Muller, J. K. 1987. Replacement of a lost clutch: a strategy for optimal resource utilization
in Necrophorus vespilloides (Coleoptera: Silphidae). Ethology 76:74--80.
Muller. J. K. and A-K. Eggert. 1989. Paternity assurance by "helpful" males: adaptations
to sperm competition in burying beetles. Behav. Ecol. Sociobiol. 24:245-249.
Muller, J. K. and H. H. Shwarz. 1990. Differences in carrier preference and evidence of
reproductive isolation between mites of Poecilochirus carabi (Acari: Parasitidae) living
phoretically on two sympatric Necrophorus species (Coleoptera. Silphidae). Zool.
lahrb. Syst. 117:23-30.
Peck, S. B. and M. M. Kaulbars. 1987. A synopsis of the distribution and bionomics of
the carrion beetles (Coleoptera: Silphidae) of the conterminous United States. Proc.
Entomol. Soc. Onto 118:47-81.
Rice, W. R. 1987. Speciation via habitat specialization: the evolution of reproductive
isolation as a correlated character. Evol. Ecol. 1:301-314.
SAS Institute Inc. 1985. SAS Users Guide-Statistics, Version 5. SAS Institute. Cary, NC.
Scott, M. P. and James F. A. Traniello. 1987. Behavioural cues trigger ovarian develop-
ment in the burying beetle, Nicrophorus tomentosus. 1. Insect Physiol. 33:693-696.
Service. P. M. 1985. Physiological mechanisms of increased stress resistance in Droso-
phila melanogaster. Physiol. Zool. 58:380-9.
Springett, B. P. 1968. Aspects of the relationship between burying beetles, Necrophorus
spp. and the mites, Poecilochirus necrophori, Vitz. 1. Anim. Ecol. 37:417-424.
Trumbo, S. 1988. The ecology of parental care in burying beetles (Silphidae: Necropho-
rus). Ph.D. thesis, North Carolina State Univ., Raleigh, NC.
Wilson, D. S. 1982. Genetic polymorphism for carrier preference in a phoretic mite. Ann.
Entomol. Soc. Am. 75:293-296.
Wilson, D. S. 1983. The effect of population structure on the evolution of mutualism: a
field test involving burying beetles and their phoretic mites. Am. Nat. 121:851-870.
Wilson, D. S. and W. G. Knollenberg. 1987. Adaptive indirect effects: the fitness of
burying beetles with and without their phoretic mites. Evol. Ecol. 1:139-159.
Wilson, D. S., W. G. Knollenberg and J. Fudge. 1984. Species packing and temperature
dependent competition among burying beetles. Ecol. Entomol. 9:205-216.
Wilson, D. S. and M. Turelli. 1986. Stable underdominance and the evolutionary invasion
of empty niches. Am. Nat. 127:835-850.
Wise, G. U., M. K. Hennessy and R. C. Axtell. 1988. A new species of manure-inhabiting
mite in the genus Poecilochirus (Acari: Mesostigmata: Parasitidae) predacious on house
fly eggs and larvae. Ann. Entomol. Soc. Am. 81:209-224.
Yoder, W. A. 1972. Acarina (Arthropoda: Arachnida) associated with selected Michigan
Silphidae (Coleoptera). Ph.D. thesis, Michigan State Univ., East Lansing, MI.
2
Life-History Patterns of Hummingbird Flower

Mites in Relation to Host Phenology
and Morphology
Robert K. Colwell and Shahid Naeem
CONTENTS
1. INTRODUCTION
2. EFFECTS OF HOST-PLANT PHENOLOGY ON HUMMINGBIRD
FLOWER MITES
2.1 Adaptations of Mites to S~:asonal Flowering
2.2 Behavioral Adaptations of Mites to the Phenology of Individual
Flowers
2.3 The Role of Host Phenology in Mite Population Growth and Regu-
lation
3. EFFECTS OF HOST-PLANT MORPHOLOGY ON HUMMINGBIRD
FLOWER MITES
3.1 Mite Body Size in Relation to Flower Size
3.2 Mite Breeding-Group Size in Relation to Flower Size
3.3 Sex Ratio of Hummingbird Flower Mites in Relation to Breeding-
Group Size
3.4 Sex Ratio Among Mites Dispersing on Hummingbirds
4. CONCLUSIONS
1. Introduction
Hummingbirds and the flowers that they pollinate provide an unambiguous exam-
ple of mutualism. In many cases the associations present clear evidence of
coevolution, in the strictest sense of the term (e.g. Colwell 1989). Certain species
of mites (hummingbird flower mites) exploit this bird-plant mutualism, with
known examples throughout most of the geographic range of the hummingbirds
(Trochilidae), which spans the New World from Alaska to Tierra del Fuego
(Colwell 1985). This ecologically-defined group of gamasid mites (all within the
Ascidae) encompasses all described species of the genus Rhinoseius, which
inhabit a zone from northern Califo:mia to central Chile, plus a diverse tropical
23
24 I R. K. Colwell and S. Naeem
lineage within the genus Proctolaelaps. These two ecologically similar lineages
have spawned an impressive adaptive radiation of species (Colwell 1979).
To date, only 46 species of hummingbird flower mites have been described
(Baker and Yunker 1964; Dusbabek and Cerny 1970; Hunter 1972; Fain et al.
1977a, 1977b; Flechtmann and Johnston 1978; Hyland et al. 1978; Colwell
and Naeem 1979; Fain and Hyland 1980; Micherdzinski and Lukoschus 1980;
Zamudio 1985; OConnor et al. 1991). Additional specimens are currently under
study that represent collections from 50 hummingbird species and over 100 plant
taxa (17 different families). Moreover, many geographical areas (including most
of the Amazon) remain entirely unexplored for hummingbird flower mites.
Hummingbird flower mites feed and mate within the floral corolla, and females
lay their eggs on the host plant. The ontogeny begins with a brief egg stage,
followed by a six-legged larva, succeeded by an eight-legged protonymph, a
deutonymphal stage, and then adult males and females. No diapause is known to
occur among these species, and generation time is about a week (Colwell 1973,
Dobkin 1984). All stages feed on nectar and later stages include pollen in their
diet as well.
Although mites move freely on foot among newly opened flowers within an
inflorescence and rest in refuges beneath bracts or bud-clusters of that inflores-
cence (Dobkin 1984), movement among inflorescences or plants is almost exclu-
sively by hitch-hiking on hummingbirds (Colwell et al. 1974). The mites ride
within the nasal cavity of these birds, but they are not parasitic and have no
detectable effect on the birds under normal densities (1-15 mites per bird)-a
clear case of phoresy (Athias-Binche 1991).
In this chapter, we will explore the role that the host plant plays in the evolution
of the life history traits of hummingbird flower mites. We will show that the
seasonal timing of flowering profoundly affects patterns of host affiliation,
whereas daily flowering patterns affect the evolution of mite behavior. The size
of an inflorescence and its phenology play key roles in the population growth and
dispersal of these mites. Floral morphology affects mite body size and local
breeding-group size, which in tum lead to adaptive differences among species in
both the sex ratio of mites within flowers and the sex ratio of dispersers on
hummingbirds.
2. Effects of Host-Plant Phenology on Hummingbird Flower Mites
2.1 Adaptations of Mites to Seasonal Flowering
The local species richness of hummingbird flower mites ranges from a single
species, at the latitude of California or central Chile, to some 15 sympatric species
in lowland tropical forests, such as the Arima Valley of Trinidad (Colwell 1986a).
The annual phenology of plants largely determines patterns of host-plant species
used by hummingbird flower mites. Each mite species depends upon a clearly
Life History Patterns of Hummingbird Flower Mites / 25
delimited host-plant repertoire of one to several species of hummingbird-polli-

nated plants. Monophagy is the rule for mites whose host produces flowers all
year round-a common flowering pattern in some parts of the wet lowland
tropics. In the Arima Valley of Trinidad, for example, 11 of the 15 sympatric
hummingbird flower mite species (for which we have adequate data) are monopha-
gous. Each has a single host-plant species that flowers throughout the year
(Colwell 1986a), although there are often distinct flowering peaks and lags
(Feinsinger et al. 1982). Since hummingbird flower mites have no diapause stage,
monophagous species can exist only on such reliable host-plant species.
Where flowering is seasonal (in tropical montane, subtropical, and temperate
habitats) hummingbird flower mites are almost exclusively polyphagous and
follow an annual cycle of host shifts. As flowering wanes in one host-plant
species, they move onto another just coming into bloom. For these "sequential
specialists," the annual repertoire of movements is usually tied to hummingbird
visitors to these plants, which have the same shifts.
A less common expression of polyphagy in hummingbird flower mites relies
on the exploitation of one or two "home base" host-plant species that flower year-
round and the additional utilization of one or more secondary hosts that have a
brief flowering season. Examples include Proctolaelaps certator in Trinidad, and
Rhinoseius colwelli and R. richardsoni at Cerro de la Muerte in the Costa Rican
highlands (Colwell 1973, 1983).
Among polyphagous species, host-plant utilization appears to be largely uncor-
related with host-plant phylogeny. R. chiriquensis from Monteverde, Costa Rica,
for example, occupies five sequential hosts that belong to four different plant
orders. R. epoecus, which travels on migrant California hummingbirds, expresses
a variation on the sequential specialist theme. It has summer host plants in
California, and shifts between winter host plants and summer ones, in different
plant families, in west-central Mexico (Colwell and Naeem 1979). In the case of
monophagous mites, cospeciation in response to the evolutionary divergence of
their host plants remains a possibility. An ongoing investigation seeks to explore
the phylogenetic relationships of the mites in relation to the phylogenetic relation-
ships of their host plants to evaluate this possibility.
Most host-plant species support only a single species of hummingbird flower
mite, but a few cases of "host sharing" by two species are known. In these cases,
the role of host phenology is doubly evident. In virtually all known cases of
host sharing, the two species involved have identical host repertoires, reflecting
independent evolutionary responses to host phenology. We have documented
cases of monophagous pairs (e.g. P. contumex and R. uniformis [Fig. 2.1] share
the plant Cephaelis muscosa in Trinidad) as well as polyphagous pairs (P. certator
and R. klepticos both share two species of H eliconia in Trinidad) (Colwell 1986a).
Like these two examples, all other known cases of regular host sharing also
involve a species of the genus Rhinoseius and a species of genus Proctolaelaps,
never two species of the same genus. Host sharing is a key piece of evidence in
26 / R. K. Colwell and S. Naeem
Figure 2 .i. Hummingbird flower mite, a male Rhinoseius uniformis (Gamasina: Ascidae)
from Trinidad, W.I. This species inhabits the flowers of the plant Cephaelis muscosa
(Rubiaceae) and travels between inflorescences primarily on the hummingbird Amazilia
tobaci. Drawing and copyright by Shahid Naeem.
support of the hypothesis that the host range is narrowed and that host fidelity is
amplified in these mites by selection for mate-finding, using the host plant as a
congregation cue (ColwellI986a, 1986b). The constraint that host sharers must be
noncongeners is explained by the considerable differences observed in courtship
behavior and morphology between genera. According to this hypothesis, conge-
ners must use different host plants as mate-finding cues to avoid accidental
matings.
In contrast to the strong fidelity that mites have for particular host-plant species,
their use of hummingbirds for dispersal appears to be entirely opportunistic. An
individual hummingbird, regardless of species, usually carries a sampling of
mites from all the host plant species the bird has recently visited. The passenger
manifest sometimes includes as many as five mite species. Yet each mite disem-
barks from the bird only at flowers of the preferred plant species. Behavioral tests
show that mites prefer the nectar of their usual host-plant species over nectar of
host plants characteristic of sympatric hummingbird flower mite species, or a
plain sugar solution (the control) (Heyneman et al. 1991).
2.2 Behavioral Adaptations of Mites to the Phenology of individual Flowers
Among plant species, individual floral longevity generally tends to increase with
both altitude and latitude (Stratton 1989). Flowers utilized by hummingbird flower
mites also vary in the period of time they remain in good condition and continue
to produce nectar. Depending on plant species, some flowers last less than a day
whereas others may persist for more than a week. In the lowland tropics, very
few hummingbird-pollinated flowers last more than a single day (Feinsinger et
al. 1982, Primack 1985).
Floral longevity profoundly affects the lives of hummingbird flower mites.

Behavioral differences among mite species, correlated with longevity, appear to
be clearly adaptive. For example, at Cerro de la Muerte in Costa Rica (3100
m), R. colwelli completes its entire life cycle within flowers of two species of
Centropogon (Lobeliaceae). These protandrous flowers produce nectar for more
than a week, as they mature from the staminate to the pistillate stage. R. colwelli
lays its eggs in communal clusters inside the base of the floral tube, where the
eggs are bathed in nectar. The eggs require 2-3 days to hatch (Colwell 1973). In
lowland Trinidad, the only common plant with flowers that persist for more than
a day is another species of Centropogon. The reproductive behavior of its resident
mite, P. glaucis, is identical to that of R. colwelli, even though it belongs to a
different mite genus.
In contrast with the persistent flowers of Centropogon, some hummingbird-
pollinated plants in the tropics flower before dawn and by early afternoon not
only cease producing nectar, but actually shed their flowers. Mite species affiliated
with these plants clearly would not do well to lay their eggs in these flowers-
and indeed they do not.
In Trinidad, Dobkin (1984, 1990) has studied R. trinitatis, which inhabits the
flowers of Heliconia hirsuta (Heliconiaceae). In the morning hours the flowers
teem with mites, but none can be found in the same flowers later when they fall
from the plant, almost synchronously, between 1400 and 1500 h. These mites
retreat to cincinnal bracts of H. hirsuta to lay their eggs and to await the opening
of fresh flowers to feed on the following morning.
The plant H. psittacorum, home of P. phaethornis in Trinidad, also drops all
open flowers each afternoon, but not before the mites abandon the flowers for
the safety of the inflorescence bracts. When Dobkin (1984) introduced an "alien"
Proctolaelaps species (P. cerlator,. which had no historical association with H.
psittacorum) into the flowers of this Heliconia, the aliens failed to leave the
flower before excision and ultimately perished. The flowers of the four plant
species that P. certalor normally inhabits (Colwell 1986a) all remain on the plant,
even beyond pollination and wilting. The behavior of P. phaethornis permits it
to exploit one-day, deciduous flowers, while the behavior or P. certator makes
sense in context of the persistent flowers of its own host plant.
In Costa Rica, we have studied in detail the behavior of P. kirmsei, which
inhabits flowers of Hamelia patens (Rubiaceae). In this plant, the tubular flowers
begin to open at about 0100 h. Mites that had been waiting in groups in the axils
of the cymose inflorescence rush into the slowly enlarging aperture at the tip of
the flower as soon as it is wide enough. They immediately begin burrowing into
the anthers to feed on pollen grains, while dramatically increasing the level of
social interaction. Most matings take place within the flowers before dawn, as
nectar begins to flow and hummingbirds begin to visit. By noon, the flowers are
easily dislodged from the plant and many fall to the ground, but by then the mites
have left the flowers to return to their staging areas in the axils of the inflorescence,
or beneath the first pairs of leaves, where they lay their eggs (Colwell 1985).
Remarkably, P. kirmsei repeated the same temporal pattern of behavior in a

completely artificial "habitat" (Fig. 2.2A) in a series of experiments conducted
in a screened laboratory at La Selva Biological Station in Costa Rica, under
ambient temperature and light conditions. This apparatus was constructed of a
lattice of intersecting capillary tubes representing the "inflorescence." Projecting
outer tubes represented the "flowers," with fresh, virgin nectar from H. patens
in their tips; all other tubes were dry. P. kirmsei, placed in the outer ("flower")
tubes at the beginning of an experiment, initially moved freely throughout the
lattice. But mites tended to return to the "flower" tubes at about the same time
of night (0100-0700 h) that the flowers of H. patens were opening outdoors.
Later, in the middle of the day, they moved back out of the "flower" tubes into
the lattice as the flowers began to fall from the plants outdoors, even though
plenty of nectar remained in the capillary tubes (Fig. 2.2B).
2.3 The Role of Host Phenology in Mite Population Growth and Regulation
The rate at which an inflorescence produces flowers varies greatly among plant
species. Most plants pollinated by hummingbirds in the wet tropics produce one
or two flowers per inflorescence each day. However, the "lifetime" of any single
inflorescence usually spans a few weeks and sometimes much longer. Especially
in plants pollinated by circuit-foraging hummingbirds ("trapliners," see Fein-
singer and Colwell 1978), an individual plant often produces only one flowering
inflorescence at a time. Some inflorescences, such as those of certain Costus and
Heliconia species, may flower for an entire year. In contrast, plants pollinated
by territorial hummingbirds tend to have many inflorescences in flower at once,
each producing one or a few flowers per day over several weeks.
In all cases we have studied, it is clear from observations and experiments that
mites move freely (on foot) between successively or simultaneously open flowers
of the same inflorescence. Phoresy on hummingbirds is the general rule for
movement among inflorescences within a plant, and a necessity for movement
among plants. Based on 90 individual hummingbirds representing nine humming-
bird species in Trinidad, the number of hummingbird flower mites apparently
averages fewer than five per bird (range 0-15). In contrast, the total number of
mites collected from all the flowers of an individual hummingbird's exclusive
territory or on its foraging circuit would be 2-4 orders of magnitude greater than
the mean number of mites the bird carries at any given moment. The inescapable
conclusion is that dispersal on birds, however important in the global population
structure of these mites, is a relatively rare event in the lives of individuals.
Indeed, the great majority of individual hummingbird flower mites very likely
never leave their natal inflorescence.
We have carried out a detailed study of the population structure and dynamics
of one hummingbird flower mite, P. kirmsei, at La Selva Biological Station in
Costa Rica. Its host plant, H. patens, an understory treelet that can reach 3-4 m
@=~==t::::::6:::::::1===t::::::6:::::::1====t::::::6:::::::l=====-!~~il
[§I F===f::::::6:::::::I=====t:::::::~::::::=F- ==t:<::

[~ [~
(A)
Figure 2.2. Apparatus and results for an experiment demonstrating adaptive die! move-
ments of hummingbird flower mites in the field laboratory. A) Lattice apparatus. Each of
nine Plexiglas blocks (50X50X6 mm) had a central chamber (10 mm 10, 3 mm deep),
with four lateral holes drilled to receive standard coagulation capillary tubes (75 mm long,
1 mm ID). Prior to starting an experiment, each central chamber was covered with a
circular cover slip (18 mm), secured with clear tape. To represent "flowers," a drop of
virgin nectar was placed in the distal tip of each of the outer tubes, which were capped
with Critocap PVC tube closures. Mites were introduced by coaxing them into the uncapped
end of the lateral tubes before inserting the tubes into the blocks. Mites moved freely
throughout the sealed lattice during each experiment. B) Proportion of 48 mites (Proctolae-
laps kirmsei) found within 3 em of nectar drops at various hours of the day. Mite movement
in the tubes paralleled the pattern of flower use seen in the field. Having started out in the
lateral tubes (the "flowers"), the mites tended to move away from them at roughly the time
of day when their host flowers cease to be habitable in the field, returning to the lateral
tubes during the hours when their host flowers begin to open in nature. Solid and open
points represent two replicates typical of a longer series of experiments. Shaded bars
represent nighttime hours.
29
-
Dark Light
··en 50 •
CI)
~
-.
0 40 •••
u •
··t: • •
30 • 0 00
en 00 0
..,
CI) 0
•
:e 20 0
....
-
0
.c 1 0
CI)
E
:l
Z
0
12 24 12
Time of Day
(B)
Figure 2.2. (Continued)
in height, bears from 1-100 simultaneously flowering inflorescences, depending

on plant size. The plant flowers all year round, and there is no evidence of
synchrony in the initiation of flowering of different inflorescences on the same
plant. At the study site, each active inflorescence produces a mean of 1.5 open
flowers per day (range: 0-5 open flowers per day). The total number of flowers
produced during the life of an inflorescence is quite variable, ranging from about
30 (three weeks of flowering) to more than a 100 (10 weeks of flowering)
(Newstrom et al., in press).
One can accurately estimate the number of days since the initiation of flowering
of an inflorescence of Hamelia (the "age" of the inflorescence) by summing the
number the attached fruits and the number of pedicel scars (indicating fruits
removed by frugivorous birds or aborted) and dividing by the mean number of
flowers per day (1.5 at the study site). Estimating inflorescence age in this manner,
we documented the rate of local population growth in inflorescence breeding

groups by censusing the mites in inflorescences of different ages. To census an
inflorescence, all open flowers were picked on successive days until no more
mites were found. The mites from these flowers were tallied by stage and sex.
Although the great majority of mites were usually collected on the first day,
newly-hatched larvae and stragglers of later stages often appeared for up to 3-4
days. After the first day, the inflorescence was covered with a nylon mesh bag
and the subtending peduncle (inflorescence stem) was ringed with Tanglefoot to
prevent entry or exit of mites, either on foot or by phoresy on hummingbirds.
The results of these censuses show a clear pattern of density-dependent popula-
tion growth, with no evidence of a "lag phase" (no inflection point) preceding
the most rapid phase of population growth (Fig. 2.3). We do not yet know
whether a decrease in birth rate, an increase in mortality, emigration, or a
combination of these factors accounts for the rapid decline in population growth
as the population nears its carrying capacity. Nor do we yet know the potential
sources of mortality.
Experimental populations were later initiated by allowing hummingbirds to
visit previously censused and cleared inflorescences, followed by rebagging and
then censusing at intervals (details to be reported elsewhere). The resulting best-
fit popUlation growth curve did not differ significantly from the curve in Figure
2.2. These experiments also produced an estimated immigration rate from birds
of only 4-8 mites per day per inflorescence. One day's immigrants from hum-
mingbirds were sufficient to initiate inflorescence populations indistinguishable
from those in Figure 2.2B.
What happens to the mites that remain on an inflorescence of Hamelia after it
finishes flowering? Because buds are formed several days before opening, it is
easy to identify an inflorescence that has just one bud left to open before complet-
ing its period of flowering. On the morning that the final flower opens, mites
gather in a dense aggregation at its tip. A twig touched gently to such a flower
is quickly covered with mites rushing to depart. One might presume that a
hummingbird's bill receives the same response. In contrast, equally numerous
mites inhabiting younger inflorescences can rarely be seen on the flowers at all
during the day.
A simple experiment demonstrated the fate of those mites that fail to mount a
hummingbird's bill from the final flower in a Hamelia inflorescence. Ten such
flowers were located. Five were left untouched; the peduncles (inflorescence
stems) of the other five were ringed with Tanglefoot to prevent emigration on
foot by the mites. No bags were applied in either treatment, leaving all flowers
open to visitation by hummingbirds. The final flowers appeared the following
day. On the second day, when all flowers had fallen from the inflorescences or
had wilted, the inflorescences were examined carefully for mites. In each of the
inflorescences that had been ringed with Tanglefoot, we found numerous mites
wandering actively on the branches of the inflorescence. In contrast, none of the
control inflorescences had any mites at all. Clearly, the mites in these inflores-
--
-
..:.•
Z
en
Q)
()
c:
Q)
()
en 100 • • •
...o
Q)
••
:;::
c:
• • •• •• •
W•
c: I •
en
Q)
:!::
• •
10
:5
-...
o
Q)
N(t) = K (1- e
- (r/K)t)
.a
E o
Z
::::J
o 10 20 30 40 50
Fruits (t)
Figure 2.3. Density-dependent population growth for inflorescence breeding groups of
the mite Proctolaelaps kirmsei on the host plant Hamelia patens, inferred from censuses
of groups of different ages. "Breeding group," defined here as the total number of adults
present (males plus females), is plotted on a logarithmic scale. The flowering age of the
inflorescence, and thus the age of its group of inhabiting mites, can be estimated from the
number of fruits plus fruit scars on that inflorescence. At the study site (La Selva Biological
Station, Costa Rica), the host plant produced an average of 1.5 fruits per day during the
study, so that 10 fruits approximate a period of one week. The line was fitted by nonlinear
regression (R 2 = 0.84) with a least-squares loss function (Wilkinson 1989), with parameters
rand K estimated from the data: in arithmetic units, r = 7.56 and K = 33.8 mites.
cences had left on foot to seek their fortunes elsewhere on the plants. The striking
universality of this emigration behavior suggests that it must sometimes payoff.
3. Effects of Host-Plant Morphology on Hummingbird Flower Mites
3.1 Mite Body Size in Relation to Flower Size
The body size of hummingbird flower mites, as measured by the length of the
dorsal shield, varies between 0.3 mm-D. 7 mm (OConnor etal. 1991). The flowers
that these mites inhabit range from 10 mm to more than 70 mm, as measured by
corolla depth. That mite size is positively correlated with flower size (Fig. 2.4)
may seem reasonable (an inverse correlation would certainly be more surprising),
but no explanation for this pattem can be advanced with certainty. Nectar flow
rate (per flower) is generally correlated with flower size in plants (Cruden et al.
1983), and physical space inside the corolla is certainly related to tube depth, on
average. But neither nectar flow rate nor total physical space available provides
a logical explanation for the relation between mite size and flower size.
Two anomalous cases present informative exceptions. Both the largest mite,
Proctolaelaps contentiosus (P. c. in Fig. 2.4) and the smallest mite, P. glaucis
(P. g. in the figure), inhabit flowers of medium length. The urn-shaped corollas
of Renealmia exaltata flowers, however, which are inhabited exclusively by P.
contentiosus, have much greater internal volume than other flowers of medium
depth that we studied, perhaps pemlitting this large mite to prosper. In contrast,
the corollas of Centropogon cornutus flowers, inhabited exclusively by P.
glaucis, permit access to the nectaries only through five narrow openings (about
0.4 mm in diameter) between the bases of the filaments (Colwell 1986b). Visiting
hummingbirds extract nectar with their tongues through these openings; the
unusually small size of P. glaucis permits the mite to reach the nectar by walking
through them. The body of P. glaucis is only slightly smaller than the diameter
of the openings.
With these clues in mind, we conjecture that (on average) physical constraints
on movement within flowers scale with flower size such that larger mites are at
a competitive disadvantage, as compared to smaller mites, in smaller flowers (see
Kirk 1991). To complete the explanation, though, we must also propose some
advantage to larger size in larger flowers, or else all mites would do just as well
to be as small as those in the smallest flowers. Candidate forces include natural
selection for greater fecundity, for decreased susceptibility to desiccation (Dobkin
1985) or for faster running, or sexual selection for greater body size through
female choice or male-male combat (Colwell 1973).
Selection for faster running might at first seem logical because longer-tubed
flowers are necessarily visited by longer-billed hummingbirds (Feinsinger and
Colwell 1978). Thus, mites disembarking at such flowers have farther to run to
reach a point of contact between bill and corolla, as the bird feeds on the flower.
On the other hand, visits to larger flowers last longer because larger flowers have
more nectar to be harvested. This issue clearly cannot be resolved by qualitative
arguments.
3.2 Mite Breeding-Group Size in Relation to Flower Size
Not surprisingly, the more abundant nectar flow and pollen supply of larger
flowers tend to support a greater biomass of hummingbird flower mites than
smaller flowers can support. Because mites that live in larger flowers are larger
600
P. c.
• •
3:
-Q)
.~
500 • • •
en
>-
'0
o
m
•
Q)
.'t::
~ 400
r = .54
P. •g. P = .038
300
0 20 40 60 80
Corolla Depth (mm)
Figure 2.4. Body size of hummingbird flower mites as a function of the depth of the
corolla tube of their host plants. Each point on the graph represents a different species of
hummingbird flower mite in its characteristic host-plant species. The regression line and
significance level indicated were computed for all points, including outliers marked "P.
c.," which represents Proctolaelaps contentiosus in its host plant Renealmia exaltata, and
"P. g.," which represents P. glaucis in the flowers of its host plant Centropogon comutus
(without these two outliers, r = 0.776, P = 0.002). These two cases are discussed in the
text. Corolla tube depth was measured inside each flower, from the deepest point to the
lower "lip" (in zygomorphic flowers) of the corolla. "Mite size" represents the length of
the dorsal shield, computed as the intersex mean. The data include all mite species listed
in Table 24.1 of Colwell (l986b) for Arima Valley, Trinidad, West Indies, except for
those with unknown (P. mermillion) or poorly known (P. phoreticus) host plants.
34
Life History Patterns of Hummingbird Flower Mites I 35
in body size (Fig. 2.4), however, larger flowers might nonetheless support the
same number of mites as smaller flowers. In fact, hummingbird flower mite
species that inhabit larger flowers live in larger groups, as measured by the
number of adult mites per inflorescence (Fig. 2.5). This pattern would simply be
amplified if mites of all species had the same body size.
3.3 Sex Ratio of Hummingbird Flower Mites In Relation to Breeding-Group

Size
The life history consequences of mite breeding-group size (and thus, of host-
plant morphology) that we have studied, to date, center on issues of variation in
100
•
40
20
•
•
10
• ••
-...
o 4 •
Q)
.Q • r = .64
E
2 • • = .004
•
::l P
Z
1
0 20 40 60 80
Corolla Depth (mm)
Figure 2.5. Mean numbers of adult hummingbird flower mites in flowers in relation to
corolla depth of their host plants. Each point represents a different mite species in a
characteristic host-plant species. Data include the same species as in Figure 2.4, with the
addition of species listed for Cerro de la Muerte, Costa Rica, in Table 24.1 of Colwell
(1986b) and Proctolaelaps kirmsei in two secondary hosts in Trinidad. The Y-axis is scaled
logarithmically; Y-values are estimated as the antilog of the mean log number of adults
per flower in samples of flowers (n = 4-37, depending upon plant species). Corolla length
was measured as described for Figure 2.4.
sex ratio. Like many other species of mites, as well as other arthropods that live
in small, relatively isolated breeding groups (Hamilton 1967; Wrensch et aI., this
volume), hummingbird flower mites have female-biased sex ratios. The degree
of bias, however, varies greatly among hummingbird flower mite species and
depends upon the typical size of the inflorescence breeding group (Fig. 2.6),
defined here as the total number of adults present (males plus females). Mite
.50
'"
Q)
u
c:::
Q)
.40
u
...'0"
Q)
.30
:;
c:::
c:::
-
.20
'"
Q)
:i
j!
tU
.10 •
:i:
c::: .05
0
...
:;::
0 r = .78
c. P < .001
...c.0 .01
1 2 4 10 20 40 100
Breeding Group Size:
Number of Adult Mites in Inflorescences
Figure 2 .6. Sex ratio of hummingbird flower mites (plotted as proportion males) on their
host plants in relation to breeding-group size (number of adults). Species that live in
smaller groups have more female-biased sex ratios. The Y-axis is an arcsine-square-root
scale; Y-values of the points plotted represent arithmetic equivalents of the means of
arcsine-square-root transformations of the proportion males collected from individual
inflorescences (the number of inflorescences ranged from 4-37, depending upon plant
species). The X-axis is scaled logarithmically; X-values of points are estimated as the
antilog of the mean log number of adults per inflorescence (for the same samples used for
Y-values). The points represent the same species as in Figure 2.5, except that the data for
Proctolaelaps kirmsei on its alternate hosts are not included.
species that breed in small groups (in small flowers) have much more female-
biased sex ratios than mites that live in larger groups (in larger flowers). Species
with the largest groups of all, such as Rhinoseius fidelis, which live in groups of
up to 1,000 adults (mean about 100) in the giant flowers of Costus arabicus (=
C. niveo-purpurea of Colwell 1986a) in Trinidad, have nearly equal numbers of
male and females.
Unlike certain wasps (e.g. Werren 1980, Herre 1985), hummingbird flower
mites show no correlation, within species, between breeding-group size and sex
ratio. The characteristic sex ratio of each hummingbird flower mite species is
apparently a fixed adaptive response to the average conditions the species encoun-
ters, rather than the expression of an adaptive capacity for facultative sex-ratio
adjustment.
Why should mites living in smaller groups have more female-biased sex
ratios? Fisher (1930) showed that, in a random-mating population, a female can
maximize her fitness, as measured by copies of her genes among grandprogeny,
by producing half daughters and half sons. Colwell (1981) demonstrated that
Fisher's conclusions apply with equal force within random-mating, finite groups,
however small-even among the progeny of just two females. In a population
that is structured into temporarily separate groups, however, those groups with the
most female-biased progeny sex ratio produce the most grandprogeny (assuming
fecundity is independent of sex ratio). In other words, within-group selection
favors unbiased sex ratios, while between-group selection favors the maximum
level of female bias possible, consistent with full fertilization.
In the case of hummingbird flow{~r mites and other organisms with temporary
breeding groups that persist for several generations, breeding-group size enters
into sex-ratio evolution by way of between-group genetic variation. It is this
variation that is the grist for the mill of group selection, just as among-individual
(in this case, within-group) genetic variation is the raw material of individual
selection. For any genetically variable trait, variation in gene frequencies among
small groups is greater than that among larger groups, simply due to sampling
error. Thus, in a species that tends to form smaller breeding groups, the force of
group selection (which favors female progeny) more effectively counters the
force of individual selection (which favors equal numbers of sons and daughters)
than in a species that forms larger breeding groups. The graded balance between
these two opposing levels of selection would be expected to produce just the kind
of relationship between group size and sex ratio shown in Fig. 2.6 (Wilson and
Colwell 1981).
Alternative models for the evolution of female-biased sex ratios based on genic
selection (e.g. Hamilton 1967) are mathematically equivalent to the levels-of-
selection approach for the single-generation case (Colwell 1981), but much more
difficult to apply in the case of multi generational groups. Moreover, the verbal
exegesis usually given these genic models, which is based on competition for
mates (local mate competition; e.g. Alexander and Sherman 1977; Harvey et a1.
1985), has little meaning for long-lived groups and may be seriously questioned
even for one-generation groups (Colwell 1981, 1982).
To evaluate the potential for significant among-group genetic variation in
hummingbird flower mites, a genetic-demographic model is under development
that incorporates parameters estimated from the experimental work on P. kirmsei
discussed above. We will test its predictions through direct molecular assessment
of the partitioning of genetic variation within and among groups (Christiansen
1992).
3.4 Sex Ratio Among Mites Dispersing on Hummingbirds
From the analysis of mites collected from hummingbirds, we have discovered

that hummingbird flower mite species vary in the sex ratio of dispersing individu-
als. One might imagine, as a first guess, that the variation would parallel sex-
ratio differences among mite species in the flowers of their host plants (Fig. 2.6).
Even if females were in general more likely to disperse than males (a common
pattern among phoretic mites [Athias-Binche 1991]), a plot of the proportion of
migrating males regressed against the size of the inflorescence breeding groups
for the same set of species would at least be expected to have a positive slope,
although with an intercept below that of Figure 2.6.
In fact, the sex ratio of mites on birds shows precisely the opposite relationship
from this naive expectation. Males of mite species that live in smaller groups
(which have highly female-biased sex ratios in flowers) are far more likely to
disperse on birds than males of mite species that live in larger groups (which have
less biased sex ratios), relative to females. The resultant plot of the proportion of
males on birds against group size for the same species in flowers (Fig. 2.7) yields
a negative slope.
The explanation we propose for this pattern depends upon three premises-( I)
that there is some cost or risk to dispersal; (2) that the primary reward for dispersal
among female mites is the successful founding of a new dynasty in a newly-
flowering, unoccupied inflorescence or movement to a less crowded inflorescence;
and (3) that the benefit to dispersal among male mites is increased access to
unmated females.
There is no reason to expect that the probable dispersal reward to females
should vary among species in any regular way with breeding-group size. In
contrast, males of species that live in smaller groups often have more to gain
from dispersal than males that live in larger groups, because sex ratio ought to
vary stochastically more among smaller groups than among larger groups, simply
due to binomial sampling error. Dispersal should be a risk worth taking for a
male of a species that lives in small groups and who also happens to find himself
in a group with a greater proportion males than the average for his species. The
next inflorescence the hummingbird visits may well have considerably more
females per male. On the other hand, the sex ratio in a species that lives in large
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Breeding-Group Size:
Number of Adult Mites in Inflorescences
Figure 2.7. Sex ratio of hummingbird flower mites (plotted as proportion males) on their
hummingbird carriers in relation to breeding-group size (number of adults) for the same
mite species on their host plants. Males of species that live in smaller groups are more
likely to disperse on birds than males of species that live in larger groups. Axes are scaled
as in Figure 2.6. Y-values of the points plotted represent arithmetic equivalents of the
arcsine-square-root-transformation of the proportion male mites collected from humming-
birds (pooled data for mites collected from 90 hummingbirds of seven species; sample
size for the mite species plotted ranged from 16-153 individuals, depending upon mite
species). X-values, which correspond to those of Figure 2.6, represent breeding-group
size for the characteristic host plant of each mite species. The data plotted are limited to
Trinidad and to species for which at least IS mites were collected from hummingbirds
during the study.
39
groups varies little among inflorescences. In such a species, moving from one
inflorescence to another by hummingbird yields little gain for the risk.
As expected from the binomial theorem, variation in sex ratio among inflores-
cences (estimated by the standard deviations of male proportions, transformed to
arcsines of square roots) is negatively correlated with breeding-group size, among
mite species (r = - 0.71, P = 0.021 for the same species plotted in Figure 2.6).
The positive correlation between sex-ratio variation in flowers and the proportion
of male mites on birds, however, is equally significant (Fig. 2.8; r = 0.71, P =
0.022), concordant with the hypothesis that male mites disperse when variation
in sex ratio among groups makes it worthwhile.
We are currently using two experimental approaches to test some of the
implications of this hypothesis. First, we have confirmed the ability of male mites
to detect local sex ratios and to react behaviorally by seeking groups with more
favorable ratios. These experiments were done in experimental "lattices" like the
one depicted in Figure 2.2A (data to be reported elsewhere). Second, we have
begun to investigate the affects of sex-specific odors in nectar on the behavior of
both male and female mites, using apparatus described by Heyneman et al. (1991).
We expect these studies to provide a better understanding of the hypothesized
relationships among breeding-group size, sex ratio, and migration.
4. Conclusions
The hummingbird flower mites represent an ecologically and phylogenetic ally

coherent group of species. They have enjoyed a highly successful adaptive
radiation onto a phylogenetic ally , phenologically, and morphologically broad
spectrum of host-plant lineages, which are united only by their reliance on
hummingbirds for pollination. From our explorations of variation in morphology,
behavior, and life history among these mites, we conclude that virtually every
aspect of their lives is affected by features of host-plant phenology and morphol-
ogy-including mite body size, daily cycles of behavior, annual shifts in affilia-
tion with host plants, population growth and regulation, breeding-group size,
patterns of dispersal, genetic structure of populations, and sex ratio.
Acknowledgments
We gratefully acknowledge the collaboration of David Dobkin and Amy

Heyneman in key phases of this work. We also express our thanks, for assistance
both technical and intellectual, to Beth Braker, Eugenia Chavarria, Robin Chaz-
don, Kim Christiansen, David Clark, Deborah Clark, Peter Feinsinger, Marilyn
Houck, Marek Kaliszewski, and Barry OConnor. George Hurtt derived the equa-
tion fitted in Figure 2.3. This work would not have been possible without the
hospitality and facilities of Simla Research Station (Trinidad) and La Selva
Biological Station (Costa Rica) or without financial support from the National
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Standard Deviation of Proportion Male
Mites in Inflorescences
Figure 2 .8. Sex ratio of hummingbird flower mites (plotted as proportion males) on their
hummingbird carriers in relation to sex-ratio variation for the same mites species on their
host plants. Males of species that live in groups that vary more in sex ratio are more likely
to disperse on birds than males of species that live in groups that vary less in sex ratio.
Y-values of the points plotted and the species included are the same as in Figure 2.7. X-
values of the points, which represent variation in mite sex ratio among inflorescences for
the characteristic host plant of each mite species, represent arithmetic equivalents of the
standard deviations of arcsine-square-root transformations of the proportion males col-
lected from individual inflorescences (the number of inflorescences ranged from 4-37,
depending upon plant species).
Science Foundation (DEB-7812038, BSR 86--04929, BSR-8906228, and BSR-

9025024) and from the Universities of California and Connecticut.
References
Alexander, R. D. and P. W. Sherman. 1977. Local mate competition and parental

investment in social insects. Science 196:494-500.
Athias-Binche, F. 1991. Ecology and evolution ofphoresy in mites. In: Modern Acarology,
Vol. 1 (F. Dusbabek and V. Bukva eds.). Academia, Prague, and SPB Academic Publ.,
The Hague. Pp. 27-41.
Baker, E. W. and C. E. Yunker. 1964. New blattisociid mites (Acarina: Mesostigmata)
recovered from Neotropical flowers and hummingbirds' nares. Ann. Entomol. Soc. Am.
57: 103-126.
Christiansen, K. M., R. K. Colwell and M. J. Kaliszewski. 1992. Cellulose acetate
electrophoretic techniques for the genetic analysis of individual ascid mites (Mesostig-
mata: Ascidae). Int. 1. Acarol. 18:97-105.
Colwell, R. K. 1973. Competition and coexistence in a simple tropical community. Am.
Nat. 107:737-760.
Colwell, R. K. 1979. The geographical ecology of hummingbird flower mites in relation
to their host plants and carriers. In: Recent Advances in Acarology. Vol. 2 O. G.
Rodriguez ed.). Academic Press, NY. Pp. 461-468.
Colwell, R. K. 1981. Group selection is implicated in the evolution of female-biased sex
ratios. Nature 290:401-404.
Colwell, R. K. 1982. Female-biased sex ratios. Reply to Charlesworth and Toro, Wildish.
and Borgia. Nature 298:494-496.
Colwell, R. K. 1983. Rhinoseius colwelli (Acara floral del colibri, totolate floral de colibri,
hummingbird flower mite). In: Costa Rican Natural History (D. H. Janzen ed.). Univ.
Chicago Press, Chicago. P. 619, and pp. 767-768.
Colwell, R. K. 1985. Stowaways on the Hummingbird Express. Nat. Hist. 7:56-63.
Colwell, R. K. 1986a. Community biology and sexual selection: Lessons from humming-
bird flower mites. In: Ecological Communities (T. J. Case and J. Diamond eds). Harper
and Row, NY. Pp. 406-424.
Colwell, R. K. 1986b. Population structure and sexual selection for host fidelity in the
speciation of hummingbird flower mites. In: Evolutionary Processes and Theory (S.
Karlin and E. Nevo eds.). Academic Press. NY. Pp. 475-495.
Colwell, R. K. 1989. Hummingbirds of the Juan Fernandez Islands: natural history,
evolution and population status. Ibis 131:548-566.
Colwell, R. K. and S. Naeem. 1979. The first known species of hummingbird flower mite
north of Mexico: Rhinoseius epoecus n.sp. (Mesostigmata: Ascidae). Ann. Entomol.
Soc. Am. 72:485-491.
Colwell, R. K., B. 1. Betts, P. Bunnell, F. L. Carpenter and P. Feinsinger. 1974.
Competition for the nectar of Centropogon valerii by the hummingbird Colibri thalassi-
nus and the flower-piercer Diglossa plumhea, and its evolutionary implications. Condor
76:447-452.
Cruden, R. W .. S. M. Hermann and S. Peterson. 1983. Patterns of nectar production and
plant-pollinator coevolution. In: The Biology of Nectaries (B. Bentley and T. Elias
eds.). Columbia Univ. Press. NY. Pp. 80-125.
Dobkin, D. S. 1984. Flowering patterns of long-lived Heliconia inflorescences: implica-
tions for visiting and resident nectarivores. Oecologia 64:245-254.
Dobkin, D. S. 1985. Heterogeneity of tropical floral microclimates and the response of

hummingbird flower mites. Ecology 66:536---543.
Dobkin, D. S. 1990. Distribution patterns of hummingbird flower mites (Gamasida:
Ascidae) in relation to floral availability on Heliconia inflorescences. Behav. Ecol.
1:131-139.
Dusbabek, F. and V. Cerny. 1970. The nasal mites of Cuban birds. I. Ascidae, Ereyneti-
dae, Trombiculidae (Acarina). Acarologia 12:269-281.
Fain, A. and K. E. Hyland. 1980. New species of the genus Rhinoseius Baker and Yunker,
1964 (Meso stigmata: Ascidae) phoretic on Colombian hummingbirds. Int. 1. Acarol.
6:15-24.
Fain, A., K. E. Hyland and T. H. G. Aitken. 1977a. Nouveaux acariens Ascidae (Meso-
stigmates) phoretiques dans les fosses nasales de colibris (Note preliminaire). Bull. Ann.
Soc. R. Beige Entomol. 113:185-186.
Fain, A., K. E. Hyland and T. H. G. Aitkin. 1977b. Flower mites of the family Ascidae
phoretic in nasal cavities of birds (Acarina: Mesostigmata). Acta Zool. Pathol. Antverp.
69:99-154.
Feinsinger, P. and R. K. Colwell. 1978. Community organization among neotropical
nectar-feeding birds. Am. Zool. 18:779-795.
Feinsinger, P., J. A. Wolfe and L. A. Swarm. 1982. Island ecology: reduced hummingbird
diversity and the pollination biology of plants, Trinidad and Tobago, West Indies.
Ecology 63:494--506.
Fisher, R. A. 1930. The Genetical Theory of Natural Selection, 2nd rev. ed. Dover, NY.
291 pp.
Flechtmann, C. H. W. and D. E. Johnston. 1978. The rediscovery and redescription of
Rhinoseius braziliensis (Acari: Ascidae). Rev. Bras. Entomol. 22:165-166.
Hamilton, W. D. 1967. Extraordinary sex ratios. Science 156:477-488.
Harvey, P. H., L. Partridge and L. Nunney. 1985. Group selection and the sex ratio.
Nature 313:10-11.
Herre, E. A. 1985. Sex ratio adjustment in fig wasps. Science 228:896---898.
Heyneman, A. 1., R. K. Colwell, S. Naeem, D. Dobkin and B. Hallet. 1991. Host plant
discrimination: experiments with hummingbird flower mites. In: Evolutionary Ecology
of Tropical Herbivores (P. W. Price, T. M. Lewinsohn, G. W. Fernandes and W. W.
Benson eds.). Wiley-Interscience, NY. Pp. 455-485.
Hunter, P. E. 1972. New Rhinoseius species (Mesostigmata: Ascidae) from Costa Rican
hummingbirds. 1. Ga. Entomol. Soc. 7:27-36.
Hyland, K. E., A. Fain and A. S. Moorhouse. 1978. Ascidae associated with the nasal
cavities of Mexican birds (Acarina: Mesostigmata). 1. NY Entomol. Soc. 86:260-267.
Kirk, W. D. 1991. The size relationship between insects and their hosts. Ecol. Entomol.
16:351-359.
Micherdzinski, W. and F. S. Lukoschus. 1980. Rhinoseius rafinskii, a new species from
Ecuador and Venezuela (Acari, Gamasina, Ascidae). Zool. Meded. (Leiden) 55:65-79.
Newstrom, L. E., G. W. Frankie, H. G. Baker and R. K. Colwell. 1993. Diversity of

flowering patterns at La Selva. In: La Selva: Ecology and Natural History of a Lowland
Tropical RainForest (L. McDade, K. S. Bawa, G. S. Hartshorn, and H. A. Hespenheide
eds.). Univ. Chicago Press, Chicago (in press).
OConnor, B. M., R. K. Colwell and S. Naeem. 1991. Flower mites of Trinidad II. The
genus Proctolaelaps (Acari: Ascidae). Great Basin Nat. 51:348-376.
Primack, R. B. 1985. Longevity of individual flowers. Annu. Rev. Ecol. Syst. 16: 15-37.
Stratton, D. A. 1989. Longevity of individual flowers in a Costa Rican cloud forest:
ecological correlates and phylogenetic constraints. Biotropica 21 :308-318.
Werren, 1. 1980. Sex ratio adaptations to local mate competition in a parasitic wasp.
Science 208: I ~57-1158.
Wilkinson, L. 1989. SYSTAT: the system for statistics. SYSTAT Inc., Evanston, IL.
Wilson, D. S. and R. K. Colwell. 1981. Evolution of sex ratio in structured demes.
Evolution 35:882-897.
Zamudio, M. 1985. Acaros foreticos (Mesostigmata: Ascidae) de las cavidades nasales
de colibries de Mexico. I. Folia Entomol. Mex. 64:81-91.
3
Mites as Potential Horizontal Transfer Vectors

of Eukaryotic Mobile Genes: Proctolaelaps
regalis as a Model
Marilyn A. Houck
CONTENTS
I. INTRODUCTION
1.1 What are Transposable Elements?
1.2 Horizontal Gene Transfer
2. P TRANSPOSABLE ELEMENTS IN DROSOPHILA
2. I The Structure of P Elements
2.2 Transformation Due to P Element Insertion
2.3 Gene-Cytotype Incompatibility
2.4 The Hypothesized Origin of P Elements
2.5 Geographic Distribution of P Elements
2.6 Hypotheses Concerning the Spread of P Elements
2.7 Evidence for Horizontal Gene Transfer of P Elements
3. THE SEARCH FOR A POTENTIAL P ELEMENT VECTOR
4. PROCTOLAELAPS RECALlS
4.1 Feeding Morphology
4.2 Feeding Behavior
4.3 P Element Experiments
4.4 Has Proctolaelaps regalis Previously Been Observed in Culture?
5. PROSPECTUS: DETECTING P ELEMENT TRANSMISSION EVENTS
5.1 Novel Potential for Incorporation of P Elements Into the Proctolae-
laps regalis Genome
5.2 Frequency of P Element Transmission
1. Introduction
The chapters in this volume give acarine examples of how ecological and evolu-
tionary events have contributed to the diversification, speciation, adaptation, or
coevolution observed within lineages. This chapter focuses on the issue of hori-
zontal transfer of genes between unrelated species, an event that can lead to the
rapid alteration of a genome by means of the insertion of foreign DNA. This novel
45
46 / M. A. Houck
source of genetic variation is independent of the usual hereditary mechanisms

occurring in sexual organisms, and can result in a rapid influence on the phenotype
with profound consequences for the lineage of the recipient.
Horizontal gene transfer of transposable (mobile) elements is becoming an
increasing important realm of investigation for phylogenetic systematists, and
will likely continue to be so for some time. The following is a summary of the
role one mesostigmatid mite may play in the horizontal transfer process. However,
the Mesostigmata in general offer especially fertile opportunities as the focus of
similar studies for many reasons including the large number of species, cosmopoli-
tan occurrence, common ecological interactions with other species (arthropods,
nematodes etc.), rapid mobility, and nature of feeding.
1.1 What are Transposable Elements?
Transposable elements are genes that can move freely from site to site within a
genome; they are not restricted to a fixed location on a chromosome. They have
been called "jumping genes" by some authors, and were first described in maize
by Barbara McClintock (1948). Transposable elements are not rare but, in fact,
have been found in all organisms in which they have been sought.
Transposable elements have been conceptually organized into "families" ac-
cording to their internal sequence topology, and mechanism of transposition.
There are approximately 50 different families of transposable elements, repre-
sented by two major classes (Finnegan 1989, 1990): Class I ("viral") elements
transpose by a mechanism of reverse transcription of an RNA intermediate (DNA-
RNA-DNA), and their action is similar to that of a retrovirus; Class II ("non-
viral") elements are believed to transpose directly from DNA to DNA (e.g. P
elements, detailed below).
The precise mechanism by which Class II elements transpose is not completely
understood, but it is known that the elements code for transposases which catalyze
their own mobility (O'Hare and Rubin 1983). Because transposable elements
have a significant influence on their own biological activity (transposition), they
have been called the ultimate "parasitic" or "selfish DNA" by some researchers
(Doolittle and Sapienza 1980).
1.2 Horizontal Gene Transfer
There is currently special phylogenetic interest in transposable elements because

it is now apparent that not only can transposable elements bolt from one genomic
site to another within a genome, but that they also have the potential for mobility
leading to interspecific incorporation into unrelated and uninfected species (hori-
zontal gene transfer).
While prokaryotes are well known for the ability to accomplish competent
interspecific gene transfer, the possibility of horizontal transfer among eukaryotes
Mites as Potential Horizontal Transfer Vectors of Eukaryotic Mobile Genes / 47
has only been suspected. Specific mechanisms of transfer have not been found.
For example, transfer has been suspected to have occurred between: (1) Drosoph-
ila melanogaster and D. funebris (Mizrokhi and Mazo 1990); (2) Drosophila and
Zaprionus (Maruyama and Hartl 1991); (3) Drosophila and yeast (Xiong and
Eickbush 1988); (4) D. melanogaster and Caenorhabditus elegans (Harris et al.
1988); and (5) even between Drosophila and the plant Arabidopsis thaliana,
since three retrotransposons of A. thaliana had a greater affinity to the copia
elements of D. melanogaster than they had to other A. thaliana retrotransposons
(Konieczny et al. 1991). Vectors can play an important role in the horizontal
transfer of genes, and viruses have been implicated in the transfer of some
transposable elements (Miller and Miller 1982).
Most startling was the recent documentation that mouse DNA (homologous to
mouse intracisternal A particle and endogenous type C retrovirus) from a particu-
lar strain of mice was detected in the DNA of its parasite (Schistosomajaponicum)
(Iwamura et al. 1991). In this case, host DNA was apparently integrated into the
genome of the adult parasites and detectable in their eggs.
Transposable elements hold a lot of promise as candidates for the study of
horizontal transfer, as they control their own mobility and usually increase in
copy number when inserted into a new genomic site (or new host). Thus, hori-
zontal transfer between eukaryotic species is more likely to be successful with a
self-regulating, mobile, multiple-copy gene than with single-copy non-mobile
genomic DNA. The increased representation of replicated elements is an impor-
tant factor, as it reduces the probability of element loss following insertion and
enhances the chance of gene representation in future generations, as compared
to single-copy genes.
Though, as a rule, genetic mutations resulting from mobile transposable ele-
ments are often deleterious, it is clear that transposition could have played an
important role in the structuring of eukaryotic genomes (Finnegan 1989). It is an
alternate source of genetic variation for diploid species which, under normal
circumstances, is influenced mainly by sexual recombination and mutation. No
one can yet predict how frequently such events occur, but no one doubts that it
can be a powerful evolutionary force.
2. P Transposable Elements in Drosophila
Between 10%-20% of the genome of Drosophila melanogaster consists of trans-

posable elements (Engels 1983, MacKay 1985, Finnegan and Fawcett 1986),
occurring as dispersed moderately repetitive sequences which are approximately
randomly scattered throughout the genome (Rubin 1983). Approximately half of
all spontaneous mutations in D. melanogaster are thought to be due to insertions
of transposable elements (Finnegan 1990). P elements represent one of the most
intensively studied groups of transposable elements in D. melanogaster (Engels
1988).
48 I M. A. Houck
2. I The Structure of P Elements
P elements are mobile genes which code for a transposase required for gene
mobility (Rio et al. 1986, Snyder and Doolittle 1988). Elements consist of a
single large gene comprised of 2907 base pairs (bp), flanked by short 31 bp
inverted repeats (O'Hare and Rubin 1983). P elements are not polymorphic in
sequence, but can be heterogeneous with respect to size (Daniels et al. 1990).
There are two categorical types of P elements which are ranked according to
relative size (Kidwell et al. 1988): (1) Autonomous (complete elements) = 2.9
kbp elements and (2) Nonautonomous (defective elements) possessing internal
deletions of various numbers of base pairs. Major differences in the complement
of autonomous and non autonomous elements in the genome of Drosophila strains
have been observed in populations from different geographic origins (Kidwell et
al. 1983, Anxolabehere et al. 1984, 1985b, 1988; Kidwell and Novy 1985,
Boussy 1987, Boussy and Kidwell 1987). Defective elements « 2.9 kbp) are
derived from complete P sequences by internal deletions (O'Hare and Rubin
1983). Defective elements can undergo transposition only when in the presence
of active autonomous elements (Daniels et al. 1990), probably because they are
incapable of accurately coding for their own transposase.
P elements are apparently inserted randomly into a genome (Rubin 1983) or
(if defective) inserted adjacent to other intact P elements (Finnegan 1990). They
are present in high copy numbers (30-50 copies; Bingham et al. 1982) per haploid
genome in individuals of some strains of D. melanogaster (called P strains), but
functional P elements are completely missing in other strains of D. melanogaster
(called M strains) (Bingham et al. 1982, Todo et al. 1984).
2.2 Transformation Due to P Element Insertion
In the early embryological development of Drosophila, the primordial germline

cells migrate to the posterior pole of the egg, are enveloped in a membrane, and
are expelled from the syncytial mass of the egg. P elements can be artificially
injected into fertilized eggs of M (P-deficient) strains of D. melanogaster and
transformed into P strains under controlled laboratory conditions (Rubin and
Spradling 1982). Elements inserted in this manner jump into the germline of the
receiving M strain, with normal phenotypic expression of the P element (Finnegan
1990). Study of the fate of lab-microinjected DNA indicates that injected DNA
becomes inserted into the germline of the young embryos (:S 512 cell stage; 90
min @ 25°C) and that which remains in the cytoplasm slowly degrades (Steller
and Pirrotta 1985). Transposition of P elements is often premeiotic, identically
influencing all resultant progeny (Rubin 1983).
The insertion of P elements into an M genome can result in seriously phenotypic
consequences which are most commonly restricted to the germplasm (Kidwell et
al. 1977, Bregliano et al. 1980, Kidwell 1983, Bregliano and Kidwell 1983).
These consequences include a high frequency of temperature-sensitive gonadal

sterility, male recombination, chromosomal aberrations, and an increased number
of lethal mutations (Kidwell and Novy 1979).
On the basis of the degree of the dysfunctional properties expressed, the P
element family includes three kinds of strains (Kidwell 1979, Engels and Preston
1981, Kidwell 1983, Kidwell et al. 1988): (1) P strains which contain functional
P elements which can potentially lead to sterility in strain hybrids (hybrid dysgene-
sis); (2) Q strains which do not express any potential for sterility, but do express
other P element characteristics (e.g. chromosomal aberrations); (3) M strains
which possess no functional P elements and no sterility effects; M' (pseudo M)
strains possess P elements but the phenotypic expression of traits varies from low
to relatively high.
Recently, P element transposition in Drosophila has also been utilized as a
vehicle to vector foreign DNA into a fertilized eggs of Drosophila (Rubin and
Spradling 1982, Spradling and Rubin 1982, Cooley et al. 1988). This procedure
has tremendous potential for designer engineering of the genome.
2.3 Gene-Cytotype Incompatibility
There are significant gene-cytotype interactions which govern the expression of

P element hybrid dysgenesis (Engels and Preston 1979). P elements are neutral
(do not cause dysgenesis) when expressed in a compatible P-cytotype cytoplasm
(inter se parental crosses). However, a mismatch between genome and cytoplasm
can have dire consequences, the magnitude of which depends upon whether the
contributing parent was the mother or the father.
Crosses between P-strain males and M-strain females result in gonadal sterility,
while interstrain matings between P-strain females and M-strain males result in
no symmetrical dysgenic abnormalities. In P-strain crosses, therefore, males can
provoke gonadal sterility in the hybrid offspring, while the female cytotype of P
strains seems to be able to suppress such a phenotypic disaster (Engels and Preston
1979, Rubin et al. 1982, for review see Engels 1988).
The ability to repress P element transposition is a mechanism to moderate
(reduce) harmful effects of P elements (Snyder and Doolittle 1988). Under
these conditions, it would be anticipated that P elements would be lost from
populations, or that consummated hybrid matings would be selected against. But
"selfish" mutants, which were exempt from such repressor action, would be
predicted to increase in a population under such circumstances. Such anti-repres-
sor elements could quickly prove fatal to Drosophila populations and selection
against their propagation would occur at the group level ("the group being the
population of P elements in a population of flies"; Snyder and Doolittle 1988).
Fitness loss can also be overcome by transposition efficiency (Kidwell et al.
1988). The highly invasive nature of active P elements is clearly observed when
introduction into susceptible populations is followed over time in lab cultures, or
50 I M. A. Houck
when accomplished by simulation modeling (Hickey 1982, Kiyasu and Kidwell

1984, Daniels et al. 1987, Good et al. 1989). Such studies indicate that changes
in strain status from M to P can occur relatively rapidly in the laboratory (Kidwell
et al. 1981). Simulations, using a mathematical population model (Hickey 1982)
have shown that selection against heterozygotes carrying a transposable element
can be offset by a relatively high rate of transposition. In sexual species, P
elements can become fixed even when fitness is reduced by 50%. P elements,
which could exist in low frequencies in populations for long periods of time
(Kidwell 1983), could proceed to fixation rather rapidly once a critical threshold
is reached.
There are also ecological influences on the phenotypic expression of gonadal
sterility in hybrid matings, as well as cytological influences. Where dysgenesis
is a potential (hybrid of P male X M female cross), there is a temperature-
dependant expression of the gonadal sterility (Engels and Preston 1979, Schaefer
et al. 1979, Kidwell 1983). At high environmental temperatures (27-29°C) there
is significant to complete sterility and an obvious reduction in parental Darwinian
fitness. Development at lower temperatures are less threatening.
2.4 The Hypothesized Origin of P Elements
Little is known concerning the evolution of mobile elements in general (Daniels

et al. 1990). They may have arisen de novo by mutation or recombination
(Finnegan 1985) or by horizontal transfer from another organism (Hagemann et
al. 1990). Homologous P sequences are widespread in the Sophophora radiation
of the Drosophilidae (Brookfield et al. 1984, Anxolabehere et al. 1985a, Daniels
and Strausbaugh 1986, Daniels et al. 1990, Montchamp-Moreau et al. 1991),
and are also known to occur in Opomyza germinationis (Diptera: Opomizydae)
and Trixoscelis frontalis (Diptera: Trixoscelididae) (Anxolabehere and Periquet
1987). This indicates that this family of P elements may be plesiomorphic and
present in the common ancestor of the family Drosophi1idae (Hagemann et al.
1990) or may have occurred even earlier in the phylogeny of the Diptera.
Though the P element is present in every species group in the subgenus
Sophophora, its distribution within species groups is discontinuous (Lansman et
al. 1985). P elements probably have had a long evolutionary history in the
willistoni and saltans lineages (Daniels and Strausbaugh 1986), but it does not
occur in other species of the melanogaster subgroup (e.g. D. simulans, D.
mauritiana and D. sechellis [Daniels et al. 1990]). P elements are unique in that
while they are common in D. melanogaster, they are not present in all strains of D.
melanogaster. And, they are completely absent in species most phylogenetic ally
related to D. melanogaster (Brookfield et al. 1984, Daniels and Strausbaugh
1986).
There is near-identity of P element sequences from D. melanogaster and D.
willistoni with only one base pair difference (Daniels et al. 1990) and high
Mites as Potential Horizontal Transfer Vectors of Eukaryotic Mobile Genes I 51
sequence similarity among D. melanogaster P elements from diverse geographic

locations (O'Hare and Rubin 1983).
Though P elements occur sporadically across the Scaptodrosophila radiation,
there is a lack of congruence between P element sequence divergence and the
divergence time between Drosophila species pairs (Hagemann et al. 1990). It is
speculated that the genus Drosophila originated within the Drosphilidae sometime
during the Eocene (40-50 mya; Throckmorton 1975, Beverly and Wilson 1984)
and that the Sophophoran radiation produced three modem lineages: (1) melano-
gaster in the Old World tropics; (2) obscura in the north temperate (Holarctic)
zone; and (3) willistoni/saltans in the New World tropics (Patterson and Stone
1952, Throckmorton 1975). Thus, the evolution of the P element seems not
to have diverged exclusively by classical radiation in the course of speciation
(Hagemann et al. 1990).
2.5 Geographic Distribution of P Elements
Natural populations of D. melanogaster collected in North America, South

America, and Africa are dominated by individuals possessing P elements, while
most European and Asian populations have defective P homologous sequences
(Finnegan 1990). Australia has both P element strains and M strains (Boussy
1987). A P-M hybrid dysgenesis cline exists in eastern Australian in D. melano-
gaster with discrete P, Q, and M regions being nearly contiguous (Boussy 1987,
Boussy and Kidwell 1987).
P elements are present in contemporary wild populations of D. melanogaster
and no true M strains have been collected from wild populations of flies since
1974 (Anxolabehere et al. 1988). By comparison, P elements are absent from
laboratory strains which were brought into the lab more than 30-40 years ago
(Bingham et al. 1982, Kidwell 1983, Bregliano and Kidwell 1983, Kidwell et
al. 1983).
2.6 Hypotheses Concerning the Spread of P Elements
Two hypotheses exist which account for the geographic patterns observed in
the P element distribution in D. melanogaster (Kidwell 1983): (1) Recent-loss
hypothesis: the loss of P elements from laboratory stocks, but with persistence
of P elements in the wild, has led some to speculate that there has been a stochastic
loss of these elements in laboratory populations due to drift (Engels 1981).
Evidence supporting this point of view is that there has been an observed change
from P to M strains in one laboratory population (Engels and Preston 1980).
While this is interesting, there is no evidence that this event could be repeated
with the required frequency or magnitude needed to explain the rapid loss of
elements hypothesized. The main problem with the Recent Loss Hypothesis is
that it requires that individual strains of Drosophila must have lost all 30-50
52 / M. A. Houck
copies of the P element in a short period of time, which is unlikely given the
invasive biological nature of the element.
A second hypothesis is called the Rapid-invasion hypothesis (Kidwell 1979,
1983) which hypothesizes that P elements are recent invaders of Drosophila
populations. This theory is supported by the fact that until recently P elements
have been absent in natural populations of D. melanogaster, and have only
recently been observed to spread in frequency in wild popUlations. It is hypothe-
sized that prior to 1930 P element families were absent (or in low frequency) in
all natural populations and that about 30 years ago P strains began a rapid
infiltration which lasted until about 1960. After which time, P strains were
essentially ubiquitous in the wild.
Interspecific transfer of P elements can occur by vertical (mating-dependent =
orthologous) transfer or by horizontal (mating-independent = xenologous) trans-
fer (e.g. Montchamp-Moreau et al. 1991). It has been suggested that the rate of
global spread of P elements could best be explained by mechanisms other than
the epidemiological spread through normal sexual contact and interspecific hy-
bridization. Interspecific horizontal gene transfer has been proposed as a potential
mechanism for the dissemination of P elements worldwide.
The geographic site of origin of the purported recent invasion event was
speculated to have been the New World, as evidenced by the fact that the P
element first appeared there in D. melanogaster supposedly in the 1950' s (Kidwell
1983). P strains were not found to be present in Europe, Asia, or Australia until
about 10 years later. Since 1980, M strains have been determined to occur only
in the Iberian peninsula, central Asia, and the southeastern coast of Australia
(Anxolabehere 1985b, Kidwell 1986).
2.7 Evidence for Horizontal Gene Transfer of P Elements
Several corroborating pieces of information endorse the hypothesis of the recent

introduction of the P transposable element into D. melanogaster, from a species
of the willistoni group (Daniels and Strausbaugh 1986) by means of horizontal
gene transfer: (l) the uneven world-wide pattern of distribution of P elements in
D. melanogaster (Anxolabehere et al. 1985b, Anxolabehere et al. 1988); (2) the
high sequence fidelity among D. melanogaster P elements from incongruous
geographic locations (Kiyasu and Kidwell 1984, Daniels et al. 1987, Good et al.
1989); (3) the prevalence of P elements in members of the willistoni species
group, relative to their rarity in the melanogaster species group (O'Hare and
Rubin 1983, Brookfield et al. 1984); (4) the single base pair difference existing
between P element sequences from D. melanogaster and D. willistoni (Daniels
and Strausbaugh 1986); (5) the lack of correlation between P element sequence
and topography and the evolutionary divergence time between Drosophila species
pairs (Daniels et al. 1990); and (6) the recent finding that P element sequences
of D. melanogaster and D. nebulosa (willistoni species group) are more similar
to each other than either is to D. bifasciata (obscura species group) (Hagemann

et al. 1990).
3. The Search for a Potential P Element Vector
As outlined above, indirect evidence from several lines of investigation strongly

suggest that P elements in Drosophila are interspecific ally transmitted by hori-
zontal gene transfer. There are numerous biological candidates found in associa-
tion with Drosophila which could potentially participate (unilaterally or in combi-
nation) in this gene transfer. These include: bacteria, fungi and molds, protozoans,
spiroplasms and mycoplasms, viruses, and several kinds of small arthropods
(hymenoptera and mites being common associates).
At least 14 different mite species co-occur with Drosophila (Ashbumer 1989).
These include four Astigmatid genera (Glycyphagus, H istiostoma, H ormosianoe-
tus, and Tyrophagus), three Prostigmatid genera (Leptus, Trombidium, and an
unidentified Smaridiidae), and seven Mesostigmatid genera (Androlaelaps, Arcto-
seius, Fuscuropoda, Gamasides, Macrocheles, Parasitus, and Proctolaelaps).
Those species previously identified from Drosophila laboratory cultures in-
clude: Androlaelaps casalis, Glycyphagus domesticus, Histostoma jeroniarum,
Histostoma laboratoriun, Histostoma sapromyzarium, Hormosianoetus aeschli-
manni, Proctolaelaps hypudaei (= P. pygmaeus) , and Tyrophagus putrescentiae.
Over time, I have seen several species of mites arrive in fly shipments to
individual researchers at several universities. H. laboratorium probably is the
most common contaminant of Drosophila cultures, but it was not a logical
candidate for gene transfer because it is primarily a filter-feeder of dissolved and
suspended materials in culture media. The deutonymphal instar is phoretic (=
passive disperser) on adult flies but has no known trophic interaction with the
flies.
A very interesting mite, Proctolaelaps regalis (Gamasina: Ascidae) (DeLeon
1963), was discovered in fly cultures at the University of Arizona in 1986. P.
regalis was intriguing because it seemed to meet the minimum requirements for
a potential horizontal transfer candidate (opportunity, motive, and means). (1)
Opportunity: It is syntopic (on rotting fruit) with members of the suspected donor
species-group (willistoni) and with the P element recipient, D. melanogaster;
and it is sympatric with D. melanogaster and wild populations of the willistoni
species group in the hypothesized site of P element radiation (Florida, Central
America, and South America [Ehrman and Powell 1982]). (2) Motive: it is an
omnivore which feeds on Drosophila. (3) Means: it has a peripatetic feeding
behavior, with rapid transit time between potential prey, accomplishing its attack
in fruit rot where all fly stages are present.
A realistic hypothesis which could unite accumulating observations, is that P.
regalis might vector P elements if it attacked a member of the willisoni species
54 / M. A. Houck
group, and then immediately inserted the "bloody" gnathosoma into the posterior
pole of aD. melanogaster egg (younger than the 512 stage [Steller and Pirrotta
1985]). For these reasons P. regalis was the only observed acarine which I chose
as appropriate for such detective scrutiny.
4. Proctolaelaps Regalis
Proctolaelaps regalis is a Parasitiform mite of the suborder Gamasida. The

Gamasida currently contains about seven superfamilies, most of which are fluid
feeders. P. regalis is of the superfamily Ascoidea which are known to be widely
distributed throughout the tropics and temperate habitats, feeding primarily on
nematodes, insects, and fungi (Krantz 1978).
It is a member of the family Ascidae, a large taxonomic group with significant
ecological success in terrestrial and subaquatic habits, resulting in a large adaptive
radiation (Lindquist 1965). This family exploits habitats on every continent except
Antarctica (Lindquist 1965) and is probably one of the most diversified families
in North America (Lindquist 1971). Most members of the Ascidae are free-living
predators, common on plant foliage in the tropics but seldom in temperate regions,
because the Phytoseiidae have competitively dominated that habitat.
P. regalis is in the subfamily Ascinae, one of the "largest and by far the most
diverse" subfamilies of the Ascidae (Lindquist 1965). The genus Proctolaelaps
(erected by Berlese in 1923) is itself cosmopolitan and consists of about 70
species (Lindquist 1965).
P. regalis is a fruit, leaf, bark and litter species (Muma 1975) occurring in the
habitat utilized by Drosophila. In nature, P. regalis is found associated with a
"variety of insects in various stages of development" (DeLeon 1963), and E. E.
Lindquist (Biosystematics Research Centre, Agriculture Canada) has a "variety
of material at hand compared with the type material of this species. It seems to
be frequently associated with fallen or rotting fruit" (Biosystematics Research
Centre Identification Report 89-0818-01).
4.1 Feeding Morphology
The feeding structures of P. regalis are associated with the gnathosoma which is
a body region distinctive among mites, having no homologous or analogous
tagma in insects or other arachnids. Many traditional "head" structures are not
associated with the gnathosoma (e.g. eyes and brain) but are associated with the
more caudal idiosoma ("body").
The chelicerae and the pedipalps (Fig. 3.1A) are associated with the gnatho-
soma. The chelicerae are retractable supraoral structures and in the free-living
Mesostigmata are represented by an elongate pistonlike structure, with a muscula-
ture that can be used for thrusting penetration of host tissues. It is somewhat
progressed toward the form of a piercing stylet, "able with little modification to
Figure 3.1. The chelicerae and the pedipalps of mites are associated with the gnathosoma.
(M. A. Houck, Science 1991,253:1125; Copyright 1991 by the AAAS. A) The feeding
posture of an adult female Proctolaelaps regalis (body length = - 400/Lm) when attacking
a pupa of Drosophila melanogaster. Feeding on the pupa requires a significant amount of
effort (thrusting and piercing) to penetrate the hard crysalis. B) Omnivores such as P.
regalis often retain chelate-dentate chelicerae (with a fixed and a movable digit) to handle
a broad range of food types. This mite is positioned with the venter-side up.
achieve the same functions as sty lets in bloodsucking insects" (Radovsky 1985).
The two digits of the chelicerae are approximately the same length in adults.
Cheliceral morphology of ascids correlates with trophic specialization (Evans
et al. 1961), with a great deal of diversification. The primitive chelate-dentate
state allows for grasping, shearing, and piercing of prey, as opposed to long
slender chelicerae with small teeth usually found in mites feeding on other
mites or small insects. Obligate parasites may have edentate chelicerae, reduced
chelicerae, or a reduced fixed digit.
Omnivores such as P. regalis retain chelate-dentate chelicerae (with a fixed
and a movable digit) to handle a broad range of food types (Fig. 3.1B), while
the over-all morphology of its gnathosoma is (like most other Mesostigmata) well
adapted for fluid-feeding (van der Hammen 1964). Even though there are trends
in the correlation between cheliceral specialization and the food types eaten in
the Mesostigata "some parasites are so subtle that it occasionally may not be
possible to tell by morphology alone whether a species is an obligatory parasite"
(Radovsky 1985).
This cheliceral morphology is central to the evolutionary success of the Meso-
56 I M. A. Houck
stigmata and essential in the adaptation to a parasitic life style (see Radovsky
this volume). There is a forked structure (tritosternum) located ventrad to the
chelicerae. The tritosternum interacts with the deutosternum to recover the over-
flow of liquid foods during feeding, and move it back to the oral area (Wernz
and Krantz 1976).
P. regalis has two large secretory salivary styli (= siphunculi) (Fig. 3.2)
positioned laterad and ventrad to the chelicerae. They probably carry the ducts
of the salivary glands which are extended in parasitic forms, are partly sclerotized,
and are thought to empty into the hypos tome where they assist in preoral digestion
(Krantz 1978, Woolley 1988).
The spermadactyl (Fig. 3.2) is the male insemination structure used in copula-
tion and is also associated with the chelicerae. Mating is accomplished when the
male knocks the female over, and as she recovers her balance he positions himself
underneath her with the cheliceral spermadactyl inserted into the sperm induction
pores on either side of the mid-ventral epigynal opening (Fig. 3.3, 3.4).
The midgut in the Gamasina (= ventriculus) typically has 2-3 pairs of caecae
that consist of cuboidal cells on a basement membrane, and larger vacuolated
cells interspersed. As the wall of the gut is extended, the larger cells are pinched
Figure 3.2. Proctolaelaps regalis has large secretory salivary styli (= siphunculi) ("s")
which are chitinous at the proximal end and fleshy at the distal tip. The spermadactyl
(insemination organ) (arrows) of the male is located in the chelicerae and posterioventrad
to the salivary styli. The sperrnadactyl is seen here in its fully extended state (posteriorly
recurved).
Fig"" 3.3
. -rhc " " ''
,. .. ,. In g "" '' g "",Ition
of " o c to l"
,penno<I>'",\t\on (Logs 1. n.ln. ,l a P ' "ga
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" ,t e ,I '" on
,1 I, " '' '' '' '"
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of "
" " "",teOd'" " f _Ic ', bOdy ( gcn ltill ,pertu" al< p o , I " I, '" , nonnolcl
"" , " " " " x1 Y - " ,l o w . Tb<
" " f" " " c . Fig· 3 .4). Logs m(3 " " ,d 'h " " w'Y fron ma
do"un> o f
fc.na\c. Lo L " > th
g I ( l) of " og Il (2 ) of ) ,d
"",Itlonlng " .na\c ,,,,,1\,, " " mal< w '" (4) of " " " " I< g c
of " " ,I " " tb< fo " pa " l" _ n d Icg '' ''
" " " " " y i. O rt of b l, bO IV of thc
n ly " " d o " dy " '" po"l
,1 , u d = o
with the su
bstratum. f thc .na\c b blY ,I d ' In " "
a ' phy,loa!
o ff into th " " ,t a c t
e lumen o f
to supply d th e g u t ",here the
oc-
ig y fom> ,p h rical
lu ' as evid estive juices. Inuac e b o d l. ,. Th
enced b y th ellulor dig ey ore thou
e presence estion prob ght
o bly
(envelope)
i, added to
o f v ,, " o lo
re d cells. in the ventr c u
the bolus A . p e r i_ h iC i -
to proteCt membrane
the gut.
4.2 Feedin
I would useg Behavior
the tenD se
tion of P . miparasite
,e g '. It (or omnivo
prey) or a a li Is possible re) to .re.c b e
s a parasite th a t the m ri the tro
In the labo (do ite maY act phiC specia
ratorY 1 o es not kill bost). de either as a liza-
(feeding p bServed th pending up predator (k
erhaPS o n at P . regalis On illS
appoor to fre
reproduce e nutrients. fungUS. can surviv conditions.
under these c e o n fty me
b u t p . reg alisdia alone
ta p e indic and yeast).
a",d th a t p onditions.
. reg jl x ., o
n in a ti n o do
b y rapid ch
elicera! thrU alis also f<eds o n all f IS hours es not
sting. T h is I o f videO
action is ac m - " " g " o f D . m
complishe e
d ,,,,Ift\y. se la n o g "u''lo''r
nding cell
58 / M. A. Houck
Figure 3.4. Venter of a female of Proctolaelaps regalis, with the epigynial plate indi-
cated.
inclusions into the hollow space between the cheliceral shafts (Fig. 3.5). Feeding
can last only a few seconds per attack, and immediate feeding on subsequent
adjacent hosts is common. In mixed-species fly cultures this behavior provides
potential for transfer of cellular inclusions (including DNA) from one individual
host to another.
Adult mites also feed on Drosophila pupae, where penetration of the puparium
requires prolonged thrusting of the chelicerae (continuing for as long a 2 mini
attack). Sometimes contamination of fly strains by P. regalis ends in population
degradation or elimination, possibly as a result of this second (damaging) type
of feeding.
All of the various aspects of the biology of this mite, including the semi-
parasitism itself, are consistent with P. regalis having had a co-evolutionary
association with what are now "domesticated" Drosophila. This mite may have
been co-collected with wild-caught fly stocks in the U.S. originally, but it is
equally likely that it secondarily invaded U. S. laboratory stocks because of its
natural association with Drosophila in the wild. In short, P. regalis has the
morphological and behavioral capacity, and the ecological and geographical
opportunity, to act as a vector for P elements.
Figure 3.5. Scanning electron photomicrograph of the cheliceral digits of Proctolaelaps

regalis. Inclusions (spores) are located in the rotund, hollow, cavity formed between the
closed cheliceral digits (arrows).
4.3 P Element Experiments
In order to determine if P. regalis mites were acquiring P element sequences

from D. melanogaster during feeding, genomic DNA was isolated from mites
associated with both P and M strain fly cultures. The first attempt to determine
whether P elements could be detected in P. regalis came in 1986, using Southern
blot hybridization, a very laborious task which sometimes resulted in a weak
positive signal. This required harvesting 400 mites per sample, using a dissecting
scope, and washing each one as collected so as to remove any surface contamina-
tion. Once Polymerase Chain Reaction (PCR) technology became generally acces-
sible (Appenzeller 1990), studies such as this became much easier.
Results of Southern blot analyses indicated that hybridization to a P element-
specific probe occurred only with DNA extracted from the Harwich-w (P) fly
strain or with DNA extracted from mites associated with that P element strain
(for details see Houck et al. 1991). DNA from the Canton-S (M) strain of D.
melanogaster and from P. regalis associated with the Canton-S strain consistently
showed no detectable hybridization to the P element probe.
Specific PCR primers were synthesized for D. melanogaster P elements.
60 I M. A. Houck
Eight separate samples of template DNA from the Harwich-w strain (P) of D.
melanogaster and mites associated with that strain were used in PCR with these
primers. All consistently yielded a fragment of the correct size. Results from both
the Canton-S template and that from mites associated with the Canton-S strain
were negative.
To demonstrate that the fragment produced from the mite template DNA was
indeed P-specific, the product was isolated and a 250 bp segment was sequenced.
The nucleotide sequence in this region was identical to that previously determined
(O'Hare and Rubin 1983) for the D. melanogaster P element.
The most parsimonious explanation for these results is that P. regalis can
acquire Drosophila P element sequences during feeding. However, two alterna-
tive explanations had to be considered. First, that the DNA samples from P.
regalis (collected from the Harwich-w fly cultures) were contaminated. Second,
that the mites themselves carried endogenous sequences with homology to P
elements.
To address the first question, adult H istiostoma laboratorium (ecological corre-
late) were isolated from the same Harwich-w culture as were P. regalis and DNA
was prepared in the same manner. No P-specific product was detected when
Histiostoma DNA was used as a template in PCR, indicating that physical
association with the flies was not of itself sufficient to give positive results.
To address the second issue of whether endogenous P sequences in Harwich-
associated mites might be pleisomorphic or synapomorphic in ascid lineages,
we obtained isolates of two species closely related to P. regalis (Lasioseius
subterraneus and a Proctolaelaps spp.). Again no P-specific product was de-
tected.
A final important question was whether other gene sequences could also be
detected in the mites. The non-mobile small-subunit (18S) rRNA gene was chosen
because, like the P element, it is present in multiple copies in the D. melanogaster
genome. Primers, corresponding to highly variable regions within the 18S rRNA
gene, were synthesized to be specific for the D. melanogaster small subunit rRNA
gene.
Because no acarine small-subunit rDNA sequences had been published, we
could not rule out that these primers were in fact hybridizing to the endogenous
P. regalis genes. DNA was isolated from the three mite species sampled pre-
viously: H. laboratorium, L. subterraneus, and the unnamed Proctolaelaps spe-
cies. No PCR product was detected using template DNA from any of these three
species, indicating that the Drosophila rDNA primers were not hybridizing to
endogenous mite sequences.
The amplified DNA fragment from P. regal is which was produced with D.
melanogaster-specific rDNA primers was also isolated and purified. A 300 bp
region of the product was sequenced and found to be identical to the corresponding
segment of the D. melanogaster 18S rDNA. These results suggest that P. regalis
was acquiring 18S rDNA and P element Drosophila DNA sequences during its
association with fly cultures, a conclusion consistent with the morphology, ecol-
ogy, behavior and geography of this mite.
4.4 Has Proctolaelaps regalis Previously Been Observed in Culture?
In light of the controversy surrounding the origin and spread of P elements, I

wanted to determine how often P. regalis had been observed in Drosophila
cultures by other researchers. From surveying the literature, it became clear that
there was no way to estimate this frequency of occurrence. The reasons for
uncertainty come from: (1) unfortunate inaccuracies in a chapter on mites in a
text heavily consulted and referenced concerning all aspects of the culture of
Drosophila (Ashburner and Thompson 1978); and (2) neglect of (or disinterest in)
the accurate reporting of the mite species encountered by Drosophila researchers.
The most comprehensive summary (prior to 1989) concerning mites in Dro-
sophila cultures, came from a chapter by Ashburner and Thompson (1978). This
reference included a figure (their Fig. 29, p. 75) of a "dangerous egg predator,"
a mesostigmatid mite. The authors identify this mite as Proctolaelaps hypudaei
(= P. pygmaeus). But it is not clear whether all Proctolaelaps individuals thus
far found in fly bottles are restricted to the species hypudaei.
This is not a trivial issue, as a correct identification of any species provides
considerable insight into the ecological role and potential impact of the organism
in an ecological community. The genus Proctolaelaps can express a wide range of
potential diet preferences, depending upon species. P. hypudaei is a cosmopolitan
omnivore which is known as a predator of mites (Nesbitt 1951) and also consumes
fungus (Muma 1961). It is a very versatile mite, being found primarily in: leaf
mould and litter, mouldy wheat and barley, rotting wood and plant bulbs, and on
leaf surfaces of orchard trees and citrus where they feed on insects, and Tet-
ranychid mites (Nesbitt 1951, Mathys and Tencalla 1959, Ehara 1964, Muma
1975, Hughes 1976). P. nauphoetae, however, is solely an ectoparasite of cock-
roaches (Egan and Hunter 1975); P. bombophilus and P. longisetosus feed on
pollen in bumblebee nests (Krantz 1978), and species of Proctolaelaps discussed
by Colwell (this volume) feed on nectar as well as pollen. A correct species
identification is important to all further assumptions and interpretations concern-
ing the biology of an organism, and can be essential as an intellectual guide or
if incorrect can misdirect further studies.
Cantelo and Boswell (1973) reported P. hypudaei in their Drosophila cultures
in 1973. But, the nature of this mite's interaction with Drosophila was undocu-
mented, and the focus of the commentary was mite eradication. These authors
state:
When we were confronted by a large infestation of mites in our Drosophila

colony, we treated the colony with benzyl benzoate, which had been found by
others to eliminate mites from their colonies (DIS 20:96, DIS 46:156). How-
ever, this treatment was ineffective for us, possibly because we had a different
62 / M. A. Houck
mite species. Our colony was infested with Proctolaelaps hypudaei (Oudemans)
(det. R. L. Smiley) of the family Ascidae. a cosmopolitan mite. It feeds on
mites and other small arthropods and probably caused depletion of the Droso-
phila culture by feeding on the Drosophila eggs and affecting the Drosophila
behavior.
The fact that various other insecticides (e.g. binapacryl, dicofol, propargite
and methyl benzoate) also did not effectively kill these mites could indicate that
some resistance to chemicals had developed over time and that these mites had
been more frequent in lab stocks than thought.
The second confirmed report of Proctolaelaps occurring in Drosophila cultures
was from Ashbumer and Thompson's own lab. They state that "in Cambridge
we suffered at one time from an unidentified species of the same genus." Their
cavalier lack of interest in exactly which species points to the second serious
issue; the attitude that somehow all species of Proctolaelaps are ecologically
equivalent. This attitude, by prominent researchers, is regrettable considering
that the focus of their mite chapter was to educate the uneducated.
One cannot safely assume that all the Proctolaelaps encountered in Drosophila
cultures have been P. hypudaei. From the whole-body drawings of the Mesostig-
mata, which are quite comparable among species to the untrained eye, P. regalis
could have been easily missed or mistaken. In any event, the genus Proctolaelaps
is reported to have had serious effects on lab cultures at least twice previously,
and I have had lab strains of P. regalis which have ranged from lethal to relatively
benign, depending on the fly strain cultured.
If other sightings of P. regalis have occurred in cultures, these mites have either
not been correctly identified or perhaps the observed high virulence discouraged
interest in the mite beyond that of rapid extermination. On my own first encounter
with P. regalis, I was asked to advise on its eradication. If systematic acarology
had not been one of my interests, this mite would probably have been eradicated
without eulogy or acknowledgment. I wonder if that has been the fate of other
populations. And, what of the potential unknown genetic impact on Drosophila
cultures prior to local mite extermination?
5. Prospectus: Detecting P Element Transmission Events
5.1 Novel Potential for Incorporation of P Elements into the Proctolaelaps

regalis Genome
The above findings are particularly intriguing because the feeding behavior of the
mite appears to simulate the method of microinjection in the laboratory which
has been used by many Drosophila researchers for intraspecific and interspecific
transfer of genes by P element transformation. It is not yet know whether Procto-
laelaps regalis has the ability to incorporate P elements into its own genome, as
was observed in Schistosomajaponicum (Iwamura et a1. 1991). P. regalis may,

in fact, act only as a mechanical vector with no consequence to its own genome.
Curiously, a very unusual set of circumstances specific to the Mesostigmata
could allow for a remarkable mechanism for integration without necessarily
invoking transovarial transmission or other such means of secondary vectoring.
Since the spermadactyl (Fig. 3.2) of the male of P. regalis is used in copulation
and also potentially for feeding, there is the potential mechanism for the integra-
tion of P elements into the mite genome as a direct result of copulation. What
would be required is that the male feed on Drosophila containing the P element
and subsequently insert the "bloody" chelicerae (with spermadactyl) into the
sperm induction pores (Krantz 1978) of the female (Fig. 3.4). Because of the
powerful mobility and invasive nature of transposable elements, there is a possibil-
ity (no matter how remote) of these elements invading awaiting mite eggs. The
door is open to the development of testable hypotheses.
What is not yet known is whether males of P. regalis can, or do, actively
feed. This is an important question about P. regalis males that needs to be
experimentally explored (see for example discussion by F. Radovsky, this
volume).
5.2 Frequency of P Element Transmission
Acquiring P elements by mites during feeding may be dependent on stochastic

events involving several environmental, behavioral, and demographic factors of
both the mites and the flies. The likelihood of heuristically observing a gene-
transmission events would be expected to be relatively small; partly because gene
transfer itself may be an infrequent event, and partly because of the statistical
vagaries involved in assigning responsibility once it has occurred.
The minimum experimental conditions needed for the potential detection of
such an event would require that: (1) a P element strain of Drosophila and an M
strain syntopically co-occur (same fruit rot or culture bottle); (2) an egg is laid
by an M strain female in proximity to a P strain individual (any immature fly
stage) giving P. regalis the opportunity to sequentially feed on the P strain and
then on the egg of the M strain (mechanical vectoring); (3) the M strain fly eggs
be less than 3 hours old (5l2-cell stage) so that the germ line can incorporate the
vectored P element; (4) the mite, in fact, feeds on the P and M strains sequentially
and not interrupt the feedings to graze on fungus or other nutrients and thus
potentially purging the gnathosoma of acquired P elements; (5) the habitat com-
plexity be conducive to transfer; habitat complexity is a function of culture age
and fly density increases as a direct function of habitat complexity, but so does
the density offungal spores. An increase in fungus is correlated with the increased
access to fungus which interferes with the relative frequency of mites feeding on
flies; (6) any egg receiving the vectored P element must survive the act of transfer
(feeding) by the mite; (7) any egg receiving the vectored P element must be of
64 / M. A. Houck
the correct cytotype; (8) any adult resulting from that mite-injection event (as a
egg) must be under the scrutiny of a researcher, and sampled for P element
analysis. If each of these events has a low independent probability, the combined
probability of detection is multiplicative and extremely low.
In contrast, the factors which act in favor in detecting a successful transfer of
P elements are: (1) the very invasive and infective nature of the elements them-
selves; (2) their control over their own excision and transposition; and (3) their
mechanism for entering the germ line in multiple copies. Even if the initial
frequency of infection is low, once incorporated in the germline, P elements
would persist, perpetuate, and become a potentially significant evolutionary force.
In the future I am going to pursue the question of horizontal transfer by P.
regalis by uncoupling the above stochastic events, determine a probability esti-
mate for each of the independent events and then stochastically model the interac-
tions. Hopefully this approach will be productive in establishing the first realistic
estimate of the frequency of horizontal transfer of P transposable elements.
Acknowledgments
The molecular aspects of this work were done in cooperation with K. Peterson
(Southern blot analysis) and J. Clark (PCR analysis), in the lab of M. Kidwell,
while I was on the faculty of the University of Arizona. I thank S. Daniels, 1.
Boussey, M. Kidwell, and K. Kymoura for stimulating discussions about P
element biology. The late M. J. Kaliszewski provided the samples of Lasioseius
subterraneus, and the unnamed Proctolaelaps species.
Special thanks to E. E. Lindquist and G. W. Krantz forcIarifying the synonomy
of Proctolaelaps hypudaei and P. pygmaeus, and for directing me to the correct
use of the term "induction pore". Also, thanks to E. E. Lindquist and R. E.
Strauss for their meticulous reading of the body of the text and for many helpful
comments.
References
Anxolabehere, D., H. Kai, D. Nouaud, G. Periquet and S. Ronsseray. 1984. The geo-
graphical distribution of P-M hybrid dysgenesis in Drosophila melanogaster. Genet.
Set. Evol. 16:15-26.
Anxolabehere, D., D. Nouaud, G. periquet. 1985a. Sequences homologues a l'eIement
P chez des especes de Drosophila du groupe obscura et chez Scaptomyza pallida
(Drosophilidae). Genet. Silo Evol. 17:579-584.
Anxolabehere, D., D. Nouaud, G. Periquet and P. Tchen. 1985b. P-eIement distribution
in Eurasian populations of Drosophila melanogaster: a genetic and molecular analysis.
Proc. Natl. Acad. Sci. USA 82:5418-5422.
Anxolabehere, D. and G. Periquet. 1987. P-homologous sequences in Diptera are not

restricted to the Drosophilidae family. Genet. IMr 39:211-222.
Anxolabehere, D., M. G. Kidwell and G. periquet. 1988. Molecular characteristics of
diverse populations are consistent with the hypothesis of a recent invasion of Drosophila
melanogaster by mobile P elements. Mol. Bioi. Evol. 5:252-269.
Appenzeller, T. 1990. Democratizing the DNA sequence. Science 247:1030-1031.
Ashburner, M. 1989. Drosophila: A Laboratory Handbook. Cold Spring Harbor Labora-
tory Press, NY.
Ashburner, M. and J. N. Thompson, Jr. 1978. The Laboratory Culture of Drosophila. In:
The Genetics and Biology of Drosophila, Vol 2A (M. Ashburner and T. R. F. Wright
eds.). Academic Press, NY. pp. 1-109.
Beverly, S. M. and A. C. Wilson. 1984. Molecular evolution in Drosophila and the higher
Diptera II. A time scale for fly evolution. 1. Mol. Evol. 21:1-13.
Bingham, P. M., M. G. Kidwell and G. M. Rubin. 1982. The molecular basis of P-M
hybrid dysgenesis: the role of the P element, a P strain specific transposon family. Cell
29:995-1004.
Boussy, I. A. 1987. A latitudinal cline in P-M gonadal dysgenesis potential in Australian
Drosophila melanogaster populations. Genet. Res. 49:11-18.
Boussy, I. A. and M. G. Kidwell. 1987. The P-M hybrid dysgenesis cline in eastern
Australian Drosophila melanogaster: discrete P, Q, and M regions are nearly contigu-
ous. Genetics 115:730-745.
Bregliano, J. c., G. Picard, A. Bucheton, A. Pelisson, J. M. Lavige and P. L'Heritier.
1980. Hybrid dysgenesis in Drosophila melanogaster. Science 207:606-611.
Bregliano, J. C. and M. G. Kidwell. 1983. Hybrid dysgenesis determinants. In: Mobile
Genetic Elements (1. A. Shapiro ed.). Academic Press, NY. Pp. 363-410.
Brookfield, J. F. Y, E. Montgomery and C. H. Langley. 1984. Apparent absence of
transposable elements related to the P elements of D. melanogaster in other species of
Drosophila. Nature 310:330-331.
Cantelo, W. W. and A. L. Boswell. 1973. Mite control with chemicals in a Drosophila
culture. Drosophila Inj. Servo 50:163.
Cooley, L., R. Kelley and A. Spradling. 1988. Insertional mutagenesis of the Drosophila
genome with single P elements. Science 239: 1121-1128.
Daniels, S. B. and L. D. Strausbaugh. 1986. The distribution of P element sequences in
Drosophila: the willistoni and saltans species groups. 1. Mol. Evol. 23:138-148.
Daniels, S. B., S. H. Clark, M. G. KidwellandA. Chovnick. 1987. Genetic transformation
of Drosophila melanogaster with an autonomous P element: phenotypic and molecular
analyses of long-established transformed lines. Genetics 115:711-723.
Daniels, S. B., K. R. Peterson, L. D. Strausbaugh, M. G. Kidwell and A. Chovnick.
1990. Evidence for horizontal transmission of the P transposable element between
Drosophila species. Genetics 124:339-355.
DeLeon, D. 1963. A new genus and twelve new species of mites from Mexico and
Southeast United States (Acarina: Blattisocidae). Florida Entomol. 46:196-198.
66 / M. A. Houck
Doolittle, W. F. and C. Sapienza. 1980. Selfish genes, the phenotype paradigm and
genome evolution. Nature 284:601-603.
Ehara, S. 1964. Some mites of the families Phytoseiidae and Blattisocidae from Japan
(Acarina: Mesostigmata). 1. Fac. Sci. Hokkaido Univ. Zool. 15:378-394.
Egan, M. E. and P. Hunter. 1975. Redescription of a cockroach mite, Protolaelaps
nauphoetae, with notes on its biology. Ann. Entomol. Soc. Am. 68:361-364.
Ehrman, L. and J. R. Powell. 1982. The Drosophila willistoni species group. In: The
Genetics and Biology of Drosophila Vol. 3B (M. Ashbumer, H. Carson and J. N.
Thompson, Jr. eds.). Academic Press, London. Pp. 193-226.
Engels, W. R. 1981. Hybrid dysgenesis in Drosophila melanogaster and the stochastic
loss hypothesis. Cold Spring Harbor Symp. Quant. Bioi. 45:561-565.
Engels, W. R. 1983. The P family of transposable elements in Drosophila. Annu. Rev.
Genet. 17:315-344.
Engels, W. R. 1988. P elements in Drosophila melanogaster. In: Mobile DNA (D. E.
Berg and M. Howe eds.). A. S. M. Publications, Washington DC. Pp. 437-484.
Engels, W. R. and C. R. Preston. 1979. Hybrid dysgenesis in Drosophila melanogaster:
the biology of female and male sterility. Genetics 92:161-174.
Engels, W. R. and C. R. Preston. 1980. Components of hybrid dysgenesis in a wild
population of Drosophila melanogaster. Genetics 95: 111-128.
Engels, W. R. and C. R. Preston. 1981. Drosophila Inf. Servo 56:35-37.
Evans, G. 0., J. G. Sheals and D. MacFarland. 1961. The Terrestrial Acari of the British
Isles. Volume I. Introduction and Biology, British Museum (Nat. Hist.), London. 219
pp.
Finnegan, D. J. 1985. Transposable elements in eukaryotes. Int. Rev. Cytol. 93:281-326.
Finnegan, D. J. 1989. Eukaryotic transposable elements and genome evolution. Trends
in Genetics 5: 103-107.
Finnegan, D. J. 1990. Transposable elements. Drosophila Inf. Servo 68:371-382.
Finnegan, D. J. and D. H. Fawcett. 1986. Transposable elements in Drosophila melano-
gaster. Oxford Surveys of Eukaryotic Genes, Vol. 3 (N. Maclean ed.). Oxford Univ.
Press, London. Pp. 1-62.
Good, A. G., H. Brock, T. A. Grigliatti and D. Hickey. 1989. Rapid spread of transposable
P elements in experimental populations in the genus Drosophila melanogaster. Genetics
122:387-396.
Hagemann, S., W. 1. Miller and W. Pinsker. 1990. P-related sequences in Drosophila
bifasciata: a molecular clue to the understanding of P-element evolution in the genus
Drosophila. 1. Mol. Evol. 31 :478-484.
Hammen van der, L. 1964. The morphology of Glyptholaspis confusa (FOA, 1900)
(Acarina, Gamasina). Zool. Verh. 71: 1-56.
Harris, L. J., D. L. Baillie, and A. M. Rose. 1988. Sequence identity between an inverted
repeat family of transposable elements in Drosophila and Caenorhabditus. Nucleic
Acids Res. 16:5993-5998.
Hickey, D. A. 1982. Selfish DNA: a sexually transmitted nuclear parasite. Genetics

101:519-535.
Houck, M. A., 1. B. Clark, K. R. Peterson and M. G. Kidwell. 1991. Possible horizontal
transfer of Drosophila genes by the mite Proctolaelaps regalis. Science 253: 1125-
1129.
Hughes, A. M. 1976. The Mites of Stored Food and Houses. Minist. Agric. Fish. Food
Tech. Bull. No.9. H.M.S.O., London. 400 pp.
Iwamura, Y., Y. Irie, R. Kominami, T. Nara and K. Yasuraoka. 1991. Existence of host-
related DNA sequences in the schistosome genome. Parasitology 102:397--403.
Kidwell, M. G. 1979. Hybrid dysgenesis in Drosophila melanogaster: the relationship
between the P-M and I-R interaction systems. Genet. Res. 33:205-217.
Kidwell, M. G. 1983. Evolution of hybrid dysgenesis determinants in Drosophila melano-
gaster. Proc. Natl. Acad. Sci. USA 80:1655-1659.
Kidwell, M. G. 1986. Molecular and phenotypic aspects of the evolution of hybrid
dysgenesis systems. In: Evolutionary Processes and Theory (S. Karlin and E. Nevo
eds). Academic Press, NY. Pp. 169-198.
Kidwell, M. G., J. F. Kidwell and J. A. Sved. 1977. Hybrid dysgenesis in Drosophila
melanogaster: a syndrome of aberrant traits including mutation, sterility, and male
recombination. Genetics 86:813-833.
Kidwell, M. G. and J. B. Novy. 1979. Hybrid dysgenesis in Drosophila melanogaster:
sterility resulting from gonadal dysgenesis in the P-M system. Genetics 92: 1127-1140.
Kidwell, M. G., J. B. Novy and S. M. Feeley. 1981. Rapid unidirectional change of
hybrid dysgenesis potential in Drosophila. 1. Hered. 72:32-38.
Kidwell, M. G., T. Frydryk and J. B. Novy. 1983. The hybrid dysgenesis potential of
Drosophila melanogaster strains of diverse temporal and geographical origin. Droso-
phila Inf. Servo 59:63-69.
Kidwell, M. G. and J. B. Novy. 1985. The distribution of hybrid dysgenesis determinants
in North American populations of Drosophila melanogaster. Drosophila Inf. Servo
61:97-100.
Kidwell, M. G., K. Kimura and D. M. Black. 1988. Evolution of hybrid dysgenesis
potential following P element contamination in Drosophila melanogaster. Genetics
119:815-828.
Kiyasu, P. K. and M. G. Kidwell. 1984. Hybrid dysgenesis in Drosophila melanogaster:
the evolution of mixed P and M populations maintained at high temperature. Genet.
Res. 44:251-259.
Konieczny, A., D. F. Voytas, M. P. Cummings and F. M. Ausubel. 1991. A superfamily
of Arabidopsis thaliana retrotransposons. Genetics 127:801-809.
Krantz, G. W. 1978. A Manual of Acarology, 2nd ed. Oregon State Univ. Book Stores,
Corvallis, OR. 509 pp.
Lansman, R. A., S. N. Stacey, T. A. Grigliatti and H. W. Brock. 1985. Sequences
homologous to the P mobile element of Drosophila melanogaster are widely distributed
in the subgenus Sophophora. Nature 318:561-563.
68 I M. A. Houck
Lindquist, E. E. 1965. Taxonomic concepts in the Ascidae, with a modified setal nomencla-
ture for the idiosoma of the Gamasina (Acarina: Mesostigmata). Mem. Entomol. Soc.
Can. 47:1-65.
Lindquist, E. E. 1971. New species of Ascidae (Acarina: Mesostigmata) associated with
forest insect pests. Can. Entomol. 103:919-942.
MacKay, T. F. 1985. Transposable element-induced response to artificial selection in
Drosophila melanogaster. Genetics 111:351-374.
Maruyama, K. and D. Hartl. 1991. Evidence for interspecific transfer of the transposable
element mariner between Drosophila and Zaprionus. 1. Mol. Evol. 33:514-524.
Mathys, G. and Y. Tencalla. 1959. Note preliminaire sur la biologie et la valeur predatrice
de Proctolaelaps hypudaei Oudms. (Acarien, Mesostigmata, Aceosejidae). Annu.
Agric. Suisse 60:645-654.
McClintock, B. 1948. Mutable loci in maize. Carnegie Inst. Wash. Yrbk. 47:155-169.
Miller, D. W. and L. K. Miller. 1982. A virus mutant with an insertion of a copia-like
transposable element. Nature 299:562-564.
Mizrokhi, L. J. and A. M. Mazo. 1990. Evidence for horizontal transmission of the mobile
element jockey between distant Drosophila species. Proc. Natl. Acad. Sci. 87:9216-
9220.
Montchamp-Moreau, c., G. Periquet and D. Anxolabehere. 1991. Interspecific transfer
of P elements by crosses between Drosophila simulans and Drosophila mauritiana. J.
Evol. Bioi. 4:131-140.
Muma, M. H. 1961. Mites associated with citrus in Florida. Bull. Univ. Fla. Agric.
Exp. Sta. 640 pp.
Muma, M. H. 1975. Mites associated with citrus in Florida. Bull. 640 A, Agric. Exp.
Sta. Instit. Food and Agric. Sci. Univ. Florida, Gainsville. 92 pp.
Nesbitt, H. H. J. 1951. A taxonomic study of the Phytoseiinae (family Laelapidae)
predaceous upon Tetranychidae of economic importance. Zool. Verh. vol. 12 (64 pp).
O'Hare, K. and G. M. Rubin. 1983. Structures of P transposable elements of Drosophila
melanogaster and their sites of insertion and excision. Cell 34:25-35.
Patterson,1. T. and W. S. Stone. 1952. Evolution in the genus Drosophila. Macmillan,
NY.
Radovsky, F. J. 1985. Evolution of Mammalian Mesostigmate mites. In: Coevolution of
Parasitic Arthropods and Mammals (K. C. Kim ed.). Wiley, NY. 800 pp.
Rio, D. c., F. A. Laski and G. M. Rubin. 1986. Identification and immunochemicaI
analysis of biologically active Drosophila P element transposase. Cell 44:21-32.
Rubin, G. M. 1983. Dispersed repetitive DNAs in Drosophila. In: Mobile Genetic Ele-
ments (J. A. Shapiro ed.). Academic Press, NY. 688 pp.
Rubin, G. M. and A. C. Spradling. 1982. Genetic transformation of Drosophila with
transposable element vectors. Science 218:348-353.
Rubin, G. M., M. G. Kidwell and P. M. Bingham. 1982. Cell 29:987-994.
Mites as Potential Horizontal Tramfer Vectors of Eukaryotic Mobile Genes / 69
Schaefer, R. E., M. G. Kidwell and A. Fausto-Sterling. 1979. Hybrid dysgenesis in

Drosophila melanogaster: morphological and cytological studies of ovarian dysgenesis.
Genetics 92:1141-1152.
Snyder M. and W. F. Doolittle. 1988. P elements in Drosophila: selection at many levels.
Trends in Genetics 4:147-149.
Spradling, A. C. and G. M. Rubin. 1982. Transposition of cloned P elements into
Drosophila germ line chromosomes. Science 218:341-347.
Steller, H. and V. Pirrotta. 1985. Fate of DNA injected into early Drosophila embryos.
Dev. Bioi. 109:54.
Throckmorton, L. H. 1975. The phylogeny, ecology and geography of Drosophila. In:
Handbook of Genetics, Vol. 3 (R. C. King ed.). Plenum Press, NY. Pp. 421--469.
Todo, T., Y. Sakoyama, S. I. Chigusa, A. Fukunga, T. Honjo and S. Kondo. 1984.
Polymorphism in distribution and structure of P elements in natural populations of
Drosophila melanogaster in and around Japan. lpn. l. Genet. 59:441-451.
Wemz, J. G. and G. W. Krantz. 1976. Studies on the function of the tritostemum in
selected Gamasida (Acari). Can. l. Zool. 54:202-213.
Woolley, A. 1988. Acarology: Mites and Human Welfare. John Wiley and Sons, NY.
484 pp.
Xiong, Y. and Eickbush, T. H. 1988. Similarity of reverse transcriptase-like sequences
of viruses, transposable elements and mitochondrial introns. Mol. Bioi. Evol. 5:675-
690.
4
Evolution of Life-History Patterns

in the Phytoseiidae
Maurice W. Sabelis and Arne Janssen
CONTENTS
I. INTRODUCTION
2. CRITERIA FOR DATA SELECTION
3. REVIEW OF THE LITERATURE
4. WITHIN-SPECIES, WITHIN-GENUS AND BETWEEN-GENUS
TRENDS
5. REPRODUCTION SCHEDULES AND THEIR EFFECT ON THE IN-
TRINSIC RATE OF INCREASE
6. EVOLUTION OF LIFE-HISTORY PATTERNS IN THE PHYTO-
SEIIDAE: AN HYPOTHESIS ON CONSTRAINTS
1. Introduction
Among mites that inhabit plants, the Phytoseiidae rank as being well studied with
respect to their life-history patterns and capacity for population increase. The
number of published papers on the Phytoseiidae (between 1950-1991) is not
much less than that for economically important phytophagous mites; there are c.
150 papers on Phytoseiidae, compared to c. 200 for the Tetranychidae (phytopha-
gous spider mites). The impetus to study life-history patterns in detail comes
from the successful use of the Phytoseiidae as predators to control phytophagous
mites on agricultural crops (Helle and Sabelis 1985a, 1985b). Fortunate as this
abundance of Phytoseiidae literature may seem to anyone interested in studying
life-history patterns, there is a danger that the range of species studied is biased
towards phytoseiids that are successful predators of economically important plant
mites. This would be a serious problem when research hypotheses merely emerge
from comparisons among life-history data, but less so when hypotheses stem
from more general considerations about the ecological conditions under which
life histories may have evolved. Hence, the approach taken here is to formulate
hypotheses independent of the actual life-history data. Support by the data does
70
Evolution of Life-History Patterns in the Phytoseiidae / 71
not mean that the hypotheses hold true, but merely that they are not rejected thus
far. The data are only used to falsify hypotheses, and to stimulate thought on
more precise hypotheses and more critical tests.
What follows first is a literature review of life-history traits of phytoseiid mites
(excluding such aspects as survival, diapause, and dependence on abiotic factors),
i.e. rate of development, fecundity and sex ratio. This review relates to the
relevant literature published up to mid-1991. As such, it is an updated version of
an earlier paper reviewing the literature up to mid-1984 (Sabelis 1985a, 1985b,
1985c, 1985d).
Subsequently, we will argue why local popUlations of phytoseiid mites are
likely to be transient, and then proceed by formulating hypotheses on life-history
trends under unconstrained r-selection and by testing them using the literature
data. Deviations from these hypotheses serve to indicate possible constraints on
life-history evolution. Finally, we formulate and discuss a new hypothesis that
takes these constraints into account.
2. Criteria for Data Selection
Life-history studies show quite some variation in experimental setup. For exam-
ple, studies are done at different temperatures, with various food types, and with
groups of females or isolated individuals. For these reasons, data were selected
according to the following criteria: (l) an ample supply of tetranychids should be
offered as prey; (2) temperature should fall within the range of 23°-27°C, and
preferably be equal to 25°C; (3) sex ratio should be assessed in the offspring of
isolated females; (4) peak and/or mean rates of oviposition should be presented;
(5) the intrinsic rate of increase should be calculated from a life table using
Lotka's equation (and not from approximating formulas based on simplified
reproduction schedules). The data selected are listed in Appendix 4.1 and Appen-
dix 4.2.
3. Review of the Literature
To elucidate what life-history patterns are common among mites and which salient
properties pertain to the mite group under consideration, it is useful to compare
life-history trends in the Phytoseiidae (Acari: Mesostigmata) with those observed
in other mite families. To date, such a comparison can only be made with data
from the Tetranychidae (spider mites), as compiled by Sabelis (1991) according
to the same selection criteria. This family of phytophagous mites belongs to
the order Prostigmata, but, being phytophagous, these mites live in the same
microhabitat as phytoseiid mites and have a similar body size. Furthermore, they
represent a very important prey item on the menu of phytoseiid mites. Hence,
comparison of their life histories goes beyond that of comparing families with
n(Tl)
n(T2)
0 ATl T2
0 15 30
age x
[days]
(A)
16
14
12
10
6
•
4
4 6 8 10 12 14
A
(B)
Figure 4.1. A generalized reproduction schedule of phytoseiid mites. A) An example of
a typical reproduction schedule: Data for Amblyseius idaeus (Dinh et al. 1988). The x-
axis gives the age of the female (x). The symbols A, T J , T2 and W represent the age at first
oviposition, age at the start of peak oviposition, age at the end of the peak oviposition
period and age at the end of the oviposition period. The y-axis shows the ovipositional
rate (n(x)). B) Correlation and regression between A and T T = 1.73 + 1.03A (54 data
J : J
points; R2= 0.789). C) Correlation and regression between A and T2 : T2 = 6.76 + 1.56A
(45 data points; R2= 0.261). D) Correlation and regression between A and W : W = 15.2
+ 2.47A (51 data points; R2= 0.282).
72
40
• •
30
20
10
4 6 8 10 12 14
A
(C)
60
•
50 •
40
30
20 • •
4 6 8 10 12 14
A
(D)
widely different phylogenies: it is a comparison of ecological life styles (i.e.

predator vs. prey).
Consider the reproduction curves of the species in the families Phytoseiidae
and Tetranychidae. Lewontin (1965) suggested that reproduction curves are often
triangular. Indeed, the reproduction curves of spider mites generally have such
74 I M. W. Sabelis and A. Janssen
a form (Sabelis 1991). The rate of oviposition steeply rises to a peak soon after
the onset of reproduction, and then decreases gradually. This triangular curve
was also observed in phytoseiid mites, but only in less than 20% of the cases.
The more general form was a trapezoid, of which an example is shown in Figure
4.IA (following Lewontin's notation as closely as possible). As in spider mites,
the ovipositional rate (fi(x» rapidly increases from the beginning of the reproduc-
tion period (A) until it reaches a peak at age T but it then levels off, with a slight
J,
increase or decrease towards the end of this plateau phase (Tz). It subsequently
decreases until it becomes zero at the end of reproductive life (W). We define
peak rate of oviposition as the rate of oviposition at age T J (i.e. n(T J», and the
mean rate of oviposition (fi(x» as the average over the entire reproductive period
(from age A to W).
Although the trapezoid qualitatively seems the most common shape of the
reproduction curve, its dimensions may vary considerably. Figure 4.1B shows
that the age at peak oviposition, T follows within two days after the onset of
J,
oviposition at age A and that T J is linearly and positively correlated with A;

however, as shown in Figure 4.1C and 4.1D, the age at the end of peak oviposition
(Tz) and the age at last oviposition (W) are much less associated with A. In
conclusion one may consider the reproduction curve to approximate a rectangular
trapezoid of rather variable form.
In Figure 4.2A the rate of development is regressed on the (mean or peak)
rate of oviposition and in Table 4.1 the reverse regression is given. There is
unambiguous evidence for a linear relation. This is in contrast to what has been
found for spider mites (Sabelis 1985e, Sabelis 1991). The correlations in the
latter taxonomic group is clearly non-linear, indicating that the developmental
rates may reach a maximum, whereas oviposition continues to increase.
For phytoseiid mites, the best-fitting regression models are linear, suggesting
the absence of a maximum developmental rate. Much the same conclusions can
be drawn by considering the relation between fecundity and the rate of develop-
ment (Table 4.1). For phytoseiid mites this relation is linear, whereas for spider
mites it is non-linear. When considering the relation between fecundity and the
rate of oviposition for both phytoseiid mites and spider mites (Fig. 4.2B and
Table 4.1), the relations do not deviate from linearity. Thus, there is no reason
to assume that there is a physiological maximum to either of the two traits.
Figure 4.2C and Table 4.1 show that for phytoseiid mites the proportion of
daughters increases starting from 57% up to 91 % with the mean and peak rate of
oviposition (Sabelis and Nagelkerke 1992). In contrast to earlier reports on
logarithmic relations (Sabelis 1985d, Sabelis and Nagelkerke 1988), the extended
data set here is described somewhat better by a linear relationship. For spider
mites, sex ratios are also always female biased (varying from 55%-91 % daugh-
ters), but there is no significant correlation with the ovipositional rate (Sabelis
1991 and Table 4.1).
Given that the life-history traits underlying the population growth capacity are
0.3
-
C
III
E •
Q.
0
0.2
Cii>:
> ca
-
111'0
'0-
~
-
0 0.1
III
ca
~
• •
0.0
0 1 2 3 4 5
mean rate of oviposition
[eggs/female/day]
0.3
-C
ell
E
Q.
0
0.2
Cii>:
> ca
-...
~~
......
-..
0 0.1
ell
ca
o 234 5 6
peak rate of oviposition
[eggs/female/day]
(A)
Figure 4.2. Correlations and regressions between various life-history components and
either peak or mean rate of oviposition. A) Regression of rate of development on mean
(87 data points, R2 = 0.619, Y = 0.0740 + 0.028 x) and peak (52 data points, R2 = 0.576,
Y = 0.083 + 0.019 x) rate of oviposition. B) Regression of fecundity on mean (97 data
points, R2 = 0.45, Y = 12.4 + 12.0 x) and peak (54 data points, R2 = 0.48, Y = 8.5 +
10.9 x) rate of oviposition. C) Regression of proportion daughters in the offspring on mean
(42 data points, R2 = 0.43, Y = 0.60 + 0.056 x) and peak (28 data points, R2 = 0.21,
Y = 0.61 + 0.040 x) rate of oviposition. D) Regression of the intrinsic rate of increase on
mean (45 data points, R2 = 0.76, Y = 0.07 + 0.075 x) and peak (38 data points, R2 =
0.83, Y = 0.05 + 0.069 x) rate of oviposition.
75
80 •
•••
•• • •
I,... '• •.•
• •
Qj' 60
>--
_tIS
;;E •
•••
•
•,"'. •.
CQ)
•
,. ••
;:,- 40
(,)-
•
Q)1Il
_t»
t»
..
Q)
......
20
•
• •• • •
0
0 1 2 3 4 5
[eggs/female/day]
80
• ••
....Q) • • •
60
• •
.:-• •••
>-tIS
=E
• •
'CQ)
C_
;:,- 40
••
(,)1Il
Q)t»
-t»
Q)
......
20
•
• •• • •
0
0 2 3 4 5 6
[eggs/female/day]
(8)
76
1.0
...III
-
CI)
.c
CI
:::J
ca
0.9
0.8
"0
-...
C
.2 0.7
0
0.
...
0
0.
0.6
•
....
•••
0.5
0 1 2 3 4 5
[eggs/female/day]
1.0
...
-
III
CI) 0.9
.c
•• •
• • ••
CI
:::J
ca 0.8
"0
-...
C
••
.2 0.7
0
0.
...
• •
0
0.
0.6 • •
0.5
2 3 4 5 6
[eggslfemale/day]
(C)
77
0.5
,
CD
1/1
cu
... 0.4
•.
CD
. •_
(J
.=
0.3 ,
-........--
-~
0>-
CD'C
cu
• •
• •• 1-•
cu,...
0.2
(J
'iii ••
-c:
i:
c:
0.1
0.0
0 1 2 3 4 5
[eg gs/female/day]
0.5
CD
1/1
cu
...
CD
(J
0.4
.=
-~ 0.3
---
0>-
cu
CD'C
........
CU,...
0.2
(J
'iii
-c:
i:
.=
0.1
0.0
0 234 5 6
[eg gs/female/day]
(D)
78
Table 4.1. Regression equations and correlation coefficients between life history
traits of phytoseiid mites and tetranychid mites (Janssen and Sabelis 1992, Sabelis
1990). Note that N represents the number of data pairs and R2 is the square of the
correlation coefficient. The regression equations and correlations obtained merely
serve descriptive purposes. Error in the x-variables, such as ovipositional rate and
developmental rate, is usually quite small, justifying the use of univariate regression.
Variable
Independent Dependent R2 Regression Equation N
PHYTOSEIID MITES:
Rate of Mean Rate of 0.619 y = -0.885 + 22.15 x 87
Development Oviposition
Peak Rate of 0.576 y = -1.296 + 29.75 x 52
Oviposition
Fecundity 0.232 y = 9.24 + 219.5 x 76
Sex Ratio 0.434 y = 0.503 + 1.67 x 28
Tm 0.637 Y = -0.119 + 2.66 x 37
Mean Rate of Rate of 0.619 y = 0.074 + 0.028 x 87
Oviposition Development
Fecundity 0.450 y = 12.4 + 12.0 x 97
Sex Ratio 0.432 y = 0.60 + 0.056 x 42
Tm 0.755 Y = 0.07 + 0.075 x 45
Peak Rate of Rate of 0.576 y = 0.083 + 0.019 x 52
Fecundity 0.478 y = 8.5 + 10.9 x 54
Sex Ratio 0.213 y = 0.61 + 0.04 x 28
Tm 0.834 Y = 0.053 + 0.069 x 38
TETRANYCHID MITES:
Rate of Peak Rate of 0.639 y = 0.7 * 10" 82,
45
Development Oviposition
Fecundity 0.485 y = 7.85 * 10"5lx 44
Sex Ratio 0.063 37
Tm 0.631 Y = -0.007 + 2.67 x 40
Mean Rate of Rate of 0.235 y = 0.06 + 0.0041 x 27
Fecundity 0.578 y = 1.81 + 0.031 x 26
Sex Ratio 0.123 18
Tm 0.646 Y = 0.123 + 0.012x 32
Peak Rate of Rate of 0.564 y = 0.039 + 0.022 log x 45
Fecundity 0.717 y = 1.425 + 11.5 x 37
Sex Ratio 0.044 34
Tm 0.550 Y = 0.013 + 0.011 x 35
79
80 / M. W. Sabelis and A. Janssen
linearly interrelated, what would one expect of the relation with r m (intrinsic rate
of increase of a population)? Considering the data presented in Figure 4.2D and
Table 4.1, the r m of phytoseiid mites is linearly related to the rate of development
and the (mean or peak) rate of oviposition. The same type of relation was found
for spider mites (Sabelis 1991, Janssen and Sabelis 1992). Why this is the case,
will be discussed after the next section, in which the data are scrutinized for the
effects of overrepresentation of species or genera.
4. Within-Species, Within-Genus and Between-Genus ltends
One may wonder to what extent these results are biased by overrepresentation of
some species in the data set, especially Phytoseiulus persimilis and Typhlodromus
occidentalis (represented by 10 and 6 data pairs respectively in the data set
concerning developmental and ovipositional rates). Figure 4.3A shows that the
data of P. persimilis alone have a trend of rates of development increasing with
mean rates of oviposition in the range of 2.5-5.0 eggs per day. This trend is quite
close to the overall regression of the rate of development on the mean rate of
oviposition based on averages per species. This suggests that the trends within
species conform to those between species, but more rigorous tests are needed.
Unfortunately, the few data available for T. occidentalis (Fig. 4.3A) vary over
a rather small range and are too clustered to negate the hypothesis that within-
species trends conform to between-species trends.
Another bias may result from overrepresentation of particular genera. To
investigate this effect, Figure 4.38 shows within-genus trends (where means/
species are shown and each data set per species is represented by a character
indicating the genus). Considering the well represented genera, Amblyseius and
Typhlodromus, the within-genus regression lines conform quite closely to the
overall regression lines (albeit that the former is somewhat higher and the latter
is systematically lower!). The data of the less represented genera, Phytoseius and
Phytoseiulus, are remarkably close to the overall regression line, which strongly
argues for conformity of within-genus trends and within-family trends. In all
further analyses we assume that this conformity holds true, making overrepresen-
tation of species or genera less of a problem. However, this assumption needs
scrutiny in future investigations.
5. Reproduction Schedules and Their Effect on the Intrinsic Rate of

Increase (rm)
That rm is linearly related to the rate of oviposition is surprising when considering

the following model for the relation between r m' net reproductive rate (Ro) and the
rate of development (lIA) for the simple case of big-bang reproduction (a single,
large clutch of eggs produced immediately when reaching the reproduction phase):
0.3
-
cII)
E
0.2 P P
Q.
.2>:
-..
11)111
>-0
11)_
-o~
0
II) 0.1
1ii
o
o 2 4
[eggs/female/day]
(A)
Figure 4.3. Examples of within-species and within-genus correlations and regressions.
A) Correlations and regressions between mean rate of oviposition and the rate of develop-
ment for two species of the Phytoseiidae. Shown are the regression lines for Phytoseiulus
persimilis (dashed line; IO data points, R2 = 0.25, Y = 0.10 + 0.016 x), Typhlodromus
occidentalis (dotted line; 6 data points, R2 = 0.05, y = 0.14 - 0.008 x) and for all species
(drawn line; 48 data points, R2 = 0.568, y = 0.064 + 0.032 xl. Bl Correlations and
regressions between peak rate of oviposition and rate of development for four genera of
the Phytoseiidae. Each data point represents the average value per species and is indicated
by a character referring to the genus: A. = Amblyseius, P. = Phytoseiulus, Ph. =
Phytoseius and T. = Typhlodromus. Shown are the regression lines for all species (drawn
line; 27 data points, R2 = 0.67, Y = 0.069 + 0.024 x), for Amblyseius (broken line; 17
data points, R2 = 0.64, y = 0.072 + 0.025 xl and for Typhlodromus (dotted line; 5 data
points, R2 = 0.76, y = 0.049 + 0.026 xl.
Clearly, rm is not linearly, but logarithmically related to Ro (and thus also to

the ovipositional rate) and linearly to the rate of development (lIAl (and thus also
to the ovipositional rate via the regression in Figure 4.2A). However, for phyto-
seiid mites ovipositional and developmental rates covary, which may cause that
the effect of one variable on rm masks the effect of the other. To investigate this
effect, a better approximation of rm is needed than provided by the above formula
(which for Ro taken equal to fecundity times sex ratio grossly overestimates the
rm calculated by the Lotka equation, and for Ro taken equal to the peak oviposi-
0.2
A
>\-----
--------
0.15 4.. P ------ p
~ --A
E
•Ea..
.2-;:
)ltr-- -- -- A ~/
~ 0.1 -- A~"-
"".:r-.....--- A
ID
.l!. A
........... _----- ............
"0::.
a T
!•
0.05
o +----.----.----.---.----.----.----r---,----,
0.5 1.5 2.5 3.5 4.5
[eggs/female/day)
(B)
tional rate times the sex ratio grossly underestimates the rm calculated by the
Lotka equation). Such a simple, but better approximator is obtained by taking
the reproduction schedule of Figure 4.5a as a starting point, further referred to
as the Methuselah version. Here, oviposition reaches its peak immediately upon
reaching the reproduction phase and remains so for ever. The formula for calculat-
ing rm is presented in Appendix 4.3. Using this model and taking the linear
regressions of the developmental rate and the sex ratio on the peak rate of
oviposition (Fig. 4.2A, C) into account (while ignoring age-dependent mortality),
the relation between rm and the peak rate of oviposition becomes linear (Fig.
4.4), showing that the changes in the rate of development have a more profound
effect on rm than changes in the rate of oviposition.
Figure 4.4 also demonstrates another important conclusion, which emerges
when comparing the Methuselah calculations (where mortality, the increase phase
and the decrease phase in the oviposition curve are altogether ignored) and the
Lotka calculations based on the full life table (including mortality and age related
changes in oviposition). The difference between the two calculations is rather
small and will become even less when taking juvenile mortality, the initial
increase phase of the oviposition curve, mortality and oviposition later in life into
account. Hence, there is little need to discriminate between reproduction sched-
ules such as rectangular, triangular or trapezoid forms (Fig. 4.5b, c, d). The
Evolution of Life-History Patterns in the Phytoseiidae I 83
a b
:g :g
c c
A A w
x x
c d
:g :g
c c
A w A w
x x
Figure 4.4. Four simplified age-specific reproduction functions (graphs of n(x) against
x): (a) the Methuselah schedule; (b) the rectangular schedule; (c) the triangular schedule;
(d) the trapezoid schedule.
caricature of Methuselah performs rather well and may therefore be considered

to capture the essence of the traits relevant to r-selection. Thereason for all this
is that reproduction later in life is devalued in terms of its effect on rm by a factor
with a negative exponent including r m and age x (i.e. exp (-r mX) in the Lotka
equation; see Appendix 4.3, Caswell and Hastings 1980, Caswell 1982).
6. Evolution of Life-History Patterns in the Phytoseiidae: an Hypothesis

on Constraints
As argued by Sabelis (1991) local populations of spider mites are likely to be

transient. Phytoseiid mites are among the causative factors that contribute to
extinction of local spider mite populations (Sabelis and Van der Meer 1986,
Janssen and Sabelis 1992). Consequently, local populations of phytoseiid mites
go through high peaks and troughs, even more so when taking harsh weather
conditions (e.g. wind, drought and rain) into account. Under these conditions
selection for colonizing ability and for production of dispersers (i.e. r-selection)
is likely to prevail. It may well be that fluctuations are less vigorous due to the
presence of alternative food or the provision of shelter by host plants (acarodo-
mafia). However, for one thing, alternative food is usually of low quality (honey-
dews, phloem exudates; see Bakker and Klein 1992) or deficient in some nutrients
(e.g. pollen, see Dicke et al. 1986) and, for another, plant structures providing
shelter can only decrease the impact of weather conditions, but not prevent
84 / M. W. Sabelis and A. Janssen
0.10 0.15 0.20 0.25 0.30 0.35

0.5 -t---'.!.!--,-----,-----,-----.,,----,------,------
0.4
.
CC
..E
.!!.. 0.3
E
.
E
0
..E
0.2
2 3 4 5
n(T1)
[eggs/female/day]
Figure 4.5. Estimation of rm at various ovipositional rates, assuming that mortality is

negligible (I, = I for all values of x) and that the rate of oviposition (daughter production)
reaches a peak (equal to m(T1) = n(T 1) s(T1» immediately after the developmental period
and remains indefinitely so (i.e. the Methuselah version of the Lotka equation). The
estimation procedure is outlined in Appendix 4.3 and is visualized by the intersection
(open dots) of the horizontal lines (with rm on the y-axis) and the curves (with m(T 1) exp(-
rrnA) for different values of rm on the y-axis). The drawn line represents the regression of
rm on n(T1) (Figure 4.2D). In all calculations the developmental time, A, and the sex ratio
s(T1) are treated as a function of the peak ovipositional rate, n(Tl): A = [0.084 + 0.019
n(T1)r 1 (see Figure 4.4A) and s(T 1) = 0.61 + 0.04 n(T1) (see Figure 4.2C).
them. Moreover, it should be realized that either presence of alternative food or

protection will not change the direction of the selective forces.
Returning to the life-history patterns underlying the capacity for population
increase, the most salient conclusion is that most life-history traits of phytoseiid
mites strongly covary in a positive and linear fashion. This suggests that all life-
history traits can change simultaneously so as to increase r m' and, thus, that there
are no trade-offs between the traits involved. Why then, do not all phytoseiid
species have a maximum rate of population increase? One possibility is that
selection proceeds at a different pace for each species, but, given enough genera-
tions, the end product would be that all species ultimately multiply at a maximum
rate. The other possibility is that life-history evolution of the Phytoseiidae is

determined primarily by external, rather than internal constraints.
Are there life-history phenomena indicating the presence of (external) con-
straints? Our review of life-history patterns of the Phytoseiidae did not show an
upper asymptote on the rate of development, as was the case for spider mites
(Sabelis 1991). Also, non-linearities were absent in all other regressions between
life-history components. The only exception is the reproduction schedule, which
one would expect to have a single peak early in the reproduction period. This is
expected because: (1) shifting reproductive effort to younger ages (i.e. at the
expense of reproduction later in life) is most effective in terms of increasing rm'
and because (2) selection on deleterious mutations becomes progressively weaker,
the later in life they are expressed (Caswell and Hastings 1980, Caswell 1982).
This would lead to evolution of reproduction schedules starting from the Methu-
selah type to the triangular type. Clearly, phytoseiid mites have a reproduction
schedule of a rectangular trapezoid shape, which may be interpreted as 'a trun-
cated triangle.' Moreover, as revealed by our analysis of life-history patterns, the
most significant differences between species of phytoseiid mites are found in the
timing and magnitude of peak oviposition. We suggest that the truncation of the
triangle points to the presence of constraints in the process of egg production.
What determines the rate of egg production? As in most predatory arthropods
(Sabelis 1992), this strongly depends on both food acquisition and conversion into
egg biomass. Phytoseiid mites allocate a remarkably large fraction of food ingested
to egg production. For example, P. persimilis converts 70% of the food ingested
into eggs and it produces a daily egg biomass equal to its own body weight. In
general, oviposition is strongly correlated with predation (Janssen and Sabelis
1992) and both reach an upper asymptote with increasing prey densities, but the
level of the asymptotes differs between species. As shown by Sabelis (1986, 1990),
the asymptotes are determined by gut capacity and the relative rate of gut emptying.
Because egg size and gut volume are roughly in proportion to the size of the adult
predator, the trait relevant to explaining the interspecific differences in asymptotes
is the relative rate of gut emptying rather than the gut volume. Thus, our original
question concerning the rate of egg production can now be rephrased as "What
determines interspecific variation in the relative rate of gut emptying?" or "Why
should not all predators have a maximal rate of gut emptying?"
We suggest that the relative rate of gut emptying (and conversion into egg
biomass) has evolved into an optimum between prey intake rates and the costs
associated with food conversion. If the predator would digest and convert slowly,
it would save costs involved in food conversion, while loosing opportunity to
produce more eggs per time unit. If the predator would be capable of rapid
digestion and rapid conversion per unit biomass, it would use energy for food
conversion at the expense of egg production. Hence there should be an optimum
in the relative rate of food conversion, set by the rate of food intake. For this
reason we suppose that the actual constraints are not physiological, but relate to
the densities of the preferred prey. There are good reasons to think that the diets
of phytoseiid mites differ, that their prey preferences differ and that various prey
types occur in widely different densities (Sabelis and Dicke 1985, Dicke et al.
1988). For example, spider mites do not only differ in the way they defend
themselves against their predators, but their densities are partly species-specific
and partly host-plant related. This has led to the concept of characteristic prey
densities (Sabelis 1985e, 1991), which may not only be crucial for understanding
life-history evolution of spider mites, but also to understand life-history evolution
of phytoseiid mites, their main predators: characteristic prey densities determine
the maximum predation rates, the optimal rates of food conversion and thus the
(peak) rate of oviposition. In addition to explaining the evolution of the oviposi-
tional rate, characteristic prey densities may also be a key factor in explaining the
evolution of sex ratios in phytoseiid mites (Sabelis 1985d, Sabelis and Nagelkerke
1988, Sabelis and Nagelkerke 1992).
To conclude, we suggest that the evolution of life-history patterns in the
Phytoseiidae is critically dependent on the local distribution patterns of their prey
and, as argued earlier (Sabelis 1991), the evolution of local distribution patterns
of the prey may at least partly be determined by the impact of predation by
phytoseiid mites. The extent to which life-history and distribution patterns are
molded by coevolution, is a major question for future research.
Acknowledgments
We thank Andre de Roos for stimulating discussions and Tine Dijkman-
Korzilius for moral support and a constant flow of coffee.
References
Bakker, F. M. and M. E. Klein. 1992. Transtrophic interactions in cassava. Exp. Appl.

Acarol. 14:293-311.
Caswell, H. 1982. Life-history theory and the equilibrium status of populations. Am. Nat.
120:317-339.
Caswell, H. and A. Hastings. 1980. Fecundity, developmental time and population growth
rate: an analytical solution. Theor. Populo Biol. 17:71-79.
Dicke, M., M. W. Sabelis and A. Groeneveld. 1986. Vitamin A deficiency modifies the
response of the predatory mite Amblyseius potentillae to a volatile kairomone of the
two-spotted spider mite. J. Chem. Ecol. 12:1389-1396.
Dicke, M., M. W. Sabelis and M. de long. 1988. Analysis of prey preference in phytoseiid
mites by using an olfactometer, predation models and electrophoresis. Exp. Appl.
Acarol. 5:225-241.
Helle, W. and M. W. Sabelis. 1985a. Spider Mites: Their Biology, Natural Enemies and
Control, Vol. 1 A. Elsevier, Amsterdam. 403 pp.
Helle, W. and M. W. Sabelis. 1985b. Spider Mites: Their Biology, Natural Enemies and
Control, Vol. 1 B. Elsevier, Amsterdam. 458 pp.
Evolution of Life-History Patterns in the Phytoseiidae I 87
Janssen, A. and M. W. Sabelis. 1992. Phytoseiid life-histories, local predator-prey dynam-

ics, and strategies for control of tetranychid mites. Exp. Appl. Acarol. 14:233-250.
Lewontin, R. C. 1965. Selection for colonizing ability. In: The genetics of colonizing
species (H. G. Baker and G. L. Stabbins eds.). Academic Press, NY. Pp. 79-94.
Sabelis, M. W. 1985a. Capacity for population increase. In: Spider Mites, their Biology,
Natural Enemies and Control, Vol. I B (W. Helle and M. W. Sabelis eds). Elsevier,
Amsterdam. Pp. 35-41.
Sabelis, M. W. 1985b. Development. In: Spider Mites, their Biology, Natural Enemies
and Control, Vol. I B (W. Helle and M. W. Sabelis eds.). Elsevier, Amsterdam.
Pp.43-53.
Sabelis, M. W. 1985c. Reproduction. In: Spider Mites, their Biology, Natural Enemies
and Control, Vol. 1 B (W. Helle and M. W. Sabelis eds.). Elsevier, Amsterdam. Pp.
73-82.
Sabelis, M. W. 1985d. Sex Allocation. In: Spider Mites, their Biology, Natural Enemies
and Control, Vol. 1 B (W. Helle and M. W. Sabelis eds.). Elsevier, Amsterdam. Pp.
83-94.
Sabelis, M. W. 1985e. Reproductive strategies. In: Spider Mites, their Biology, Natural
Enemies and Control, Vol. 1 A (W. Helle and M. W. Sabelis eds.). Elsevier, Amster-
dam. Pp. 265-278.
Sabelis, M. W. 1986. The functional response of predatory mites to the density of two-
spotted spider mites. In: Dynamics of Physiologically Structured Populations, Lecture
Notes in Biomathematics 68 (1. A. 1. Metz and O. Diekmann eds.). Springer, Berlin.
Pp. 298-321.
Sabelis, M. W. 1990. How to analyze prey preference when prey density varies: a new
method to discriminate between effects of gut fullness and prey type composition.
Oecologia (Berl.) 82:289-298.
Sabelis, M. W. 1991. Life-history evolution of spider mites. In: The Acari, Reproduction,
Development and Life-History strategies (R. Schuster and P. W. Murphy eds.). Chap-
man and Hall, London. pp. 23-49.
Sabelis, M. W. 1992. Predatory arthropods. In: Natural Enemies: The Population Biology
of Predators, Parasites, and Diseases (M. 1. Crawley ed.). Blackwell, Oxford. pp.
225-264.
Sabelis, M. W. and M. Dicke. 1985. Long range dispersal and searching behaviour. In:
Spider Mites, their Biology, Natural Enemies and Control, Vol. 1 B (W. Helle and M.
W. Sabelis eds.). Elsevier, Amsterdam. Pp.141-160.
Sabelis, M. W. and J. Van der Meer. 1986. Local dynamics of the interaction between
spider mites and predatory mites. In: Dynamics of Physiologically Structured Popula-
tions, Lecture Notes in Biomathematics 68 (1. A. J. Metz and O. Diekmann eds.).
Springer, Berlin. pp 322-344.
Sabelis, M. W. and C. 1. Nagelkerke. 1988. Evolution ofpseudo-arrhenotoky. Exp. Appl.
Acarol.4:301-318.
Sabelis, M. W. and C. J. Nagelkerke. 1992. Sex allocation and pseudo-arrhenotoky in
phytoseiid mites. In: The Evolution and Diversity of Sex Ratio in Insects and Mites (D.
Wrensch and M. Ebbert eds.). Chapman and Hall, NY. Pp. 512-541.
Appendix 4.1. Characteristics of the reproductive schedule of phytoseiids. Ages are expressed in days since the start of the egg stage. (A.
Amblyseius, P. = Phytoseiulus, Ph. = Phytoseius, T. = Typhlodromus).
Species A' T, T 2" W n(T,) n(T2 )" References
A. aberrans 10.3 12.3 24.3 37.3 1.2 1.2 Kropczynska et al. 1988
A. andersoni 10.4 14.4 24.4 52.4 2.0 1.8 Amano & Chant 1977
A. anonym us 7.3 9.0 20.0 40.0 2.6 2.5 Van Dinh et al. 1988
A. bibens 6.5 8.5 21.5 35.5 3.7 3.0 Blommers 1976
A. bibens 6.4 8.4 13.4 35.4 3.8 3.4 Lababidi 1988
A. citrifolius 7.1 10.1 23.1 41.1 2.2 2.3 De Moraes & McMurtry 1981
A. cucumeris 9.5 11.5 43.5 2.0 Lababidi 1988
A. degenerans 7.7 9.7 20.7 46.7 2.4 2.8 Takafuji & Chant 1976
A. deleoni 6.5 8.5 14.5 3.5 2.7 Saito & Mori 1981
A·fal/acis 6.3 9.3 31.3 3.4 Lababidi 1988
A. fal/acis 7.1 9.1 19.1 29.1 2.5 2.7 Boyne & Hain 1983
00 A·fal/acis 7.3 9.3 19.3 34.3 2.7 2.8 Boyne & Hain 1983
00
A. finlandicus 9.8 10.8 15.8 37.8 0.6 0.7 Kropczynska et al. 1988
A. idaeus 7.3 9.0 19.0 34.0 2.8 2.7 Van Dinh et al. 1988
A. idaeus 7.0 8.0 11.0 27.0 2.4 2.8 Janssen & Rook unpubl.
A. largoensis 8.8 10.8 16.8 31.8 1.8 2.0 Tanaka & Kashio 1977
A. longispinosus 6.4 8.4 30.4 3.6 Lababidi 1988
A. longispinosus 7.7 11.5 20.0 45.0 2.9 3.0 Lo & Ho 1979
A. longispinosus 4.5 5.5 21.5 29.5 3.8 3.4 Mallik & ChanaBassavanna 1983
A. longispinosus 5.5 7.5 15.5 25.0 4.5 2.5 Saito & Mori 1981
A. longispinosus 6.7 9.0 19.0 29.0 1.9 1.5 Shih & Shieh 1979
A. longispinosus 6.2 7.2 12.2 31.2 3.5 4.0 Xin et al. 1984
A. mckenziei 9.9 11.9 40.9 2.1 Lababidi 1988
A. mesembrinus 6.0 9.0 13.0 39.0 1.8 2.1 Abou-Setta & Childers 1989
A. mesembrinus 6.0 8.0 28.0 2.0 Abou-Setta & Childers 1989
A. mesembrinus 6.0 9.0 46.0 1.7 Abou-Setta & Childers 1989
A. ovalis 8.0 8.5 21.0 25.5 1.0 1.6 Shih & Shu unpub!.
A. paraki 8.0 10.0 20.0 3.5 2.3 Saito & Mori 1981
P.longipes 8.2 9.2 33.2 4.3 Badii & McMurtry 1984
P. macropilis 6.8 7.8 13.0 2.8 2.9 Shih et a!. 1979
P. persimilis 8.1 9.1 21.1 43.1 3.0 3.7 Amano & Chant 1977
P. persimilis 5.0 7.0 24.0 5.0 Janssen & Bol unpub!.
P. persimilis 6.0 7.0 16.0 24.0 4.5 4.8 Janssen & Bol unpub!.
P. persimilis 6.0 7.0 15.0 29.0 5.0 4.2 Janssen & Bol unpub!.
P. persimilis 5.8 8.8 14.8 29.8 4.7 4.7 Lababidi 1988
P. persimilis 6.4 8.4 23.4 34.4 4.6 3.8 Takafuji & Chant 1976
P. soleiger 9.5 11.5 21.5 43.5 1.6 I.3 Kropczynska et a!. 19!!!!
00 Ph. macropilis 8.8 10.8 24.8 37.8 1.5 0.9 Kropczynska et al. 1988
\0
T. exhilaratus 8.4 9.4 26.4 41.4 2.0 2.0 Castagnoli & Liguori 1986a
T. exhilaratus 9.2 9.2 32.2 42.2 1.3 1.0 Castagnoli & Liguori 1986a
T. exhilaratus 9.0 10.0 14.0 44.0 1.6 1.9 Castagnoli et a!. 1989
T. fioridanus 11.0 13.0 35.0 39.0 2.0 I.7 Tanigoshi & McMurtry 1977
T. occidentalis 8.3 10.3 16.3 26.3 2.8 2.9 Pruszynski & Cone 1973
T. occidentalis 11.0 13.0 20.0 28.0 2.6 2.7 Tanigoshi et al. 1975
T. occidentalis 9.0 10.0 18.0 24.0 3.0 2.7 Tanigoshi et a!. 1975
T. occidentalis 7.9 9.9 16.9 39.9 2.4 2.4 Lababidi 1988
T. phialatus 12.5 15.5 20.5 57.5 I.7 2.3 Ferragut et a!. 1987
T. pyri 11.6 14.6 37.6 1.0 Kropczynska et a!. 1988
"A = Age at first reproduction

bT, and T2 = Age at the first and second peak of oviposition
'w = Age at the end of the reproductive period
d neT,) and n(T2) = Reproductive peaks (eggs/female/day).
Appendix 4.2. A summary of all data used for the review of life history characteristics of phytoseiids.
Oviposition Sex"
,
Species Mean Peak Fcc" Dev" rm Ratio Pred' References
A. aberrans 0.89 1.20 19.4 0.095 0.126 Kropczynska et al. 1988

A. andersoni 1.32 2.00 46.3 0.104 Amano & Chant 1977
A. anonymus 2.27 2.60 49.2 0.131 0.274 0.830 12.4 Van Dinh et al. 1988
A. bibens 2.84 57.1 Bloomers & van Arendonk 1979
A. bibens 2.15 3.72 64.1 0.143 0.326 0.830 13.4 Blommers 1976
A. bibens 3.10 3.80 49.8 0.168 0.795 16.8 Lababidi 1988
A. bibens 4.62 0.823 Schulten et al. 1978
A. brazilii 0.50 0.110 EI.Banhawy 1975
A. brazilii 0.60 0.087 EI. Banhawy 1975
A. californicus 2.61 41.0 0.702 10.1 Friese & Gilstrap 1982
A. chilenensis 3.10 43.3 0.151 0.287 16.2 Ma & Laing 1973
\Q
a A. citrifolius 2.10 2.33 49.7 0.145 0.793 De Moraes & McMurtry 1981
A. cucumeris 1.40 2.22 0.109 Dosse 1955
A. cucumeris 1.80 2.00 37.8 0.108 0.639 11.9 Lababidi 1988
A. degenerans 2.24 2.40 67.8 0.126 0.248 0.740 Takafuji & Chant 1976
A. deleoni 3.50 0.286 0.577 Saito & Mori 1981
A. fal/acis 3.50 55.0 0.227 Ball 1980
A. fal/acis 1.98 2.70 28.9 0.146 Boyne & Hain 1983
A. fallacis 2.50 2.50 31.4 0.152 Boyne & Hain 1983
A .fallacis 2.20 3.40 46.3 0.173 0.764 15.7 Lababidi 1988
A lal/acis 2.82 4.40 37.6 0.172 McClanahan 1968
A. fal/acis 3.20 53.2 0.192 10.6 Smith & Newsom 1970a,b
A. finlandicus 0.90 0.093 Kropczynska 1970
A ..{inlandicus 0.69 0.60 7.2 0.102 0.087 Kropczynska et al. 1988
A. finlandicus 1.60 0.620 Sabelis unpubl.
A. fustis 1.73 19.1 0.091 0.806 Ezulike & Odebiyi 1985
A. gossypi 1.20 34.3 0.068 Rasmy & EI.Banhawy 1975
A. idaeus 1.79 2.36 20.8 0.286 0.836 Janssen & Rook unpuh!.
A. idaeus 2.35 2.80 48.2 0.142 0.279 0.800 12.8 Van Dinh et a!. 1988
A. largoensis 1.75 1.80 20.6 0.114 Tanaka & Kashio 1977
A. limonicus 2.30 0.118 McMurtry & Scriven 1965
A. longispinosus 2.30 3.60 48.8 0.171 0.697 17.6 Lahahidi 1988
A. longispinosus 2.33 2.85 55.6 0.125 0.229 Lo & Ho 1979
A. longispinosus 3.70 3.80 74.6 0.200 0.410 0.785 Mallik & ChanaBassavanna 1983
A. longispinosus 4.50 0.333 0.630 Saito & Mori 1981
A. longispinosus 1.39 1.90 22.2 0.146 0.194 10.7 Shih & Shieh 1979
A. masiaka 1.85 0.115 Blommers 1974
A. mckenzie 2.00 2.10 43.4 0.101 0.625 9.8 Lahahidi 1988
A. mesembrinus 1.25 1.80 23.7 0.142 0.199 Ahou-Setta & Childers 1989
\0
...... A. ovalis 2.42 3.00 42.7 0.146 0.255 17.2 Shih & Shu unpuh!. data
A. ovalis 0.79 1.00 6.5 0.131 0.094 Shih & Shu unpuh!. data
A. paraki 3.50 0.245 0.672 Saito & Mori 1981
A. potentillae 2.00 0.111 Overmeer 1981
A. potentillae 2.00 0.188 Sahelis 1985
A. pseudolongispinosus 2.80 3.50 48.5 0.154 0.332 Xin et a!. 1984
A. soleiger 1.04 1.60 24.9 0.101 0.144 Kropczynska et a!. 1988
A. teke 1.90 36.0 0.154 0.800 Ochieng et a!. 1987
A. temperellus 1.20 50.2 0.096 Ball 1980
A. tetranychivorus 1.57 45.3 Gupta 1985
A. tetranychivorus 1.15 34.5 0.103 Krishnamoorty 1982
A. umbraticus 1.30 36.0 0.108 0.582 Knisley & Swift 1971
Continued
Appendix 4.2. Continued
Oviposition Sex d
,.
Species Mean Peak Fec' Dev b rm Ratio Pred' References
P. longipes 2.59 4.25 53.6 0.149 0.366 Badii & McMurtry 1984
P. macropilis 2.20 38.9 0.133 Ball 1980
P. macropilis 2.62 51.8 0.183 0.820 6.1 Prasad 1967
P. macropilis 1.90 2.80 48.3 0.128 0.270 0.714 9.5 Shih et al. 1979
P. persimilis 2.91 3.00 66.3 0.134 Amano & Chant 1977
P. persimilis 0.20 9.0 Ashihara et al. 1978
;S P. persimilis 2.69 60.4 0.148 0.374 Badii & McMurtry 1984
P. persimilis 3.80 76.5 0.834 25.0 Friese & Gilstrap 1982
P. persimilis 3.79 60.6 Gerlach & Sengonca 1985
P. persimilis 4.10 5.00 0.162 Hamamura et al. 1976
P. persimilis 4.56 5.02 40.7 0.181 0.410 0.820 Janssen & Bol unpubl.
P. persimiiis 3.50 4.70 74.8 0.197 0.813 24.6 Lababidi 1988
P. persimilis 3.78 5.20 53.5 0.200 McClanahan 1968
P. persimilis 4.00 0.910 Nagelkerke unpubl.
P. persimiiis 4.30 0.800 Sabelis unpubl.
P. persimilis 3.00 0.155 Sabelis 1981
P. persimilis 4.01 0.876 Schulten et al. 1978
P. persimilis 3.69 4.60 79.5 0.146 0.317 0.820 Takafuji & Chant 1976
P. piumifer 1.00 22.3 0.115 Rasmy & EI. Banhawy 1975
Ph. hawaiiensis 0.87 11.9 Sanderson & McMurtry 1984
Ph. hawaiiensis 0.82 0.086 Sanderson & McMurtry 1984
Ph. hawaiiensis 0.68 31.4 0.068 Sanderson & McMurtry 1984
Ph. macropilis 0.85 1.50 17.1 0.112 0.113 Kropczynska et al. 1988
Ph. plumifer 2.10 4.00 44.8 0.165 Zaher et al. 1969
T. annectens 1.30 28.0 0.095 Badii et al. 1990
T. annectens 1.06 9.5 Badii et al. 1990
T. athiasae 1.10 26.4 0.099 Hessein 1977
T. bambusae 1.70 28.5 0.112 0.164 0.610 8.4 Saito 1990
T. exhilaratus 1.33 1.63 31.7 0.178 0.675 Castagnoli et al. 1989
T. exhilaratus 1.21 1.25 30.0 0.093 Castagno Ii & Liguori 1986a
T. exhilaratus 1.61 2.00 34.4 0.100 Castagnoli & Liguoir 1986a
T. exhilaratus 0.82 22.9 0.100 0.122 0.650 Castagnoli & Liguori 1986b
T. fioridanus 1.97 2.04 41.2 0.086 0.159 0.643 12.2 Tanigoshi & McMurtry 1977
T. longipilis 3.10 28.1 0.182 Ball 1980
T. longipilus 1.90 46.0 Burrell & McCormick 1964
T. longipilus 1.00 26.0 Burrell & McCormick 1964
~ T. longipilus 1.20 20.0 Burrell & McCormick 1964
T. occidentalis 1.84 34.5 0.123 0.260 Badii & McMurtry 1984
T. occidentalis 1.00 8.4 Badii et al. 1990
T. occidentalis 2.88 43.8 0.244 0.677 Bruce-Oliver & Hoy 1990
T. occidentalis 2.40 12.0 Bruce-Oliver & Hoy 1990
T. occidentalis 2.66 33.6 0.207 0.667 Bruce-Oliver & Hoy 1990
T. occidentalis 2.30 36.8 0.213 Croft 1972
T. occidentalis 1.23 9.4 0.685 14.4 Friese & Gilstrap 1982
T. occidentalis 2.30 25.6 Hoy 1984
T. occidentalis 1.90 2.44 36.3 0.147 0.603 15.8 Lababidi 1988
T. occidentalis 2.30 9.8 Pruszynski & Cone 1973
Continued
Appendix 4.2. Continued
Oviposition Sex"
Species Mean Peak Fec' Dev b rm Ratio Pred' References
T. occidentalis 2.45 2.80 35.2 0.137 Pruszynski & Cone 1973

T. occidentalis 1.10 33.7 0.131 Lee & Davis 1968
T. phialatus 1.10 1.70 44.6 0.094 0.144 0.630 Ferragut et al. 1987
T. pini 0.95 17.7 0.079 1.9 Charlet & McMurtry 1977
T. porresi 0.59 7.9 Badii et al. 1990
T. porresi 1.28 27.6 0.087 Badii et al. 1990
~ T. pyri 0.43 1.00 10.2 0.081 0.089 Kropczynska et al. 1988
T. pyri 0.68 23.0 0.067 Herbert 1961
T. pyri 0.63 38.7 0.D78 0.076 Ovenneer 1981
T. rickeri 1.90 27.5 0.106 McMurtry & Scriven 1964
T. .\'essor 0.79 0.101 Sciarappa & Swift 1977
T. validus 1.\0 2.8 Charlet & McMurtry 1977
, Fecundity
h Developmental rate
,. Intrinsic rate of increase
d Proportion of daughters
, Predation rate on prey eggs
Appendix 4.3. Derivation of equations:

The classic Lotka or Euler equation for estimating the intrinsic rate of increase. r m' from life table
data is given by:
W
2: exp (-r~) l,n,s, = I
x=A
where x = age, A = age at first oviposition, W = age at last oviposition, i, = probability of survival
from age 0 to age x, no = ovipositional rate of a female of age x, and Sx = the proportion of daughters
in the offspring of a female of age x. This formula expresses that the age-specific net rate of
reproduction (/xnxsx) is weighted by a negative exponential (exp (- r mX)) and that r m should be chosen
so as to make the sum of the weighted, age-specific, net rates of reproduction sum to unity.
This formula reduces to more transparent forms for the following simplified reproduction schedules
(with T representing the age at peak oviposition), as visualized in Figure 4.5:
(I) Rm exp (-rmA)r m-' = I
for the Methusalem schedule (R(x < A) = 0, R(A) = R(x > A) = R (n)'
(2) Rmlexp(-rmA) - exp(-rmW)]rm-' = I
for the rectangular schedule (R(x < A) = 0, R(A) = R(W) = R(n),
(3) (Rm{(T-Ar' [exp (-r mAl - exp (rmn + (W - n-'
[exp (-rmW) - exp (-rmnn rm -, = I,
for the triangular schedule (R (x < A) = R(W) = 0, R(n > 0, R(x > W) = 0; see Lewontin,
1965),
(4) Rm {{(T, - A)-' [exp (-rmA) - exp (-rmT])] + (W - T,)-' [exp (-rmW) - exp (-rmT,)]}
r m-' + [exp (-rmT,) - exp (-RmT,)] rm-'} = I;
for the trapezoid schedule (R(x < A) = 0, R (T,) = R(,) > 0, R(x > W) = 0; see Figure 4.IA).
Note that each of the equations can be written in the form:
rm = Rmf(rm. A, T, ..... )
Hence, it is possible to graphically determine the R(n values for which the rm horizontal (the left
hand side of the equation) intersects the curve of R(nftrm, A, T, . .. ) against R(n (the right hand
side of the equation). An example is given in Figure 4.4 for the case of a Methusalem schedule,
whereNm, A, . . . ) = exp (-rmA).
Literature Reviewed in Appendices 4.1 and 4.2
Abou-Setta, M. M. and C. C. Childers. 1989. Biology of Euseius mesembrinus (Acari:

Phytoseiidae): Life tables and feeding behaviour on tetranychid mites on citrus. Environ.
Entomol. 18:665-669.
Amano, H. and D. A. Chant. 1977. Life history and reproduction of two species of
predaceous mites, Phytoseiulus persimilis Athias-Henriot and Amblyseius andersoni
(Chant) (Acarina: Phytoseiidae). Can. J. Zool. 55:1978-1983.
Badii, M. H. and J. A. McMurtry. 1984. Life history of and life table parameters for
Phytoseiulus longpipes with comparative studies on P. persimilis and Typhlodromus
occidentalis (Acari: Phytoseiidae). Acarologia 25:111-123.
Badii, M. H. and J. A. McMurtry. 1984. Life history of and life table parameters for
Phytoseiulus longpipes with comparative studies on P. persimilis and Typhlodromus
occidentalis (Acari: Phytoseiidae). Acarologia 25:111-123.
Ball, J. C. 1980. Development, fecundity, and prey consumption of four species of
predaceous mites (Phytoseiidae) at two constant temperatures. Environ. Entomol.

9:298-303.
Blommers, L. 1974. Preliminary studies on two predators (Acarina: Phytoseiidae) of the
spider mite Tetranychus neocaledonicus Andre (Acarina: Tetranychidae). Z. Angew.
Entomol. 75:315-321.
Bloomers, L. 1976. Capacities for increase and predation in Amblyseius bibens (Acarina:
Phytoseiidae). Z. Angew. Entomol. 81 :225-244.
Bloomers, L. and R. C. M. van Arendonk. 1979. The profit of senescence in phytoseiid
mites. Oecologia 44:87-90.
Boyne, J. V. and F. P. Hain. 1983. Responses of Neoseiulus jaliacis (Acarina: Phytoseii-
dae) to different prey densities of Oligonychus ununguis (Acarina: Tetranychidae) and
to different relative humidities. Can. Entomol. 115: 1607-1614.
Bruce-Oliver, S. J. and M. A. Hoy. 1990. Effect of prey stage on life-table attributes of
a genetically manipulated strain of Metaseiulus occidentalis (Acari: Phytoseiidae). Exp.
Appl. Acarol. 9:201-207.
Burrell, R. W. and W. J. McCormick. 1964. Typhlodromus and Amblyseius (Acarina:
Phytoseiidae) as predators on orchard mites. Ann. Entomol. Soc. Am. 57:483-487.
Castagnoli, M. and M. Liguori. 1986a. Tempi di sviluppo e ovideposizione di Typhlodro-
mus exhilaratus Ragusa (Acarina: Phytoseiidae) allevato con vari tipi di cibo. Redia
69:361-368.
Castagnoli, M. and M. Liguori. 1986b. Laboratory rearing and construction of a life table
for Typhlodromus exhileratus Ragusa (Acarina: Phytoseiidae). Redia 69:591-596.
Castagno1i, M., F. Amato and M. Monagheddu. 1989. Osservazioni e parametri demo-
grafici di Eotetranychus carpini (Oudemans) (Acarina: Tetranychidae) e del suo preda-
tore Typhlodromus exhileratus Ragusa (Acarina: Phytoseiidae) in condizioni di laborato-
rio. Redia 72:545-557.
Charlet, L. D. and J. A. McMurtry. 1977. Systematics and bionomics of predaceous and
phytophagous mites associated with pine foliage in California. Hilgardia 45: 173-236.
Croft. B. A. 1972. Prey stage distribution, a factor affecting the numerical response of
Typhlodromus occidentalis to Tetranychus mcdanieli and Tetranychus pacificus. Great
Basin Nat. 32:61-75.
De Moraes, G. J. and J. A. McMurtry. 1981. Biology of Amblyseius citrifolius (Denmark
and Muma) (Acarina: Phytoseiidae). Hilgardia 49:1-29.
Dosse, G. 1955. Aus der Biologie der Raubmilbe Typhlodromus cucumeris Oud. (Acar.,
Phytoseiidae). Z. Pjianzenkr. Pjianzenschutz 62:593-598.
EI-Banhawy, E. M. 1975. Biology and feeding behaviour ofthe predatory mite Amblyseius
brazilli (Mesostigmata: Phytoseiidae). Entomophaga 20:353-360.
Ezulike, T. O. and J. A. Odebiyi. 1985. Life history of Amblyseiusjustis (Pritchard and
Baker), an indigenous predator of the cassava red mite, Oligonychus gossipii (Zacher)
in South Western Nigeria. Insect Sci. Appl. 6:193-197.
Ferragut, F., F. Garcia-Mari, J. Costa-Comelles and R. Laborda. 1987. Influence of food
and temperature on development and oviposition of Euseius stipulatus and Typhlodro-

mus phialatus (Acari: Phytoseiidae). Exp. Appl. Acarol. 3:317-330.
Friese, D. D. and F. E. Gilstrap. 1982. Influence of prey availability on reproduction and
prey consumption of Phytoseiulus persimilis, Amblyseius californicus and Metaseiulus
occidentalis (Acarina: Phytoseiidae). Int. J. Acarol. 8:85-89.
Gerlach, S. and <;. Sengonca. 1985. Comparative studies on the effectiveness of the
predatory mite Phytoseiulus persimilis Athias-Henriot, and the predatory thrips, Sco-
loth rips longicornis Priesner. Z. Pjlanzenkr. Pjlanzenschutz 92:138-146.
Gupta, S. K. 1985. Handbook Plant Mites of India. Calcutta: Zoological Survey of India.
Hamamura, T., N. Shinkaji and W. Ashihara. 1976. The relationship between temperature
and developmental period, and oviposition of Phytoseiulus persimilis Athias-Henriot
(Acarina: Phytoseiidae). Bull. Fruit Tree Res. Stn., Series E 1:117-125.
Herbert, H. J. 1961. Influence of various numbers of prey on rate of development,
oviposition, and longevity of Typhlodromus pyri Scheuten (Acarina: Phytoseiidae) in
the laboratory. Can. Entomol. 43:380-384.
Hessein, N. A. 1977. Life history of the predatory mite Typhlodromus athiasae Porath
and Swirski (Acarina: Phytoseiidae). Libyan J. Agric. 6:45-48.
Hoy, M. A. 1984. Genetic improvement of a biological control agent: Multiple pesticide
resistance and nondiapause in M etaseiulus occidentalis (Nesbitt) (Phytoseiidae). Acarol-
ogy 6:673-679.
Knisley, C. B. and F. C. Swift. 1971. Biological studies of Amblyseius umbraticus
(Acarina: Phytoseiidae). Ann. Entomol. Soc. Am. 64:813-822.
Krishnamoorty, A. 1982. Effect of temperature on the development, survival and fecundity
of the predatory mite, Amblyseius tetranychivorus (Gupta) (Acarina: Phytoseiidae).
Entomon 7:447-450.
Kropczynska, D. 1970. Biologia I ekologia drapieznego roztocza Typhlodromus finlandi-
cus (Oud.) (Acarina: Phytoseiidae). Zesz. Probl. Post. Nauk. Roln. 109: 11-42.
Kropczynska, D., M. van de Vrie and A. Tomczyk. 1988. Bionomics of Eotetranychus
tiliarium and its phytoseiid predators. Exp. Appl. Acarol. 5:65-82.
Lababidi, M. S. 1988. Biologische Bekampfungsmoglichkeiten der Baumwollspinnmilbe
Tetranychus cinnabarinus (Biosduval) (Acari: Tetranychidae). Ph.D. thesis, Institut fUr
Pflanzenkrankheiten der Rheinischen Friedrich-Wilhelms-Universitat Bonn.
Lee, M. S. and D. W. Davis. 1968. Life history and behavior of the predatory mite
Typhlodromus occidentalis in Utah. Ann. Entomol. Soc. Am. 61:251-255.
Lo, K. C. and C. C. Ho. 1979. Influence of temperature on life history, predation and
population parameters of A. longispinosus (Acarina: Phytoseiidae). J. Agric. Res. China
28:237-250.
Ma, W. and J. E. Laing. 1973. Biology, potential for increase and prey consumption of
Amblyseius chilenensis (Dosse) (Acarina: Phytoseiidae). Entomophaga 18:47-60.
Mallik, B. and G. P. ChannaBasavanna. 1983. Life history and life tables of Tetranychus
ludeni and its predator Amblyseius longispinosus (Acari: Tetranychidae: Phytoseiidae).
Indian J. Acarol. 8:1-12.
98 I M. W. Sabelis aad A. Janssen
McClanahan, R. J. 1968. Influence of temperature of the reproductive potential of two

mite predators of the two-spotted spider mite. Can. Entomol. 100:549-556.
McMurtry, 1. A. and G. T. Scriven. 1964. Biology of the predaceous mite Typhlodromus
rickeri (Acarina: Phytoseiidae). Ann. Entomol. Soc. Am. 57:362-267.
McMurtry, 1. A. and G. T. Scriven. 1965. Life-history studies of Amblyseisu limonicus
with comparative observations on Amblyseius hibisci (Acarina: Phytoseiidae). Ann.
Ochieng, R. S.,m G. W. 0100 and E. O. Amboga. 1987. An artificial diet for rearing the
phytoseiid mite, Amblyseius teke Pritchard and Baker. Exp. Appl. Acarol. 3:169-173.
Overmeer, W. P. J. 1981. Notes on breeding phytoseiid mites from orchards (Acarina:
Phytoseiidae) in the laboratory. Med. Fac. Landbouww. Rijksuniv. Genet. 46:503-509.
Prasad, V. 1967. Biology of the predatory mite Phytoseiulus macropilis in Hawaii (Aca-
rina: Phytoseiidae). Ann. Entomol. Soc. Am. 60:905-908.
Pruszynski, S. and W. W. Cone. 1973. Biological observations of Typhlodromus occiden-
talis (Acarina: Phytoseiidae) on hops. Ann. Entomol. Soc. Am. 66:47-51.
Rasmy, A. H. and E. M. EI-Banhawy. 1975. Biology and predatory efficiency of two
phytoseiid mites as affected by long-term pollen feeding. Entomophaga 20:93-95.
Sabelis, M. W. 1981. Biological control of two-spotted spider mites using phytoseiid
predators, Part I. Wageningen: Pudoc.
Sabelis, M. W. 1985. Capacity of population increase. In: Spider Mites, Their Biology,
Natural Enemies and Control, Vol. IB, edited by W. Helle and M. W. Sabelis, 35-
40. Amsterdam: Elsevier.
Saito, Y. 1990. Life-history and feeding habit of Typhlodromus bambusae, a specific
predator of Schizotetranychus celarius (Acari: Phytoseiidae, Tetranychidae). Exp. Appl.
Acarol. 10:45-51.
Saito, Y. and H. Mori. 1981. Parameters related to potential rate of population increase in
three predacious mites in Japan (Acarina: Phytoseiidae). Appl. Entomol. Zool. 16:45-47.
Sanderson, J. P. and 1. A. McMurtry. 1984. Life-history studies of the predaceous mite
Phytoseius hawaiiensis. Entomol. Exp. Appl. 35:227-234.
Schulten, G. G. M., R. C. M. van Arendonk, V. M. Russell and F. A. Roorda. 1978.
Copulation, egg production and sex-ratio in Phytoseiulus persimilis and Amblyseius
bibens (Acarina: Phytoseiidae). Entomol. Exp. Appl. 24:145-153.
Sciarappa, W. J. and F. C. Swift. 1977. Biological studies of Typhlodromus sessor
(Acarina: Phytoseiidae). Ann. Entomol. Soc. Am. 70:283-288.
Van Dinh, N., A. Janssen and M. W. Sabelis. 1988. Reproductive success of Amblyseius
idaeus and A. anonymus on a diet of twos potted spider mites. Exp. Appl. Acarol. 4:41-
51.
Xin, 1., L. Liang and L. Ke. 1984. Biology and utilization of Amblyseius pseudolongi-
spinosus (Acarina: Phytoseiidae) in China. In: Acarology VI, Vol. 2, edited by D. A.
Griffiths and C. E. Bowman, 693-698. Chichester: Ellis Horwood Limited.
Zaher, M. A., A. K. Wafa and K. K. Shehata. 1969. Life history of the predatory mite
Phytoseius plumifer and the effect of nutrition on its biology (Acarina: Phytoseiidae).
Entomol. Exp. Appl. 12:383-388.
5
Evolutionary Aspects of Oribatid Mite
Life Histories and Consequences for the Origin
of the Astigmata
Roy A. Norton
CONTENTS
1. INTRODUCTION
2. DIVERSITY AND PHYLOGENY OF ORIBATID MITES
3. REVIEW OF ORIBATID MITE LIFE-HISTORY TRAITS
3. 1 Life Cycle and Parity
3.2 Fertilization and Thelytoky
3.3 Fecundity
3.4 Developmental Rates
3.5 Survivorship, Adult Longevity and Sources of Mortality
3.6 Voltinism and Generational Synchrony
3.7 Net Reproductive Rates
3.8 Dispersal
3.9 Summary of Life Histories in Temperate Soil
4. LIFE HISTORIES IN APOTYPIC HABITATS
4.1 Species in Cold Environments
4.2 Species in Hot Deserts
4.3 Freshwater Species
4.4 Tropical Species
5. SYNTHESIS OF IDEAS ON LIFE-HISTORY EVOLUTION IN
ORIBA TID MITES
5.1 Three Views of "K-attributes"
5.2 Constraints in Oribatid Mite Life-Histories
6. LIFE-HISTORY ASPECTS OF THE ORIGIN OF THE ASTIGMATA
7. PROSPECTUS FOR FURTHER RESEARCH
8. CONCLUSIONS
1. Introduction
With densities of several hundred thousand individuals per square meter, oribatid
mites are often the most diverse and numerically dominant arthropods in organic
99
JOO / R. A. Norton
layers of temperate forest soils, where they feed primarily on decomposing higher
plant material and on fungi (Harding and Stuttard 1974, Wallwork 1983, Norton
1985). This chapter represents a first attempt at developing a phylogenetic context
for the surprisingly large volume of literature that deals with various aspects of
oribatid life histories.
A popular approach to life-history studies is to seek an adaptive explanation
for any trait that seems important to an organism in its present ecological setting.
Sets of such traits are often considered coadapted to form evolutionary "strate-
gies." But claims of life-history adaptation often disregard phylogenetic relation-
ships (Wanntorp et al. 1990), thus ignoring the simpler possibility that a trait is
ancestral, and that its prior possession allowed the species to invade its current
environment. Much of the literature on oribatid mite life histories seems to suffer
from such a one-sided viewpoint, and making this fact more apparent is my
primary goal.
Has life-history adaptation played a significant role in oribatid mite diversifica-
tion? I will address this question simply by seeking patterns in life-history traits.
If patterns seem predominantly taxonomic, e.g. if a higher taxon is ecologically
diverse but shows constancy in traits, then historical constraints are probably
operating. If instead, traits seem correlated with ecological parameters, then
hypotheses of life-history adaptation are reasonable. My analysis is incomplete
and often unsatisfying, due to our poor knowledge of oribatid mite phylogeny,
fragmentary life-history data, and lack of information that would allow us to
distinguish heritable variation from phenotypic plasticity. Demographic aspects
of life history will be stressed, but aspects of life cycle and reproductive biology
are also considered. I do not directly refer to many laboratory studies concerning
development time; these can be obtained from cited sources (especially reviews
by Lebrun and Luxton). No attempt is made to evaluate the various methods used
to investigate oribatid mite demography, though some assumptions are critiqued
where relevant. These include life-table analyses (Mitchell 1977a, Schatz 1983,
Fernandez and Athias-Binche 1986), deterministic models (Stamou 1987) and
other mathematical treatments (Cancela da Fonseca 1980).
Polarization of traits, i.e. their characterization as ancestral (plesiotypic) or
derived (apotypic), is necessary in any phylogenetic discussion, and some traits
relating to life cycle and reproductive biology can be easily addressed in this
manner. For example, fertilization via spermatophores and the oviposition of
eggs appear to be plesiotypic within the order Acariformes. But the various
demographic traits of individuals and populations are less easily polarized, and
the following approach is taken.
Most available data relate to species from temperate forest soils (a habitat
which I consider to be ancient and relatively plesiotypic, if not original) and after
a general review, the traits of such species will be summarized. Then I examine
oribatid mites living in more extreme habitats or in nonsoil microhabitats (situa-
tions that can be considered apotypic) and look for apparent adaptations. The
Evolutionary Aspects of Oribatid Mite Life-Histories / 101
approach can be criticized for overgeneralization and lack of rigor, neither of

which can be avoided at present. A secondary objective is to examine the deriva-
tion of the Astigmata from a life-history perspective. In general, the traits exhib-
ited by this group differ greatly from those of oribatid mites, and a logical
transition is not obvious.
2. Diversity and Phylogeny of Oribatid Mites
The mite suborder Oribatida (= Cryptostigmata, Oribatei) includes about 7,O()()

nominal species. Oribatid mites have existed at least since the Devonian Period
(Norton et al. 1988a), and even some rather derived genera are known from the
Jurassic (Krivolutsky and Druk 1986). An impressive morphological diversity
exists in some groups (e.g. the Enarthronota, see Norton 1984), and to some
extent they utilize non-soil microhabitats (Trave 1963). Yet compared to other
major taxa, oribatid mites seem to have been highly conservative in most aspects
of their biology. This is often attributed to a paucity of the interspecific relation-
ships with plants and animals that characterize radiations in other mite groups
(Krantz and Lindquist 1979, OConnor 1982, Norton 1985).
In part, the conservatism of oribatid mites is illusory in that the Oribatida does
not represent a natural, historical group. In its usual sense it is clearly paraphyletic,
having given rise to the Astigmata, a diverse group in which interspecific relation-
ships are key (OConnor 1982, 1984). Still, the species richness of oribatid mites
is of the same order of magnitude as that of the Astigmata, Prostigmata or
Mesostigmata (Parker 1982) and the apparent biological conservatism has made
their taxonomic diversity somewhat enigmatic (Anderson 1975a, Norton 1985).
Partial explanations for this relate to micro-distribution (Aoki 1967, Hammer
1972, Fujikawa 1974, Anderson 1978a) and feeding specificity (see Harding and
Stuttard 1974).
As with any biological attribute, meaningful conclusions about life-history
evolution must be rooted in an assessment of phylogeny. A few groups have been
analyzed, but there are no published hypotheses relating monophyletic higher
taxa of the Oribatida using the rigor of cladistic methodology. Without offering
supporting evidence, my view of the relationships of the six commonly recognized
but unranked "taxa" of oribatid mites (Grandjean 1969, Marshall et al. 1987) and
the Astigmata is shown in Fig. 5.1. This level of resolution is of little value
here, but it does provide a framework for discussion. What can be called the
"glandulate" oribatid mites (having paired opisthosomal glands) is a monophyletic
group, but the relationships of its outgroups, Enarthronota and Palaeosomata, are
as yet undefined (see Grandjean 1969). The Parhyposomata seems monophyletic,
but the Mixonomata is paraphyletic, having given rise to the Desmonomata
(= Nothroidea). The latter is doubly paraphyletic, having produced both the
Brachypylina ("higher" oribatid mites, = Circumdehiscentiae) and the Astigmata.
102 / R. A. Norton
6
8
NffiA
MATA
!, Opisthosomal
I I ~and
,
:
I
I
I
I
I
Figure 5.1. Schematic relationships of major oribatid mites groups and the Astigmata
(see text for explanation).
3. Review of Oribatid Mite Life-History Traits
3.1 Life Cycle and Parity
Oribatid mites retain the ancestral acariform life cycle of six postembryonic instars
(prelarva, larva, protonymph, deutonymph, tritonymph, and adult), though in
the aberrant and highly regressive enarthronote family Pediculochelidae the pres-
ence of a tritonymph has not been proven. The prelarva is inactive in all known
oribatid mites. It is a calyptostase that exhibits various states of regression, and
it usually occurs totally or partially within the egg membrane, so that the larva
appears to hatch from the egg. Among the remaining instars there are no known
cases of calyptostasis; where studied, the larva, nymphs, and adult are active and
feed normally.
Oribatid mites vary in the timing of parity relative to offspring development.
Most species lay eggs (oviposit) in which case embryos are released at an
early developmental stage, but in some species eggs are retained throughout
embryogenesis, which ends with the formation of the prelarva. Parity may occur
at this point (prelarviposition), or the female may release progeny only after the
larval ins tar is reached (larviposition). Delayed parity has been called "uterine
development" (Lange 1960), but the term "egg retention" will be used here. The
taxonomic distribution of egg retention may be underestimated, since eggs can
be seen in females with clutches not yet ready for deposition.
Some taxonomic correlates are apparent (Lange 1960, Sitnikova 1960,
Grandjean 1962, Lions 1973, Trave 1976), though a paucity of information
makes generalization tenuous. Egg retention is especially common in Ptyctima,
with prelarviposition evidently fixed in one superfamily, Phthiracaroidea. In the
other superfamily, Euphthiracaroidea, all three parity modes are represented,
but internal pattern may exist. For example, members of the genus Oribotritia
(Oribotritiidae) seem to consistently prelarviposit, while oviposition is common
in the family Euphthiracaridae. Prelarviposition is common in the Desmonomata,
especially within the family Camisiidae. It is also widespread in Ameronothridae
(including Podacaridae of authors), and further retention (larviposition) is charac-
teristic of Ameronothrus, species of which are found in marine littoral regions
and estuaries (Luxton 1964, Schulte and Weigmann 1977). Larviposition seems
to be the rule in Trimalaconothrus (or at least the subgenus Tyrphonothrus),
members of which inhabit fresh water. However, egg retention often has a
mosaic distribution among taxa. Larviposition is known from two species of
Maerkelotritia (Walker 1965, pers. observ.), but a third, M. sellnicki, lays eggs.
Eggs of the latter develop a thick chorion that is absent from those of larvipositing
species. Various species of Nothrus exhibit all three parity modes, and brachypy-
line genera such as Damaeus and Liodes may oviposit or prelarviposit, depending
on species.
Many of the higher taxa that exhibit egg retention share other biological
attributes. For example, all Ptyctima immatures are endophagous, burrowing in
decaying wood or other plant tissues; is there an adaptive rationale? If moisture
level is positively correlated with successful substrate penetration by larvae, a
female has a better chance of selecting an appropriate substrate if hatching is
immediate or only briefly delayed. From another viewpoint, prelarviposition may
reduce the time during which eggs are exposed to predators, as Lebrun et. al.
(1991) suggested for Steganacarus magnus. Yet many burrowing oribatid mites
living similar life styles oviposit, such as Adoristes ovatus (Lions and Gourbiere
1988), Carabodes willmanni (Bellido 1979), Cepheus pegazzanoae (Bernini and
Nannelli 1982), and Xenillus punctatus (pers. observ.).
Ameronothrus and Trimalaconothrus are aquatic or semi aquatic genera; is
their larviposition somehow ecologically adaptive? Luxton (1967) suggested that
larviposition by A. schneideri precludes eggs being washed away by tidal action.
The fact that species of Trimalaconothrus are commonly, but not exclusively,
found among submerged vegetation in rapidly moving streams and rivers is
consistent with Luxton's hypothesis, as is the fact that Hydrozetes and Limnozetes
species (all of which oviposit) are characteristic of stationary waters. In contrast,
104 / R. A. Norton
Mucronothrus nasalis oviposits yet commonly lives in lotic environments (Norton

et al. 1988b), while larviposition is typical of those Astigmata living in water-
filled treeholes (Fashing 1977).
While neither aquatic habitation nor flow rate correlate perfectly with larviposi-
tion, all oribatid species that consistently larviposit are aquatic, suggesting a need
for an adaptive explanation. This pattern extends to the genus Nothrus, in which
an undescribed species inhabiting wet sphagnum bogs in the northeastern United
States is the only known fully larviparous member of the genus (unpublished
data). There are conflicting reports concerning N. palustris, a species commonly
associated with wet meadows. Akimov and Yastrebstov (1987) found fully devel-
oped larvae in females from the USSR, while it seems to be prelarviparous in
Europe and the United States (Lebrun 1970a, pers. observ.). Grishina (1991)
suggested, from field data, that the parity mode of N. palustris varies with season
in the USSR, with "oviposition" (probably actually prelarvaposition) in spring
and "viviparity" (larviposition) in summer, but this remains to be proven.
There is a single reliable record of mixed-parity mode in oribatid mites, and
this seems unrelated to the presence of free water. Haq et al. (1991) found
Scheloribates jijiensis from pasture soil in India to mostly oviposit, but some
larvipositing females were noted in both cultures and field samples. Whether its
parity mode is environmentally or genetically controlled is unstudied.
A thorough survey of the distribution of egg retention may clarify these trends
and elucidate others. For example, allometric scaling may playa role in egg
retention. Among arboreal species, those which prelarviposit (Camisia spp. and
some, but not all Liodes species) are generally larger than those for which there
are no records of egg retention (e.g. the genus Scapheremaeus, the family
Oripodidae). Also, prelarviposition is known from the larger-sized species of
Nothrus (N. palustris, Lebrun 1970a) and Damaeus (D. onustus, Grandjean
1954), but apparently not from smaller species.
A seemingly related phenomenon, in which living larvae are regularly found
in the dead and hollow bodies of female oribatid mites of terrestrial species, was
considered by some early authors to be a special case of egg retention referred to
as "aparity." In effect, it was viewed as a form of semelparity in which progeny
feed on the dead mother's body and emerge through a body aperture. In small
mites such as Limnozetes sphagni, where only one or two eggs are carried at a
time, Willmann (1933) suggested that earlier clutches may be laid in the form of
eggs, with aparity restricted to the last clutch. Jacot (1933) believed that aparity
was necessary if egg diameter was larger than that of the genital aperture.
However, Grandjean (1956a) noted that the elasticity of egg membranes allows
oviposition to occur even through a small opening, and discounted aparity as a
normal reproductive process. Rather, if mature eggs ar; not deposited prior to
the mother's death they may (by default) complete development (i.e. to hatching
of the larva) inside her body. Arlian and Woolley's (1970) observation of a dead
female Liacarus cidarus that contained 12 larvae plus other shriveled eggs is
consistent with this explanation. I have observed larvae in dead adults in a variety
of Brachypylina species, but no members of earlier-derivative taxa. The same
phenomenon occurs in astigmatic mites (e.g. Fain and Herrin 1978, Rodriguez
and Stepien 1973), where such larvae have been noted to die without emerging
from the mother's body.
3.2 Fertilization and Thelytoky
With few known or suspected exceptions, fertilization is indirect in oribatid mites.

Males produce free-standing spermatophores and have no direct association with
females, though local female activity may noticeably increase spermatophore
deposition rates (Pauly 1956, Shereef 1972, Haq and Adolph 1981). Only in
Collohmannia is fertilization clearly direct, though all details of the process are
not known. Males of C. gigantea have a well-defined courtship behavior during
which nuptial food is produced to entice cooperation of a female (Schuster
1962). I observed similar behavior in an undescribed species from West Virginia;
sperrnatophores were not produced, and fertilization may have occurred by direct
contact of the long genitalia. Sexual dimorphism or behavioral peculiarities
suggest the presence of courtship rituals, or at least close association of mates,
in several other groups (e.g. Grandjean 1956b). Male dimorphism can include
modified tarsal setae that may have courtship functions, as in Hydrozetes and
Montgaillardia (Grandjean 1948, 1961). Notogastral porose areas are known to
be associated with glands (Woodring and Cook 1962a), and the hypertrophied
porose areas in males of such taxa as Mochloribatula and Zachvatkinibates
maritimus (Norton 1983, Behan-Pelletier 1988) may be involved in sexual be-
havior.
Many oribatid mites dispense with fertilization altogether and exhibit thelytoky,
the parthenogenetic production of females. Thelytoky is commonly considered
adaptive, since the effective reproductive rate of a thelytokous female is theoreti-
cally twice that of a sexual counterpart. This may be quite significant in a group
with generally low fecundity, such as oribatid mites. The colonization advantage
is also much discussed, since any offspring can establish a population, regardless
of the ontogenetic stage at which it disperses. Based on field sex-ratio evidence
(Grandjean 1941, Luxton 1981a, Norton et al. 1988c, Palmer and Norton 1991)
and laboratory proofs (Taberly 1987, Palmer and Norton 1990 and included
references), thelytoky is common in oribatid mites. Nearly 10% of known oribatid
species may be thelytokous, a figure that is one or two orders of magnitude above
the estimates of Bell (1982, 1% of known insects) or White (1978, 0.1 % of
animals).
As discussed elsewhere (Norton and Palmer 1991), most thelytokous oribatid
mites are in families without sexual species. Examples include the moderate to
large families Lohmanniidae, Brachychthoniidae, Nanhermanniidae, Camisiidae,
Malaconothridae and Trhypochthoniidae, as well as many species-poor families
106 / R. A. Norton
included in the Parhyposomata and Enarthronota. Clearly thelytoky can be plesio-

typic, a reproductive mode of long historical standing, rather than always being
a recent adaptation to the current lifestyle of a particular species. For example,
it would be incorrect to consider thelytoky in Mucronothrus nasalis as an adapta-
tion to life in cold oligotrophic streams and deep lakes, since all species in its
family (Trhypochthoniidae) are thelytokous, regardless of their habitat. There is
a strong probability that in such groups speciation and radiation occurred in the
absence of sexual reproduction, and none of the standard biological correlates of
thelytoky seem to obtain (Norton and Palmer 1991).
In contrast, thelytoky may be a recently evolved and adaptive life-history trait
when we see it in some members of a genus but not in others, i.e. when its
taxonomic distribution conforms to theoretical predictions of a sporadic, but non-
random, distribution (Bell 1982). Among the early-derivative (non-Brachypylina)
groups such a taxonomic distribution is rare. Examples include two genera of the
Euphthiracaridae, Rhysotritia and Microtritia; common Holarctic or Pale arctic
species are thelytokous, but each genus is represented by sexual species in
California (Walker 1965). Also, Epilohmannia (Epilohmanniidae) contains both
sexual and thelytokous species apparently throughout its range (Wallwork 1962,
pers. observ.).
Among the Brachypylina the taxonomic distribution of thelytoky conforms to
theoretical predictions by being taxonomically scattered. Wholly thelytokous
genera are rare, with exceptions being the aquatic or semiaquatic genus Limno-
zetes (Behan-Pelletier 1989) and the cosmopolitan genus Tectocepheus. Norton
and Palmer (1991) noted that the ecological distribution of thelytokous Brachypy-
lina agrees with standard interpretations of the adaptive value of thelytoky. For
example, they are commonly early colonizers in newly created habitats, such as
bulldozed soil (Beckman 1988) and fresh volcanic substrates (Ryabinin and
Pan'kov 1987). They also dominate the oribatid fauna of disclimax habitats, such
as periodically flooded soil of reservoirs (Tamm et al. 1984), cultivated soils
(Norton and Sillman 1985), and other regularly perturbed sites.
The wide geographic and habitat distribution of many thelytokous Brachypylina
is consistent with the hypothesis that they have "general purpose genotypes" (e.g.
Lynch 1984). The competing "biotic uncertainty" hypothesis, that thelytokous
species are relegated to biologically depauperate habitats by their inflexible ge-
nomes (Bell 1982), seems incompatible with the observed persistence of these
colonizing species in successionally more mature, complex environments.
Other biological traits have also been suggested to correlate with thelytoky,
only some of which are supported by patterns observed in oribatid mites (Norton
and Palmer 1991). Reduction in egg viability is known in some thelytokous
organisms (Bell 1982), but has not been observed in oribatid mites. Nor are
generation times shorter in thelytokous species, as was suggested by Gilyarov
(1982). Small body size has been suggested to promote thelytoky since there is
a lower limit to egg size (Dybas 1966). Presumably, if only one or two eggs are
carried at a time, and egg turnover rate is low, the "two-fold advantage" would
be important in keeping fecundity at a viable level. This is consistent with
the distribution of thelytoky in some mostly sexual genera of Brachypylina; if
thelytokes exist, they are often among the smallest species in the genus. Habitat
may also correlate with thelytoky. Only half the known species of Hydrozetes
are sexual, perhaps reflecting selective forces favoring thelytoky in their aquatic
medium. Life in the small pore spaces of deep soil (euedaphic) horizons may
promote thelytoky in oribatid mites due to the uncertainty of finding mates. The
typically small size of deep soil taxa may contribute to thelytokous tendencies,
or may be coincidental to the evolution of this reproductive mode. In some
brachypyline genera, no biological or distributional factors seem to apply. For
example, the oppiid genus Quadroppia includes sexual subspecies among its
smallest members (Lions 1982), with no microdistributional pattern evident.
3 .3 Fecundity
Lifetime fecundity of oribatid mites is low relative to many other mite groups
(usually several dozen eggs per lifetime or fewer), but taxonomic or ecological
patterns are not retrievable from the sparse data. Instantaneous clutch sizes are
known for some organisms (e.g. Luxton 1981a) but are of little use without
corresponding information on turnover rates, which appear to vary with species.
The small-bodied species Oppiella nova usually carries a single egg but lays
about 12 eggs/week in culture (Woodring and Cook 1962b), whereas the large-
bodied species Steganacarus magnus matures a single clutch of about six eggs
(developed to prelarvae) laid individually at lengthy intervals (Webb 1989).
Several factors are known to influence the fecundity of animals raised in
culture. A negative effect of crowding on oviposition rate has been demonstrated
for Nothrus palustris (Lebrun 1970a), Alaskozetes antarcticus (Peckham 1967),
Achipteria holomonensis (Stamou et al. 1981) Carabodes willmanni (Bellido
1990), and Oppia nodosa (Bhattacharya et al. 1978), but crowding seems irrele-
vant in Pergalumna emarginata (Rockett and Woodring 1966a, = P. omnipha-
gous). Stamou and Asikidis (1989) found that in Scheloribates cf latipes and
Achipteria oudemansi an optimum density may exist, since very low densities
had a negative effect on fecundity. Food quality may also be of prime importance.
Shereef (1970) found that species-level differences in fungal food can have a
major influence on oviposition rates in Epidamaeus kamaensis and Oppia con-
color. Such nutritional effects have also been shown by Reddy et al. (1978)
for Galumna flabellifera and by Saichuae et al. (1972) for Nothrus biciliatus.
Microclimatic influences can also be expected to contribute to variability in
fecundity (Bellido 1990), but effects of parameters such as temperature and
humidity are rarely partitioned experimentally.
Studies of fecundity conducted by various laboratories are seldom comparable,
since we are usually ignorant about where in the spectrum offood quality, ambient
J08 / R. A. Norton
temperature and population density the given culture conditions lie. There is a
uniform general picture of low to modest fecundity even under optimal conditions,
but future comparative studies will be needed to assess adaptation, especially
ones linked to studies of energetics.
Do oribatid mites exhibit the clutch size patterns suggested for insects by
Godfray (1987)? For example, is clutch size directly related to female body size,
with oviposition sites being readily available and the optimal egg number being
more than a mite of given size could produce? Such an argument might be made
for Archegozetes longisetosus, a mite that fills its hysterosoma with eggs. Or do
some groups exhibit optimum clutch sizes, determined by the rates of energy
procurement and a limited number of appropriate oviposition sites? Steganacarus
mag nus , a slightly larger mite that may produce fewer than 10 eggs in its lifetime
(Webb 1989), might be an example.
3.4 Developmental Rates
Developmental rate is the most investigated life-history trait of oribatid mites

(see summaries by Lebrun 1970a, 1971, Luxton 1981a, and Grishina, 1991).
Studied mostly between 20°-30° C, the egg-adult developmental period varies
from about three weeks in the small Oppiella nova to more than one year in
Conoppia palmicincta (Woodring and Cook 1962b, Michael 1884 , respectively).
Various developmental studies are often incongruent, even when done at similar
temperatures. At room temperature (about 20° C), Haarlov (1960) and Hartenstein
(1962) respectively noted development times of 41 days and 119-149 days for
Ceratozetes gracilis, and of 332 days and 150 days for Platynothrus peltifer.
Such major discrepancies can result from a variety of culture effects, though
heritable popUlation differences cannot be discounted. For example, temperature
conditions cannot fully be described by reporting mean values. The stimulating
effect of fluctuating (vs. constant) temperature can be striking, due to high QIO
values (Lebrun and Ruymbeke 1971, Lebrun 1977, Stamou 1989, Stamou and
Sgardelis 1989, Bellido 1990). Nor can temperature effects be assumed to be
constant over the course of ontogeny; they may vary among eggs and instars, as
well as among species (Vera and Berthet 1988, Taberly 1989). Other influential
factors are food quality (Saichuae et al. 1972, Mitchell and Parkinson 1976,
Young and Block 1980, Stefaniak and Seniczak 1981), density (Stamou et al.
1981) and even illumination (Lebrun 1970a).
Few existing laboratory studies have direct field application, if only because
cultures are commonly 50-100% warmer than natural conditions. In useful stud-
ies, temperature regimes reflect environmental patterns (Weigmann 1975), rear-
ing chambers are placed directly in the field (Lebrun 1971), or mites are studied
in near-natural situations where oviposition and emergence can be estimated
(Gourbiere et al. 1985, Lions and Gourbiere 1988). Following changes in age-
class distribution is a useful field technique (Mitchell 1977a, Thomas 1979,
Luxton 1981a, 1981b), but only if oviposition is temporally circumscribed and

cohorts can be distinguished throughout ontogeny. Often cohort identity is weak-
ened or lost as development proceeds due to increasing length and variability of
instar duration, and in such cases populations are rather stable (Lebrun 1970a,
Mitchell 1977a, Schatz 1983, 1985).
Gross patterns recognized from the early literature by Lebrun (1970a, 1971)
seem to have reasonable applicability. "Higher" oribatid mites (Brachypylina)
usually develop more rapidly than most similar-sized early-derivative groups,
and within a taxonomic grouping (perhaps at a family or superfamily level) larger
species have more lengthy development.
In temperate forest soils the development of most species probably takes from
several months to well over a year. Even Oppiella nova, which can develop in
the laboratory in only three weeks (Woodring and Cook 1962b), appears to
have a single annual generation in Denmark (Luxton 1981 b). Even under ideal
conditions a quarter to a third of development is spent inactive, in preecdysial
resting stages (Luxton 1981a), and cold-induced dormancy ("coma" or "quies-
cence") during winter can significantly extend development. When laboratory
studies have included trials at low temperatures, a threshold has been noted below
which development is suspended (Weigmann 1975, Bhattacharya et al. 1978,
Schatz 1985, Stamou 1989, Taberly 1989, Bellido 1990 ). Such dormancy has
been considered an adaptation by some (e.g. Stamou 1989), but is more simply
explained as a manifestation of metabolic constraints at low temperatures (Cannon
and Block 1988 and included references).
In discussing the ecological significance of slow developmental rates, Mitchell
(l977b) noted that oribatid mites generally are not able to track and exploit short-
term changes in resources. However, their low metabolic rates should enable
them to survive periods of low food availability.
3.5 Survivorship, Adult Longevity and Sources of Mortality
Reliable laboratory studies suggest that survivorship is optimal at particular

culture densities (Stamou and Asikidis 1989), and is inversely related to tempera-
ture (e.g. Saichuae et al. 1972, Stamou et al. 1981, Cannon 1987). Moderate to
high death rates reported in some studies (e.g. Sengbusch 1954, Woodring 1965)
might simply reflect unsatisfactory culture conditions.
Field survivorship studies are few, and most concern species in habitats other
than temperate forest soil. Natural mortality seems concentrated in the immature
instars, with the rate of loss decreasing during ontogeny. Survivorship to adult in
two unrelated species, the alpine Oromurcia sudetica and the aquatic Hydrozetes
lemnae, is similar, about 10% and 8-12% respectively (Schatz 1983, Fernandez
and Athias-Binche 1986). Mitchell's (l977a) estimate for the boreal species
Ceratozetes kananaskis was twice as high (24%), but he assumed one clutch was
produced per year. If in fact there are two clutches per year, survivorship would
110 / R. A. Norton
be similar to the other estimates. Whether the general climate is temperate or

cold, little mortality of immatures seems to be associated with winter dormancy
(Mitchell 1977a, Schatz 1983, Stamou 1989), probably due to inactivity brought
on by chill coma. The ability of adult oribatid mites to withstand freezing
temperatures by supercooling is well documented (Cannon and Block 1988).
From laboratory data (summarized by Luxton 1981a) adult longevity of over
a half-year is common, and Damaeus onustus and Neoribates gracilis adults can
survive about two years at room temperature. Luxton (1981a) suggested that field
longevity should be overestimated by culture data, but the opposite may be true.
Low temperatures may considerably extend longevity (e.g. Nannelli 1975), and
if winter dormancy is included in rate estimates then 1-2 year longevities may
not be uncommon in temperate soils. As a result, iteroparity may be routine
(Mitchell 1977b), both within and between years. Multiple clutch production
cannot be assumed a priori, however; the large-bodied species Steganacarus
magnus may live longer than three years, yet produce a single small clutch of
eggs (Webb 1989).
What are the likely abiotic causes of mortality? In winter, forced quiescence
and supercooling ability may keep winter losses low, while summer desiccation
may be a principal abiotic mortality factor (Madge 1964). In some dry climates,
the need to migrate deeper into soils to encounter moisture may put a premium
on small size since mites must traverse pore spaces that generally decrease in size
with depth (Athias-Binche 1985, 1989). Biotic mortality sources are varied but
little studied. Whereas soft-bodied immatures are vulnerable to a wide array of
predaceous arthropods (Luxton 1964, Lebrun 1970b, Wallwork 1980, Walter et
al. 1989), the sclerotized adults have fewer known enemies. The latter may
include featherwinged beetles (Ptiliidae, Riha 1951), anti ike stone beetles (Scyd-
maenidae, Schmid 1988), short-winged mold beetles (Pselaphidae, Park 1947,
but see Walker 1965), ants (E. O. Wilson, pers. comm., 1989), and dragonfly
nymphs (Y. Behan-Pelletier, pers. comm., 1990). The bdellid mite Cyta lati-
rostris (Alberti 1973), and probably a variety of small salamanders (e.g. Norton
and MacNamara 1976) are also predators of sclerotized adults. Parasitic nema-
todes and sporozoans may be significant causes of mortality (Walker 1965,
Baumler 1970, Purrini 1980). Occasionally oribatid mites host ectoparasitic
larvae of the mite family Erythraeidae (Norton et al. 1988d).
Evidence of an evolutionary emphasis on adult survival can be seen in a
morphology adapted for predator defense. Most adults have a hardened cuticle,
while that of immatures is distinctly softer. Hardening usually results from
sclerotization, but in some taxa (e.g. Hypochthonioidea, some Ptyctima) it is
primarily due to calcification (Norton and Behan-Pelletier 1991). Adult pty-
choidy, in which legs are retracted and the prodorsum folds ventrad to cover
them, is a defense that has evolved independently at least three times (Norton
1984). Many other taxa have evolved an amazing array of cuticular structures
(tecta) that protect vulnerable articulations and effectively deter most potential
predators.
3.6 Voltinism and Generational Synchrony
The number of annual generations in temperate soil species has frequently been
overestimated in the literature (Mitchell 1977b, Norton 1985). Perhaps guided
by a general belief that mites reproduce rapidly, authors have often simply divided
laboratory development time into 365 calendar days to obtain the number of
annual generations (see review by Luxton 1981a). This simplistic approach
considers neither the unrealistic temperature regime of most studies nor seasonal
dormancy enforced by cold weather in nature.
Even if age-distribution studies suggest a one-year ontogeny, it may be incor-
rect to assume univoltinism. Authors often have ignored the weeks or months
necessary for cuticular hardening (teneral period), the procurement of sufficient
energy resources, and the development of eggs, as well as the rate-depressing
effects of decreasing fall temperatures. It may be common for winter to intervene
between the appearance of an adult and its progeny, at least for the later-maturing
part of a given cohort. The specific time an egg is laid within the reproductive
period can also significantly impact development and therefore generation time
(Murphy and Balla 1973, Weigmann 1975, Luxton 1981a). Interpretations vary,
but available field studies suggest that the generation time of most oribatid mites
is one or two years in temperate soils (e.g. Luxton 1981a, 1981b, Kaneko 1989).
Few patterns in reproductive phenology have been noted in the literature, only
two of which are taxonomic; the Phthiracaridae and Liacaridae seem to bear eggs
(or prelarvae) continually (Table 2 of Luxton 1981a). Two ecological patterns
that have been suggested are somewhat conflicting. Luxton (l981a) found that
females of species inhabiting litter layers in a Danish beechwood soil carried eggs
throughout the year. However, Mitchell (1977a) found those oribatid mites living
in surface layers of a Canadian aspen woodland soil to have circumscribed egg
maturation (spring-summer). Those of the deeper (humus) layers contained eggs
throughout the year, a pattern also suggested by Smrz (1989). Adaptive explana-
tions for either pattern are easily imagined. One could argue that circumscribed
oviposition is beneficial in surface layers that may be more seasonally variable
(e.g. in moisture regime, according to Mitchell). One could also argue that the
continual presence of eggs in mature females is beneficial in variable surface
layers, since eggs could be laid opportunistically when environmental conditions
are temporarily favorable.
3.7 Net Reproductive Rates
Net reproductive rate per female (Ro) has been estimated for only a few oribatid
species. The relatively stable densities often observed in soil oribatid mites
112 / R. A. Norton
(Lebrun 1970a, 1970b, Mitchell 1977a) suggest net reproductive rates are near
unity, as Mitchell (l977a) calculated for a boreal forest soil species, Ceratozetes
kananaskis. Various mathematical models utilized by Cancela da Fonseca ( 1980)
for three temperate oribatid mites yielded Ro values above or below 1.0, depending
on the model applied.
As noted above, Mitchell (1977b) thought oribatid mite populations are unable
to respond numerically to short-term changes in resource availability. Schenker
(1986) depicted reproductive traits of temperate oribatid mites quite differently.
High rates for Platynothrus peltifer, Oribatula tibialis and Scheioribates pallidu-
ius (Ro = 8.82, 9.46 and 6.03, respectively) during what he considered to be
periods of changing population density led him to suggest that "new resources
(litter etc.) are utilized efficiently." His values are grossly exaggerated, however,
since survivorship of adults, rather than survivorship from birth, was used in the
calculation of Ro (see Southwood 1978). Several less critical details of his study
are unclear. For example, analyses were based on data from periods of supposed
population change, but high variance caused by the aggregated distribution of
oribatid mites (described at this site by Schenker 1984) often makes trends difficult
to ascertain, and no statistical support for this was offered. The means by which
the age-specific number of female offspring (mJ was determined in this field
study were not mentioned; simply counting the number of eggs present for the
latter is insufficient since turnover rates were not estimated (see above). The one-
month sampling period may approximate the clutch turnover period, but more
likely it does not. The author also did not mention whether the fact that P. peitifer
is thelytokous was considered in fertility calculations. In short, there seems to be
no evidence that these three oribatid mites have any unusual ability to track
changes in resource availability.
3.8 Dispersal
Dispersal remains one of the least known aspects of oribatid mite biology, but it
probably occurs principally in the adult instar. Adults seem better equipped to
deal with exposure to predation during dispersal than are immatures. This is
clearly true if immatures are strict endophages (e.g. Ptyctima, Carabodidae,
Hermanniellidae, many Liacaridae and Xenillidae); they do not emerge from their
burrows in decaying wood, leaves, fungi, or lichens before reaching the adult
instar. Those few oribatid species known to be phoretic on insects (always insects
associated with decaying wood) disperse only as adults (Norton 1980).
Dispersal may usually encompass little more than the seeking of food or
favorable oviposition sites by gravid females. Active horizontal movements of
soil species may be restricted to a distance of a few centimeters (e.g. Berthet
1964), though vertical migrations into vegetation may be more substantial, both
diurnally (e.g. Tarras-Wahlberg 1961) and seasonally (Murphy and Balla 1973).
Potentially long dispersal distances may be possible in some Hydrozetes species,
in which adults (but not immatures) are made buoyant in water columns by gas
bubbles formed in their guts (Newell 1945, Burford 1976).
3.9 Summary of Life Histories in Temperate Soil
The life-history attributes of temperate, soil-dwelling oribatids mites seem typical

of organisms considered to be "K-selected" or to have "K attributes" (MacArthur
and Wilson 1967, Pianka 1970). Life-cycles and generation times are usually
long relative to other mites, often exceeding one year. Fecundity is low, even
though adults are probably long-lived and often iteroparous. Mortality is concen-
trated in immature instars, and net reproductive rates are such that adult population
density fluctuates little from year to year. The ultimate cause of these traits, i.e.
whether they are best explained as direct or indirect responses to selective forces,
or rather result from internal, historical constraints, will be addressed later.
Assuming this suite of traits to be plesiotypic, do we see apotypic traits in
other situations, such as more specialized habitats or regions of environmental
severity, that are likely to be adaptive?
4. Life Histories in Apotypic Habitats
4.1 Species in Cold Environments
Oribatid mites of cold environments have attracted considerable attention. Adap-

tive life-history traits have been suggested, but not clearly demonstrated, and
some patterns probably are simply a function of heat budget. For example, a low
heat budget seems responsible for the long mean generation time (4.2 years) of
Ceratozetes kananaskis in boreal Canadian aspen soil (Mitchell 1977b). Heat
budget probably also controls the demographics of Oromurcia sudetica in alpine
Austria, a climatically similar site (Schatz 1983, 1985). For this species extended
and variable duration of instars results in overlapping generations, such that
development requires 2--4 years with an additional year needed before females
Jay eggs.
Those studies suggesting life-history adaptation to cold environments are vul-
nerable to criticism. For three species, West (1982) recognized adaptations to the
cold and unpredictable climate of the sub-antarctic island of South Georgia. He
considered Platynothrus skoettsbergi to have adapted by becoming semelparous.
Using field age-class data (but without supportive laboratory studies), he sug-
gested a one-year life cycle, and proposed that population "reserves" were usually
present as high numbers of larvae that could rapidly develop into adults in
unpredictable periods of favorable conditions. This scenario seems unlikely for
several reasons. First, the age-class data (his Fig. 5) could easily be interpreted
as showing a development of two years or more; the deutonymph alone seems to
take almost one year. Adults of this species (which he called "feeble") are unlikely
114 / R. A. Norton
to produce the suggested burst of reproduction, even in relatively favorable

conditions. Clutch sizes were not mentioned, but Chilean representatives have a
maximum clutch size of only 11 eggs per female (pers. observ.), which in
the cold South Georgian climate may comprise the annual production. The
development of this mite is probably no faster than that of P. peltifer, which has
a mean generation time of two years in northern Europe (Thomas 1979, Norton
1985). A plesiotypic, iteroparous life history controlled by low heat budget seems
much more likely than the demographic adaptations implied by West (1982).
Based on age-class data, West (1982) suggested Eobrachychthonius oudemansi
had a two-year life cycle, and considered the accumulation of tritonymphs,
rather than larvae, to constitute a population "reserve." He also considered it
semelparous, but seme1parity, definable as a one-time reproductive "burst" (Cole
1954), is hardly feasible in such a small mite, especially when only one or two
eggs can develop at a time (Trave 1968). This species is probably thelytokous
like other known Brachychthoniidae, I but females must average more than one
life-time clutch to maintain a population. As noted above, an accumulation of
late instars can be induced by low heat budgets, and therefore E. oudemansi has
no known life-history traits that can be reasonably called adaptations to cold or
unpredictable environments.
West (1982) suggested that the life history of Edwardzetes elongatus is charac-
terized by an emphasis on adult longevity and iteroparity at the expense of
fecundity, and considered this an adaptive strategy in the cold, unpredictable
climate. His data are not dissimilar to those of the confamilial (Ceratozetidae)
mites studied by Mitchell (l977b) and Schatz (1983, 1985). In fact, as favorable
as this combination seems to be, it is typical of oribatid mites in general, and the
life history of E. elongatus seems to be plesiotypic, rather than adaptive.
Block (1980) argued that Alaskozetes antarcticus has an adaptive life-history
strategy. He felt that in the cold, rigorous environment of continental Antarctica,
selection favored several observed traits: slow development with delayed repro-
duction; decreased mortality; a longevity of more than one year2; and shunting
of only a small part of assimilated energy into reproduction. Such traits were
suggestive of "K-selection," but he noted that others, including small adult body
size and absence of a competitive environment, were associated with r-strategists.
However, this mite is quite large for an oribatid, and r-K selection theory stresses
relativity. Also, a lack of resource competition and the severe environmental
'West (1982) assumed that the nongravid, light colored specimens were males, but this is unlikely.
Females do not darken or develop eggs until after a teneral period (Trave 1968).
'Block (1980, his Fig. 3) proposed a minimum generation time of 14 months, which would require
a female to molt from the tritonymph, pass the teneral period, mate, develop eggs, and retain eggs
to prelarvae during the same summer. But from a combined energy budget and degree-day analysis,
Bum (1986) suggested that the duration of just the deutonymph and tritonymph might together occupy
more than three years in a natural temperature regime.
rigor should not force conclusions that something is unusual about the evolution
of this particular mite. Instead, it further emphasizes the general utility of the
typical oribatid mite life history. Their constrained physiology (rather low feeding
and growth rates) does not allow them to adapt in any special way to cold,
unpredictable environments, but at the same time their modest requirements and
high adult survival give them the quality of perseverance.
In short, A. antarcticus seems to exhibit no life-history traits, or combination of
them, that clearly constitute adaptation to an Antarctic environment. Survivorship
curves are not yet available, but like other known oribatid mites they probably
incur most mortality in immature ins tars (an important determinant of life histories
according to Hom 1978) and adults seem to be dispersive (Covarrubias 1968).
Though life history per se may not be adaptive in Alaskozetes antarcticus,
physiological adaptations may somewhat counter low heat budgets. Cold adapta-
tion in this mite seems to consist of a higher temperature-specific metabolic rate
than in temperate species, due perhaps to lower activation energies of enzymes
(Block 1977, Block and Young 1978, Young 1979). A facet not yet examined is
the involvement of gut microbes in digestion (see below). Is observed tempera-
ture-dependance of physiological traits in oribatid mites due in any significant
way to parameters of microbial physiology? Another physiological trait, the
ability to supercool, was first considered a specific adaptation to extreme climates
(Block 1980), but now is known also to occur in temperate-zone oribatid mites
(Cannon and Block 1988).
The evidence for specific life-history adaptations to cold environments is weak,
especially when traits of temperate species are considered, and Danks (1981)
expressed similar thoughts about arctic arthropods in general. Oribatid mite
species with wide ecological distributions seem to respond to cold climates by
elongating the life cycle as a function of heat budget. The cosmopolitan species
Tectocepheus velatus illustrates this. It seems to be semivoltine in alpine Norway
(SolhS'lY 1975), but bivoltine in more temperate regions of Europe (Thomas
1979, Schenker 1986). Rather than having a rigid diapause control, it exhibits
considerable plasticity in being able to overwinter in most, if not all instars.
Elongation of the life cycles of arthropods in cold climates may indeed confer a
resistance to catastrophic losses of a single age-class (e.g. West 1982, Ring and
Tesar 1981). But if elongation is simply due to limited heat resources, it should
be considered neither an adaptation nor the principal part of a "strategy" for life
in such environments, as some have suggested (e.g. MacLean 1975).
4.2 Species in Hot Deserts
In hot deserts a high heat budget allows relatively rapid life cycles, while repro-
ductive contributions may often be limited by moisture regimes. We have little
information on life histories of oribatid mites living in hot, dry climates, but some
116 / R. A. Norton
adaptive traits have been suggested. As with studies of oribatid mites in ,cold
climates, much of the speculation is unconvincing. '
Using a combination of Berlese-funnel and flotation methods, Wall work ( 1972)
studied Joshuella striata and Haplochthonius variabilis under Juniperus bushes
in the Mojave Desert of California. He suggested that reproduction occurred once
annually, with full development occurring within weeks in the litter layer, either
at the time of winter rainfall (1. striata) or in spring (H. variabilis). However,
immatures were present in all but one sampling period, suggesting that reproduc-
tion may not in fact be so highly circumscribed. Also, he took few samples,
reported no estimates of variation, and only noted the depth of mineral soil
samples (8-14 cm.) in a later paper (Wallwork 1980).
Referring to the ideas of Noy-Meir (1973), Wallwork (1980) considered these
as opportunistic, r-selected species, tracking a resource (in this case moisture)
with pulses of reproduction. But even if we accept the relatively unconvincing
data in this study, r-selection seems an unreasonable hypothesis. There is no
evidence of the multivoltinism, short adult life, and high reproductive potential
normally associated with such life histories.
Studies of experimentally watered Chihuahuan desert soil (Wallwork et al.
1984, 1986) suggested that reproduction in lornadia Larrea and two species of
PassaLozetes occurs only in summer and cannot be triggered by artificial rainfall.
The authors considered this seasonal recruitment an adaptation to the summer
rainfall in the region. However, data from Luxton (1981a, his Table 2) indicates
that most poronotic oribatid mites (a group including PassaLozetes and Jornadia)
produce eggs seasonally, particularly in summer. The observed timing could
simply be plesiotypic (i.e. ancestral in poronotic mites), "preadapting" them to
the moisture regime of the Chihuahuan Desert.
In contrast, Joshuella striata appears able to reproduce throughout the year
and does well in the different moisture regimes of both the Mojave and Chihua-
huan Deserts (Wallwork et al. 1984, 1986). But the data supporting opportunistic
tracking of moisture levels are equivocal, and this mite species may simply have
a historical tendency to carry eggs throughout the year. At present we have no
data for other members of the family Gymnodamaeidae.
4.3 Freshwater Species
Few oribatid mite lineages have made the transition to freshwater, and while
morphological adaptations are known, clear life-history adaptations are not.
Thelytoky appears to be derived and probably adaptive in brachypylines, such as
Hydrozetidae, but is ancestral and perhaps "preadaptive" in freshwater members
of early-derivative groups (e.g. Trhypochthoniidae) (Norton and Palmer 1991).
Fragmentary laboratory and field information (Norton et al. 1988b, Norton and
Palmer 1991, unpublished observations) suggests that aquatic Trhypochthoniidae
are demographically at least as conservative as soil-dwelling relatives. Living
Evolutionary Aspects of Oribatid Mite Life-Histories I 117
in cold, oligotrophic waters, Mucronothrus nasalis probably has a multiyear

generation time and low fecundity.
Adaptive life histories have been suggested for the thelytokous brachypyline
species Hydrozetes lemnae, associated with duckweed (Lemna gibba) in temper-
ate Argentina (Athias-Binche and Fernandez 1986, Fernandez and Athias-Binche
1986). Immatures burrow in the duckweed leaflets and adults disperse. The
studied captive population appeared to be bivoltine with nonoveriapping summer
and winter generations, and though females of each generation laid about 30
eggs, net reproductive rate per female (Ro) was much lower in winter females
than in summer females (0.63, 1.59 respectively).
Fernandez and Athias-Binche (1986) suggested that immatures of the Argentine
population are specialized duckweed endophages, and will drown when innun-
dated (due to the absence of a plastron). But if this is true, it is not clear why
immatures of European and North American H. lemnae may be found dissociated
from duckweed (Grandjean 1948, pers. observ.) and are easily reared on fully
immersed, decomposing leaves (Burford 1976, Johnson 1983).
Fernandez and Athias-Binche (1986) also suggested that H. lemnae tends
toward an r-selected demography, but they did not specify traits they considered
to be so selected. Reproductive rate seems to be no higher than expected for soil
species, and they had no laboratory data on development time. Burford (1976)
estimated a rather short development time for H. lemnae (misidentified as a new
species), but considered it univoltine in Colorado. A similar development time
was observed by Johnson (1983, mean = 51 days). One could argue that a slightly
higher heat budget may be responsible for the proposed bivoltinism of H. lemnae
in Argentina. If true, such environmental differences reflect heat budgets and not
adaptation. Although the analyses of Fernandez and Athias-Binche (1986) are
elegant, this experiment was not replicated, and with a single sample taken per
time period the significance of the data cannot be judged.
4.4 Tropical Species
Beck (1969, 1972) concluded that the rather depauperate oribatid mite fauna of
flooded forests in the Amazon Basin adapted some life-history traits to the
seasonal flood rhythm. Only RostrozetesJoveolatus seems to survive the extended
flooding as adults, though densities are rather low. Females develop eggs while
still under water, and Beck considered the thelytoky exhibited by this species
a prerequisite for population survival, since low densities and environmental
conditions preclude indirect sperm transfer by spermatophores. But since he
found R. Joveolatus also to be thelytokous in non-flooded forests (true also of all
North American populations I have examined), this may instead be a "preadapted"
trait.
Several other species gradually became abundant after flood waters receded.
Beck suggested that their short development time (3-5 months) is synchronized
118 I R. A. Norton
to flood periodicity, and that flooding was endured by diapausing eggs, since
Berlese funnel samples failed to produce specimens. However, laboratory studies
will be necessary to confirm the diapause, a phenomenon currently unknown for
any oribatid mite species. Also, most species studied were found in nonflooded
forests as well (where their life histories were undetermined). This suggests
that eurytypic biologies, rather than specific life-history adaptations, may be
responsible for their establishment in flood-zone forests.
5. Synthesis of Ideas on Life-History Evolution in Oribatid Mites
5.1 Three Views of UK-attributes"
As noted by Crossley (1977), the general life-history traits of oribatid mites

exemplify those of so-called "K-selected" species. In this view, life-history traits
such as delayed maturity, low reproductive potential, iteroparity and long adult
life are adaptations to existence in a competitive environment at stable population
densities.
Is competition a significant force in the organic horizons of soil? It may be
hard to imagine food as a limiting factor in such environments, but in the spatial
mosaic that constitutes this system (Mitchell and Parkinson 1976, Mitchelll979a)
quality food may be quickly utilized. This is supported by observations of seasonal
shifts in oribatid mite diets, particularly from fungi to higher plant material as
the former becomes less available (Anderson 1975b). Observed redistributions
of oribatid mite species in microcosms also seem attributable to competition
(Anderson 1978b).
"Bet-hedging" (Stearns 1977) is a second hypothesis consistent with the life-
history attributes of most oribatid mites. In such a model, if a variable environment
results in variable immature mortality, the above-noted suite of life-history traits
could result as a "syndrome." Delayed maturity, smaller and iteroparous reproduc-
tive effort, and greater longevity are then viewed as buffers against catastrophic
population reductions. If such unpredictable mortality occurs in oribatid mite
populations, it seems reasonable that the immatures would bear the brunt of it.
In a recent analysis Lebrun et al. (1991) seem to embrace both ideas, but is it
necessary to invoke either model? In a reevaluation of ideas about life-history
evolution, Stearns (1980) suggested that individual life-history traits may have
strong evolutionary interactions with physiological traits, and constraints in physi-
ology can overwhelm any co-adaptation of life-history traits predicted from
theory. Thus, the following third approach to oribatid mite life-history evolution
should be considered.
5.2 Constraints in Oribatid Mite Life Histories
Historical constraints, especially those related to digestive physiology, may be

the ultimate cause of many life-history traits of oribatid mites. For example,
iteroparity is theoretically one of natural selection's responses to the concentration

of mortality in immatures or to the high risk of reproductive failure in any given
season (Stearns 1976, 1977, Hom 1978). Yet in small-bodied species that carry
only one or two eggs, semelparity is impossible. Even in larger species, slow
digestive processes, low metabolic rates (Luxton 1975, Mitchell 1979b, Thomas
1979), and an inability to store significant amounts of energy (Wallwork 1979)
may lead to iteroparity.
Can aspects of ancestral feeding biology explain a generally low metabolic
rate? Microbial tissues, principally fungal mycelia and spores, were probably the
major food of early oribatid mites. Saprophagy (feeding on decaying higher plant
structural material) perhaps evolved as a facultative means of getting at non-
surface microbial tissue or metabolites when surface mycelia were in short supply
(Norton 1985, but see Luxton 1979). Such particulate feeding is very different
from that of the fluid-feeding predators that presumably constituted the earliest
Acari. Accumulating evidence suggests involvement of gut microbes in the
digestive processes of oribatid mites, whether they are fungivorous or sapropha-
gous (Stefaniak and Seniczak 1976, Seniczak and Stefaniak 1978, Stefaniak and
Seniczak 1981, Wolf and Rockett 1984, Haq and Konikkara 1988). Yet these
intestinal microbes appear to represent a nurtured component of the external
microbial community, rather than a specialized obligate flora. The shift from
predation to fungivory and saprophagy may have been related to an increased
reliance on metabolites or biomass produced by facultative gut microbes. Such
reliance may impose upper limits on food utilization, thus constraining metabolic
and growth rates. .
Based on this idea, Fig. 5.2 suggests possible interrelationships of some life-
history traits of oribatid mites. Low metabolic rate is the driving force in this
model, resulting in slow development and low time-specific fertility. Due to the
latter, population maintenance requires long adult lives. Limited body size plus
limited energy storage promote iteroparity. The need for adult longevity provides
a selective force for morphological and behavioral adaptations for defense, some
of which also enhance dispersal ability. Maintenance requirements during this
long adult life and energy costs of dispersal probably further reduce fertility.
The rather stable adult population seen by many authors results from extended
development, adult longevity and iteroparity.
6. Life-History Aspects of the Origin of the Astigmata
A generalization that life-history evolution did not play a principal role in the
radiation of oribatid mites would have one outstanding exception, the Astigmata.
These mites exploit protein-rich, high quality foods that are patchy in time and
space, and in doing so have evolved important relationships with both plants and
animals (OConnor 1982). Such biologies demand life-history traits very different
120 I R. A. Norton
Low Time-specific
Fertility ... Low Metabolic
Rate
Slow
Development
Iteroparity
t
Long Adult
Life
Adult Stable
Dispersal Populations
Figure 5.2. Possible relationships of some aspects of oribatid mite life histories, based
on low metabolic rate as the dominant influence (see text for explanation).
from those of oribatid mites. The great diversity of free-living and parasitic life
styles (see OConnor 1982) and their corresponding life-history adaptations make
generalization tenuous, but the Astigmata usually have higher fecundity, much
faster development, and thus much higher reproductive rates than do oribatid
mites. Adults are relatively short-lived, and egg turnover rates are relatively high
(e.g. Gerson et a1. 1983). In short, these colonizing mites may exhibit true r-
selected demographies, unlike any known oribatid mite.
Dispersal ancestrally occurs in the heteromorphic deutonymph Chypopus"), a
nonfeeding instar morphologically and physiologically adapted to phoresy,
though in some species the instar may be omitted or included only facultatively.
In terms of life-cycle, the loss of one instar in such taxa represents a lowering of
age at reproduction, a common trait of exploitative, r-selected species. Mating
and internal fertilization are ubiquitous in the Astigmata, in contrast to the free-
standing spermatophore of oribatid mites.
If the Astigmata originated within an oribatid lineage, two intriguing questions
are immediately posed. With such a dichotomy between the basic life histories,
how did the transition occur? Since mites are notorious for mUltiple origins of
exploitative life styles, why in the long history of oribatid mites did such a major
change in life style occur in only one lineage? The questions may have the same
ultimate answer if one aspect of oribatid mite life history was particularly difficult
to change, such that it constituted a barrier (in the sense of Steams 1980) to
"breaking out" of the self-reinforcing system suggested in Fig. 5.2.
Some trait changes are unlikely to have initiated the transition. The abandon-
ment of indirect fertilization by the Astigmata certainly increased mating effi-
ciency, but associative mating seems to have evolved independently several times
in oribatid mites (see above) without producing major life-history shifts.
Could a shift to higher quality resources have been the key? Many oribatid
mites have been characterized as opportunistic feeders that can utilize protein-
rich food. For example, species whose guts normally contain leaf and fungal
fragments may feed almost exclusively on pollen at times of peak release by
plants (Hammer 1972, Behan-Pelletier and Hill 1983, pers. observ.). Some
Brachypylina readily eat living nematodes when they are available (Rockett and
Woodring 1966b, Muraoka and Ishibashi 1976, Rockett 1980, Walter and Ikonen
1989). Food quality alone was probably not the key to life-history transition.
A more efficient digestive physiology, allowing higher metabolic and growth
rates, probably appeared early in the origin of the Astigmata. Even when environ-
ments and food seem similar, the Astigmata are more metabolically active. For
example, the acarid Niadacarus arboricolus has apparently reverted to an ori-
batid-like feeding regime by feeding on dead leaves. For an astigmatid mite it is
considered "K-selected" but its development is shorter and reproductive capacity
much higher than that of leaf-feeding oribatid mites (Fashing, this volume). If
gradual physiological improvements were the key to the original success of the
Astigmata, we might expect intermediate forms of life history in early-derivative
groups, but there is no evidence of this.
One clear life-history difference is that oribatid mites disperse as adults while
astigmatid mites disperse as immatures, at least ancestrally. The phoretic deuto-
nymph has been a key to the radiation of the Astigmata, but could it have arisen
ad hoc from an oribatid mite life cycle? An even more basic life-history change,
the shifting of dispersal from the adult to one or more immature instars, was
probably a necessary precedent (see Houck, Chapter 11, this volume, for discus-
sion of why deutonymph is the only immature instar involved in disperal).
Hom (1978) considered age at dispersal to be a major factor in molding life
histories. If dispersal as immatures is somehow introduced into a "K-style" life
history, prior constraints and reinforcements may be profoundly affected. If
females are nondispersive, more energy can be invested in egg production. The
increased reproductive uncertainty involved with dispersal of immatures places
a high priority on maximizing propagules at the expense of adult survival, and
such a shift in emphasis characterizes r-selected Astigmata.
What could have allowed a change from dispersal as adults to dispersal as
immatures in the lineage that produced the Astigmata? Could some functional
indifference in the age of dispersal have been involved, such that immatures
and adults were equally effective? This hypothesis seems doomed, since a pre-
reproductive individual in a sexually reproducing species is less valuable as
122 I R. A. Norton
dispersive "currency" than is a fertilized female. But if the ancestral lineage was
thelytokous there is little difference in the value of adults and immatures as
propagules. Immature females are less likely to survive to oviposition, but this
is offset by a greater abundance of immatures relative to adults.
Since thelytokous taxa are usually considered long-term evolutionary dead
ends, it is necessary to consider the cladistic relationships of the Astigmata to
appreciate this possibility (Norton and Palmer 1991). The Astigmata appear to
have evolved from within the Desmonomata (Fig. 5.1), but particularly from
within the Trhypochthonioidea (including Trhypochthoniidae sensu lato, Malaco-
nothridae; also Mucronothridae, Allonothridae of authors). This group contains
no sexual species (Norton et al. 1988c), and appears to have radiated in a
thelytokous reproductive mode. Many of these mites are only weakly sclerotized
as adults, such that the difference in cuticular hardness between adults and
immatures is not great.
If this scenario is correct, the predominance of sexuality in the Astigmata
means that a reversion to sexual reproduction occurred early in their evolution
(Norton and Palmer 1991), and the added evolutionary plasticity associated with
sex may have fueled other changes. Such a proposal goes against the grain of
current theory, and for some a reversal to sexuality may be even more difficult
to accept than is radiation in a fully thelytokous taxon. Yet, a population of
Oribatula sakamorii in Japan seems to have incurred such a reversal during
gradual habitat improvement (Fujikawa 1987). New cytogenetic perspectives on
such reversals are discussed in Chapter 11 of this volume.
Whatever the evolutionary reasons, in giving rise to the Astigmata oribatid
mites had a single "fling" at major life-history radiation. The very success of this
radiation from an otherwise conservative group has delayed our recognition of
its origins.
7. Prospectus for Future Research
In the future it will be important to learn the proximate cause of the relatively
low metabolic rates in oribatid mites and the possible contribution of their non-
specific gut flora to digestive processes. Even the hydrolytic enzymes from
ingested fungal food may contribute, though there is no strong evidence for this
in other studied arthropod detritivores (Martin 1987).
Within this framework, we need to understand the physiological basis for the
more rapid temperature-specific development seen in more derived groups. For
example, Haq (1978) found the rather primitive species Lepidacarus ornatissimus
to have a one year generation time even in tropical India, a laboratory development
seven times longer than that of similarly sized galumnid mites (Brachypylina).
Such studies will be of general interest in soil ecology. For example, collembo-
lans generally have higher ingestion rates, higher metabolic rates, and shorter
generation times than do oribatid mites (Crossley 1977), while feeding on similar
materials. This implies a considerable difference in competitive ability. Though
they are of a similar geologic age as oribatid mites, collembolans have a very
different evolutionary history and probably did not incur a major shift in food
base. Collembolans may also have an advantage from the standpoint of feeding
mechanisms. Their mandibulate mouthparts, often with grinding molar plates,
seem more efficient for processing fungal and leaf tissue than are the chelicerae
of oribatid mites. Chelicerae evolved in association with predation, and probably
became useful in particulate feeding only with the origin of the subcapitular
rutella; these function with the chelicerae to cut minute individual pieces of
substrate.
Further studies of thelytokous parthenogenesis should be especially rewarding,
as it appears to be a long-established plesiotypic trait in some groups but a recent
apotypic trait in others. Just as importantly, detailed studies of thelytokous species
could aid our understanding of phenotypic plasticity. Heritable genetic variation
in life-history traits currently cannot be distinguished from phenotypic respon-
siveness to environmental conditions, making discussions of life-history adapta-
tions rather pointless (Stearns 1980, Sweeney 1984, Scharloo 1989, Stearns
1989). Like collembolans (Amelsvoort and Usher 1989), some members of the
Mesostigmata and the Astigmata show phenotypic plasticity (Gerson et al. 1983,
Athias-Binche 1987, KnOlle 1991), such that development time and fecundity
can exhibit r- or K-attributes, according to quality of food provided.
The multiplicity of clones found in natural populations of thelytokous oribatid
mite species (Norton and Palmer 1991, Palmer and Norton 1992) can provide
us with fixed genotypes for testing responses to differences in resources and
environmental variables. Using thelytokous mites, plasticity can be examined in
both colonizing species (e.g. brachypyline species in which thelytoky is probably
recently derived) and those characteristic of more stable habitats (e.g. many
Desmonomata in which thelytoky is plesiotypic).
Knowledge of clonal composition, which is not difficult to obtain, would have
been beneficial in two interesting recent studies. One (Fujikawa 1988) examined
long-term changes in a population of the colonizing thelytokous species Tecto-
cepheus velatus during gradual site improvement in a field previously farmed
with conventional methods. According to the data (her Fig. 4) this popUlation
may have changed from univoltine to bivoltine, or at least developed a second
oviposition period. Was this due to clonal selection, or the addition of another
clone? Or does it reflect phenotypic plasticity in one or more original clones,
such that voltinism is related to environmental quality? The latter is not unreason-
able, and food-based changes in voltinism have been suggested in insects
(Sweeney 1984). Vera and Berthet (1988) found popUlations of the thelytokous
Platynothrus peltifer from two forest types to differ in certain developmental
parameters. An analysis of clonal structure could have supported their claims of
heritable, adaptive differences.
124 / R. A. Norton
One wholly thelytokous family would be an excellent choice for study. The
Trhypochthoniidae contains an interesting array of genera that exhibit a wide
range of life styles, including Archegozetes (colonizers of disturbed habitats in the
tropics, with relatively short life cycles and high clutch sizes), Trhypochthonius
(mostly temperate, noncolonizing species with moderate life-history parameters),
and M ucronothrus (long-lived inhabitants of springs and other oligotrophic fresh-
water) (see Norton and Palmer 1991 and included references). The family is of
added interest because of probable close phylogenetic ties with the Astigmata.
Lastly, such studies will not significantly advance our understanding of life-
history evolution in the absence of a phylogenetic framework. Carefully con-
structed hypotheses on phylogenetic relationships of oribatid mites, encompassing
at least the common families, will be essential.
8. Conclusions
To suggest that oribatid mites never exhibit adaptive life-history traits would be
unreasonable, but most current claims of adaptation are not convincing. Studies
initiated with the intent of finding adaptive demographic traits or "strategies"
usually fail to address the possibility that beneficial traits are plesiotypic. In the
terminology of Gould and Vrba (1982), authors usually do not distinguish between
adaptations (apotypic traits developed in response to selective pressures in the
environment under study) and exaptations ("preadaptive" plesiotypic traits ac-
crued before the current environmental relationship existed). The general suite
of life-history traits exhibited by oribatid mites (slow development, low fecundity,
iteroparity and long adult life) seems well suited to life in many different environ-
ments, but all may result directly or indirectly from a low metabolic rate.
The Astigmata exhibit the only significant deviations from these traits. As a
major radiation from oribatid mites (and hence belonging to the oribatid mites in
the cladistic sense), they often have both life cycles and demographic traits that
seem adaptive. Compared to their close relatives (the Trhypochthonioidea), life
histories seem little constrained by metabolic rate.
Acknowledgments
Research leading to the development of ideas expressed in this paper was

supported by a grant from the National Science Foundation (BSR 8415747). I
am grateful to several colleagues for their helpful comments on the manuscript:
Drs. F. Athias-Binche (Laboratoire Arago, Banyuls sur Mer, France), V. M.
Behan-Pelletier (Biosystematics Research Centre, Ottawa), N. Fashing (College
of William and Mary, Williamsburg), M. Luxton (Liverpool Polytechnic, Liv-
erpool, England) and M. J. Mitchell (S.U.N.Y.-C.E.S.F., Syracuse).
References
Akimov, I. A. and A. V. Yastrebtsov. 1987. Morphology of certain organ systems of the

oribatid mite Nothrus palustris (Oribatei, Nothroidae). In: Soil Fauna and Soil Fertility
(B. R. Strigatova ed.). "Nauka", Moscow. Pp. 534-538.
Alberti, G. 1973. Ernahrungsbiologie und Spinnvermogen der Schnabelmilben (Bdellidae,
Trombidiformes). Z. Morphol. Tiere 76:285-338.
Amelsvoort, P. A. M. van and M. B. Usher. 1989. Egg production related to food
quality in Folsomia candida (Collembola: Isotomidae): effects on life history strategies.
Pedobiologia 33:61-66.
Anderson, 1. M. 1975a. Succession, diversity and trophic relationships of some soil
animals in decomposing leaf litter. 1. Anim. Ecol. 44:475-95.
Anderson, J. M. 1975b. The enigma of soil animal species diversity. In: Proc. Vth Int.
Colloq. Soil Zool. (1. Vanek ed.). W. Junk Pub!., The Hague. Pp. 51-58.
Anderson, J. M. 1978a. Inter- and intra-habitat relationships between woodland Crypto-
stigmata species diversity and the diversity of soil and litter microhabitats. Oecologia
32:341-8.
Anderson, J. M. 1978b. Competition between two unrelated species of soil Cryptostigmata
(Acari) in experimental microcosms. 1. Animal Ecol. 47:787-803.
Aoki, J.-i. 1967. Microhabitats of oribatid mites on a forest floor. Bull. Nat. Sci. Mus.
(Tokyo) 10:135-138.
Arlian, L. G. and T. A. Woolley. 1970. Observations on the biology of Liacarus cidarus
(Acari: Cryptostigmata, Liacaridae). 1. Kans. Entomol. Soc. 43:297-301.
Athias-Binche, F. 1985. Analyse demographique des Uropodides (Arachnides: Anactino-
triches) de la hetraie de la Massane, France. Pedobiologia 28:225-253.
Athias-Binche, F. 1987. Signification adaptative des differents types de developpements
postembryonnaires chez les Gamasides (Acariens, Anactinotriches). Can. 1. Zool.
65: 1299-1310.
Athias-Binche, F. 1989. Polymorphismes et heteromorphies chez les acariens, et la notion
de stase selon Grandjean. In: L'Ontogenese et Ie Concept de Stase Chez les Arthropodes
(H. M. Andre and J.-C. Lions eds.). Agar Pub!., Wavre, Belgium. Pp. 41-57.
Athias-Binche, F. and N. A. Fernandez. 1986. Analyse demographique d'une population
d'Hydrozetes lemnae Coggi, Acarien Oribate infeode a la lentille d'eau Lemna gibba
L. en Argentine. 2. Les relations predateur/proie. Zool. lahrb. Syst. 113:229-249.
Baumler, W. 1970. Zur Morphologie, Biologie und Okologie von Hermannia gibba
(C. L. Koch) (Acarina: Oribatei) unter Beriicksichtigung einiger Begleitarten. II. Z.
angew. Entomol. 66:337-62.
Beck, L. 1969. Zum jahreszeitlichen Massenwechsel zweiger Oribatidenarten (Acari) im
neotropischen Uberschwemmungswald. Zool. Anz. (Suppl.) 32:535-40.
Beck, L. 1972. Der Einfluss der jahresperiodische Uberflutungen auf den Massenwechsel
der Bodenarthropoden im zentral-amazonischen Regenwaldgebiet. Pedobiologia
12:133-148.
126 / R. A. Norton
Beckmann, M. 1988. The development of soil mesofauna in a ruderal ecosystem as

influenced by reclamation measures 1. Oribatei (Acari). Pedobiologia 31:391-408.
Behan-Pelletier, V. M. 1988. Redefinition of Zachvatkinibates (Acari: Mycobatidae), with
description of a new species and immatures of Z. maritimus Shaldybina 1973. Can.
Entomol. 120:797-813.
Behan-Pelletier, V. M. 1989. Limnozetes (Acari: Oribatida: Limnozetidae) of Northeastern
North America. Can. Entomol. 121:453-506.
Behan-Pelletier, V. M. and S. B. Hill. 1983. Feeding habits of 16 species of Oribatei
(Acari) from an acid peat bog, Glenamoy, Ireland. Rev. Ecol. Bioi. Sol 20:221-268.
Bell, G. 1982. The Masterpiece of Nature. Univ. Calif. Press, Berkeley. Pp. 635.
Bellido, A. 1979. Development postembryonnaire de Carabodes willmanni Bernini 1975
(Acari, Oribatei). Acarologia 20:419-32.
Bellido, A. 1990. Characteristiques biodemographiques d'un acarien oribate (Carabodes
willmann i) des pelouses xerophiles. Can. J. Zool. 68:2221-2229.
Bernini, F. and R. Nannelli. 1982. Notulae Oribatologicae XXVI. Contribution to the
knowledge of the genus Cepheus (Oribatida, Acarida) in Italy. Redia 65:155-188.
Berthet, P. 1964. Field study of the mobility of Oribatei (Acari) using radioactive tagging.
J. Anim. Ecol. 33:443-449.
Bhattacharya, T., V. C. Joyand and S. Joy. 1978. Studies on the effect of temperature on
the development of Oppia nodosa Hammer (Acari: Cryptostigmata: Oppiidae). Entomon
3:149-155.
Block, W. 1977. Oxygen consumption of the terrestrial mite Alaskozetes antarcticus
(Acari: Cryptostigmata). 1. Exp. Biol. 68:69-88.
Block, W. 1980. Survival strategies in polar terrestrial arthropods. Biol. 1. Linn. Soc.
14:29-38.
Block, W. and S. R. Young. 1978. Metabolic adaptations of Antarctic terrestrial micro-
arthropods. Comp. Biochem. Physiol. 61 A:363-368.
Burford, D. A., Jr. 1976. Morphology and life history of Hydrozetes bushnelli n.sp.
(Oribatei, Hydrozetidae). Ph.D. dissertation, Univ. Colorado, Boulder, CO. 127 Pp.
Burn, A. J. 1986. Feeding rates of the Cryptostigmatid mite Alaskozetes antarcticus. Br.
Antarct. Surv. Bull. 71:11-18.
Cancela da Fonseca, 1. P. 1980. Quelques approches analytiques en dynamique des
populations edaphiques (Acariens Oribates). Rev. Ecol. Biol. Sol 17:445-447.
Cannon, R. 1. C. 1987. Effects of low-temperature acclimation on the survival and cold
tolerance of an Antarctic mite. 1. Insect Physiol. 33:509-521.
Cannon, R. 1. C. and W. Block. 1988. Cold tolerance of microarthropods. Bioi. Rev.
Camb. Philos. Soc. 63:23-77.
Cole, L. C. 1954. The population consequences of life history phenomena. Q. Rev. Bioi.
29:103-137.
Covarrubias, R. 1968. Some observations on Antarctic Oribatei (Acarina). Liochthonius
australis sp.n. and two Oppia ssp.n. Acarologia 10:313-356.
Crossley, D. A., Jr. 1977. Oribatid mites and nutrient cycling. In: Biology ofOribatid
Mites (D. L. Dinda1 ed.). SUNY-CESF, Syracuse. Pp. 71-85.
Danks, H. V. 1981. Arctic arthropods. A review of Systematics and Ecology with Particu-
lar Reference to the North American Fauna. Entomol. Soc. Canada, Ottawa. 608 pp.
Dybas, H. S. 1966. Evidence for parthenogenesis in the featherwing beetles, with a
taxonomic review of a new genus and eight new species (Coleoptera: Ptiliidae). Fieldi-
ana Zool. 51:11-12.
Fain, A. and A. Herrin. 1978. La pre1arve chez les astigmates (Acari). Acarologia 20:566--
571.
Fashing, N. J. 1977. The resistant tritonymphal instar and its application in the population
dynamics of Naiadacarus arboricolus Fashing, a mite restricted to water-filled treeholes
(Acarina: Acaridae). Am. Midi. Nat. 95:337-346.
Fernandez, N. A. and F. Athias-Binche. 1986. Analyse demographique d'une population
d' Hydrozetes lemnae Coggi, Acarien Oribate infeode a la lentille d'eau Lemna gibba
L. en Argentine. I. Methodes et techniques, demographie d'H. lemnae comparaisons
avec d'autres Oribates. Zool. lahrb. Abt. Syst. Oekol. Geogr. Tiere 113:213-228.
Fujikawa. T. 1974. Comparison among oribatid faunas from different microhabitats in
forest floors. lap. l. Appl. Entomol. Zool. 9:105-114.
Fujikawa. T. 1987. Biology of Oribatula sakamorii Aoki, a dominant species of the
oribatid fauna in nature farming field. In: Soil Fauna and Soil Fertility-Proc. 9th Int.
Congr. Soil Zool. (B. R. Strigatova ed.). "Nauka," Moscow. Pp. 544--552.
Fujikawa. T. 1988. Biology of Tectocepheus velatus (Michael) and T. cuspidentatus
Kniille. Acarologia 29:307-315.
Gerson, U., S. Capua and D. Thorens. 1983. Life history and life tables of Rhizoglyphus
robini Claparede (Acari: Astigmata: Acaridae). Acarologia 24:439-448.
Gilyarov, M. S. 1982. The ecological role of parthenogenesis. Adv. Mod. Bioi. (Moscow)
93:10-22. (In Russian).
Godfray, H. C. J. 1987. The evolution of clutch size in invertebrates. In: Oxford Surveys
in Evolutionary Biology, Vol. 4 (P. H. Harvey and L. Partridge eds.). Oxford Univ.
Press, NY. Pp. 117-154.
Gould, S. J. and E. S. Vrba. 1982. Exaptation-a missing term in the science of form.
Paleobiology 8:4--15.
Gourbiere, F., J.-c. Lions and R. Pepin. 1985. Activite et developpement d'Adoristes
ovatus (C. L. Koch, 1839) (Acarien, Oribate) dans les aiguilles d'Abies alba Mill.
Relations avec la decomposition et les microflores fongiques. Rev. Ecol. Bioi. Sol
22:57-73.
Grandjean, F. 1941. Statistique sexuelle et parthenogenese chez les Oribates (Acariens).
C. R. Seances Acad. Sci. 212:463-467.
Grandjean, F. 1948. Sur les Hydrozetes (Acariens) de I'Europe occidentale. Bull. Mus.
nat. Hist. natur. 20:328-335.
Grandjean, F. 1954. Observations sur les Oribates (31e serie). Bull. Mus. nat. Hist. natur.
26:582-589.
128 I R. A. Norton
Grandjean, F. 1956a. Observations sur les Oribates (33e serie). Bull. Mus. nat. Hist.
natur.28:111-118.
Grandjean, F. 1956b. Observations sur les Galumnidae (Ire serie). (Acariens, Oribates).
Rev. Fr. Entomol. 23:137-146.
Grandjean, F. 1961. Les Amerobelbidae (Oribates) (Ire serie). Acarologia 3:303-343.
Grandjean, F. 1962. Prelarves d'Oribates. Acarologia 4:423-439.
Grandjean, F. 1969. Considerations sur Ie c1assement des Oribates. Leur division en 6
groupes majeurs. Acarologia 11: 127-153.
Grishina. L. G. 1991. Length of the life cycle of oribatid mites (Sarcoptiforrnes, Oribatei).
Sib. Bioi. Zh. 3:37-47. (In Russian).
Haarlov, N. 1960. Microarthropods from Danish soils. Ecology, phenology. Oikos (Suppl)
3:1-176.
Haq, M. A. 1978. Breeding biology of oribatid mites. In: Soil Biology and Ecology in
India (c. A. Edwards and G. K. Veeresh eds.). Univ. Agric. Sci., Techn. Ser. 22,
Bangalore. Pp. 145-151.
Haq, M. A. and C. Adolph. 1981. Spermatophore deposition and transfer in Pelokylla
malabarica (Acari: Oribatei). Entomon 6: 135-141.
Haq, M. A. and 1. D. Konikkara. 1988. Microbial associations in xylophagous oribatids.
In: Progress in Acarology, Vo!' 1 (G. P. ChannaBassavan and C. A. Viraktamath eds.).
Oxford and IBH Pub!. Co. Pvt. Ltd., New Delhi. Pp. 469-474.
Haq, M. A., K. Sheela and P. Neena. 1991. Ovoviviparity in oribatid mites. In: Advances
in Management and Conservation of Soil Fauna (G. K. Veeresh, D. Rajagopal and
C. A. Viraktamath eds.). Oxford and IBH Pub!. Co. Pvt. Ltd., New Delhi.
Hammer, M. 1972. Microhabitats of oribatid mites on a Danish woodland floor. Pedobio-
logia 12:412-423.
Harding, D. J. L. and R. A. Stuttard. 1974. Microarthropods. In: Biology of Plant Litter
Decomposition (c. H. Dickinson and G. J. F. Pugh eds.). Academic Press, NY. Pp.
489-532.
Hartenstein, R. 1962. Soil Oribatei. V. Investigations on Platynothrus peltifer (Acarina:
Camisiidae). Ann. Entomol. Soc. Am. 55:709-713.
Hom, H. 1978. Optimal tactics of reproduction and life-history. In: Behavioural Ecology:
an evolutionary Approach (J. R. Krebs and N. B. Davies eds.). Blackwell Sci. Pub!.,
Boston. Pp. 411-429.
Jacot, A. P. 1933. Aparity among the Oribatidae (Acarina). Can. Entomol. 65:263-64.
Johnson, K. 1983. The ontogeny and descriptive anatomy of Hydrozetes lemnae (Coggi)
(Acari: Oribatei: Hydrozetidae). Thesis, Univ. Kansas, Lawrence, KS. Pp. 57.
Kaneko, N. 1989. Life histories of four oribatid mite species in a mull type soil in a cool
temperate forest in Japan. Pedobiologia 33:117-126.
Kniille, W. 1991. Life-cycle strategies in unpredictably varying environments: genetic
adaptations in a colonizing mite. In: The Acari: Reproduction, Development and Life-
history Strategies (R. Schuster and P. W. Murphy eds.). Chapman and Hall, London.
Pp.51-55.
Krantz, G. W. and E. E. Lindquist. 1979. Evolution of phytophagous mites ('lcari).

Annu. Rev. Entomol. 24:121-158.
Krivolutsky, D. A. and A. Ya. Druk. 1986. Fossil oribatid mites. Annu. Rev. Entomol.
31 :533--45.
Lange, A, P. 1960. The prelarva of mites of the order Acariformes and its peculiarities
in palaeacarids (Palaeacariformes). Zool. Zh. 39:1819-1834. (In Russian).
Lebrun, P. 1970a. Ecologie et biologie de Nothrus palustris (c. L. Koch 1839) 3eme
note: Cycle de vie. Acarologia 12:193-207.
Lebrun, P. 1970b. Ecologie et biologie de Nothrus palustris (c. L. Koch 1839). (Acarien,
Oribate). IV. Survivance-econdite-action d'un predateur. Acarologia 12:827-848.
Lebrun, P. 1971. Ecologie et biocenotique de quelques peuplements d' arthropodes edaph-
iques. Inst. R. Sci. Nat. Belg. Mem. 165:1-203.
Lebrun, P. 1977. Comparaison des effets des temperatures constantes ou variables sur la
duree de developpement de Damaeus onustus (Acarina: Oribatei). Acarologia 19: 136-
143.
Lebrun, P. and M. van Ruymbeke. 1971. Interet ecologique de la relation entre la
temperature et la duree de developpement des Oribates. Acarologia 13:176-185.
Lebrun, P., G. Van Impe, D. DeSaint Georges-Gridelet, G. Wauthy and H. M. Andre.
1991. The life strategies of mites. In: The Acari: Reproduction, Development and Life-
pp.3-22.
Lions, J.-C. 1973. Quelques prelarves nouvelles d'oribates. Acarologia 15:356-370.
Lions, J. -c. 1982. Statistique sexuelle chez deux formes d' oribates proches de Quadroppia
quadricarinata (Michael 1885). Acarologia 23:373-389.
Lions, J. -c. and F. Gourbiere. 1988. Populations adultes et immatures d' Adoristes ovatus
(Acarien, Oribate) dans 1es aiguilles de la litiere d'Abies alba. Rev. tcol. Bioi. Sol
25:343-352.
Luxton, M. 1964. Some aspects of the biology of salt-marsh Acarina. Acarologia (jasc.
h.s.) 6:172-182.
Luxton, M. 1967. The zonation of salt marsh Acarina. Pedobiologia 7:55-66.
Luxton, M. 1975. Studies on the oribatid mites of a Danish beech wood soil. II. Biomass,
calorimetry, and respirometry. Pedobiologia 15:161-200.
Luxton, M. 1979. Food and energy processing by oribatid mites. Rev. tcol. Bioi. Sol
16: \03-111.
Luxton, M. 1981 a. Studies on the oribatid mites of a Danish beech wood soil. IV.
Developmental biology. Pedobiologia 21 :312-340.
Luxton, M. 1981 b. Studies on the oribatid mites of a Danish beech wood soil. VI. Seasonal
population changes. Pedobiologia 21:387--409.
Lynch, M. 1984. Destabilizing hybridization, general-purpose genotypes and geographic
parthenogenesis. Q. Rev. Bioi. 59:257-290.
MacArthur, R. H. and E. O. Wilson. 1967. The Theory of Island Biogeography. Princeton
Univ. Press, Princeton, NJ. 203 pp.
130 I R. A. Norton
MacLean, S. F. 1975. Ecological adaptations of tundra invertebrates. In: Physiological

Adaptation to the Environment (F. J. Vernberg ed.). Intext Educ. Publ., NY. Pp. 269-
300.
Madge, D. S. 1964. The water relations of Belba geniculosa Oudms. and other species
of oribatid mites. Acarologia 6:199-223.
Marshall, V. G., R. M. Reeves and R. A. Norton. 1987. Catalogue of the Oribatida
(Acari) of continental United States and Canada. Mem. Entomol. Soc. Can. No. 139.
Martin, M. M. 1987. Invertebrate-Microbial Interactions. Ingested Fungal Enzymes in
Arthropod Biology. Comstock Publ. Assoc., Ithaca, NY. Pp. 148.
Michael, A. D. 1884 (1883). British Oribatidae, Vol. 1. R. Soc., London. Pp. 1-336,
pI. 1-24.
Mitchell, M. J. I 977a. Population dynamics of oribatid mites (Acari, Cryptostigmata) in
an aspen woodland soil. Pedobiologia 17:305-319.
Mitchell, M. J. 1977b. Life history strategies of oribatid mites. In: Biology of Oribatid
Mites (D. L. Dindal ed.). SUNY-CESF, Syracuse. Pp. 65-69.
Mitchell, M. J. 1979a. Effects of physical parameters and food resources on oribatid mites
in forest soils. In: Recent Advances in Acarology, Vol. I (1. G. Rodriguez ed.).
Academic Press, NY. Pp. 585-592.
Mitchell, M. 1. 1979b. Energetics of oribatid mites in an aspen woodland soil. Pedobio-
logia 17:305-319.
Mitchell, M. 1. and D. Parkinson. 1976. Fungal feeding ofOribatid mites (Acari: Crypto-
stigmata) in an aspen woodland soil. Ecology 57:302-312.
Muraoka, M. and N. Ishibashi. 1976. Nematode-feeding mites and their feeding behavior.
Appl. Entomol. Zool. 11:1-7.
Murphy, P. W. and A. N. Balla. 1973. The bionomics of Humerobates rostrolamellatus
Grandjean (Cryptostigmata-Ceratozetidae) on fruit trees. In: Proc. 3rd Int. Congr.
Acarol., Prague, 1971. pp. 97-104.
Nannelli, R. 1975. Osservazioni sulla biologia di Oppia concolor in condizioni sperimen-
tali di allevamento. Redia 56: 111-116.
Newell, I. M. 1945. Hydrozetes Berlese (Acari, Oribatoidea): The occurrence of the genus
in North America, and the phenomenon of levitation. Trans. Conn. Acad. Arts Sci.
36:253-68, pis. 1-3.
Norton, R. A. 1980. Observations on phoresy in oribatid mites (Acari: Oribatei). Int. 1.
Acarol. 6:121-130.
Norton, R. A. 1983. Redefinition of Mochloribatula (Acari: Mochlozetidae), with new
species, recombinations and notes on plant associations. Acarologia 24:449-464.
Norton, R. A. 1984. Monophyletic groups in the Enarthronota (Sarcoptiformes). In:
Acarology VI, Vol. 1 (D. A. Griffiths and C. E. Bowman eds.). Ellis Horwood Ltd.,
Chichester. Pp. 233-240.
Norton, R. A. 1985. Aspects of the biology and systematics of soil arachnids, particularly
saprophagous and mycophagous mites. Quaest. Entomol. 21:523-541.
Norton, R. A. and M. C. MacNamara. 1976. The common newt (Notophthalmus virides-

cens) as a predator of soil mites in New York. J. Ga. Entomol. Soc. 11:89-93.
Norton, R. A. and D. Y. Sillman. 1985. Impact of oily waste application on the mite
community of an arable soil. Exp. Appl. Acarol. 1:287-305.
Norton, R. A., P. M. Bonamo, J. D. Grierson and W. M. Shear. 1988a. Oribatid mite
fossils from a terrestrial Devonian deposit near Gilboa, New York State. J. Paleontol.
62:259-269.
Norton, R. A., D. D. Williams, I. D. Hogg and S. C. Palmer. 1988b. Biology of the
oribatid mite Mucronothrus nasalis (Acari: Oribatida: Trhypochthoniidae) from a small
coldwater springbrook in eastern Canada. Can. J. Zool. 66:622-629.
Norton, R. A., S. C. Palmer and H-f. Wang. 1988c. Parthenogenesis in Nothridae and
related groups. In: Progress in Acarology, Vol. I (G. P. ChannaBassavan and C. A.
Viraktamath eds.). Oxford and IBH Publ. Co. Pvt. Ltd., New Delhi. Pp. 255-259.
Norton, R. A., W. C. Welbourn and R. D. Cave. 1988d. First records of Erythraeidae
parasitic on oribatid mites (Acari, Pro stigmata: Acari, Oribatida). Proc. Entomol. Soc.
Wash. 90:407-410.
Norton, R. A. and S. C. Palmer. 1991. The distribution, mechanisms and evolutionary
significance of parthenogenesis in oribatid mites. In: The Acari: Reproduction, Develop-
ment and Life-history Strategies (R. Schuster and P. W. Murphy eds.). Chapman and
Hall, London. pp. 107-136.
Norton, R. A. and V. M. Behan-Pelletier. 1991. Calcium carbonate and calcium oxalate
as cuticular hardening agents in oribatid mites (Acari: Oribatida). Can. J. Zool. 69: 1504-
1511.
Noy-Meir, I. 1973. Desert ecosystems: environment and producers. Annu. Rev. Ecol.
Syst.4:25-51.
OConnor, B. M. 1982. Evolutionary ecology of astigmatid mites. Annu. Rev. Entomol.
27:385-409.
OConnor, B. M. 1984. Phylogenetic relationships among higher taxa in the Acariforrnes,
with particular reference to the Astigmata. In: Acarology VI, Vol. 1 (D. A. Griffiths
and C. E. Bowman eds.). Ellis Horwood Ltd., Chichester. Pp. 19-27.
Palmer, S. C. and R. A. Norton. 1990. Further experimental proof ofthelytokous partheno-
genesis in oribatid mites (Acari: Oribatida: Desmonomata). Exp. Appl. Acarol. 8: 149-
159.
Palmer, S. C. and R. A. Norton. 1991. Taxonomic, geographic, and seasonal distribution
of thelytokous parthenogenesis in Desmonomata (Acari: Oribatida). Exp. Appl. Acarol.
12:67-81.
Palmer, S. C. and R. A. Norton. 1992. Genetic diversity in thelytokous oribatid mites
(Acari: Acariformes: Desmonomata). Biochem. System. Ecol. 20:219-231.
Park, O. 1947. Observations on Batrisodes (Coleoptera: Pselaphidae), with particular
reference to the American species east of the Rocky Mountains. Bull. Chic. Acad. Sci.
8:45-132, II pIs.
Parker, S. B. 1982. Synopsis and Classification of Living Organisms, Vol. 2. McGraw-
Hill, NY.
132 / R. A. Norton
Pauly, F. 1956. Zur Biologie einige Belbiden und zur Funktion ihrer Pseudostigmatischen
Organe. Zool. lahrb. Abt. Syst. Oekol. Geogr. Tiere 84:275-328.
Peckham, V. 1967. Studies of the mite Alaskozetes antarcticus (Michael). Antarct. 1.
U.S. 2:196--197.
Pianka, E. R. 1970. On r- and K-selection. Am. Nat. 104:592-597.
Purrini, K. 1980. On the incidence and distribution of parasites of soil fauna of mixed
coniferous forests, mixed leaf forests, and pure beech forests of lower Saxony. West
Germany. In: Soil Biology as Related to Land Use Practices (D. L. Dindal ed.). U.S.
Environ. Protection Agency, Washington, DC. Pp. 561-582.
Reddy, A. S., R. Kumar and S. N. Mathur. 1978. Studies on the biology of Galumna
fiabellifera Hammer, 1958 and its role as fungal spore carrier. In: Soil Biology and
Ecology in India. (C. A. Edwards and G. K. Vereesh eds.). Univ. Agri. Sci., Tech.
Ser. 22. Hebbal, Bangalore. Pp. 134--143.
Riha, G. 1951. Zur Oko10gie der Oribatiden in Kalksteinboden. Zool. lahrb. Abt. Syst.
Oekol. Geogr. Tiere 80:407--450.
Ring, R. A. and D. Tesar. 1981. Adaptations to cold in Canadian arctic insects. Cryobiol-
ogy 18: 199-211.
Rockett, C. L. 1980. Nematode predation by oribatid mites (Acari: Oribatida). Int. 1.
Acarol. 6:219-224.
Rockett, C. L. and J. P. Woodring. 1966a. Biological investigations on a new Ceratozetes
and Pergalumna (Acarina: Cryptostigmata). Acarologia 3:511-520.
Rockett, C. L. and J. P. Woodring. 1966b. Oribatid mites as predators of soil nematodes.
Ann. Entomol. Soc. Am. 59:669-671.
Rodriguez, J. G. and Z. A. Stepien. 1973. Biology and population dynamics of Calogly-
phus berlesei (Michael) (Acarina: Acaridae) in xenic diet. 1. Kans. Entomol. Soc.
46:176--183.
Ryabinin, N. A. and A. N. Pan'kov. 1987. The role of parthenogenesis in the biology of
armored mites. Ekologiya 1987:62-64. (In Russian).
Saichuae, P., U. Gerson and Y. Henis. 1972. Observations on feeding and life history of
the mite Nothrus biciliatus (Koch). Soil Bioi. Biochem. 4:155-164.
Scharloo, W. 1989. Developmental and physiological aspects of reaction norms. Biosci-
ence 39:465-471.
Schatz, H. 1983. Uber lebensrate von Oromurcia sudetica Willmann (Acari, Oribatei)
von einer alpinen Wiese Tirols (ObergurgL Zentralalpen). Zool. lahrb. Abt. Syst.
Oekol. Geogr. Tiere 110:97-109.
Schatz, H. 1985. The life cycle of an alpine oribatid mite, Oromurcia sudetica Willmann.
Acarologia 26:95-100.
Schenker, R. 1984. Spatial and seasonal distribution patterns of oribatid mites (Acari:
Oribatei) in a forest soil ecosystem. Pedobiologia 27:133-150.
Schenker, R. 1986. Population dynamics of oribatid mites (Acari: Oribatei) in a forest
soil ecosystem. Pedobiologia 29:239-246.
Schmid, R. 1988. Morphologische Anpassungen in einem Rauber-Beute-System: Amei-
Evolutionary Aspects ofOribatid Mite Life-Histories I 133
senkiifer (Scydmaenidae, Staphylinoidea) und gepanzerte Milben (Acari). Zool. lahrb.

Abt. Syst. Oekol. Geogr. Tiere 115:207-228.
Schulte, G. and G. Weigmann. 1977. The evolution of the family Ameronothridae (Acari:
Oribatei). II. Ecological aspects. Acarologia 19:167-173.
Schuster, R. 1962. Nachweis eines Paarungszeremoniells bei den Hornmilben (Oribatei).
Naturwissenschaften 49:502-503.
Sengbusch, H. G. 1954. Studies on the life history of three oribatid mites with observations
on other species. Ann. Entomol. Soc. Am. 47:646-67.
Seniczak, S. and o. Stefaniak. 1978. The microftora of the alimentary canal of Oppia
nitens (Acarina, Oribatei). Pedobiologia 18:110-119.
Shereef, G. M. 1970. Observations on the feeding, reproduction and faeces obtained from
oribatids fed on different species of Penicillium and Aspergillus. IV Colloq. Int. Zool.
Sol 1970. Dijon, France.
Shereef, G. M. 1972. Observations on oribatid mites in Laboratory cultures. Acarologia
14:281--291.
Sitnikova, L. G. 1960. Pre larvae of oribatid mites. Parazitol. Sb. 19:220-236. (In
Russian).
Smrz, J. 1989. Reproductive biology of some soil oribatid and acaridid mites (Acari:
Actinedida). In: Regulation of Insect Reproduction IV (M. Tonner, T. Soldan and B.
Bennettova eds.). Academia Praha, Prague.
Solh0y, T. 1975. Dynamics ofOribatei populations on Hardangervidda. In: Fennoscandian
Tundra Ecosystems. Part 2: Animals and Systems Analysis (F. Wielgolaski ed.). Spring-
er-Verlag, Berlin. Pp. 111-116.
Southwood, T. R. E. 1978. Ecological Methods, 2nd ed. Chapman and Hall, London.
Pp. 524.
Stamou, G. P. 1987. A phenological model applied to oribatid mites data. Rev. Ecol.
Bioi. Sol 23:453-460.
Stamou, G. P. 1989. Studies on the effect of temperatures on the demographic parameters
of Achipteria holomonensis (Acari, Oribatida). Acarologia 30:171-180.
Stamou, G., M. Kattoulas, J. P. Cancela da Fonseca and N. S. Margaris. 1981. Observa-
tions on the biology and ecology of Achiptera holomonensis (Acarina, Oribatida).
Stamou, G. P. and M. D. Asikidis. 1989. The effect of density on the demographic
parameters of two oribatid mites. Rev. Eeol. Bioi. Sol 26:321-330.
Stamou, G. P. and S. P. Sgardelis. 1989. Seasonal distribution patterns of oribatid mites
(Acari, Cryptostigmata) in a forest ecosystem. 1. Anim. Ecol. 58:893-904.
Steams, S. C. 1976. Life-history tactics: a review of the ideas. Q. Rev. Bioi. 51:3-47.
Steams, S. C. 1977. The evolution of life history traits: a critique of the theory and a
review of the data. Annu. Rev. Ecol. Syst. 8:145-171.
Steams, S. C. 1980. A new view of life-history evolution. Oikos 35:266-281.
Steams, S. C. 1989. The evolutionary significance of phenotypic plasticity. Bioscience
39:436-471.
134 / R. A. Norton
Stefaniak, O. and S. Seniczak. 1976. The microflora of the alimentary canal of Achipteria
coleoptrata (Acarina, Oribatei). Pedobiologia 16: 185-194.
Stefaniak, O. and S. Seniczak. 1981. The effect of fungal diet on the development of
Oppia nitens (Acari, Oribatei) and on the microflora of its alimentary tract. Pedobiologia
21 :202-210.
Sweeney, B. W. 1984. Factors influencing life-history patterns of aquatic insects. In: The
Ecology of Aquatic Insects (V. H. Resjh and D. M. Rosenberg eds.). Praeger Pub!.
Co., NY. Pp. 56-100.
Taberly, G. 1987. Recherches sur la parthenogenese thelytoque de deux especes d' Acariens
Oribates: Trhypochthonius tectorum (Berlese) et Platynothrus peltifer (Koch). l. Acaro-
logia 28:187-198.
Taberly, G. 1989. L'influence de la temperature sur la duree des differentes stases
immatures des oribates. In: L'Ontogenese et Ie Concept de Stase Chez les Arthropodes
(H. Andre and J.-c. Lions eds.). Agar Pub!., Wavre, Belgium. Pp. 117-122.
Tamm,1. c., H.-W. Mittman and S. Woas. 1984. ZurLandmilbenfaunaeinesjahresperio-
disch trockenfallenden Stauseebodens (Edertalsperre, BRD). Pedobiologia 27:395-
404.
Tarras-Wahlberg, N. 1961. The Oribatei of a central Swedish bog and their environment.
Oikos (Suppl.) 4:1-56.
Thomas, J. O. M. 1979. An energy budget for a woodland population of oribatid mites.
Trave, J. 1963. Ecologie et biologie des Oribates (Acariens) saxico1es et arboricoles. Vie
Milieu (Suppl.) 14:1-267.
Trave, J. 1968. Sur I'existence d'yeux lateraux depigmentes chez Eobrachychthonius
Jacot (Oribate). Acarologia 10:151-158.
Trave,1. 1976. Les prelarves d'Acariens. Mise au point et donnees recentes. Rev. Ecol.
Bioi. Sol 13: 161-171.
Vera, H. and P. Berthet. 1988. Frequence de mue et taux de survie de deux populations
de Platynothrus peltifer (Acari: Oribatidae). Acta Oecol.!Oecol. Gener. 9:281-291.
Walker, N. A. 1965 (1964). Euphthiracaroidea of California Sequoia litter: with a Reclassi-
fication of the Families and Genera of the World (Acarina: Orib.). Fort Hays Studies-
Science Series, No.3. Hays, Kansas. Pp. 154.
Wallwork, J. A. 1962. Sexual dimorphism in the genus Epilohmannia Berl. 1916. Rev.
Zool. Bot. Afr. 65:90--96.
Wallwork, J. A. 1972. Distribution patterns and population dynamics of the micro-
arthropods of a desert soil in southern California. J. Anim. Ecol. 41:291-310.
Wallwork, J. A. 1979. Energetics of soil mites: the experimental approach. In: Proc. 4th
Int. Congr. Acarol. (E. Pifft ed.), Saalfelden, 1974. Akademiai Kiad6, Budapest.
Wallwork, J. A. 1980. Desert soil microarthropods, an "r" selected system. In: Soil
Biology as Related to Land Use Practices (D. L. Dindal ed.). U.S. Environ. Protection
Agency, Washington, DC. Pp. 759-769.
Wallwork, J. A. 1983. Oribatids in forest ecosystems. Annu. Rev. Entomol. 28:109-130.
Wallwork, J. A., B. W. Kamill and W. G. Whitford. 1984. Life styles of desert litter-
dwelling microarthropods, a reappraisal based on the reproductive behavior of cryptos-
tigmatid mites. S. Afr. J. Sci. 80:163-169.
Wallwork, J. A., M. MacQuitty, S. Silva and W. G. Whitford. 1986. Seasonality of
some Chihuahuan Desert soil oribatid mites (Acari: Cryptostigmata). J. Zool. (Lond.)
208:403-416.
Walter, D. E. and E. K. Ikonen. 1989. Species, guilds, and functional groups: taxonomy
and behavior in nematophagous arthropods. J. Nematol. 21:315-327.
Walter, D. E., 1. C. Moore and S. J. Loring. 1989. Symphylella sp. (Symphyla: Scolopen-
drellidae) predators of arthropods and nematodes in grassland soils. Pedobiologia
33:113-116.
Wanntorp, H-E., D. R. Brooks, T. Nilsson, S. Nylin, F. Ronquist, S. C. Steams and N.
Wedell. 1990. Phylogenetic approaches in ecology. Oikos 57:119-132.
Webb, N. R. 1989. Observations on the life cycle of Steganacarus magnus (Acari:
Cryptostigmata). Pedobiologia 33:293-299.
Weigmann, G. 1975. Labor-und Freilanduntersuchungen zur Generationsdauer von Ori-
batiden (Acari:Oribatei). Pedobiologia 15: 133-148.
West, C. 1982. Life histories of three species of sub-antarctic oribatid mites. Pedobiologia
23:59-67.
White, M. J. D. 1978. Modes of Speciation. Freeman, San Francisco.
Willmann, C. 1933. Oribatei (Acari) gesammelt von des Deutschen Limnologischen
Sunda-Expedition 2. Nachtrag. Arch. Hydrobiol. Suppl. 1/, Trap. Binnengewiisser
3:597-603.
Wolf, M. M. and C. L. Rockett. 1984. Habitat changes affecting bacterial composition
in the alimentary canal of oribatid mites (Acari: Oribatida). Int. J. Acaral. 10:209-215.
Woodring, J. P. 1965. The biology of five new species of oribatids from Louisiana.
Woodring, J. P. and E. F. Cook. 1962a. The internal anatomy, reproductive physiology
and molting process of Ceratozetes cisalpinus. Ann. Entomol. Soc. Am. 55:164-181.
Woodring, J. P. and E. F. Cook. 1962b. The biology of Ceratozetes cisalpinus Berl.,
Scheloribates laevigatus Koch, and Oppia neerlandica Oudemans with a description of
all stages. Acarologia 4:101-137.
Young, S. R. 1979. Effect of temperature change on the metabolic rate of an Antarctic
mite. J. Compo Physiol. 131 :341-346.
Young, S. R. and W. Block. 1980. Some factors affecting metabolic rate in an Antarctic
mite. Oikos 34:178-185.
6
Life-History Modifications in Astigmatid Mites

Barry M. OConnor
CONTENTS
I. INTRODUCTION
2. HABITAT AND HOST ASSOCIATIONS
2. I Habitat Types
2.2 Habitats Created by Plants and Fungi
2.3 Habitats Created by Animals Through Noninteractive Processes
2.4 Habitats Created by Interaction of Hosts with the Environment
2.4.1 Habitats Created by Insects
2.4.2 Mammal Hosts
2.4.3 Bird Hosts
2.4.4 Habitat Shifts in Nest-inhabiting Astigmatid Mites
3. DEMOGRAPHICS
4. DISPERSAL
4.1 Phoretic Dispersal by Deutonymphs
4.2 Nonphoretic Dispersal by Deutonymphs
4.3 Loss of the Dispersal (Deutonymphal) Morph
4.4 Dispersal of Permanent Parasites
4.5 Dispersal and Adverse Changes in the Environment
5. HOST ASSOCIATIONS
6. EVOLUTION OF PARASITISM
7. SUMMARY
I. Introduction
The Astigmata is a diverse group of acariform mites specialized for exploiting

spatially or temporally restricted habitats. This natural lineage is hypothesized to
have arisen from within the "glandulate" oribatid mites (OConnor 1984a; Norton,
this volume) through paedomorphic modifications of the adult morphology and
through extreme morphological and behavioral modification of the deutonymphal
instar. This modified deutonymph, termed "hypopus" in older literature, is spe-
136
Life-History Modifications in Astigmatid Mites / 137
cialized for dispersal and resisting adverse environmental conditions (OConnor

1982a). Dispersal is typically accomplished by phoretic association with an insect
or other arthropod or with a vertebrate, which carries the deutonymph to another
suitable habitat patch. Phoresy in the Astigmata has recently been reviewed by
Houck and OConnor (1991).
Along with these morphological and behavioral modifications, the lineage of
astigmatid mites has diverged strongly from its closest "oribatid" relatives in a
number of life-history parameters. Related groups of "oribatid" mites typically
inhabit stable environments, have long generation times and adult life spans,
disperse over relatively short distances as adults and accomplish sperm transfer
via spermatophores deposited on the substrate (see Norton, this volume). In
contrast to these typically "K-selected" traits, most astigmatid mites live in
ephemeral habitats, have short generation times and adult life spans, disperse
over relatively long distances as deutonymphs, and achieve sperm transfer by
direct copulation.
Brooks (1985) pioneered a method for analyzing the evolution of ecological
associations such as commensalism and parasitism which are exhibited by most
species of astigmatid mites. This method entails a phylogenetic analysis of the
organisms under study and a subsequent superposition of ecological associations
on the resulting phylogenetic tree. Evolutionary shifts in ecology, behavior and
life history can be tracked using this method. The discussions presented here are
based on phylogenetic analyses of family and subfamily relationships among
the non-psoroptidid Astigmata presented in OConnor (1981). The family-level
cladograms were transformed into a phyletic ally sequenced Linnaean classifica-
tion which was presented in OConnor (1982b) and is followed here.
In this paper I will review the habitat types colonized and exploited by astig-
matid mites, discuss some of the life-history parameters exhibited by representa-
tive species, and discuss the evolution of these traits and the shift from commen-
salistic to parasitic associations in the group.
2. Habitat and Host Associations
Astigmatid mites have successfully colonized and specialized on an incredible

variety of microhabitat types, most of which are spatially restricted (patchy) and/
or temporally restricted (ephemeral). Although I will not attempt to enumerate
all habitat types exploited by astigmatid mites, I will provide some overview of
the types of habitats used, the diversity and origin of the mites found therein, and
the resources used by the mites. Patchy or ephemeral habitats exploited by
astigmatid mites typically arise through biotic processes, or through interaction
of both physical and biotic processes. Patchy habitats created by purely physical
processes such as sand dunes, rock clefts, ponds, lakes and springs rarely harbor
astigmatid mites. Suitable habitats are formed when concentrations of organic
138 / B. M. OConnor
materials which can serve either directly as food or substrate for microbial or
fungal growth accumulate. Because the ability to disperse directly is limited in
mites, most suitable habitats for astigmatid mites must also be attractive to other
organisms which serve as hosts to phoretic deutonymphs.
2.1 Habitat Types
It is also useful to distinguish between habitat types that are the result of biotic
processes which do not involve modification of the environment by a host (e.g.
growth, death, decay) and those resulting from ongoing interaction between the
host and the environment (e.g. food provisioning, nest building, etc.). Examples
of the first include nonmobile habitats such as flowers, roots, tubers, fungal
fruiting bodies, subcortical spaces, treeholes and other plant cavities, sap flows,
algal mats, dung and carrion. This category also includes mobile habitats, i.e.
the bodies of living animals. The second category includes the nests, burrows,
galleries, refuse piles and food stores of solitary, communal and social insects as
well as birds and mammals, including humans. Life-history patterns of astigmatid
mites which live in these different habitat classes typically differ in the nature,
quality, and degree of specificity of the association with the insect or vertebrate
on which the mite depends for dispersal and/or permanent habitat.
2.2 Habitats Created by Plants and Fungi
Many astigmatid mites inhabit substrates associated with plants or fungi, how-
ever, few occur on such relatively nonpatchy substrates as bark or leaves of living
plants. Some astigmatid mites exploit living plant tissue. For example, species
of Rhizoglyphus (Acaridae) are well known to burrow in and feed on living tissues
of bulbs and tubers. A few taxa include species which can feed on living leaf
tissue although most species living on leaf surfaces are primarily grazers on fungi
growing on the leaves. These taxa include species of Czenspinskia and Oulenzia
(Winterschmidtiidae) and Neotropacarus and some Tyrophagus (Acaridae). In-
florescences serve as habitat for some Carpoglyphus (Carpoglyphidae) and several
undescribed genera of Histiostomatidae. Specialized plant parts which hold water
(phytotelmata) harbor a diversity of taxa of Histiostomatidae, Algophagidae and
Acaridae. Water-filled leaves of two families of pitcher plants are known to
harbor specific genera of Histiostomatidae: Creutzeria, Zwickia and several un-
named genera inhabit the Old World Nepenthaceae, while Sarraceniopus inhabits
the New World Sarraceniaceae. Leafaxils of the Bromeliaceae are habitat for
Bromeliaglyphus, Naiacus and some species of Rhizoglyphus and Schwiebea
(Acaridae) as well as undescribed species of Hormosianoetus (Histiostomatidae).
The histiostomatid mites are presumed to be microbial feeders while the feeding
habits of the Acaridae in these habitats remain unstudied.
Fruiting bodies of fleshy fungi are exploited by some species of Histiostoma
Life-History Modifications in Astigmatid Mites I 139
(Histiostomatidae), Congovidia (Hemisarcoptidae), Rhizo glyphus, Sancassania

and several other undescribed genera of rhizoglyphine Acaridae. Tougher fruiting
bodies of polypore and xylariaceous fungi are inhabited by Rhizoglyphus and
Boletacarus species (Acaridae) and Nanacaroides and some species of Nanacarus
(Hemisarcoptidae). These species tend to specialize either on mycelial tissue or
on spores (OConnor 1984b).
Other vegetative substrates occupied by astigmatid mites include holdfasts of
marine algae which serve as habitat for species of Hyadesiidae and marine
algal mats and halophytic plants or freshwater mosses which harbor species
of Algophagidae (Algophagopsis, Algophagus and Neohyadesia). Based upon
examination of gut contents, these species appear to be primarily algal feeders.
A much greater diversity of taxa is associated with dead and decaying plants
and fungi. Subcortical spaces in decaying tree trunks and logs are inhabited by
several genera of rhizoglyphine Acaridae including Calvoliella, Histiogaster,
Schwiebea and Thyreophagus. Some Histiostomatidae such as Bonomoia and
many Histiostoma species may also be found in decaying wood. Species in these
genera typically live in the rotting wood itself and are not restricted to insect
galleries as are some other taxa. The Acaridae in these habitats are primarily
fungal grazers, while the Histiostomatidae filter microorganisms from wet sub-
strates. Treeholes also provide habitats for a diversity of astigmatid mites. Water
filled treeholes contain species of Naiadacarus (Acaridae), Hormosianoetus (His-
tiostomatidae) and Algophagus and another, undescribed genus of Algophagidae.
These taxa have been the subject of exhaustive studies by Fashing (see Fashing,
this volume) and will not be discussed further here. Treeholes which are not
permanently wet are commonly inhabited by species of Acotyledon, Fagacarus,
Rhizoglyphus, Sancassania, and Schwiebea (Acaridae) and Histiostoma (Histios-
tomatidae). Tree wounds which exude fermenting sap serve as substrates for
Fusohericia and Hericia (Algophagidae) as well as species of Histiostoma and
Sellea (Histiostomatidae). Decaying fungal fruiting bodies are the preferred habi-
tat for Boletoglyphus (Acaridae) and Allocalvolia and Saproglyphus (Winter-
schmidtiidae). The primary diets of all of these species appear to be fungi,
including yeasts.
2.3 Habitats Created by Animals Through Noninteractive Processes
Habitats created by animals through non interactive processes also harbor a diver-
sity of astigmatid mites. Dung produced by individual vertebrates can contain an
extensive community of astigmatid mites including representatives of the families
Acaridae (Sancassania), Histiostomatidae (Ameranoetus, Aphodanoetus, Copro-
nomoia, Fibulanoetus, Glyphanoetus, H istiostoma, Myianoetus, Rhopalanoetus,
Syringanoetus, and probably others), and Winterschmidtiidae (unnamed genus).
Guano accumulations produced by colonies of bats or birds contain unique
communities composed of species of Rosensteiniidae (many genera), Aeroglyphi-
140 / B. M. OConnor
dae (Aeroglyphus and Glycycometus), Histiostomatidae (Glyphanoetus and Histi-

ostoma), Guanolichidae (Guanolichus and Neoguanolichus), Acaridae (Acarus
and Troglocoptes), and Glycyphagidae (G/ycyphagus). Frass generated by the
activities of wood-inhabiting scarabaeid beetles also serves as habitat for Aco-
tyledon and Sancassania species (Acaridae). Vertebrate carrion serves as substrate
for species of Acarus (Acaridae), Pelzneria and Spinanoetus (Histiostomatidae)
in early decay stages, while Lardoglyphus (Lardoglyphidae) species inhabit older
carcasses. These species are primarily fungivores or microorganismal feeders,
but the acarid and lardoglyphid mites may also feed directly on the substrate
material.
The bodies of living animals are permanent habitats for a great diversity of
astigmatid mites. Over half of all nominal genera of Astigmata comprise the
monophyletic group Psoroptidia, most species of which live permanently on or
in the bodies of birds or mammals. Psoroptidid mites are microhabitat specialists,
with many species often coexisting on a single host. Birds provide an exceptional
diversity of microhabitats. The greatest diversity of mite taxa occur on the flight
and tail feathers, living along the rachis, between the barbs or in the spaces
at the bases of the barbs (families Alloptidae, Avenzoariidae, Caudiferidae,
Cheylabididae, Crypturoptidae, Eustathiidae, Fa1culiferidae, Freyanidae, Gabu-
ciniidae, Kramerellidae, Ochrolichidae, Proctophyllodidae, Pterolichidae, Ptilox-
enidae, Rectijanuidae, Thoracosathidae, Vexillariidae, and some Analgidae).
Species of the families Analgidae, Psoroptoididae and Xolalgidae typically live
on plumaceous barbs of contour feathers or at the bases of flight feathers. The
spaces between coverts and flight feathers are the typical habitat for species of
Trouessartiidae. The space within the feather quills serves as habitat to species of
Dermoglyphidae, Gaudoglyphidae, Oconnoriidae, Ptyssalgidae, Syringobiidae,
some Proctophyllodidae and some Pyroglyphidae. Species of Epidermoptidae
live in the superficial layers of the skin and in feather follicles, while species
of Laminosioptidae inhabit deeper, subcutaneous tissues and the follicles of
developing feathers. The respiratory tract of birds is inhabited by species of
Turbinoptidae in the nostrils and Cytoditidae deeper in the trachea, lungs and air
sacs. These species may feed as actual parasites on host skin, pygidial gland
secretions, skin exudates, keratin rich materials from the quills and feather barbs,
or rarely, on blood. Mites living on feather surfaces also commonly ingest detritus
such as fungal spores and algal cells (Dubinin 1951).
The bodies of mammals provide an equally rich source of exploitable microhab-
itats. Species of Atopomelidae, Chirodiscidae and Listrophoridae live on the hair
shafts of small and medium sized mammals. The Lobalgidae consists of species
specialized for the flattened, grooved hairs of Neotropical sloths and spiny rats.
The skin surface of many groups of terrestrial mammals is substrate for species
of Psoroptidae, some of which also enter the ear openings and inhabit the ear
canals. The uniquely modified species of the family Chirorhynchobiidae attach
to the wing membrane edges of Neotropical bats, while species of Myocoptidae
anchor themselves to body hairs while feeding from the skin. Species of the
Rhyncoptidae (including Audycoptidae) live in hair follicles of primates, carni-
vores and rodents, while species of Sarcoptidae actually enter the skin and live
in the epidermal layers of many mammal groups, most notably bats. As in birds,
the respiratory tract is also exploited. Species of Gastronyssidae inhabit the nasal
passages of rodents and bats, while Lemurnyssidae occupy similar habitats in
primates. The Pneumocoptidae consists of a few species which live in the lungs
of rodents. The Gastronyssidae also includes species specialized for living in the
orbits of the eyes and in the stomach of their chiropteran hosts. These mites
exploit similar resources as do the bird associates although none is known to feed
directly on hair proteins. Again, feeding on host blood is rare.
The bodies of birds and mammals are also exploited by other groups of
astigmatid mites not belonging to the Psoroptidia. The ears of large mammals
harbor populations of the genera Auricanoetus, Loxanoetus, Otanoetus and an
undescribed genus (family Histiostomatidae). Some taxa of Rosensteiniidae
(Cheiromelichus, Chiroptoglyphus and some Nycteriglyphus) live permanently
on the skin of their bat hosts. Feeding habits of these species are unstudied, but
the histiostomatids are presumed to be filtering materials from the ear secretions.
Many arthropods are also permanent hosts to astigmatid mites. All species in
the families Canestriniidae and Heterocoptidae and the genus Linobia (Hemisar-
coptidae) live their entire lives on the bodies of many groups of Coleoptera. All
species in these taxa parasitize only adult hosts and tend to be specialized for life
either on the ventral body surface or in the subelytral space. Most of these mites
are presumed to be exudate feeders, but Linobia coccinellae pierces the cuticle
to feed on host hemolymph. Species in several lineages of Rosensteiniidae have
evolved permanent associations with noncoleopterous insects. Species of Rosen-
steinia and one undescribed genus inhabit the bodies of cockroaches (Blattaria)
and are superficially similar to the above mentioned Canestriniidae in morphology
and presumably feeding habits. Species of Micronychites and Micronychitoides
have been collected from earwigs of the genera Arexenia and Xenaria (Dermapt-
era: Arexeniina). Their feeding ecology is unknown. Decapod crustaceans are
host to an unusual group of genera in the family Acaridae. Their distinctive
morphology has led previous workers to recognize this group as a separate family,
Ewingiidae. Species of Ewingia, Hoogstraalacarus and Kanakobia live in the gill
chambers of hermit crabs (Coenobitidae) and fresh-water crabs (Potamonidae).
Species of Askinasia and one undescribed genus live attached to leg or abdominal
setae of hermit crabs. The feeding ecology of these mites is unknown.
2.4 Habitats Created by Interaction of Hosts with the Environment
In contrast to the great diversity of habitat types indicated above as harboring

astigmatid mites, habitats which are created by the activities of other animals
often contain an even greater diversity of these mites.
142 / B. M. OConnor
2.4.1 Habitats Created by Insects
Insects which create habitats exploitable by astigmatid mites include many

Coleoptera and Hymenoptera and the Diaspididae (Homoptera). The tunnels of
wood-boring beetles of the family Passalidae are home to specialized astigmatid
mites such as Kanoetus and Seolianoetus (Histiostomatidae) and Passaloglyphus
and some Sehwiebea species (Acaridae). Galleries constructed by Scolytidae or
Bostrichidae harbor species of Afroealvolia, Wintersehmidtia and related unde-
scribed genera (Winterschmidtiidae), some Histiogaster and Thyreophagus spe-
cies (Acaridae), and some Histiostoma (Histiostomatidae). Several other genera
of Histiostomatidae have been described only as deutonymphs collected from
various other groups of beetles which excavate cavities in wood. Associated with
Tenebrionidae are Kaszabanoetus from Uloma species and Chiloanoetus from
various genera of Pycnocerini. Species of Cureulanoetus are associated with palm
weevils of the genus Rhynchophorus. Beetles of the family Scarabaeidae which
make excavations in wood (Dynastinae, Rutelinae) or brood cells in soil provi-
sioned with dung or other materials create habitats for species of Saneassania
(Acaridae). Most of these species are known or presumed to be fungivores
(Acaridae) or microorganismal feeders (Histiostomatidae), however Afroealvolia
nataliae (= Calvolia fraxini) is a predator on eggs and young larvae of its scolytid
host (Kielczewski and Seniczak 1972). The other genera of Winterschmidtiinae
also share this habitat type and may also be predaceous.
Colonies formed by scale insects of the family Diaspididae are exploited by
specialized mites of the genera Hemisareoptes (Hemisarcoptidae) and Thyreopha-
gus (Acaridae). Species of Hemisareoptes are predaceous on the scale insects
and their eggs, while Thyreophagus species are fungivores (Houck and OConnor
1991; Houck, Chapter 10, this volume).
The greatest diversity of astigmatid mites living in habitats created by other
arthropods is associated with the nests of solitary and social Hymenoptera.
The nests of solitary wasps harbor most species of the subfamily Ensliniellinae
(Winterschmidtiidae). Hosts include crabronine Sphecidae (of the mite Crabrovi-
dia) and eumenine Vespidae (of the mites Ensliniella, Kennethiella, Macroharpa,
Monobiacarus, Vespaearus, Zethaearus, Zethovidia and numerous undescribed
genera). Species of Ensliniella, Kennethiella and Vespacarus feed on hemolymph
of the host larva or on provisioned prey, while Monobiaearus feeds only on
provisions (Krombein 1967, Klompen et al. 1987). Some Hemisarcoptidae (Con-
govidia) and Acaridae (Lackerbaueria) have also been collected from solitary
sphecid nests. The latter is apparently a cleptoparasite (Krombein 1967), while
the former is likely a fungivore. Solitary bees of the family Megachilidae also
harbor enslinielline mites of the genus Vidia, species of which feed on fungi in
the nest lining (OConnor and Eickwort 1988).
A much greater diversity of solitary bee associates is found in other families
of Astigmata. As these associations have been the subject of recent reviews by
Eickwort (1979, Chapter 9, this volume) and OConnor (1988), I will only
summarize the associations. All species in the family Chaetodactylidae inhabit
the nests of bees: Chaetodactylus primarily associated with Megachilidae and
Xylocopinae, and Sennertia with Xylocopinae. In the family Acaridae, all genera
in the subfamily Horstiinae have obligatory associations with bees, the majority
of which are solitary. These genera include: Halictacarus and Schulzea from the
Halictidae; Megachilopus, Neohorstia and Sennertionyx from the Megachilidae;
Horstia from Xylocopinae; Horstiella from euglossine Apidae; and an unde-
scribed genus from Anthophorinae. Although not belonging to the Horstiinae,
another acarid genus, Ctenocolletacarus, is found in the nests of stenotritid bees
in Australia. Solitary bee nests may also harbor species of Histiostomatidae
(Anoetus and some Histiostoma from Halictidae; some Glyphanoetus from Col-
letidae and Xylocopinae). Finally, species of Tortonia (Suidasiidae) inhabit the
nests of both solitary wasps and bees. Feeding ecologies of these taxa range from
microorganismal filtration (Histiostomatidae) to provision thieves (Sennertia) to
true cleptoparasites (Chaetodactylus, Horstia, some Tortonia).
The nests of social Hymenoptera and Isoptera also harbor an extensive fauna
of astigmatid mites which has been reviewed by Eickwort (1990). Among the
social Vespidae, Polistes species harbor species of Sphexicozela (Winterschmid-
tiidae), while the genera Medeus (Acaridae) and Tortonia (Suidasiidae) occur in
Vespula nests. Social halictid bee nests are habitat for some species of Anoetus
(Histiostomatidae), while a diversity of taxa in several families are associated with
social Apidae. These include: Kuzinia (Acaridae) and Cerophagus (Gaudiellidae)
associated with Bombus, some species of Carpoglyphus (Carpoglyphidae) and
Forcellinia (Acaridae) with Apis, and all species of Meliponocoptidae (Melipono-
coptes, Meliponoecius and one undescribed genus) and most Gaudiellidae (Gau-
dietla, Partamonacoptes, Platyglyphus and unnamed genera) with meliponine
stingless bees. Finally, the nests of ants (Formicidae) harbor many genera of
mites, primarily from the family Acaridae. A number of these taxa are also
shared with the nests of termites (Isoptera). These genera include: Cosmoglyphus,
Forcellinia, Froriepia, Lasioacarus, Ocellacarus, Rettacarus, Sancassania,
Tyrophagus and others. Other families represented in the faunas of ant and
termite nests include the Suidasiidae (Lemaniella) and Histiostomatidae (Histi-
ostoma).
2.4.2 Mammal Hosts
The nests of mammals harbor an even greater diversity of astigmatid mites

than do the nests of social insects. Some taxa in all major clades are found in
these associations although few species have been studied with respect to their
ecology and life history. Among the Histiostomatidae, some species of Myianoe-
tus and Psyllanoetus are associated with mammal nests or nest-inhabiting insects.
Species of Psylloglyphus (Winterschmidtiidae) have also been described from
144 / B. M. OConnor
phoretic associations with nest-inhabiting insects. Most taxa in the superfamily

Glycyphagoidea are known or presumed mammal nest associates. These include
the families Chortoglyphidae (Alabidopus, Aplodontopus, Chortoglyphus and
two undescribed genera) associated with rodents, insectivores and primates;
Echimyopodidae (Echimyopus, M armosopus, M arsupiopus and Oryzomyopus)
associated with marsupials and rodents; and Glycyphagidae (many genera) associ-
ated with marsupials, edentates, rodents, carnivores and insectivores. Some
members of the family Acaridae have been described from mammal nests or nest-
inhabiting arthropods. Genera include Acarus, Acotyledon, Paraceroglyphus,
Trichopsyllopus, and Viedebanttia. Finally, some species of Pyroglyphidae (Pyr-
oglyphus and occasionally other genera) have been collected from mammal nests.
2.4.3 Bird Hosts
The nests of birds also serve as habitat for specialized taxa of astigmatid mites.
Comyianoetus, H exanoetus and some H istiostoma species (Histiostomatidae)
have been collected from the nests of raptors. The monobasic families Euglycy-
phagidae and Glycacaridae have been collected in nests of raptors and a petrel
respectively. Some Glycyphagidae (Glycyphagus and Lophuromyopus), Aero-
glyphidae (Aeroglyphus and Glycycometus), Acaridae (Acotyledon and Notiopsyl-
lopus), Lardoglyphidae (Lardoglyphus) and Suidasiidae (Sapracarus) are also
encountered in bird nests. Finally, almost all species of Hypoderatidae and most
nonparasitic species of the family Pyroglyphidae (many genera) inhabit bird nests.
The feeding ecologies of vertebrate nidicoles are probably varied, including
filter feeding on microorganisms (Histiostomatidae), fungivory (many glycypha-
goids), consumption of actual nest materials as well as fungi (Acaridae) and
ingestion of prey remains (Lardoglyphidae). Many Glycyphagidae exhibit strong
preferences for a restricted number of fungal species as food resources (Sinha
1966), and nidicolous species are notoriously difficult to culture away from
natural substrates (Lukoschus et al. 1971, Fain et al. 1972, Lukoschus et al.
1972, Lukoschus et al. 1979).
2.4.4 Habitat Shifts in Nest-inhabiting Astigmatid Mites
An interesting habitat shift has occurred among species representing many

genera of vertebrate nest-inhabiting Astigmata and a relatively few taxa from
other ecological types. A large number of species has adapted to living in and
around human habitations. This diversity of "stored product" and "house dust"
mites contains the majority of well-studied species of Astigmata (Hughes 1976).
The majority of these taxa belong to the families Acaridae (Acarus, Aleurogly-
phus, Cosmoglyphus, Histiogaster, Madaglyphus, Rhizoglyphus, Sancassania,
Thyreophagus, Tyrolichus and Tyrophagus), and Glycyphagidae (Ctenoglyphus,
Diamesoglyphus, Glycyphagus, Gohieria, Lophuromyopus and Tropilichus).
Other families are represented by fewer taxa: Histiostomatidae (Histiostoma) ,

Winterschmidtiidae (Acalvolia and Procalvolia), Hemisarcoptidae (Nanacarus),
Carpoglyphidae (Carpoglyphus) , Chortoglyphidae (Chortoglyphus), Echimyo-
podidae (Blomia), Aeroglyphidae (Aeroglyphus and Glycycometus), Suidasiidae
(Suidasia) , Lardoglyphidae (Lardoglyphus) , and Pyroglyphidae (Euroglyphus,
Dermatophagoides, Malayoglyphus and Pyroglyphus).
3. Demographics
In contrast to other lineages within the suborder Sarcoptiformes, the Astigmata

may be characterized by a series of life-history modifications related to their
exploitation of temporary habitats. These so-called "r-selected" characteristics
include a relatively short generation time, high fecundity, relatively short adult life
span, internal fertilization, and dispersal ancestrally as deutonymphs. Although
demographic information is available for a number of taxa of astigmatid mites,
a word of caution is in order. Studies on these mites have concentrated on
species associated with human habitations and food stores or parasites of domestic
animals, and the majority of published life-history data deals with these species.
Fortunately, there is a diversity of evolutionary lineages represented among these
studies, so generalizations may have some validity. On the other hand, many of
the ecological categories discussed earlier are completely unrepresented or have
few species which have been studied. For example, due to the difficulties of
maintaining parasitic astigmatid mites away from their hosts, almost no demo-
graphic information is available for this great diversity of taxa.
In examining the available demographic data for astigmatid mites, several
general patterns can be observed. The first and most common pattern includes
taxa with a generation time in the range of 10--15 days (egg to egg, ordeutonymph
to deutonymph, in a temperature regime of 22°_27°C), and an average female
reproductive period in the range of 15-40 days. Three subgroups may be recog-
nized within this category with respect to the total egg production per female.
Some taxa in this group exhibit a moderate fecundity in the range of 100-300
eggs per female. These include soil and litter inhabiting species in the family
Acaridae such as Tyrophagus putrescentiae (Rivard 1959, 1961; Barker 1967a),
Schwiebea falticis and S. rocketti (Woodring 1969); insect nidicoles such as
Carpoglyphus lactis (Carpoglyphidae) (Chmielewski 1971) and Acotyledon for-
mosani (Acaridae) (Phillipsen and Coppel 1977a); and Glycyphagus domesticus
(Glycyphagidae) (Barker 1968), a species derived from a vertebrate nidicolous
ancestry, but which exhibits a very wide habitat range. A similar length of life
cycle and female reproductive period but a lower total fecundity (10-100 eggsl
female) is common among vertebrate nidicoles and other stored product mites
derived from nidicolous ancestry: Aleuroglyphus ovatus (Acaridae) (Hsin and
Chen 1964), Gohieria fusca (Glycyphagidae) (Boulanova 1937), Aeroglyphus
146 / B. M. OConnor
robustus (Aeroglyphidae) (Barker 1967b), and Dermatophagoides pteronyssinus,

(Pyroglyphidae) (Hart and Fain 1988). Finally, some Acaridae which inhabit
concentrated sources of organic matter such as dung, compost, treeholes, bulbs,
tubers, fungal fruiting bodies and subcortical spaces exhibit a much higher fecun-
dity (300-1400 eggs/female) within the same temporal parameters. These include
Sancassania berlesei (Hughes 1976, Timms et al. 1981), S. anomalus (Woodring
1969, Pillai and Winston 1969, Barker 1974), S. rodriguezi (Rodriguez and
Stepien 1973), Rhizoglyphus robini (Gerson et al. 1983), R. echinopus (Woodring
1969), Histiogaster arborsignis and H. rotundus (Woodring 1969). High fecun-
dity is also exhibited by Kuzinia laevis (Acaridae), an inhabitant of bumblebee
nests (Chmielewski 1969).
A second demographic category is exemplified by most species in the family
Histiostomatidae for which life-history information is available. These species
typically inhabit very ephemeral resources and have shorter generation times,
typically in the range of 4-8 days. Female oviposition period and life span are
also shorter (5-15 days), with a total egg production between 20-120 eggs/
female. Species for which information is available include Histiostoma heine-
manni (Hill and Deahl 1978), H. julorum (Hughes and Jackson 1958) and H.
polypori (Behura 1957), which typically inhabit decaying vegetation or fungal
fruiting bodies; H. cataglyphi (Yousef et al. 1979), and H. formosani (Phillipsen
and Coppel 1977b), from the nests of an ant and a termite respectively; H.
laboratorium (Perron 1954) from Drosophila cultures, and H. murchei (Oliver
1962), a predator in annelid egg cocoons. The last mentioned species differs from
the others in having a much higher fecundity (up to 500 eggs/female). I have
observed undescribed North American species of the carrion inhabiting genera
Spinanoetus and Pelzneria which exhibit the same pattern of very short generation
time and female life span, and moderate egg production. In contrast, preliminary
observations on undescribed species in the genera Kanoetus and Scolianoetus,
which are associated with the galleries of wood-boring insects, indicate a much
longer generation time and adult life span for these taxa.
A third pattern is observed among species which inhabit certain types of
insect nests and galleries. Some data is available for the winterschmidtiid genera
Afrocalvolia, associated with bark beetle galleries, and Ensliniella, Kennethiella
and Vespacarus, which inhabit the nests of solitary vespid wasps. In these taxa,
the period between original infestation by deutonymphs and the production of the
next generation of deutonymphs or tritonymphs is in the range of 20-30 days. In
the enslinielline genera mentioned, female oviposition period is short (4-7 days)
and egg production is in the range of 25-125 eggs/female, depending on the
number of foundresses per cell (Krombein 1967, Cowan 1984, Klompen et al.
1987).
The final category includes species which have more prolonged generation
times (30---45 days), longer female reproductive period (40-80 days) and generally
low to moderate fecundity. The best studied species, Naiadacarus arboricola
(Acaridae), inhabits water-filled treeholes which may persist for yars. The life
history of this species has been discussed in detail by Fashing (1975,1979; this
volume) and will not be repeated here. Other examples of this pattern include
some species of Pyroglyphidae which inhabit stored products and house dust:
Dermatophagoides farinae, Euroglyphus /ongior and E. maynei (Hart and Fain
1988). The natural habitats of most Dermatophagoides species are birds' nests.
Euroglyphus species have not been collected regularly from natural habitats, but
a related species, Pyroglyphus morlani, lives in the nests of wood rats (Neotoma
spp.), many of which are perennial and may be inhabited by a series of hosts for
centuries. As pointed out by Fashing (1979) with reference to Naiadacarus
arboricola, mites exhibiting this type of life-history pattern may be better de-
scribed as "K-selected" although this is only in comparison with other astigmatid
mites. When compared with the ancestral and more common life-history pattern
in the Sarcoptiformes (i.e. generation times of 1-3 years, female reproductive
periods measured in years; see Norton, this volume), these species still show
much shorter generation times and life spans.
The few species of astigmatid mites parasitic on vertebrates which have been
studied in detail exhibit different demographic parameters. Both Sarcoptes scabiei
(Sarcoptidae), which lives in the upper epidermal layers of mammalian skin,
and species of Psoroptes (Psoroptidae), which live on the skin surface, have a
generation time similar to the common pattern among free-living Astigmata, i.e.
10-12 days (MelIanby 1972, Meleney 1985, Arlian and Vyszenski-Moher 1988).
However, it should be noted that the normal temperature under which these mites
develop (i.e. host body temperature) is much higher than that used in laboratory
studies of free-living mites. A major difference between these species is evident
in the female oviposition period which may extend for 60 days in Sarcoptes while
only lasting 21 days in Psoroptes. Correlated with the female life span, the total
fecundity of Sarcoptes is reported as 120-180 eggs/female, while in Psoroptes,
it is only 35-40. A third species, Chorioptes bovis (Psoroptidae), which like
Psoroptes inhabits the skin surface, is quite distinct in having a much longer
generation time (21-28 days), shorter female oviposition period (16 days) and
much lower fecundity (16 eggs/female) (reviewed in Meleney 1985). Unpublished
observations on other sarcoptid taxa suggest other patterns. For example, species
of Nycteridocoptes which parasitize Megachiroptera probably have a generation
time of one year, based upon the observation that adult females are present only
during the breeding season of the hosts (1. S. H. Klompen, pers. comm.).
Two serious caveats must be expressed with regard to interpreting the above
studies on astigmatid mite demographics. First, with few exceptions, these studies
were carried out in laboratory cultures under constant environmental conditions.
Many of the studies noted above report variation in life-history parameters under
different temperature and humidity regimes, however, most such studies do not
duplicate the natural conditions in which the mites actually live. Studies on
several species of Acaridae by Boczek and his co-workers indicate that the life
148 I B. M. OConnor
spans of these species may be considerably extended when they are cultured under
suboptimal conditions (Boczek 1973, Boczek and Czajkowska 1973, Boczek and
Sosnowska 1975). In laboratory culture most taxa exhibit the expected reaction
of poikilothermic animals in that developmental time decreases as temperatures
increase to the thermal death point. Response to humidity is also predictable in
that species whose normal habitat is relatively dry (e.g. Aeroglyphus robustus
and Glycyphagus domestieus) do better under drier conditions than nearer satura-
tion. The reverse is true for Histiostomatidae and other taxa which normally
inhabit saturated environments. An appropriate food source is also important in
this type of study. More success has been achieved with relative generalists such
as the Acaridae and Histiostomatidae than with specialists, a category which
apparently includes most Glycyphagoidea and Hemisarcoptoidea. Sinha (1966)
has demonstrated that species of Glycyphagidae inhabiting stored food are much
more particular about the fungal species upon which they will feed than are
species of Acaridae in the same habitats. The difficulties in culturing nidicolous
Glycyphagidae (Baloghella melis [= M elesodectes auricularis], Lophioglyphus
lieiosus [= Apodemopus apodemiJ and Marsupialiehus marsupialis) and Echimy-
opodidae (Marsupiopus zyzomys) have been documented by Lukoschus and his
co-workers (Lukoschus et al. 1971, Fain et al. 1972, Lukoschus et al. 1972,
Lukoschus et al. 1979). Similarly, despite the high level of taxonomic diversity
in the family, there are few reports of species of Winterschmidtiidae (= Saprog-
Iyphidae) being successfully cultured away from their natural substrates.
A second caveat regards the interpretation of generation time. The life cycle
of most astigmatid mites is similar to the ancestral pattern observed in acariform
mites (i.e. egg, prelarva, larva, protonymph, deutonymph, tritonymph, adult;
see Fashing, Fig. 7.4, this volume) except that in most species, formation of the
deutonymphal instar is facultative, or it is not formed at all. In the laboratory
cultures which formed the basis for the demographic information reported above,
generation time was typically determined for individuals which bypassed the
deutonymphal instar. This shortening of the life cycle by the facultative or
permanent elimination of an ontogenetic stage has been suggested as a characteris-
tic of "r-selected" taxa. On the other hand, it seems reasonable to view as
a general pattern the observations that certain astigmatid mites overwinter as
deutonymphs. For example, the winterschmidtiid species Afrocalvolia nataliae
(= Calvolia fraxini) undergoes two generations per year in the galleries of its
scolytid host, Leperisinus fraxini, in Poland (Kielczewski and Seniczak 1972).
The summer generation is passed during the month of July and individuals bypass
the deutonymphal stage. Offspring of the summer generation, however, all enter
the deutonymphal stage in August and overwinter on the adult bark beetle host
until the following May, at which time they enter the feeding and reproductive
phase of the life cycle. This overwintering generation actually has a generation
time of 11 months, while the summer generation time is one month.
A similar situation has been observed among species of the winterschmidtiid
subfamily Ensliniellinae associated with the nests of solitary vespid wasps. Spe-
cies in three genera have been studied in some detail: Kennethiella trisetosa
associated with Aneistrocerus antilope (Krombein 1967, Cowan 1984), Ves-
paearusfulvipes with Paraneistroeerusfulvipes (Krombein 1967), and Ensliniella
kostylevi with Allodynerus rossi (Klompen et al. 1987) and E. parasitica with A.
delphinalis (Cooreman 1942). Each of these hosts is bivoltine, with the mite
development closely associated with the development of the host larva and pupa.
These species differ from Afroealvolia nataliae in that all surviving individuals
in each generation pass through the deutonymphal ins tar. Mites of the winter
generation pass the winter as deutonymphs attached to the host prepupa or pupa.
Contrasting data is available on other insect nidicoles. Krombein (1967) reported
that Horstia virginiea (Acaridae) and Chaetodaetylus krombeini (Chaetodactyli-
dae) underwent multiple generations within cells of their solitary bee hosts.
4. Dispersal
4.1 Phoretie Dispersal by Deutonymphs
One major modification in the life cycle of astigmatid mites which has enabled
the lineage to undergo such a successful radiation in temporary habitats is the
shift from limited dispersal ability restricted to the adult instar to a much greater
dispersal potential achieved in a preadult instar, the deutonymph. As noted above,
the deutonymphal instar in the Astigmata has a highly modified morphology and
behavior which function both in dispersal and typically in resisting adverse
conditions. Dispersal in the Astigmata can occur in several modes. The ancestral
condition in the group, as evidenced by the morphology of the earliest derivative
lineage, the Schizoglyphidae, is dispersal by deutonymphs via phoretic associa-
tion with an arthropod. The subject of phoresy in the Astigmata has been recently
reviewed by Houck and OConnor (1991) and will not be detailed again here.
Suffice it to say that phoresy by deutonymphs remains the primary dispersal mode
in the non-psoroptidid Astigmata, with phoretic hosts including many groups of
arthropods and vertebrates.
4.2 Nonphoretie Dispersal by Deutonymphs
A second dispersal mode known in the Astigmata is nonphoretic dispersal by

deutonymphs. This type of dispersal is accomplished via two distinct mecha-
nisms. In the first case, deutonymphs retain the ancestral morphology, including
the attachment structures used by phoretic individuals, however, dispersal is
typically under the mites own power. Examples of this type of dispersal include
species of Saneassania (= Caloglyphus) (Acaridae) which are associated with
certain scarabaeid beetles and their larvae. Feeding stages of the mites occur on
dead beetles or larvae; deutonymphs disperse in the soil, encounter beetle larvae
150 / B. M. OConnor
and remain with them until their death (Chmielewski and Lipa 1967). An analo-
gous situation possibly occurs with Histiostoma murchei (Histiostomatidae), in
which the feeding stages are predaceous in the egg cocoons of earthworms
(Oliver 1962). Phoresy is unknown in this species, withdeutonymphs presumably
dispersing through the litter in search of suitable habitats. Finally, phoresy is
poorly documented in the histiostomatid taxa associated with pitcher plants.
Robert Naczi (pers. comm.) has observed that species of Sarraceniopus only
leave the water-filled leaf pitchers as deutonymphs. Deutonymphs wander about
the plant and congregate at the tips of unopened leaf pitchers. When the pitchers
open, the mites immediately enter. These deutonymphs retain the modifications
associated with phoresy and likely use phoresy for long distance dispersal, but
most individuals disperse to new pitchers within a single plant or members of a
single clone. Few records of phoresy among the Old World Nepenthes associates
are also known, suggesting a similar dispersal mode.
A more profound modification of the deutonymph, involving highly regressive
morphological changes, has led to passive dispersal via air currents in two taxa
of Glycyphagidae. Both Glycyphagus (G.) domesticus and G. (Lepidoglyphus)
destructor have deutonymphs in which the body setation and legs are strongly
regressive or lacking altogether. These deutonymphs typically do not emerge
from the protonymphal cuticle which dries around the cyst-like deutonymph
(Hora 1934; Kniille 1959, 1987). In contrast with other taxa in which regressive
deutonymphs are formed (Acarus, Alabidopus, Chaetodactylus and Hericia) but
typically do not disperse, deutonymphs of the two Glycyphagus species actually
do disperse via air currents.
4.3 Loss of the Dispersal (Deutonymphal) Morph
Many taxa of astigmatid mites have lost the ability to form deutonymphs, and in
these taxa it is presumed that all dispersal must be accomplished by other instars.
These taxa include the family Hyadesiidae, species of which are restricted to
marine, intertidal and tidal habitats; arboreal leaf-inhabiting species of the genera
Czenspinskia and Oulenzia (Winterschmidtiidae), and Neotropacarus (Acaridae);
most species of the genus Tyrophagus (Acaridae) which occur in soil, litter and
synanthropic habitats; the Aeroglyphidae-Rosensteiniidae lineage which ances-
trally occur in bat colonies; and the numerous taxa with nondeutonymphal stages
parasitic on arthropods or vertebrates, although a few exceptions to the last
occur. Deutonymphs have not been described for a number of other lineages of
Astigmata, however, the fragmentary nature of the available data on these species
does not permit a definitive statement as yet. Some of these taxa where I suspect
deutonymphs are never formed are the subfamily Algophagine (Algophagidae),
the genera Fusacarus, Gohieria, and Tropilichus (Glycyphagidae), Suidasia
(Suidasiidae), and Aleuroglyphus (Acaridae).
4.4 Dispersal of Permanent Parasites
Few controlled experimental data are available concerning the details of dispersal
by nondeutonymphal stages of astigmatid mites. Dubinin (1951) summarizes a
considerable number of observations on the dispersal of astigmatid mites inhab-
iting bird feathers. He concludes that three basic dispersal modes operate: (1)
direct transmission from parent to offspring, in which case the preponderance of
dispersers are preadults or teneral adults; (2) direct transfer between adult birds,
which accounts for the presence of specific parasites on birds which do not
rear their own young; and (3) transfer via the nest. The latter mode, although
documented for some individuals of some species (e.g. Gabucinia delibata [Ga-
buciniidae] on crows), was not deemed an important mode of dispersal for any
species. Direct contact between hosts seems to be the required mode of dispersal
among astigmatid mite parasites of mammals (Meleney 1985), although some
species, notably the scabies mite, Sarcoptes scabiei (Sarcoptidae), can survive
for short periods away from a host (Mellanby 1972).
The life histories of permanently parasitic mites of arthropods (Canestriniidae,
Heterocoptidae and some Rosensteiniidae and Hemisarcoptidae) have not been
studied. Because these mites parasitize only adult insects, dispersal must take
place through direct contact between individuals, presumably during copulation.
An interesting potential exception may be found in the genus Megacanestrinia
(Canestriniidae). This genus, the earliest derivative genus in the family, is the
only one of all the permanent parasites of arthropods in which the deutonymph
is retained in the life cycle. Feeding stages of the mites occur in the subelytral
space on their hosts, African carabid beetles of the genus Tejjfus, while deuto-
nymphs congregate on the venter of the thorax. In this instance, it seems possible
that dispersal to new hosts still involves the deutonymph as this stage is positioned
for easier access to another individual during mating.
4.5 Dispersal and Adverse Changes in the Environment
Correlated with the morphological specializations for dispersal in astigmatid mite

deutonymphs is the ability to withstand adverse changes in the environment which
would be fatal to other ontogenetic stages. In a number of taxa, decline in
environmental quality induces individuals to enter the deutonymphal stage (Wal-
lace 1960, Woodring 1963, Griffiths 1966). In taxa in which the ability to form
deutonymphs has been lost, the tritonymph typically takes over the function of
surviving adverse periods. This phenomenon has been demonstrated for Czenspin-
skia transversostriata (= lordi) (Winterschmidtiidae) (Dosse and Schneider
1957), Tyrophagus longior (Acaridae) (Sorokin 1948), and populations of Car-
poglyphus lactis (Carpoglyphidae) which are unable to form deutonymphs (Zy-
romska-Rudzka 1964). Populations of Dermatophagoides (Pyroglyphidae) typi-
cally survive adverse conditions in either the protonymphal or tritonymphal instars
152 / B. M. OConnor
(Wharton 1976). Interestingly, Naiadacarus arboricola (Acaridae) also survives

adverse periods as tritonymphs (Fashing 1976); the deutonymph in this species
apparently functioning only in dispersal.
5. Host Associations
An integral aspect of the life history of most astigmatid mites is the quality,
duration and specificity of association with another organism. Until recently, it
was presumed that the association between astigmatid mite deutonymphs and
other arthropods was a case of simple commensalism, with the mite benefiting
solely through phoretic dispersal. Recent studies by Houck (Houck and OConnor
1991) which are developed more fully in this volume (Chapter 10) suggest that
the association may be more complicated in some taxa, in that deutonymphs may
require a period of time spent on a host before developing further. It has long
been known that some deutonymphs which are found in mammalian hair follicles
and the subcutaneous tissues of birds and mammals are true parasites, acquiring
material in an as yet unknown manner from their hosts (Fain and Bafort 1967,
Lukoschus et al. 1972).
Specificity of association varies widely among astigmatid mite taxa. Species
which live in environments which are only visited by other organisms, and not
created by them, tend to show little specificity. For example, Tiirk and Tiirk
(1957) recorded numerous hosts for species which develop in decaying organic
matter and fungal fruiting bodies in Germany. Similarly, OConnor (1990) col-
lected Histiogaster arborsignis (Acaridae), a species which inhabits subcortical
spaces, from 22 species of insects belonging to three orders. OConnor (1991)
noted that this relative nonspecificity was a general pattern among astigmatid
mites inhabiting subcortical habitats in Michigan. On the other hand, some
species living in other habitats not created by interactive processes exhibit more
pronounced specificity. This may relate to a limited pool of potential host species
visiting the habitat as in the associations of Naiadacarus arboricola with syrphid
flies of the genus Mallota (Fashing 1975), and Hemisarcoptes species with
coccinellid beetles of the genus Chi/ocorus (Houck and OConnor 1990). Or it
may reflect ecological changes in the habitat itself. For example, different species
of Histiostomatidae which develop in cattle dung in the Netherlands use different
dung-breeding insects for dispersal (Bongers et al. 1985). These insects typically
come to dung piles at different periods during the succession of stages marking
the decomposition of the dung, suggesting that the mite species may be exploiting
the dung during different time periods as well.
In contrast to these patterns, mites which inhabit host-created environments
tend to be specialized for dispersal on those hosts and few others. Specificity
among nidicolous mites associated with insects and vertebrates is high. In many
such species, life histories of the mites and their hosts are strongly correlated.
This synchronicity of development has been documented for the enslinielline

associates of Hymenoptera (Krombein 1967, Cowan 1984, Klompen et al. 1987),
some glycyphagid associates of mammals such as Lophioglyphus liciosus (Lu-
koschus et. al. 1972), and hypoderatid associates of birds such as Hypodectes
prop us (Fain and Bafort 1967). Some correlation of life histories between verte-
brate hosts and permanently parasitic Astigmata has also been noted. Dubinin
(1951) noted the correlation between the size and age structure of feather mite
populations with the breeding and molting patterns of the host birds. Similarly,
some sarcoptid parasites of bats may time the production of offspring to coincide
with the reproduction of their hosts (Klompen, pers. comm.).
6. Evolution of Parasitism
Using the method of Brooks (1985) to hypothesize ecological shifts, the shifts in
essential life-history parameters which mark the transition from commensalistic
associations to true parasitism may be hypothesized to have occurred in at least
21 different lineages of astigmatid mites (parasitism is here defined in the broadest
sense of living permanently on a host or feeding directly from it). Parasitism of
arthropods has evolved on 10 separate occasions, seven of which involve perma-
nent parasitism: (1) the family Canestriniidae; (2) the family Heterocoptidae; (3)
the genus Rosensteinia (Rosensteiniidae); (4) an undescribed genus of Rosenstei-
niidae also parasitic on roaches which is related to the nonparasitic genus Nycterili-
chus; (5) the genera Micronychites and Micronychitoides (Rosensteiniidae) which
form a monophyletic group; (6) the genus Linobia (Hemisarcoptidae); (7) the
genera Askinasia, Ewingia, Hoogstraalacarus, Kanakobia and two undescribed
genera (Acaridae) living on decapod crustaceans. Parasitism of arthropods by
species which still retain the deutonymph in the life cycle and disperse in this
stage has evolved twice: (1) the clade comprising the genera Ensliniella, Kenneth-
iella and Vespacarus (Winterschmidtiidae), and (2) the genus Hemisarcoptes
(Hemisarcoptidae) which may act either as a predator or a parasite of diaspidid
scale insects depending on the number of mites per host and the stage of the host
attacked. Finally, a last lineage of arthropod parasites should be mentioned in
which a shift in host and life history has occurred. The family Epidermoptidae
comprises species which are normally parasitic on the skin of birds. The genus
Myialges has undergone a transformation such that the adult females leave the
bird host and parasitize lice or hippoboscid flies, the males and nymphs remain
on bird hosts, but females lay their eggs on the arthropod host.
A similar analysis of the evolution of parasitism of vertebrates yields a hypothe-
sis of 11 separate instances. Two distinct life-history shifts have occurred, perma-
nent parasitism by feeding stages with the concomitant loss of the deutonymph
from the life cycle, and parasitism by deutonymphs only, with the other stages
remaining free-living nidicoles. The first pathway has occurred in at least four
154 / B. M. OConnor
lineages: (1) the Psoroptidia forms a monophyletic grouping of approximately 40

families which appears to have originated as parasites of birds, with a secondary
radiation onto mammals; (2) the genera Loxanoetus and Otanoetus (Histiostomati-
dae) which inhabit the ears of large mammals form a monophyletic group (it is
problematical whether these mites are true parasites although it seems likely that
at least some of their diet is material of host origin); (3) the genus Chiroptogl)phus
represents a very early derivative lineage in the family Rosensteiniidae, species
of which live permanently in the fur of bats; (4) the rosensteiniid taxa Cheiromeli-
chus and "Nycteriglyphus" asiaticus probably form a monophyletic lineage,
species of which attach to the skin of molossid bats of the genus Cheiromeles.
In seven additional lineages species have made the transition to parasitism by
a shift from simple phoresy by deutonymphs to a closer association in which the
deutonymph actually obtains materials from the host. The exact mechanism of
food uptake remains unknown as deutonymphs lack a functional mouth, however,
breakdown of host tissue around the mite has been demonstrated in some Glycy-
phagidae (Lukoschus et al. 1972) and growth of the mite within the deutonymphal
stadium can be pronounced. Six of the lineages exhibiting this shift belong to the
superfamily Glycyphagoidea, where nondeutonymphal instars are mammalian
nidicoles. The lineages include: (I) the monobasic family Pedetopodidae, the
single species of which lives as deutonymphs in the hair follicles ofthe springhare,
Pedetes capensis; (2) the family Chortoglyphidae which parasitize the hair folli-
cles of rodents and occasionally other mammalian groups; (3) the family Echimyo-
podidae which occur in hair follicles or subcutaneous tissues of marsupials,
edentates and rodents; and three lineages within the family Glycyphagidae; (4)
the genus Baloghella representing the subfamily Melesodectinae, deutonymphs
of which live in the tissues of the ear conchae of European badgers; (5) the
subfamily Metalabidophorinae which live in hair follicles of rodents and rarely
insectivores; (6) the lineage comprising the subfamilies Lophuromyopodinae and
Ctenoglyphinae which live in the hair follicles of rodents, and finally; (7) the
nonglycyphagoid family Hypoderatidae, deutonymphs of which occur subcutane-
ously in birds and rarely in mammals.
7. Summary
The Astigmata is an extremely successful lineage of mites which owes its success-
ful diversification and adaptive radiation to an ancestral switch in life-history
parameters which allowed the colonization and exploitation of patchy or ephem-
eral resources. The ability to quickly colonize such habitats via phoretic associa-
tions with arthropods, and to quickly exploit the resources before their disappear-
ance has allowed these mites to diversify in the absence of most other potentially
competing groups of mites. Phoretic exploitation of other arthropods, typically
insects, which are potential competitors for the same resources, has in numerous
instances led to closer associations with the hosts. As hosts undergo ecological
shifts themselves which involve the creation of new habitat types, mites can be
carried along, ecologically and evolutionarily speaking. Close phoretic associa-
tions may evolve into mutualistic relationships (Eickwort 1979) or parasitic ones.
Ultimately, as mites adapt to a completely parasitic existence in a relatively stable
"host" environment, the selective pressures which originally favored life-history
traits such as fast generation time and good dispersal ability become somewhat
reversed and coevolutionary processes begin to dominate. Most parasitic astig-
matid mites are relatively innocuous, suggesting a period of coadaptation on the
part of both mite and host species.
References
Barker, P. S. 1967a. The effects of high humidity and different temperatures on the
biology of Tyrophagus putrescentiae (Schrank) (Acarina: Tyrogliphidae). Can. 1. Zool.
45:91-96.
Barker, P. S. 1967b. Effect of humidity and temperature on the biology of Aeroglyphus
robustus (Banks) (Acarina: Glycyphagidae). Can. 1. Zool. 45:479-483.
Barker, P. S. 1968. Bionomics of Glycyphagus domesticus (de Geer) (Acarina: Glycypha-
gidae), a pest of stored grain. Can. 1. Zool. 46:89-92.
Barker, P. S. 1974. Bionomics of Caloglyphus anomalus Nesbitt (Acarina: Acaridae).
Manitoba Entomol. 8:41-47.
Behura, B. K. 1957. The life-history of Histiostoma polypori (Oud.) (Acari: Tyrogly-
phoidea). 1. NY Entomol. Soc. 65:51-78.
Boczek,.r. 1973. Procesy starzenia sie u owadow i roztoczy. Kosmos 6:611-621.
Boczek, J. and B. Czajkowska. 1973. Some aspects of aging in Acarus siro (L.) (Acarina:
Acaridae). Ekol. pol. 21:173-184.
Boczek, J. and B. M. Sosnowska. 1975. Studies on aging in acarid mites, II. Zesz. Probl.
Postepow Nauk. Roln. 171:169-177.
Bongers, M. G. H., B. M. OConnor and F. S. Lukoschus. 1985. Morphology and
ontogeny of histiostomatid mites (Acari: Astigmata) associated with cattle dung in the
Netherlands. Zool. Meded. (Leiden) 223:1-56.
Boulanova, E. 1937. Notes morphologique et biologique sur Ferminiafusca Ouds. Bull.
Soc. Nat. Moscow Bioi. N.S. 46:304-316.
Brooks, D. R. 1985. Historical ecology: a new approach to studying the evolution of
ecological associations. Ann. Mo. Bot. Gard. 72:660--680.
Chmielewski, W. 1969. Obserwacje nad biologia now ego dla akarofauny polskiej gatunku
Kuzinia laevis (Dujardin, 1849) (Acarina, Acaridae). Pol. Pismo Entomol. 39:603-
617.
Chmielewski, W. 1971. Morfologia, biologia i ekologia Carpoglyphus lactis (L., 1758)
(Glycyphagidae, Acarina). Pro Nauk. Inst. Ochr. Rosi. 13:63-166.
156 / B. M. OConnor
Chmielewski, W. and 1. 1. Lipa. 1967. Biological and ecological studies on Caloglyphus

mites (Acarina: Acaridae) associated with Scarabaeidae. Acta Parasitol. Pol. 14: 179-
186.
Cooreman, 1. 1942. Notes et observations sur les acariens, II. Bull. Mus. r. Hist. nat.
Belg. 18:1-10.
Cowan, D. P. 1984. Life history and male dimorphism in the mite Kennethiella trisetosa
(Acari: Winterschmidtiidae), and its symbiotic relationship with the wasp Ancistrocerus
antilope (Hymenoptera: Eumenidae). Ann. Entomol. Soc. Am. 77:725-732.
Dosse, G. and I. Schneider. 1957. Biologie und Lebensweise von Czenspinskia lordi
Nesbitt (Acar., Sarcoptiformes). Z. Angew. Zool. 44:403-418.
Dubinin, V. B. 1951. Feather mites (Analgesoidea). Part I. Introduction to their study.
Fauna of the USSR, Arachnida, Vol. 6 (no. 5). (In Russian). 365 pp.
Eickwort, G. C. 1979. Mites associated with sweat bees (Halictidae). In: Recent Advances
in Acarology, Vol. I (1. G. Rodriguez ed.). Academic Press, NY. Pp. 575-581.
Eickwort, G. C. 1990. Associations of mites with social insects. Annu. Rev. Entomol.
35:469-488.
Fain, A. and J. Bafort. 1967. Cycle evolutif et morphologie de Hypodectes (Hypodec-
toides) propus (Nitzsch), acarien nidicole a deutonymphe parasite tissulaire des pigeons.
Bull. Acad. R. Beige Classe Sci. 53:501-533.
Fain, A., A. W. A. M. de Cock and F. S. Lukoschus. 1972. Parasitic mites of Surinam
XVII. Description and life cycle of Marsupialichus marsupialis sp. n. from Didelphis
marsupialis (Glycyphagidae: Sarcoptiformes). Acarologia 14:81-93.
Fashing, N. J. 1975. Life history and general biology of Naiadacarus arboricola Fashing,
a mite inhabiting water-filled treeholes (Acarina: Acaridae). 1. Nat. Hist. 9:413-424.
Fashing, N. 1. 1976. The resistant tritonymphal instar and its implications in the population
dynamics of Naiadacarus arboricola Fashing (Acarina: Acaridae). Acarologia 18:704-
714.
Fashing, N. 1. 1979. Naiadacarus arboricola, a "K-selected" acarid mite. In: Recent
Advances in Acarology, Vol. I (J. G. Rodriguez ed.). Academic Press, NY. pp. 525-
529.
robini Claparede (Acari: Astigmata: Acaridae). Acarologia 24:439-448.
Griffiths, D. A. 1966. Nutrition as a factor influencing hypopus formation in the Acarus
siro species complex (Acarina, Acaridae). 1. Stored Prod. Res. 1:325-340.
Hart, B. 1. and A. Fain. 1988. Morphological and biological studies of medically important
houst-dust mites. Acarologia 29:285-295.
Hill, A. and K. L. Deahl. 1978. Description and life cycle of a new species of Histiostoma
(Acari: Histiostomidae) associated with commercial mushroom production. Proc. Ento-
mol. Soc. Wash. 80:317-329.
Hora, A. M. 1934. On the biology of the mite, Glycyphagus domesticus de Geer (Tyrog-
lyphidae, Acarina). Ann. Appl. Bioi. 21:483-494.
Houck, M. A. and B. M. OConnor. 1990. Ontogeny and life history of Hemisarcoptes

cooremani (Acari: Hemisarcoptidae). Ann. Entomol. Soc. Am. 83:869-886.
Houck, M. A. and B. M. OConnor. 1991. Ecological and evolutionary significance of
phoresy in the Astigmata. Annu. Rev. Entomol. 36:611-636.
Hsin, K.-L. and C.-P. Chen. 1964. Studies on the life history of Aleuroglyphus ovatus
Troupeau (Acarina, Acaridae). Acta Entomol. Sin. 13:428-435. (In Chinese).
Hughes, A. M. 1976. The Mites of Stored Food and Houses, 2nd. ed. Min. Agric.
Fisheries, Food, Tech. Bull. 9, H. M. S. O. London. 400 pp.
Hughes, R. D. and C. G. Jackson. 1958. A review of the Anoetidae (Acari). Virginia J.
Sci. 9, N.S.(l):5-198.
Kielczewski, B. and S. Seniczak. 1972. Cykl rozwojowy drapieznego roztocza Calvolia
fraxini E. TUrk et F. TUrk (Tyroglyphidae, Acarina). Pro Z. Zakr. Lesn., Poznan 34:83-
88.
Klompen,1. S. H., F. S. Lukoschus and B. M. OConnor. 1987. Ontogeny, life history
and sex ratio evolution in Ensliniella kostylevi (Acari: Winterschmidtiidae). J. Zool.
(Lond.) 213:591-607.
KnUlle, W. 1959. Morphologische und entwicklungsgeschichtliche Untersuchungen zum
Phylogenetischen System der Acari: Acarifonnes Zachv. II. Acaridiae: Acaridae. Mitt.
Zool. Mus. Berl. 35:347-417.
KnUlle, W. 1987. Genetic variability and ecological adaptability of hypopus formation in
a stored product mite. Exp. Appl. Acarol. 3:21-32.
Krombein, K. V. 1967. Trap Nesting Wasps and Bees: Life Histories, Nests and Associ-
ates. Smithsonian Press, Washington, DC. 496 pp.
Lukoschus, F. S., A. W. A. M. de Cock and A. Fain. 1971. Life cycle of Melesodectes
auricularis Fain and Lukoschus (Glycyphagidae, Sarcoptifonnes). Tijdschr. Entomol.
114:173-183.
Lukoschus, F. S., A. Fain and F. M. Driessen. 1972. Life cycle of Apodemopus apodemi
(Fain 1965) (Glycyphagidae: Sarcoptifonnes). Tijdschr. Entomol. 115:325-339.
Lukoschus, F. S., G. H. S. Janssen Duijghuijsen and A. Fain. 1979. Parasites of Western
Australia IV. Observations on the genus Marsupiopus Fain 1968 (Acarina: Astigmata:
Glycyphagidae). Rec. West. Aust. Mus. 7:37-55.
Meleney, W. P. 1985. Mange mites and other parasitic mites. In: Parasites, Pests and
Predators. World Animal Science B2 (S. M. Gaafar, W. E. Howard and R. E. Marsh
eds.). Elsevier, Amsterdam. Pp. 317-346
Mellanby, K. 1972. Scabies, 2nd ed. E.W. Classey Ltd., Middlesex, England. 81 pp.
OConnor, B. M. 1981. A systematic revision ofthefamily group taxa in the nonpsoroptidid
Astigmata. Ph.D. Thesis, Cornell Univ., Ithaca, NY. 594 pp.
OConnor, B. M. 1982a. Evolutionary ecology of astigmatid mites. Annu. Rev. Entomol.
27:385-409.
OConnor, B. M. 1982b. Acari: Astigmata. In: Synopsis and Classification of Living
Organisms II (S. Parker ed.). McGraw-Hill, NY. Pp. 146-169.
OConnor, B. M. 1984a. Phylogenetic relationships among higher taxa in the Acarifonnes,
158 I B. M. OConnor
with particular reference to the Astigmata. In: Acarology VI, Vol. I (D. A. Griffiths
and C. E. Bowman eds.). Ellis Horwood Ltd., Chichester. Pp. 19-27.
OConnor, B. M. 1984b. Acarine-fungal relationships: the evolution of symbiotic associa-
tions. In: Fungus-Insect Relationships: Perspectives in Ecology and Evolution (Q.
Wheeler and M. Blackwell eds.). Columbia Univ. Press, NY. Pp. 354--81.
OConnor, B. M. 1988. Coevolution in Astigmatid mite-bee associations. In: AJricanized
Honey Bees and Bee Mites. (G. R. Needham, R. E. Page, Jr, M. Delfinado-Baker and
C. Bowman eds.). Ellis-Horwood, Ltd. Chichester. Pp. 339-346.
OConnor, B. M. 1990. Ecology and host associations of Histiogaster arborsignis (Acari:
Acaridae) in the Great Lakes region, particularly in the Huron Mountains of Northern
Michigan. Great Lakes Entomol. 23:205-209.
OConnor, B. M. 1991. A preliminary report on the arthropod-associated astigmatid mites
(Acari: Acariformes) of the Huron Mountains of Northern Michigan. Mich. Acad.
24:307-320.
OConnor, B. M. and G. C. Eickwort. 1988. Morphology, ontogeny, biology and systema-
tics of the genus Vidia (Acari: Winterschmidtiidae). Acarologia 29: 147-174.
Oliver, J. H., Jr. 1962. A mite parasitic in the cocoons of earthworms. J. Parasitol.
48: 120--123.
Perron, R. 1954. Untersuchungen tiber Bau, Entwicklung und Physiologie der Milbe
Histiostoma laboratorium Hughes. Acta Zool. (Stockh.) 35:71-176.
Phillipsen, W. 1. and H. C. Coppel. 1977a. Acotyledon Jormosani sp.n. associated
with the Fonnosan subterranean tennite, Coptotermes Jormosanus Shiraki (Acarina:
Acaridae-Isoptera: Rhinotennitidae). J. Kans. Entomol. Soc. 50:399-409.
Phillipsen, W. J. and H. C. Coppel. 1977b. Histiostoma formosana sp.n. associated
with the Formosan subterranean tennite, Coptotermes formosanus Shiraki (Acarina:
Acaridae-Isoptera: Rhinotennitidae). J. Kans. Entomol. Soc. 50:496--502.
Pillai, P. R. P. and P. W. Winston. 1969. Life history and biology of Caloglyphus
anomalus Nesbitt (Acarina: Acaridae). Acarologia 2:295-303.
Rivard, I. 1959. Influence of humidity on longevity, fecundity, and rate of increase of the
grain-infesting mite Tyrophagus castellani (Hirst) (Acarina: Acaridae) reared on mould
cultures. Can. Entomol. 91:31-35.
Rivard, I. 1961. Influence of temperature and humidity on mortality and rate of develop-
ment of immature stages of the mite Tyrophagus putrescentiae (Schrank) (Acarina:
Acaridae) reared on mold cultures. Can. J. Zool. 39:419-426.
ph us berlesei (Michael) (Acarina: Acaridae) in xenic diet. J. Kans. Entomol. Soc.
46: 176--183.
Sinha, R. N. 1966. Feeding and reproduction of some stored-product mites on seed-borne
fungi. J. Econ. Entomol. 59:227-232.
Sorokin, S. 1948. Population of grain mites in hay. Zool. Zh. 27:487-491. (In Russian).
Timms, S., D. N. Ferro and R. M. Emberson. 1981. General biology and nomenclature
of Sancassania berlesei (Michael). Acarologia 22:385-390.
Life-History Modifications in Astigmatid Mites I J59
Turk, E. and F. Turk. 1957. Systematik und Okologie der Tyroglyphiden Mitteleuropas.
In: Beitriige zur Systematik und Okologie Mitteleuropiiischer Acarina, Vol. I (H. 1.
Stammer ed.). Akad. Verlagsges, Leipzig. Pp. 3-231.
Wallace, D. R. J. 1960. Observations on hypopus development in the Acarina. 1. Insect
Physiol. 5:216-229.
Wharton. G. W. 1976. House dust mites. 1. Med. Entomol. 12:577-621.
Woodring, J. P. 1963. The nutrition and biology of saprophytic Sarcoptiformes. In:
Advances in Acarology Vol. I (1. A. Naegle ed.). Comstock Publ. Assoc., Ithaca, NY.
Pp. 89-111.
Woodring, 1. P. 1969. Observations on the biology of six species of acarid mites. Ann.
Yousef, A. A., E. A. El-Badry and S. H. Metwally. 1979. Life history of the anoetid
mite Histiostoma cataglyphi Yousef et Metwally, with a description of the immature
stages (Acari, Astigmata, Anoetoidea). Z. Angew. Entomol. 87:225-229.
Zyromska-Rudska, A. 1964. Abundance, dynamics and age structure of populations of
Carpoglyphus lactis (L.) (Acarina, Glycyphagidae) in closed cultures. Ekol. Pol. Ser.
A. 12:355-367.
7
Life-History Patterns of Astigmatid Inhabitants

of W ater-Filled Treeholes
Norman J. Fashing
CONTENTS
I. INTRODUCTION
2. CHARACTERISTICS OF WATER-FILLED TREEHOLES
2.1 The Treehole Habitat
2.2 Arthropod Inhabitants of Treeholes
3. BEHAVIOR OF ASTIGMATID INHABITANTS OF TREEHOLES
3. I Feeding Behavior and Morphology
3.2 Dispersal Patterns
4. LIFE-HISTORY AND REPRODUCTIVE PATTERNS
4.1 Survivorship Curves
4.2 Life-History Parameters
4.3 Fecundity
4.4 Survival During Periods of Starvation
4.5 Habitat and Niche Breadth
5. SUMMARY
I. Introduction
It has been known for well over 100 years that certain terrestrial plants hold small
bodies of water, and that these bodies of water often contain communities of
aquatic arthropods (Fish 1983). Varga (1928) coined the term "phytotelmata"
(Greek: phyton = plant, telma = pool) to describe such habitats which include
the modified leaves of pitcher plants, inflated leafaxils of such plants as bromeli-
ads and palms, water-collecting flowers such as Heliconia, internodal spaces of
broken bamboo stems, and the water-collecting depressions on trees (treeholes).
In fact, Fish (1983) estimated that habitats suitable for aquatic arthropod develop-
ment can be found in over 1500 plant species.
In recent years, phytotelmata have received considerable attention as micro-
cosms which can be easily manipulated to investigate fundamental problems in
community ecology (see Phytotelmata: Terrestrial Plants as Hosts for Aquatic
160
Life-History Patterns of Astigmatid Inhabitants of Water-Filled Treeholes / 161
Insect Communities, 1983, edited by Frank and Lounibos). In this regard, water-
filled treeholes have been excellent subjects for the investigation of food-chain
length and food-web complexity (Kitching 1971, Kitching and Pimm 1985, Pimm
and Kitching 1987, Kitching 1987).
Water-filled treeholes occur in forest ecosystems throughout the world. In areas
of frequent rainfall, they contain standing water most of the year and can attain
a relatively permanent status. They provide a unique habitat for a number of
organisms, many of which are obligate residents. Indeed, it is the exclusive
habitat for several acarine species, as well as for the larval instars of certain
aquatic dipteran and coleopteran species (Kitching 1971, Fashing 1975a, Kitching
and Callaghan 1982, Kitching and Pimm 1985). It is the adaptation of the mite
fauna to this unique habitat that forms the focus of this chapter.
I have divided the chapter into five sections. Since habitat is an important
factor in shaping the life-history pattern of a species (Edwards 1988), the water-
filled treehole habitat is described first, followed by a brief description of the
arthropod inhabitants. I then focus on the most common mite inhabitants, the
Astigmata, in terms of trophic adaptation. Since the ability to utilize a spatially
scattered resource such as water-filled treeholes relies on an ability to disperse,
I have devoted a section to dispersal patterns. The fourth section considers general
life-history and reproductive patterns common to astigmatid treehole dwellers.
Finally, a brief summary concludes the discussion.
2. Characteristics of Water-Filled Treeholes
2.1 The Treehole Habitat
A water-filled treehole (hereafter referred to simply as treehole) is defined as any

cavity created by the natural morphology of a tree or any other depression on the
surface of a tree which is capable of collecting and retaining water. Treeholes
may be classified as "pans," which have an unbroken bark lining and are formed
by the natural growth of the plant (e.g. the divergence oflimbs or buttress roots),
or "rot-holes" which lack a bark lining and have a layer of decomposing wood
below. Rot-holes are a result of injury to the tree and may eventually enlarge due
to further decomposition of tissue or they may decrease in size due to callus
formation (Kitching 1971).
Obligate arthropod inhabitants can exploit only those treeholes which contain
some water throughout the year. Free water may evaporate during periods of low
rainfall, high temperatures, low humidity, and/or wind, but the treehole debris
must remain sufficiently moist to provide a refuge for the organisms until rain
replenishes the water (Fashing 1975a). During severe drought, smaller treeholes
can dry completely causing most (if not all) of the arthropod inhabitants to perish.
Treehole communities are generally simple in both energy flow and species
composition (Fish and Carpenter 1982). In temperate deciduous forests, autumn-
162 / N. J. Fashing
shed leaves landing in the treeholes provide the main allochthonous energy source.
Additional nutrients may be derived from dissolved and suspended materials in
stem flow (water that runs down the bark during rains) (Carpenter 1982), addi-
tional drifting plant matter, and from arthropods which fall into the treehole and
die (Fashing 1975a). The treehole community is therefore a detritus based system.
Detrital layering partitions the treehole into microhabitats. The uppermost layer
consists of the air-water interface. The second layer is composed of the most
recently added leaves in a state of initial decay. Most insects and mites inhabit
this second layer. The third layer consists of leaf-mold; leaves which are in more
advanced stages of decomposition due to the action of bacteria. If the treehole
lacks a bark lining, there is an additional layer of decomposing sapwood (Snow
1958, Kitching 1971).
Microorganisms playa vital role in the treehole community. Through detritus
cycling, they increase the available nutrient content of the leaf litter for the
macroinvertebrates (Suberkropp and Klug 1976). Microbial activity in the tree-
hole is limited by low temperature in fall and winter. In spring, fungi invade the
leaf litter and synthesize extracellular enzymes (pectinases and cellulases) to
break down the leaves (Suberkropp and Klug 1976). Fungal hyphae cover the
leaves and extend above them, and macroinvertebrates graze on the fungal hy-
phae. Together the fungi and the macroinvertebrates break the leaves into pieces.
This process increases the total surface area of leaves and prepares them for
bacterial invasion. As the number of bacteria increases, the fungal count decreases
(Suberkropp and Klug 1976): Fungi are therefore important in the initial stages
of leaf decomposition and bacteria complete the process of leaf decay.
Leaves from different tree species vary in their concentration of lignins, tan-
nins, etc., which in turn influences the type of microbial growth a leaf can
support. Leaf palatability for treehole herbivores depends on the fungal complex
that attacks the leaves initially. The available protein of leaves can double de-
pending on the dynamics of fungal growth (Kaushik and Hynes 1971). Therefore
the food preferences of detritus feeders are dependent not only on the species of
a decaying leaf and the particular stage of decay, but also on the colonizing fungal
species.
Since autumn-shed leaves are the primary energy resource for the treehole
community, energy input is primarily restricted to one short period during the
year. There is a heavy demand on this common resource and it is often exhausted
by mid or late summer. This creates a "lean period" for many treehole arthropods,
often lasting two months or more (Fashing 1975a). However, this "lean period,"
like winter, is a cyclical and therefore a predictable stress and one to which
treehole organisms must adapt.
2.2 Arthropod Inhabitants of Treeholes
A large diversity of organisms collected from water-filled treeholes are repre-
sented in the faunal record (e.g. Lacky 1940, Snow 1949, Rohnert 1950). Many
of these can be considered transient or accidental visitors to this community (the

"Dendrolimnetoxenen", Rohnert 1950), and others are simply attracted to any
moist or semiaquatic habitat (the "Dendrolimnetophilen", Rohnert 1950). This
chapter concerns the "Dendrolimnetobionten" (Rohnert 1950), organisms which
are obligate inhabitants of treeholes and seldom, if ever, found elsewhere. These
obligate residents are: mid to polysaprophytic, eurythermic, resistant to changes
in water chemistry (e.g. solute concentration and pH), able to withstand freezing,
and have a high tolerance for dessiccation (Rohnert 1950). To this list I add the
requirement that they must also be tolerant of relatively long periods with little
food.
In most cases, the obligate insect fauna of treeholes consists of only a small
number of species in any given locality. They are present as larvae and include
members of the dipteran families Ceratopogonidae, Chironomidae, Culicidae,
Psychodidae, and Syrphidae, as well as the coleopteran family Scirtidae (Fig.
7. I). These insect families are present in treeholes throughout the temperate
regions of the world, with the exception that the Chironomidae are not represented
in North America.
Other than an occasional notation concerning the observation of their presence
(e.g. Lackey 1940), the first published literature on mites from treeholes appeared
in 1973 (Fashing 1973). Between 1973 and 1980, four species were described
Figure 7.1. Common inhabitants of water-filled treeholes in eastern North America.

(Not drawn to scale). a) Culicidae, b) Ceratopogonidae, c) Psychodidae, d) Astigmata, e)
Syrphidae, f) Scirtidae.
164 / N. 1. Fashing
from North American treeholes (Fashing 1973, 1974; Fashing and Wiseman
1980) and North America remained the only known location for treehole mites
until Kitching and Callaghan reported acarine inhabitants from southeast Australia
in 1982. To date, eight species of mites representing five families have been
reported in the literature (Table 7.1). In addition, R. F. C. Naczi has found four
new species of histiostomatids from treeholes in North America (pers. comm.).
3. Behavior of Astigmatid Inhabitants of Treeholes
Life-history studies have been conducted on only three treehole mite species, all
of which are astigmatid mites: Naiadacarus arboricola, Algophagus pennsylvani-
cus, and Hormosianoetus mallotae (Fig. 7.2). In particular, much is known
concerning the biology of N. arboricola, some concerning A. pennsylvanicus,
and a smaller amount concerning H. mallotae. The remaining portion of this
chapter deals primarily with these three species.
N. arboricola is found throughout the midwestern and eastern United States,
having been recorded from: Arkansas, Florida, Illinois, Kansas, Michigan, Min-
nesota, Missouri, New Hampshire, New Jersey, New York, Oklahoma, Pennsyl-
vania, South Carolina, Texas, and Virginia (Fashing 1974, unpublished; OConnor
1989; Naczi, pers. comm.). H. mallotae probably shares the same distribution,
but has been collected in fewer locations: Kansas, Oklahoma, Arkansas, Illinois,
Michigan, Pennsylvania, Virginia and Florida (Fashing 1973; Naczi, pers.
comm.; OConnor, pers. comm.). A. pennsylvanicus is recorded thus far from
Table 7.1. Acarine Inhabitants of Water-Filled Treeholes.

Taxon Locality References
Mesostimata:
Ascidae
Cheiroseius sp. S.E. Australia Kitching and Callaghan (1982) .
Prostigmata:
Arrenuridae
Arrenurus kitchingi Smith & Harvey S. E. Australia Smith and Harvey (1989)
Astigmata:
Acaridae
Naiadacarus arboricola Fashing Eastern USA Fashing (1974)
Naiadacarus oregonensis Fashing Oregon, USA Fashing (1974)
Algophagidae
Algophagus pennsylvanicus Fashing &
Wiseman Eastern USA Fashing and Wiseman (1979)
New Species 1 S.E. Australia Kitching and Callaghan (1982)
New Species 2 S.E. Australia Kitching and Callaghan (1982)
Histiostomatidae
Hormosianoetus mallotae (Fashing) Eastern USA Fashing (1973)
F ig " " 7.2
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165
166 / N. J. Fashing
only four states: Oklahoma, Michigan, Pennsylvania and Virginia (Fashing and
Wiseman 1980; Fashing, unpublished; Naczi, pers. comm.; OConnor, pers.
comm.).
Of the three species, N. arboricola is the most common in terms of occurrence
in treeholes as well as numbers within a treehole, and A. pennsylvanicus is the
second most common. H. mallotae is relatively rare, occurring in less than five
percent of the treeholes and usually in low numbers (Fashing and Campbell,
unpublished). In areas of sympatry, all three species may be found occupying the
same treehole, although such instances are rare. The simultaneous occurrence of
N. arboricola and A. pennsylvanicus, however, is quite common.
3.1 Feeding Behavior and Morphology
Since decaying leav.:s are the energy base for the treehole community, and since
food is usually the most limiting resource for an animal species, one would
expect vigorous competition for this common resource. Partitioning of resources,
therefore, may account for the successful sympatric coexistence of tree hole mites.
Examination of the mouthparts of N. arboricola, A. pennsylvanicus, and H.
mallotae reveals important morphological differences (Fig. 7.3). H. mallotae
differs considerably from the other two species by possessing an elongate soleni-
dion as well as a long eupathidial seta on the terminal segment of the pedipalp.
In addition, it has chelicerae with no movable digit and the fixed digit is serrated
and rakelike, bearing 18-20 small teeth (Fig. 7. 3C) (Fashing unpublished).
Observations on feeding behavior indicate that H. mallotae does not feed on
coarse particulate matter, but like most other members of the Histiostomatidae
collects fine particulate matter from the fluid medium (Hughes 1953, Krantz
1978, OConnor 1982a, 1984). The whiplike pedipalps are used to move small
particles in the fluid medium toward the tip of the rostrum where they are raked
into the mouth by the back and forth movement of the chelicerae (Hughes 1953).
Members of this species are often observed on leaves near the water surface
feeding from the area just below the surface film, an area rich in fine particulate
matter as well as microbes (= filtering collector, Cummins and Klug 1979). At
other times they feed at the leaf surface, using the pedipalps to stir up fine
particulate matter and microbes (= gathering collector, Cummins and Klug 1979)
(Fashing unpublished).
N. arboricola and A. pennsylvanicus differ considerably from H. mallotae in
that their mouthparts are the typical sarcoptiform type with chelate chelicerae and
short solenidia and setae on the terminal ends of the pedipalps (Figs. 7 .3A, 7.38).
However, scanning electron microscopy reveals quite distinct morphological
differences between the chelicerae of N. arboricola and A. pennsylvanicus which
in tum are correlated with a difference in mode of feeding (Fashing and Campbell
1992, Fashing unpublished).
The cheliceral bases of A. pennsylvanicus are less massive than those of N.
Life-History Patterns of Astigmatid Inhabitants of Water-Filled Treeholes I 167
Figure 7.3. Scanning electron photomicrographs of the mouthparts of astigmatid mites

from water-filled treehoIes. (Scale bar = 10jLm). A) Naiadacarus arboricola, B) Algopha-
gus pennsylvanicus, C) Hormosianoetus mallotae, D) Undescribed species of algophagid
from S.E. Australia.
arboricola (Figs. 7.3A, B), indicating less musculature to the movable biting
digits. In addition, the fixed and movable digits of A. pennsylvanicus are not as
robust. Further examination indicates that the biting digits of N. arboricola have
strong teeth over the entire biting surfaces of both digits, and that these teeth
interlock when the digits close (Fig. 7.3A). Such chelicerae are adapted for biting
and crushing (Fashing unpublished). The biting digits of A. pennsylvanicus, on
the other hand, have teeth only on the basal portion of the movable digit, the
entire biting surface being adapted for cutting and shearing. The biting edges
slide past each other in a scissor-like manner when the digits close. Furthermore,
the tips of the biting digits curve mesially and are serrate or rake like (Fig. 7.3B)
(Fashing and Campbell 1992).
Behavioral correlates are consistent with the morphological differences ob-
served in N. arboricola and A. pennsylvanicus. Control leaves left without mites
remain intact and become covered with mats of fungal hyphae, whereas leaves
on which N. arboricola are cultured are skeletonized (Fashing 1975a, unpub-
lished). In contrast, leaves on which A. pennsylvanicus are cultured show no
evidence of skeletonization, however an examination of the leaf surface reveals
only small amounts of fungi (Fashing and Campbell 1992). It is apparent that N.
168 / N. 1. Fashing
arboricola feeds by biting chunks out of leaves (= shredder, Cummins and Klug
1979), thereby ingesting leaf material along with any associated microbes. A.
pennsylvanicus, on the other hand, feeds by grazing fungal hyphae from the
leaf surface (= scraper, Cummins and Klug 1979). Direct observation of A.
pennsylvanicus also reveals a possible second mode of feeding behavior. Individu-
als are often found on leaves or other substrate near the surface film, where they
can be seen rapidly extending and retracting their chelicerae through the surface
film in an alternating manner. The surface film is rich in microbes and fine
particulate matter, and it appears that the serrated distal ends of the chelicerae
are used to feed on this resource (= filtering collector, Cummins and Klug 1979)
(Fashing and Campbell 1992).
In summary, feeding behavior and diet differ for the three species of treehole
mites. N. arboricola feeds on coarse particulate organic matter by biting chunks
out of leaves. This type of herbivore is typically called a "shredder" and is the
most common form in a detritus based system (Barlocher and Kendrick 1973,
Cummins and Klug 1979). A. pennsylvanicus feeds by shearing fungal hyphae
from the leaf surface with specialized chelicerae. It is a "scraper" (= grazer)
and represents the second most common type of detritus feeder (Barlocher and
Kendrick 1973, Cummins and Klug 1979). In addition, it is possible that A.
pennsylvanicus filters fine particulate organic matter from the surface film and is
therefore a filtering "collector" as well. And finally, H. mallotae has mouthparts
highly specialized for feeding on fine particulate organic matter and appears to
be an extremely efficient filtering and gathering "collector." Little is known
concerning the diet of other species of tree hole mites, however a cursory examina-
tion of one of the two Australian species utilizing SEM suggests it is a shredder
(Fig. 7.30). Studies on resource partitioning by the Australian species will prove
quite interesting since they are closely related members of the same family
(Algophagidae).
3.2 Dispersal Patterns
In most free-living astigmatid mites, dispersal is effected by a highly specialized

and facultative deutonymphal instar (hypopus) (Fig. 7.4). The hypopus, in con-
trast to other instars, is heavily sclerotized and resistant to desiccation. It has a
greatly reduced gnathosoma without a mouth or mouthparts, and bears a ventral
sucker plate as well as specialized tarsal setae utilized for phoretic attachment to
other organisms (OConnor 1982b, Houck and OConnor 1991).
In most free-living species, the hypopus is present in low numbers or totally
absent in a population as long as the habitat is favorable for population growth.
However, when environmental conditions become unfavorable, protonymphs
molt into hypopi (deutonymphs) rather than directly into tritonymphs. The hypopi
then await and attach to organisms that utilize the same habitat, and are then
carried by them to a fresh habitat where they leave the host, molt into tritonymphs,
LARVA
~
TRITONYMPH
.j).)Cf~~~
I
" 'I'
PROTONYMPH
\
,, /
--
/
DEUTONYMPH
(Hypopus)
Figure 7.4. Life cycle of Hormosianoetus mallotae, typical of the Astigmata except that
this species is larviparous. A quiescent period occurs at the end of each immature stadium,
after which ecdysis occurs. Note the heteromorphic deutonymphal instar (hypopus). which
is phoretic.
169
170 I N. J. Fashing
and resume their normal life cycle. In this new habitat they may undergo several
generations before dispersal, and therefore significant hypopal formation again
becomes an important part of their life history.
Both N. arboricola and H. mallotae conform to the basic astigmatid life cycle
containing a facultative hypopus. They do not, however, form hypopi in response
to adverse environmental conditions. Rather, hypo pi are formed seasonally (only
during May and June) when environmental conditions in treeholes appear optimal
for population growth (Fashing 1976a). Decomposing leaves (the energy base)
are most abundant in spring, and spring rainfall maintains a high water level in
treeholes. If adverse conditions stimulated dispersal, hypopi would be found
during late summer or early autumn when the food is usually depleted and drying
of treeholes more frequent (Fashing 1976a).
In laboratory studies, N. arboricola did not form hypopi in response to over-
crowding, accumulation of waste products, gradual evaporation of water, and/or
lack of food (Fashing 1976a). No hypopal formation resulted among mites reared
from larvae on leaves of tree species found to be inadequate for complete develop-
ment and/or adult reproductive success (Fashing 1975b). In addition, no hypopal
formation was observed under thermal stress. Protonymphs maintained at 2°C
for four months molted into tritonymphs when transferred to 25°C, bypassing the
hypopal stage. Mites reared at 15°C developed into tritonymphs but did not
progress beyond this stage (Fashing 1975b). When cultured at 30°C, protonymphs
died without completing development (Fashing 1976a).
Studies on Sancassania boharti (Cutcher and Woodring 1969), a free-living
astigmatid mite, suggest that any adverse condition which retards protonymphal
development might induce hypopal development. However, N. arboricola reared
on seven different resources of varying nutritional values resulted in a wide range
of time spent in the protonymphal instar (means of 2.7-7.7 days), but no hypopal
formation (Fashing 1975b).
In summary, hypopal formation could not be induced by adverse environmental
conditions in the laboratory (Fashing 1976a). Field observations also reveal no
direct correlation between adverse conditions and hypopal formation. The relative
incidence of hypopi in treeholes in areas of predominantly red oak, the leaves of
which are known to be of limited nutritional value for N. arboricola, is no higher
than in areas where the predominant tree species have leaves of high nutritional
value (Fashing 1976a). In the same treehole, one can find some protonymphs
transforming into hypopi and others into tritonymphs. This occurs even in tree-
holes with substantial numbers of hypo pi. These treeholes will continue to support
mite populations throughout the rest of the year and in subsequent years. It is
also interesting that hypopi not encountering a host simply transform to trito-
nymphs after a period of time even though they are still in the same treehole in
which they previously transformed to hypopi (Fashing 1976a).
All evidence, both field and laboratory, therefore indicates that adverse environ-
mental conditions do not induce hypopal formation in N. arboricola. Although
Life-History Patterns of Astigmatid Inhabitants of Water-Filled Treeholes I 171
H. mallotae has not been studied as extensively, evidence to date indicates that
it follows the same pattern as N. arboricola. This pattern makes sense when one
considers the water-filled treehole habitat in which these species live. Once a
treehole is formed, it remains a part of the forest ecosystem for a number of
years, both in location and in physical characteristics. Fish (1983) estimated the
turnover time for treeholes in an oak woodlot in Indiana to be approximately lO
years. My estimate for both eastern Kansas and eastern Virginia is 15-20 years.
In either case, treeholes provide a reasonably permanent and stable habitat for an
arthropod.
The stability of habitat might also be indirectly inferred from the relatively
large number of obligate inhabitants (Snow 1949). Treehole inhabitants are
guaranteed a recurring food supply from the autumn leaf fall, and such resource
replenishment occurs simultaneously in all treeholes in a given geographic area.
In addition, environmental stress in any locality would probably also be shared
equally.
To disperse in response to adverse conditions would not be beneficial since a
dispersing mite would almost certainly encounter similar adverse conditions in
another proximate treehole (Fashing 1976a). The answer to the question concern-
ing the evolution of dispersal behavior in N. arboricola and H. mallotae may lie in
the degree of permanence of the water-filled treehole habitat. In this environment,
selection would favor dispersal when conditions are optimal, thus maximizing
the success of the dispersers. It can be hypothesized that the hypopi of these two
species have evolved to serve purely as dispersal agents for colonization and
outcrossing, not as agents to escape a declining environment (Fashing 1976a).
This is probably also true for the insect hosts on which the mites are phoretic;
the adults of the eristaline syrphid flies M allota posticata and M. bautias. The
larvae of these flies are "rat-tailed" maggots which inhabit the lower levels of
leaf debris in water-filled treeholes (Fig. 7.1). Adults are present only in May
and June, and hypopi utilize female flies for dispersal. Female flies return to
treeholes to oviposit, while males seldom reenter treeholes and are therefore
ineffective agents for dispersal (Fashing 1976a).
Evidence to date indicates that only females of H. mallotae disperse as hypopi.
Of 19 hypopi reared to adults, all were female (Fashing, unpublished). In all
histiostomatid mites thus far examined, sex is determined by arrhenotoky with
fertilized eggs being female and unfertilized eggs male (Norton et al. 1992), and
H. mallotae is no exception (Fashing, unpublished). If individuals developing
from hypopi are arrhenotokous females, it is not necessary for both sexes to
disperse since female dispersers can produce male offspring which in tum mate
with them. It is of interest that the development to adulthood of H. mallotae
reared at 25°C is significantly faster for males than for females (males, mean =
14.8 days; females, mean = 19.8 days) (Fashing, unpublished). Since there are
usually many dispersers on a fly, it is improbable that a female migrant will mate
with her own sons.
172 / N. J. Fashing
In N. arboricola sex is determined by diplo-diploidy, thereby necessitating

simultaneous dispersal by males and females. Unlike H. mallotae, the immature
development rate is not significantly different for the two sexes (Fashing 1975b).
Little is known concerning dispersal in A. pennsylvanicus. Like other known
members of the subfamily Algophaginae, the hypopus (deutonymph) is absent
from its life cycle. Which instar(s) is used for dispersal is unknown. Evidence to
date indicates, however, that even without a hypopal stage, A. pennsylvanicus
may be as efficient at dispersal as N. arboricola (Fashing unpublished).
4. Life-History and Reproductive Patterns
The life-history patterns of obligate treehole astigmatid mites are probably best
introduced by stating that they emulate those of species referred to ecologically
as "K-selected" (Pianka 1970) or "equilibrium species" (Albert 1983).
There have been a number of critical appraisals of r- and K-selection theory in
recent years (e.g. Steams 1977, Ito 1980, Boyce 1984, Begon 1985). It is not
my intent to provide yet another appraisal concerning the limitations of this theory
nor to accept or refute it, but rather to use its well known correlates (Pianka 1970)
as a convenient focal point for discussion of treehole astigmatid mites (Table
7.2). A comparison among species or popUlations is necessary to label an attribute
as "r-selected" or "K-selected" (Force 1975), and such relative statements of
selection must involve organisms of similar type (Begon and Mortimer 1986). I
will therefore make comparisons whenever possible, and such comparisons will
be made with "peer species"; that is, other free-living astigmatid mites. It should
be pointed out, however, that detailed life-history studies of astigmatid mites
have dealt primarily with pest species and that such species tend to have r-type
life histories. My comparisons are therefore mainly with so called "r-selected
species" (Tables 7.3 and 7.4). OConnor (this volume) provides life-history data
for several additional species I did not include since only limited data is available
concerning their biologies. When more is learned concerning their life histories,
it may well tum out that several are "K-selected" species.
4.1 Survivorship Curves
K-type species typically demonstrate a Type I survivorship curve (= low mortality

until old age) or Type II survivorship curve (= constant mortality rate for all age
groups) (Deevey 1947). An r-type species, on the other hand, has a characteristic
Type III survivorship curve (= high mortality in young age groups) (Deevey
1947).
Survivorship curves have been determined for Naiadacarus arboricola and
Algophagus pennsylvanicus; the former exhibits a Type I curve (Fashing 1975b)
and the latter exhibits a curve intermediate between Type I and Type II (Fashing
and Campbell, unpublished). As far as I know, however, all investigations on
L(fe-History Patterns of Astigmatid Inhabitants of Water-Filled Treeholes / 173
Table 7.2. Some Correlates of r- and K-Selection as Related to Tree-Hole Astigmatid

Mites: Generalities Adapted from Pianka (1970).
r-Selection K -Selection
Climate and Variable and/or Fairly Constant and/or

Habitat: Unpredictable Predictable
(Uncertain) (More Certain)
Mortality: Often Catastrophic, More Directed,

Nondirected
Density-independent Density-dependent
Survivorship: Often Type III (Deevey 1947)* Usually Type I and II (Deevey 1947)*
Population Size: Variable in Time Fairly Constant in Time

Nonequilibrium Equilibrium
Usually Well Below Carrying At or Near Carrying
Capacity Of Environment Capacity of Environment
Unsaturated Communities Saturated Communities
(or portions thereof)
Recolonization Each Year No Recolonization Necessary
Ecological Vacuums
Intraspecific and
Interspecific Variable, Often Lax Usually Keen
Competition:
Selection favors: 1) Rapid Development I) Slower Development

2) High r m" 2) Lower Resource Thresholds
3) Early Reproduction 3) Delayed Reproduction
4) Small Body Size 4) Larger Body Size
5) Single Reproduction 5) Repeated Reproduction
6) Parental Care
7) Greater Competitive Ability
Length of life: Usually Shorter Usually Longer
Leads to: High Productivity High Efficiency
* Deevey, E. S., Jr. 1947. Life tables for natural populations of animals. Quart. Rev. Bioi. 22:
283-314.
mortality of astigmatid mites have been conducted in the laboratory under re-
stricted conditions. Given this fact, it may be unrealistic to use these lab-derived
survivorship curves for comparison (also see arguments of Norton, this volume).
Under optimal conditions in the laboratory, all species, whether r- or K-type,
would almost certainly demonstrate Type I or II curves. Likewise, given a poor
nutritional source for the same species, a Type III and even a Type IV curve
(Slobodkin 1964) could be generated (see Fashing 1975b for a discussion of the
influence of diet on N. arboricola). Survivorship data collected on field popula-
tions would clearly be more meaningful, but such data is not available and would
be quite difficult (if not impossible) to generate.
Table 7.3. Comparative Life History Data for Varioas Free-living Astigmatid Mite Species. Data Other than Egg Mortality is Expressed as Means.
Time Periods in Days. NG = Not Given; NA = Not Applicable. ~ = Treehole species.
Pre-
Egg-4 Larva--+ % Egg Repro. 1st Repro. Tot. Eggs/
Larva Adult Mort. Period Repro. Period # Eggs Day Longev.
Taxon (Diet) °C 2 3 4 5 6 7 8 9 References
ALGOPHAGIDAE
~Algophagus pennsylvanicus 25 NA 17.9 0.0 6.5 24.4 11.0 18 1.6 44.2 Fashing & Campbell
(Fusarium oxysporum) (unpublished)
HISTIOSTOMA TIDAE
Histiostoma polypori 26 0.9 2.4 NG 1.0 4.3 6.0 74 15.9 14.1 Behura (1957)
(Decomposing insects &
plants)
~Hormosianoetus mal/otae 25 NA 19.2 0.0 NG NG NG NG NG 73.0** Fashing (unpublished)
(Microbes on Green Ash
leaves)
ACARIDAE
--~ Acarus siro 20 4.9 NG 12.5 2.0 NG 23.6 634 26.9 28.1* Cunnington (1985)
(Wheat germ) 25 4.2 NG 18.9 1.0 NG 16.9 365 21.9 20.2*
Histiogaster arborsignus 23 4.0 10.1 NG NG NG NG 715 21.9 46.7 Woodring (1969)
(Brewer's yeast)
H. rotundus 23 4.0 8.0 NG NG NG NG 771 29.1 38.5 Woodring (1969)
(Brewer's yeast)
~Naiadacarus arboricola 20 NA 30.2 0.0 11.4 41.6 55.5 35 0.6 214.6 Fashing (l975b)
(20', 25"=Green Ash; 25" NA 17.0 0.0 8.2 25.2 43.3 62 1.4 82.8
25'2=American Elm; 25'2 NA 17.2 0.0 7.3 24.5 57.6 132 2.3 101.7
25']= Bitternut Hickory 25'3 NA 15.2 0.0 6.8 22.0 97.0 85 0.9 133.1
leaves)
Rhizoglyphus echinopus 23 5.0 11.2 NG NG NG NG 285 13.4 39.5 Woodring (1969)
(Dead mealworms)
R. robini 27 3.8 7.2 18.6 0.9 11.8 25.6 661 25.8 42.2 Fashing & Hefele (1991)
(Bot & Meyer's medium)
Sancassania anomalus 15 6.5 8.3 48.0 3.9 18.7 NG NG NG NG Pillai & Winston (1969)
(Escherichia coli/Bonner's 20 3.6 6.2 27.8 2.1 12.1 21.4 738 34.5 31-45
medium) 25 3.9 5.4 21.8 NG NG NG NG NG NG
30 2.4 3.6 50.0 1.3 7.3 NG NG NG NG
ACARIDAE
Sancassania anomalus 23° 3.0 6.5 NG 2.0 11.5 NG 930 45.0 32.9 Woodring (1969)
(Dead mealworms)
S. rodriguezi (Xenic diet) 25" 2.4 5.6 25.0 1.5 9.6 12.5 588 47.1 23.6 Rodriguez & Stepien (1973)
Schwiebia falticus 23° 2.0 9.2 NG NG NG NG 155 4.5 46.2 Woodring (1969)
(Brewer's yeast)
S. rocketti (Brewer's yeast) 23° 2.0 11.2 NG NG NG NG 125 3.9 45.5 Woodring (1969)
Suidasia nesbitti (Wheat germ) 28 3.2 9.7 4.0 NG NG 8.3 140 16.9 29.2 Mathur and Dalal (1989)
Tyrophagus putrescentiae 20" 8.0 9.1 26.0 3.1 20.2 29.1 276 9.4 44.2 Rivard (I961a, 1961b)
(Aspergillis) 25" 5.3 7.3 44.5 2.1 14.7 23.2 255 11.0 27.8
30 4.8 6.0 49.5 1.9 12.7 10.8 101 9.4 19.0
T. putrescentiae 27" 4.5 9.5 6.5 2.2 16.2 11.8 118 10.0 NG Kumud & Mathur (1989)
(Wheat Flour + Yeast)
CARPOGL YPHIDAE
Carpoglyphus lactus 20° 4.0 8.0 11.0 NG NG NG 261 NG 33.0 Chmielewski (1971)
--
~ (Brewer's yeast) 25" 3.0 6.0 14.0 2.0 11.0 NG 278 NG 29.0
30° 3.0 6.0 15.0 NG NG NG 76 NG 20.0
GL YCYPHAGIDAE
Glycyphagus destructor 25° 4.1 12.2 49.0 3.2 19.5 28.8 140 4.9 39.1 Chmielewski (1987)
(Wheat germ + Baker's
yeast)
Glycyphagus domesticus 25' 4.2 14.7 63.0 3.7 22.6 18.1 51 3.3 35.1 Chmielewski (1988)
(Wheat germ + Baker's
yeast)
PYROGL YPHIDAE
Dermatophagoides pteronyssinus 23° 8.1 25.6 14.0 ~4 38.0 26.2 68 2.8 56.8 Arlian et al. (1990)
(Animal Protein + Yeast) 35 3.9 11.1 13.0 <2 17.0 11.6 48 4.3 26.6
*Adult longevity,
**Maximum observed.
Table 7.4. Comparative Statistics on the Population Dynamics of Various Astigmatid Mites.
Species (Diet) C rm (Days) "(Days) "(Weeks) References
A cotyledon formosani 25 0.46 1.59 25.20 Phillipsen & Coppel (1977)

(Wax moth medium)**
Carpoglyphus lactus 20' 0.23 1.26 4.93 Chmielewski (1971)
(Baker's yeast) 25 0.29 1.34 7.61
30 0.23 1.26 4.93
Glycyphagus destructor 25 0.13 1.13 2.41 Chmielewski (1987)
(Wheat germ & yeast)
Glycyphagus domesticus 25 0.12 1.12 2.25 Chmielewski (1988)
(Wheat germ & yeast)
Rhizoglyphus robini (Garlic) 27 0.22 1.24 4.60 Gerson et al. (1983)
(Peanuts) 27 0.29 1.33 7.35
(Bot & Meyer's medium*) 27 0.26 1.29 5.98 Fashing & Hefde (1991)
Sancassania berlesi 25' 0.38 1.46 13.85 Rodriguez & Stepien (1973)
--~ (Artificial diet)
Tyrolichus casei 30 0.36 1.43 12.00 Nangia & ChannaBasavanna (1989)
(Wheat bran & yeast)
Tyrophagus putrescentiae 28 0.20 1.22 4.10 Barker (1967)
(Brewer's yeast) 30' 0.27 1.30 6.41
32" 0.33 1.39 9.92
34' 0.21 1.23 4.24
Naiadacarus arboricola
(Green Ash leaves) 25' 0.09 1.09 1.86 Fashing (I 975b)
(American Elm leaves) 25 0.12 1.12 2.25
(Bitternut Hickory leaves) 25' 0.10 1.10 2.01
Algophagus pennsylvanicus 25 0.07 1.07 1.60 Campbell & Fashing (unpublished)
(Fusarium oxysporum)
* Bot and Meyer 1969.

** Beck 1960.
4.2 Life-History Parameters
Long life, slow immature development, delayed onset of reproduction and low
fecundity are attributes of K-type species. Table 7.3 compares these demographic
statistics, where known, for three treehole species (N. arboricola, A. pennsylvani-
cus, and H. mallotae) with a number of mostly r-type free-living astigmatid
species.
N. arboricola demonstrates much greater longevity than other free-living astig-
matid mites (Table 7.3, column 9), and A. pennsylvanicus and H. mallotae are
at the high end of the longevity range. All three treehole species demonstrate an
exceptionally long development time as immatures (column 2). The time interval
from adult molt to first reproduction (prereproductive period; column 4) is consid-
erably longer for both N. arboricola and A. pennsylvanicus. This coupled with
a long immature development extends the period before first reproduction dramati-
cally (column 5), thus constituting a delayed reproduction when compared to the
other species. At least part of the delay is due to larviparity, a characteristic
shared by all three treehole species (Fashing 1975a). Most astigmatid mites are
oviparous, with a comparatively long embryonic development taking place out-
side the mother's body (column 1). Egg mortality can be high in oviparous species
(column 3), but this source of mortality is virtually eliminated in larviparous
species. Larviparity might be considered a type of parental care since eggs are
retained within the mother until hatching; parental care is yet another characteristic
of K-type species.
4.3 Fecundity
Relative fecundity is quite low in N. arboricola and A. pennsylvanicus. For both,

the average number of young produced per day (Table 7.3, column 8) and over
a lifetime (column 7) fall well below that for the r-type species. In fact, the
maximum number of young produced by N. arboricola over a 24-hour period
was nine (Fashing 1979). In contrast, 35 has been recorded for Sancassania
anomalus (Pillai and Winston 1969),47 for S. rodriguezi (Rodriguez and Stepien
1973), and 52 for Rhizoglyphus robini (Gerson et al. 1983).
The above demographic characteristics can be summarized using the intrinsic
rate of increase, rm (Birch 1948). K-type species are typified by a low rate of
increase and r-type by a high rate. The rates of increase for the two treehole
inhabiting species (N. arboricola andA. pennsylvanicus) are quite low in compari-
son to most other species (Table 7.4). Such information can also be summarized
using the finite rate of increase (lambda = factor by which the population increases
during a time interval) (Table 7.4). To put this into perspective, in one week
under optimal laboratory conditions a population of R. robini would increase
7.35 times, Carpoglyphus lactus 7.61 times, Tyrophagus putrescentiae 9.92
178 / N. 1. Fashing
times, Tyrolichus casei 12.0 times, and Sancassania rodriguezi 13.85 times.] In
the same time interval, however, a population of N. arboricola would increase
only 2.25 times and one of A. pennsylvanicus only 1.60 times. It is quite
apparent that the reproductive pattern of treehole astigmatid mites results in a low
reproductive potential relative to most other astigmatid mites.
4.4 Survival during Periods of Starvation
The ability to endure periods with limited food resources is yet another life-
history trait of K-type species. As discussed above, autumn-shed leaves are the
primary energy source for the treehole and this source is often depleted by late
summer. In addition, treehole species may be unable to feed during periods when
lack of rain has eliminated "free water" in the treehole. N. arboricola, the only
treehole species studied in this regard, is adapted to withstand long periods
without food. In laboratory experiments at 25°C, the average longevity without
food for the various instars was found to be: tritonymph 83 days, protonymph 52
days, male 37 days, female 37 days, and larva 10 days (Fashing 1976b). In
contrast, instars of C. lactus maintained at optimal temperature and humidity
(25°C, 85% RH) without food had much lower longevities: tritonymph 15 days,
proto nymph seven days, adults 29 days, and larva five days (Chmielewski 1971).
It is clear that N. arboricola is well adapted to cope with these stressful and cyclic
levels of food availability.
4.5 Habitat and Niche Breadth
Habitat characteristics of r- and K -type species also differ. Generally, r-type

species utilize transient and unpredictable habitats. They also tend to be opportu-
nistic, often feeding on a wide range of substrata and under a wide range of
environmental conditions. T. putrescentiae may be found almost anywhere that
humidity is high and fungus is present. This species has been observed feeding
and reproducing on fungi, lichens, algae, grass clippings, and dead or injured
mites, as well as on live nematodes (Walter et al. 1986). In addition, it has been
reared at temperatures as low as 10°C and as high as 35°C (Cunnington 1969).
Schwiebea rocketti was observed to feed on decaying root material, decomposer
fungi, nematode-destroying fungi, and small soil invertebrates including nema-
todes and protozoa (Walter and Kaplan 1990). C. {actus has been reared at
temperatures from 3°C-45°C (Chmielewski 1971), Acarus siro from 5°C-30° C
(Cunnington 1965, 1985), and R. robini from 16°C-35°C (temperatures below
lAcotyledon!ormosani has been reported to have extremely high rates of increase (see Table 7.4);
e.g. it can increase its population by over 25 times in one week. However, careful examination of
the published life-history data (immature mortality 41%, immature development time 9.6 days,
oviposition period 14.6 days, oviposition rate 7.8 eggs/day, etc.) suggests an error was probably
made in calculating the intrinsic and finite rates of increase.
Life-History Patterns of Astigmatid Inhabitants of Water-Filled Treeholes ! 179
16°C were not attempted) (Gerson et al. 1983). Such r-type species have a wide
niche breadth in regard to habitat, range of diet, and temperature tolerance.
Obligate treehole astigmatid mites appear to have a much narrower niche
breadth. They inhabit only water-filled treeholes, and their diet range is more
restricted. N. arboricola, the only species studied in regard to temperature effects,
has a very restricted range for immature development. It has been reared success-
fully only at 20°C and 25°C. At 30°C molting is inhibited and death occurs, and
at 15°C development occurs only to the tritonymphal instar (Fashing 1975b). K-
type species evolve toward specialization in order to more efficiently utilize their
habitat. Treehole astigmatid species certainly fit this pattern.
Not all of the potential ecological correlates in Table 7.2 can be addressed in this
discussion. Some correlates are not addressed due to lack of basic information. We
know little concerning population trends of treehole mites (e.g. equilibrium vs.
nonequilibrium), and most sources of natural mortality are unknown. We do
know, however, that egg mortality is virtually eliminated due to larviparity, and
there are no known predators of mites in North American treeholes (Fashing
1975a). Only one density independent source of mortality is actually known for
treehole mite species; the extended period of drought leading to complete drying
of a treehole. However, except in treeholes which collect only a small volume
of water, this source of mortality is probably rare.
Other correlates yet unstudied include inter- and intra-specific competition. It
is thought, through the examination of mouthpart morphology, that there is little
(if any) interspecific competition for food among the three species of treehole
mites discussed. H. mallotae is a collector, A. pennsylvanicus is a scraper!
collector, and N. arboricola is a shredder. Among the treehole inhabitants there
are, however, insect larvae in all three of the above functional feeding groups
(collectors, shredders, and scrapers) (Merritt and Cummins 1978). Acarine-insect
competition and resource partitioning has not yet been studied.
Body size does not seem important when comparing peer species. In fact, in
mites a large female body size often indicates the production of a large number
of eggs and might thus even be associated with an r-rather than a K-type species.
Since even the longest lived free-living astigmatid species are univoltine and most
are multivoltine, the correlate of single vs. repeated reproductions is meaningless.
5. Summary
Due to their small size, it is quite difficult, if not impossible, to gather reliable
life-history data from natural populations of most astigmatid species and such data
is generally obtained from laboratory populations. Some caution must therefore be
taken when interpreting it in light of natural popUlations. Laboratory data does
provide, however, information on the known upper potential of a given species
and a comparison of such potentials between species is valid even if they are
never realized in nature.
180 I N. J. Fashing
While Pianka's (1970) correlates of r- and K -selection provide a convenient

means for describing the life-history and reproductive pattern of a species, they
do not constitute a currently accepted model for life-history evolution. 2 Over the
past two decades, a number of theories for life-history evolution have been
proposed, but all have their limitations. Each species has its own unique adaptive
response to its entire environment and perhaps a single all encompassing model
cannot be achieved without making it so simplistic as to be useless. To reiterate
Parry (1981), there are many dimensions to a life-history pattern, and life histories
can be shaped by constraints imposed by many factors including seasonality,
habitat stability, severe climatic stresses, predation, and the need for dispersal.
It is my opinion that the relatively permanent (stable) and seasonal but predictable
habitat of the water-filled treehole has been extremely influential in shaping the
K-type life-history pattern observed in the astigmatid inhabitants.
Most astigmatid mites studied thus far exploit habitats which are ephemeral
and unpredictable, thus leading to r-type life-history patterns. In this regard,
many, if not most, of these species are opportunists with a wide niche breadth.
In contrast, N. arbaricala, A. pennsylvanicus andH. mal/alae are specialists with
much narrower niche breadths, utilizing only water-filled treeholes as a habitat.
The obligate treehole inhabiting astigmatid mites studied thus far are unique in
many ways, and it will be interesting to discover whether all treehole mites
worldwide exhibit similar patterns once they are studied in detail. In this regard,
the two Australian algophagid species are of special interest due to the presence
of predators in the treeholes.
Acknowledgments
I thank Barry M. OConnor and Robert F. C. Naczi, University of Michigan,

for information concerning the distribution of treehole mites in North America,
and Roger Kitching, University of New England, Armidale, N. S. W., Australia,
for specimens of Australian treehole mites. Special appreciation goes to Dr. Gisela
Fashing, Virginia Department of Health, for critically reading the manuscript, and
to Jewel Thomas, College of William and Mary, for her technical assistance.
And finally, I thank Marilyn Houck, Texas Tech University, for her critical
reading and editing. Some of the research leading to the development of ideas
expressed in this paper was supported by grants from the College of William and
Mary. The original manuscript was written while the author was on a William
and Mary Faculty Semester Research Assignment.
'Those that do accept r- and K-selection as a useful concept restrict its meaning to that originally
intended by McArthur and Wilson (1967); the term r-selection restricted to selection for high
population growth in uncrowded populations and K-selection to competitive ability in crowded
populations (see Parry 1981 for details).
L(fe-History Patterns of Astigmatid Inhabitants of Water-Filled Treeholes I 181
References
Albert, A. M. 1983. Life cycle of Lithobiidae-with a discussion of the r- and K-selection

theory. Oecologia 56:272-279.
Arlian, L. G., C. M. Rapp and S. G. Ahmed. 1990. Development of Dermatophagoides
pteronyssinus (Acari: Pyroglyphidae). 1. Med. Entomol. 27:1035-1040.
Barker, P. S. 1967. The effects of high humidity and different temperatures on the biology
of Tyrophagus putrescentiae (Schrank) (Acarina: Tyroglyphidae). Can. 1. Zool. 45:91-
96.
Barlocher, F. and B. Kendrick. 1973. Fungi in the diets of Gammarus pseudolimnaeus
(Amphipoda). Oikos 24:295-300.
Beck, S. D. 1960. Growth and development of the Greater Wax Moth, Galleria mellonella
(L.) (Lepidoptera: Galleriidae). Trans. Wis. Acad. Sci. Arts Lett. 49:137-148.
Begon, M. 1985. A general theory of life-history variation. In: Behavioral Ecology (R.
M. Sibley and R. H. Smith eds.). Blackwell Sci. Pub!., Boston. Pp. 91-97.
Begon, M. and M. Mortimer. 1986. Population Ecology, a Unified Study of Animals and
Plants. Blackwell Sci. Pub!., Boston. 220 pp.
Behura, B. K. 1957. The life history of Histiostoma polypori (Oud.) (Acari: Tyroglyphi-
dae). 1. NY Entomol. Soc. 65:51-78.
Birch, L. C. 1948. The intrinsic rate of natural increase of an insect population. 1. Anim.
Ecol. 17: 15-26.
Bot, J. and M. Meyer. 1969. An artificial rearing medium for acarid mites. 1. South Afr.
Entomol. Soc. 29:199.
Boyce, M. S. 1984. Restitution of r- and K-selection as a model of density-dependent
natural selection. Annu. Rev. Ecol. Syst. 15:427-447.
Carpenter, S. R. 1982. Stemflow chemistry: effects on population dynamics of detritivor-
ous mosquitoes in tree-hole ecosystems. Oecologia 53:1-6.
Chmielewski, W. 1971. Morfologia, biologia i ekologia Carpoglyphus lactus (L., 1958)
(Glycyphagidae, Acarina). Pro Nauk. lOR, Pozan 13:63-166.
Chmielewski, W. 1987. Parameters of population development of Glycyphagus destructor
(Schr.) (Acarida, Glycyphagidae)-mite species found in bee-hives. Pszyr. Zesz. Nauk.
31:213-221.
Chmielewski, W. 1988. Biological potential of house mite-Glycyphagus domesticus
(DeGeer) (Acarida, Glycyphagidae )-a pest of pollen and bee bread. Pszyr. Zesz. Nauk.
32:169-180.
Cummins, K. W. and M. J. Klug. 1979. Feeding ecology of stream invertebrates. Annu.
Rev. Ecol. Syst. 10:147-172.
Cunnington, A. M. 1965. Physical limits for complete development of the grain mite,
Acarus siro (Acarina, Acaridae), in relation to its world distribution. 1. Appl. Ecol.
2:295-306.
Cunnington, A. M. 1969. Physical limits for complete development of the copra mite,
182 / N. J. Fashing
Tyrophagus putrescentiae (Schrank) (Acarina, Acaridae). In: Proc. 2nd Int. Congr.
Acarol. (G. O. Evans ed.). Sutton Vonington, England, 1967. Akademiai Kaid6,
Budapest. Pp. 241-248.
Cunnington, A. M. 1985. Factors affecting oviposition and fecundity in the grain mite
Acarus siro L. (Acarina: Acaridae), especially temperature and relative humidity. Exp.
Appl. Acarol. 1:327-344.
Cutcher, 1. 1. and 1. P. Woodring. 1969. Environmental regulation of hypopial apolysis
of the mite, Caloglyphus boharti. J. Insect Physiol. 15:2045-2057.
Deevey, E. S., 1r. 1947. Life tables for natural populations of animals. Q. Rev. Bioi.
22:283-314.
Edwards, P. B. 1988. Field ecology of a brood-caring dung beetle Kheper nigroaeneus-
habitat predictability. Oecologia 75:527-534.
Fashing, N. 1. 1973. The post-embryonic stages of a new species of Mauduytia (Acarina:
Anoetidae). J. Kans. Entomol. Soc. 46:454-468.
Fashing, N. 1. 1974. A new subfamily of Acaridae, the Naiadacarinae, from water-filled
treeholes (Acarina: Acaridae). Acarologia 14:166-181.
Fashing, N. 1. 1975a. Life history and general biology of Naiadacarus arboricola Fashing,
a mite inhabiting water-filled treeholes (Acarina: Acaridae). J. Nat. Hist. 9:413-424.
Fashing, N. 1. 1975b. Influence of temperature and food on development and popUlation
dynamics of Naiadacarus arboricola Fashing (Acarina: Acaridae). Acarologia 17: 138-
152.
Fashing, N. 1. 1976a. The evolutionary modification of dispersal in Naiadacarus arbori-
cola Fashing, a mite restricted to water-filled treeholes (Acarina: Acaridae). Am. Midi.
Nat. 95:337-346.
Fashing, N. 1. 1976b. The resistant tritonymphal ins tar and its implications in the popula-
tion dynamics of Naiadacarus arboricola Fashing (Acarina: Acaridae). Acarologia
18:704-714.
Fashing, N. 1. 1979. Naiadacarus arboricola, a "K-selected" acarid mite. In: Recent
Advances in Acarology, Vo!. 1 (1. G. Rodriguez ed.). Academic Press, NY. pp. 525-
529.
Fashing, N. 1. and L. L. Wiseman. 1980. Algophagus pennsylvanicus-a new species of
Hyadesidae from water-filled treeholes. Int. J. A carol. 6:79-84.
Fashing, N. 1. and D. L. Middleton. 1983. Notes on the biology of Algop hag us pennsylvan-
icus, a mite inhabitant of water-filled treeholes. VA J. Sci. 34: 128.
Fashing, N. 1. and W. 1. Hefe1e. 1991. Biology of Rhizoglyphus robini (Astigmata:
Acaridae) reared on Bot and Meyer artificial medium. In: Modern Acarology, Vol. 2
(F. Dusbabek and V. Bukva eds.). Academia, Prague and SPB Academic Pub!., The
Hague. Pp. 499-503.
Fashing, N. J. and D. M. Campbell. 1992. Observations on the feeding biology of
Algophagus pennsylvanicus (Astigmata: Algophagidae), a mite restricted to water-filled
treeholes. Int. J. Acarol. 18:77-81.
Fish, D. 1983. Phytote1mata: Flora and Fauna. In: Phytotelmata: Terrestrial Plants as
Hosts for Aquatic Insect Communities (1. H. Frank and L. P. Lounibos eds.). Plexus
Publ., Medford, NJ. pp.I-27
Fish, D. and S. R. Carpenter. 1982. Leaf litter and larval mosquito dynamics in tree-hole
ecosystems. Ecology 63:283-288.
Force, D. C. 1975. Succession of rand K strategists in parasitoids. In: Evolutionary
Strategies of Parasitic Insects and Mites (P. W. Price ed.). Plenum Press, NY. Pp.
112-129.
Frank, J. H. and L. P. Lounibos. 1983. Phytotelmata: Terrestrial Plants as Hosts for
Aquatic Insect Communities. Plexus Publ., Medford, NJ. 293 pp.
robini Claparede (Acarai: Astigmata: Acaridae). Acarologia 24:439--448.
Houck, M. A. and B. M. OConnor. 1991. Ecology and evolutionary significance of
phoresy in the Astigmata. Annu. Rev. Entomol. 36:611-636.
Hughes, T. E. 1953. The functional morphology of the mouth parts of the mite Anoetus
sapromyzarum Dufour, 1839, compared with those of the more typical sarcoptiformes.
Proc. Acad. Sci. Amst. 56C:278-287.
Ito, Y. 1980. Comparative Ecology. Cambridge Univ. Press, NY. 436 pp.
Kamud and R. B. Mather. 1989. Influence of ultraviolet radiation on the survival of the
acarid mite, Tyrophagus putrescentiae (Astigmata: Acaridae). In: Progress in Acarol-
ogy, Vol. 2 (G. P. ChannaBasavanna and C. A. Viraktamath eds.). Oxford and IBH
Publ. Pvt. Ltd., New Delhi. Pp. 249-253.
Kaushik, N. K. and H. B. N. Hynes. 1971. The fate of dead leaves that fall into streams.
Arch. Hydrobiol. 68:465-515.
Kitching, R. L. 1971. An ecological study of water-filled treeholes and their position in
the woodland ecosystem. J. Anim. Ecol. 40:281-302.
Kitching, R. L. 1987. Spatial and temporal variation in food webs in water-filled treeholes.
Oikos 48:280--288.
Kitching, R. L. and C. Callaghan. 1982. The fauna of water-filled tree holes in box forest
in south-east Queensland. Aust. Entomol. Mag. 8:61-70.
Kitching, R. L. and S. L. Pimm. 1985. The length of food chains: phytotelmata in
Australia and elsewhere. Proc. Ecol. Soc. Aust. 14:123-140.
Krantz, G. W. 1978. A Manual of Acarology, 2nd ed. Oregon State Univ. Book Stores,
Corvallis, OR. 509 pp.
Lacky, J. B. 1940. The microscopic flora and fauna of tree holes. Ohio J. Sci. 40:186--
192.
MacArthur, R. H. and E. O. Wilson. 1967. The Theory ofIsland Biogeography. Princeton
Univ. Press, Princeton, NJ. 203 pp.
Mathur, S. and M. Dalal. 1989. Influence of food quality on the development and growth
of the acarid mite, Suidasia nesbitti (Acari: Acaridae). In: Progress in Acarology, Vol.
2 (G. P. ChannaBasavanna and C. A. Viraktamath eds.). Oxford and IBH Publ. Pvt.
Ltd., New Delhi. Pp. 231-239.
184 I N. 1. Fashing
Merritt, R. W. and K. W. Cummins. 1978. An Introduction to the Aquatic Insects of

North America. KendalllHunt Publ., Dubuque, IA. 441 pp.
Nangia, N. and G. P. ChannaBasavanna. 1989. Influence of temperature and relative
humidity on the development of Tyrolichus casei (Astigmata: Acaridae). In: Progress
in Acarology, Vol. 2 (G. P. ChannaBasavanna and C. A. Viraktamath eds.). Oxford
and IBH Publ. Pvt. Ltd., New Delhi. Pp. 259-264.
Norton, R., J. B. Kethley, D. E. Johnston and B. M. OConnor. 1992. Phylogenetic
perspectives on genetic systems and reproductive modes of mites. In: Evolution and
diversity of sex ratio in insects and mites (D. Wrensch and M. Ebbert eds.) Chapman
and Hall Pub!., NY. Pp. 8-99.
OConnor, B. M. 1982a. Acari: Astigmata. In: Synopsis and Classification of Living
Organisms (S. P. Parker ed.), McGraw-Hili, NY. Pp. 146-169.
OConnor, B. M. 1982b. Evolutionary ecology of astigmatid mites. Annu. Rev. Entomol.
27:385-409.
OConnor, B. M. 1984. Acarine-fungal relationships: the evolution of symbiotic associa-
tions. In: Fungus-Insect Relationships: Perspectives in Ecology and Evolution (G.
Wheeler and M. Blackwell eds.). Columbia Univ. Press, NY. Pp. 354-381.
OConnor, B. M. 1989. Systematics, ecology and host associations of Naiadacarus (Acari:
Acaridae) in the Great Lakes region. Great Lakes Entomol. 22:79-94.
Parry, G. D. 1981. The meanings of r- and K-selection. Oecologia 48:260-264.
Phillipsen, W. J. and H. C. Coppel. 1977. Acotyledon formosani sp. n. associated
with the Formosan subterranean termite, Coptotermes formosanus Shiraki (Acarina:
Acaridae-Isoptera: Rhinotermitidae). 1. Kans. Entomol. Soc. 50:399-409.
Pianka, E. R. 1970. On r- and K-selection. Am. Nat. 104:592-597.
Pillai, P. R. P. and P. W. Winston. 1969. Life history and biology of Caloglyphus
anomalus Nesbitt (Acarina: Acaridae). Acarologia 11 :295-303.
Pimm, S. L. and R. L. Kitching. 1987. The determinants of food chain lengths. Oikos
50:302-307.
Rivard, I. 1961a. Influence of temperature and humidity on mortality and rate of develop-
ment of immature stages of the mite Tyroglyphus putrescentiae (Schrank) (Acarina:
Acaridae) reared on mold cultures. Can. 1. Zool. 39:419-426.
Rivard, I. 1961 b. Influence of temperature and humidity on longevity, fecundity, and rate
of increase on the mite Tyroglyphus putrescentiae (Schrank) (Acarina: Acaridae) reared
on mold cultures. Can. 1. Zool. 39:869-976.
ph us berlesi (Michael) (Acarina: Acaridae) in xenic diet. 1. Kans. Entomol. Soc.
46:176-183.
Rohnert, U. 1950. Wasserfullte Baumhohlen und ihre Besied1ung. Ein Beitrag zur Fauna
Dendrolimnetica. Arch. Hydrobiol. 44:472-516.
Slobodkin, L. B. 1964. Growth and Regulation of Animal Populations. Holt, Rinehart
and Winston, NY. 184 pp.
Smith, I. M. and M. S. Harvey. 1989. Description of adult Arrenurus (?Micruracaraus)
Life-History Patterns oj Astigmatid Inhabitants oJ Water-Filled Treeholes / 185
kitchingi sp. nov. (Acarina: Arrenuridae) from water-filled tree holes in Australia. Can.
Entomol. 121 :283-289.
Snow, W. E. 1949. The Arthropoda of Wet Treeholes. Ph.D. dissertation, Univ. Illinois,
Urbana, IL. 219 pp.
Snow, W. E. 1958. Stratification of arthropods in a wet stump cavity. Ecology 39:83-88.
Steams, S. C. 1977. The evolution of life-history traits. Annu. Rev. Ecol. Syst. 8:145-
171.
Suberkropp, K. and M. 1. Klug. 1976. Fungi and bacteria associated with leaves during
processing in a woodland stream. Ecology 57:707-719.
Varga, L. 1928. Ein interessanter Biotop der Bioconose von Wasserorganismen. Bioi.
Zentralbl.48:143-162.
Waiter, D. E., R. A. Hudgens and D. W. Freckman. 1986. Consumption of nematodes
by fungivorous mites, Tyrophagus spp. (Acarina: Astigmata: Acaridae). Oecologia
70:357--361.
Walter, D. E. and D. T. Kaplan. 1990. Feeding observations on two astigmatid mites,
Schwiebea rocketti (Acaridae), and Histiostoma baked (Histiostomatidae) associated
with citrus feeder roots. Pedobiologia 34:281-286.
Woodring, J. P. 1969. Observations on the biology of six species of acarid mites. Ann.
8
The Evolution of Parasitism and the Distribution
of Some Dermanyssoid Mites (Mesostigmata) on
Vertebrate Hosts
Frank 1. Radovsky
CONTENTS
1. INTRODUCTION
2. LIFE-CYCLE PATTERNS OF DERMANYSSOIDS
3. ORIGIN AND EVOLUTIONARY SEQUENCE OF A SERIES OF RE-
LA TED PARASITES
3.1 Hypoaspidinae to Laelapinae: the Move to Obligatory Nest Associa-
tion and the Beginnings of Parasitism on Vertebrates
3.2 The Laelapinae on Bats and the Line to the Macronyssidae
3.3 The Macronyssinae and the First Macronyssid Radiation on Bats
3.4 The Ornithonyssinae and the Higher Macronyssid Radiation
3.5 The Rhinonyssidae and the Great Endoparasitic Radiation in Birds
3.6 Sternastama tracheacalum and a Contemporary Rhinonyssid Radi-
ation
4. SUMMARY
1. INTRODUCTION
Despite the considerable number of species ... associated with various other animals.
there is, however, in only a very limited number of cases any precise knowledge of what
the mite does. An urgent need is for an increased knowledge of the biology of the
commoner species, for without this it is impossible to arrive at even a relatively true
appreciation of the relationships of mites to the general problems of animal ecology.
T. E. Hughes (1959)
.. the gaps in knowledge of the bionomics and basic host-parasite relationships are
especially glaring. Following a period of considerable interest in the 1950s and early
1960s, there has been a decline in biological studies of the vertebrate-associated Mesostig-
mata. This important area of research should be revitalized.
F. 1. Radovsky (1985)
186
Dermanyssoid Mites / 187
Whether the subclass Acari is monophyletic or polyphyletic remains unsettled,

but the early (pre-Devonian) separation of the orders Parasitiformes and Aca-
riformes is generally accepted (Krantz 1978, Lindquist 1984, Woolley 1988).
The suborder Mesostigmata is one of the largest and most ecologically varied of
the Acari, and it is the only suborder of Parasitiformes in which there has
been significant adaptive radiation into a broad spectrum of general niches. The
Mesostigmata associated with vertebrates have notably diverse host relationships,
but nearly all are in one superfamily, the Dermanyssoidea.
The importance of using life histories to understand phylogenetic relationships
among the dermanyssoid Mesostigmata was first recognized in the 1960s (Brege-
tova 1964,1969; Radovsky 1966, 1967, 1969; Evans and Till 1966). Additional
information on the life cycles of vertebrate associates in that superfamily is pre-
sented here. My principal objective is to clarify the role played by modifications in
life-history patterns in inducing taxonomic radiations and new host associations.
The correlation between adaptive shifts in life histories and speciation events in this
group has previously been discussed, but only cursorily (Radovsky 1985).
After reviewing the plesiomorphic life cycle of dermanyssoids, the vertebrate-
host relationships, and the types of life cycles, I treat the origin of parasitism and
the history of two related families, Macronyssidae and Rhinonyssidae, to show
that taxonomic radiations follow certain adaptive events.
Because most Mesostigmata associated with vertebrates, and nearly all species
parasitic on vertebrates, are in the superfamily Dermanyssoidea, this chapter
focuses on the evolution of vertebrate parasitism in one of the major acarine
suborders. Mesostigmatid associates of invertebrates are also richly represented
in the Dermanyssoidea; however, that is not a problem when dealing with the
vertebrate associates separately, because the evolutionary lines from free-living
dermanyssoids to those associated with invertebrates and vertebrates, respec-
tively, are independent.
Furthermore, that invertebrate/vertebrate separation is reflected in current clas-
sification (Table 8.1). It is only in the laelapid subfamily Hypoaspidinae, a stem
group from which other dermanyssoids appear to have evolved, that associates
of both invertebrates and vertebrates (as well as free-living mites) are classed
together. Hypoaspidine associates of vertebrates are basically predatory nidicoles,
although some species appear to utilize host-generated food sources opportunisti-
cally [e.g. Hypoaspis sardoa (Berlese»), and some use nest-building animals for
dispersal (Radovsky 1985).
The higher-order classification of the Dermanyssoidea was developed princi-
pally by Vitzthum (1940-1943). Subsequent changes resulted, to a large extent,
from the recognition of distinctive life cycles as characters appropriate to taxo-
nomic definition at the level of the family group. The classification given here
(Table 8.1) agrees in general with Krantz (1978), based primarily on summations
by Evans and Till (1966) and Radovsky (1966, 1967, 1969).
The evolutionary sequences of some vertebrate-associated Dermanyssoidea are
188 I F. 1. Radovsky
Table 8.1. The classification and feeding relationships of the Dermanyssoidea a .

Taxon Feeding Relationships
Laelapidae
Hypoaspidinae -Free-living;
predators in nests of vertebrates or invertebrates; commensals or
parasites on invertebrates
Laelapinae -Facultative or obligatory parasites in nests, principally of mammals
Haemogamasinae -Facultative or obligatory parasites, nonparasitic predators, or
generalists; in nests of mammals
Hirstionyssinae -Nest parasites of mammals
Myonyssinae -Nest associates, probably parasitic, of mammals
Mesolaelapinae -Associated with mammals
Alphalaelapinae -One species associated with the primitive rodent Aplodontia rufa
Melittiphinae -One species in beehives
Iphiopsinae -Associated with terrestrial arthropods; includes obligatory parasites
Macronyssidae
Macronyssinae -Nest or permanent parasites of mammals, principally bats
Omithonyssinae -Nest or permanent parasites of mammals, birds, and reptiles
Rhinonyssidae -Parasites in the respiratory passages of birds
Halarachnidae
Halarachninae -Parasites in the respiratory passages of mammals
Raillietiinae -Parasites in the external ear of mammals
Ixodorhynchidae -Parasites of snakes
Omentolaelapidae -One species parasitic on snakes
Entonyssidae -Parasites in the respiratory passages of snakes
Dermanyssidae -Nest parasites of birds (principally) and rodents
Hystrichonyssidae -One species parasitic on rodents
Spinturnicidae -Permanent parasites of bats
Dasyponyssidae -Parasites of armadillos
Manitherionyssidae -One species parasitic on pangolins
Varroidae -Nest parasites of honeybees
"Subfamilies given for families only where relevant to text.
well suited to host-parasite analysis because of the persistence of intermediate

types to modem times. However, it is not necessary to postulate the contemporary
existence of ancestral and descendant forms. The extant links are ecological types
that have survived because of the continued existence of a suitable general niche.
The general niche is a functional role in an animal community that can be
occupied by various species that are not necessarily taxonomically related (Elton
1966). I postulate, of course, that an intermediate extant form, discussed here to
support an evolutionary sequence, is taxonomically related to ancestral forms that
occupied the same general niche.
The central thesis of this chapter is that various points of novel adaptation
along one extended evolutionary pathway have each been followed by a subse-
quent major taxonomic radiation. The adaptations relate to (or influence) host-
parasite relationships and therefore are more easily discernible than adaptations
Dermanyssoid Mites I 189
to a free-living environment: the parasite and host represent the interaction be-
tween only two genotypes, compared to the numerous organisms (hence geno-
types) that interact with a free-living animal. That close interaction between host
and parasite is the basis for Fahrenholz's Rule, which states that parasites evolve
in concert with their hosts so that there is a correspondence in the two evolutionary
patterns. Despite many exceptions to the rule, it frequently can provide insight
into the history of a parasitic group as well as the history of the host group. For
example, a remarkable model of host-parasite coevolution is provided by chewing
lice associated with pocket gophers. These interactions have been extensively
studied to the benefit of both mammalogists and entomologists (reviewed by
Hellenthal and Price 1991). Some parasitologists use the term host-tracking for
host-parasite interactions that conform to Fahrenholz's Rule and apply the term
resource-tracking (related to the concept of ecological transfer) for host-parasite
patterns that appear to lack consonance (Kethley and Johnston 1975).
2. Life-Cycle Patterns of Dermanyssoids
Dermanyssoid parasitism is permanent (the mite remains on the host throughout

its life cycle) or nidicolous (the mite spends part of its life cycle in the nest, roost,
or other dwelling but is also found on the host). All endoparasitic mites (e.g.
those located in respiratory passages or ear canals) are permanent parasites and
leave their internal location only briefly, to transfer between hosts when the hosts
are in close contact.
The primitive dermanyssoid life cycle is that of the free-living Mesostigmata:
egg, hexapod larva, octopod protonymph, octopod deutonymph, and adult (fe-
male and male). Each successive developmental stage shows an increase in the
proportion of the idiosomal surface covered by plates (or shields) and an increase
in the number of setae on the idiosoma and appendages.
The larva is a nonfeeding stage that has mouthparts too weakly sclerotized to
be functional. The protonymph and deutonymph are active feeding stages with
sclerotized mouthparts similar to those of the adult female. The most prominent
feature of the functional mouthparts is a pair of chelicerae, which are adaptively
comparable to the bill of a bird or the teeth of mammals. Each chelicera of free-
living females and immatures (other than the larva) has a sturdy shaft tipped by
a pair of opposable chelae, one fixed and the other movable. Both chelae are stout
and toothed (Fig. 8.1, Hypoaspis aculeifer). These chelate-dentate chelicerae are
employed in a number of ways, including grasping and penetrating the cuticle of
small arthropods during predation. The male chelicera in the free-living type of
mite is usually much like that of the female except that the movable chela has an
appended spermadactyl, a structure used to transfer sperm packets from the male
genital opening to the female (Fig. 8.1) (also see Houck, Chapter 3, this volume).
Table 8.2 shows the range of life cycles occurring in dermanyssoids associated
Figure 8.1. Some dermanyssoid chelicerae. Left, Hypoaspis aculeifer (Canestrini),

female. Other illustrations of male chelae, from left to right: H. aculeifer, Androlaelaps
hirsti Keegan, Haemagamasus ambulans (Thorell), Haemogamasus liponyssoides Ewing.
Redrawn from various sources.
with vertebrates. These selected examples are in part chosen because of their
relevance to the remainder of the chapter. Free-living hypoaspidines and many
vertebrate-associated dermanyssoid groups have the primary free-living life cycle
as described above, with the larva nonfeeding and all later stages feeding. A
majority of the laelapines have this developmental pattern, and so do a number
Table 8.2. Life cycles in Dermanyssoidea associated with vertebrates.

Proto- Deuto- Adult
Egg Larva nymph nymph Female" Examplesb
HB NF FD FD FD Free-living Hypoaspidinae, most

Laelapinae. Dermanyssidae
IV IV FD FD FD Some Laelapinae,
Spintumicidae
HB NF NF FD FD Haemogamasinae (in part)
HB/IV NF FD NF FD Macronyssidae, Rhinonyssidae
HB/IV NF NF NF FD Halarachnidae
"Male excluded because ability to feed, with chelicerae modified for mating, is generally not
known.
bNot all examples are exclusive but exceptions are rare: e.g. a macronyssid in which the larval
stage is entirely intrauterine.
HB = Eggs released into the habitat: in the general environment of free-living mites; nests, roosts,
etc. of nidicoles and some parasites; onto the surface of the host or in tissues of some parasites.
IV = Develops in the parental uterus throughout the stage.
NF = Nonfeeding mobile stage.
FD = Feeding and usually requiring food to complete development.
of parasitic dermanyssoid groups. The primary life cycle shows that one sequence
of active stages can be correlated with very different biologies, e.g. free-living
hypoaspidines and parasitic dermanyssids.
The Dermanyssidae are highly adapted parasites that feed rapidly on the blood
of their hosts using long styletiform chelicerae that probably penetrate a venule
of the host in a similar fashion to elements of the mosquito fascicle (Radovsky
1969). Nevertheless, mites in this family have retained the same basic life
cycle as their free-living ancestors. The dermanyssids may be captives of their
specialized mouthparts: the styletiform chelicerae, which have evolved in all
feeding stages beginning with the protonymphs, may present a barrier to reversal
of a trend and suppression of feeding in any post-larval stage. Although no
dermanyssid is known to be a host-restricted parasite or to have suppressed any
stage, species such as Dermanyssus grochovskae Zemskaya and D. quintus
Vitzthum tend towards permanent parasitism; they are usually found on birds,
attach their eggs to the feathers of their host, have a reduced engorgement
capacity, and have strong legs adapted to clinging to volant hosts (Moss 1978).
Most dermanyssids are typical blood-sucking nest parasites: (1) they spend most
of the time in the nest when not feeding; (2) females represent the dispersal stage
and are most often collected on the host; (3) mite eggs are deposited in the host
nest (or crevices of roost or under nearby bark); and (4) they have a high
engorgement capacity and a very pronounced ability to withstand starvation for
months. The last attribute is essential for the survival of nest parasites, particularly
those of migrating avian hosts.
Some laelapines illustrate an abbreviation of the general life cycle by the
retention of the egg by the female, or by the retention of both the egg and
the larva. Thus, they may be larviparous (many facultatively so) presumably
depending on nutritional state. Some can deposit either eggs, larvae, or pro-
tonymphs, as in the case of Androlaelaps casalis (Berlese) (Men 1959).
We should seek a plausible interpretation for the significance of each alteration
of the life cycle, in order to understand the evolutionary patterns in these mites.
The Dermanyssoidea, in which there is, overall, a rich representation of extant
intergradient forms, provide an exceptional opportunity to examine the origins
of parasitism and the steps taken from one kind of host-parasite relationship to
another. The situation contrasts with fleas, for example, a group for which forms
representing intermediates between highly evolved parasites and an ancestral
free-living insect have not survived to be observable today.
The adaptive significance of any characteristic is measurable by the degree to
which it increases reproductive capacity, decreases mortality, or both. Suppres-
sion of the egg or egg and larva by retention in the female protects the developing
mite from mortality factors that would otherwise affect those early stages. At the
same time, a general consequence of larvipary and nymphipary is the reduction
in net reproductive capacity of the mother, because the individual offspring
192 I F. J. Radovsky
requires more time in utero. However, the nutritional cost to the mother need not
be changed by retention of the egg or larva in utero, because there is no feeding
in those stages.
For those laelapines that are ovoviviparous, there must be a trade off between
the elimination of such mortality factors as desiccation and predation directly
affecting the delicate and defenseless egg (or egg and larva) and the greater
investment per offspring by the female. Most nest mites oviposit, presumably
because the reduced reproductive capacity resulting from egg retention counter-
balances the protection that that behavior provides.
The highly specialized blood-sucking Spintumicidae, on the other hand, are
unifonnly nymphiparous. These mites occur only on bats and usually are restricted
to the hairless membranes of the wings and tail, to which they can reliably cling
because of specializations in the structure of the body and legs. The spintumicid
ontogeny is fundamentally changed. Evans (1968) studied the development of
Spinturnix myoti Kolenati and found that the egg was followed by an embryonic
prelarva that transfonned into a protonymph inside the mother, without fonning
a larva. By suppressing the egg and larva, the spintumicid life cycle is restricted
to active blood-feeding stages that contribute to maturation or reproduction; the
egg and inactive larva that might most easily be lost from the host are eliminated
as free stages. However, there are extensive and successful groups of other
pennanent ectoparasites that retain the inactive stages. For example, both chewing
and sucking lice finnly glue their eggs to the host feathers or hair; all nymphal
instars as well as adults feed actively and all of them have legs specialized for
reliably clinging to the host.
In one large genus, Haemogamasus, with more than 40 species, and in some
other Haemogamasinae, the protonymph is present in the environment (usually
the nest of a rodent or insectivore) but has weakly sclerotized chelicerae and does
not feed. Haemogamasus is extraordinary in its range of host relations, from
polyphagous nest associates to obligatory blood-feeders with chelicerae adapted
for puncturing the host's skin.
Only a single species, Haemogamasus pontiger (Berlese), has been character-
ized as facultative in its nest associations, either implicitly by the range of substrates
given or explicitly as in Radovsky (1985). However, this species may be adaptiveIy
dependent in nature on host and nest associations for its long-tenn survival. H.
pontigeris sometimes found on both native rodents and insectivores andon domesti-
cated rodents (Mus and Rattus). The many other records, which could be thought
of as free-living, may be extensions of the nest habitat of domesticated rodents (e. g.
barley, rice straw, hay packing, old burlap bagging, and grain spill). The mite may
enter these synanthropic habitats from rodent nests or directly from rodents in that
environment and survive for some time on such substrates, but the species may be
consistently associated with nests and hosts in nature.
For all Haemogamasus species then, the rich concentration of food in the nest!
host association can account for elimination of feeding in the protonymph. The
female can invest more in each offspring by providing sufficient nutrients in the
egg to carry the offspring through to the deutonymphal stage. In those species
that have been studied, the non feeding stages are brief, typically 1-2 days each
for larva and protonymph (Radovsky I 960b ). The deutonymph, which may
require weeks or months to mature (depending on the status of food in the nest),
is more protected than earlier stages by its size, sclerotization, and setation and
therefore better able to cope with the hazards of the environment.
Of all the dermanyssoid life cycles, I think the Macronyssidae/Rhinonyssidae
specialization is the least likely to have been suspected prior to its discovery. In
these two families the proto nymph is an active feeding stage and the deutonymph
is nonfeeding, relatively inactive, and largely suppressed. 1 Most Macronyssidae
are ectoparasites of bats, other mammals, birds, and reptiles. At least in those
species that I believe have been adequately studied, the protonymph is a fixed
feeder (i.e. it attaches to the host typically for one to several days prior to
engorgement). The development that often accompanies such extended feeding
is known as neosomy (Audy et al. 1972), which is discussed more fully below,
and may lead to unusual levels of engorgement as it does in ixodid ticks. The
macronyssid protonymph takes sufficient nutrients so that it can pass through two
molts to reach adulthood. The adults of macronyssids apparently are all rapid
feeders, engorging in minutes.
The Rhinonyssidae are parasites of respiratory passages of birds, principally
the nasal region. They evolved from the Macronyssidae and retain the same life
cycle with a feeding protonymph and nonfeeding deutonymph. Internal parasites
such as the Rhinonyssidae must have one or more stages that can move between
hosts. Adult and protonymphal rhinonyssids are poor transmission stages as they
are generally highly specialized as internal parasites and have poorly developed
claws and caruncles. The ambulacral apparatus of the deutonymph is reduced in
the family as it is most macronyssids. The rhinonyssid larva, however, typically
has more robust claws than those of any other stage. Thus, it appears that the
larva is the stage that serves for interhost transmission in this family. That is
interesting from an evolutionary standpoint, because it is a clear reversal of an
adaptive trend. The Ornithonyssinae, from which the Rhinonyssidae arose, all
have reduced claws and other ambulacral structures as larvae. However, although
'Domrow (1987) transferred the genera Bewsiella and Ichoronyssus from Macronyssidae (Macro-
nyssinae of Domrow) to Laelapinae, giving this rationale: "A deutonymph of B.fiedermaus (Hipposi-
deros calclIratus Dobson, Kukuba Caves. P. N. G, I. ix 1972, R. L. Vanderwal) shows fully developed
functional chelicerae, allowing transfer of this genus (and Ichoronyssus on the adult character
peritrematal shields setose) from Macronyssinae to Laelapinae." Damrow's proposed action should
be deferred pending further study. Ichoronyssus is nonfeeding as a deutonymph, based on the
nonfunctional chelicerae (Dusbabek 1964), and Ichoronyssus and Bewsiella have numerous synapo-
morphies showing that they are closely related. The presence of peritremal plate setae in both of
these genera has no bearing on family placement; the Neotropical genus Parichoronyssus, which
indisputably has a macronyssid life cycle, also has a setose peritremal plate.
194 / F. J. Radovsky
reduced, the functional elements of the larval ambulacra have been retained, and
apparently they have been readapted for active locomotion in the Rhinonyssidae.
The last family listed (Table 8.2) that exemplifies a distinctive dermanyssoid
life cycle is the Halarachnidae. That family now encompasses two groups of
endoparasites associated with mammals (Radovsky 1969), a relationship for
which there is a clear consensus (Potter and Johnston 1978, Furman 1979,
Domrow 1980, Fonseca and Faccini 1985). The Halarachninae occur in the
respiratory passages (nares to lungs) of a wide range of mammals. The Raillie-
tiinae are restricted to the ears of bovids. 2 The two subfamilies are similar in life-
cycle pattern, with both protonymph and deutonymph being nonfeeding stages
and the larva involved in transmission. From a trophic viewpoint, this family is
extreme in that all feeding is, or at least can be, concentrated in one stage;
sufficient nutrients are stored in the egg to allow complete development with
feeding only accomplished by the female.
Of the four species of Raillietia occurring in bovids, R. auris Leidy in cattle has
been sampled extensively. In the first large-scale study ofthat species, Tsymbal and
Litvishko (1955) recovered only larvae (10.2%) and adults (81.8% females and
8.0% males). Fonseca and Faccini (1985) carried out an even larger study and also
found only larvae and adults from among 12,726 mites flushed from the ears of
cattle. Those authors also reared mites in vitro, and they obtained both nymphal
stages. Females were larviparous and larvae progressed through the two nymphal
stages in about five days. Fonseca and Faccini (1985) observed that "larvae ...
taken from the ears of cattle appear to have fed (large, guts filled with white and
opaque material); lab-reared larvae are small and translucent." That larvae do not
have to feed is shown by 90% becoming adults in vitro with no food present. If
feeding by larvae, whether active or passive, does occur in the host, it might actually
extend the duration of the larval stage. The significantly large percentage oflarvae
taken from the host indicates that the stage is not as transitory as would be judged
from the in vitro studies, and food could cause the mites to remain in the larval stage
in order to act in transmission to new host individuals.
The Halarachninae include about 35 species that parasitize primates, terrestrial
carnivores, phocid and otariid seals, rodents, hyraxes, and artiodactyls. Informa-
tion on the biology of these mites has been gathered over several decades by the
careful researches on species from several genera by a number of investigators
(Hull 1956, Furman and Smith 1973, Furman et al. 1974, Kim et al. 1980; and
2Raillietia australis Domrow is known from females taken from the ear of the common wombat
(Vombatus ursinus); it is distinct in a number of morphological features from all other Raillietia
species, which form a compact group in morphology as well as hosts. Domrow (1980) questioned
his earlier placement of the species: "It may be that this morphologically and zoogeographically
distinct species ... should be transferred from Raillietia (Halarachninae) to some laelapine genus
near Mesolaelaps and Rhodacantha, whose hosts are also largely Australian marsupials rather than
Old World artiodactyls." I believe that Domrow was correct in his assessment and I have not included
R. australis in the Raillietiinae here.
others). Halarachnines have nonfeeding ephemeral protonymphs and deuto-

nymphs that have very rarely been recovered from a host. Some of the species
are larviparous and some oviparous. The larva has well developed ambulacra
(Popp 1961) and appears to be the only stage capable of moving between hosts.
This reversal of the dermanyssoid trend to reduce the ambulacral size and func-
tional capability in the larva is a convergent feature in the endoparasitic families
Halarchnidae and Rhinonyssidae.
The range of life-cycle types in the Dermanyssoidea is extraordinary and is
related to the variety of symbiotic relationships in which these mites are involved.
3. Origin and Evolutionary Sequence of a Series of Related Parasites
3.J Hypoaspidinae to Laelapinae: the Move to Obligatory Nest Association

and the Beginnings of Parasitism on Vertebrates
Whether one places the Hypoaspidinae in the Laelapinae (Evans and Till 1966,
1979) or recognizes them as separate subfamilies (Vitzthum 1940--43, Radovsky
1967, 1985) should not obscure the morphological similarity between some
genera from each of the two groups combined with a marked biological differentia-
tion between the groups. Laelapinae (s. str.) are characterized by male chelicerae
strongly modified for sperm transfer. In the majority of Laelapinae, including the
largest and typical genera Androlaelaps and Laelaps, the fixed chela of the male
is short and slender and the movable chela has become a weak structure to which
is attached an enlarged, often extremely long spermadactyl. It is difficult to see
how these chelae can function in feeding (Fig. 8.1). This contrasts with Hypoaspis
(and related genera) that I include in the Hypoaspidinae, in which the male
chelicerae are chelate and usually dentate, typically much like those of the female
but with the spermadactyl appended to the dorsal surface of the movable chela
(Fig. 8.1). Such chelae appear to be adapted both for feeding and for sperm
transfer, representing a balanced compromise in function. This distinction in the
male chelicerae is the only morphological separation between some species in
the Hypoaspis group and Androlaelaps.
The Hypoaspis group comprises free-living mites, generally found in soil and
litter. Androlaelaps and Laelaps are nest mites, usually associated with small
mammals and infrequently with birds. To the extent that these laelapine mites
have been studied, they are typically opportunistic feeders, able to use a variety
of foods: small nest arthropods, ectoparasites, scabs from or on the host. They
sometimes also feed directly from the host by punching a crater in the skin or by
imbibing lachrymal fluids or other secretions (see Radovsky 1985, for review).
Androlaelaps and Laelaps presumably have been drawn to the host's nest
because of the rich food supply and the nest has made male feeding relatively
unimportant. One can take this line of reasoning further to suggest that the nest
habitat makes male feeding superfluous and thereby allows the specialization of
196 / F. 1. Radovsky
the chelicerae for fertilization to become a dominant selective influence. The

male can easily locate females in the circumscribed sphere of the nest, and a
female, once fertilized, retains sperm to last its reproductive life.
At the same time that these mites are functionally bound to the nest, they are
also bound to the host. The nest usually represents an ephemeral habitat and even
in the more durable dwellings of some hosts (e.g. some Neotoma [wood rat]
houses, Aplodontia [mountain beaver or sewellel] burrow systems) the nest
proper may be moved at intervals. The host provides the dispersal capability that
compensates for nest-changing and permits nest-inhabiting to be a dependable
and successful general niche for small arthropods with limited vagility. Among
laelapine nest mites, it is usually the female that is the dispersal stage and the
stage that is most often found on the host.
I suspect that most nest laelapines have retained an ability in the male to feed
at least opportunistically. These mites feed on liquid food, or food that they
liquify, and it is likely that free-flowing blood from host wounds, liquid remains
of larger arthropods, and similar substrates will occur in the nest and may be fed
on even by males with strongly specialized chelicerae.
Specializations for strict parasitism have occurred because they give access to
a more dependable and richer food supply than opportunistic feeding. The use of
the host for dispersal may encourage such specializations. The intermittent pres-
ence of thin-skinned suckling young incapable of much grooming may encourage
them. Some laelapines have become obligatory parasites (see below), and various
strictly parasitic laelapid subfamilies, (e.g. Hirstionyssinae) and dermanyssoid
families (e.g. Macronyssidae) have branched off the Laelapinae lineage.
As described here, there was a major adaptive shift when the laelapine line,
through changes observable in the genus Androlaelaps, became bound to the nest
(primarily of small mammals) and that event was followed by a taxonomic
radiation. Independently but with striking parallels, Haemogamasus branched
from a hypoaspidine stock, became bound to the nest environment of small
mammals, developed male chelicerae extremely adapted for sperm transfer rather
than feeding (Fig. 8.1), and radiated taxonomically (Radovsky 1985). Haemoga-
masus is not in the sequence of taxa that is being traced here; however, it is a
parallel example that supports my evaluation of laelapine nest adaptation.
3.2 The Laelapinae on Bats and the Line to the Macronyssidae
Bats are ecologically diverse in feeding and in roosting sites and are one of the
most successful orders of mammals, second only to the rodents in the number of
living species. Among the laelapine mites, only Neolaelaps (three species) (Fig.
8.2) and Notolaelaps (one species) are known from bats and they are restricted
to the suborder Megachiroptera, the Old World fruit and blossom bats.
The rich bat-associated fauna of Macronyssidae occurs only on Microchiroptera
and not on Megachiroptera. Macronyssids share some apomorphic features with
Figure 8.2. Neolaelaps spinosus Berlese. Chelicerae, left to right: adult female, deuto-
nymph, protonymph, adult male. Female venter. After Radovsky (1967).
the bat-associated laelapines (see below), which demonstrate their relatedness.

The segregation of the bat-associated representatives of these mite families on
the two extant chiropteran suborders suggests host-tracking, which is supported
by the distribution of other groups of ectoparasites, as in the following examples.
In the Spintumicidae, the two distinctive genera Ancystropus and Meristaspis,
which share conservative features, are on Megachiroptera, and all other spintur-
nicid genera are on Microchiroptera (Rudnick 1960, Radovsky 1969), producing
a situation closely analogous to the Laelapinae-Macronyssidae segregation on the
two bat suborders. The bat-fly families Nycteribiidae and Streblidae and the flea
family Ischnopsyllidae each have separate genera that parasitize each of the bat
suborders without any overlap (see appendix in Kim 1985). The consistency of
nonrepresentation of some parasitic groups on the two bat suborders is equally
impressive, notably all bats lack both sucking lice (Anoplura) and chewing lice
(Mallophaga) (Radovsky 1967, 1969, 1985).
Bats usually have been treated as a monophyletic group, the only mammals to
have evolved powered flight and with such consistent features as uniformity in
the general structure of the wing. However, there are differences between the
two living suborders of bats, and some specialists have concluded that the order
Chiroptera is diphyletic (e.g. Smith and Madkour 1980). The fossil record is
of limited use. Microchiroptera representing several Recent families and some
assignable to extant genera are known from the Eocene (Table 8.3), but Megachi-
roptera are known from only two pre-Pleistocene fossils, the earliest in an Oligo-
cene formation (Baker et al. 1991). Interest in a possible diphyletic origin of
bats has increased in the past few years, with presentations supporting diphyly
(Pettigrew et al. 1989, Pettigrew 1991) or monophyly (Baker et al. 1991, Sim-
mons et al. 1991) of the Megachiroptera and the Microchiroptera. Host-parasite
Table 8.3. Classification and distribution of bats: families (and number of recent
species) from Nowak (1991); superfamilies of Microchiroptera from Eisenberg (1981).
Taxon Distribution
Eochiroptera
Palaeochiropterygoidea" Laurasia
Megachiroptera
Pteropodidae (173) Old World
Microchiroptera
Emballonuroidea
Rhinopomatidae (3) Old World
Emballonuridae (48) Old World; Neotropical
Craseonycteridae (I) Thailand
Rhinolophoidea
Nycteridae (13) Old World
Megadermatidae (5) Old World
Rhinolophidae (69)b., Old World
Hipposideridae (63)b., Old World
Phyllostomoidea
Mormoopidae (8) Neotropical
Noctilionidae (2) Neotropical
Phyllostomidae (148) Neotropical
Vespertilionoidea
Mystacinidae (I) New Zealand
Natalidae (5) Neotropical
Furipteridae (2) Neotropical
Thyropteridae (2) Neotropical
Myzopodidae (I) Madagascar
Vespertilionidae (355)b.d Cosmopolitan
Molossidae (86)b., Cosmopolitan
'Extinct; fossils principally Eocene. last in Oligocene (Hand 1984).

'Eocene fossils assigned to family (Koopman 1984).
'Eocene fossils, from Europe, assigned to Recent genera: Rhinolophidae-Rhinolophus, Hipposi-
deridae-Hipposideros, Molossidae-Tadarida (Hand 1984, Koopman 1984).
dMyotis, the most speciose Recent vespertilionid genus, appears in the Oligocene of Europe (Hand
1984).
associations were not included in those analyses. (Hall [1984] who refers to the
monophyly/diphyly controversy, mentions evidence from insect parasites.)
Parasite associations of other vertebrates have provided convincing evidence
concerning the phylogeny of the hosts. For example, the large array of identical
or closely related parasites of the ostrich in Africa and the rhea in South America
was know before the close relationship of those two ratites had become widely
accepted on other grounds. 3 Indeed, one proponent of bat diphyly cited distinctive
associations of spinturnicid mites with bats when raising the microchiropteran
group Mormoopidae to family level (Smith 1972). Data on Laelapinae-Macronys-
sidae and other ectoparasites, briefly summarized above, provides evidence of
the monophyly of the Chiroptera that is difficult to refute. How else can one
explain the shared higher-group associations of so many parasitic taxa? I suggest
that mammalogists concerned with bat origins need to accommodate parasitic
relationships in their conclusions. Because advanced microchiropterans are
known from the Eocene, the separation of the suborders must have occurred by
that time, and probably in the earlier Paleocene (65-55 my a) (Hall 1984). Ac-
cepting synchronous early evolution of Laelapinae-Macronyssidae with bat hosts,
we can conclude that the Macronyssidae first evolved at that early time.
The only clear distinction of Neolaelaps and Notolaelaps in those features that
have generally been used to characterize Laelaps and its close relatives (Tipton
1960) is the specialization of the chelae, which are edentate and relatively weak-
in fact, the female chelae of Neolaelaps spinosus (Berlese) (Fig. 8.2) are interme-
diate between those of the free-living hypoaspidine type and the skin-penetrating
macronyssine type. Nevertheless, these two bat-associated genera are highly
specialized parasitic mites that are phylogenetically closer to the Maconyssidae
than other laelapines.
Neolaelaps have the pair of spiracular openings (stigmata) enormously en-
larged, a feature for which the adaptive significance is obscure (Fig. 8.2). These
mites are apparently nymphiparous and feed on blood in both nymphal stages as
well as when adults (Fig. 8.2). From our present knowledge, they are probably
permanent parasites. They are found on Pteropus (the large flying foxes) and on
other Pteropodinae of the Australasian and Oriental regions. They have been
found on pupiparous bat flies (Nycteribiidae, Streblidae) a number of times; they
may use the flies to help them stay on a host, for dispersal among host individuals,
or both. The male chelae are suggestive of those in macronyssids (Fig. 8.2). In
addition, the sensory field setation of tarsus I is very macronyssid-like (more than
in Notolaelaps), which confirms a macronyssid relationship (Fig. 8.3).
Notolaelaps novaguinea Womersley was known from only six females on three
bats in the mountains of New Guinea, of which two of the hosts were identified
as nectar-feeding bats of the genus Syconycteris (Macroglossinae) found in Aus-
31957. Premier Symposium sur la Specificite Parasitaire des Parasites de Vertebres. Insf, Union
BioI. Sci., Ser. B, no. 32,156-158.
200 / F. 1. Radovsky
Figure 8.3. Dorsal view of tip of tarsus I showing sensory field, with some setae labelled
to show homologies: left, Neolaelaps spinosus (Berlese); right Steatonyssus antrozoi
Radovsky and Furman. After Radovsky (1967).
tralia, New Guinea, and other Australasian islands. In March 1985, I collected
six more females plus two males of N. novaguinea from three specimens of
Syconycteris at I 100m near Mount Dayman in eastern Papua (Milne Bay Prov-
ince, Papua New Guinea; Radovsky, unpublished data). These mites were very
difficult to recover by brushing or combing the bat or by washing the surface.
Nearly all of them were found by watching the small white mites emerge from
the fur and move over the contrasting dark surface of the host. I examined all of
these mites alive with a stereoscopic microscope, and none had the appearance
of red or dark material in them that could be associated with blood-feeding. I
conclude that these mites are probably obligate parasites that feed on some
material secreted by the host that does not darken the body, perhaps lachrymal
fluids or a mucous secretion from some other body orifice or exocrine gland.
The female chelae of Notolaelaps have remained short and relatively stout, as
compared to Neolaelaps, which supports their not being used to penetrate tissues
such as skin. We lack evidence to suggest whether Notolaelaps novaguinea is or
is not a permanent parasite (as opposed to a roost parasite). Nothing is known
about the developmental stages. That the immatures have not been taken from
the host may be related to the general difficulty in collecting this mite (and the
small size of the nymphs), or the immatures may be in a cryptic location on the
host, or they may develop primarily in the roost area.
The male chelicera of Noto[aelaps, not previously described, is very similar
to that of Neolaelaps, which is additional evidence that the two genera represent
a single lineage and which further supports their close relationship to the Macro-
nyssidae. No other laelapine mite has male chelae that are as close to the macro-
nyssid type as Notolaelaps, especially to the chelae of the more conservative
macronyssines. Comparing these structure in Notolaelaps to the typical form in

Macronyssus species, the pilus dentilis on the fixed chela is more developed in
Notolaelaps, the dorsal arm of the movable chela is straighter and more slender,
and the tip of the spermadactyl is more distinctly and sharply curved dorsad.
In my prior writings (Radovsky 1969, 1985) and earlier in this chapter, I have
emphasized the sexual dimorphism that has developed in the chelae with adoption
of the nest habitat, the apparent reduction of feeding capability in the male, and
the sometimes bizarre structures that have evolved in the male chelae to better
effect sperm transfer. However, those trends are moderated or even reversed as
mites in the same evolutionary lines become obligate parasites. Thus, the male
of Neolaelaps spinosus has a chelicera (Fig. 8.2) that appears to be used in
feeding, certainly more so than in most Androlaelaps and Laelaps species. Most
Macronyssidae, Hirstionyssinae, Myonyssinae, etc. have male chelae that are
similar in length to those of the female and that appear to have the capacity of
working together as the tip of a tissue-penetrating chelicera, somewhat compara-
ble to those of the female though not as effective. Haemogamasus provides an
interesting parallel, in that the bizarre male chelae of the polyphagous Haemoga-
masus reidi group can be contrasted with the simple male chelae, quite like those
of the female, in the strictly hematophagous Haemogamasus liponyssoides group
(Radovsky 1960a, 1960b; Williams et al. 1978) (Fig. 8.1).
An explanation of this apparently significant phenomenon may be that the
polyphage, taking advantage of the trophic potential of the nest, must use its
chelicerae as multi-purpose and adaptable tools. Thus, a female Laelaps echidni-
nus Berlese may use its chelicerae to punch a hole in the skin of a rodent, to
grasp and puncture a mite or louse, to liquify a scab, to scrape lachrymal material
from the comer of a rat's eye, etc. (Furman 1959, Radovsky 1985). Some of those
feeding substrates demand chelate-dentate chelicerae, and extreme adaptation of
the male for effective insemination is a more practical course for these mites.
The obligatory parasite concentrates on one feeding substrate in most cases.
Penetration of the skin requires a specialized adaptation; however, that adaptation
is to use the chelicerae as a piercing structure for which they are preadapted. The
primary requirement in adapting for hematophagy is for the chelae to become
slender and more or less pointed, so that they can act together as the tip of a
thrusting apparatus. Chelicerae appear to have acquired this form many times in
the females of dermanyssoids that have become obligatory parasites (Radovsky
1969). The puncturing capability of these chelicerae apparently is more compati-
ble with sperm transfer than the chelate-dentate structure required for the all-
purpose feeding for which chelicerae are used by polyphagous nest mites. The
chelicerae of male parasitic dermanyssoid mites are rarely if ever as effective in
feeding as those of the female. However, they apparently have an adaptive
advantage in feeding that has resulted in a renewed balance between the trophic
and reproductive functions of the male chelicerae in these parasitic groups.
Why laelapines have not radiated more widely on the Megachiroptera is not
clear. Neolaelaps and Notolaelaps are both specialized and limited taxa, although
Neolaelaps spinosus has many pteropodine hosts within its geographic range.
3.3 The Macronyssinae and the First Macronyssid Radiation on Bats
The transition from a laelapine bat-associated ancestor to the Macronyssidae

(Radovsky 1966, 1967) was marked by an extraordinary change in the life cycle:
the suppression of the deutonymph, which is expressed in the morphological
differences between the protonymphal and deutonymphal stages (Fig. 8.4, 8.5).
No species of the subfamily Macronyssinae, which encompasses the earlier
radiation of mites in this family and is the most diverse, has been reared or
observed in the laboratory, so our information about the biology of the Macronys-
sinae is partly suppositional. However, the protonymph is collected so frequently
from the host, relative to other stages, that there can be little question that it is
uniformly slow-feeding. In addition, there are direct observations of Radfordiella
proto nymphs embedded in the oral mucosa (see below). We can state with even
greater assurance that most and perhaps all species of Ornithonyssinae, a more
clearly defined and compact group, are fixed feeders as protonymphs and rapid
feeders as adults, which is discussed below. The feeding behaviors of the adult
and protonymph have diverged, and the nature of the protonymphal feeding gives
the mite the capacity to pass through the deutonymphal stage without additional
feeding. The deutonymph has become a resting pupa-like stage. A corollary of
that theory is that the proto nymph exhibits neosomatic development (Audy et al.
1972), a phenomenon that is also discussed in the following section.
The macronyssid transition to a novel life cycle was accompanied by a major
taxonomic radiation, which was almost entirely restricted to bat hosts. There are
only three macronyssine species in two genera on rodents, and these are Neotropi-
cal forms derived from bat-infesting genera. Of the 12 genera that I assign to the
Macronyssinae, eight appear to have originated in the Neotropical Region. The
other four are Old World in origin (Table 8.4). Macronyssus, the one genus with
many species, secondarily entered the New World, radiated moderately in North
America, and has a limited presence in the Neotropics (where there are few
species and only one endemic). That pattern of distribution raises many questions,
at least some of which have plausible answers based on the host associations and
the phylogeny of the Chiroptera.
During the Mesozoic Era, the Pangean world continent broke into northern
Laurasia (North America, Europe, Asia) and southern Gondwanaland (South
America, Africa, India, Australia, Antarctica). Although mammalogists are not
in full agreement on the geographic location of early bats, most specialists support
a Laurasian origin (Hand 1984). Archonta, a superordinal grouping in which bats
are placed with Dermoptera (colugos or gliding lemurs), Scandentia (tree shrews),
and Primates by some mammalogists, is considered Laurasian in origin. All the
Figure 8.4. Venter of Steatonyssus stages, clockwise from upper left: larva, protonymph,
deutonymph, adult female. Female is S. leptus Radovsky, others are S. antrozoi Furman
and Radovsky. After Radovsky (1967).
203
204 f F. J. Radovsky
Figure 8.5. Chelicerae of Steatonyssus antrozoi Furman and Radovsky, from left: larva,
protonymph, deutonymph, adult female, adult male. After Radovsky (1967).
oldest bat fossils (Eocene) and all paleochiropteroid fossils are know only from
Laurasia. The present distribution of bats fits most closely with dispersal from
Laurasia to the southern continents, which is also true of the distribution of their
parasites. One of the microchiropteran superfamilies, Phyllostomoidea (Table
8.3), was long isolated in the Neotropics, radiated there, and is still restricted to
that region except for a small number of species that have entered the southern
Nearctic in recent geologic time.
The present distribution of Macronyssinae is understandable if we consider
that the migrant bat or bats from which the phyllostomoid lineage came was
carrying one or more macronyssines when entering South America in the early
Tertiary. There is general agreement that the radiation of microchiropteran super-
families was not later than the Eocene. In the early Eocene, about 55 mya, South
America and North America were sufficiently close to have allowed easy dispersal
of a flying mammal across the intervening ocean.
There is one more, particularly fascinating piece of evidence that supports such
an early dispersal of the phyllostomoid stock into South America. The monotypic
bat family Mystacinidae is endemic to New Zealand. It is the only indigenous
land mammal there except for another bat that descended from an ancestor that
flew from Australia in late geologic time. As summarized by Hand (1984),
immunological studies published in 1982 demonstrated that Mystacina was
closely related to the phyllostomoids and those studies plus reexamination of the
morphology unquestionably put Mystacina "as an early offshoot of the phyllosto-
moid lineage" (Table 8.4 follows a conservative interpretation).
Table 8.4. The classification and distribution of genera of the Macronyssidae. The
approximate number of valid described species is given in parentheses, where the
number exceeds three. Hosts that are apparently accidental are excluded: e.g. a
species of Macronyssus known from only one collection on a rat or Chiroptonyssus
attacking humans.
Taxon Host Range Geographic Range'
Macronyssinae
Bewsiella Rhinolophoidea Old World
Ichoronyssus Vespertilionidae, Rhinolophoidea Old World
Macronyssus (40) Vespertilionidae, Rhinolophoidea Cosmopolitan
Megistonyssus Rhinolophidae Ethiopian
Synasponyssus Thyropteridae Neotropical
Parichoronyssus (5) Phy llostomidae, Emballonuridae Neotropical
Radfordiella (6) Phy llostomidae Neotropical
Macronyssoides Phyllostomidae Neotropical
Chirocoetes Phyllostomidae Neotropical
Nycteronyssus Phyllostomidae Neotropical
Acanthonyssus Rodents Neotropical
Argitis Rodents Neotropical
Ornithonyssinae
Trichonyssus (7) Vespertilionidae primarily, other Australian
Microchiroptera
Mitonyssus Noctilionidae, Molossidae Neotropical
Chiroptonyssus (4) Molossidae New World
Chelanyssus Molossidae Ethiopian
Parasteatonyssus (4) Molossidae Old World
Steatonyssus (40) Microchiroptera (excluding Cosmopolitan
Phyllostomoidea)
Pellonyssus (6) Birds Old World, Nearctic
Lepidodorsum Rodents Neotropical
Lepronyssoides Rodents Neotropical
Ornithonyssus (25) Rodents and other mammals New World
primarily; birds
Cryptonyssus (20) Mammals (including Microchiroptera) Old World, Nearctic
Ophionyssus (8) Lizards and Snakes Old World
Draconyssus Lizards Neotropical
'In a few cases, regions are omitted where they are marginal (e.g. Radfordiella on some phyllos-
tomid bats in the southern Nearctic Region) or there apparently were range extensions of mites as the
result of dispersal by humans in post-Columbian times (e.g. three species of Ornithonyssus widely
distributed in the Old World, one species of Ophionyssus widely distributed on snakes and lizards in
captivity in the New World).
Crossing the ocean gap from the southern tip of South America to Antarctica-
Australia and then over another ocean barrier to New Zealand by the mystacinid
ancestor would have been most likely not later than the early Oligocene, which
"suggests that chiropteran stock ancestral to the phyllostomoids probably entered
South America from Laurasia by (at least) the late Eocene" (Hand 1984). The
question will inevitably be asked as to what parasites on Mystacina tuberculata

may shed light on this relationship; unfortunately that New Zealand bat has lost
all of its original parasites. The parasites it now has have evolved on it, probably
in New Zealand, or have secondarily transferred to it from another resident host.
Other widespread microchiropteran families apparently entered South America
while it was an island continent (Hand 1984). The Molossidae and Emballonuri-
dae may first have arrived there in the Oligocene and Vespertilionidae in the
Miocene. The crossover of macronyssids among these groups and between them
and phyllostomoids seems to have been limited, which again suggests a high
level of host-tracking.
3.4 The Ornithonyssinae and the Higher Macronyssid Radiation
The more derived macronyssids, subfamily Ornithonyssinae (Table 8.4), are a

relatively uniform group with: (1) a higher capacity for engorgement by the adult
female than in most Macronyssinae; (2) a tendency for reduction of idiosomal
plates; (3) a loss of some primary plate setae but often hypertrichy in relation to
engorgement; and (4) some characteristic identifying structures, such as the
anteriorly directed ventral process on the first free palpal segment (trochanter).
Most ornithonyssines probably represent one lineage, but it is plausible that two
or more lines came from the macronyssine grade.
The ornithonyssine species that is best understood biologically from laboratory
observations and experiments is Chiroptonyssus robustipes (Ewing). This is a
parasite of the molossid bat Tadarida brasiliensis and is relatively easily observed
because the protonymph consistently feeds on the glabrous wing membrane and
the adults will feed there also. I found that protonymphs require about two days
after molting before they are ready to feed and generally need 4-5 days on the
host before they are engorged, though some engorged after as little as three
days (Radovsky 1964, 1967). With a stereoscopic microscope I observed that
protonymphs remain attached in one place unless disturbed. They showed no
change in color though they gradually increased in size, yet all mites were bright
red when they left the host showing that they had engorged on whole blood.
Lavoipierre and Beck (1967) used a high-power light microscope to examine
feeding on the transilluminated bat wing. They injected bats with Evans' blue
stain, which showed that protonymphs ingest extra-vasated tissue fluids during
their long period of feeding. Then after 3-6 days the protonymphs puncture a
venule and engorge rapidly (in about 15-20 minutes) on whole blood before
leaving the host. Adult females always feed rapidly by rupturing a vessel and
imbibing the blood that pools outside it.
Lees (1952) was the first to demonstrate the ontogenetic basis of major external
change of an active arthropod in the absence of a molt, a phenomenon especially
widespread among symbionts. He showed that a female ixodid tick, Ixodes ricinus
(Linnaeus), spends most of its 6-7 days on a host feeding slowly and growing
new cuticle, in order to double the thickness of its soft integument. It engorges on
whole blood during its last half-day on the host, stretching the integument back to
its original thickness and allowing the tick to enlarge about 125 times. Arthur (1965)
reported that I. ricinus feeds on tissue fluids and other materials until the rapid
engorgement phase. Audy et al. (1972) applied the term neosomy to the formation
of a new external structure or significant enlargement with the secretion of new
cuticle within an active stadium. They noted examples among Acari, fleas, bat flies,
parasitic Crustacea, some termite and ant queens, and others.
The protonymph of Chiroptonyssus robustipes does not enlarge to anything
approaching the scale of a female ixodid tick. However, it does enlarge suffi-
ciently to carry through to the deutonymphal stage without feeding, which is
more than dermanyssoid mites usually can take in. I postulate that cuticular
growth is taking place during the long period of feeding by the C. robustipes
protonymph before it engorges, and hence this is an instance of neosomy. Further-
more, I think that fixed feeding and neosomatic growth are characteristic of
ornithonyssines, and perhaps of all Macronyssidae.
I also studied Steatonyssus antrozoi Radovsky and Furman, a parasite of the
vespertilionid Antrozous pallidus (Radovsky 1967). This mite stays in the fur of
the host and was not directly observed when feeding. Protonymphs left the host
in the engorged state after 1.8-4.0 days, usually after 2.5-3.5 days. Some
females engorged and left the host in three hours. These results indicate that the
protonymph is a fixed slow-feeder and that the adult female is a rapid feeder.
The protonymphs of three species of the macronyssine genus Radfordiella are
fixed parasites in the oral mucosa (palate) of phyllostomid bats (Phillips et al.
1969, Radovsky et al. 1971). The adults of these mites are not known but
presumably are quick-feeding external parasites, as other Radfordiella adults
appear to be.
Camin (1953) studied the biology of the snake mite, Ophionyssus natricis
(Gervais), in detail. He observed the protonymph to feed within 24 hours of
molting and to remain in one spot, under a scale, until engorged (in 16-21 days
at 15°C and in 3-7 days at 25°C). He did not explicitly state the duration of
feeding by the adult female. All feeding was on a host and the mite was under
a scale. Apparently individual mites were not followed.
Extensive research has been done on three species of Ornithonyssus because:
(1) two species are pests of poultry; (2) their potential for pathogen transmission;
(3) their direct attacks on humans in the absence of a more natural host; and (4)
the usefulness of one species as a laboratory model for filarial studies. These are
Ornithonyssus bacoti (Hirst), the tropical rat mite; O. sylviarum (Canestrini and
Fanzago), the northern fowl mite; and o. bursa (Berlese), the tropical fowl mite.
Despite extensive culturing of these species, I am not aware of any study that has
demonstrated the nature of protonymphal feeding in which the mites were ob-
served under natural conditions.
Bertram et al. (1946) conducted an impressive set of studies on O. bacoti on
208 I F. J. Radovsky
a natural host, the cotton rat (Sigmodon hispidus) , and on the laboratory rat.
Mites were given access to the scarified tail of a rat, and the females fed readily,
some becoming fully engorged within 10 minutes. However, protonymphs did
not feed significantly and the authors concluded that they could obtain fully
engorged protonymphs only by giving them free access to a host and recovering
them when they dropped off. Skaliy and Hayes (1949) also used the scarified rat
tail to feed O. bacoti; they believed that protonymphs fed satisfactorily but they
noted that mites in that stage required mUltiple blood meals, and the measurements
of "fed" protonymphs suggest that they had fed hardly at all. Sikes and Chamber-
lain (1954) reported that an individual of O. bursa feeding on chickens "usually
requires at least two feedings (one or more partial meals and a final complete
engorgement) in order to molt." How they were able to conclude that from their
experimental design is not clear, but they may have been misled by a study in
which they put freshly molted protonymphs (not yet ready to feed) on a chick
and recovered mites within six hours that, not surprisingly, had the appearance
of having fed only partially, if at all. Similarly, studies on O. sylviarum, more
recently involving partially developed chicks in eggs or on membranes over
blood, have repeatedly been combined with statements that this species needs
two or more blood meals in its protonymphal stage (Hogsette et al. 1991).
Research protocols that allow fixed feeding in combination with observability of
the process are difficult to design for many omithonyssine mites that normally feed
beneath the feathers or fur. It is not surprising that partial feedings have been ob-
tained by many scientists who preconceived protonymphal feeding based on the
adult model and provided artificial feeding systems or hosts. I gave Chiroptonyssus
robustipes protonymphs access to suckling mice and found that 8/80 (10%) took
some blood though they did not engorge (Radovsky 1967). Without the opportunity
to study these mites on the wing of a bat, I obviously could have reached some
wrong conclusions. Further research is needed before it can be dependably stated
that the protonymph of any omithonyssine mite feeds partially and repeatedly or
takes blood initially in feeding. Unless such a demonstration is made, I believe we
should extrapolate from those species that have been studied and from what is
logically adaptive based on our current knowledge, to anticipate that each omitho-
nyssine protonymph is a fixed feeder taking tissues other than whole blood until it
engorges on whole blood just before completing its single meal in that stage. The
same supposition about slow feeding by the protonymph can be made for the Ma-
cronyssinae, although the evidence is more limited.
The omithonyssine adaptation is a quantifiable change in feeding capacity in
which both the protonymph and the adult female appear capable of greater
engorgement than is generally found in the macronyssines; that adaptation led to
further radiation on bats and also to radiations on other mammals, birds, and
reptiles. About half of the omithonyssine genera are found on bats (Table 8.4),
including Steatonyssus, which is cosmopolitan and notably speciose. There are
several basically Neotropical genera on rodents, of which Ornithonyssus has
radiated significantly. Pellonyssus on birds originated in the Old World and is

close to Steatonyssus. Ophionyssus originated on snakes and lizards and is also
Old World in origin. Draconyssus, known from only two collections of females
in Panama, was found in the nares of lizards (Yunker and Radovsky 1966).
Cryptonyssus, on bats and other mammals, originated in the Old World and
has only a few species on bats in North America (Radovsky 1967, 1969, 1985).
Many of the Old World species assigned to Ornithonyssus by authors should be
included in Cryptonyssus, pending further study, because of their similarities to
Cryptonyssus desultorius Radovsky 1966, the type species of the genus, and
because placement in Ornithonyssus is clearly misleading and obscures the sys-
tematic and zoogeographic significance of that genus. 4 Furman and Radovsky
(1963) redefined Ornithonyssus, noting two features that are particularly impor-
tant in recognizing the genus: the adult female and male and the protonymph all
have a number of tapered setae that bear small barbs on one side and the male
has a prominent seta-bearing swelling on the palpal femur. Based on those features
and the diagnosis as a whole, Ornithonyssus originated in the Neotropics and has
spread to the Nearctic on such hosts as the opossum and the cotton rat. Some
forms have transferred to Nearctic hosts and speciated. The distribution of the
genus has been confused by the spread of three species to many parts of the
world: O. bacoti (includes O. ondatrae), O. sylviarum, and O. bursa. All three
species are now relatively nonspecific, which suggests their recent dispersal, and
all three species are found primarily in relation to domestic, domiciliated, or
generally anthropotopic hosts, which tends to confirm their nearly cosmopolitan
spread by human activities in post-Columbian times. An interesting association
of O. bacoti is its role as the vector and intermediate host of Litomosoides carinii,
a filarial worm parasitic on Sigmodon hispidus, confirming the New World origin
of the mite in association with that basically Neotropical rodent.
Ornithonyssus is primarily parasitic on rodents [though O. wernecki (Fonseca)
is on opossums of the genus Didelphis]. However, repeated reference has been
made here to two species on birds: O. sylviarum and O. bursa. These seem to be
isolated cases and potentially the starting points for new radiations. Distinctions
between these two mites both morphologically and biologically suggest that
they were independent transfers to birds. O. sylviarum is also interesting as an
omithonyssine that is well on its way to becoming a permanent parasite; most
eggs are fastened to feathers and all stages may remain on the host, though vast
4Among the host of species lumped into the genus Ornirhonyssus by Micherdzinski (1980), I
believe the following should be retained in or transferred to Crypronyssus: C. conciliarus Radovsky,
1967; C. cosrai (Micherdzinski, 1980), new combination; C. desulrorius Radovsky, 1966; C. dogieli
(Bregetova, 1953); C. fiexus Radovsky, 1967; C. larro (Domrow, 1963), new combination; C.
niridulae (Costa, 1961), new combination; C. perauri (Micherdzinski, 1980), new combination; C.
pipisrrelli (Oudemans, 1904); C. praedo (Domrow, 1971), new combination. Probably some other
Australian species listed in Ornirhonyssus by Domrow (1987) will eventually be placed in Crypronys-
sus (and others in Trichonyssus). Further analysis of these questions belongs in revisionary works.
numbers of females and protonymphs will leave the host to disperse. Perhaps
parasitological or other clues can be found to the original bird hosts of these two
species, as has happened with O. bacoti, which could shed much light on their
evolution and adaptations.
The Nearctic Region appears to have been primarily a corridor and place for
secondary speciation events in the Macronyssidae. The two centers for radiations
were the Old World and the Neotropics, and the latter was free of the other
continents from the Mesozoic until several million years ago. Macronyssus in the
Macronyssinae and Steatonyssus in the Omithonyssinae are each speciose genera
on bats that originated in the Old World. Each came to the Nearctic rather late
judging by its more limited radiation there. It appears that each began to enter
the Neotropics quite late, perhaps not until the Pliocene-Pleistocene rejoining of
the continents. Each genus appears to have produced only a single new species
in the Neotropics. While Old World genera have moved into the New World with
bat hosts such as vespertilionids, there has not been any significant movement in
the other direction. The typically Neotropical taxa in the Macronyssidae have
apparently been restricted by the limited spread of their hosts to the north and by
the failure of those host groups to colonize the Old World.
3.5 The Rhinonyssidae and the Great Endoparasitic Radiation in Birds
It appears unlikely that the suppression of the deutonymph and the retention of
a feeding protonymph should have happened twice, and that is one basis for
relating the Rhinonyssidae to the Macronyssidae (Radovsky 1964, 1966, 1969).
As far as we know, all rhinonyssids have the macronyssid type of life cycle.
Strandtmann (1961) published a landmark paper on the life histories of a major
grouping of rhinonyssid genera, in which he said of the protonymph that it is
"quite obviously a feeding stage" and of the deutonymph that it is "obviously a
nonfeeding stage."
As it happens, we can also demonstrate the relatedness of rhinonyssids to
macronyssids and the origin of the former in the latter by a graded series of
transitional forms. That series starts with the bat-parasitizing omithonyssine genus
Steatonyssus, which includes some species parasitic on bats that roost in treeholes.
Pellonyssus is derived from Steatonyssus but is on birds, and the most primitive
Pellonyssus is on treehole-nesting African woodpeckers, an obvious opportunity
for ecological transfer between hosts. The features differentiating the most conser-
vative rhinonyssids from Pellonyssus are slight, though the former consistently
have more pronounced plate reduction and hypotrichy (Radovsky 1969).
The Rhinonyssidae are an extraordinarily successful group of parasites. A high
proportion of bird species that have been examined are parasitized. Levels of
host specificity vary greatly but some rhinonyssids are quite specific. Some
acarologists have reported congruence between host and rhinonyssid evolution,
have applied rhinonyssid data to problems of avian relationships within host
families, and have suggested host-tracking at higher levels (e.g. Pence and Castro
1976). I am sure that host-tracking has occurred at lower taxonomic levels and
I will not attempt to evaluate those cases that have been put forth. At the same
time, I question the concept that rhinonyssids tracked the evolutionary radiation
of birds at the higher levels such as orders or even families. The more conservative
and "omithonyssine" of the rhinonyssids are now put in the genus Tinaminyssus
and this group includes mites in a wide range of bird orders, including Passeri-
formes. One of the most conservative members of the family, separable from
Pellonyssus only by somewhat more marked reduction of plates and idiosomal
setae, was described by Strandtmann and Clifford (1962) from the varied thrush
(Passeriformes: Turdidae).
The rhinonyssids apparently derived from a highly specialized omithonyssine
in or near the genus Pellonyssus, which is associated with passeriform and
piciform hosts. That, in combination with the lack of agreement between relations
among parasites and among hosts at higher taxonomic levels, indicates that the
rhinonyssids adopted life in the nasal passages after the radiation of the birds into
their contemporary orders and most of their present families, no later than the
Miocene Epoch, perhaps IS million years ago. How then did the rhinonyssids
spread so quickly and become so ubiquitous in birds compared to the macronyssid
radiations on their hosts? I believe there are two factors. First, endoparasites,
most particularly in avian nasal passages and feeding on or through the mucosa,
are in a relatively constant environment among the greater part of the range of
avian hosts; that environmental consistency should encourage resource-tracking
and the easy transfer among hosts that come into rather casual contact (see
Strandtmann 1958, on the relation of rhinonyssid transfer to gregariousness of
hosts). Second, birds surpass all other organisms in their vagility. They are not
only preeminent fliers, they also migrate over great distances. The rhinonyssids
have gone through several grades of refinement for intranasal parasitism. At each
point, there was very likely the relaxation in barriers to changing hosts that we
have observed repeatedly with novel parasitic adaptations. At those times, given
the relatively uniform substrate and the widespread contact among birds around
the globe, it is probable that major resource-tracking radiations took place.
3.6 Sternostoma tracheacolum and a Contemporary Rhinonyssid Radiation
Most species in the genus Sternostoma are nasal mites. However, S. tracheacolum
Lawrence parasitizes the inner respiratory tract, including the lungs and air sacs
(Furman 1957, Fain and Hyland 1962, Domrow 1987). This mite species has
been found in Co1umbiformes, Psittaciformes, and many families of Passeri-
formes (among others) and is known from wild birds on all the continents. The
dissemination of this mite may be assisted by human activities, because it is
found in such caged birds as canaries. Nevertheless, we see now a mite species
with a fresh adaptation that occurs in a great array of hosts, that has an unusual
level of morphological variation, and that causes pathologies indicating recent

association with some of its hosts. It appears to be a classic instance of an incipient
taxonomic radiation in a parasite that has adopted a new host-parasite relationship,
with the emphasis in this case on resource-tracking.
4. Summary
Table 8.5 summa~izes the principal sequence of mites in three families that
is traced in this charter, gives some characteristics associated with new host
relationships and indil-utes the nature of the relationships. In nearly every case,
Table 8.5. Notable taxa, and associated characteristics, listed in a sequence

progressing from free-living predators (Hypoaspis complex) through various parasitic
relationships in three families of dermanyssoid mites.
Morphological
Taxon' Characteristic(s) Relationship with Hosts
Laelapidae
Hypoas[ ,. 'mplex Chelicerae of males similar to Free-living predators (few
females (chelate-dentate), spp. = nest associates)
but with appended
spermadactyl
AndrolaelapslLaelaps Chelicerae of males not Nidicolous; polyphagous
chelate·dentate, extremely opportunists with
adapted for sperm transfer varying degrees of
parasitic feeding
N otolaelapslNeo: qe/aps Tarsus I sensory field Ectoparasites of
chaetotax y and male megachiropteran bats
chelicerae similar to those
of Macronyssidae
Macronyssidae
Macronyssus Deutonymph non feeding Ectoparasites of
microchiropteran bats
Steatonyssus Increased engorgement in Ectoparasites of
protonymph and female microchiropteran bats
Pellonyssus Much like Steatonyssus but Ectoparasites of birds
idiosomal plate area
reduced
Rhinonyssidae
Tinaminyssus Further reduction in plates and Intranasal parasites of birds
in setae
Sternostoma, Extreme reduction in plates Intranasal parasites of birds
(most spp.) and in setae
Sternostoma Extreme variability in remnant Parasites in the lungs and
tracheacolum plates and reduced setae air sacs of birds
'Some genera selected as typifying a grade: e.g. Macronyssus typical of Macronyssinae and
Steatonyssus of Ornithonyssinae; the latter genus also is close in ancestry to Pellonyssus.
the adaptation is accompanied by a taxonomic radiation. The series is unusual in

that we can track these changes through study of extant forms and reconstruct the
history of the parasites with the help, in some cases, of the host group, including
paleontological evidence. The sequence, running through three families of mites
and extending from a free-living predatory type to a parasite that lives deep in
the respiratory system, is unusual and instructive.
References
Arthur, D. R. 1965. Feeding in ectoparasitic Acari with special reference to ticks. Adv.
Parasitol. 3:249-298.
Audy, J. R., F. J. Radovsky and P. H. Vercammen-Grandjean. 1972. Neosomy: radical
intrastadial metamorphosis associated with arthropod symbioses. 1. Med. Entomol.
9:487-494.
Baker, R. J., M. J. Novacek and N. B. Simmons. 1991. On the monophyly of bats. Syst.
Zool.40:216-231.
Bert~m, D. S., K. Unsworth and R. M. Gordon. 1946. The biology and maintenance of
Liponyssus bacoti Hirst, 1913, and an investigation into its role as vector of Litomosoides
carinii to cotton rats and white rats, together with some observations on the infection
in the white rats. Ann. Trop. Med. Parasitol. 40:228-254.
Bregetova, N. G. 1953. Mites of the genus Bdelionyssus Fonseca, 1941. Tr. Inst. Zool.
Akad. Nauk UKRSSR 13:310-319. (In Russian)
Bregetova, N. G. 1964. Some Problems of Evolution of the Rhinonyssoid Mites. (Report
presented at the 1st Int. Congr. Parasitol.). Leningrad: Nauka. Pp. 1-7.
Bregetova, N. G. 1969. Ontogeny of gamasid mites as a basis of their natural system.
Proc. 2nd. Int. Congr. Acarol. (G. O. Evans ed.). Sutton Bonington, England, 1967.
Akademiai Kaid6, Budapest. Pp. 289-295.
Camin, J. H. 1953. Observations on the life history and sensory behavior of the snake
mite, Ophionyssus natricis (Gervais) (Acarina: Macronyssidae). Chic. Acad. Sci., Spec.
Publ. No. 10. 75pp.
Costa, M. 1961. Mites associated with rodents in Israel. Bull. Br. Mus. (Nat. Hist.) Zool.
8:1-70.
Domrow, R. 1963. New records and species of Austomalayan laelapid mites. Proc. Linn.
Soc. N. S. W. 88:199-220.
Domrow, R. 1971. A new Australian species of Ornithonyssus Sambon (Acari: Dermanys-
sidae). 1. Aust. Entomol. Soc. 10:109-111.
Domrow, R. 1980. The genus Raillietia Trouessart in Australia (Acari: Dermanyssidae).
Proc. Linn. Soc. N.S.W. 104:183-193.
Domrow, R. 1987 <\cari Mesostigmata parasitic on Australian vertebrates: an annotated
checklist, keys and bibliography. Invertebr. Taxon. 1:817-948.
Dusbabek, F. 1964. Parasitische Fledermausmilben der Tschechoslowakei. II. Familie
Dermanyssidae Kol., 1859 (Acarina: Gamasides). Cesk. Parasitol. 11:77-125.
214 ! F. J. Radovsky
Eisenberg, 1. F. 1981. The Mammalian Radiations. Univ. Chicago Press, Chicago. Pp.
1-610.
Elton, C. 1966. Animal Ecology. University of Washington Press, Seattle (First published
in 1927). Pp. 1-237.
Evans, G. O. 1968. The external morphology of the post -embryonic developmental stages
of Spinturnix myoti Kol. (Acari: Mesostigmata). Acarologia 10:589-608.
Evans, G. O. and W. M. Till. 1966. Studies on the British Dermanyssidae (Acari:
Mesostigmata). Part 2. Classification. Bull. Br. Mus. (Nat. Hist.), Zool. 14:109-370.
Evans, G. O. and W. M. Till. 1979. Mesostigmatic mites of Britain and Ireland (Chelic-
erata: Acari-Parasitiformes). An introduction to their external morphology and classifi-
cation. Trans. Zool. Soc. Lond. 35:139-270.
Fain, A. and K. Hyland. 1962. The mites parasitic in the lungs of birds. The variability
of Sternostoma tracheacolum Lawrence, 1948, in domestic and wild birds. Parasitology
52:401-424.
Fonseca, A. H. and 1. L. H. Faccini. 1985. In vitro development of Raillietia auris
(Leidy) (Acarina: Mesostigmata). Acaralogia 26:211-214.
Furman, D. P. 1957. Revision of the genus Sternostoma Berlese and Trouessart (Acarina:
Rhinonyssidae). Hilgardia 26:473-495.
Furman, D. P. 1959. Feeding habits of symbiotic mesostigmatid mites of mammals in
relation to pathogen-vector potential. Am. J. Trap. Med. Hyg. 8:5-12.
Furman, D. P. 1979. Specificity, adaptation and parallel evolution in the endoparasitic
Mesostigmata of mammals. In: Recent Advances in Acarology, Vol. 2 (1. G. Rodriguez
ed.). Academic Press, NY. Pp. 329-337.
Furman, D. P., H. Bonasch, R. Springsteen, D. Stiller and D. F. Rahlmann. 1974. Studies
on the biology of the lung mite Pneumonyssus simicola Banks (Acarina: Halarachnidae)
and diagnosis of infestation in macaques. Lab. Animal Sci. 24:622-629.
Furman, D. P. and F. 1. Radovsky. 1963. A new species of Ornithonyssus from the
white-tailed antelope squirrel, with a rediagnosis of the genus Ornithonyssus (Acarina:
Dermanyssidae). Pan-Pac. Entomol. 39:75-79.
Furman, D. P. and S. W. Smith. 1973. In vitro development of two species of Orthohalar-
achne (Acarina: Halarachnidae) and adaptations of the life cycle for endoparasitism in
mammals. J. Med. Entomol. 4:415-416.
Hall, L. 1984. And then there were bats. In: Vertebrate Zoogeography and Evolution in
Australia (M. Archer and G. Clayton eds.). Hesperian Press, Carlisle (W. Australia).
Pp. 837-852.
Hand, S. 1984. Bat beginnings and biogeography: a southern perspective. In: Vertebrate
Zoogeography and Evolution in Australia (M. Archer and G. Clayton eds.). Hesperian
Press, Carlisle (W. Australia). Pp. 853-904.
Hellanthal, R. A. and R. D. Price. 1991. Biosystematics of the chewing lice of pocket
gophers. Annu. Rev. Entomol. 36:185-203.
Hogsette, 1. A., 1. F. Butler, W. V. Miller and R. D. Hall. 1991. Annotated bibliography
of the northern fowl mite, Ornithonyssus sylviarum (Canestrini and Fanzago) (Acari:
Macronyssidae). Entomol. Soc. Am. Misc. Publ. 76:1-62.
Hughes, T. E. 1959. Mites or the Acari. Athlone Press, London. Pp. 1-225.
Hull, W. B. 1956. The nymphal stages of Pneumonyssus simicola Banks, 1901 (Acarina:
Halarachnidae). J. Parasitol. 42:653-656.
Kethley, J. B. and D. E. Johnston. 1975. Resource tracking patterns in bird and mammal
ectoparasites. Misc. Publ. Entomol. Soc. Am. 9:231-236.
Kim, K. C. (ed.). 1985. Coevolution of Parasitic Arthropods and Mammals. Wiley, NY.
800 pp.
Kim, K. C., V. L. Haas and M. C. Keyes. 1980. Populations, microhabitat preference,
and effects of infestation of two species of Orthohalarachne (Halarachnidae: Acarina)
in the northern fur seal. J. Wildl. Dis. 16:45-51.
Koopman, K. F. 1984. Bats. In: Orders and Families of Recent Mammals of the World
(S. Anderson and J. K. Jones, Jr. eds.). Wiley, NY. Pp. 145-186.
Krantz, G. W. 1978. A Manual of Acarology, 2nd edition. Oregon State Univ. Book
Stores, Corvallis, OR. 509 pp.
Lavoipierre, M. M. J. and A. J. Beck. 1967. Feeding mechanisms of Chiroptonyssus
robustipes (Acarina: Macronyssidae) as observed on the transilluminated bat wing. Exp.
Parasitol. 20:312-320.
Lees, A. D. 1952. The role of cuticle growth in the feeding process of ticks. Proc. Zool.
Soc. Lond. 121:759-772.
Lindquist, E. E. 1984. Current theories on the evolution of major groups of Acari and
their relationships with other groups of Arachnida, with consequent implications for
their classification. In: Acarology V1, Vol. 1 (D. A. Griffiths and C. E. Bowman eds.).
Ellis Horwood Ltd., Chichester. Pp. 28-46.
Men, Y. T. 1959. Concerning the feeding of the mite Haemolaelaps casalis (Gamasoidea,
Parasitiformes). Medsknya Parazitol. 28:603-609. (In Russian).
Micherdzinski, W. 1980. Eine Taxonomische Analyse der Familie Macronyssidae Oude-
mans, 1936. 1. Subfamilie Ornithonyssinae Lange, 1958 (Acarina, Mesostigmata).
Panstwowe Wydownictwo Nauk., Warsaw. Pp. 1-264.
Moss, W. W. 1978. The mite genus Dermanyssus: a survey, with description of Dermanys-
sus trochilinus, n. sp., and a revised key to the species (Acari: Mesostigmata: Dermanys-
sidae). J. Med. Entomol. 14:627-640.
Nowak, R. M. 1991. Order Chiroptera. In: Walker's Mammals of the World, Vol. 1 (5th
ed.). Johns Hopkins Univ. Press, Baltimore. Pp. 190--393.
Oudemans, A. C. 1904. Notes on Acari, eleventh series. Tijdschr. Entomol. 46:93-104.
Pence, D. B. and S. D. Castro. 1976. Studies on the variation and morphology of the
Ptilonyssus "sairae" complex (Acarina: Rhinonyssidae) from North American passeri-
form birds. J. Med. Entomol. 13:71-95.
Pettigrew. J. D. 1991. Wings or brain? Convergent evolution in the origins of bats. Syst.
Zool. 40: 199-216.
Pettigrew, J. D., B. G. M. Jamieson, S. K. Robson, L. S. Hall, D. I. McAnally and H.
M. Cooper. 1989. Phylogenetic relationships between microbats, megabats and primates
(Mammalia: Chiroptera and Primates). Phil. Trans. R. Soc. Lond., B, Bioi. Sci.
325:489-559.
Phillips, C. J., J. K. Jones, Jr. and F. J. Radovsky. 1969. Macronyssid mites in the oral
mucosa of long-nosed bats: occurrence and associated pathology. Science 165: 1368-
1369.
Popp, E. 1961. Bau und Funktion des Ambulacrums der Larve von Orthohalarachne
laetalis Popp (Acarina: Halarachnidae). Zool. Anz. 167:29-33.
Potter, D. A. and D. E. Johnston. 1978. Raillietia whartoni sp. n. (Acari-Mesostigmata)
from the Uganda Kob. J. Parasitol. 64: 139-142.
Radovsky, F. J. 1960a. Haemogamasus liponyssoides hesperus n. ssp. with a discussion
of the H. liponyssoides complex (Acarina: Haemogamasidae). J. Parasitol. 46:401-
409.
Radovsky, F. J. I 960b. Biological Studies on Haemogamasus liponyssoides Ewing (Aca-
rina: Haemogamasidae). J. Parasitol. 46:410-417.
Radovsky, F. J. 1964. The Macronyssidae and Laelapidae (Acarina: Mesostigmata)
parasitic on bats. Ph.D. dissertation, Univ. of California, Berkeley, CA. 600 pp.
Radovsky, F. J. 1966. Revision of the macronyssid and laelapid mites of bats: outline of
classification with description of new genera and new type species. J. Med. Entomol.
3:93-99.
Radovsky, F. J. 1967. The Macronyssidae and Laelapidae (Acarina: Mesostigmata) para-
sitic on bats. Univ. Calif. Publ. Entomol. 46:1-288.
Radovsky, F. J. 1969. Adaptive radiation in the parasitic Mesostigmata. Acaralogia
II :450-483.
Radovsky, F. J. 1985. Evolution of mammalian mesostigmate mites. In: Coevolution of
Parasitic Arthropods and Mammals (K. C. Kim ed.). Wiley, NY. Pp. 441-504.
Radovsky, F. J., 1. K. Jones, Jr. and C. J. Phillips. 1971. Three new species of Radfordiella
(Acarina: Macronyssidae) parasitic in the mouth ofphyllostomid bats. J. Med. Entomol.
8:737-746.
Rudnick, A. 1960. A revision of the mites of the family Spinturnicidae (Acarina). Univ.
Calif. Publ. Entomol. 17: 157-284.
Sikes, R. K. and R. W. Chamberlain. 1954. Laboratory observations on three species of
bird mites. J. Parasitol. 40:691-697.
Simmons, N. B., M. J. Novacek and R. J. Baker. 1991. Approaches, methods, and the
future of the chiropteran monophyly controversy: a reply to J. D. Pettigrew. Syst. Zool.
40:239-243.
Skaliy, P. and W. J. Hayes. 1949. The biology of Liponyssus bacoti (Hirst, 1913) (Acarina:
Liponyssidae). Am. J. Trap. Med. 29:759-772.
Smith, 1. D. 1972. Systematics of the chiropteran family Mormoopidae. Misc. Publ. Mus.
Nat. Hist., Univ. Kans. 56:1-132.
Smith, J. D. and G. Madkour. 1980. Penial morphology and the question of chiropteran
monophyly. Proc. 5th Int. Bat Res. Conf. (D. E. Wilson and A. L. Gardner eds.).
Texas Tech Press, Lubbock, TX. Pp.347-365.
Strandtmann, R. W. 1958. Host specificity of bird nasal mites (Rhinonyssidae) is a

function of the gregariousness of the host. Proc. 10th Int. Congr. Entomol. 1:909-911.
Strandtmann, R. W. 1961. The immature stages of the Ptilonyssus complex (Acari:
Mesostigmata: Rhinonyssidae). Proc. 11th Int. Congr. Entomol. 1:283-286.
Strandtmann, R. W. and C. M. Clifford. 1962. A new genus and species of nasal mite
from the varied thrush lxoreus neveus (Gmelin) (Acarina: Rhinonyssidae). J. Parasitol.
48 :723-725.
Tipton, V. 1. 1960. The genus Laelaps with a review of the Laelaptinae and a new
subfamily Alphalaelaptinae. Univ. Calif. Publ. Entomol. 16:233-356.
Tsymbal, T. G. and N. T. Litvishko. 1955. Acariasis of the ear in cattle. Zool. Zh.
34:1229-1241. (In Russian).
Vitzthum, H. G. 1940-43. Acarina. In: Klassen und Ordnungen des Tierreichs (H. G.
Braun ed.). Leipzig 5(4), Book 5:1-1011.
Williams, G. L., R. L. Smiley and B. C. Redington. 1978. A taxonomic study of the
genus Haemogamasus in North America, with descriptions of two new species (Acari:
Mesostigmata, LaeJapidae). Int. J. Acarol. 4:235-273.
Woolley, T. A. 1988. Acarology: Mites and Human Welfare. Wiley, NY. Pp. 1-484.
Yunker, C. E. and F. 1. Radovsky. 1966. The dermanyssid mites of Panama (Acarina:
Dermanyssidae). In: Ectoparasites of Panama (R. L. Wenzel and V. 1. Tipton eds.).
Field Museum of Natural History, Chicago. Pp. 83-103.
9
Evolution and Life-History Patterns of Mites

Associated with Bees
George C. Eickwort
CONTENTS
I. INTRODUCTION
2. HOST TAXA
3. ASSOCIATED MITES
3.1 Astigmata
3.2 Prostigmata
3.3 Mesostigmata
4. LIFE-HISTORY STRATEGIES
4. I Nutrition
4.2 Mutualism
4.3 Phoresy and Developmental Synchronization
5. EVOLUTIONARY AND PHYLOGENETIC CONSIDERATIONS
5. 1 Evolutionary Implications of Phoresy
5.2 Patterns of Host Specificity
5.3 Phylogenetic Implications
6. CONCLUSIONS
1. Introduction
Bees (superfamily Apoidea, order Hymenoptera) represent one of the major

success stories in evolution. With about 20,000 species in 11 families (Michener
1979), they are twice as diverse as birds. All species, except cleptoparasites
(cuckoos), construct nests and provision cells with pollen and concentrated nectar
(honey), the sole food of both larvae and adults. This niche is otherwise occupied
only by a few vespid wasps.
Like other nest-making animals (e.g. birds, rodents, scarab beetles, wasps,
ants and termites), bees are hosts to a wide diversity of mites. While recent
reviews have dealt with the mites associated with social bees (especially honey
bees, stingless bees, and bumble bees) (Delfinado-Baker et al. 1989; Eickwort
1988, 1990 and references therein), there has been no attempt to present an
218
Evolution and Life-History Patterns of Mites Associated with Bees / 219
overview of the mites associated with a much greater diversity of solitary bees.
This chapter compares the mites that are associated with each of the major bee
lineages and outlines their life-history strategies. The evolutionary patterns of
these mites with respect to those of their hosts are also discussed.
I will consider only those mites that are largely or exclusively dependent upon
nourishment provided by bees or their nests. As a result, the large number of
species that incidentally occur in nests but which also commonly occur in other
habitats are excluded. These incidental species may be the most abundant and
conspicuous mites in social bee nests, especially the scavenger "stored product
mites" that invade the hives of honey bees (Eickwort 1988, 1990). I also exclude
generalized parasites which are not host-specific to bees. Although some of these
mites can be ecologically important to their hosts, they show no evidence of
having evolved specific adaptations for living in bee nests, and their evolutionary
patterns have developed independently of apoid evolution.
The distinction between important and incidental associates is not often made
in the literature. Most accounts of bee mites involve only descriptions of those
stages that are phoretic on the bees. It is not true that every mite that "hitch-
hikes" on a bee developed in that bee's nest. For example, the conspicuous
deutonymphs of Uropodidae are frequently phoretic on solitary bees (e.g. Haese-
ler 1982), but there is no evidence that any uropodine species develops in solitary
bee nests. Moreover, the study of bee mites is in its infancy, and only a few of
the vast number of mite species found attached to bees in museum collections
have been described.
Given these restrictions, the summary of important bee mites in Tables 9.1-
9.3 is mostly preliminary. These tables are based on associations reported in the
literature and supplemental associations based on material in the Cornell Univer-
sity Insect Collections. Where one host subfamily predominates among several
recorded for a mite genus, that subfamily is marked with an asterisk in the tables.
2. Host Taxa
Traditionally, bees have been divided into two major groupings, the supposedly
more primitive "short-tongued bees" (Andrenidae, COlletidae, Ctenoplectridae,
Halictidae, Melittidae, Oxaeidae, and Stenotritidae), and the more advanced
"long-tongued bees" (Anthophoridae, Apidae, Fideliidae, and Megachilidae)
(Michener 1979). Recent studies indicate that most families of short-tongued bees
are not of the evolutionary lineage that gave rise to the long-tongued bees, and
the relationships among these families are obscure, with considerable plesiomor-
phy and convergence masking their true phylogeny. My hypothesis of relation-
ships among bee families and subfamilies with known mite associates is given in
Figure 9.1.
Most short-tongued bees nest solitarily or communally, with primitively euso-
220 / G. C. Eickwort
Table 9.1. Acari associated with short-tongued bees. Numbers in parentheses

represent the numbers of described species.
Genus Host taxon Distribution b Ecology'
ASTIGMATA
Histiostomatidae
Anoetus (10) Halictinae NE, NT. PA,
AU
Glyphanoetus' (I) Nomiinae NE
Histiostoma' Diphaglossinae NE,NT
Acaridae
Sancassania' (I) Halictinae & Nomiinae NE c, s
Schulzea' (2) Halictinae & Hylaeinae NT, PA, OR s<)
Konoglyphus (I) Halictinae NT s?
Halictacarus (I) Halictinae ET s')
Ctenocolletacarus (3) Stenotritidae AU c, s?
Winterschmidtiidae
New genus d Hylaeinae AU s"
PROSTIGMATA
Trochometridiidae
Trochometridium' (I) Halictinae, Nomiinae, & NE.NT
Panurginae
Pygmephoridae
Parapygmephorus (Sicilipes) (5) Halictinae NE,NT, PA
P. (Parapygmephorus;' (I) Nomiinae & Halictinae ET, OR
Scutacaridae
/ mparipe s' (11) Halictinae, Nomiinae, NE,NT, PA
Rophitinae, & Andreninae
Scutacarus' (I) Halictinae NE
Nasutiscutacarus (2) Nomiinae OR
MESOSTIGMAT AAmeroseiidae
Neocypholaelaps' (I) Hylaeinae OR c
Laelapidae
Hypoaspis s.l.' Diphaglossinae NT pr
Laelaspoides (I) Halictinae NE, AU? c
a = Some species not associated with short-tongued bees.

b = AU = Australian, ET = Ethiopian, NE = Nearctic, NT = Neotropical, OR = Oriental,
PA = Palearctic.
c = c = provisions (c1eptoparasite); pr = predator; s = scavenger or saprophyte.
d = From OConnor, 1988.
cial colonies occurring only in sweat bees (Halictinae). Most short-tongued bees
nest in the soil (a few nest in rotting wood) and line their cells with glandular
secretions (Fig. 9.2a). These secretions provide a homeostatic environment for
the stored provisions (a semi-solid loaf of dilute honey and pollen) and developing
larvae. The adult bees do not tend their brood after they oviposit and close the
cells. If a bee larva fails to develop, the provision mass is quickly enveloped by
Table 9.2. Acari associated with long-tongued bees (except Apidae). Numbers in
parentheses represent the numbers of described species. Where a host subfamily is
predominantly used, among several recorded for a mite genus, that subfamily is
marked with an asterisk.
ASTIGMATA
Histiostomatidae
Histiostoma s.I.' (2) Anthophorinae & Xylocopinae NE,NT,ET
Acaridae
Sancassania' Megachilinae NE c, s
Horstia' (14) Xylocopinae* & Megachilinae NE, NT, PA, ET, c, s?
OR, AU
Neohorstia (I) Megachilinae PA s?
Cerophagopsis' (2) Megachilinae OR,PA,NE s?
Megachiiopus (I) Megachilinae ET s?
Sennertionyx (I) Megachilinae PA, NE s?
Schulzea' (I) Megachilinae PA s~
New genus d Anthophorinae s?

New genus d Anthophorinae NT s?
Suidasiidae
Tortonia' (3) Megachilinae & Xylocopinae PA,OR,NE,ET c, s?
Winterschmidtiidae
Vidia (7) Megachilinae PA,NE,OR, ET
Chaetodactylidae
Chaetodactylus (15) Megachilinae*, Lithurginae, NE,NT,PA,ET c
Xylocopinae, &
Anthophorinae
Sennertia (59) Xylocopinae* & Megachilinae NT, AU, PA, NE, e
OR,ET
Roubikia (I) Anthophorinae NT c?
PROSTIGMATA
Cheyletidae
Cheletophyes (13) Xylocopinae ET,OR,NT pr
Tarsonemidae
Tarsonemus' (2) Xylocopinae NT,OR s?
Trochometridiidae
Trochometridium' (I) Anthophorinae NE
MESOSTIGMATA
Ameroseiidae
Ajrocypholaelaps' (2) Megachilinae & Xylocopinae ET c
Neocypholaelaps' (6) Ctenoplectridae, Anthophorinae, ET c
Megachilinae, & Xylocopinae
Laelapidae
Hypoaspis s.l.' (2) Xylocopinae & Megachilinae OR,ET pr
Dinogamasus (36) Xylocopinae PA, ET, OR s?
a = Some species not associated with long-tongued bees.

PA = Palearctic.
c = c = provisions (cleptoparasite); pr = predator; s = scavenger or saprophyte.
d = From OConnor, 1988.
221
Table 9.3. Acari associated with apid bees. Numbers in parentheses represent the
numbers of described species.
ASTIGMATA
Meliponocoptidae
Meliponocoptes (3) Meliponinae NT sry
Meliponoecius (I) Meliponinae NT sry
New genus" NT ry
Meliponinae
Acaridae
Kuzinia (6) Bombinae PA,NE,OR s, c
Cerophagopsis' (I) Meliponinae AU sry
Horstiella (2) Euglossinae NT s?
Gaudiellidae
C erophagus (2) Bombinae PA,NE s?
Platyglyphus (I) Meliponinae OR s?
Gaudiella (2) Meliponinae NT s?
Partamonacoptes (I) Meliponinae NT s?
Meliponopus (I) Meliponinae NT sry
Carpoglyphidae
Carpog/yphus' (1) Apinae NE, PA c
PROSTIGMATA
Tydeidae
Proctotydeus' (3) Meliponinae NT
Melissotydeus (I) Meliponinae NT s?
Scutacaridae
lmparipes' (2) Apinae & Bombinae NE, PA
Scutacarus' (3) Apinae & Bombinae PA,NE, NT
Parascutacarus (I) Bombinae OR
Tarsonemidae
Tarsonemus' (I) Apinae PA s?
P seudacarapis (1) Apinae OR ry
Acarapis (3) Apinae NT. PA, NE, AU, pa
OR,ET
Podapolipidae
Locustacarus' (I) Bombinae NE, AU, PA, OR pa
MESOSTIGMAT A
Parasitidae
Parasitellus (18) Bombinae PA, NE pr, c
Family?
Meliponipachys (I) Meliponinae NT pr?
Macrochelidae
Macrocheles' (1) Apinae & Bombinae NE pr
Trigonholapsis (1) Meliponinae NT pr?
Grafia (3) Meliponinac NT pr?
Ascidae
Proctolaelaps' (2) Bombinae PA, NE c?
Continued
222
Table 9.3. Continued.

Ameroseiidae
Afrocypholaelaps' (1) Meliponinae & Apinae ET, AU c
NeocyphoLaelaps' (7) Meliponinae & Apinae AU, OR, ET, PA c
EdbareLLus (1) Apinae AU c
Laelapidae
Hypoaspis s.l.' (3) Meliponinae NT pr
Urozercon' (I) Meliponinae NT pr
PneumoLaeLaps (18) Bombinae PA,NE pr, c
Neohypoaspis (I) Meliponinae NT pr
Hunteria (I) Meliponinae NT pr?
SteveLus (I) Meliponinae NT pr?
Melittiphisoides (I) Meliponinae NT pr?
MeLiponaspis (I) Meliponinae ET pr?
EumelLitiphis (3) Meliponinae OR,NT pr?
Zontia (I) Meliponinae NT pr?
Bisternalis' (5) Meliponinae NT pr
Melittiphis (I) Apinae AU, PA, NE, OR, c
TropiLaeLaps (2) Apinae AU pa
Varroidae
Varroa (2) Apinae OR, NT, NE, PA, pa
ET, AU
E uvarroa (I) Apinae OR pa
Trachyuropodidae
Oplitis' (I) Meliponinae NT s?
UrodiscelLa' (I) Meliponinae NT s?
Diplogyniidae
CaLaenosthanus (I) Meliponinae NT ?
Triplogyniidae
TripLogynium' (I) Meliponinae NT ?
a = Some species not associated with apid bees.

PA = Palearctic.
c = c = provisions (cleptoparasite); pr = predator; pa = parasite; s = scavenger or saprophyte.
d = B. M. OConnor, pers. comm.
fungus. If the larva survives, it defecates on the cell wall after it consumes the
provision mass, and this fecal mass often becomes fungus-infected. Nematodes
and small annelids (Enchytraeidae) also commonly infest provision masses and
feces. Mites within nests of solitary bees are most often restricted to individual
cells and they typically enter them by being phoretic on the mother bees. Some
mites, however, can move through the soil to invade closed cells.
An exception to the above pattern is found in most Colletidae, which line their
cells with a cellophane-like secretion and store fluid provisions. The Hylaeinae
are renters, reusing natural or insect-made cavities (often in twigs or logs) rather
224 I G. C. Eickwort
Apinae
Meliponinae
Euglossinae
Anthophorlnae
Xylocopinae - - « . P I D A E
. . Megachilinae
Llthurglr;;al
ANTHOPHORIDAE ...,
CTENOPLECTRIDAE
Figure 9.1. Hypothesized phylogenetic relationships offamilies and subfamilies of bees

associated with mites.
than digging burrows themselves. These nests are exposed to mites that inhabit
woody vegetation rather than soil.
The long-tongued bees form a monophyletic lineage. Most Megachilidae line
their cells with foreign materials (e.g. leaves, plant hairs, or resin) instead of a
glandular secretion (Fig. 9.2b). While more primitive Megachilidae excavate
nests in soil or occasionally solid wood, many megachilid lineages include renters
of preexisting cavities and builders of free-standing masonry nests.
The two subfamilies of noncleptoparasitic Anthophoridae are quite different in
their nesting biology. The Anthophorinae are principally solitary or communal
soil-nesters, making similar nests to those of the short-tongued bees. The Xylo-
copinae, or carpenter bees, mostly excavate nests in wood or pithy stems and do
PROVISIONS
Laelapidae
Acaridae FUNGUS
Pygmeph~ridae
Scutacandae
."
" .,'
SURFACE
MICROBES
Histiostomati HALICTIDAE
(A)
Figure 9.2. Mite feeding guilds. (A) Feeding guilds of mites within nests of sweat bees
(Halictidae). (B) Feeding guilds of mites within nests oflarge carpenter bees (Anthophori-
dae: Xylocopa) and leafcutter bees (Megachilidae: Megachile). (C) Feeding guilds of mites
within nests of bumble bees (Apidae: Bombus) and honey bees (Apidae: Apis).
not secrete a thick cell lining. Adult carpenter bees are comparatively long-lived,
most have overlapping generations, and many are semisocial or primitively
eusocial.
Bees in the family Apidae (Fig. 9.2c) build free-standing cells of secreted wax
and/or foreign materials, especially resins, that are typically clustered in natural
cavities. Apid bees are comparatively long-lived and an overlap of generations
and reuse of cavities is common. The subfamily Euglossinae are solitary or
semi social neotropical orchid bees, and the remaining apids are all eusocial.
Bumble bees (Bombinae) are primitively eusocial and form annual colonies,
Their nests are often built in abandoned rodent nests and are consequently exposed
to mite residents of those habitats.
The advanced eusocial stingless bees (Meliponinae) and honey bees (Apinae)
form perennial colonies that are initiated by swarms of workers accompanying a
queen, and they store honey and pollen separate from the developing brood. In
contrast to nests of bees in other families, there is extensive waste material
MEGACHILE
SURFACE
FEEDER
Dinogamasus
PREDATOR
Cheyletidae
FUNGUS
XYLOCOPA Winterschmidtiidae
(B)
produced in apid nests, and this waste provides an ample substrate on which
mites can develop outside of the brood cells.
3. Associated Mites
3.1 Astigmata
The Astigmata are typically the most abundant mites in nests of bees, as they are
in nests of social insects in general (Eickwort 1990). They are unusual among
mites because they are nonpredators that specialize in the exploitation of nutrient-
rich, temporary habitats, especially insect and vertebrate nests (OConnor 1982).
The development of a specialized phoretic deutonymph is an important aspect of
Evolution and Life-History Patterns of Mites Associated with Bees I 227
ADULT
PARASITE
&.ar.apis
BROOD
PARASITE
Tropi laelaps
PREDATOR Varroidae
Parasitidae
Macrochelidae
(C)
their adaptation to nest-building insect hosts. The production of deutonymphs is

typically synchronized with the emergence of new adult bees within a nest. The
phylogeny of insect-associated Astigmata has been the subject of intensive study
by OConnor, and his recent review of Astigmata associated with Apoidea (1988)
forms the basis of the following summary.
Histiostomatid mites have chelicerae modified for filter feeding and they typi-
cally inhabit surfaces with liquid films from which they obtain microorganisms.
Anoetus, as defined by Mahunka (1974), contains only obligatory associates of
halictine (sweat) bees, and they are the most commonly encountered mites in
halictine nests worldwide. These mites occur in association with both solitary
and social halictine species. Some species of the halictine genus Lasioglossum
carry deutonymphs of Anoetus in a specialized acarinarium on the anterior surface
of metasomal tergum I. Deutonymphs remain on their female hosts while the
latter hibernate, and they detach from host bees as new cells are constructed in
the spring. Tritonymphs and adult females are subsequently found on the provi-
sions where they sweep the surface, presumably feeding on microorganisms. A
very small (larva-sized) adult male then becomes apparent, typically when it
climbs on the dorsum of a female. 1 suspect that these males develop rapidly from
the first unfertilized eggs laid by the females, perhaps skipping all nymphal
instars, and then mate with females of the parental generation. The inseminated
females then lay fertilized eggs, all of which develop into females. Those female
eggs are laid on the cell wall and bee larvae, and mite larvae and protonymphs
feed on the surfaces of the bee larvae and pupae, apparently consuming microor-
ganisms; they do not harm the bees upon which they feed (Eickwort 1979, and
in prep.).
Histiostomatids currently placed in the plesiomorphic catch-all genera Histio-
stoma and Glyphanoetus occur on other taxa of bees (Tables 9.1, 9.2). These
mites can develop huge populations in cells without killing their hosts, and their
development and biology appears similar to that of Anoetus.
The Acaridae include numerous mites that occur as scavengers and cleptopara-
sites in nests of both solitary and social bees, feeding on fungi, honey and pollen.
Many of these are stored-product pests that can become the most numerous mites
in honey bee hives (Eickwort 1988), although they are not phoretic on bees and
are not specialized for associations with them. Sancassania (= Caloglyphus)
contains species with a wide variety of associations with arthropods, including
soil-nesting bees (Eickwort 1979; Cross and Bohart 1969, 1991). In cells these
mites may occur on feces deposited by bee larvae, but they are especially abundant
in cells containing dead bees and moldy provisions. The mites burrow through
and tear apart the provision masses, consuming pollen, fungi, and dead brood.
There is, however, no evidence that the mites kill the brood; they are presumably
scavengers that take special advantage of food resources in cells in which brood
fail to develop. Deutonymphs are facultatively produced and are phoretic on bees
that develop in other cells; it is probable that these deutonymphs move through
the soil to locate their hosts in the nest burrows.
Ctenocolletacarus, an acarid genus closely related to Sancassania (OConnor
1988), is restricted to bees of the genus Ctenocolletes (Stenotritidae) (Fain 1984a,
Fain and Houston 1986). In the nest cells, the deutonymphs molt into tritonymphs
and then into adults. Adults are found on the provision masses and cell walls,
where females lay eggs. The larval and protonymphal mites occur on developing
bee larvae, provisions, and fecal masses. Gut analyses indicate that these mites
first consume pollen grains from the provision masses, and then feed on an
amorphous substance that may originate from the bee larva's surface or from its
feces. Deutonymphs are obligatory and are found in specialized acarinaria on
each side of the third and fourth metasomal terga of female bees. Of adult female
Ctenocolletes, 74%-90% (four species) carry deutonymphs (Houston 1987).
A diverse lineage of the Acaridae, the subfamily Horstiinae (= Tyrophaginae
of OConnor, 1982), has evolved in association with bees (OConnor 1988). This
includes Kuzinia associated with bumble bees; Horstia (including Ceroglyphus)
associated primarily with carpenter bees; Horstiella associated with Euglossinae;
Sennertionyx, Neohorstia, Cerophagopsis, and Megachilopus associated with
Megachilinae and Meliponinae, two unnamed genera associated with Anthophori-

nae, and Konoglyphus, Halictacarus and Schulzea associated with Halictinae
(species of the latter genus also occur on other bees) (OConnor 1988).
Kuzinia is typically the most abundant mite in bumble bee nests, where they
feed on pollen, honey, organic refuse, and cocoon substances but do not harm
developing bees (Chmielewski 1969, 1971). Horstia virginica may produce large
populations in cells of the carpenter bee Xylocopa virginica after the bee brood
die. The mites feed on nectar in the provisions, and it has been hypothesized that
the mites frequently kill the bee brood (Krombein 1962a). Infestation rates were
very low in Krombein's study; only three nests of "several hundred" contained
mites. Although most species of Horstia have been described from xylocopine
bees, individual deutonymphs have been found on other bees and wasps (Fain
1984b), and one species has even been recovered from house dust (Fain and
Chmielewski 1987).
Nothing has been published about the biology of other genera of this lineage,
although collection data for three genera indicate that they do not harm the bee
brood (OConnor 1988). Also, the females of Thectochlora alaris (Halictinae)
have a specialized acarinarium on metasomal tergum I in which deutonymphs of
an unnamed species of Schulzea are phoretic (Eickwort and OConnor, unpubl.).
The Suidasiidae includes Tortonia, whose species are all associates of various
bees and wasps (OConnor 1988). The biology of Tortonia species appears to vary
according to host, and host specificity also varies. Some species are apparently
obligate associates of Megachilidae, while T. quadridens is associated with
solitary wasps and the carpenter bee X. virginica. T. quadridens may kill carpenter
bee brood before acting as a cleptoparasite or scavenger (OConnor observed T.
quadridens killing brood of the sphecid wasp Trypoxylon, although Krombein
[1962a] observed mites developing in cells containing live larvae of the vespid
Monobia).
A related lineage of obligatory bee associates has been placed in the family
Gaudiellidae by OConnor (1988). It includes Cerophagus, associated with bum-
ble bees (OConnor 1992a), and four genera associated with stingless bees. The
biology of these mites is unknown.
The superfamily Hemisarcoptoidea is primitively fungivorous and associated
with wood-boring insects (OConnor 1982). Representatives of four families have
associations with bees. Vidia (Winterschmidtiidae) is primarily associated with
megachiline bees. These mites occur on the leaf pieces that form the cell linings
of leafcutter bees (Megachile) , where they apparently feed solely on fungi.
Deutonymphs are obligatory and attach to the mature bee larva before it spins its
cocoon, spending the winter on the diapausing bee larva (OConnor and Eickwort
1988).
An undescribed genus ofWinterschmidtiidae occurs in association with Austra-
lian Hylaeinae. Feeding stages are attached to the bee larvae (T. Houston,
reported in OConnor 1988). The Meliponocoptidae consists of specialized genera
(Meliponocoptes, Meliponoecius; and an undescribed genus, OConnor, pers.

comm.) known from adults in stingless bee nests (Fain and Rosa 1983); nothing
is known about their biology.
The family Chaetodactylidae is restricted to associates of bees. Chaetodactylus
is associated primarily with Megachilidae (Fain 1981b), and Sennertia is associ-
ated primarily with Xylocopinae (Fain 1981a). Roubikia is associated with Tet-
rapedia (Anthophorinae) (Baker et al. 1987, OConnor 1992b). As with Horstia
and Tortonia, Sennertia may occur in large numbers on the provision masses in
cells of Xylocopa that lack developing brood, apparently feeding on pollen (Skaife
1952). Lombert et al. (1987) hypothesized that this mite is a cleptoparasite that
may kill the brood. However, Sennertia also develops in cells without killing
brood (Skaife 1952, Watmough 1974, OConnor 1988). Chaetodactylus have
been observed to kill eggs or young larvae and then develop as cleptoparasites,
feeding on the provisions and undergoing several generations in a cell (Krombein
1962b, Fain 1966, Maeta 1978), although Torchio (pers. comm.) has observed
that brood killing is facultative in a species associated with Osmia lignaria.
Two types of deutonymphs are produced when the provisions are consumed,
an inert deutonymph which is pharate in the protonymphal cuticle and an active
deutonymph. The active deutonymphs attach to bees that emerge from other cells
and pass through the infested cell, while the inert deutonymphs remain in the
cells as a reservoir to infest hosts that reuse a burrow. Infestation rates are low;
typically less than 15% of cells in nests of seven species of Osmia.
The family Carpoglyphidae is best known as stored product mites, and Carpo-
glyphus lactis occurs in foods with high sugar content that have begun fermenta-
tion, including stored pollen and honey in honey bee hives (Eickwort 1988). All
nondeutonymphal stages of a species of Carpoglyphus have been collected inside
flowers and deutonymphs are also phoretic on butterflies and moths (Fain and
Rack 1987). It is possible that Carpoglyphus (under natural conditions) develops
much like Neocypholaelaps (Mesostigmata) in flowers, using various flower-
visiting insects as phoretic hosts, and is also capable of reproducing on stored
provisions in apid colonies.
3.2 Prostigmata
Relatively few taxa of the diverse suborder Prostigmata have evolved important
relationships with bees. Among the "red velvet mites" of the Parasitengona,
larvae of Leptus (Erythraeidae) commonly parasitize bees (e.g. Southcott 1989)
but there is no indication that they specialize on them. Fungivorous Proctotydeus
and Melissotydeus (Tydeidae) are abundant in stingless bee colonies and may
be mutualistic (Flechtmann and Camargo 1979). Predaceous Prostigmata may
facultatively occur in nests (especially of social apids) where they feed predomi-
nantly on Astigmata. Species of Cheletophyes (Cheyletidae) are restricted to
associations with large carpenter bees (Xylocopinae) (Fain et al. 1980, Smiley
and Whitaker 1981, Putatunda and Kapil 1988). All stages occur in nests and
adult females are phoretic, often found in the acarinaria of the female bees that
house Dinogamasus (Mesostigmata). Cheletophyes apicola occurs in separate
thoracic acarinaria on Xylocopes latipes (OConnor 1993). Cheletophyes are un-
doubtedly predators on astigmatid mites in carpenter bee nests, and OConnor
(1993) hypothesizes that the increased sclerotization on astigmatids associated
with Old World Xylocopa may be an evolutionary response to this predator.
The majority of the prostigmatid bee associates are in the Heterostigmata.
Trochometridium tribulatum (Trochometridiidae) occurs in the nests of diverse
soil-dwelling bees and other insects (Cross and Bohart 1979). Adult females,
which are phoretic, possess well-developed cavities (sporothecae) in which they
place fungal spores (Lindquist 1985). The fungus infests the provision masses in
cells in which the bee brood has died, and adult female mites feed on the fungal
hyphae. The inactive larvae do not feed before molting into adults. Adult males
also do not feed, and they mate with females immediately upon the latter's
emergence. Newly mated females disperse from cells to locate bees elsewhere in
the nest. Careful observations by Cross and Bohart indicate that these mites do
not develop in cells containing living brood; it is not known if the Trochometrid-
ium actually kill the brood.
Species of the Pyemotes ventricosus complex (Pyemotidae) often occur as
parasites of bee larvae in nests (Cross and Moser 1975, Eickwort 1988) and P.
ventricosus itself was described from nests of Anthophora (Anthophorinae).
However, the mites are not phoretic and there is no indication that any species
in the complex is specialized as a bee parasite.
The families Pygmephoridae and Scutacaridae are fungus-feeding heterostig-
matids that are among the most frequent and diverse associates of bees, second
in abundance only to the Astigmata. Parapygmephorus (Sicilipes) are restricted
to the Halictinae. The life cycle of P. (S.) costaricanus closely follows that of
its host, Agapostemon nasutus (Rack and Eickwort 1980). Adult female mites
are phoretic and detach when the bees prepare cells. They occur on the cell wall
(or possibly in the surrounding soil) while the bee larva consumes its provisions.
The mites move onto the feces when the mature bee larva defecates. There they
lay eggs which hatch into larvae, which feed on the fungus in the feces. The
larvae molt into adult males and females, and after mating the females move onto
the cell walls. They transfer to the adult bees upon their emergence. The mites
do not feed on the surface of either the provisions or the developing bees, and
they do not occur in cells in which the brood has died and provisions are moldy.
Many species of Imparipes (Imparipes) (Scutacaridae) are bee associates,
especially of soil-nesting solitary bees. Imparipes apicola has been recovered
from diverse taxa of bees (Delfinado and Baker 1976), has been studied in
association with halictine bees (Eickwort 1979) and is being studied in association
with the alkali bee Nomia melanderi by Bohart and Cross (pers. comm.). The
life cycle is similar to that of Parapygmephorus costaricanus. In contrast to P.
costaricanus, the adult females appear to readily move through the soil and thus
have the potential to invade numerous cells. When the halictine bee brood dies,
the mites readily feed on the fungus that infests the decaying brood or provision
mass, and several generations and very large populations can develop (although
this is not usual in nests of Nomia).
Under laboratory conditions, I have observed female mites moving onto bee
eggs and becoming physogastric. As halictine eggs nearly always perish under
laboratory conditions, this is not evidence that the mites kill the eggs, and Cross
has not observed this with Nomia. The mites can develop in cells in which living
brood occurs, feeding on the fungus that infests the bee feces.
Most Scutacarus are not bee associates, but Scutacarus acarorum is a cosmo-
politan associate of bumble bees. About half of all Danish overwintering bumble
bee queens bear phoretic females (Schousboe 1986). Under laboratory conditions,
S. acarorum fed and developed preferentially on Histioplasma, a common fungus
in old rodent nests (a preferred nesting site for bumble bees). S. acarorum
occasionally occurs in honey bee hives, perhaps introduced by bumble bee queens
which invaded the hives. Despite the frequent co-occurrence of S. acarorum and
bumble bees, the species appears not to be restricted to associations with bees,
as it is a common inhabitant of meadow soils.
Many Tarsonemidae are also fungivorous, and at least some species phoretic
on bees are probably incidental associates (Eickwort 1988). Two Tarsonemus
species recently described from large carpenter bee nests and in the acarinaria of
female bees (Magowski 1986, OConnor 1993) exhibit morphological characters
that suggest evolutionary modifications for bee association, as does Pseudacar-
apis indoapis in association with an Asian honey bee (Lindquist 1986). The genus
Acarapis is restricted to honey bees (Apinae), and its species are parasites of the
adult bees. This genus includes the economically important tracheal mite, A.
woodi, of the European honey bee.
The related family Podapolipidae consists entirely of insect ectoparasites,
most of whose hosts are beetles and orthopteroids. The genus Locustacarus,
predominantly parasites of grasshoppers, contains one species (L. buchneri)
which is a cosmopol;tan ectoparasite of bumble bees (Husband and Sinha 1970).
Like A. woodi, L. buchneri is a tracheal mite; only the inseminated larval female
leaves the tracheae to disperse to other bees.
3.3 Mesostigmata
Mesostigmatid mites are primarily large, free-living predators. In comparison to

the other suborders, proportionately more mesostigmatid associates occur in nests
of long-tongued bees than in nests of short-tongued bees. Predatory mites may,
however, incidentally invade the nests of all bees.
Both Macrochelidae and Parasitidae frequently invade the nests of social Api-
dae, often becoming the most conspicuous mites in them. Macrocheles are not
usually phoretic on their bee hosts and are probably not restricted to bee nests.
Even Macrocheles praedafimetorum, described from bumble bee nests and com-
mon as a predator on nematodes and fly maggots in them, depends on beetles as
phoretic hosts (Richards and Richards 1977). Cross and Bohart (pers. comm.)
found Macrocheles feeding on nematodes in an alkali bee (Nomia melanderi)
nest site, and these mites were phoretic upon the bees. Two genera of Macrocheli-
dae known only as associates of stingless bees (Vitzthum 1930, Krantz 1962)
have also been described from nests rather than as phoretic females.
Parasitellus (previously Parasitus) (Parasitidae) do appear to be specialized
associates of bumble bees, with deutonymphs phoretic on adult bees, including
overwintering queens. Under laboratory conditions, the mites feed on provisions
and wax as well as being predators on other arthropods (Richards and Richards
1976). Parasitellus occur in 96% of bumble bee nests in Canada and on 25%-
28% of overwintering potential queens in Denmark (Schousboe 1987).
The subfamily Hypoaspidinae of the Laelapidae contains a diverse assemblage
of free-living and insect-associated mites (see Eickwort 1990). The catch-all
genus Hypoaspis sensu lato contains species found in nests of diverse bees,
ranging from ground-nesting colletids, to carpenter bees, to stingless bees. The
biology of these mites has not been studied in bt'e nests.
The closely related genera (or subgenera of Hypoaspis) Pneumolaelaps and
Laelaspoides are restricted to bees. The former genus is associated with bumble
bees, in whose nests they may be very common. They move rapidly through the
nest to explore nectar pots and brood cells. They appear to be especially attracted
to bee larvae during provisioning periods. The mites remove honey and surface
lipids of pollen from the provisions (Royce and Krantz 1989). They also feed on
injured bees and are predators of astigmatid mites (Costa 1966, Hunter and
Husband 1973). Laelaspoides is associated with halictine bees, in whose nests it
also feeds on pollen (Eickwort 1979). The unrelated hypoaspidine genus Melit-
tiphis occurs in Apis hives (Eickwort 1988), where it has been shown by Gibbins
and van Toor (1990) to feed on pollen.
Dinogamasus is restricted to the Old World subgenera of Xylocopa, especially
Mesotrichia, Koptortosoma, and Afroxylocopa, those large carpenter bees in
which females possess a pouch-like acarinarium on the first metasomal tergum
(LeVeque 1930; Watmough 1974; OConnor 1993; Newell, pers. comm.). Studies
by Skaife (1952) and especially Madel (1975) have elucidated some aspects of
the biology of these fascinating symbionts. The acarinarium contains adult female
Dinogamasus mites (on average, 21 D. villosior on the host X. flavorufa). The
mites disembark gradually as the bees provision cells, so that all cells in a nest
receive some mites. The female mites stay on the bee larvae as the latter feed,
and each mite lays two to three eggs on the surface of a bee larva or pupa. The
developing ins tars also occur on bee larvae and pupae, and all instars (except the
nonfeeding larva) obtain their nourishment from the host's cuticle, probably from
surface "exudates" (or contaminants?). They do not appear to harm their hosts
(however, Watmough (1974) considers them to be ectoparasites and claims that

there is a weight loss in pupae proportionate to the mite load). Adult female mites
transfer to the acarinaria of newly emerged adult female bees; those developing
in cells with male bees apparently contact female bees emerging from other cells.
Apparently Dinogamasus is thelytokous as only females were found in the two
studies involving reared material.
Nine hypoaspidine genera are known only from stingless bee nests. Little is
known about the biology of these mites; Neohypoaspis ampliseta is a predator of
astigmatid mites in nests of Trigona (Delfinado et al. 1983). Despite the fact that
all stages occur in vast numbers in the nests, N. ampliseta is not phoretic on the
bees, as is also true of other hypoaspidine associates of stingless bees. In contrast,
Tropilaelaps, Varroa, and Euvarroa have evolved as ectoparasites of honey bee
brood (Eickwort 1988), with the species in the former two genera becoming
serious economic pests.
A different association with bees is exhibited by Neocypholaelaps and related
genera in the Ameroseiidae, as well as by some Proctolaelaps (Ascidae). These
mites reproduce in flowers and use bees and other insects as phoretic hosts,
similar to the hummingbird mites studied by Colwell (see Chapter 2, this volume).
The mites feed on nectar and pollen and may invade provisions if they enter bee
nests. Most species appear to be nonspecific as to their phoretic hosts, and a wide
variety of bees, both solitary and social, are represented among the hosts of
Neocypholaelaps and AJrocypholaelaps. However, N. phooni and N. malayensis
have characteristics that suggest a more intimate association with their Asian
stingless bee hosts (Delfinado-Baker et al. 1989).
A number of other mesostigmatid mites have been described from stingless
bee nests, although the level of association is unknown. These include the
enigmatic gamasine Meliponapachys, the trigynaspid Calaenosthanus, and uro-
podines of two genera (Oplitis and Urodiscella) whose species are otherwise
associated with ants or termites and which may be incidental in stingless bee
nests.
4. Life-History Strategies
4.1 Nutrition
Saprophagy, especially fungivory, is the predominant nutritional mode among

the important mite associates of bees, characterizing 53% of the genera in Tables
9.1-9.3. In solitary bee nests with secreted cell linings, fungal hyphae are not
available to mites until the bee larvae finish their provisions and defecate on the
cell walls. The feces then commonly become moldy, and saprophagous mites
feed, develop, and reproduce on them. If, however, the bee brood dies, the
provisions and the brood itself quickly become moldy and many saprophagous
mites are able to take advantage of this opportunity and produce large numbers
of offspring. There should be strong selective pressure for such mites to enhance
their reproductive potential by killing the bee egg or larva, and this is suspected
for Imparipes, Trochometridium, and Tortonia.
There is a contradictory selective pressure for saprophagous mites not to kill
the brood in the cells they occupy, because the emerging adult bees will serve as
phoretic hosts to take the next generation of mites to new nests. Indeed, in most
cases bee brood develops successfully in cells in which saprophagous mites also
reproduce. Fungivorous and bacteriophagous mites may even be beneficial to the
bees, as discussed in the next section.
The opportunities for fungivorous mites are somewhat different in nests of bees
that lack secreted cell linings and in nests of the social apids. The leaves that line
the cells of leaf-cutter bees typically become moldy, and this fungus apparently
is a nutritional resource for Vidia. In the nests of bumble bees, honey bees, and
stingless bees, fungal contamination is not limited to the contents of closed brood
cells, and saprophagous mites (both obligatory and facultative) may become
extremely abundant in moldy debris (Eickwort 1990).
A different type of saprophagy characterizes the bee-associated Histiostomati-
dae, which appear to be bacteriophages. These mites sweep the surfaces of
provision masses and the brood itself, without harming the bees. Dinogamasus
may also remove surface microbes from carpenter bee brood.
Saprophagous mites in feces and in provision masses may consume pollen and
honey as well as fungus and other contaminants. It thus can be difficult to separate
cleptoparasitism, the "stealing" of pollen and honey provisions, from saprophagy.
Chaetodactylus, Ctenocolletacarus, Horstia, Kuzinia, Sancassania, Sennertia
and Tortonia are Astigmata (presumably with saprophagous ancestry) that have
been recorded as feeding on provisions. As with strict saprophages, there should
be a selective advantage for a mite to kill the bee brood in order to have
exclusive use of the provisions for its own reproduction. This has been observed
facultatively in Chaetodactylus and Horstia.
The phoretic instars produced in cells in which the brood was killed must locate
adult bees which successfully developed in other cells in the nest. These mites
thus characteristically attack bees which construct cells in linear series (such as
carpenter bees and megachilid bees). Bees emerging from cells basad to infested
cells acquire phoretic mites when they pass through those cells. An alternative
strategy requires phoretic mites to leave infested cells and move through nest
burrows or surrounding soil to actively locate other bees, as occurs with Sancas-
sania boharti (Cross and Bohart 1991), Imparipes and Trochometridium. The
strategy of killing brood fails if all cells in a nest are infested, and indeed
infestation rates are low.
While one would expect the bees to be under selective pressure to recognize
and remove these mites, no such behavior has been observed in solitary bees.
However, halictid bees (including Nomia) pack cells containing brood killed by
fungus or mites with soil, perhaps isolating them from viable cells in the nest
(Cross and Eickwort, unpub!').
Cleptoparasitism also occurs among mites with different evolutionary back-
grounds than saprophagy. Pollen and nectar-feeding mites that develop in flowers
frequently use bees as phoretic hosts, and these mites can also act as cleptopara-
sites if they leave their phoretic hosts in nests instead of on flowers. This is most
common in the nests of social apids, in which the provisions are stored separate
from the brood, and Neocypholaelaps (and related genera) and Carpoglyphus in
particular can develop huge populations in honey bee and stingless bee nests.
A third route to cleptoparasitism is through predation. Lineages of predatory
Mesostigmata have produced genera (Laelaspoides, M elittiphis, Parasitellus,
and Pneumolaelaps) whose species are at least partially cleptoparasitic. These
mites feed on provisions without harming the brood of their bumble bee hosts,
and they occur in most nests of bumble bees.
In contrast to the situation with most other social insects, in which cleptoparasi-
tism by mites is uncommon (Eickwort 1990), bee-associated mites commonly
practice cleptoparasitism (facultative or obligatory), which occurs in 21 % of the
genera in Tables 9.1-9.3. This probably occurs because bees store high-quality
protein and carbohydrate (pollen and honey) for relatively long periods in nests,
in contrast to the progressive provisioning without long-term storage characteristic
of ants, termites, and social wasps.
Predators of other associates in bee nests comprise 23% of the mite genera in
Tables 9.1-9.3. These mites are disproportionately represented in nests of social
apids, where they typically occur outside of the brood cells. The exception is in
the nests of large carpenter bees, where Cheletophyes are obligate associates.
The absence of obligatorily associated predators with other solitary bee taxa
is surprising, given the reliable occurrence of Astigmata, Heterostigmata, and
nematodes in their nests.
True parasites of adult or immature bees (feeding directly on their hosts) are
few among the mites, represented by only 6% of the genera in Tables 9.1-9.3.
These are all associates of social apids. Parasitism of larvae, followed by phoresy
on other adult bees which develop in the nest, occurs in Varroa, Euvarroa and
Tropilaelaps, associated with honey bees. Why this strategy has not evolved
among mites associated with stingless bees or the numerous other bee lineages
which do not care for their brood after oviposition is difficult to understand.
Parasitism of adult bees occurs in bumble bees (with Locustacarus) and honey
bees (with Acarapis). This strategy requires that adult bees of two generations
frequently interact (so mites can transfer from generation to generation), and this
excludes most solitary bees as potential hosts. It does not exclude the Xylocopi-
nae, Euglossinae, and Meliponinae, and it is surprising that ectoparasitic mites
have not been found on those bees.
There should be strong selective pressure for bees to evolve means of detecting
and eliminating both brood and adult parasites. This, coupled with the major
evolutionary steps necessary to transform a saprophagous or predatory mite into
a parasite, may account for the rarity of this strategy.
4.2 Mutualism
The majority of mites are commensalistic with their host bees. Their activities in
gathering nutrients from nests as saprophages or predators have neither a benefi-
cial nor a harmful effect on the bees, and even those mites that steal pollen and
honey may not remove enough nutrients to adversely affect the development of
the brood. Consequently, I hypothesize that bees have undergone little or no
selection to modify their behavior, physiology, morphology, or development in
response to the presence of most mites. In contrast, the mites have undergone
considerable selection to modify the timing of their development, the abilities of
the various instars to locate appropriate nutrients and phoretic hosts, and to grasp
onto (and possibly transfer between) phoretic hosts. One result of this selection
is that most lineages of mites are adapted for survival on only one, or a few
ecologically similar, lineages of hosts despite the general similarity of nutrients
available in most bee nests.
Mutualism, in which the bees benefit from the presence of mites, can be
expected to occur when the predatory activities of mites significantly reduce the
population levels of other harmful animals in the nests or when their saprophagous
activities reduce the level of infestation of fungi or bacteria on provisions or brood.
One suspected case of mutualism involving predators concerns Parasitellus with
Bombus (Schousboe 1987); queen bumble bees carrying mites have low levels of
parasitic nematodes. The presence of specialized thoracic acarinaria containing
Cheletophyes in Old World carpenter bees also implies mutualism, as these
predatory mites consume astigmatid mites that kill brood of their hosts (OConnor
1993). Mutualism should also be investigated for N eohypoaspis and other laelapid
genera associated with stingless bees.
In contrast, there is strong circumstantial evidence for mutualism between
several lineages of saprophagous mites and their hosts. Anoetus have been hypoth-
esized to be mutualistic with halictine bees, removing bacteria from the provisions
and brood cuticle (Eickwort 1979). Ctenocolletacarus may prevent contamination
by microbes that infest feces and uneaten pollen. The mites appear to ingest
pollen grains that adhere to bee larvae and to convert the pasty feces to a firmer,
drier state (Houston 1987). Dinogamasus feed on the surfaces of carpenter bee
brood (Madel 1975) and may ingest microbes, while Proctotydeus therapeutikos
deters fungus infestation in stingless bee nests (Flechtmann and Carmargo 1979).
Despite the appeal of truly mutualistic interactions, there have been no studies
that have actually demonstrated a quantifiable benefit (in terms of increased
reproduction or decreased mortality) to a bee from a mite's presence. Mutualism
implies that the hosts also have undergone selection to encourage the presence of
mites, and the strongest evidence for mutualism is the presence of specialized
regions of the female bee's body (acarinaria) for transporting phoretic instars.
Acarinaria occur in those Xylocopa, Ctenocolletes, Lasioglossum, and Thecto-
chlora which are associated with mites, but they are absent in species of Xylocopa,
Ctenocolletes, and Lasioglossum which do not consistently carry mites.
4.3 Phoresy and Developmental Synchronization
As is the case with social insects (Eickwort 1990), phoresy is the principal
adaptation required of a mite in order to become an important associate of bees.
Bee nests are widely scattered in the environment, and the nutritional resources
within them are largely enclosed in cells that are protected by linings from the
surrounding substrate. Nests may provide resources for soil-dwelling or arboreal
mites that facultatively encounter them, but reliable location of these resources
requires that a mite be phoretic on a bee which leaves one nest to initiate another.
All obligatory solitary bee associates reproduce within closed cells, and they have
specific ins tars which are adapted to attach onto adult bees that emerge from the
same cells, or from other cells in the same nest.
The phoretic instar must possess the sensory capability to identify an adult bee,
and the mechanical ability to climb onto and "fly" with the bee while it locates
and builds a new nest and forages for provisions. Female bees also possess
excellent grooming abilities which the phoretic mites must be able to resist or
avoid. Finally the phoretic instar must also possess the sensory capability to
identify a newly provisioned cell and be able to disembark and locate the appro-
priate place where food is or will be available within the cell.
The developments of solitary bees and their obligatory associates are closely
synchronized. Mite feeding and reproduction take place in the cell when specific
nutrients are available, and a single generation of mites is produced in all cases
where the bee brood is not killed. The obligate phoretic instar is produced during
the late larval or pupal stadium of the bee, and it remains in the cell until the
pupa molts into an adult. In cases in which the host is a univoltine bee, only a
single generation of mites is produced in a year, despite the fact that related mites
may pass through a generation in a matter of weeks. The phoretic instar is the
most resistant stage to adverse environmental conditions and starvation, and is
the stage which survives the winter (or other inactive periods).
A v~ant is seen in those mites that develop as saprophages or cleptoparasites
in cells in which the bee brood has died. In such cells the mites typically produce
several generations without the interspersing of an obligatorily phoretic ins tar.
The phoretic instar is produced when the food is consumed or otherwise deterio-
rates, and the timing of this event must coincide with the availability of phoretic
hosts that emerge from other cells.
The phoretic instar either firmly grasps host setae with its pretarsal claws or
chelicerae (Mesostigmata, Heterostigmata, Chaetodactylidae) or it adheres to the
cuticle with suckers (Astigmata). Phoretic mites are not randomly distributed on
the bee. They are highly localized in places that are not groomed, such as ventrally
(on the postgenae of the head, between the coxae, on the metasomal sterna), at
the junction of the head and thorax (occiput, pronotum), at the junction of the
thorax and metasoma (above the leg bases on the propodeum, anterior surface of
metasomal tergum I), in the intersegmental spaces between the metasomal sterna
and terga, in the genital chamber, on the thorax by the wing bases, and on the
surfaces of the wings. Observations of pupal bees indicate that the mites actively
seek out these locations, rather than simply being groomed from other sites on
the body.
Moreover, different mite species attach to different locations on the same host.
On Xylocopa, for example, Sennertia prefers the head-thorax, thorax-metasoma,
and wing base sites, while Horstia prefers the metasomal sterna and genital
chamber (Abrahamovich and Alzuet 1989). On Nomia, lmparipes prefers the
thorax by the wing bases, Glyphanoetus prefers the wing surfaces and (on male
hosts) posterior metasomal sterna, and Sancassania prefers the intersegmental
spaces between the metasomal terga and sterna (Cross and Bohart 1969). In
contrast, Trochometridium, a nonspecific associate of bees, attaches more or less
at random on its phoretic hosts (Cross and Bohart 1969, Eickwort unpubl.).
Male bees do not enter nest cells and are thus less effective vectors of mites
to new reproductive sites. All studies that have examined the question of whether
phoretic instars avoid cells in which male eggs are laid have determined that the
mites do not discriminate between the sexes, and that the mites develop success-
fully in cells that contain hosts of both sexes. A few studies (Cross and Bohart
1969, Madel 1975, Richards and Richards 1976) have indicated that the phoretic
instars either attach less often to the emerging male bees or that they later leave
the males in order to seek female bees which emerged from other cells in the
nest. For instance, only 20% of recently emerged male Nomia melanderi carried
phoretic lmparipes apicola in contrast to 87% of females, although mites were
actually more frequent on overwintering male larvae than on females (Cross and
Bohart 1969). However, phoretic instars often do attach to both sexes, and it is
typical that the mites attach to the venter (especially the metasomal sterna) or in
the genital chamber of the male hosts (Cross and Bohart 1969, OConnor and
Eickwort 1988, Eickwort unpubl.). These are the appropriate locations for mites
to quickly move to a female bee when copulation occurs. Although such venereal
transfer has been documented in Kennethiella trisetosa (Winterschmidtiidae) on
the solitary vespid wasp Ancistrocerus antilope (Cowan 1984), it has not yet been
verified in bees. There is no parallel among bee mites for the situation with K.
trisetosa, which successfully develop only in cells containing male wasp larvae.
Social bees pose a different situation because, by definition, more than one
brood of bees develops within a nest. Social sweat bees do not promote any
different developmental strategies of their mite associates than occur in nests of
solitary sweat bees. Bumble bee nests, although typically annual, have food
available outside of brood cells, and mites such as Parasitellus and Pneumolae-
laps can pass through several generations per year. At the end of the season, it
is necessary for phoretic instars to be produced and that they locate the overwinter-
ing new queens. This evidently occurs with Pneumolaelaps, Parasitellus and
Scutacarus, whose phoretic ins tars occur in greater numbers on overwintering
queens than on workers and males (Hunter and Husband 1973; Richards and
Richards 1976; Schousboe 1986, 1987).
The highly social honey bees and stingless bees present an unusual condition
for developmental synchronization of mites. On the one hand, these bees have
perennial colonies, in which mites can reproduce for many generations without
having to intersperse a phoretic instar. On the other hand, these mites require that
the phoretic instars attach to the single queen which accompanies a swarm to a
new nest site (or to those workers which form the swarm). It is quite striking that
the only mites that are commonly phoretic on honey bees are the true parasites;
the numerous saprophagous Astigmata in honey bee colonies are facultative and
do not invade on the bodies of the bees themselves (Eickwort 1988).
Stingless bee workers are also almost completely free of phoretic mites, despite
the very diverse and abundant mite fauna in their colonies. This fauna is largely
composed of genera that appear to be obligatory associates and that would be
expected to have phoretic ins tars . How these mites move from nest to nest remains
a mystery; however, nest-founding swarms and their accompanying queens have
not yet been examined for mites. Stingless bees gradually prepare a new nest and
move into it, in contrast to the abrupt swarming that characterizes nest founding
in honey bees. Perhaps mites associated with stingless bees are moved to new
nests with materials that are carried by the workers.
5. Evolutionary and Phylogenetic Considerations
5.1 Evolutionary Implications of Phoresy
With few exceptions, mites in a solitary bee nest trace their ancestry to the
phoretic instars that were carried on the female bee which constructed the nest.
By itself, this should lead to extreme inbreeding, as female mites would have
only their brothers and first cousins available as mates. Local mate selection
should be extreme, and in haplo-diploid lineages (which include most of the bee
mites) this should lead to a highly biased female:male sex ratio (Hamilton 1967,
Klompen et a\. 1987). Unfortunately, sex ratios have never been accurately
determined for mites associated with solitary bees, but my informal observations
indicate that the sex ratio is indeed female-biased, culminating in the scarce
appearance of tiny Anoetus males and the complete absence of Dinogamasus
males. The sex ratio is also highly female-biased in Kennethiella trisetosa,
associated with a solitary vespid wasp (Cowan 1984; see Klompen et a\. 1987).
However, the above model of extreme inbreeding is not completely valid.
Mites have mechanisms which enable host switching, and these same mechanisms
permit mites with different parents to meet within individual nest cells. This
results in occasional competition among nonrelated male mites for insemination
of females (Cowan 1984).
Con specific mites with different parents will meet when phoretic mites move
from a male bee to a female bee when their respective hosts copulate. The same
type of transfer may occur if a female bee carrying mites attempts to enter another
bee's nest in order to steal provisions or when usurpation is attempted. Similarly,
a mite-carrying bee may reuse a vacated nest that contains mites which developed
in the previous owner's brood cells.
Mites in cells in which socially parasitic or cleptoparasitic bees or other parasitic
insects develop may be phoretic on these insects, as has been observed on
Coelioxys, Nomada, Oreopasites, Psithyrus, Sphecodes bees, and on tiphiid,
chrysidid and mutillid wasps (Richards and Richards 1976; Cross and Bohart
1979; Schousboe 1986, 1987; OConnor and Eickwort 1988; Eickwort unpub!.).
Such parasites may visit many host nests and serve as potent vectors for the
phoretic mites. If mites occasionally leave their phoretic hosts when the latter
visit flowers or nest material sites (Roubik 1987), host transfer will occur if
the mites then attach to other bees that visit the same locations. For instance,
Parasitellus deutonymphs have been collected on flowers visited by bumble bees
(Richards and Richards 1976).
The same mechanisms can account for transfer of mites to new host species.
Bees frequently attempt to usurp nests or reuse vacant nests made by other
species. Cavities in wood and stems are particularly valued nest sites for diverse
lineages of "renting" bees, and usurpation of such cavities is common, readily
allowing transfer of mites among the cavity-dwelling lineages. Bumble bee
queens attempting to steal provisions from honey bee colonies have been hypothe-
sized as the source for typical bumble bee mites in Apis nests (Schousboe 1987).
Social parasites, cleptoparasites and other parasites commonly investigate nests
made by several potential host species. Since male bees may pounce on any
visual stimulus that vaguely resembles a female, even mistaken copulatory at-
tempts could lead to mite transfer.
It is likely, therefore, that mites are readily transferred among diverse bee
lineages. From a mite's viewpoint, it should be adaptive to develop in any nest
which it encounters. The fact that most mite lineages are restricted to related bees
(see next section) implies that adaptations for coexistence with bees requires some
degree of specificity.
5.2 Patterns of Host Specificity
As may be expected among such an evolutionarily diverse group as the bee mites,
there are numerous patterns of host specificity. As noted in the introduction,
determining the level of host specificity for any taxon of mites is not easy
from the available literature. With this caveat, the following generalizations are
apparent concerning the species of mites belonging to the genera listed in Tables
9.1-9.3:
(1) Very few species develop regularly in association with hosts that belong
to more than one subfamily. These include Tortonia quadridens, Im-
paripes apicola, Trochometridium tribulatum, and AJrocypholaelaps
aJricana. The latter species is a flower-feeding mite which is primarily
phoretic on its various hosts.
(2) Relatively few mite species develop in association with only one host
species when other congeneric potential hosts occur in the same habitat.
Well-documented examples of monophagous mites primarily involve
associates of honey bees: Varroa underwoodi and Pseudacarapis in-
doapis on Apis cerana, and Melittiphis alvearius on A. melliJera (De-
lfinado-Baker et al. 1989). I expect that mites currently restricted to
either A. mellifera or A. cerana will eventually occur on the other
species now that these previously allopatric hosts occur in sympatry,
as has happened with Varroa jacobsoni.
(3) The majority of mite species occur in association with many or most
congeneric host species in their ranges, and individual hosts may bear
more than one congeneric species of mite. This is especially apparent
in the well studied Scutacarus, Parasitellus and Pneumolaelaps mites
associated with bumble bees (Hunter and Husband 1973; Richards and
Richards 1976; Schousboe 1986, 1987). Even those mites that appear
to be the most highly specialized for life with their hosts, as evidenced
by the development of host acarinaria, are not entirely host specific.
Species of Ctenocolletacarus, associated with Ctenocolletes (Fain
1984a, Fain and Houston 1986), and Dinogamasus, associated with
Xylocopa (Vitzthum 1930), typically occur on several closely related
host species. It is, however, risky to generalize a pattern for any mite
genus. For example, some species of Imparipes (e.g. I. apicola) are not
specific in their bee hosts while others (e.g. I. ithacensis on Dialictus
rohweri, I. vulgaris on Lasioglossum titusi) may be quite host specific
(Delfinado and Baker 1976).
Equivalent patterns of host specificity exist at the generic level. About 29% of
the genera in Tables 9.1-9.3 contain species that are also known from hosts other
than bees. The flower-dwelling mites (Neocypholaelaps and AJrocypholaelaps,
perhaps Carpoglyphus and Proctolaelaps) are included here because they have
developed only loose relationships with their phoretic hosts, including butterflies,
beetles, and flies. Also included here are those genera of mites (Forcellinia,
Oplitis, Triplogynium, Urodiscella, and Urozercon) which are most frequently
associated with ants, tennites or other insects but also have representative species
in nests of stingless bees or honey bees-the extent to which these species are
obligate associates of bees is unknown (Eickwort 1990). Similarly, species of
Macrocheles occur in various social apid nests, but their closer association might
be with beetles and other insects that are their true phoretic hosts (Richards and
Richards 1987). Many included genera are large, "catch-all" taxa (Histiostoma,
Hypoaspis, Imparipes, Proctotydeus, Sancassania, Scutacarus, and Tarso-
nemus), and further phylogenetic analysis might lead to recognition of the bee-
associated species as comprising monophyletic subunits (subgenera or species
groups). A few well-defined genera, however, are found on diverse host taxa,
suggesting that some mites evolved close associations with bees while their
congeneric relatives did not. Perhaps the most striking example is Locustacarus,
which includes species that are tracheal parasites of both grasshoppers and bumble
bees (Husband and Sinha 1970).
The remaining 71 % of genera listed in Tables 9.1-9.3 contain species that are
all obligatorily associated with bees. This association in addition suggests that
mites in each genus are predominantly found on a single subfamily (or closely
related subfamilies) of bees. Where more than one family of hosts is associated
with a mite genus, the hosts are ecologically similar (e.g. species of Chaetodacty-
Ius, Horstia, Sennertia, and Tortonia are associated with wood-dwelling carpen-
ter bees and megachilid bees). A few apparently incongruous host associations
can be similarly explained; for instance, the record of Vidia undulata phoretic on
Hylaeus could easily be due to the fact that Hylaeus will make its nests in
abandoned megachilid nests (OConnor and Eickwort 1988). I have not included
obviously incongruous records in Tables 9.1-9.3 when they are based solely on
phoretic instars (e.g. Sennertia collected from honey bees; Baker and Delfinado-
Baker 1983). Other incongruous records may be clarified in the future by system-
atic analysis. For instance, "Pneumolaelaps" machadoi, described from an Afri-
can megachilid bee (Elsen 1973), lacks some characters of other Pneumolaelaps,
all of which are associated with bumble bees (Hunter and Husband 1973), and
probably represents a separate derivative from a Hypoaspis-like ancestry.
What has caused some genera of mites to be speciose (e.g. Chaetodactylus,
Dinogamasus, Parasitelius, Pneumolaelaps, and Sennertia) while others contain
just a few, wide-ranging species with numerous hosts (e.g. Locustacarus, Cero-
phagus) remains unanswered. What is evident is that each mite genus has gener-
ally been found to be associated with its host subfamily throughout the world
whenever potential hosts have been adequately sampled (Tables 9.1-9.3). This
is especially true of Vidia and Chaetodactylus (with megachilines), Horstia and
Sennertia (with xylocopines), and Anoetus (with halictines), where the ranges of
both hosts and mites extend to Australia. I conclude that the mite-bee associations
are thus very old, predating the geographic partitioning of the bee lineages and
thus originating probably in the Cretaceous.
5.3 Phylogenetic Implications
The evolution of important mite associates of bees can best be summarized as a

phenomenon with many independent evolutionary origins, and with subsequent
diversification of the mite lineages within major bee lineages. I hypothesize a
minimum of 31 separate origins of important bee mites: Histiostoma, Anoetus,
Sancassania (+ Ctenocolletacarus) , Horstiinae, Tortonia, Gaudiellidae, Vidia,
Meliponocoptidae, Chaetodactylidae, Melissotydeus, Cheletophyes, Trochome-
tridium, Parapygmephorus, Imparipes, Scutacarus, Tarsonemus, Pseudacar-
apis, Acarapis, Locustacarus, Parasitellus, M eliponipachys, Trigonholapsis +
Grafia, Neocypholaelaps, Hypoaspis, Pneumolaelaps + Laelaspoides, Dinoga-
masus, Neohypoaspis + seven related genera, Melittiphis, Tropilaelaps, Varroi-
dae, and Calaenosthanus. Five of the above may have had multiple separate
origins of bee mites within them (Histiostoma, Hypoaspis, Imparipes, Sancas-
sania, Scutacarus) , and I have excluded some genera in which the extent of
adaptation for life in social bee nests is uncertain (Forcellinia, Macrocheles,
Oplitis, Proctolaelaps, Triplogynium, Urozercon, and Urodiscella).
Evolutionary analysis within the mite genera awaits phylogenetic studies of
both the bees and the mites, which have not been undertaken for any pair of
lineages. The literature suggests that evolutionary patterns in those mite genera
that are closely adapted to specific host genera will in part reflect host phylogeny,
although strict cospeciation of mites and hosts has not occurred. For example,
two closely related species of Ctenocolletes share the same two closely related
species of Ctenocolletacarus, while a third species of Ctenocolletacarus occurs
on two other host species (Fain 1984a, Fain and Houston 1986). Most subgenera
and species groups of Sennertia are confined to particular biogeographic regions
(Fain 1981 a), and separate subgenera of H orstia occur in the New and Old Worlds
(Fain 1984b). Separate lineages of Anoetus and Vidia have evolved with different
host lineages (OConnor 1988). Different groups of mites are associated with two
lineages of Apis (Delfinado-Baker et al. 1989).
On a broader scope of bee phylogeny, mite lineages are not well correlated
with host lineages above the subfamily level. Mite genera are either broadly
spread among bees or they are restricted to only specific subfamilies in a given
family of bees. Genera with species that occur in different families of soil-
dwelling bees (Histiostoma, Hypoaspis, Imparipes, Sancassania, Schulzea, and
Scutacarus) are mostly little modified from their non-bee-associated ancestors
and may represent separate invasions in each bee lineage. As an example of
subfamily specialization, the mites (Anoetus and Sicilipes) adapted to Halictinae
do not occur on the Rophitinae, the most primitive subfamily in the Halictidae.
There is almost no concordance of mite lineages (only Chaetodactylus) between
the Anthophorinae and Xylocopinae of the Anthophoridae, or among the Apinae,
Bombinae, and Meliponinae of the Apidae (only Gaudiellidae and Laelapidae).
Similarly, few mites (possibly Horstiinae and Laelapidae) occurring in social
apid nests have a common ancestry with those that occur with solitary bees . .Mite
lineages thus offer little phylogenetic information concerning the relationships of
bee subfamilies and families. The close phylogenetic relationships among the
mites that occur with Megachilidae and Xylocopinae reflect similar nesting habits
of those two bee taxa, not their phylogenetic relationship.
A summary of mite genera presently known from major bee families and
subfamilies is given in Figure 9.3. The Meliponinae are hosts to the greatest
diversity of mite genera, which might be explained in large part by their complex
perennial nests with abundant and diverse food resources. The Apinae also have
complex nests and societies, but the level of diversity of obligate mite associates
is only half that of the Meliponinae. This may in large part be explained by many
fewer species represented in the Apinae, and until recent times their restriction
to the Old World. The facts that only two closely related species (Apis mellifera
and A. cerana) build nests in cavities which provide a habitat for saprophagous
mites and their predators, and that differences in swarming and nest-founding
make phoresy to new nests more difficult, may also contribute to the relative
sparsity of mite associates of Apinae. The Bombinae also exhibit a high diversity
of mites, probably due to the diverse and abundant food resources in their nests,
as well as their wide distribution.
Solitary bee lineages all present basically the same nutritional resources for
mites. One might expect that the lineages have roughly equivalent diversities of
mites associated with them, but that is not the pattern exhibited in Figure 9.3.
Host
(number species)
I/: A5
COLLETIDAE (3000 spp)
"_2
/ A 13
HALICTIDAE (5000 spp)
ANDRENIDAE (4000 spp)
"'14
MEGACHILIDAE. (3000 spp)
/ ... 7
ANTHOPHORINAE (2000 spp)
/ ..AI 11
XYLOCOPINAE (1000 spp)
/ .... 10
BOMBINAE (200 spp)
MELIPONINAE (250 spp)
... 29
/ .... 14
APINAE (8 spp)
o 10 20 30
Number Mite Genera

Figure 9.3. Numbers of genera of mites associated with major families and subfamilies
of bees. Approximate number of species in each bee taxon indicated in parentheses.
Among the soil-nesting bees, the Halictidae (Halictinae and Nomiinae) exhibit
the greatest diversity of mite associates. This may in part be due to my own
concentration of studies on these associations, but mites are simply not so apparent
on and in nests of other soil-dwelling solitary bees (Cross and Bohart 1969). The
fact that many halictines are parasocial or eusocial does not seem to be an adequate
explanation, because the mites are not unique to the social species, and parasocial
(communal) colonies are also frequent among Andrenidae and Anthophorinae.
The second obvious pattern among solitary bee hosts is the greater diversity
of mites associated with the predominantly wood-dwelling and cavity-renting
Xylocopinae and Megachilinae as compared with most soil-nesting bees, includ-
ing the Anthophorinae. Unique taxa of mites have evolved to inhabit the nests of
carpenter and leafcutter bees, such as Chaetodactylus, Cheletophyes, Dinogama-
sus, Sennertia, Vidia, and six acarid genera (Table 9.2), with only three genera
of Astigmata playing an equivalent role with the Anthophorinae. The mites that
inhabit nests of Xylocopinae and Megachilidae (with the exception of a few
species of the ecologically broad-ranging genera Sancassania, Schulzea, and
Hypoaspis) are distinctly separate in their evolutionary origins from those that
occur with all other groups of solitary bees.
Ecology may playa major role in explaining these differences. Neither Xylo-
copinae nor Megachilinae line their cells with impenetrable secreted linings, and
the cells are typically constructed in series, facilitating mite transfer. Xylocopine
bees are long-lived, facilitating transfer of mites between generations. Both
groups typically reuse nest cavities. The frequently arboreal nests are subject to
invasion from arboreal lineages such as the Winterschmidtiidae (OConnor 1988),
and these mites may share ancestry with those associated with arboreal-nesting
solitary wasps. While mites are poorly known from the cavity-renting Hylaeinae,
the few records indicate a closer relationship with mites inhabiting megachilid or
xylocopine nests than those of other Colletidae.
The patterns of diversity of the mites associated with the major bee subfamilies
support the hypothesis that the long-tongued bee families are at least as old
phylogenetic ally as the short-tongued bee families. The mites associated with
solitary long-tongued bees (especially the Megachilidae and Xylocopinae) are
more morphologically distinctive on the average than are those associated with
short-tongued bees, suggesting longer periods of coevolution between bee and
mite lineages. The mites associated with stingless bees and honey bees are among
the most highly modified of all Astigmata and Gamasina, again suggesting early
divergence of these mite lineages from their non-bee-associated ancestors.
6. Conclusions
The majority of mites that have established important relationships with solitary
bees are saprophytes or pollen-honey feeders within their nests. Predatory mites
are only important in social bee nests. There are few true parasites of bee brood
and adults, and these are limited to the highly social bees.
The most important adaptation for a mite to establish an important relationship
with bees is phoresy upon nest-founding female bees. A mite must also modify
its developmental cycle to synchronize with that of its host.
Most mites are commensalistic in bee nests, neither harming nor benefitting
their hosts. Some species may kill brood in order to feed on the provisions or the
microbes that then infest them. Other species may be mutualistic with the bees,
principally by deterring microbes. Evidence for diffuse coevolution between
mites and bees lies principally in the presence of specialized pouches (acarinaria)
on certain female bees for carrying phoretic mites.
Most mite genera are each restricted to one subfamily of bees, or to subfamilies
which are ecologically similar. A minority of mite genera are associated with
unrelated bee families, or with other insects. Mite evolution has not paralleled
bee evolution above the subfamily level. Most mite species are not restricted to
just one species of bee, and there is no evidence for bee-mite cospeciation.
The study of bee mites is truly in its early stages. While there is an increasing
literature on the few mites that are pathogenic to domestic honey bees, most
bee mites are totally neglected biologically. Numerous mite species have been
described, but there has been little effort to analyze them phylogenetic ally . Bee
biologists should be encouraged to observe and preserve the mites that occur
inside cells, especially those containing developing brood. Many exciting bee-
mite associations are awaiting discovery.
Acknowledgments
Dr. Barry OConnor of the University of Michigan has provided many insights
on the Astigmata, Dr. Phil Torchio of the USDA Bee Biology and Systematics
Lab at Utah State University provided information on Chaetodactylus, and Dr.
Earle Cross of the University of Alabama provided unpublished information on
mites associated with alkali bees. Dr. Mercedes Delfinado ofthe USDA Beneficial
Insects Laboratory at Beltsville, Maryland has generously shared her research on
the acarine associates of honey bees and stingless bees. Drs. OConnor, Torchio,
Delfinado, and Cross, and Carol Henderson, Kenna MacKenzie, Ulrich Mueller,
and Janet Shellman-Reeve of Cornell University provided helpful comments on
this manuscript. I thank Dr. Marilyn Houck for the invitation to contribute to this
symposium volume, and for her editorial assistance.
References
Abrahamovich, A. H. and A. D. B. de Alzuet. 1989. Relaciones foreticas entre acaros

(Acaridae y Chaetodactylidae) e himenopteros (Anthophoridae, Xylocopinae). Rev.
Soc. Entomol. Argent. 47:115-122.
Baker, E. W. and M. Delfinado-Baker. 1983. New mites (Sennertia: Chaetodactylidae)

phoretic on honey bees (Apis mellifera L.) in Guatemala. Int. 1. Acarol. 9:117-121.
Baker, E. W., D. W. Roubik and M. Delfinado-Baker. 1987. The developmental stages
and dimorphic males of Chaetodactylus panamensis, n. sp. (Acari: Chaetodactylidae)
associated with solitary bee (Apoidea: Anthophoridae). Int. 1. Acarol. 13:65-73.
Chmielewski, W. 1969. Obserwacje nad biologia nowego dla akarofauny polskiej gatunku
Kuzinia laevis (Dujardin, 1849) (Acarina, Acaridae). Pol. Pismo Entomol. 39:603-617.
Chmielewski, W. 1971. The mites (Acarina) found on bumble-bees (Bombus Latr.) and in
their nests. Ekol. Pol. 19:57-71.
Costa, M. 1966. The biology and development of Hypoaspis (Pneumolaelaps) hyatti
(Acari: Mesostigmata). 1. Zool. 148:191-200.
Cowan, D. P. 1984. Life history and male dimorphism in the mite Kennethiella trisetosa
(Acarina: Winterschmidtiidae), and its symbiotic relationship with the wasp Ancistro-
cerus anti/ope (Hymenoptera: Eumenidae). Ann. Entomol. Soc. Am. 77:725-732.
Cross, E. A. and G. E. Bohart. 1969. Phoretic behavior of four species of alkali bee mites
as influenced by season and host sex. 1. Kans. Entomol. Soc. 42:195-219.
Cross, E. A. and G. E. Bohart. 1979. Some observations of the habits and distribution of
Trochometridium Cross, 1965 (Acarina: Pyemotidae). Acarologia 20:286--293.
Cross, E. A. and G. E. Bohart. 1991. Notes on the life history of Sancassania boharti
(Acari: Acaridae) and its relationship to the alkali bee Nomia melanderi (Hymenoptera:
Halictidae). J. Kans. Entomol. Soc. 63:603-610.
Cross, E. A. and J. C. Moser. 1975. A new, dimorphic species of Pyemotes and a key to
previously-described forms (Acarina: Tarsonemoidea). Ann. Entomol. Soc. Am.
68:723-732.
Delfinado, M. D. and E. W. Baker. 1976. New species ofScutacaridae (Acarina) associated
with insects. Acarologia 18:264-301.
Delfinado-Baker, M., E. W. Baker and A. C. G. Phoon. 1989. Mites (Acari) associated
with bees (Apidae) in Asia, with description of a new species. Am. Bee 1. 129:609-
610, and 612-613.
Delfinado-Baker, M., E. W. Baker and D. W. Roubik. 1983. A new genus and species
of Hypoaspidinae (Acari: Laelapidae) from nests of stingless bees. Int. 1. Acarol. 9:195-
203.
Eickwort, G. C. 1979. Mites associated with sweat bees (Halictidae). In: Recent Advances
in Acarology, Vol. 1 (J. G. Rodriguez ed.). Academic Press, NY. Pp. 575-581.
Eickwort, G. C. 1988. The origins of mites associated with honey bees. In: Nricanized
C. Bowman eds.). Ellis-Horwood, Ltd., Chichester, England. Pp. 327-338.
Eickwort, G. C. 1990. Associations of mites with social insects. Annu. Rev. Entomol.
35:469-488.
Elsen, P. 1973. Pneumolaelaps machadoi spec. nov. (Acarina: Mesostigmata) et autres
acariens mesostigmatiques phoretiques d'Hymenopteres Apidae (Insecta) d' Angola.
Publ. Cult. Cia. Diamantes Angola 87:179-186.
Fain, A. 1966. Notes sur la biologie des Acariens du genre Chaetodactylus et en particulier
de C. osmiae, parasite des abeilles solitaires Osmia rufa et O. cornuta en Belgique
(Sarcoptiformes: Chaetodactylidae). Bull. Ann. Soc. R. Beige Entomol. \02:249-261.
Fain, A. 1981a. A revision of the phoretic deutonymphs (hypopi) of the genus Sennertia
Oudemans, 1905 (Acari, Astigmata, Chaetodactylidae). Syst. Parasitol. 3:145-183.
Fain, A. 1981b. Notes on the hypopi of the genus Chaetodactylus Rondani, 1866 (Acari,
Chaetodactylidae). Bull. Inst. R. Sci. Nat. Belg. Entomol. 53:1-9.
Fain, A. 1984a. A new genus of mite (Acari: Acaridae) phoretic on bees (Ctenocolletes)
in Australia. Rec. W. Aust. Mus. 11:77-86.
Fain, A. 1984b. Notes sur les hypopes du genre Horstia Oudemans, 1905 (Acari, Acaridae),
phoretiques sur Ies Hymenopteres. Acarologia 25:259-270.
Fain, A. and W. Chmielewski. 1987. Horstia (Horstia) longa spec. nov. (Acari, Acaridae)
from house-dust in Poland. Pol. Pismo Entomol. 57:367-372.
Fain, A. and T. F. Houston. 1986. Life cycle stages of mites ofthe genus Ctenocolletacarus
Fain (Acari: Acaridae) associated with Ctenocolletes bees in Australia. Rec. West. Aust.
Mus. 13:67-77.
Fain, A., F. S. Lukoschus and M. Nadchatram. 1980. Two new species of Cheletophyes
Oudemans, 1914 (Prostigmata: Cheyletidae) from the nest of a carpenter bee in Malaysia.
Int. J. Acarol. 6:309-312.
Fain, A. and G. Rack. 1987. Notes on the mites living in the flowers of Espletia spp.
(Asteraceae) in Colombia. I. Carpoglyphus sturmi sp. n. (Acari, Carpoglyphidae).
Entomol. Mitt. Zool. Mus. Hamb. 9:9-19.
Fain, A. and A. E. Rosa. 1983. Acari domum meliponinarum brasiliensium habitantes.
IV. New astigmatic mites from the nest of the bee Partamona sp. (Meliponidae). Bull.
Inst. R. Sci. Nat. Belg. 55:1-13.
Flechtmann, C. H. W. and C. A. de Camargo. 1979. Acari associated with stingless bees
(Meliponidae, Hymenoptera) from Brazil. In: Proc. 4th Int. Congr. Acarol., (E. Piffi
ed.), Saalfelden, 1974. Akademiai Kiad6, Budapest. Pp. 315-319.
Gibbins, B. L. and R. F. van Toor. 1990. Investigation of the parasitic status of Melittiphis
alvearius (Berlese) on honeybees, Apis mellifera L., by immunoassay. J. Apic. Res.
29:46--52.
Haeseler, V. 1982. Solitare Wespen und Bienen als Transporteure der Wandemymphen
von Uropodiden. Mikrokosmos 8:227-229.
Houston, T. F. 1987. The symbiosis of acarid mites, genus Ctenocolletacarus (Acarina:
Acariformes), and stenotritid bees, genus Ctenocolletes (Insecta: Hymenoptera). Aust.
J. Zool. 35:459-468.
Hunter, P. E. and R. W. Husband. 1973. Pneumolaelaps (Acarina: Laelapidae) mites from
North America and Greenland. Fla. Entomol. 56:77-91.
Husband, R. W. and R. N. Sinha. 1970. A revision of the genus Locustacarus with a key
to genera of the family Podapolipidae (Acarina). Ann. Entomol. Soc. Am. 63:1152-
1162.
Klompen, J. S. H., F. S. Lukoschus and B. M. OConnor. 1987. Ontogeny, life history

and sex ratio evolution in Ensliniella kostylevi (Acari: Winterschmidtiidae). J. Zool.
213:591-607.
Krantz, G. W. 1962. A review of the genera of the family Macrochelidae Vitzthum 1930
(Acarina: Mesostigmata). Acarologia 4: 143-173.
Krombein, K. V. 1962a. Biological notes on acarid mites associated with solitary wood-
nesting wasps and bees. Proc. Entomol. Soc. Wash. 64:11-19.
Krombein, K. V. 1962b. Natural history of Plummers Island, Maryland XVI. Biological
notes on Chaetodactylus krambeini Baker, a parasitic mite of the megachilid bee, Osmia
(Osmia) ligna ria Say (Acarina: Chaetodactylidae). Proc. Bioi. Soc. Wash. 75:237-249.
Le Veque, N. 1930. Symbiotic mites used to separate species of a genus of bees. Science
71:607-608.
Lindquist, E. E. 1985. Discovery of sporothecae in adult female Trochometridium Cross,
with notes on analogous structures in Siteroptes Amerling (Acari: Heterostigmata). Exp.
Appl. Acaral. 1:73-85.
Lindquist, E. E. 1986. The world genera of Tarsonemidae (Acari: Heterostigmata): A
morphological, phylogenetic, and systematic revision, with a reclassification of family-
group taxa in the Heterostigmata. Mem. Entomol. Soc. Can. 136:1-517.
Lombert, H. A. P. M., B. M. OConnor, F. S. Lukoschus and J. O. Whitaker, Jr. 1987.
Ontogeny, systematics and ecology of Sennertia (Amsennertia) americana Delfinado
and Baker, 1976 (Acari: Chaetodactylidae) from the nest of the carpenter bee, Xylocopa
virginica (Hymenoptera: Anthophoridae). Int. J. Acarol. 13:113-129.
Madel, G. 1975. Vergesellschaftung der Milbenart Dinogamasus villosior mit der ostafri-
kanischen HolzbieneXylocopajlavoruJa (Acarina: Laelaptidae/Hymenoptera: Xylocopi-
dae). Entomol. Ger. 1:144-150.
Maeta, Y. 1978. Comparative studies on the biology of the bees of the genus Osmia of
Japan, with special reference to their managements for pollinations of crops (Hymenop-
tera: Megachilidae). Bull. Tohoku Nat. Agric. Exp. Stn. (Morioka) 57:1-221.
Magowski, W. 1986. Two new species of Tarsonemus (Acari: Prostigmata) associated
with Xylocopa carpenter bees (Hymenoptera: Apoidea). Entomol. Mitt. Zool. Mus.
Hamb. 8:289-306.
Mahunka, S. 1974. Beitrage zur Kenntnis der an Hymenopteren lebenden Milben (Acari)
II. Folia Entomol. Hung. 27:99-108.
Michener, C. D. 1979. Biogeography of the bees. Ann. Mo. Bot. Gard. 66:277-347.
27:385-409.
OConnor, B. M. 1988. Coevolution in astigmatid mite-bee associations. In: AJricanized
C. Bowman eds.). Ellis-Horwood, Ltd. Chichester, England. Pp. 339-346.
OConnor, B. M. 1992a. Ontogeny and systematics of the genus Ceraphagus, mites
associated with bumblebees (Acari: Gaudiellidae). Great Lakes Entomol. 25:173-189.
Evolution and Life-History Patterns of Mites Associated with Bees / 25i
OConnor, B. M. 1992b. Generic relationships in the Chaetodactylidae (Acari: Astigmata)

with description of a new genus (submitted for publication).
OConnor, B. M. 1993. The mite community associated with Xylocopa latipes (Hymenop-
tera: Anthophoridae: Xylocopinae) with description of a new type of acarinarium. into
1. Acarol., Vol. 19 (in press).
OConnor, B. M. and G. C. Eickwort. 1988. Morphology, ontogeny, biology and systemat-
ics of the genus Vidia (Acari: Winterschmidtiidae). Acarologia 29:147-174.
Putatunda, B. N. and R. P. Kapil. 1988. Seven new species of Cheletophyes (Acari:
Prostigmata: Cheyletidae) associated with carpenter bees in India. In: Progress in
Acarology, Volume I (G. P. Channabasavanna and C. A. Viraktamath eds.). Oxford
and IBH Publ. Co. Pvt. Ltd., New Delhi. Pp. 317-328.
Rack, G. and G. C. Eickwort. 1980. Biology and description of a new pygmephorid mite
(Acarina: Tarsonemida) associated with the soil-nesting bee Agapostemon nasutus
(Hymenoptera: Halictidae). Acarologia 21:267-278.
Richards, K. W. and L. A. Richards. 1977. A new species of Macrocheles (Acarina:
Macrochelidae) found in bumble bee nests (Hymenoptera: Apidae). Can. Entomol.
109:711-719.
Richards, L. A. and K. W. Richards. 1976. Parasitid mites associated with bumblebees
in Alberta, Canada (Acarina: Parasitidae; Hymenoptera: Apidae). II. Biology. Univ.
Kans. Sci. Bull. 51:1-18.
Roubik, D. W. 1987. Notes on the biology of anthophorid bee Tetrapedia and the mite
Chaetodactylus panamensis Baker, Roubik and Delfinado-Baker (Acari: Chaetodactyli-
dae). into 1. Acarol. 13:75-76.
Royce, L. A. and G. W. Krantz. 1989. Observations on pollen processing by Pneumolae-
laps longanalis (Acari: Laelapidae), a mite associate of bumblebees. Exp. Appl. Acarol.
7:161-165.
Schousboe, C. 1986. On the biology of Scutacarus acarorum Goeze (Acarina: Trombidi-
formes). Acarologia 27:151-158.
Schousboe, C. 1987. Deutonymphs of Parasitellus phoretic on Danish bumblebees (Paras it-
idae, Mesostigmata; Apidae, Hymenoptera). Acarologia 28:37-41.
Skaife, S. H. 1952. The yellow-banded carpenter bee, Mesotrichia caffra Linn, and its
symbiotic mite, Dinogamasus braunsi Vitzthum. 1. Entomol. Soc. South. Afr. 15:63-
76.
Smiley, R. L. and J. O. Whitaker, Jr. 1981. Studies on the idiosomal and leg chaetotaxy
of the Cheyletidae (Acari) with descriptions of a new genus and four new species. int.
1. Acarol. 7: 109-127.
Southcott, R. V. 1989. A larval mite (Acarina: Erythraeidae) parasitizing the European
honey bee in Guatemala. Acarologia 30:123-129.
Vitzthum, H. 1930. Acarologische Beobachtungen (14. Reihe). Zool. lahrb. Syst. Oekol.
Geogr. Tiere 59:281-350.
Watmough, R. H. 1974. Biology and behaviour of carpenter bees in southern Africa. 1.
Entomol. Soc. South. Afr. 37:261-281.
10
Adaptation and Transition into Parasitism from

Commensalism: A Phoretic Model
Marilyn A. Houck
CONTENTS
I. INTRODUCTION
2. PHORESY IN THE ASTIGMATA
2.1 What is Phoresy?
2.2 Morphological Adaptations of Phoretic Mites
2.3 Ecological and Evolutionary Consequences
2.4 Which Developmental Stage is Phoretic?
3. NATURAL STABILIZING SELECTION OF A PARTICULAR DEMO-
GRAPHIC STAGE FOR PHORESY
3.1 Differential Benefits of Phoresy Examined by Age Class
3.2 Relative Survivorship and Mortality Examined by Age Class
3.3 Shifting Selection Pressures at Two Ends of the Survivorship Curve
3.4 The Meaning of a U-shaped Mortality Curve
3.5 Risks of Dispersal Assessed by Age Class
3.6 Further Selection for Dispersal Characteristics in the Hypopus
4. EVOLUTION AND TRANSITION INTO PARASITISM
4.1 Hemisarcoptes as an Example of Potential Evolutionary Transition
4.2 Evidence for "Something Other than Phoresy" in Hemisarcoptes
cooremani
4.2.1 Interruption of Ontogenesis
4.2.2 Contribution to Mite Nutrition
4.2.3 Hemisarcoptes Has Adapted to Chi/ocorus Refiexed Hemo-
lymph
4.2.4 Hemisarcoptes Acquires Materials from Chi/ocorus
4.3 Hypothesis for the Evolution of Parasitism from Phoresy
5. FUTURE WORK AND PROSPECTUS
1. Introduction
A parasite is "any organism that grows, feeds and is sheltered on or in a different

organism while contributing nothing to the survival of its host" (The American
252
Adaptation and Transition into Parasitism from Commensalism / 253
Heritage Dictionary of the English Language). The etymology of the word has
its origin in the Greek word parasitos, "fellow guest." Parasitism is an important
ecological and evolutionary role assumed by a variety of animals, and it has been
suggested that parasitic insects comprise as many as half of all animals living on
earth today (Price 1980). While a comparable projection is not yet available for
mites, it is clear that the Acari have been particularly prominent in the exploitation
of this mode of existence, both as ectoparasites and (to a lesser extent) as
endoparasites (e.g. Pneumocoptes = lung parasites of the rodents Peromyscus,
Onychomys, and Cynomys; Baker 1951).
Vertebrates (especially birds and mammals, but not fish), are commonly the
focus of acarine parasitization. A major exploitation of birds has occurred world-
wide in all habitats. Feather mites are obligatory ectoparasites of all major groups
of birds except penguins (Peterson 1975) and are thought to have evolved from
nidicolous ancestors. Man has not escaped parasitism by mites either and is host
to many medically important species of Acari (e.g. chiggers [Trombiculidae]
which transmit tsutsugamushi fever [Wharton 1946]; and Liponyssus bacoti, the
agent of endemic human typhus [Ewing 1933]). Sarcoptes scabiei (the sarcoptic
mange mite), which infests the skin of domesticated animals (camels, cattle,
dogs, goats, horses, rabbits, and sheep) is thought to have originated as an
ectoparasite of man (Fain 1968). Husbandry and domestication practices have
led to secondary infestation of animals in cohabitation with man; perhaps only
the house cat has escaped this common fate (Fain 1968).
Interest in the origin of parasitism, per se, is not specific to acarology, but
crosses all disciplinary boundaries. The generalities concerning parasitism come
from many research areas. The evolution of parasitism is a process which is
constrained by four unifying principles: (1) potential hosts protect themselves
from exploitation using morphological, physiological, and behavioral defenses,
while potential parasites must counterrespond to host defenses in order to success-
fully continue the relationship (Ehrlich and Raven 1964, Feeny 1976, Berenbaum
1983); (2) subsequent acceleration of attack and counterattack results in parasites
and their hosts becoming coevolved (Kim 1985a); (3) the process of attack and
counterattack occurs over evolutionary time (Holmes 1973); and (4) commensal-
ism or mutualism may act to initiate the processes leading to parasitism (Price
1980). This last point is significant because it implicitly endorses the concept of
a free-living ancestor representing the primitive node in all parasitic clades, with
commensalism or mutualism being more advanced states of interaction, and
parasitism most highly derived. The feather mites mentioned above are thought
to have evolved in such a way, originating from nidicolous free-living ancestors
(Peterson 1975).
A number of paradigms have been developed to explain or define host-parasite
coevolution (e.g. Ewing 1912, Fain 1969, Fain 1971, Kethley and Johnston
1975, Brooks 1979, Waage 1979, Price 1980, Timm 1983, Kim 1985b, Houck
1992), but experimental evidence regarding the mechanisms and processes in-
254 / M. A. Houck
volved in the evolution of parasitism from commensalism is difficult to obtain.

A deterrent to the understanding of the evolution of parasitism within a particular
monophyletic clade is that all grades of interactions (free-living forms, commen-
sals, and parasites) must be available for study. Astigmatid mites (Acari: Astig-
mata) represent such a monophyletic clade and offer a unique opportunity for the
investigation of the evolution of parasitism from a particularly interesting form
of commensalism called phoresy. This chapter offers some insights and proposed
mechanisms into the channels responsible for such a phoretic transition in one
astigmatic mite, Hemisarcoptes corremani (Hemisarcoptidae).
2. Phoresy in the Astigmata

2.1 What is Phoresy?
Phoresy has been defined, for the Astigmata, as "a phenomenon in which one
organism (the phoretic) receives an ecological or evolutionary advantage by
migrating from the natal habitat while superficially attached to a selected interspe-
cific host for some portion of the individual phoretic's lifetime. Benefit is not
conferred as a nutritional or developmental influence on the phoretic stage"
(Houck and OConnor 1991). While the concept of phoresy is susceptible to
oversimplification (e.g. "commensalism with the implication of dispersal"), this
definition in its entirety has the advantage of explicitly addressing the conse-
quences of phoresy at two temporal levels: (1) in terms of increased survival and
fitness, via ecological interactions (proximate level); and (2) in terms of potential
for speciation and major shifts in niche exploitation, across evolutionary time
(ultimate level).
Functionally, this definition offers testable criteria to distinguish phoresy as a
distinct phenomenon, separate from all other interspecific interactions or dispersal
mechanisms: (1) the host is selected (not randomly elected), with potential ramifi-
cations for coevolution to follow; (2) neither the phoretic nor the host receive
benefit from the relationship other than passive dispersal; if benefit accrues (e.g.
nutrition or enhanced development) then some other form of relationship is
suspect (e.g. parasitism or mutualism); (3) it introduces the concept that phoresy
may have significant evolutionary benefits, not uncovered by studying ecological
interactions alone. The qualifications of nutritional status and developmental
participation, first considered by Farish and Axtell (1971), are very important
and allow for null and testable hypotheses to become confirmational in defining
phoretic associations. If a given interaction contributes to the nutrition or ontogen-
esis of the phoretic, the relationship is something other than phoresy, and needs
further clarification.
2.2 Morphological Adaptations of Phoretic Mites
Phoresy is a prevalent form of commensalism among animals and one of the least
understood of the potential ecological interactions. The most spectacular radiation
of phoretic associations occurs in the Acari (mites). The Astigmata, in particular,

are masters of phoretic association and have taken the concept to the extreme.
There are substantial differences in the effectiveness of phoresy among species
of astigmatic mites depending upon variation in: (1) the extent and morphological
development of attachment organs; (2) the specificity and predictability of hosts;
and (3) the environmental durability of the phoretic stage.
The degree of morphological specialization of the phoretic stage in mites can
be classified into three general types: unspecialized homeomorphs, specialized
homeomorphs, and heteromorphs (for a review see Houck and OConnor 1991).
Heteromorphs are morphologically very different from all other stages of their
life cycle. They have been categorized according to their functional morphology
and mode of attachment (Zachvatkin 1941, Fain 1968, Fain 1969, Volgin 1971).
The most common is the entomophilous ("insect loving") heteromorph, which is
very different in morphology from the general body plan of the species (Fig.
1O.1A, B, C).
The entomophilous Astigmata are characterized by a dispersal stage which is
exemplified by a suite of correlated characters (Stolpe 1938, Hughes and Hughes
1939, Oboussier 1939, Perron 1954, Ttirk and Ttirk 1957, Hughes 1959, Wallace
1960, Evans et al. 1961, Kuo and Nesbitt 1971, Woodring and Carter 1974,
Hughes 1976, Krantz 1978, Binns 1982, OConnor 1982) including: (1) a rudimen-
tary gnathosoma (Fig. 10.1 B); (2) a solid nonfunctional gut; (3) extensive dorsal
and ventral sclerotization to withstand long periods of environmental stress while
in transit; and (4) an extensive caudoventral sucker plate for attachment to
arthropods. An organism with such a heteromorphic suite of morphological
characteristics is frequently referred to as a hypopus.
While the typical hypopus is as described above, variations on the phoretic
theme have occurred in the Astigmata. A modification expressed by some glycy-
phagids includes passive aerial distribution by an atypical nonphoretic hypopus
which is highly regressed from the ancestral hypopal morphology (Kntille 1959,
Fain and Philips 1981, Barker 1982, Kntille 1987). This morph is essentially a
"mite seed," which lies dormant within a protective modified protonymphal
exuvium. It can withstand months of pernicious environmental challenges that are
lethal to all other stages. Lepidoglyphus destructor, for example, can withstand
pesticide fumigation used commercially to control stored-product pests (Barker
1982).
2.3 Ecological and Evolutionary Consequences
Partly because of their small body size, the Astigmata have become champions
of phoretic associations. Ecologically, phoresy helps overcome the liability of
small size in long-distance migration, the lack of morphological attributes for
migration (e.g. wings), the absence of diapause (in most Astigmata), and the
threat of predation during migration. It is a means oflocating ephemeral resources
256 I M.
A. Houck
F ig '"
(A
")
,n thO _
10.1. Tw
,tag'"
h i e " "o,, " in
thOt" " " u o ,, " . . ththoo\i" " d " ,, " ,, '" of H'''''''''oP'''
fc e y d
p b " , , , , , d o n n patIC'" d i" " ro •. No'" ThO \if. eyde '00""""; whi,
l_
, i _ . Latcm m c d in Ch of H. ,oO" b '•.
1 ",I<' 7 (Fig m""; fo"n,pow
on D i" p id
i" '" bArroW ,iow of on ,dUlt f.mol. . 7.4)· A ) s
_ing ""n '
' (oblig'" p<
mag " '' ' of thO (ndi,,1< tho "",ilion of cdat0<y ",g on
e
ct of tM go e do,,", " ,I < " o m '" ," l, whicb f " " "
nifte
e h e li " o te a l "pc th
" '' '' '' B) Sc ath",om" ." "
bYpopU') in ""
_ , 1 ",ipooge d " " " " pbOtom ,d fn< fcolin ,rt, '" . .,,,,k,.cd
of tM .yo> t. A i,
- in ru " '' '' ' ,,,g ,,,,b. hC o g ; " " 'w , roM
mocpbOlogicin thi, ,tAg" thO po.itiT o n o t- - " " o "
,
mocpb tho
al , _ t i " o n m " " '" of thO rigbt bc t£CO
of tho ,,,,te on of tho body, - 'to"F'igtoure 10 .1A. T
.y•. Nol< th (on
O " " ,i ti "
und m " ,t oal " p c c t of thO " ,. . . tbC .yc<. In h i' lundro
t"" gnath",oma .",1< . . - " , m a ""
<Crt' un i" '' , • .. ,. ,. ." '"
'' 'c d m. . . . thO
hypo",.tie,) l "cuet.re> (""""," ,bowing tho _ n '" fteution
,,,,",1 Th~
po,\tion of . to of
in tho " ,. e '" pe Fig · 1 0.\ A)· " " " thO e h o
" p o e t.
s u c k " plat< lm,,,di,l ''mouth.'' C) T w in d i" '"li '' " ''
is • .cd fn< " h tftC
an enlargem
ent of the ".lytca! "" . ,,.udal "ntcal ".eke<
vestigial gen ,,,,moot to pl'l<,
ital and an C h ;" ," " '"
with some al opening l" " rt '
degree o f s.
certUntY (
1 ) 1 - ' and
phoPrehoticcesy Cross 197
shaorelf e 5) when th
habitat deg atscoampmootennntiic a lhfo
e . ' c
e b o s l and
the
rades. Suc olonizatio
plan'" o f _ h tran,itoe n of fresb
1 co_un )' h abita'" tna h a b i. ." , w h e n
it ie s , nest y include: the natal
s of _ o p c a n io n , du
o d s and v ng, vascula
ertebrateS, r
phytotel""
,ta,
(B)
and temporary accumulations of decaying materials such as beach wrack. Because

of the hypopus, members of the Astigmata have become specialists in exploiting
environments in which resources are rich and prevalent, but unpredictably patchy
and fleeting.
The hypopus is the only life-cycle stage to have contact with the phoretic host
and therefore the only stage to have the potential to construct coevolutionary
relationships with the host. Physiological and morphological coevolution is fo-
cused on the hypopal stage, while the remainder of the ontogeny remains morpho-
logically conserved and ostensibly unaffected by host-related selection pressures.
However, any physiological or chemical adaptations accomplished by the pho-
retic, which are specific to a host, are accommodations that are secondarily
conferred to subsequent nonphoretic developmental stages, because they repre-
sent individual units of the same ontogeny.
2.4 Which Developmental Stage is Phoretic?
Where phoresy exists as a dispersal strategy in mites, not all ontogenetic stages
in the life cycle have equal capacity for dispersal. In some groups of mites only
the adult female is phoretic, while in other groups such as the Astigmata a nymph
258 / M. A. Houck
(C)
(hypopus) is phoretic. The ancestral ontogenetic sequence in astigmatid mites

proceeds as follows: egg ~ prelarva ~ larva ~ protonymph ~ deutonymph
(hypopus)~ tritonymph ~ adult (male or female) (refer to Fig. 7.4, this volume).
Typically, the deutonymph is the only stage that is phoretic (but see Fashing 1976
for an exception).
If the hypopus is facultative, as it is in many Astigmata, it occurs only in a
particular season, under certain environmental stresses, or is expressed only by
some genotypes in the popUlation. The absence of that stage at other times
prohibits successful phoretic migration and colonization. When colonization at-
tempts are successful, resource exploitation and reproduction by these small
creatures immediately follow, and crowding can quickly occur in the rich contin-
gency habitat. Such crowding may provoke serial migration, but any subsequent
migration is the responsibility of the next generation of hypopi.
3. Natural Stabilizing Selection of a Particular Demographic Stage

for Phoresy
3.J Differential Benefits of Phoresy Examined by Age Class
What demographic or selective factors determine which stage of the life cycle
becomes the disperser? The consequences for natural selection of adult dispersal
are obvious and have been covered in the literature. If dispersers are gravid
females or adult parthenogens, each individual is potentially a propagule and
colonization of a new habitat is immediate. It is not surprising that in many
organisms the sole responsibility for dispersal falls to the reproductive females
in the population. A corollary to this is that if phoretics are inseminated females
or adult parthenogens, there is little selection pressure for synchronous group
migration. If instead, dispersers are sexually mature adults (but not gravid),
synchronous migration would provide a selective advantage in the new habitat.
Synchronous migration need not imply large numbers of simultaneous dispersers.
Mitchell (1970), using a simple probabilistic model, proposed that on average
only four individuals are required for both sexes to be represented in the colonizing
population, at least 88% of the time.
It is curious that the phoretic dispersal stage in the Astigmata is not an adult,
but instead it is a juvenile. In the Astigmata, it is an immature hypopus that
arrives at the immigrant habitat. The hypopus must molt into the tritonymphal
stage, also sexually immature, before finally molting into a functional adult. This
naturally leads to the question of how, and under what conditions, does an
intermediate developmental stage become the optimal dispersal stage. Again as
a corollary, because the hypopus is not a capable propagule, synchronous group
dispersal would be expected to correlate with non adult migration. And, that is
often the case in the Astigmata.
The clue to how a juvenile stage takes prominence in the role of dispersal lies ,
at least in part, in the examination of the relative survivorship and mortality of
the various stages in the life cycle.
3.2 Relative Survivorship and Mortality Examined by Age Class
Survivorship and mortality are complementary events in a population and are

described in terms of rate functions, particularly in terms of the forms that these
functions assume (Deevey 1947). Though survivorship and mortality curves
represent a family of continuous curves, they are often partitioned into five basic
types: (1) Type I survivorship curves (log scale, Fig. 1O.2A) describe populations
with high juvenile survivorship (= low juvenile mortality rates), with an exponen-
tial increase in mortality rate (Fig. 10. 2B) until adulthood is reached (= decline
in survivorship). This is known in the amortization literature as Gompertz's law
which has been thought to describe human survivorship. (2) Type II survivorship
curves describe populations with a nonlinear decrease in survivorship with age
and a linear acceleration of mortality rate with age; mortality rate is highest at
adulthood. (3) Type III survivorship curves describe populations with relatively
equitable survival (and mortality) across all age groups. (4) Type IV survivorship
curves describe populations with a nonlinear deceleration of survivorship with
age; mortality rate is lowest at adulthood. (5) Type V survivorship curves describe
populations with high neonate mortality rate, an exponential deceleration of
A. SURVIVORSHIP CURVES
-
..!
a
u
-
II)
CI
.9
Q. ......
:i: 4 ......
f Type III ............
o
>
~
::l
II)
Larva Proto Deuto Trlto Adult

Demographic Stage
B. AGE-SPECIFIC MORTALITY CURVES
Type V Type I
1---------.:..-1=-· _. _. _. _. -._. -'- .-.
Larva Proto Deuto Trito Adult

Demographic Stage
Figure 10.2 . Generalized forms of ecological survivorship and mortality curves. Adapted
from Ricklefs (1973). A) The five general survivorship curves (logarithmic scale) extracted
from the continuum of curves which can describe survivorship in animals. B) Mortality
rate curves. Bold arrows indicate the central point, in Euclidean space, about which the
potential continuum of curves pivot when there is fluctuation in mortality at either end of
the curve.
260
Adaptation and Transition into Parasitism from Commensalism I 261
mortality rate with age, and survivorship becoming relatively asymptotic through-
out all postneonate age groups and on into adulthood.
An assumption of the survivorship model is that the environment and other
constraints differentially influences organisms within a life cycle. Even under
stable environmental conditions, selection pressure may be heavier on some
demographic stages due solely to things such as body size or age-related effects.
For example, an increase in ambient temperature that is tolerated well by adults
may impact nymphs severely in terms of increased evaporative stress due to a
higher surface-to-volume ratio in smaller individuals.
The process of molting is also a source of significant risk to mites which
influences mortality rate, and the youngest immature stages are the most vulnera-
ble to the vagaries of the ecdysal process. Each successful molt results in a greater
probability of survival to adulthood. This risk is additive to the risks of predation
and other environmental selective pressures.
Population density may also influence mortality rates at eclosion, as it does in
the medfly (Ceratitis capitata), the only organism thus far tested in this manner
(Carey et al. 1992). Mortality is lowest for medflies maintained in solitary growth
chambers, and highest for flies maintained in groups. Since migration in the
Astigmata is often correlated with degradation of the natal habitat, resource
depletion, and increased population density, high eclosion mortality (Type V
survivorship curve) would be experienced in the natal habitat prior to migration,
with a potentially lower eclosion mortality in the immigrant habitat (perhaps Type
I curve).
The recent studies on C. capitata offer a serious caveat to studies of life-history
patterns in general and to the Astigmata in particular. Because of the transient
life style of the Astigmata, survivorship and mortality rates need to be examined
as phenotypic characters of individuals (or populations) relative to the expression
of the genotype in various habitats (e.g. natal vs. immigrant). It cannot be
assumed that individuals (or populations) have a canalized genetic program for
survivorship and mortality expectation. That is to say, there is genotype/habitat
interaction (see the excellent work ofW. Kniille 1987, 1990, 1991) expressed in
the mortality rate, and because habitats vary drastically across the life cycle, one
would expect there to be fluctuations in the relative frequency of "survival
genotypes" correlated with dispersal history.
All demographic stages except postmolt adults suffer from the potential hazards
of molting. However, adults face a unique additional source of mortality. Adult
females, in particular, are susceptible to the vulnerabilities and vagaries associated
with reproduction; the consequences of unsuccessful parturition or egg laying,
injury during mating, and drain of energy allocated to developing progeny. Such
risks are in addition to the consequences of molting, and environmental selection,
and reproduction-related risks would be expected to increase as habitat quality
decreases due to the loss of female vigor.
262 / M. A. Houck
3.3 Shifting Selection Pressures at Two Ends of the Survivorship Curve
In populations expressing the Type III mortality and survivorship curves, mortal-
ity rates and survival are equitable and selection for a "good" demographic stage
for dispersal is a moot and irrelevant question. Any stage of the ontogeny would
make as good a dispersal agent as any other. Realistically, however, the forces
of selection are not constant across time for the Astigmata, but rather vary
among the ephemeral habitats they exploit, with preferential impact on various
demographic stages in the natal habitat and yet another impact in the immigrant
habitats. Because of the inherent differential mortality due to size, age, and
habitat shifts, a Type III curve is unrealistic for the Astigmata. Given this, we
may ask what stage in the life cycle of the Astigmata has the highest probability
of survival across all habitats encountered and across all life-history experiences;
or at what stage does the highest mean survivorship occur?
As developed above, under stable environmental conditions Type I and Type V
mortality-rate curves are influenced by the relative constraints of the physiological
processes of eclosion at one end of the cycle and reproduction at the other
end. Mid-life stages (e.g. deutonymphs), on average, experience less impact of
mortality due to molting and size constraints than do the larvae, and no mortality
due to reproduction. At the populational level, the cumulative effect of fluctuating
mortality at the two ends of the Type I and Type V survival curves results in a
U-shaped mortality-rate curve, over demographic time.
Such a U-shaped curve can be accentuated by genetic polymorphisms for age-
related death rates (e.g. polymorphism for reduced larval mortality or delayed
senescence) or by deviations from Gompertzian kinetics (exponential increase in
mortality with age) (Carey et al. 1992, Curtsinger et al. 1992). Such deviations
can occur because various demes experience different ecological experiences
(spatial variation). Deviations can also occur because larvae and adults within a
lineage experience different physical habitats and the developmental stages occur
in sympatry but are not syntopic. Hence, fluctuating gene frequencies track
changes in habitat (temporal shifts).
3.4 The Meaning of a V-shaped Mortality Curve
A U-shaped populational mortality curve is the response to selective mortality

(in time and space) between Type I-Type V curves. Pooled across curves, a
central point exists in Euclidean space, about which the potential continuum of
curves pivots (Fig. IO.2B, arrows). Under varying environmental and stochastic
selection pressures, which may be unstable in time, space, or genotype, the point
of inflection (most predictable mean survival across time) falls at the middle stage
(deutonymph, where there are five life stages). The ecological operative here is
predictable. It is the point at which, under any given set of vagrant selective
forces, the mean mortality rate attains a stable equilibrium value. Because it is
most predictable, and can be tracked through evolutionary time. It is the point at
which selection acts to favor survival during dispersal.
3.5 Risks of Dispersal Assessed by Age Class
Dispersal by any demographic stage can be a high risk event which is in addition
to mortality losses due to predation and physical stress. If the disperser is success-
ful in subsequent colonization, however, the payback to the entire genetic lineage
is enormous. If an ecological void is encountered, the results can be catastrophic.
If we assess the magnitude of the risks associated with a catastrophic loss of
any single age class, it is clear that all age classes do not equally impact the
survival of the lineage. The loss of dispersers exclusively made up of the youngest
age class (larvae) could terminate a lineage if a new habitat is not located before
the natal habitat is depleted. Dispersal larvae migrating into this ecological void
would drain the lineage of any potential of further phoretic recruitment, and
therefore survival from extinction. All subsequent adult reproduction would be
wasted, when phoretic larvae are lost.
Adults would also offer a significant potential loss for the lineage if migration
were unsuccessful in the quest for a transient habitat. For adults represent not
only the loss of a colonizing individual but the loss of an ontogeny (potential
larval recruits in the natal habitat which could magnify the colonization probability
at some later time).
Migration of an intermediate stage (i.e. deutonymphs) does not disturb the
potential for replacement of recruits from the ranks of the larval cohort and eggs
produced sometime later by reproductive adults. Migration by a nymph adds two
important time lags to the system for further migration attempts: one due to the
time delay for dispersal recruitment from the ranks of larvae, and one due to the
time delay for dispersal recruitment from the ranks of eggs contributed by paren-
tals. The temporal component (time lag) of a few hours or of a few days between
any single migration event and the migration of subsequent recruits is very
valuable to the success of new waves of phoretics. Even a small pulse in time
delay may be sufficient to allow for significant local environmental change,
sufficient to prevent potential future extinction. In the vagaries of vacillating
resource quality, in time and space, this hedge could be critical. For example,
it may allow for natural periodicity to replenish resources (e.g. beach wack
accumulating and dislodging with the tides), unpredictable resources to be replen-
ished (e.g. intermittent rains), or untrackable events to occur (e.g. the death of an
organism that will become available carrion).
The least negative influence on the population comes from intermediate stages
being invoked for dispersal. Intermediate stages (e.g. deutonymphs), if lost,
would be replaced from the ranks of the younger cohort (larvae) and from potential
offspring provided at some later time by the parental generation. Again, the time
264 / M. A. Houck
lag associated with recruitment could provide critical time for enhancement of
habitat options.
Thus, I suggest that two influences are critical to the selection of the deuto-
nymph as the dispersal stage for the Astigmata when immigrant habitats are
ephemeral and unpredictable: (I) the influence of fluctuating habitat/genotype
variation on relative survivorship and mortality; and (2) relative impact of the
loss of the developmental stage to the survival of the genotype lineage. I offer
this as a hypothesis of how (ultimately) the deutonymph became the prominent
dispersal stage characteristic of the Astigmata.
3.6 Further Selection for Dispersal Characteristics in the Hypopus
Assuming that selection for phoretic deutonymphs was initiated as a primitive

trait in the Astigmata (OConnor 1982), following the above reasoning, dispersal
would be further enhanced by increased modification of this stage over and
above that occurring in the rest of the ontogeny. The development of the typical
sci erotized hypopal morphology (with caudal ventral suckers etc.) further extends
the initial selective process, would enhance longevity while on the host, and
allow a greater time component for the selection of a "good" habitat prior to
disembarking from the host. The consequences of evolving a hypopus have
significantly enhanced the adaptive radiation of the astigmatid lineage.
Ancestrally the Astigmata consisted of free-living fungivores (OConnor 1979),
but because of the possession of the hypopus they now exploit a diversity of
niches (Fashing 1976, Fashing and Wiseman 1980, Norton 1980; also see Fash-
ing, Norton, and OConnor in this volume) including parasitism. They have
become saprophages, nidicoles, synanthropic pests of stored foods, and perma-
nent parasites. Many astigmatid mites are nidicolous (nest) associates of mammals
and birds. The nidicolous condition now includes synanthropic "nests" created by
the agroeconomic practices of man (e.g. granaries, warehouses, barns, mushroom
houses etc.).
Historically, habitat diversification by the Astigmata was also correlated with
a wide range of new ecological associations with arthropods. It is the mite-
arthropod association which will be the focus of the remainder of the discussion.
4. Evolution and Transition into Parasitism
The discussion thus far has focused on ecological/phenotypic participation in the

evolution of a phenomenon called phoresy in the Astigmata. An equally compel-
ling and important theme will now be developed that argues that the evolutionary
consequence of phoresy in the Astigmata is to rescue astigmatid lineages from
the ravages of constant migration, made necessary by chronic ephemeral ecologi-
cal shifts. Phoresy has provided the necessary and sufficient prerequisites for
mites to enter into a different (and ecologically more stable) evolutionary contract
with the host-that of parasitism.
4.1 Hemisarcoptes as an Example of Potential Evolutionary Transition
Hemisarcoptes is the type genus of the family Hemisarcoptidae. Free-living

stages of Hemisarcoptes (larvae, protonymphs, tritonymphs and adults) (Fig.
1O.IA) are generalist predators of diaspidid scale insects, a speciose parasitic
family attacking most perennial vascular plants worldwide. Hypopi of Hemisar-
coptes have established stenoxenic phoretic relationships with beetles ofthe genus
Chilocorus (Coleoptera: Coccinellidae) (Gerson and Schneider 1982, Houck
1989, Gerson et al. 1990, Houck and OConnor 1990, Houck and OConnor 1991,
Houck and Cohen ms.). Both Hemisarcoptes and Chilocorus occur in all habitable
continents of the world. Both are predators of scale insects (Fig. 10.3).
Hemisllrcoptes cooremani (Thomas) is indigenous to southern North America,
and is commonly phoretic on Chilocorus cacti. Once on the beetle, the mite
positions itself subelytrally (Fig. IO.4A, B, C) and is subsequently transported
to a new habitat as the beetle forages for scale insects. Since H. cooremani and
C. cacti both prey on scale insects, post-deutonymphal development of the mite
occurs within the habitat of its appropriate prey (Fig. 10.3). Only the phoretic
hypopus of Hemisarcoptes occurs on the beetle, and all other stages remain under
the caps of the scale insects to feed.
LePidOSa~hes
11\ r
\ -
/ ~
Imm
t-----I
predation predation
phoresy _ _ _ _ _ _......._
H emisarcoptes
Figure 10.3. Diagram of the tropic and phoretic pathways of interaction among Hemisar-
coptes, Chilocorus and their prey (Diaspididae).
266 I M. A
. Houck
._Figb"o"d1to0.4.
the
" ,_ ,n g o
,n '' ''
J."uon """tomicrO"' ' '
ore PO""QUOd o be '' ' ,n d o « of C h i" " .' " ofo A
wi,h the,. g n th e " n d ov " " ' " " r i. Not< ) H e " '' '' '· P '' ' , • •
,,-'
""""0",,, ,,,,,,v'dual'
oathO""'''' on " " o the .. .jori
wing of Ch""".''''' F "
,o d poin"n o f the d y tt ° n . B) flY
g ,, ,. d ,l Iy ,
in u
""'"
ty o f
the " n d o "
,n " " ,ucW o U '" " 'g ' of the Forewn ;! o ,, " and , - , , ' toWo n the - "
onlY" o n th "
e " " d e oJy ,.te" w , ll " the de C",,,,,·,",·
'ng o f " 1 l " Hind
from one el
ytrOn of o
""". '" man
Y " 400 hY
li "te "
l"'l" o f H.
M
"'""" (,,",w). C) _ b ite ' "in,
"S,...,.. roo'"
ne individ ,,,.,,-'
ual of C. ca ha
ve -
cti. " ,1 I« te d
4.2 Eviden
ce fo , "Som
ething O ,h
Hemisarco
ptes cooremani
" ,han pho
re"''' 'n
4.2.1 Interr
uption of O
T h e dento ntogenesis
pOpulation n y tnph o f H .
(HOU ' an " . o , , _ i i, f" ,. ,t v
e n c O u n te d a U e and re
r, b " " tCwhil o e o n n o r ,990). HY p
they die. T e w .i ti n g to m i" " PO'" o f H. resents only 6% o f th
his ,i tu a l te , do not coo,,,,. .ni '
OIolt to cO that do no
ion haS aI'O be<tt d i" OIplete o n t
,. v e re d in
other " ti g ntatid to g e n e ,i ';
miteS (e.g·
Lardaglyphus; M. Okamoto, pers. comm.). Thus, host contact may not only be
employed as an environmental monitor but may also be vital for survival.
This then violates one of the central constructs of the definition of phoresy:
"benefit is not conferred as a developmental ... influence on the phoretic stage."
This interruption of ontogenesis, associated with the absence of a host, was one
of the earliest clues that something other than phoresy was likely.
4.2.2 Cantributian ta Mite Nutrition
A second piece of evidence that the Hemisarcaptes-Chilacarus interaction

should not be considered phoretic is that hypopi maintain a long residency time
on Chilacarus (5-21 days), which is not completely explained by the need to
disperse. Host-attachment may continue even when fresh resources are readily
available (pers. observ .). Also, while attached to the host the mites were observed
to undergo a visible morphological change (swelling) prior to disembarking from
Chilacarus (Fig. 10.5).
These observations led to the hypothesis that some "material(s)" essential to
hypopal survival and/or development can be acquired in transit. A potential
source of available "materials" for hypopi while on the host is reflexed beetle
hemolymph. Chilacarus defends itself by exuding hemolymph from tibio-femoral
joints and from the pronotal-elytral junction. This "reflexive bleeding" is an
effective antipredator deterrent, associated with aposematic coloration (Pasteels
et al. 1973). Since the hemolymph contains alkaloids (work in progress, with T.
Eisner) a serious irritation occurs to the attacker, while the hemolymph oxidizes,
coagulates, and cements a potential predator's mouthparts together. Thus the
hemolymph acts to chemically and mechanically debilitate the predator.
4.2.3 Hemisarcaptes Has Adapted ta Chilacarus Refiexed Hemalymph
Reflexed hemolymph, exuded from the pronotal area, runs down and swaths
the subelytral surfaces of Chilacorus. It is in this area where Hemisarcaptes is
attached. Evidence for the adaptation of the mites to this caustic chemical is that
it does not appear to cause any mechanical or chemical damage to the mites (Fig.
10.7). They are capable of escaping entrapment and show no signs of ill effects
from alkaloids with which they come in contact (pers. observ.).
Active conservation of selected hemolymphal nutrients by the beetle does not
appear to occur prior to hemolymphal ejection. Reflexed hemolymph is similar
to that in the body cavity, in chemical makeup and concentration, where these
have been evaluated (e.g. proline and sucrose, pers. observ.). The mites have
direct access to this hemolymph, rich in nitrogen and sugar, whenever the beetle
is disturbed. The "disturbance" response can be readily invoked simply by brush-
ing the surface of the beetle with the soft bristles of an artist's brush.
F ig '" 10.5 . S e " " ,i n g "
" ,t w n p _ "
'' '' '' '' ,' '' ., ,i c rO S " p
individu" (A. B) " " " b (SEM) of
H,m'''''''''''''
"",",_,,,n,to~ re' "~'"i",
" " ,d it io n w o f C h il O
\ton oollcc
" in "",,
'' '' " ' ,, ,, ti . "
Both mito' o
twO hYpop
' of
w x ." te
m it " , whO
n ,1 ted . T h i' '" d from o
tho "",,,,h " t i " ond a pth
o'ogica' ,b p o " '" to h'aebin-rge=I
" " '"
to bOth S E I0w ,d a"ociaUon wit ood
M _ o r i anM '. (SEM "",o h th ' _ " , a n g ' that "
,ab""k~
d Ot'. G. G toPli'' '' '' w . Se'" " " ,, 0 " in
th '
o o < d ' doring a ith tho " " i"
o . F ig ure ,O.5A i' " " ,I
'' ''
,t th ' V o l" '' " ,d i" b "
" it y o"f," " " " n of
e a li foio
" ,i ', R ,,,.,,,. M
,i d o ).
268
4.2.4 Hemisarcoptes Acquires Materials from Chilocorus
From radio-labeling (HTO) studies (Houck and Cohen ms.) it was discovered
that hypopi of Hemisarcoptes acquire materials (at least water) directly from
Chilocorus. This acquisition was in addition to atmospheric water taken across
the cuticle. This then violates the second tenet of the definition of phoresy:
"benefit is not conferred as nutritional . . . influence on the phoretic stage."
There remained the curious question of the mechanism of acquisition of materi-
als in a heavily sclerotized animal without a mouth. While some water enters as
water vapor across the tanned cuticle, behavioral and morphological evidence
indicated that the suckerplate also might function in acquisition of water in
hypopi. The discoidal suckers were observed to pulsate slowly while the hypopus
was positioned subelytrally and the anus could be observed to open and close
(Hughes 1976, pers. observ.). The modified third and fourth pair of legs, posi-
tioned at a 45° angle to the body, acted as lever arms to raise and lower the sucker
plate while it is attached to the elytron. This could create a negative pressure
on soft elytral tissues sufficient to evacuate small quantities of hemolymph.
Hemolymphal drainage would then be accessible to folds of the sucker plate, the
vestigial genital opening, and the anal atrium (Fig. lO.IC). Slow acquisition
would allow the uptake of provisions, and yet remain nonpemicious to the beetle,
so as not to provoke action against the acquisition. This may account for the long
(5-21 days) host-association observed in hypopi of H. cooremani.
But where would the hemolymph go once extracted from the beetle? Examina-
tion of scanning photomicrographs of hypopi revealed vestigial anal and genital
openings on the sucker plate (Fig. 1O.IC). If the mite was indeed "feeding"
through the anus, where did the materials acquired during "feeding" go? How
was this proposed "anal feeding" possible if the gut is solid as the literature
indicated?
The logical way to examine these question was to section hypopi in situ. Such
sectioning was unsuccessfully attempted over a three-year period in an effort to
determine the physical relationship between the mite and the beetle. Because of
the practical and logistical difficulties in obtaining adequate sections, another
approach was taken. The hypodermis of the beetle elytron was chemically dehy-
drated and reflected from the procuticle, exposing the beetle-side of the hypoder-
mis (Fig. lO.8E). One could then look at the beetle tissue and examine its structure
for evidence of the effects of hypopal attachment. This procedure revealed small
triangular openings in the hypodermis. Looking through these openings, one
could observe the medial suckers of the mite sucker plate. While this does not
mean that the mites created the openings, they were at the very least associated
with them.
The problems associated with preservation and sectioning have recently been
resolved (Houck and Lindley 1993). Sectioning of mites attached (in situ) to
beetle elytra, exposed the presence of a gut in the hypopal stage (Fig. lO.6A, B).
Fig""
,op'" ,,!O,,.6,,. ,_L,ight pbOto" " " " " '' '' '' o
" " 'o n ; B
~ (4OO
x) attaO
~
f\ o n
g it u d
onudo,,,,,, u
,,l ,uc1<e< pt " " d gu ~
Biudg , '" b<d to the ,ubClytral ,u'n " " " " " " , o fa " p o p
lat< (" " 'w ). t, P Pn>,,,,trloulU
tf " '" of Ch'""o,", ,ac"·o , o f H , .. "a,·
,u~goal ,~uP"'~
hypOpO'" B T h ' hiudgu A ) P o '' '' o
", li d and . ) ""tWO< ,, '. ''
. .', ," '" tb ,,rion; F t o p '° ' on
",pbagoal
e Fote gut. T to th ,
and h o fo", gut
aof th ,
gangh .
270
Adaptation and Transition into Parasitism/rom Commensalism / 271
This gut has structural integrity which includes a proventriculus, and a midgut
which opens onto the sucker plate. The foregut is indeed solid (Fig. 1O.6B). The
gnathosomal ("head") end is nonfunctional in feeding.
In light of these findings, a reexamination of older literature (Hughes and
Hughes 1939, Oboussier 1939, Wallace 1960, Boczek et al. 1969, Woodring
and Carter 1974) revealed what appears to be a similar atrium at the vestigial
genital and anal openings in other astigmatid mites. The potential significance of
this was apparently overlooked by earlier workers. And, the actual distention of
the hypopus of Hypodectes prop us was previously observed by Fain et al. (1980):
"parvenu sous la peau, l'hypope augmente considerablement en taille, proba-
blement a la suite de l' absorption de substances nutritives par osmose." The
mechanism of this distention has not been explored. Additionally, hosts infested
by hypopi of Echimyopus dasypus illustrated hyperkeratosis and hypertrophy
around embedded mites (Fain and Lukoschus 1977). The mechanism of absorp-
tion of lysed tissues is still unexplored.
4.3 Hypothesis for the Evolution of Parasitism from Phoresy
Associations between mites and arthropods are very ancient (Poinar 1985, Poinar
and Grimaldi 1990, Norton et al. 1993). The only available fossil (in amber) of
an astigmatid mite is Amphicalvolia hurdi (Turk and Turk 1957). This specimen
dates from the Oligocene or Miocene and can be assigned to a modem lineage,
a congener which is associated with subcortical beetles (OConnor, pers. comm.).
This, coupled with the fact that hypopi are ancestral in the Astigmata, is evidence
for the fact that the Astigmata have had at least 25-38 million years of association
with their host (and probably more). Lindquist (1975) suggests that mite-insect
associations may be as old as 100 million years old. This is ample time for
coevolution to have occurred, for the mites to have gained a strategic advantage
in the relationship, and to have begun a sojourn into parasitism.
Interactions of hypopi with their respective hosts have been uniformly labeled
as "phoretic" in the Astigmata for over 100 years (Michael 1884, Stolpe 1938,
Hughes and Hughes 1939, Oboussier 1939, Perron 1954, Turk and Turk 1957,
Hughes 1959, Wallace 1960, Evans et al. 1961, Kuo and Nesbitt 1971, Woodring
and Carter 1974, Hughes 1976, Krantz 1978, Binns 1982, OConnor 1982), but
this interpretation has been based on morphological criteria alone.
From the accumulating evidence, I propose the following hypothesis of evolu-
tionary events which is compatible with all observed morphological and phyloge-
netic patterns and the radio-labeling data (Table 10.1): (1) the deutonymph
became the demographic focus of differential selection resulting in it becoming
the dispersal stage early on the evolution of the Astigmata (as developed in
sections 3.1-3.6); (2) dispersal was enhanced by morphological changes (hypopal
characteristics) and the association with a carrier organism (e.g. Chilocorus); (3)
phoresy initially became established with low energetic costs to the host; (4)
272 / M. A. Houck
Table 10.1. Summary of hypothesized "parasitization" events in the Astigmata, using

phoretic interactions of Hemisarcoptes and Chilocorus as a model. See text for support
for the hypothesized steps given.
I.) The deutonymph primitively arose in the Astigmata for dispersal among ephemeral
habitats.
2.) Selection for dispersal qualities resulted in the typical astigmatid hypopal morphology
(e. g. sucker plate, scierotizations etc.; Fig. 10.IB, C).
3. ) Dispersal was facilitated through host association.
4.) Phoresy was tolerated by hosts because of the relatively small cost.
5.) Extended host contact (over 25-100my) resulted in adaptation by the hypopus to host
reftexed hemolymph (toxic alkaloids; Fig. 10.7) which had evolved as an antipredator
defense in the host.
6.) Adaptation to toxic (and also nutrient rich) reftexed hemolymph led to hemolymphal
utilization by hypopi (Fig. 10.5).
7.) Reftexed hemolymph was central to host survival from predation. Utilization of avail-
able reftexed hemolymph (produced at the discretion of the host during predator defense)
advanced to hemolymphal extraction by action of the sucker plate and host exploitation
(Fig. 10.7).
8.) As chemical adaptation proceeded, morphology would offer no clue of the changes in
progress.
9. ) Hypopal morphology (i.e. sucker plate) was needed to maintain contact with the host
and withstand the rigors of the habitat (e.g. sclerotization) and so was conserved during
the process of parasitization.
10.) Parasitization required that the hypopus molt on the host, and that subsequent stages
also remain as ectoparasites. Subsequent stages were exapted for parasitism (Fig.
10.IA) due to gnathosomal morphology and chemical immunity conferred through
hypopal adaptation. This was a change for which there was no rapid correction by the
host, once the mutation occurred.
1 I.) The mutation for molting on the host would be heritable, the mite lineage would become
resident on the host, and dispersal would become maladaptive.
12.) The hypopus would drop from the ontogeny once the derived parasitic lineage was fully
established.
\3.) The benefit of phoresy would be superseded by the greater benefit of not needing to
disperse, once the transport vehicle became the resource.
extended contact of the hypopus with the host, and exposure to the toxic hemo-
lymph, resulted in chemical acclimatization to the hemolymph; (5) adaptation to
beetle hemolymph accelerated and graded into the utilization of the hemolymph
by the mite because of its richness in nitrogenous and energetic nutrients; and (6)
the interaction accelerated still further, from utilization of reflexed hemolymph
(controlled by the host) to removing hemolymph through the caudal ventral sucker
(host exploitation).
Fig"" 10.7
. Subelytt
of v;e'" in d al ,ari"" of Chil'''o
down the ", i" " " • p l. " , on the el
le~ " m -
,"' ,ae'i. T "
b e ly tral " ,d a c e ytton " ,h e « '' '' 'r o w in th
riglrt and . ",.gul.to< hemolymph e middle o
! and ,u _ u fro'" <be 1 f the field
,now hYl"'l' """"
of • previO
U' "".pee. ""peetively
i e " a p in g enl,,_
. In ,, rt i'
e n tl y _
t by the ho
k l. ArroW'
emoly"",b
'" " " . b a ' ro
in the ul'P'"n
an enla<ge ment . and tbe gh
left. of <be i",ag o,t
e in the " "
I f th e hypO ""
Pi th en reroat
adjustments ced on the hom to
nymphal ,ta
of scale inse es
w ould be re
g . C h e li quired for functional
" '' ''
molt. only
para
cts and t\teT of mobile ,tages are a sitism to oCcur in post
minor ~hological
<fore exapte da -<
by the hypO d fo' beetle peted to fceding on " ,f !eUto-
stages sinceP'" to chemicals in th ti " u s (Fig 0 t ti " u e '
theSe stag
es rep e hemolytn h
P is . I .1 A). A
resistan« h daptation
ypothesis su resent (genotypicallY)conferred to subseque
_ s i t i o {r ggest that th a single ind nt fceding
e hypOpus ividual. Th
n Om the free.living ex provideS th
e u lt
is toxin-
isten'" in te i""te pOten
staP hyploagraenetic mpO'ary e tial fo'
ble si n v _ ments
nally consi tic epxaisttte ern
ncSe.of hypOpaI
" " ,_ _ • to a more
st
den vari ent ",ith conclusio
es considera ns derived OIl the Astig
hos~depen
A scet i . . - ' bly {r o m my tnata are in
as defined b _ n g the 69 familie studies. W
hile
ter-
to obligate y O Connor (19 s an d :> 78 5 gen
parasitic fo 82)-- {rOm
the life cy rm s -t h e hy free·living era in the cohort
c le pO p u S has n formS (with
incompatib of any obligate hypOpi)
le. The only parasite. H ot been found to exist
p O y p oPi as pa
tion is in th and parasitiC life cy rt of
(o c o n n o r. "ible excep
pets
phic deuton . . .nun.). ColeogfyphU e supedam c
ily Cane,tr\ s arele
ymph ",hil S and Meg nioidea
e membetS acane,,,i.i
a retain a -
of the onto
geny oCcur --
as _ p a r a s
it e S posi·
274 / M. A. Houck
tioned subelytrally on the thoracic stemites of the host (Samsimik 1971). The
hypopus is lost in all more derived parasitic taxa in the superfamily, so this
actually argues for the inherent incompatibility of parasitic and hypo pal stages in
one life cycle.
H emisarcoptes hypopi are the ultimate "wolf in sheep's clothing." They acquire
materials from their host, acting as functional parasites, while retaining the
ancestral phoretic morphology. The morphology which was interpreted for so long
by researchers as phoretic may actually represents the transitional compromise
between obligate parasitism and phoresy. To date this work on Hemisarcoptes is
the only such attempt to experimentally define such "phoretic" relationships.
Experimental studies on the morphological and physiological adaptation of astig-
matid mites to their hosts could lead to a greater understanding of coevolution
and the mechanisms of the evolution of parasitism. More interest in similar
issues, surveyed across the astigmatid clade, would tell us how representative
Hemisarcoptes is of the grade of potential transitions. The most valuable place
to start is in the mites associated with the Coccinellidae and Chrysomellidae
because these families of beetles share the character of reflexive bleeding which
facilitates and promotes the critical initial process of interaction. It is less likely
that semi parasitic transitional grades will be found in associations that offer no
readily accessible stimulus or reward, or in situations where the host is provoked
to retaliate when the relationship is first established.
Hemisarcoptes may have succeeded in overcoming the defensive volley of
counterreaction by Chilocorus because it originally established a benign relation-
ship that slowly graded into use of reflexed materials. Initial steps into exploitation
required no significant defensive response from the beetle. The main target of the
development of reflexed hemolymph was attacking predators, such as ants and
other arthropods. Selection for such an important function would be strong.
Evolution of exploitation by the mite included chemical adjustment to the host
alkaloids, the beetle's major line of self defense.
Once physiologically adapted, the only major change required to bring the
transition to closure, was that the mite molt on the host instead of getting off to
molt. This has not occurred in Hemisarcoptes. This mutational step could be
accomplished within one generation, a time frame which could not be countered
by the host. Its fate accomplished, the mite would no longer need to move among
transient habitats, and the dispersal stage would be selected from the ontogeny.
The morphological shift from phoresy to parasitism, if observable, would have
had the appearance of a macroevolutionary event when in fact the "phoretic"
was slowly adapting physiologically to a parasitic nature while retaining the
morphological characters of a phoretic.
Such transition into parasitism also offers potential for the creation of a new
lineage within the astigmatid clade if the hypopus is a genetic polymorphism.
Females expressing the heteromorph have the potential to step into parasitism,
and the step once taken separates them from their nonphoretic sisters which
remain tied to the original habitat.
"Vacant niches exist for parasites" (Price 1980), but most potential hosts
can defend themselves against exploitation and parasitism by morphological,
physiological and behavioral counterreactions. As stated initially, a parasite as
"an organism living in or on another living organism, obtaining from it part or
all of its organic nutrition, and causing some degree of real damage to its
host" (quoted in Price 1980). Using this definition, there is little doubt that
Hemisarcoptes is more like a parasite than a phoretic but the transformation is
not yet complete.
5. Future Work and Prospectus
It seems that all corroborating evidence indicates that H emisarcoptes became

associated with Chilocorus because of the primitive dispersal relationship of the
heteromorphic deutonymph with adult beetles. However, recent studies indicate
that the paradigm of phoresy in H emisarcoptes is inconsistent with important
observations and that the initially benign relation has graded, over time, into a
host-parasite relationship. In order to understand how coevolution has occurred,
this research must continue to focus on the mite (Hemisarcoptes) , but additionally
work has begun to elucidate the perspective of the beetle (Chi/ocorus) in the
relationship.
If initial studies have given an accurate glimpse of past evolutionary occur-
rences, there should be some evidence that Chilocorus has indeed suffered some
differential "degree of damage" which can be correlated to degree of hypopal
association. Examination of museum and field specimens indicates that not all
Chilocorini are equally likely to transport Hemisarcoptes (pers. observ.).
Morphological examination of the subsurface of the elytron of Chilocorus has
been informative. This is the area of attachment for the mites and represents the
"habitat" of the mite while in transit on the beetle. The micro sculpturing of the
subelytral surface presents obstacles to the attachment of mites to C. cacti, in
some portions of the e1ytral surface.
In the zone just caudal to the pronotal area, the elytron projects spines that are
less than 10 /-Lm apart (Fig. 1O.8A, B). For the mite to attach at this point would
require sitting on approximately 4-5 spines, risking damage to the delicate sucker
tissues and possibly terminating mite-beetle interaction. Visually scanning the
surface caudoventrally along the medial axis, the projections become less dense,
smaller and more blunt. Approaching the caudoventral-most tip, the surface
looses the armature and the attachment plane contains a fluff of material which
is composed of what appears to be anastomosing superficial vessels (presumably
the tracheal system) (Fig. 1O.8C, D, E, F).
There is a correlation between the morphology of the beetle elytron and the
positioning of the mites. Mites which have had time to select an attachment site,
do so by anchoring only to the caudal ventral tip (Fig. IO.4A). One hypothesis
is that the beetle encourages the mites into a position on the body which provides
F ig "" 10
.8.
in . o f t' " .u ", ,, ,, ," ,, , e l" tw U ph
b o
,ubol>",,1 " olytml ,u n '" of C h iw tomi''''"'''P''' (SEM) o
bO" ""n l " , " ,, , " " ," " " ,acli. del""'"
f t' "
. , , - t to " " pronotum (No'" oJytr A) S p li t· " " ,n SEM im micro"ulpt. .·
ri .b ' oftb< on
of " " i" " ."
n ,IY'ton). S< re m '' '' '' fto m th , bod '" o f " " " ," " '' ''
in ,b " , , " ly . B) An SEM o o l"
"
of 'h < oJy"" " k " ,bOn
" (" m p ,r e
lo~m ,p " '" Mi'"
ok
" m en' of " b " " with " " " n '"
"
'" n l
, - " . . .. " ,, ' in
y; " " boad
'0 ""
Fig. 10.SA
would
k f t portio'
tip of th , "
y
with Fig 10
k ft portion " " n , whO" mire' m ''
''
.4A)· C) S p o nonn'Uy found
li ,· " " ,n SE
M
,,,,,h'" ,bi' ,n"
in
. S p in "
1 0 .s e . No f " " i" " g ' only. DJ fre<l",ntly _ b . Sea i" " ,, ' of " " ,"udO'oo
o
""re '"
~,
ti'" th" An SEM ,n l, W i ' n ",1
oJy""n " ," 0 no ,pi"" in Ja<gemoo' of " " , with " fo re '" to ,b '
" " of ,,,,
" '" ,u p
,,
e d id " and
...,tom"" ,b i' ,rea. In''''''' - ""
th , ..." b o ,1 " , " in F i.
" ln g SEM b,,,,nl of bYl"'f'i. E) to th ' ," n '" ,y ,, ,m of
(_w),
. f ) ,, ,, ,m i,
",,00 ,i O O
in Fig. 10.8
"",00 """"otOO"
photomi,,,
,,,,,,b
o
" of th ' - " f ,hO bYP""'nni" 'f b i, " "
' ' ' ,y ,, ,m
bighly m
i. " "
,bcit oriOO n(1'F.Ml of ,ho !r " b ,, 1 " " ih '"
E, ,bOwing
surface of
the beetle
e1ytron.
,.,io with ref_'" to th , ,"
" ,m o o "
hOlY""
276
the beetle with the greatest mobility or the least energetic drain. Could there be
some form of minimal-loss compromise to the occurrence of the mites, on the
part of the beetle? Is this some form of counterresponse? Or is it just an aspect
of beetle morphology related to some other function? Similar examination of
other members of the tribe Chilocorini for microsculpturing would add perspective
to this question. Thus far I have examined the two North American species of
Chilocorus (C. cacti and C. stigma), a European species (C. bipustulatus), and
oriental species (C. kuwanae), a Mideastern species (C. nigritus), and two African
species (C. distigma and C. discoideus).
Sister genera of Chilocorus found in North America (Gordon 1985), and also
within the tribe Chilocorini include: Exochromus, Brumoides, Axion, Halmus
(= Orcus), and Arawana. Thus far representatives of Exochromus, Brumoides,
and Halmus have been examined for outgroup comparison of the sculpturing as
it relates to morphological changes in the subelytral surface. Such comparison
is valuable because Exochromus, Brumoides, Axion, Halmus (= Orcus), and
Arawana are not phoretic hosts of Hemisarcoptes. A representative of the non-
chilocorine coccinellids (Rhyzobius, = Linobius) is also being examined. The
genus Rhyzobius was selected because it is also a predator of diaspidid scale
insects, is sympatric with Chilocorus, and represents an ecological and evolution-
ary contrast. The full results of these studies will be discussed elsewhere.
Acknowledgments
I would like to acknowledge Uri Gerson (Israel) for introducing me to Hemisar-

coptes in 1982, and thank Barry M. OConnor (University of Michigan) for an
early partnership in the systematic treatment of the Hemisarcoptidae and for
encouraging a deep and compelling love of mites. Dr. R. K. Summy assisted in
the location of my first field collection of Hemisarcoptes in Donna, Texas in
1983. Dr. R. E. Strauss contributed to the clarity of this text. This work was
initiated by NSF grant #83-07711 to B. M. O. C. and M. A. H. and continued
with funds generated through a Binational Agricultural Research and Develop-
ment grant # IS-1397-87.
References
Baker, E. W. 1951. Pneumocoptes, a new genus of lung-inhabiting mite from rodents

(Acarina: Epidermoptidae). 1. Parasitol. 37:583-586.
Barker, P. S. 1982. Control of a mite Lepidoglyphus destructor, including hypopi, in
wheat with carbon disulfide. 1. Econ. Entomol. 75:426-439.
Berenbaum, M. R. 1983. Coumarins and caterpillars: a case of coevolution. Evolution
37:163-179.
278 I M. A. Houck
Binns, E. S. 1982. Phoresy as migration, some functional aspects of phoresy in mites.

Bioi. Rev. 57:571-620.
Boczek, J., C. Jura and A. Krzysztofowicz. 1969. The comparison of the structure of the
internal organs of post-embryonic stages of Acarus farris (Oud.) with special reference
to the hypopus. In: Proc. 2nd Int. Congr. Acarol. (G. O. Evans ed.). Sutton Vonington,
England, 1967. Akademiai Kaid6, Budapest. Pp. 241-248.
Brooks, D. R. 1979. Testing the context and extent of host-parasite coevolution. Syst.
Zool. 28:299-307.
Carey, 1. R., P. Liedo, D. Orozco and J. W. Vaupel. 1992. Slowing of mortality rates
at older ages in large medfly cohorts. Science 258:457-461.
Curtsinger, J. W., H. H. Fukui, D. R. Townsend and J. W. Vaupel. 1992. Demography
of genotypes: failure of the limited life-span paradigm in Drosophila melanogaster.
Science 258:461-463.
Cutcher, J. J. and J. P. Woodring. 1969. Environmental regulation of hypopal apolysis
of the mite, Caloglyphus boharti. 1. Insect Physiol. 15:2045-2057.
Deevey, E. S., Jr. 1947. Life tables for natural populations of animals. Q. Rev. Bioi.
22:283-314.
Ehrlich, P. R. and P. H. Raven. 1964. Butterflies and plants: a study in coevolution.
Evolution 18:586-608.
Evans, G. 0., J. G. Sheals and D. MacFarland. 1961. The Terrestrial Acari of the British
Isles: An Introduction to Their Morphology, Biology and Classification, Vol. I. Brit.
Mus. (Nat. Hist.), London. 219 pp.
Ewing, H. E. 1912. The origin and significance of parasitism in the Acarina. Trans. Acad.
Sci. St. Louis. 21:1-70.
Ewing, H. E. 1933. New genera and species of parasitic mites of the superfamily Paras i-
toidea. Proc. US Nat. Mus. 82:1-14.
Fain, A. 1968. Etude de la variabilite de Sarcoptes scabiei avec une revision des Sarcopti-
dae. Acta Zool. Pathol. Antverp. 56:73-82.
Fain, A. 1969. Adaptation to parasitism in mites. Acarologia 11:429-449.
Fain, A. 1971. Evolution de certains groupes d'hypopes en fonction du parasitisme
(Acarina: Sarcoptiformes). Acarologia 13: 171-175.
Fain, A. and F. S. Lukoschus. 1977. New endofollicular or subcutaneous hypopi from
mammals (Acari: Astigmata). Acarologia 19:484-493.
Fain, A. and J. R. Philips. 1981. Astigmatic mites from nests of birds of prey in USA.
VI. The adult froms of Echimyopus orphanus Fain and Philips, 1977 and Dermacarus
pilitarsus Fain and Philips, 1977. Int. 1. Acarol. 7:235-237.
Fain, A., D. P. Britt and D. H. Molyneux. 1980. Myianoetus copromyzae sp. nov. (Acari,
Astigmata, Anoetidae) phoretic on Copromyza atra (Meigen 1830) in Scotland. 1. Nat.
Hist. 14:401-403.
Farish, D. J. and Axtell, R. C. 1971. Phoresy redefined and examined in Macrocheles
muscaedomesticae (Acarina: Macrochelidae). Acarologia 13: 16-29.
Fashing, N. J. 1976. The resistant tritonymphal instar and its implications in the population
dynamics of Naiadacarus arboricola Fashing (Acarina: Acaridae). Acarologia 18:704-

714.
Fashing, N. J. and L. L. Wiseman. 1980. Algophagus pennsylvanicus-a new species of
Hyadesidae from water-filled treeholes. Int. 1. Acarol. 6:79-84.
Feeny, P. P. 1976. Plant apparency and chemical defense. In: Recent Advances in Phyto-
chemistry: Biochemical interactions Between Plants and Insects, Vol. 10 (1. Wallace
and R. Mansell eds.). Plenum Press, NY. Pp. 1-40.
Gerson, U. 1967. Observations on Hemisarcoptes coccophagus Meyer (Astigmata: Hemi-
sarcoptidae), with a new synonym. Acarologia 9:623-638.
Gerson, U. and R. Schneider. 1982. The hypopus of Hemisarcoptes coccophagus Meyer
(Acari: Astigmata: Hemisarcoptidae). Acarologia 23:171-76.
Gerson, U., B. M. OConnor and M. A. Houck. 1990. Acari. In: Armored Scale Insects,
Their Biology, Natural Enemies, and Control (D. Rosen ed.). Elsevier, Amsterdam.
Pp.77-97.
Gordon, R. O. 1985. The Coccinellidae (Coleoptera) of America north of Mexico. 1. NY
Entomol. Soc. 93:1-912.
Holmes, J. C. 1973. Site selection by parasitic helminths: interspecific interactions, site
segregation, and their importance to the development of helminth communities. Can.
1. Zool. 51:333-347.
Houck, M. A. 1989. Isozyme analysis of the mite Hemisarcoptes and its beetle host.
Entomol. Exp. Appl. 52:167-172.
Houck, M. A. 1992. Morphological variation in an ectoparasite: partitioning ecological
and evolutionary influences. In: Ordinations in the Study of Morphology, Evolution,
and Systematics of Insects: Applications and Quantitative Genetic Rationales (1. T.
Sorensen and R. Foottit eds.). Elsevier, Amsterdam. Pp. 277-308.
Houck, M. A. and A. C Cohen. Ms. Transition from a free-living life form to parasitism
via phoresy: experimental evidence from the mite Hemisarcoptes.
Houck, M. A. and V. Lindley. 1993. A microwave technique for microscopical studies
involving arthropods. Am. Entomol. 39:117-119.
Houck, M. A. and B. M. OConnor. 1990. Ontogeny and life history of Hemisarcoptes
cooremani (Acari: Hemisarcoptidae). Ann. Entomol. Soc. Am. 83:161-205.
Houck, M. A. and B. M. OConnor. 1991. Ecological and Evolutionary Significance of
Phoresy in the Astigmata. Annu. Rev. Entomol. 36:611-636.
Hughes, A. M. 1976. The Mites of Stored Food and Houses. Min. Agric. Fisheries Food
Tech. Bull. 9. H. M. S. 0., London. 400 pp.
Hughes, T. E. 1959. Mites or the Acari. Athlone Press, London. 225 pp.
Hughes, T. E. and A. M. Hughes. 1939. The internal anatomy and postembryonic
development of Glycyphagus domesticus. Proc. Zool. Soc. London 108:715-33.
Kethley, J. B. and O. E. Johnston. 1975. Resource tracking patterns in birds and mammal
ectoparasites. Entomol. Soc. Am. Misc. Publ. 9:231-236.
Kim, K. C. 1985a. Evolutionary relationships of parasitic arthropods and mammals. In:
280 / M. A. Houck
Coevolution of Parasitic Arthropods and Mammals (K. C. Kim ed.). Wiley, NY. Pp.
3-82.
Kim, K. C. 1985b. Parasitism and coevolution epilogue. In: Coevolution of Parasitic
Arthropods and Mammals (K. C. Kim ed.). Wiley, NY. Pp. 3-82.
Kniille, W. 1959. Morphologische und entwicklungsgeschichtliche Untersuchungen zum
phylogenetischen System der Acari: Acariformes Zachv. II. Acaridiae: Acaridae. Mitt.
Zool. Mus. Berlin 35:347-417.
Kniille, W. 1987. Genetic variability and ecological adaptability of hypopus formation in
a stored product mite. Exp. App!. Acaro!. 3:21-32.
Kniille, W. 1990. Genetic and environmental determinants of hypopus duration in the
store-product mite Lepidoglyphus destructor. Exp. App!. Acaro!. 10:231-258.
Kniille, W. 1991. Life-cycle strategies in unpredictably varying environments: genetic
adaptations in a colonizing mite. In: The Acari: Reproduction, Development and Life-
Pp.51-53.
Krantz, G. W. 1978. A Manual of Acarology, 2nd edition. Oregon State Univ. Book
Stores, Corvallis, OR. 509 pp.
Kuo, J. S. and H. H. J. Nesbitt. 1971. Internal morphology of the hypopus of Caloglyphus
mycophagus. Acarologia 13:156-70.
Lindquist, E. E. 1975. Association between mites and other arthropods in forest floor
habitats. Can. Entomol. 107:425-437.
Michael, A. D. 1884. The hypopus question, or the life history of certain Acarina. J.
Linn. Soc. London. Zool. 17:371-394.
Mitchell, R. 1970. An analysis of dispersal in mites. Am. Nat. 104:425-431.
Moser, J. C. and E. A. Cross. 1975. Phoretomorph: a new phoretic phase unique to the
Pyemotidae (Acarina: Tarsonemoidea). Ann. Entomol. Soc. Am. 68:820-22.
Norton, R. A. 1980. Observations on phoresy in oribatid mites (Acari: Oribatei). Int. J.
Acarol. 6:121-130.
Norton, R.A., J. B. Kethley, D. E. Johnston and B. M. OConnor. 1993. Phylogenetic
Diversity of Sex Ratio in Insects and Mites (D. L. Wrensch and M. A. Ebbert eds.)
Routledge, Chapman and Hall, NY. Pp. 8-99.
Oboussier, H. 1939. Beitrage zur Bio10gie und Anatomie der Wohnungsmilben. Z. Angew.
Entomol. 26:253-96.
OConnor, B. M. 1979. Evolutionary origins of astigmatid mites inhabiting stored products.
In: Recent Advances in Acarology, Vo!' 1 (1. G. Rodriguez ed.). Academic Press, NY.
Pp. 273-278.
27:385-409.
Pasteels, J. M., C. Deroe, B. Tursch, J. C. Braekman, D. Daloze, and C. Hootele. 1973.
Distribution et activites des alcaloides defensifs des Coccinellidae. J. Insect Physiol.
19:1771-1784.
Perron, R. 1954. Untersuchungen iiber Bau, Entwicklung und Physiologie der Milbe
Histiostoma laboratorium Hughes. Acta Zool. Stockholm. 35:71-106.
Peterson, P. C. 1975. An analysis of host-parasite associations among feather mites (Acari:
Analgoidea). Misc. Publ. Entomol. Soc. Am. 9:237-242.
Poinar, G. 0., Jr. 1985. Fossil evidence of insect parasitism by mites. Int. 1. Acarol.
11:27-38.
Poinar, G. 0., Jr. and D. A. Grimaldi. 1990. Fossil and extant macrochelid mites (Acari:
Macrochelidae) phoretic on drosophilid flies (Diptera: Drosophilidae). 1. NY Entomol.
Soc. 98:88-92.
Price, P. W. 1980. Evolutionary Biology oj Parasites. Princeton Univ. Press, Princeton,
NJ. 237 pp.
Ricklefs, R. E. 1973. Ecology. Chiron Press, Portland, OR. 861pp.
Samsinak, K. 1971. Die aur Carabus-Arten (Coleoptera, Adephaga) der palaearktischen
Region lebenden Milben der Unterordnung Acariformes (Acari); ihre Taxonomie und
Bedeutung fur die Losung zoogeographischer, entwicklungsgeschichtlicher und parasi-
tophyletischer Fragen. Entomol. Abh. St. Mus. Tierk. (Dres.) 38:145-234.
Stolpe, S. G. 1938. The life cycle of the tyroglyphid mites infesting cultures of Drosophila
melanogaster. Anat. Rec. 72 (Suppl.):133-34.
Timm, R. M. 1983. Fahrenholz's rule and resource tracking: a study of host-parasite
coevolution. In: Coevolution (M. H. Nitecki ed.). Univ. Chicago Press, Chicago. Pp.
225-265.
Tiirk, E. and F. Tiirk. 1957. Systematik und oekologie der tyroglyphiden mitteleuropas.
In: Beitriige zur Systematik Oekologie Mitteleuropiiischer Acarina, Vo!' 1 (H. J. Stam-
mer ed.). Akad., Verlagsges, Leipzig. Pp. 3-231.
Volgin, V. I. 1971. The hypopus and its main types. Proc. 3rd Int. Congr. Acarol.,
Prague, 1971. Pp. 381-383.
Waage, J. K. 1979. The evolution of insect/vertebrate association. Bioi. 1. Linn. Soc.
12:187-224.
Wallace, D. R. J. 1960. Observations on hypopus development in the Acarina. 1. Insect
Physiol. 5:216-29.
Wharton, G. W. 1946. Observations on Ascoschongastia indica (Hirst 1915) (Acarina:
Thormiculidae [Trombiculidae]). Ecol. Monogr. 16: 152-184.
Woodring, J. P. and S. C. Carter. 1974. Internal and external morphology of the deuto-
nymph of Caloglyphus boharti (Arachnida: Acari). 1. Morphol. 144:275-295.
Zachvatkin, A. A. 1941. Fauna ojU.S.S.R., Arachnoidea. Trans!., A. Ratcliff, A. M.
Hughes 1959, American Institute of Biological Sciences, Washington, DC. (In Russian).
573 pp.
11
Cytogenetics of Holokinetic Chromosomes and

Inverted Meiosis: Keys to the Evolutionary
Success of Mites, with Generalizations on
Eukaryotes
Dana L. Wrensch, John B. Kethley and Roy A. Norton
CONTENTS
I. INTRODUCTION
I . I Recombination and Conservation of Genomes: A Preface
1.2 Overview of Genetic Systems and Reproductive Modes of Mites
1.3 Mites Do Things They Shouldn't
1.4 Holokinetic Chromosomes and Cytogenetics
2. PROPERTIES OF HOLOKINETIC CHROMOSOMES AND THEIR
DISTRIBUTION AMONG MITES
2.1 General Contrast of Holokinetic and Monocentric Chromosomes
2.1.1 Structure and Correlated Features
2.1.2 Behavior of Chromosomes in Mitosis
2.1.3 Normal and Inverted Meiosis
2.2 Chromosome Types in Mites: Are They All Holokinetic?
2.2.1 Evidence for Holokinetic Chromosomes in Mites
2.2.2 "Telokinetic" Behavior Is Not Diagnostic of Centromeres
2.2.3 Evidence of Inverted Meiosis in Mites
3. GENETIC RECOMBINATION AND THE SIGNIFICANCE OF IN-
VERTED MEIOSIS
3.1 Recombination, DNA Repair and Evolutionary Success
3.2 Inverted Meiosis as an Explanation for Thelytokous Higher Taxa
3.2.1 Types of Thelytoky
3.2.2 Inverted Meiosis and Terminal Fusion Conserve Maternal
Genome
3.2.3 Sexuality from Thelytokous Ancestors: the Case of the Astigmata
3.3 Diplodiploidy and Inverted Meiosis
3.3.1 What is the Role of Sperm in Mite Life Cycles?
3.3.2 Spermatogenesis and Sex Determination in Diplodiploid Mites
3.3.3 Holokinetic Chromosomes Allow Kinetic Flexibility, Neces-
sary for the Evolution of Sex Chromosomes
3.4 Haplodiploidy and Inverted Meiosis
3.4.1 Spermatogenesis and Sex Determination in Haplodiploid Mites
3.4.2 Haplodiploidy Requires Inverted Meiosis
282
Keys to the Evolutionary Success of Mites / 283
3.5 Inverted Meiosis Affects Recombination Index

3.6 Facultative Recombination by Production of Haploid Males
4. THE BIG PICTURE: HOLOKINETIC SYSTEMS AND THE EVOLU-
TION OF EUKARYOTES
4.1 Distribution of Holokinetic Chromosomes and Inverted Meiosis in
Eukaryotes
4.2 Are Holokinetic Chromosomes and Inverted Meiosis Ancestral in Eu-
karyotes?
4.3 Historical Inertia and the Monocentric Paradigm
5. PROSPECTUS FOR FURTHER RESEARCH
5.1 Empirical Needs
5.2 Mending the Cytogenetic Synthesis
6. SUMMARY
1. Introduction
1.1 Recombination and Conservation of Genomes: A Preface
The evolution of sexual reproduction has seen a recent and major resurgence as
a topic of interest. Many authors (e.g. Ghiselin 1974, Williams 1975, Maynard
Smith 1978, Bell 1982, Shields 1982, Bull 1983, Michod and Levin 1988) have
refined the now-familiar arguments that generally cast sexual reproduction as the
alternative to the asexual production of genetic clones. As theorists have moved
further from the usual cytogenetic models (i.e. humans, mice, fruitflies and
maize), we have learned that the many strange genetic systems and breeding
biologies of plants, animals and protists blur the distinction between "sexual"
and "asexual."
Two focal points have now developed, which weigh the evolutionary pros and
cons of genetic recombination, particularly that occurring at meiosis. (1) Many
authors have focused on the creative role of meiosis, i.e. the provision for genetic
flexibility. In this view, recombinant gametes are considered essential to offspring
success (various individual-selection arguments) or to the long-term success of
lineages (group-selection arguments). (2) Others have considered the conserva-
tion of successful genomes as being the more pervasive and ancient effect of
meiosis ("what is good for the mother is good for the daughter"). In this view,
recombination provides a mechanism for the editing of mutations and the double-
strand repair of damaged DNA (Shields 1982, Bernstein and Bernstein 1991). It
is the latter view that currently has the most momentum. In the "selfish-gene"
paradigm of Dawkins (1976), perhaps the best way to maximize the successful
transfer of genes into the next generation is for a female to produce eggs meioti-
cally, while being in control of recombination.
Our goal in this chapter is to redirect thinking about how genetic systems and
reproductive modes have influenced the tremendous evolutionary success of
mites. We argue that current cytogenetic models leave unresolved questions about
the evolutionary success of thelytokous and haplodiploid mites. In proposing
284 / D. L. Wrensch, J. B. Kethley, and R. A. Norton
new solutions, we focus on the poorly understood properties of holokinetic

chromosomes, and how these properties can influence the control of recombina-
tion. We end the discussion with speculations about the cytogenetic systems of
eukaryotic organisms in general.
1.2 Overview of Genetic Systems and Reproductive Modes of Mites
The Acari are generally recognized as comprising two rather distinct taxa, the
orders Parasitiformes and Acariformes. Each contains taxa of considerable medi-
cal, agricultural, and ecological significance. The many fundamental differences
between these groups have evoked questions about the monophyly of mites that
remain unanswered. In a recent set of papers dealing with the evolution of sex-
ratio patterns in insects and mites (Wrensch and Ebbert 1993), Norton et al.
(1993) synthesized available information on the genetic systems and reproductive
modes of mites (summarized below) and attempted to provide a phylogenetic
context for ideas on the evolution of these traits.
Diplodiploidy, without distinct sex chromosomes, appears to be the ancestral
system in both mite orders. Diplodiploidy is maintained in the Ixodida (ticks),
one of the two major suborders of parasitiform mites, but they have sex chromo-
somes and have mostly XO or XY males. Middle derivative members of the
suborder Mesostigmata (e.g. Parasitidae) retain the ancestral system, but most
higher Mesostigmata are haplodiploid. In the Acariformes, the ancestral system
is the dominant one in the paraphyletic suborder Oribatida; records of possible
haplodiploidy in oribatid mites need confirmation. The Parasitengona (comprising
about half the species of the suborder Prostigmata) has the ancestral system,
while the higher Prostigmata all seem to be haplodiploid. The Astigmata, a
diverse group derived from within the oribatid mites, contains both diplodiploid
(with XO or XY males, or rarely without sex chromosomes) and haplodiploid
groups.
We use the term haplodiploidy in the general sense of Wrensch and Ebbert
(1993, glossary) and Norton et al. (1993). It includes two systems in which males
are impaternate: (1) arrhenotoky, in which males develop parthenogenetically
from haploid eggs; and (2) parahaploidy (also referred to as paternal genome loss
or pseudoarrhenotoky), in which diploid male embryos either undergo expulsion
of the paternal genome at some early stage of embryogenesis (e.g. Phytoseiidae)
or undergo heterochromatization of the paternal genome and retain it in somatic
cells (Otopheidomenidae).
Males of both arrhenotokous and parahaploid species are functionally haploid,
and only two functional sperm are produced per spermatagonium; these two
sperm carry identical halves of the maternal genome. A unique and important
feature of haplodiploidy is that females control the sex ratio of progeny, by
regulating the proportion of males, in response to environmental cues (Wrensch
1993; Sabelis and Nagelkerke 1987, 1993). Clearly both arrhenotoky and para-
haploidy have evolved multiple times in mites, but their evolutionary polarity
remains unresolved.
Thelytoky-the parthenogenetic development of female offspring-has also
evolved multiple times in the Acari, and has been deri ved from each of the sexual
systems noted above. In most higher mite taxa the distribution of thelytoky fits
the theoretical prediction of being phylogenetic ally scattered (Bell 1982). But of
particular interest are sizeable genera, families, or even superfamilies of early
derivative acariform mites (e.g. certain Endeostigmata) and early to middle
derivative oribatid mites that contain no sexual species (Palmer and Norton
1990, 1991; Norton and Palmer 1991; Norton et al. 1993). As discussed next,
explanations for this and other aspects of mite reproductive biology have been
problematic.
1.3. Mites Do Things They Shouldn't
Success in Thelytokes. Theoretical arguments concerning the evolutionary poten-

tial of thelytoky as a reproductive mode usually conclude that thelytoky is a "dead
end" strategy. Depending on one's viewpoint, thelytokes fail because of an
inability to conserve a successful genome faithfully (Manning 1976, Shields
1982), or because they lack the genetic flexibility necessary to survive competition
with sexual species (Ghiselin 1974, Bell 1982) or survive environmental changes
(White 1973, Maynard Smith 1986). The last opinion was recently expressed
quite strongly by Crow (1992), in an attempt to "put the last nail in the coffin"
of thelytoky.
Theoretical considerations derived from evolutionary genetics and cytogenetics
(i.e. Suomalainen 1950, Asher 1970, White 1973, Uyenoyama 1987, John 1990)
predict disaster, through either increasing homozygosity in the various forms
of automictic (meiotic) thelytoky, or increasing mutation load with apomictic
(ameiotic) thelytoky (i.e. the infamous Muller's Ratchet).
Even if thelytokes are not short-term dead ends, as some workers have ac-
cepted, the often unstated conclusion is that they are long-term dead ends-they
should not produce significant evolutionary radiations. The existence of rather
large groups of acariform mites having no sexual species implies the contrary.
These groups are long-lived in evolutionary time and in fact have radiated in a
thelytokous reproductive mode. A similarly large and totally thelytokous group,
the bdelloid rotifers, has been referred to as an embarrassment to evolutionary
theory (Maynard Smith 1986), and the various groups of thelytokous acariform
mites add to the embarrassment.
Origin of a Successful Sexual Clade from Thelytokous Ancestors. One of us
(RAN; Norton and Palmer 1991, and Chapter 5 of this volume) has suggested
that the Astigmata, a predominantly sexual taxon with great taxonomic and
biological diversity, arose from within the oribatid mite clade Trhypochtho-
nioidea. Known species of trhypochthonioids are all thelytokous and the group
286 I D. L. Wrensch, 1. B. Kethley, and R. A. Norton
seems to have radiated in a mode of automictic thelytoky. Thus, not only have
these thelytokes been successful in the long term, but an evolutionary reversal to
sexuality in Astigmata is implied in the relationship.
Success in Highly Inbred Arrhenotokes. In theory, the reproductive advantages
of arrhenotoky are well understood. Relative to diplodiploids, arrhenotokes ex-
hibit extraordinarily rapid adaptive response to changes in environmental selection
factors (Griffing 1982), at least in part because deleterious alleles cannot "hide"
in the genetically "naked" male (Huxley 1942, Nur 1971). Indeed, in the theory
of local mate competition (Hamilton 1967) arrhenotoky plays a central and crucial
role. However, evolutionary theory predicts that highly inbred arrhenotoky (HIA)
systems should not be very successful, as they are driven to homozygosity and
lose genetic flexibility (Futuyma 1986).
This negative perception of HIA contrasts with the widespread existence of
such systems in very successful groups of mites. For example, Kethley (1971)
found that populations of an arrhenotokous mite inhabiting bird quills are founded
by a single mated female whose progeny consist of a single son and II daughters.
Sib-mating occurs and the second generation in the quill mirrors the first, by a
multiple of 11: one son and II daughters per mother. At maturity, second
generation females mate with their brothers or closer-than-first cousins and then
disperse to newly developing quills. Although quill mites represent an extreme
example of HIA, the group is quite diverse morphologically and taxonomically
(Kethley 1970, Kethley and Johnston 1973). Many Heterostigmata have obligate
sib-mating; these have a variety of life styles, and include plant feeders (e.g.
Polyphagotarsonemus latus, Flechtmann and Flechtmann 1984) and insect para-
sites (e.g. Pyemotes ventricosus, Swan 1934; Adactylidium sp., Elbadry and
Tawfik 1966). Niche constraints alone tend to ensure sib-mating in the microhabi-
tats of many species. Examples include the heterostigmatid mites that parasitize
insect respiratory systems-such as those of honey bees (Acarapis woodi, Smith
1990) and ladybird beetles (Podapolipidae, Husband 1972)-or that are commen-
sals in insect nests (e.g. Sicilipes costaricanus, Rack and Eickwort 1979). The
same is true of the economically important gall mites (Eriophyidae, de Lillo
1991).
All these mites are arrhenotokes with female-biased sex ratios, and all disperse
exclusively as inseminated females. Such attributes combine to yield highly
inbred populations. In mites, HIAs are not only unexceptional but are, in fact,
the norm in parasitic (highly derived) species-another "embarrassment" to evo-
lutionary theory.
1.4. Holokinetic Chromosomes and Cytogenetics
Below we suggest that these "embarrassments," and other interesting aspects of

mite biology, are embarrassments not to evolutionary theory, but to the current
cytogenetic paradigm. Indeed, they may prove easily explained in light of the
widespread, if not universal, possession of holokinetic chromosomes by mites.

The unusual features of holokinetic chromosomes during mitotic and meiotic
divisions are well known from extensive research on the Heteroptera (e.g.
Hughes-Schrader 1948, Brown and Nur 1964), Lepidoptera (Suomalainen 1953)
and plants such as Luzula (Nordenskiold 1962). However, their attributes are
not widely known except by specialists in cytogenetics, and the evolutionary
consequences of a holokinetic genetic system have been neglected.
In part, this lack of interest may stem from poorly founded generalities. For
example, White (1973, 496) proposed that single locus genetics should be the
same in monocentric or holokinetic organisms. But he also realized that something
significantly different might be occurring in holokinetic systems: "differences
between meiotic mechanisms in various groups with holocentric chromosomes
and in organisms with monocentric chromosomes may be vitally significant from
the standpoint of chromosome evolution." John and Lewis (1965, 142) had also
realized previously that certain cytogenetic concepts formulated for monocentric
chromosomes were not strictly applicable to holokinetic systems, or would have
different implications, but they did not specify what these distinctions might be.
In this chapter, we will attempt to do so.
2. Properties of Holokinetic Chromosomes and Their Distribution

among Mites
2.1. General Contrast of Holokinetic and Monocentric Chromosomes
2.1.1 Structure and Correlated Features
Holokinetic chromosomes are distinctive because during cell division they

behave as if the spindle attachment is not localized. Such chromosomes are also
denoted as holocentric or diffusecentric, or are described as having a nonlocalized
or diffuse centromere or kinetochore. Ultrastructural studies on the spider mite
Tetranychus urticae showed spindle microtubules to have points of attachment
extending across the entire length of the holokinetic chromosome (Templaar
1980).
Generally, holokinetic chromosomes are small (1-3 /Lm) and stain uniformly
along their whole length. Thus, one of their distinguishing traits is the absence
of the differentially staining primary constriction that marks the classic centromere
of monocentric chromosomes. Holokinetic chromosomes lack a true kinetochore
(i.e. a trilaminar disk, BaIczon and Brinkley 1990), although a faint, subterminal
constriction is sometimes seen, indicating the site of a nucleolus. We adopt the
term "holokinetic" to describe such chromosomes since it is properly descriptive
without implying the presence of a centromere, as the alternative and rather
oxymoronic term "holocentric" does. Also, "holokinetic" is currently the term
preferred by cytologists (e.g. John 1990) and acarological cytogeneticists (e.g.

Helle et al. 1984).
Holokinetic chromosomes may co-occur with unusual cytological features.
Cells typically show cask-, barrel-, or cylindrical-shaped spindles (Fig. 11.1)
which have been described as anastral (Schrader 1953, White 1973). Anastral
spindles are associated with centro somes lacking a centriole but possessing intra-
nuclear spindles (Kubai 1975). Not all taxa with holokinetic chromosomes lack
centrioles, however (e.g. hemipteran spermatogenesis, Hughes-Schrader and
Schrader 1961; see Peterson and Berns 1980 for general review).
In holokinetic systems, the nuclear membrane typically does not disintegrate
until late telophase in mitosis, or late prometaphase I in meiosis. Instead of
kinetochores and localized centromeres that connect by micro tubules to centriole-
based centrosomes, holokinetic chromosomes use a "primitive" spindle apparatus
(Heath 1980). Individually or in groups, holokinetic chromosomes are packaged
in membranes called karyomeres; these are functionally distinct from micronuclei,
which mayor may not contain chromosomes or chromosome fragments.
The absence of a localized centromere featuring a true kinetochore appears to
be linked to the absence of a pair of centrioles in a bipolar spindle arrangement.
The association of holokinetic chromosomes with persistent nuclear membranes
enables them to orient in a fundamentally different pattern than do monocentric
chromosomes in kinetochore-centriole spindle systems (see Section 2.1.3).
Another important difference between holokinetic and monocentric chromo-
somes is their response to irradiation-induced fragmentation. For holokinetic
chromosomes, diffuse kinetic activity during mitosis means that fragments are
not'llecessarily lost during cell division, and such chromosomes have "sticky
ends" by which breaks can be repaired. Fragments are more numerous in cleavage
nuclei than in meiotic figures and can persist for at least four or five consecutive
cleavage mitoses (e.g. Cooper 1972). This has been interpreted as greater "heal-
ing" capacity during the relatively much longer premeiotic interphase and pro-
phase I than is possible in the rapidly mitotically dividing nuclei and cells of early
embryogenesis. The ability of holokinetic chromosomes to fragment and fuse is
well known (Hughes-Schrader and Ris 1941, Brown and Nelson-Rees 1961,
Chandra 1962, Evans and Pond 1964, LaChance et al. 1970, Jones 1978, Tem-
plaar 1979b, Ueshima 1979), and it has both diagnostic value (Section 2.2) and
evolutionary significance (Section 4.2).
2.1.2 Behavior of Chromosomes in Mitosis (Figs. 11.1,11.2)
During mitotic metaphase (Fig. 11.1), only the centromere of monocentric

chromosomes-more precisely the kinetochore, if such a structure is present-
is strictly on the equator. In contrast, the entire holokinetic chromosome is
situated on the equatorial plate and is involved in relative positioning between
the poles (Helle et al. 1984). Furthermore, the whole holokinetic chromosome
....- ......
HOLOKINETIC CHROMOSOMES
No primary constriction
MONOCENTRIC CHROMOSOMES
Ill",
Primary constriction = centromere
METAPHASE
Complete chromosomes align' , \ !

SPINDLE EQUATOR
Microtubules (MTs) attached

along entire chromosome ~
• • u: ANAPHASE
Barrel- or cask-shaped spindle

with some bending of chromosome Bipolar spindle with centromeres
ends toward centrosomes. converging at poles before
chromosome arms.
Figure 11.1. Schematic comparison of chromosome behavior for holokinetic and mono-
centric chromosomes during mitosis.
289
B.
A'~I~
2n = 6 II Metaphase,
polar view 2n =18
J.
SPINDLE
Polar view rotated 30°,
~l 2n = 6 n =3
opening of rosette
Q d
~dJ~ .......... .
D.
~'.~~~
+ Early Anaphase
2n =4
,,", ".........;;;;
... /
i~,.,'\
,,' "',
....
\
E.
II""'''='''''''''':;'~
\. ,
...... ..... ..
'
,- ....
........ ....
SPINDLE EQUATOR
Anaphase,
lateral view
Figure 11.2. Schematic holokinetic chromosome fonnations during mitosis. A) A "ro-
sette," a distinctive metaphase polar fonnation seen in parasitifonn mites. Our interpreta-
tion is presented with white-hatched lines to represent terminal end-to-end associations
between nonsister chromosomes. Internal attachments of chromosome ends are interpreted
as stickiness caused by the nucleoli adhering together. This orientation is notable in
metaphase karyotypes in phytoseiid mites (in Nelson-Rees et al. 1980, vide Figs. 8,9,
and 12 and in Wysoki and Swirski 1968, vide Figs. 5, 6, 9, 10), in both diploid and
290
lies within the spindle, whereas chromosome arms of monocentric chromosomes

can lie outside in peripheral locations (White 1973, his Figs. 2.3d, c). When
limited space is available within the spindle on the metaphase plate, holokinetic
chromosomes often become arranged in geometric configurations that are not
found in monocentric chromosomes (Fig. 11.2B, II.C; see also Taberly 1987,
Figs. 14-16; Helle et al. 1984, Figs. 1-16). During mitosis (but not necessarily
meiosis), holokinetic chromosomes show a pattern of microtubule attachment
along the entire poleward surface (Templaar 1985, White 1973) (Fig. ILl,
anaphase).
At anaphase, holokinetic chromosomes separate and remain more or less
parallel to the equator, and perpendicular to the spindle axis, as they move
toward the poles (Fig. 11.1, anaphase). However, relatively long holokinetic
chromosomes-or even shorter ones in late anaphase-may bend the pole as they
near it, resulting in distinctly bent (V -shaped) or hooked (J-shaped) chromosome
figures (Fig. 11.1, telophase, see also Fig. 11.2E). According to Helle et al.
(1984) this effect is due to a relaxation of chromosome condensation, i.e. they
undergo despiralization.
Such shapes have been misinterpreted by some mite cytogeneticists as evidence
for the presence of localized centromeres, since monocentric chromosomes com-
monly show inverted V-, or J-shaped forms when the arms lag, as chromosomes
Figure 11.2 Continued haploid somatic nuclei. Using our interpretation, it is obvious
that the rosette readily enables total segregation of one chromosome set from the other.
As metaphase proceeds to anaphase (second figure from the top, rotated about 30° into
plane of figure), the rosette opens into a star-like chain of alternating homologous sister
chromatids. In the third figure down, sister chromatids disjoin in early anaphase, and
their alternating sequence in the chain creates complete segregation of the two sets of
chromosomes. The bottom figure shows late anaphase with the two sets completely
separated. These four sequences present a cytological mechanism through which para-
haploid reproduction (paternal genome heterochromatization or elimination) in phytoseiids
and other mesostigmatids can thus be understood. This mitotic phenomenon is, we believe,
functionally equivalent to meiotic segregation distortion created from ring or chain forma-
tions (i.e. segmental interchange complexes, Syren and Luykx 1977; translocation hetero-
zygotes, John 1990). B) Polar view of metaphase featuring an Oppia species (schematic
drawing of photo in Helle et al. 1984, vide Fig. 1). In acariform mites, holokinetic
chromosomes do not seem to align in rosette formation, but create regular geometric
patterns. Linkages between the ends of uniformly rod-shaped chromosomes create threads
forming chains or rings of chromosomes. C) Polar view of metaphase of diploid (left) and
haploid (right) tetranychid karyotypes (redrawn from photos in Helle et al. 1981, vide
Figs. 14 and 18 each having 2n = 6 as a ring of 4 + 2, and Figs. 16, 17 and 22 for n =
3). D) Lateral view of metaphase of Eylais setosa (redrawn from Key! 1957, vide Fig. 4).
Metaphase in holokinetic chromosomes features separate spindles for each duplicated
chromosome. E) Longer holokinetic chromosomes may exhibit a concentration or restric-
tion of kinetic behavior to one end, so that the chromosomes show telokinetic behavior
(Key! 1957, vide Fig. 5).
move poleward at anaphase. Clearly it is not bending alone that is diagnostic,

but rather the direction of the bend: away from the poles in monocentric chromo-
somes, but toward the poles in holokinetic chromosomes. Similar misinterpreta-
tions have been associated with "end-on" or "telokinetic" movement of rod-
shaped chromosomes in anaphase, as discussed below (Section 2.2.2).
2.1.3 Normal and Inverted Meiosis (Fig. 11.3): The Importance of Bivalent
Orientation at Metaphase I
An essential difference between meiotic behaviors ofholokinetic and monocen-

tric chromosomes lies in their orientation at metaphase 1. Whether they are axial
or equatorial with reference to spindle coordinates has a profound effect on the
sequence of the two meiotic divisions.
In monocentric systems, disjoining half-bivalents are dyads that consist of
sister chromatids held together by their centromeres (Fig. 11.3, left column).
Centromeres of monocentric bivalents show co-orientation, i.e. the centromeres
of the two homologues are in a line parallel to the spindle axis and equidistant
from the equator. Co-orientation is thus an axial orientation of homologous
chromosomes with reference to spindle coordinates. The presence of a kineto-
chore constrains synaptic monocentric chromosomes to this co-orientation, forc-
ing the duplicated maternal homologue to separate (disjoin) from the duplicated
paternal homologue at anaphase I (Fig. 11.3). Thus, the first meiotic division in
axially aligned bivalents is reductional for loci in noncrossover regions (Rhoades
1961). A schematic representation of what such a "normal" meiosis would look
like in a holokinetic system is shown in the central column of Fig. 11.3, but there
is little evidence that this occurs naturally (see Section 2.2.3).
Cytogeneticists have realized for some time that an inverted meiotic sequence-
an equational division preceding the reductional division-is strictly possible
only in organisms with holokinetic chromosomes (Battaglia and Boyes 1955,
Rhoades 1961, Brown and Cleveland 1968, Jones 1978). Only holokinetic chro-
mosomes are capable of an equatorial orientation of homologues at metaphase I
(Fig. 11.3, right column), in which the alignment of homologous chromatids is
rotated 90 0 relative to that of normal meiosis. This orientation causes equational
segregation of half-bivalents at anaphase I: sister chromatids separate while
maternal and paternal homologues remain paired.
As discussed later (Section 4.2) we believe inverted meiosis to be ancestral in
ho10kinetic systems. In such systems, a "normal," reduction-first sequence is
unequivocally present only during spermatogenesis in some heteropteran insects
(but meiosis is inverted in oogenesis); it is associated with the presence of sex
chromosomes (Section 2.2.2, see also 3.3.3). A reductional first division of
holokinetic chromosomes in oogenesis has been claimed but never proven in
naturally occurring populations (see Section 2.2.3, and Ueshima 1963 for discus-
Keys to the Evolutionary Success of Mites I 293
FIRST MEIOTIC DIVISION

Orientation of Bivalent (Tetrad)
at MET APHASE I
NORMAL MEIOSIS INVERTED MEIOSIS
Reductional Division Equational Division
(= axial orientation) (= equatorial orientation)
Monocentric Chromosomes Holokinetic Chromosomes Holokinetic Chromosomes
..-.~..... .................. .....\

"
equatorial plane
Duplicated homologues separate Sister chromatids separate
SECOND MEIOTIC DIVISION

Equational Division Reductional Division
'.. (--e'.--"
........... )st polar nucleus (PN) __ ._.. L. __
\.H.I \
": . ~ ) 1st PN
::::= ..... " i
'.~--. -~---/
J
~ ............... "'\ ( _____"" ~/r----'",
~liC\'(
< 'I ~~! /i
'.. / , " "
2nd PN ~'....... .//
2nd PN r····· ovu~""" ~~

Sister chromatids separate
Homologous (non-sister) chromatids separate
• MatemalChromatid
• PatemalChromatid
Figure 11.3. Meiosis: oogenesis with monocentric and holokinetic chromosomes.
sion). The only conclusive evidence involves experimentally created hybrids in

the hemipteran genus Cimex (Ueshima 1963).
The unique attributes of inverted meiosis are summarized next, with comments
that are relevant to any oogenesis, whether "sexual" or thelytokous; special
attributes of spermatogenesis are discussed later (Sections 3.3, 3.4).
Inverted Meiosis in Holokinetic Systems-Oogenesis in organisms with holoki-
294 / D. L. Wrensch, 1. B. Kethley, and R. A. Norton
netic chromosomes is usually described cytologically as consistent with key

features in monocentric species. One or more chiasmata are seen at diplotene.
By prometaphase I these chiasmata are described as terminal. Meiotic distinctions
between holokinetic and monocentric systems begin at metaphase I, where holoki-
netic bivalents are observed to orient with the long axis of the bivalent parallel
to the spindle's equator. This cytological orientation reflects the end-to-end
association created by telomeric pairing (Fig. 11.4B-C, Jones 1978). However,
there may be a subsequent adjustment in orientation, so that the homologues lie
side-by-side in a parallel position (Fig. II.4F, also see Schrader 1940).
Unlike monocentric bivalents, there is no repulsion between holokinetic homo-
logues (Swanson 1957,341). At diplotene/diakinesis, bivalents with one chiasma
have a cross-shape (Fig. 11.4E), while bivalents with two chiasmata form a ring
(Fig. 11.5). The cross-shape resolves into the end-to-end association, termed a
half-bivalent (Fig. 11.4F). A ring forms when both ends of each homologous
pair are attached to the nuclear membrane and both form a telomeric heteroduplex.
When the nuclear membrane disintegrates, these chromosome-membrane associa-
tions are released and as chromosome condensation intensifies in diakinesis the
cytological cross, rod, or ring shapes become visible (e.g. Hughes-Schrader
1955).
Most holokinetic chromosomes show the effects of one terminal chiasma. This
feature is the mechanical cause of equational division during the first meiotic
division and is not known to occur in monocentric chromosomes, or it occurs
only for exceptional chiasmata configurations (White 1973, John 1990). The
terminal chiasma in holokinetic chromosomes does not result in the recombination
of functional genes.
At anaphase I, equatorially oriented holokinetic bivalents separate as half-
bivalents that consist of two nonsister chromatids. These half-bivalents move
toward their respective poles with the secondary or interchromatid split (usually
the long axis) of each half-bivalent parallel to the equator (Fig. 11.3). Chromatids
separating during mitotic anaphase have a similar appearance. The half-bivalents
may bend somewhat late in anaphase I, at one or both ends. When both ends
curve, as in mitotic anaphase, the curvature is opposite that commonly seen in
monocentric chromosomes (Fig. 11.1, telophase).
Restriction or concentration of microtubules at one end of the chromatid in a
half-bivalent can cause "telokinetic" behavior (see Section 2.2.2) during anaphase
I (Fig. 11.5), but this behavior does not negate equational segregation of the half-
bivalents. When, through hybridization, bivalents form between morphologically
dissimilar homologues, the end associations are weaker or fail to form at all (Fig.
11.5C). The resulting reductional segregation at anaphase I is a mechanical
consequence of half-bivalent instability.
The second meiotic division in inverted meiosis is reductional, so that nonsister
chromatids separate to the second polar nucleus and to the egg pronucleus.
A pair of homologous, holokinetic chromosomes
Nuclear membrane
~ A. B. c.
"'.....
Nuclear membrane SC breaking down
disintegrating mi-
--
---+-
D.
E.
Figure 11.4. Holokinetic chromosome replication (A, B) and formation of bivalents by

end-to-end pairing (C-F), the basis for inverted meiosis. A) Chromosome ends imbedded
in nuclear membrane (or in karyomere membrane). B) DNA replicates, homologous
telomeres adjacent. C) Synaptemal complex (SC) forms. D) Tetrad forms bivalent, te-
lomeric DNA synthesis delayed past pachytene, telomeric DNA heteroduplex links te-
lomeric ends of nonsister chromatids. E) At diakinesis, telomeric synthesis completed,
chromatids align so that telomeric ends of paired homologous chromatids are central within
each "half-bivalent". F) Chromosome condensation with the "end-to-end" associations
that enable an "equitorial" orientation and equational segregation at metaphase I. Each
half-bivalent consists of one copy of each of the original homologous chromosomes. Half-
bivalents may fold over or shift into parallel alignment, vide Ris J942, Brown J977. Note:
a monocentric chromosome cannot perform this pattern of orientation. The kinetochore is
replicated in premeiotic interphase, but its centromeric DNA replication is delayed. Thus
in prophase I, sister chromatids are connected at the centromeric DNA region. Their
formation at premetaphase is governed then by microtubule (MT) attachments from the
centrosome to each chromosome's centromere (kinetochore MTs). Therefore, orientation
becomes axial and division is reductional because the forces due to telomeric kinetic
activity are overwhelmed by forces of kinetochore MTs.
295
Equational
Separation
at Anaphase I
Reductional
Separation
at Anaphase I
+
B.
. . ·. ·. ·. . .11·······. . · · · ·.
at
........................................................
Equational
Separation
If+
at Anaphase I
c.
.. .:................................. .
~r
Reductional
Separation
--+
at Anaphase I
Figure 11.5. Orientation and kinetic behavior of bivalents of holokinetic chromosomes.

A) Ring bivalent forms when both ends of each homologous chromatid form attachments
to the nuclear membrane. Rings may orient so that segregation is either equational or
reductional (vide Suomalainen and Halkka 1963). B) Telokinetic behavior at anaphase I
of rod-like bivalent of holokinetic chromosomes, as in female spider mites (redrawn from
Fig. 4, Schrader 1923). C) Schematic bivalent of heterologous chromosomes in which
reductional segregation at metaphase I (vide Ueshima 1963) is caused by failure of end-
to-end associations to form properly.
296
2.2 Chromosome Types in Mites: Are They All Holokinetic?
2.2.1 Evidence for Holokinetic Chromosomes in Mites
The most crucial test for a diagnosis of holokinetic chromosomes involves

inducing fragmentation of chromosomes by irradiation and studying their behavior
during subsequent cell divisions. The persistence of fragments in descendant cell
lineages is viewed as the most direct confirmation that a localized kinetochore is
not present (Cooper 1972, Hughes-Schrader and Schrader 1961). Such holoki-
netic behaviors have been confirmed in species of several groups of Prostigmata,
including water mites (Keyl 1957), spider mites (Templaar 1979 a, b), and the
Heterostigmata (Cooper 1972).
As noted above, there is a correlation between the lack of centrioles and
holokinetic chromosomes. Among mites, the absence of centrioles from the
spindle apparatus has been noted during cleavage (Siteroptes (= Pediculopsis)
graminum, Cooper 1939) and during meiosis (i.e. Caloglyphus mycophagus,
Heinemann and Hughes 1970; Histiostomaferoniarum, Heinemann and Hughes
1969; Demodex sperm, Desch 1984; and Eriophyidae sperm, Nuzzaci and Solinas
1984). Unfortunately most authors are silent as to the presence or absence of
centrioles, and we have no such information for other major mite groups. Karyom-
eres, associated with holokinetic chromosomes, have been observed in acariform
mites-such as Heterostigmata (Reuter 1909, Piitau 1936, Cooper 1939), Tetra-
nychidae (Templaar and Drenth-Diephuis 1984, Feiertag-Koppen and Pijnacker
1985), Tenuipalpidae (Pijnacker et al. 1981)-and in ticks (i.e. Ornithodoros
papillipes; Sokolov 1958).
We interpret all literature descriptions of chromosomes in acariform mites as
clearly relating to holokinetic chromosomes (Schrader 1923, Piitau 1936, Cooper
1939, Key11957, Moss et al. 1968, Cooper 1972, Helle et al. 1981, Helle et al.
1984, Taberly 1987). The papers by Schrader, Piitau, K. Cooper and Keyl are
also exceptional because they assess meiosis in both females and males, and they
provide spectacularly clear illustrations. The study of oogenesis is technically
difficult (White 1973), and we are fortunate to have excellent papers on oogenesis
in tetranychoid (Schrader 1923, Feiertag-Koppen and Pijnacker 1985), tarso-
nemid (Piitau 1936, Cooper 1939), astigmatid (Heinemann and Hughes 1969,
1970) and oribatid mites (Taberly 1987).
The interpretation of chromosome types in Parasitiformes is more equivocal.
Among Mesostigmata, six species ofParasitidae were studied by Sokolov (1934),
who concluded that chromosomes seen in spermatogenesis were holokinetic
("diffusecentric"). Oliver (1967) used the terms cephalobrachial or diffusecentric
in describing the chromosomes of Ornithonyssus, Ophionyssus and Bdellonyssus
spp., noting that no centromeres (i.e. primary constrictions) were seen. Oliver
and Bremner (1968) explicitly stated that both holokinetic and monocentric
chromosomes were found in Haemaphysalis tick species. In other reviews, Oliver
298 / D. L. Wrensch. 1. B. Kethley. and R. A. Norton
(1967, 1977) has described the autosomes of different tick species as having
terminal centromeres, or as being acrocentric or cephalobrachial.
At least in part, reluctance to accept a holokinetic diagnosis for parasitiform
mites stems from interpreting the "telokinetic" behavior of chromosomes during
meiosis as being evidence of centromeres. As we explain next, holokinetic
chromosomes can show the same behavior.
2.2.2 uTelokinetic" Behavior Is Not Diagnostic of Centromeres
In monocentric systems, rod-shaped half-bivalents may appear to move "end-

on" toward the poles at anaphase I, i.e. to have "telokinetic" behavior (Fig.
11.5B). When the presence of a terminal centromere is assumed, the term "telo-
centric" is applied, but the eminent animal cytogeneticist M. J. D. White (1973)
strongly rebuked the notion of naturally occurring telocentric chromosomes. He
insisted that chromosomes exhibiting this behavior be described as acrocentric-
having a nearly terminal centromere-even if lacking a primary constriction.
Most cytogeneticists apparently adopted his preference, and considered any end-
on or poleward orientation as prima facie evidence for acrocentric chromosomes,
whether a subterminal primary constriction was seen or not.
Thus, autosomes are invariably described as cephalobrachial or telocentric in
ticks (Oliver 1964) and acrocentric in Phytoseiidae (e.g. Wysoki and Swirski
1968, Nelson-Rees et al. 1980), even though no primary constriction has been
observed. In fact most of the terms applied to parasitiform chromosomes-
acrocentric, cephalobrachial, subterminal or telocentric-imply the presence of
a centromere, though the preeminent student of parasitiform cytogenetics, J.
Oliver, has exhibited exceptional caution in this regard. Most such diagnoses
were based simply on finding rod-shaped chromosomes that show an end-on
orientation.
Ambiguity arises from the fact that holokinetic chromosomes can exhibit a
similar behavior during meiosis (Fig. 11.5). In mitosis, holokinetic chromosomes
show relatively uniform kinetic activity along their length. However, in the highly
condensed condition at meiosis, kinetic activity can be concentrated terminally
and an end-on appearance is generated. The elegant work of Hughes-Schrader
and Schrader (1961) on Heteroptera demonstrated this ability to have diffuse
and restricted kinetic activity in mitosis and meiosis, respectively. Examples of
"telokinetic" behavior in holokinetic chromosomes of mites are well known
(e.g. Keyl 1957, Heinemann and Hughes 1970, Cooper 1972). Adding to the
confusion, chromosomes are almost always characterized during meiotic events
(i.e. spermatogenesis), when monocentric chromosomes and holokinetic chromo-
somes can exhibit similar "telokinetic" behavior.
The lack of a primary constriction in parasitiform mite chromosomes suggests
they may be holokinetic. Their "telokinetic" behavior is consistent with such a
diagnosis, but there is other evidence. For example, the metaphase arrangements
of examined parasitiform mites differ little from those seen in karyotypes that are
unambiguously holokinetic. At mitotic metaphase, phytoseiid (Nelson-Rees et
al. 1980) and dermanyssid (Oliver 1965) chromosomes form a rosette in polar
view (Fig. 11.2A), with the rod-like chromosomes arrayed like spokes on a wheel
around a clear center. This exact formation is typical of mitotic metaphase figures
in spiders (Benavente and Wettstein 1980) and Ephemeroptera (Kiauta and Mol
1977) that are clearly holokinetic.
Also supportive of a holokinetic diagnosis in the parasitiform mites are certain
parallels that exist with cytogenetically better known insects having holokinetic
chromosomes. Males of Hemiptera (Hughes-Schrader and Schrader 1961) and
males of some Homoptera (Ris 1942) have normal meiosis (a reductional first
division). The end-on configuration of their large holokinetic sex chromosomes
is very similar to that seen in tick spermatogenesis, for which chromosomes were
diagnosed as cephalobrachial or telocentric (Oliver 1964, 1965). Even more
compelling, karyotypes of Hemiptera, like those of ticks, are conspicuously
heteromorphic, and have XY or XO males. The X is usually much larger than
the autosomes, which show very little size difference.
Parallels also exist between parahaploid phytoseiid mites and parahaploid
Homoptera that are known to have holokinetic chromosomes. The photomicro-
graphs in Nelson-Rees et al. (1980) showing chromosome heterochromatization
and elimination in a phytoseiid mite, and the detailed drawings of Warren (1940)
for Dermanyssus, coupled with the sketches of Oliver (1965) which also show
elimination, are strikingly similar to the system described for diaspidid scale
insects (i.e. Brown and DeLotto 1959, Brown and Nur 1964). Even the formation
of sperm-the evagination of the binucleate spermatid's membrane and slender
elongation to form two functional sperm-looks amazingly similar, yet is un-
known outside these two groups of organisms (compare Figs. 42-53 in Nelson-
Rees et al. 1980 with figures in Brown and Nur 1964). Tantalizingly, Treat's
(1965) description and photomicrographs of the "comma" in cells in the somatic
and spermatogonial nuclei of the moth ear mite (Otopheidomenidae) suggest a
system of parahaploidy comparable to the system of holokinetic lecanoid scales
(Brown and Nelson-Rees 1961, Brown and Nur 1964).
2.2.3 Evidence of Inverted Meiosis in Mites
Over the last three decades much data has accumulated on karyotypes of mites
(mostly spider mites and ticks), but little attention has been paid to meiotic
mechanisms. Thus, little evidence exists for determining the order in which
meiotic divisions occur in various groups. The lack of evidence for anything
unusual has meant that cytogenetic dogma generally has gone unchallenged (Helle
et al. 1984) .
The order of division in a holokinetic system is often difficult to diagnose from
meiotic figures. A cytological diagnosis of normal or inverted meiosis is based
on the orientation of bivalents relative to the spindle at metaphase I, axial or

equatorial, respectively (Section 2.1.3, Fig. 11.3). This can be directly observed
when chromosomes are rod-shaped, but becomes equivocal as they approach a
highly condensed isodiametric form, and as individual chromatids lose their
distinctiveness (Ueshima 1963).
With no heteromorphic bivalents, or with all the autosomes appearing similarly
small and spherical to rod-shaped, a reductional first division may be mistakenly
inferred from the telokinetic behavior. Above, we noted that end-on telokinetic
behavior of chromosomes is not diagnostic of the presence of a centromere. As
an extension, it is not diagnostic of a reductional first division. In inverted
meiosis, holokinetic chromosomes form half-bivalents that are comprised of
end-to-end associations of nonsister chromatids. Their contact region can be
differentially constricted, and their telokinetic behavior mimics classic reduc-
tional division of telocentric chromosomes. Since the genetic consequences of
these convergent behaviors are so different, we must be careful in our interpreta-
tions of such meiotic figures (e.g. see our discussion of Taberly's work with
thelytokous oribatid mites, Section 3.2.2).
When chromosomes are small and spherical, elongated ones may be artificially
created during the irradiation procedures used to diagnose holokinetic chromo-
somes. The chromosomes and fragments produced may fuse, resulting in an
artificially elongated morphology that can provide evidence of orientation. In
mites, the only such unequivocal evidence of inverted meiosis is from the Tetra-
nychidae (Templaar 1979a, 1979b, 1980, 1985; Templaar and Drenth-Diephuis
1984).
Indirect evidence of inverted meiosis has been observed in another arrhenotoke,
the heterostigmatic mite Siteroptes (= Pediculopsis) graminum. In the tetrany-
chids, the tandem arrangement of homologous chromatids undergoes a further
modification resulting in their parallel alignment (Fig. 11.4F). Based on Cooper's
(1939) original observations, Schrader (1940) noted the same configuration in S.
graminum.
In the unusual thelytokous tenuipalpid Brevipalpus obovatus, inverted meiosis
is the only conclusion consistent with four observations of Pijnacker et al. (1981):
(1) the karyotype consists of two heterologous chromosomes; (2) the automictic
mechanism is by pre meiotic doubling; (3) the latter allows the formation of two
autobivalents; and 4) after meiosis the heterologous somatic number is restored
(Fig. 11.6). The latter configuration could only be achieved by segregation of the
homologous chromatids of each member of the heterologous chromosome pair,
which in tum could only result from equatorial orientation and equational segrega-
tion, the essential features of inverted meiosis (Fig. 11.3). Any other orientation
would cause sister chromatids to segregate at anaphase 1. The restored karyotype
would then consist of two homeomorphic rather than heteromorphic chromo-
somes, and a dysfunctional aneuploid egg would result.
1. Heterologous Pair, n = 2 2. Premeiotic Doubling

3. Meiotic Interphase,
Chromosomes Double Again 1111III1
4. Two Autobivalents
Form at Metaphase I
C> ~
~
5. Equational
Segregation
c::>
.t··c::>C
.. ···············
t::J
at Anaphase I
6. Reductional
Segregation ........................ ....................... ....
7. Four Meiotic
Products, All
Identical and
@~~
at Anaphase II I::P~')
C;~~@~
Equivalent
to Maternal Genome
Figure 11.6. Mechanism for genetically faithful thelytokous production of Brevipalpus

females with n = 2, a heterologous pair of holokinetic chromosomes.
All the above-mentioned taxa are acariform mites; the only claim of inverted
meiosis in parasitiform mites was by Oppermann (1935), who suggested an
inverted sequence during spermatogenesis in the tick Argas refiexus. Opper-
mann's conclusions were questioned by Goroshchenko (1962), but since we now
believe tick chromosomes to be holokinetic the process needs to be reexamined;
it appears to us that Oppermann was correct.
3. Genetic Recombination and the Significance of Inverted Meiosis
3.1 Recombination, DNA Repair and Evolutionary Success
The cytology of inverted meiosis has been explored in both plants and animals
(Hughes-Schrader 1948, Resende 1953, Chandra 1962, White 1973, John 1990)
but the cytogenetic consequences-for thelytokous organisms and haplodiploid
organisms in particular-have been completely overlooked.
Any organism's genetic system has itself evolved, and reflects selection for
properties that provide it with a balance between: (1) genetic stability that main-
tains high fitness; and (2) genetic flexibility that provides the variation associated
with adaptation. Whether flexibility is "purposeful" or not is contentious. Balance
is achieved through a series of trade-offs among the various elements comprising
the genetic system (Darlington 1939, Lewis and John 1972). Thoday (1953)
understood natural selection to be acting on "units of evolution" where fitness is
"compounded by stability and variability, and increase in fitness becomes a

resolution of the antagonism between stability and variability." He further viewed
the resolution of this classic conflict as "brought about either by changes of the
genetic system that increase the amount of cryptic genetic variation, or by increase
of the range of environmental conditions to which the individual is adaptable or
adapted, or by adaptation to a stable environment."
Genetic stability is obtained through mechanisms in the genetic system that
reduce or eliminate recombination of parental genotypes. As Darlington (1939)
stated "Indeed, the history of the evolution of genetic systems may be regarded
as the history of the control of recombination."
Components of the genetic system involved in recombination control include
chromosome number, mode of reproduction, and breeding system. Mites are
conspicuous among all animals for their generally low chromosome numbers
(Oliver and Nelson 1967) and they show a diversity of the latter two components.
The relationship of mode of reproduction and cytology (chromosome systems,
modifications of meiosis) to the control of genetic recombination has not been
explored in mites, but in general it is under genetic control (White 1973, Bell
1982, John 1990). The modes of reproduction known in mites span the ends of
a continuum from obligate thelytoky to haplodiploidy with obligate sib-mating,
the extreme HIA system. But from the perspective of recombination control,
obligate thelytoky and HIA are functionally equivalent. The success of HIA
systems, and the adoption of thelytokous parthenogenesis by mite lineages that
are both ancient and widely distributed (Section 3.2) appears to contradict the
traditional notions of which genetic systems permit adaptive stability and phyloge-
netic divergence.
In the remainder of this section, we summarize types of genetic recombination
and then tum to questions of how inverted meiosis affects recombination potential
in thelytokous and haplodiploid mites. Note that certain concepts associated with
recombination that were formulated in connection with monocentric systems (i.e.
prereduction, postreduction), are not strictly applicable to holokinetic ones, or
they have a modified meaning (Battaglia and Boyes 1955, John and Lewis 1965).
The distinction between crossover and noncrossover segments is ordinarily made
relative to a localized centromere. Without a centromere, the idea of crossover
segments is meaningful, but that of chromosome arms is not.
Three levels of genetic recombination (GR) within the chromosome-meiotic
systems are useful in evaluating cytological and evolutionary consequences.
(i) intra-chromosomal GR: genetic recombination during pachytene in meiotic
prophase. It is observed cytologically as chiasmata at diplotene/diakinesis, and
biochemically as a spike ofpachyDNA (Stem and Hotta 1987). This is the classic
form of GR and arises from crossingover and reciprocal exchange between
nonsister chromatids synapsed in bivalents.
Chiasmata are cytological observations of connections between nonsister chro-
matids. When they occur in the highly repetitive, nontranscribing, telomeric
DNA regions, they are genetically meaningless (John 1990). Thus, these terminal
chiasmata that form half-biva1ents are not sources of genetic recombination sensu
generating genetic variation. Observations of one terminal chiasma in bivalents
in most holokinetic species cannot be interpreted as evidence for genetic recombi-
nation. These so-called terminal chiasmata are therefore mechanical features
enabling chromosome segregation (see Section 2.1.3). Older literature refers
to "terminalization" of chiasmata implying that real genetic recombination has
occurred, and this has been shown to be incorrect (Jones 1978, John 1990).
Recent studies merging cytology and genetics have shown that intrachromoso-
mal GR requires prior chromosome pairing during zygotene, the phase during
which the synaptonemal complex (SC) forms between the duplicated homologous
chromosomes (Fig. II.4D). A series of attachment sites have been identified and
they are associated with recombination nodules of at least two sorts (Jones 1987).
The earliest event preceding pairing competence is seen in leptotene, where
each pair of sister chromatids is joined by the lateral portion of the SC, and one
or both ends of each duplicated homologous chromosome are imbedded in the
nuclear envelope. A telomeric plate forms in the nuclear membrane at this
attachment and pairing site. Such telomeric pairing is sufficient to establish the
end-to-end linkages noted earlier (Fig. 11.4) for the formation of half-bivalents,
and is required for inverted meiosis as discussed. Telomeric pairing is between
nonsister chromatids, but is not the source of genetic recombination.
Synapsis (formation of bivalents) begins in zygotene with recognition between
the telomeric regions of homologues, and is associated with a specific form of
DNA synthesis (zygDNA, Stem and Hotta 1987). Pairing competence between
homologous sister chromatids is then established by the initiation of the central
SC at telomere attachment sites. Central SC synthesis is the prerequisite for
classic GR when gene conversion occurs.
There is little information about rates of classic GR in holokinetic species. In
spider mites, recombination rates have been calculated from crosses using pig-
ment mutants (Helle 1985). Cytologically, Feiertag-Koppen and Pijnacker (1985)
reported two to three chiasmata per bivalent, but they make no issue of the genetic
consequences stemming from chiasmata location. The terminal associations are
the only ones visible at, and after diakinesis.
The failure of the central SC to form causes desynapsis and achiasmate meiosis,
even though homologues may remain paired at their ends. Thus achiasmate
bivalents, common in spermatogenesis in a variety of taxa, allow normal segrega-
tion of equal numbers of chromosome dyads at anaphase I.
The complete failure of synapsis, termed asynaptic meiosis, is relatively rare.
Univalents are seen aligning at metaphase I. With asynapsis, either synapsis fails
due to the absence of the central SC, or the central SC is not maintained, and
bivalents desynapse before diakinesis. These variations in prophase I contribute
to chromosome alignment and distribution in subsequent phases of meiosis. They
profoundly affect the second level of GR, chromosomal segregation.
(2) Inter-chromosomal GR: recombination due to segregation of homologues

in the reductional division, or of crossover regions in the equational division.
The recombination of entire chromosome sets is predicted from the expectation
of random orientation of bivalents. With haploid numbers of n = 2, 3 or 4, so
common in Mesostigmata and Prostigmata, the number of linkage groups capable
of segregation is impressively limited. Oliver (1965, 571) interpreted karyotypes
of parasitic mites as showing an evolutionary trend toward a reduction in chromo-
some number. This trend reduces the number of linkage groups, and he speculated
that enhanced linkage would lessen genetic flexibility and result in a greater
degree of adaptive specialization.
Nonrandom arrangements ofbivalents, or bivalents consisting of members that
segregate equationally rather than reductionally (in the cytological sense), all
further reduce the amount of GR produced during meiosis. Parahaploidy is an
extreme example of mitotic segregation distortion, where the entire haploid
paternal set is preferentially excluded.
(3) Gametic GR: random inclusion in functional gametes of any meiotic prod-
uct. Any distortion of gametic equivalence, or of equal probability of meiotic
inclusion, will reduce genetic recombination. Gametic selection will result from
any modification that produces one, or only a small sample, of the possible array
of haploid recombinants. Such an effect is a form of meiotic drive that suppresses
the potential overall amount of genetic recombination.
3.2 Inverted Meiosis as an Explanation for Thelytokous Higher Taxa
3.2.1 Types of Thelytoky
As discussed in the Introduction, the persistence and genetic flexibility of

thelytokous organisms depends on whether or not oogenesis includes meiosis,
and which particular meiotic mechanism is involved. Comprehensive reviews
and synopses of this topic are numerous (e. g. White 1973, Bell 1982, Templeton
1982, Cuellar 1987, Lamb and Willey 1987, Suomalainen et al. 1987), but none
considers the potential significance of inverted meiosis, and we feel apomixis has
been overemphasized, at least among animals.
Apomixis-Apomixis ("ameiotic" thelytoky) is believed to reproduce the moth-
er's genome via an essentially mitotic oogenesis, and eggs produced in this way
are considered to be faithful keepers of the clone's genetic bauplan. Such lineages
are thought to be prone to a Muller's Ratchet accumulation of mutations, though
the central hardship attending apomixis may be the loss of DNA repair at prophase
I (Bernstein and Bernstein 1991).
Although apomixis has been proclaimed the predominant thelytokous mecha-
nism in insects (Suomalainen 1950, White 1973, see also Lamb and Willey
1987), many researchers are careful to diagnose it only provisionally, and in such
cases reinvestigation is warranted. A truly meiotic division may be mistakenly
considered apomictic if bivalents fall apart before diakinesis, such that the diag-
nostic zygotene-pachytene stages could not be seen. Even the general absence of
genetic segregation is not conclusive evidence of apomixis, since holokinetic
systems with inverted meiosis may faithfully conserve the maternal genome (see
Section 3.2.2).
Further confusion arises when authors conclude that premeiotic doubling (see
below) is a form of apomixis, even though it allows autobivalents to form
during prophase I. Such a conclusion (e.g. White 1973) stems from viewing the
importance of bivalent formation in a restricted sense: crossing over between
genetically identical chromosomes does not provide new genetic variants upon
which natural selection could act. But when conservation of genome is considered
a benefit, apomixis and premeiotic doubling are not equivalent. The formation
of autobivalents in premeiotic doubling affords homologous chromosomes the
same opportunity for double-strand DNA repair that is provided by normal
bivalents.
Chapman's (1969, 442-3) assignment of apomixis to blattid, aphid, tenthre-
dinid, and curculionid insects followed the tradition of assuming that a single
maturation division is equivalent to ameiosis. White (1973) pointed out that
apomixis is more common in plants than in animals, but we note that the great
majority of animal mechanisms in his survey are automictic, with terminal fusion.
Records of apomixis in mites are rare. Heinemann and Hughes (1969) observed
it in a strain of Histiostomajeroniarum that was associated with a morphologically
indistinguishable arrhenotokous strain. The apomictic strain had only one pseudo-
maturation division and formed no bivalents (or at least none was found at
diplotene, and no cross- or ring-like configurations were observed). This single
division produced a single polar body and a functional egg. The egg contained
the diploid number of chromosomes and underwent a mitotic division during
cleavage; the polar body did not undergo a second division. Apomixis was
suggested for the ixodid Haemaphysalis iongicornis by Takenouchi et al. (1970),
a triploid (3n = 33) obligate thelytoke. The closely related bisexual strain has
2n = 22, XX females and 2n = 21, XO males. The case for apomixis is inferen-
tial, however, and Oliver et al. (1973) were not persuaded. They noted that an
aneuploid parthenogenetic race (2n = 23, 24, 25, 27, 28) was automictic.
Automixis. Automictic (= meiotic) thelytoky enables the advantages and disad-
vantages arising from crossing over, by permitting the formation of bivalents at
prophase I. The difficulties attending automixis stem from the mechanism for the
restitution· of somatic ploidy. There are at least four major forms of restitution
observed in the animal kingdom (Templeton 1982, Lamb and Willey 1987), but
only two have been reported in mites.
One involves premeiotic chromosome doubling, and was described for Brevi-
pa/pus obovatus, in which two bivalents are seen at diplotene (Pijnacker et al.
1981). Females of this obligate thelytoke occasionally produce spanandric males,
and males can be induced by irradiation. Both sexes have the same karyotype,
and their 2n = 2 ploidy is exceptional, the lowest known in animals. No cells

contain just one chromosome, and the two chromosomes are heterologous. Ear-
lier, we described indirect evidence that the meiotic sequence in this species is
inverted. An equational first division permits all four meiotic nuclei to contain
both chromosomes, so no restitution of nuclei is required (Fig. 11.6). Thus,
premeiotic doubling of the heterologous chromosome pair, which would other-
wise have difficulty forming a singleton bivalent (Fig. 11.5C), is accommodated.
All Tenuipalpidae have low numbers of chromosomes, and many are thelytokous
(Helle et al. 1980), though we do not claim that they constitute a phylogenetic
clade within the family. However, the widespread habit of polyphagy and eco-
nomic importance of these mites attests to the evolutionary vagility of such a
superficially "dead end" genetic system, one that works because of inverted
meiosis.
The second meiotic mechanism known from mites is terminalfusion, the fusion
of the egg pronucleus with the second polar nucleus (equivalent to the failure of
anaphase II segregation of the secondary oocyte). Terminal fusion has been
reported from two species of oribatid mites, Platynothrus peltifer and Trhypoch-
thonius tectorum, and was suspected in a third, Nothrus palustris (Taberly 1958,
1987). The former two species are members of large, totally thelytokous families
(Camisiidae and Trhypochthoniidae, respectively), and all known Nothrus species
are thelytokous (Palmer and Norton 1991).
A third mechanism of restitution is by the fusion of cleavage nuclei (equivalent
to endomitosis). This seems to be quite rare, (White 1973), but Regev (1974)
thought the prostigmatid mite Cheyletus malaccensis restores ploidy in this man-
ner. This conclusion has been reiterated in a number of reviews, but Helle et
al. (1984) have doubted a number of Regev' s cytological statements, and a
reinvestigation is needed.
A fourth mechanism of restitution is central fusion, in which the egg pronucleus
fuses with a second division product of the first polar nucleus. It is not known in
mites, but has some theoretical relevance (see Section 3.3.3).
Related Reproductive Modes. Other modes involving thelytoky, such as pseu-
dogamy or heterogony, can be ameiotic or meiotic. In pseudogamy (= gynoge-
netic thelytoky), the parthenogenetic development of eggs ensues after penetration
by sperm from a closely related species, without inclusion of the sperm's DNA.
Heterogony includes a variety of cyclic alterations between thelytokous and
bisexual forms. These modes are not known in mites (see discussion in Norton
et al. 1993).
3.2.2 Inverted Meiosis and Terminal Fusion Conserve Maternal Genome
According to standard interpretation (White 1973), terminal fusion would occur

between sister chromatids, resulting in a zygote homozygous at all loci except
those in regions undergoing crossingover at prophase 1. Even with some cross-
ingover, homozygotes would rapidly accumulate in the absence of very strong

selection for heterozygotes (Asher 1970, Templeton 1982). Central fusion would
seem to be much more advantageous, since in this mechanism the maternal
genome is conserved except in crossover regions, and the degree of crossingover
would presumably be under genetic control. If thelytoky serves to conserve and
propagate essentially clonal genotypes, terminal fusion should be rare and central
fusion should characterize successful automictic thelytokes.
In fact, the opposite is true. Central fusion is quite rare, and seems restricted
to insects. Only one naturally occurring species is known to use central fusion in
an obligate manner: the fly Drosophila mangabeirai (Murdy and Carson 1959).
In other insects using this mechanism-the flies Drosophila parthenogenetica
and Lonchoptera dubia, the psychid moth Solenobia triquetrella, and the honey-
bee Apis mellifera-thelytoky is sporadic or characterizes races (White 1973,
Suomalainen et al. 1987).
In contrast, terminal fusion is quite widespread. Groups in which cytological
observations have confirmed terminal fusion in thelytokes include: nematodes
(summary in Suomalainen et al. 1987); rotifers l (Birky & Gilbert 1971); tardi-
grades (Suomalainen et al. 1987, contra Ammermann 1967 and John 1990);
annelids (summary in Suomalainen et al. 1987); crustaceans, such as cladocerans
(Bacci et al. 1961, contra White 1973, who considered them apomictic), Artemia
(Wilson 1928), and isopods (Hill 1948); arachnids such as harvestmen (Tsurusaki
1986) and oribatid mites (Taberly 1958, 1987); and insects such as mantids,
aphids, thrips, and wasps, as well as occurring racially or sporadically in coccids, 2
flies and acridid orthopterans (White 1973, Suomalainen et al. 1987, John 1990).
Furthermore, another restoration mechanism, the absence of a second division
of the secondary oocyte after an equational first division, is equivalent to terminal
fusion; it is found in many planarians, grasshoppers and beetles (White 1973).
Classical cytogenetic models predict inevitable complete homozygosity and
genetic inflexibility for such systems, so the emphasis on terminal fusion for
ploidy restoration in successful groups appears problematic. Palmer and Norton's
(1992) recent discovery of a general lack of segregation in populations-and in
mother-daughter lineages-of species in the oribatid mite group studied by Ta-
berly (1958, 1987) was similarly incongruous. Apomixis or some central fusion
mechanism was hypothetically invoked to explain away the observed conservation
of heterozygosity.
'Bdelloid rotifers, which are exclusively thelytokous, have been described as having two equational
divisions: this suggests premeiotic doubling of the 2n = 13 karyotype (Birky and Gilbert 1971).
Further observations are necessary, but the presence of an odd-numbered karyotype does suggest why
males are hard to produce. Phasmid insects present another case in which both meiotic divisions were
described as equational (Hughes-Schrader 1947).
2John (1990) notes that the desynapse of bivalents into univalents has been misinterpreted as
apomixis.
308 I D. L. Wrensch. J. B. Kethley. and R. A. Norton
Such "problems" seem now to be artificial constructs. Models of thelytoky

have always assumed a nonnal, reduction-first meiosis, i.e. they were based on
a cytogenetic paradigm developed for organisms with monocentric chromosomes
(Fig. 11.3, left). But there can be a very different outcome in groups having
holokinetic chromosomes and inverted meiosis. Such a system has an equational
first division, so the secondary oocyte segregates two sets of chromatids that are
homologues (Fig. 11.3, right). Fusion of these segregants restores the maternal
genotype insofar as there is no crossingover. By minimizing chiasmata, such a
system would maximize conservation of the maternal genotype while providing
the benefits of DNA repair, and seems to represent what from a cytogenetic
viewpoint might be considered "ideal thelytoky."
From an ecological viewpoint, the widespread distribution of such a conserva-
tive system seems consistent with Lynch's (1984) "general-purpose genotype"
theory. He suggested that thelytokes are successful in frequently disturbed envi-
ronments because they avoid specialized adaptation to local conditions. This is
accomplished by producing offspring that are virtual clones; i.e. such organisms
have a unit of selection that, in effect, consists of the whole genome. By minimiz-
ing crossovers and restoring ploidy by tenninal fusion, holokinetic thelytokes
having inverted meiosis could possess such large units of selection.
At present, the only unequivocal evidence that meiosis is inverted in holokinetic
thelytokes with tenninal fusion is that of Hill (1948), who studied the isopod
Nagara modesta. Taberly (1987) assumed a monocentric system and nonnal
meiosis in his oribatid mites, as we deduce from his discussion of Hill's observa-
tions, and from the genetic implications oftenninal fusion that Taberly envisioned
(his Fig. 17). For example, he referred to prereduction and postreduction segrega-
tion, tenninology developed for monocentric systems (White 1973) and without
meaning in holokinetic systems (Section 2.1.3). Also, Taberly seems to have
suggested (399) that the absence of synaptic phenomena prior to the second
division in the isopod (the reductional division) is a source of difference between
the systems. But such phenomena are not relevant to second divisions in holoki-
netic systems.
Taberly's cytological observations are in fact quite consistent with the presence
of inverted meiosis in these mites. In our interpretation, his Fig. 10 (metaphase
I) represents nine bivalents (i.e. nine tetrads, or 36 chromatids) in profile view.
This is consistent with an equational separation of homologous chromatids. His
Figs. 11 and 12 show metaphase II in polar view; we interpret the symmetrical,
coronal distribution of nine dyads ("diplocoque") to reflect holokinetic chromo-
somes bound to an unstained karyomere membrane, as in other acarifonn mites
(e.g. Cooper 1939). Inverted meiosis is the only interpretation that is congruent
with both Taberly's observations and the conservation of maternal genome in this
group of mites, as reported by Palmer and Norton (1992).
Superficially, a central fusion restoration with nonnal meiosis seems equally
"ideal" and able to conserve one member of each homologous chromosome pair.
However, the first polar nucleus in anisogametic organisms rarely divides during
oogenesis and is unsuitably located in the peripheral cytoplasm of the egg. In
Drosophila, central fusion is enabled by an unusual 90° rotation of the first
division spindle from its normal position perpendicular to the chorion. But this
rotation is achieved at a cost, since approximately 40% of eggs are inviable
(Templeton 1982).
In summary, the genetic consequences of inverted meiosis with holokinetic
chromosomes are profoundly different-completely opposite, in fact-from
those predicted by the monocentric model of cytogenetic dogma (Fig. 11.7).
Combined with the simple restoration mechanism of terminal fusion, inverted
meiosis results in the retention of both original homologous chromosomes. We
predict that most successful thelytokes, especially those that have demonstrated
some degree of evolutionary success, will prove to have holokinetic chromosomes
PROPHASE! ANAPHASE! LATE METAPHASE II EGG GENOTYPE

AFTER
RESTITUTION
~ a~
~~ ~ ~
A
• centromere
G
OR
End-Io-End Pairing
G
Figure 11.7. Genetic consequences of intrachromosomal genetic recombination assum-
ing terminal chiasmata and one heterozygous locus. Automixis by terminal fusion: egg
pronucleus fuses with, or fails to separate from, the second polar nucleus. A) Monocentric
chromosomes, normal meiosis. B) Holokinetic chromosomes, inverted meiosis.
and inverted meiosis, and will restore ploidy by terminal fusion or an equivalent
process.
3.2.3 Sexuality from Thelytokous Ancestors: the Case of the Astigmata
Recently, Norton et al. (1993) suggested that evolutionary biologists would be

challenged to explain the reversal to sexuality that is inferred by a derivation of
Astigmata from thelytokous ancestors in the Trhypochthonioidea. When first
proposed (Norton and Palmer 1991), this reversal was viewed as a release from
the constraints of thelytoky, particularly those previously associated with terminal
fusion automixis (i.e. lack of genetic flexibility). But terminal fusion is not
necessarily an evolutionary "burden" in groups with holokinetic chromosomes
and inverted meiosis.
If we view diversification as an undesirable consequence of less rigid recombi-
nation control, then the thelytokous trhypochthonioids were not really "con-
strained" at all. In fact, they seem to have done very well. The thelytokous family
Trhypochthoniidae has existed since the Jurassic period (Krivolutsky and Druk
1986), and one extant species, Mucronothrus nasalis, probably predates the
breakup of Pangaea (Hammer 1965). But if we view diversification leading to
adaptive radiation as evolutionary success, thelytokes are still mightily con-
strained by the absence of a large gene pool. When sexual reproduction was
reestablished in the ancestors of the Astigmata, it resulted in a group of 5000
known (and many more unknown) species with amazing biological diversity.
Life-history aspects of this transition are discussed elsewhere in this book (Chapter
5).
The reversal probably represented a reactivation of an ancestral sex determining
mechanism, but sex determination in oribatid mites is not yet understood, nor do
we have strong hypotheses about the ancestral mechanism in Astigmata. The
earliest derivative astigmatid family for which information is available is the
Histiostomatidae, an arrhenotokous family. But sex determination seems to be
homoplasous in Astigmata, and our current view is that the ancestral Astigmata
were diplodiploid (Norton et al. 1993).
It is likely that the common ancestor of Astigmata had one of two karyotypes:
(1) similar karyotypes in both sexes (as in oribatid mites, where the sex determina-
tion mechanism is unknown)-this currently is known for only one astigmatid
mite, the acarid Rhizoglyphus echinopus (Sokolov 1945); or (2) an XO/XX
system, such as is currently known in Glycyphagidae and some other Acaridae.
Within Astigmata, an XY/XX system is known only in the acarid genus Tyropha-
gus (Norton et al. 1993).
Sexuality is regularly restored from thelytokous generations within annual
cycles of those (nonmite) taxa exhibiting cyclical parthenogenesis, and we can
look to such extant groups for potential mechanisms. Some examples follow, to
illustrate that such a switch is not cytogenetically difficult.
As one example, a generational switch from arrhenotoky to thelytoky exists in

amphigonic rotifers (Birky and Gilbert 1971) and cynipid gall wasps (Chapman
1969). In these organisms, the sexual generation females produce diploid daugh-
ters and haploid sons, by either restitution or nonrestitution (respectively) of
meiotically produced haploid eggs. The restitution of diploidy in Cynipidae and
other thelytokous Hymenoptera is by terminal fusion (John 1990, 284). Restitu-
tion in heterogonic rotifers is similar (Birky and Gilbert 1971, and pers. comm.,
1992). A third haplodiploid example is found in a species of the hermaphroditic
coccid I cerya sp., in which true females arise through suppression of haplodiploi-
dization in gonadal tissue (Hughes-Schrader 1963, John 1990).
Reversions to sexuality in amphigonic thelytokous aphids and hermaphroditic
nematodes follow the same mechanisms of nondisjunction of the X chromosome
(White 1973, Triantaphyllou 1984, John 1990). These aphids and nematodes-
groups with holokinetic chromosomes (see Table 11.1)-are XX, their sexual
daughters are XX from one equational meiotic division, and sons are XO. Sperma-
togenesis in these XO males involves two meiotic divisions, but in both taxa only
the X-bearing sperm are viable and thus males are homogametic.
Reversion to sexuality in crustaceans such as Daphnia may provide a model
for taxa lacking any obvious sex-determining mechanism, e.g. trhypochthonioid
mites. Daphnia males and both sexual and thelytokous females all share an
identical karyotype. Thelytoky is maintained with one equational division, but
the sex-determining mechanism is unknown.
The thelytoky option becomes curtailed in the presence of sex chromosomes,
in particular when a Y pairs with an X. The XY system in coccids still permits
equational first division meiosis because the two heterologues are achiasmate,
and orient as univalents. In the Hemiptera, the nearly universal presence of an
XY system, with normal spermatogenesis, appears to preclude thelytoky-it is
not found in the group (Ueshima 1979).
We have noted the absence of typical cyclical parthenogenesis in mites, but
there is one possible example of a reversal to sexuality from a thelytokous
population of an extant oribatid mite. During a long-term study of the Japanese
soil mite Oribatula sakamorii , Fujikawa (1987) found that males were exceed-
ingly rare (suggestive of thelytoky, with spanandric males) in a disturbed culti-
vated field, but became numerous (suggestive of bisexuality) when land use
became less intensive.
3.3 Diplodiploidy and Inverted Meiosis
3.3. I What is the Role of Sperm in Life Cycles?
Sperm are usually believed to be essential in some way to egg viability and
development. White (1973) thought all sperm donated their centrioles, but this
cannot by true for either insects (Phillips 1970) or mites (Alberti 1991), groups
in which mature sperm lack centrioles. Many think sperm are necessary for egg
activation in bisexual species, but this is obviously not the case for arrhenotokous
species, in which virgin females lay eggs that develop into males. In cases of
pseudogamous parthenogenesis, sperm serve to activate egg development, but
are then expelled. Obviously, sperm play no role at all in the many thelytokous
taxa. Sperm, then, do not have a universal role in sexual systems, and their
participation in sexual reproduction comes with a cost to females: the loss of
control of progeny sex ratio. Females cannot control sex through cytoplasmic or
chromosomal sex determination if sperm carry with them some trait essential for
offspring viability (Bacci 1965, Brown and DeLotto 1959). This dependence on
sperm arises with the evolution of sex chromosomes, as discussed below.
3.3.2 Spermatogenesis and Sex Determination in Diplodiploid Mites

(Fig. 11.8)
In diplodiploids, meiosis produces four functional products from one spermato-

gonium, and we know of no exception in mites. In this case, the orientation
DIPLOID MALE
Metaphase I
-
CHIASMATE MEIOSIS ACHIASMA TE MEIOSIS
. . . . . . . . . . It.. . . . . . . . . .
Bivalent Univalents
with end-to-end pairing Equational Separation Bivalent
Equational Separation without end-to-end pairing
Reductional Separation
HAPLOID MALE
Metaphase "I"
.............................
Univalent
Equational Separation
~ Maternal Chromatid
¢_~> Paternal Chromatid
Figure 11.8. Meiosis: spermatogenesis in diploid and haploid males with holokinetic
chromosomes. Metaphase I orientations for bivalents and univalents are shown.
of chromosomes at first or second division is of no importance genetically.

Recombination can be affected in other ways, such as by mechanisms that reduce
crossingover or interfere with random segregation. As noted by Hughes-Schrader
(1948), holokinetic chromosomes may predispose diploid males to achiasmate
meiosis, a process associated with a reduction in genetic recombination and
preservation of linkage groups (White 1973). Achiasmate spermatogenesis is
known for two species of water mites (Keyl 1957) and four species of Astigmata
(Sokolov 1945). In the water mite Hydrodroma despiciens one pair of chromo-
somes segregates precociously (precluding recombination) at anaphase I (Keyl
1957).
Sex chromosomes usually have aberrant behavior, such that they may lag
during congression to the equator at metaphase I, or they may lead precociously
or lag at anaphase I, all of which affect recombination. Also, sex chromosomes
are often heteropycnotic in males, and thus often lack synapsis and formation of
chiasmata.
Males of diplodiploid species exhibit a range of karyotypes and sex determina-
tion mechanisms. Sex determination is still a mystery for mite species in which
male and female karyotypes contain the same number and kind of chromosomes,
such as water mites (Hydrachnellae) and oribatid mites (Sokolov 1954, Taberly
1958). Most acarid mites with diploid males have an XO karyotype, where the
X chromosome is smaller than the autosomes. The sex chromosome of ixodid
ticks, which have predominantly XO males, can be larger than the autosomes or
the same size (Oliver 1977). All known argasid ticks have XY males, with the
X being much larger than other chromosomes. Tick spermatogenesis is described
as chiasmate, including one terminal association among the XY pair (Oliver
1977). In species with either XO or XY males, sex determination is assumed to
be by male digamety and sex ratios are about equal, following Mendelian princi-
ples for sex chromosome segregation.
3.3.3 Holokinetic Chromosomes Allow Kinetic Flexibility in Diplodiploids,

Necessary for the Evolution of Sex Chromosomes
Previous authors have described a normal order to meiotic divisions in diploid

spermatogenesis. Diploid male mites with no morphologically distinct sex chro-
mosomes, such as the water mite Eylais setosa (Keyl 1957), and species with
XO males, such as the acarid Caloglyphus mycophagus (Heinemann and Hughes
1970), have been interpreted as having a reductional first division. Spermatogene-
sis has also been described as achiasmate in these species. The sex chromosomes
of ticks separate reductionally at anaphase I (Oliver 1967), but the behavior of
autosomes has not been established.
An unappreciated feature of the holokinetic system is the potential for different
meiotic pathways within a species (Fig. 11.3). Inverted meiosis in oogenesis may
coexist with normal meiosis in spermatogenesis (White 1973, 492). Such a
314 / D. L. Wrensch. 1. B. Kethley, and R. A. Norton
mixed system-an equational first division in oogenesis but a reductional one

in spermatogenesis-is found in Hemiptera and Homoptera (in higher coccids
spermatogenesis is also inverted) (Suomalainen and Halkka 1963, Ueshima
1979). Similarly, the discovery of reduction at metaphase I for sex chromosomes
in ticks (i.e. Oliver 1977) does not force the conclusion that meiosis is normal in
both sexes.
This flexibility in bivalent orientation, attainable only in holokinetic organisms,
appears to be associated with the mechanism for sex determination. With diploidy,
spermatogenesis permits reduction, which is antecedent to acquiring an XO or
XY system, to male digamety, and eventually to the transfer of control over the
sex of offspring from females to males.
The recognition of heteromorphic chromosomes created the view that one
karyotype could contain a mixture of holokinetic and monocentric chromosomes
(Oliver and Bremner 1968). The hemipteran example described by Hughes-
Schrader and Schrader (1961) seems to be equivalent. Interesting parallels exist
between ticks (for which we have no information on the order of division in
oogenesis) and the mixed hemipteran system described above, in which sexes are
typically XX/XY. In ticks, the large sex chromosome gives the appearance of
restricted kinetic activity, and the sex chromosome bivalent shows reductional
division at anaphase I (Oliver 1967). A similar behavior was experimentally
induced in the ends of a long sex chromosome of a hemipteran by fusion of
smaller holokinetic chromosomes after radiation (Hughes-Schrader and Schrader
1961). Further, the long X in XO ticks looks and behaves very much like those
described in Hemiptera by Schrader (1935).
We believe that great confusion exists concerning the kinetic behaviors of mite
chromosomes, and that the actual distribution of inverted meiosis is mostly
unknowable because the key karyotypic descriptions--oogenesis in XX/XY and
XX/XO species-are generally unavailable. Both tick and hemipteran oogenetic
figures are difficult to obtain, but Helenius (1952) and Nokkala and Nokkala
(1984) discussed inverted meiosis in the hemipteran families Lygaeidae and
Nabidae, respectively.
3.4 Haplodiploidy and Inverted Meiosis
3.4.1 Spermatogenesis and Sex Determination in Haplodiploid Mites
Sex determination, and therefore sex ratio, is progamic (Bacci 1965) and is
under maternal control in haplodiploids, organisms in which males are either
genetically (arrhenotoky) or phenotypically (parahaploidy) haploid. This control
precludes the differentiation of sex chromosomes for haplodiploid males. Regard-
ing a question asked above (Section 3.3.1), the function of sperm in haplodiploids
is thus for something other than sex determination.
In arrhenotokous species spermatogenesis is highly modified, with a single
division producing two haploid sperm (Heinemann and Hughes 1969, Pijnacker
1985). This division probably represents an inverted meiosis in which the second
(reductional) division is suppressed, as discussed below (Section 3.4.2). There are
no bivalents or chiasmata, so that the event is "mitotic" in terms of chromosome
behavior and genetic consequences, i.e. the absence of type A, B, and C recombi-
nation.
Parahaploid males that start each life cycle as diploids will breed like haploids
and transmit no paternal DNA (Brown and Nur 1964). In parahaploidy resulting
from the elimination of the paternal genome early in embryogenesis (i.e. Phytosei-
idae, Nelson-Rees et al. 1980; and Dermanyssidae such as D. gallinae, Warren
1940), the spermatogenetic events are so much like those of arrhenotokous males
that Helle et al. (1978) named this parahaploid system "pseudoarrhenotoky."
Since no paternal DNA is included in haploid sperm of parahaploids, this is a
profound example of nonrandom segregation and preferential gametic inclusion.
Deviations from panmixia also rf,duce recombination possibilities. Any regular
pattern of inbreeding, such as a highly inbred arrhenotoky with obligate brother-
sister mating, will reduce the amount of GR arising from amphimixis. Any mode
of reproduction that facilitates female control of sex ratio, such as the several
forms of haplodiploidy, fosters distortion of the gametic ratio, either through
adaptive patterns of sex allocation (species' sex ratio) or by the proportion of
progeny allotted to one sex (sex ratio regulation) (see below, and Wrensch 1993
for discussion).
3.4.2 Haplodiploidy Requires Inverted Meiosis
We see the available cytogenetic information on arrhenotoky and parahaploidy

as pointing to an important general conclusion: haplodiploid systems can evolve
only in lineages having holokinetic chromosomes that exhibit inverted meiosis.
In this section we explain that spermatogenesis in haplodiploid systems is in fact
meiotic, and then discuss why this type of spermatogenesis cannot succeed in
monocentric systems with normal meiosis.
Arrhenotoky-In most known arrhenotokous species, spermatogenesis clearly
involves an equational first division with no second division (i.e. Whiting 1945,
John 1990). This seems to be the case for rotifers, whiteflies, chalcid wasps, and
iceryine scale insects, as well as mites (Whiting 1945). This one division has
generally been regarded as "mitotic" in character (i.e. Whiting 1945), due to the
absence of bivalents and the separation of univalents into single chromosomes.
Writers frequently remark upon the "failure" of an expected second division (e.g.
White 1973). However, haploid spermatogenesis clearly represents a first meiotic
division, rather than simple mitosis, for three reasons (Hughes-Schrader 1948):
(1) the duration of prophase "I" is prolonged and features a lengthy diplotene
(e. g. "confused" or "diffuse" stage) inferred from the relatively high proportion of
nuclei fixed in this part of meiotic prophase I; (2) the enlargement and subsequent
disappearance of nucleoli clearly indicate synthetic activity during meiotic pro-

phase; and (3) the chromosomes at metaphase "I" are more condensed than in
somatic metaphases.
Arrhenotoky requires a system with holokinetic chromosomes that form end-
to-end associations in the diploid female. These half-bivalents create the physical
attachments between nonhomologous chromosomes that lead to inverted meiosis.
This segregation pattern is critical to a females' ability to retain control of the
genetic content of each egg produced. To understand the significance of this
meiotic pathway, we must first consider the results theoretically obtained with
normal meiosis.
Assume that a pair of homologous chromosomes replicate and separate without
crossingover at metaphase I in normal meiosis. The secondary oocyte would
contain an identical pair of chromatids. Their segregation in the second division
would produce an egg pronucleus that is haploid for one of the two original
homologues. A haploid male arising from such an egg represents one and only
one possibility from the maternal genotype; thus, for any primary oocyte, males
would always be formed from one or the other homologue. Assuming independent
orientation at metaphase I of the bivalent, the pool of haploid eggs from any
female undergoing normal meiosis will therefore always consist of 50% one
homologue and 50% the other. Consequently, the female has no control of the
individual genetic content of her sons.
With inverted meiosis, however, secondary oocytes and polar nuclei are geneti-
cally equivalent. Thus, orientation at metaphase I is irrelevant. The secondary
oocyte contains one of each homologue, and the segregation of these homologous
chromatids at anaphase II generates haploid eggs. Within each egg, there is a
50% probability that a particular homologue is included in the haploid male.
Therefore segregation in the secondary oocyte resulting from inverted meiosis
permits female control of the genetic complement of haploid males; she controls
the genetic content of each egg. With normal meiosis, such control is impossible.
Para haploidy-The order of meiotic divisions is critical to the genetic conse-
quences of parahaploid spermatogenesis, since it is inverted meiosis that enables
the preferential segregation of only the maternal genome into two functional
sperm. Males of parahaploid scale insects have inverted meiosis, and whether
the system heterochromatizes the paternal set or eliminates it, only two functional
sperm are produced. These contain the same half of the maternal genome, i.e.
they are genetically identical. The pattern seems the same in parahaploid mites,
but their cytogenetics (including that of the confusing system of Dermanyssus,
J. Oliver, pers. comm., 1992) must be reinvestigated to confirm that meiosis is
inverted.
In discussing spermatogenesis in lecanoid coccids, John (1990) considered
inverted meiosis to be a "preadaptation" for parahaploidy. In this system two
meiotic divisions occur, but the first must be equational for normal sperm to
result. After an equational first division, the two haploid nuclei that originate
from the two euchromatic telophase II sets proceed to differentiate into the two
functional sperm. This inverted meiosis is considered to be ancestral to the
abbreviated type of meiosis in diaspidid coccids, which features just one equa-
tional division producing two sperm (Brown 1977).
3.5 Inverted Meiosis Affects Recombination Index
Levels of intrachromosomal genetic recombination (see Section 3.1, type A) can

be measured in a simple way, if we confine ourselves to relative statements.
Intrachromosomal genetic recombination levels directly impinge on the amount
of genetic variance available to natural selection. Allelic recombinations sift out
homozygotes from heterozygotes that carry cryptic variation (Mather 1953). The
integrity of linkage groups is directly affected, and sustained or disrupted by the
location and frequency of intrachromosomal, reciprocal exchanges.
To make our case for the effect of holokinetic chromosomes on evolutionary
potential, we have to compare how modes of reproduction can directly affect
levels of genetic recombination. We have computed the recombination index (RI,
Darlington 1939, White 1973) for different modes of reproduction, for each sex,
and for an average within the bisexual mode (Fig. 11.9). In addition, we have
computed RI for several modes of thelytokous reproduction, where we estimate
the values given holokinetic or monocentric karyotypes; a "male" equivalent is
based on the type of restitution. To make these comparisons relative, we assume
a standard karyotype with 2n = 6, n = 3, one functional crossover per bivalent
and progenies with equal proportions of sons and daughters.
A number of insights are gained by this comparison. First, the automictic
thelytokes that achieve restitution through terminal fusion have an RI of six,
equal to that of a diplodiploid species. Second, holokinetic chromosomes provide
consistently higher potential RI than do monocentric systems. Third, diplodi-
ploids have a reduction in their RI directly correlated with departure from normal,
complete synapsis in spermatogenesis. Fourth, as expected, all forms of haplodi-
ploidy have the same recombination index, and-given our I: I sex ratio assump-
tion-they have the lowest RI of any amphimictic mode.
What is the effect of relaxing the assumption of equal sex ratio in progenies
of bisexual modes? The answer that follows reveals how sex ratio variation serves
to alter the level of genetic recombination.
3.6 Facultative Recombination Through the Production of Haploid Males
Females of haplodiploid mites, such as the arrhenotokous spider mites (Tetrany-

chidae, Young et al. 1986) and the parahaploid Phytoseiidae (Sabelis and Nagel-
kerke 1987), produce female-biased progenies. Sex ratio is adjusted in response
to cues from the environment (Wrensch 1993), and progeny sex is determined
cytoplasmically, through mechanisms yet unknown. In parahaploids, all eggs
RI-Q fraction RI-d'fraction** RI
DIPLODIPLOIDY
Spermatogenesis chiasmate 6 6(a) 6
Spermatogenesis chiasmate, 4(b)

6 5
autosomes only (males XY, XO)
Spermatogenesis achiasmate 6 3(c) 4.5
HAPLODIPLOIDY
P ARAHAPLOIDY 5 2(d) 3.5
Paternal genome heterochromatic
PC eliminated in early embryo 5 2(d) 3.5
ARRHENOTOKY
5 2(d) 3.5
Chiasmata arc:
M H M H M B
THELYTOKY
AUTOMIXIS i. l2Ioximal 3 3(e) --L
A. Restitution by
ii. distal 6 6 6(e) 6(e) 6 6
Terminal Fusion: Egg '---
pronucleus + 2nd PN 4.5(e)
iii. (i + iO/2 4.5 4.5
i. proximal 6 6(e)
B. Restitution by
~
ii. distal 4.5 4.5 4.5(e) 4.5(e) 4.5 4.5
Central Fusion:
Two non-sister PNs -
iii. (i + ii)/2 5.25 5.25(e) 5.25
C. Restitution: Fusion of cleavage nuclei
6 6 O(e) O(e) 3 3
or endomitosis of egg pronucleus
D. Premeiotic Doubling 3 3 3(f) 3(f) 3 3
APOMIXIS O(g) O(g)

0 0 0 0
*Recombination Index (for each sex or averaged for both sexes) =

Sum of haploid number (n = No. bivalents) + mean chiasmata/cell
(= average for one meiotic division). For haplodiploids, n' = (female(n) +1)/2.
(from White, 1973)
** a) Diplodiploid sperm = haploid meiotic recombinant set

b) = a. for autosomes, but sex chromosome(s) nonrecombinant
d = a. but complete haploid set nonrecombinant
d) Haplodiploid sperm = haploid ameiotic nonrecombinant set
e) Automictic thelytokous restitution system = fusion (A,B) or doubling (C)
of haploid meiotic recombinants
f) Bivalents are "autobivalents" between sister duplicated homologues,
therefore chiasmata do not create GR
g) Apomictic thelytoky = one ameiotic nonrecombinant diploid set
Figure 11.9. Recombination index (RI)* as a function of mode of reproduction. Assume

2n = 6, n = 3, one crossover/bivalent and a progeny sex ratio of I: I. For monocentric
(M) chromosomes, RI related to location of chiasmata (i.e. proximal to centromere or
distal, with locus between centromere and chiasma). For holokinetic (H) karyotypes,
chiasmata usually form at bivalent ends. **
318
receive sperm initially, so eggs that produce males must somehow eliminate the
sperm's contribution. In arrhenotokes, females produce males by prohibiting
sperm entry into a fraction of the eggs.
White (1973, 498) recognized that the lowest RIs in the animal kingdom are
those found in mites with haploid males and chromosome counts of n = 2 or n
= 3. Wrensch (1993) argued that a conditional increase in the proportion of male
progeny represents a facultative increase in the rate of genetic recombination. To
illustrate how this effect is achieved, first consider Figure 11.10, which diagrams
the effect of haploid males (either arrhenotokous or parahaploid) inseminating
virgin females across two generations. The variability due to crossingover and
recombination is under female control because only females form bivalents during
meiosis. The amount of variability generated is a function of type A and type B
recombination (Section 3.1). The expression of this GR is through haploid males,
which act as vectors of either the conserved (without type A GR) or recombined
(with type A and type B GR) genome.
Assuming the observed level of crossingover of two per bivalent during spider
mite oogenesis (Feiertag-Koppen and Pijnacker 1985), a rough estimate can be
computed for both type A and type B GR effects. The number of different
recombinant chromosomes can be gauged from White's presentation (1973, his
Fig. 6.6) . Since spider mites have 2n = 6 chromosomes, the combinatorial for
calculating the different haploid sets of three is straightforward. 3 Figure 11.11
uses these assumptions to provide a simple numerical example of the effects of
a shift in sex ratio.
For the same number of eggs, 200, a female that increases the proportion of
haploid eggs simultaneously increases the fraction of haploid genetic recombi-
nants that her own genotype meiotically generates. A male develops from an
ovum containing an egg pronucleus and maternal cytoplasm. Given the level of
recombination observed, each male is likely to be genomically unique (Fig.
11.10).
This helps explain the apparently paradoxical success of highly inbred arrheno-
tokous (HIA) mites discussed earlier (Section 1.3): why doesn't HIA quickly lead
to homozygosity, and hence extinction? For our introductory example of quill
mites, there is little recombination potential in the first generation, which contains
a single male. However, the progeny of the second generation contains 11 males
and, by analogy to the spider mite example above, maximizes the degree of
'White'S Figure 6.6 (1973, 165) illustrates the types of crossover products that result from two
chiasmata per bivalent. Pairs of reciprocal chromatids (P), two kinds of diagonal chromatids (q, r)
and complementary chromatids (s) reflect outcomes of 2-strand, 3-strand and 4-strand exchanges,
respectively. With the haploid egg n = 3, the combination of types of crossover products is (P + q
+ r + s)'. By multiplying each combination by its relative frequency and then pooling recombinant
sets having the same mean integer of recombinant chromosomes per egg, frequencies of the four
categories of eggs in Figure Il.ll are obtained. The relative frequencies of the reciprocal, diagonal
and complementary types of crossover products are available in White (1973).
First generation of Founding Female:
Possible progeny assuming one meiotically Maternal -
generated recombinant chromosome. Recombined -=::J
Paternal ~
Sons
Daughters
SPIDER MITES: The second generation of progeny.
I
~--------,
Virgin Females I
~ @ @
CS>(jS)@
@~~
~~~
Figure 11.10. Arrhenotokous reproduction in two consecutive generations of spider
mites. Only one chromosome is tracked and is diploid in females and haploid in eggs and
in males.
320
EGGS:
3 Recombinant Chromosomes =42.19%)

2 Recombinant Chromosomes = 41.02% 96.9%
1 Recombinant Chromosome = 13.67%
No Recombinant Chromosomes = 3.12%
Sex Ratio # Eggs (= # Males) With

% of Total Progeny > 0 Recombinant
Fecundity Prop. Q That are Recombinant cJ s Chromosomes
200 0.80 19.38 38.76
200 0.70 29.07 58.14
Figure 11.11. Percent of haploid eggs containing 0, 1, 2, or 3 recombinant chromosomes

and the effects that varying sex ratio has on the proportion of progeny and the absolute
number of offspring that are haploid. Number of cross-overs is assumed to be two per
bivalent. See text for details of computations.
recombination with a minimal number of males. As with thelytoky, the paradox

is largely an artificial construct resulting from assuming a normal meiosis, rather
than the inverted meiosis that arrhenotoky requires.
A highly female-biased sex ratio will reduce RI for any of the bisexual modes
listed in Figure 11.9, where a 1: 1 ratio was assumed; such a reduction more
faithfully conserves the maternal genome in the next generation. On the other
hand, a controlled sex ratio shift that increased the proportion of haploid males
would increase RI, and therefore raise the potential for genetic variation. From
this perspective, the genetic function of males in haplodiploid systems is to make
genetic recombination a facultative process.
4. The Big Picture: Holokinetic Systems and the Evolution of Eukaryotes
4.1 Distribution of Holokinetic Chromosomes and Inverted Meiosis

in Eukaryotes
. . . with so little evidence I have no intention of entering this old battlefield of hypotheses.
(Schrader 1936)
Perhaps we should be as cautious as Schrader, but without speculation from

spotty evidence, many avenues of biology would be left unexplored. We have
suggested that holokinetic chromosomes may be pervasive in Acari, but mites
are probably not unusual in this regard. Major reviewers agree that,holokinetic
chromosomes are present in numerous animal groups (i.e. Rhoades 1961, White
1973, John 1990), but we believe authors have been conservative. What follows
is not intended as a detailed review. Rather, we summarize literature records and
suggest groups that may prove holokinetic when more closely examined. Our
purpose is to emphasize that chromosomes in numerous groups of protists and
fungi, and of both early derivative and higher animals and plants (though botanists
traditionally shun the characterization), are holokinetic.
Chromosome characterizations in Table 11.1 were taken either directly from
the cytogenetic literature or were made by us after examining primary sources.
The monomorphic condition (*) for a listed taxon is provisional. For example,
nematodes appear to be exclusively holokinetic to us, and mostly so to Trianta-
phyUou (1984); but he cautiously did not commit to a global statement because
some of the primary literature claimed one species has metacentric (and therefore
monocentric) chromosomes. Conversely, while occasional primary literature has
assigned a holokinetic karyotype to a beetle (i.e. Blackwelder 1944, Kiauta
1969), Smith and Virkki (1978, 29) regard beetle centromeres as "localized"
because "no reliable account exists of a diffuse ... centromere." Nevertheless,
at several places in the latter monograph on beetle cytogenetics, the described
chromosome behavior and morphology directly or indirectly suggest that chromo-
somes are holokinetic (e.g. Smith and Virkki, 95). In particular, Smith and Virkki
describe the chromosomes of an arrhenotokous species, Xyleborus dispar, as
". . . comparable in size to those of most Lepidoptera" (217). This comparison
seems literally correct to us, too, since Lepidoptera have holokinetic chromo-
somes, and it would be consistent with the argument we have been making
concerning holokinetic systems as a precondition for arrhenotoky.
The occurrence ofholokinetic chromosomes is even more pervasive in eukaryo-
tic organisms than has been thought. Indeed, they seem to be present in at least
some taxa of every major lineage of eukaryotes, with the conspicuous exception
of Echinodermata, Chordata. Viewed in a phylogenetic context, the character
state of having holokinetic chromosomes is potentially present at every major
node of the tree of eukaryotic life. This scattered distribution of holokinetic and
monocentric chromosomes among various protist, plant and animal groups poses
an obvious question: viewed as character states, is it the absence or the presence
of a localized kinetochore that is ancestral? Clearly, with either polarity there
must have been multiple derivations; centromeres have evolved many times or
have been lost many times.
4.2 Are Holokinetic Chromosomes and Inverted Meiosis Ancestral

in Eukaryotes?
It has been suggested that holokinetic chromosomes have given rise to monocen-
tric chromosomes (Vaarama 1954, Halkka 1956, Hughes-Schrader and Schrader
Table 11.1. Organisms known and suggested to have holokinetic chromosomes. Taxa believed to consist exclusively of holokinetic members
indicated by "*"
Taxon l Attributes 2 References'

SINGLE-CELLED EUKAR YOTES/PROTOCTIST A
Dinoflagellata Sarma 1983
BacilJariophyta* (= Diatoms) Health 1980
Euglenida Heath 1980
Ciliophora Heath 1980
Actinopoda (= Radiolaria) Grell & Ruthmann 1964
Conjugaphyta* Sharma & Sharma 1984
Desmidaceae King 1953
Zygnemataceae: Spirogyra Godward 1954, 1961
Chlorophyta
Coleochaetales: Coleochaete scutata • Margulis et al. 1990
MULTICELLULAR EUKARYOTES
~ Fungi Brown 1972, Vaarama 1954
w
Plantae
Bryophyta Vaarama 1954
Lycophyta • Jermy et al. 1967
Sphenophyta: Equisetum • Wilson 1928
Pteridophyta Walker 1984
Cycadophyta • Khoshoo 1990 and Sharma & Sharma 1984
Ginkgophyta • Khoshoo 1990
Gnetophyta: Welwitschiaceae • Khoshoo & Ahuja 1963
Coniferophyta • Khoshoo 1990
Angiospermae (Anthophyta):
Monocotyledones
Commedlinidae
Commelinaceae • Morton 1967
Cyperaceae* IMf Sharma & Sharma 1984
Gramineae • Marchant 1967
Juncaceae* IMf Sharma & Sharma 1984
Liliidae • Stebbins 1971
Table 1l.1 . Continued.
Taxon' Attributes' References 3

Dicotyledones:
Magnoliidae and Ranunculidae (=Ranales) Sybenga 1975
Dillcniidae: Cruciferae: Brassica Swanson 1957
Rosidae • Stebbins 1971, John 1990
Animalia
Mesozoa-Rhombozoa: Dicyema aegira Nieuwkoop & Sutasurya 1981
Porifera • Tuzet 1964
Cnidaria • Wijsman & Wijsman-Best 1973
Platyhelminthes Benazzi & Benazzi Lenatati 1976
Nematoda* A, IMm Traintaphyllou 1984, John 1990, and John & Lewis 1965
Rotifera* A • Birky & Gilbert 1971
Chaetognatha • Stevens 1910
Mollusca
Gastropoda • Bajer et al. 1961, Baccetti & Afzelius 1976 and Nath 1965
Bivalvia • Wilson 1928
w Cephalopoda • Gao & Natsukari 1990
Annelida PH,IMf Christiansen 1980
'""'" Tardigrada • Ammermann 1967, and Berton1ani 1975
Arthropoda:
Chelicerata
Acari* A, PH, IMf Present Work
Araneae IMf Benavente & Wettstein 1980
Opiliones • Tsurusaki & Cokendolpher 1990
Pseudoscorpionida • Nath 1965
~corpionida Shanahan 1989
Mandibulata
Crustacea Chandra 1962, Beerman 1977
Cladocera • Nath, 1965
Copepoda Beerman 1977
Decapoda Stefani & Cadeddu 1967
Isopoda IMf Hill 1948
Ostracoda • Nath 1965
Myriapoda
Chilopoda IMm Ansley 1954, White 1973
Diplopoda • Nath 1965
Continued
Table 11.1. Continued.
Taxon' Attributes' References3
Insecta:
Collembola • Nunez 1962
Ephemeroptera • Kiauta & Mol 1977, Brown 1972
Odonata IMfm White 1973, Kiauta & Mol 1977
Blattodea • John & Lewis 1958, White 1976
Dennaptera* White 1976
Isoptera* • John 1983, Syren & Luykx 1977
Orthoptera White 1973, p. 374; John 1990, p. 24
Anoplura* Bayreuther 1955
Hemiptera* IMfm Ueshima 1979
Homoptera* A, PH, IMfm Hughes-Schrader 1948
Mallophaga* Scholl 1955
Tbysanoptera* A White 1973
~ Coleoptera' A, PH, IMf Smith & Virkki 1978, Piza 1958 and Seiler 1948
v. Diptera' A, PH • White 1973, Matuszewski 1961
Hymenoptera" A,PH • Crozier 1975
Lepidoptera* IMf Suoma1ainen 1953
Megaloptera • Hughes-Schrader 1980
Strepsiptera • Rieder & Nowogrodzki 1983
Trichoptera* Suoma1ainen 1966
'Higher categories follow Margulis et al. (1990) for Protoctista, Friis et al. (1987) for Plantae and Brusca and Brusca (1990) for Animalia. The absence of a particular higher taxon
does not imply a monocenlric karyotype. For example, we have not yet checked literature for smaller invertebrate phyla or most of the unicellular eukaryotes. Higher vertebrates,
or at least their large autosomes, have centromeres. Mammalian autosomes feature a distinctive kinetochore.
'Attributes are indicated as: A-arrhenotoky, PH-parahaploidy and 1M-inverted meiosis. specifically IMf-oogenesis. IMm-sperrnatogenesis and IMfm-inverted meiosis in both
sexes. Attributes observed in a taxon do not necessarily apply to all members of that taxon.
'Authors explicitly describe karyotypes as holokinetic and having attributes listed in Table I unless preceded by ..•... which denotes reference(s) used by us in suggesting holokinetic
chromosomes in taxon.
'Smith and Virkki (1978) do not directly diagnose holokinesis or inverted meiosis when interpreting karyotypes. but they effectively grant these conditions in their discussion of
beetles in "the Oedionychina mode" on pages 96 and 136 and elsewhere. Many other species appear to be holokinetic by our diagnosis using descriptions and figures in Smith and
Virkki (1978), i.e .• Elateridae. Lampyridae. Coccinellidae (Fig. 42B. p. 96. p. 135). Chrysomelidae (Fig. 81) and Scolytidae, in particular. i.e .• Xyleborus dispar (Fig. 102).
'For primitive families Sciaridae and Cecidomyiidae. especially their limited or elimination chromosomes.
"Holokinetic-looking karyotypes in Crozier (1975) for Me/ipona quadrifasicata anthidioides. Fig. 25. and Apis cerana indica. Fig. 3.
1961, Sybenga 1981), based on the argument that holokinetic systems have
simpler mechanical constraints, and logically represent greater cellular economy.
Jones (1978), and later Holmquist and Dancis (1980), proposed that the telomeric
regions of holokinetic chromosomes are the probable ancestors of centromeres.
This hypothesis is bolstered by molecular data on monocot plants indicating that
zygDNA segments (DNA synthesized during zygotene) do not actually complete
synthesis until metaphase I (Stem and Hotta 1987). Molecular data explain the
late replicating behavior of end regions and enable the end-to-end pairing that
establishes a half-bivalent from a pair of homologous chromatids.
If such a polarity is correct, perhaps the greater plasticity that holokinetic
chromosomes seemingly confer on a karyotype was significant in eukaryote
evolution. They allow plasticity in two fundamentally different ways, both of
which relate to their demonstrated tolerance of fragmentation and fusion (Section
2.1.1). First they permit reduction in chromosome number by fusion (Schrader
1940, Hughes-Schrader and Schrader 1961) or increase by fission (Ueshima
1979), respectively. As a labile system for karyotype evolution, holokinetic
chromosomes appear superior to monocentric chromosomes, and this evolution-
ary lability extends to sex determination. For example, White (1973) discussed
the plasticity of sex chromosomes in races of the holokinetic morabine grasshop-
pers. The fusion (either tandem or centric) of a holokinetic X with an autosome
permitted male sex determination to shift from XO to XY within the same
population. First division segregation was equational when the fusion was "acro-
centric" and was reductional when the fusion was "metacentric." By ignoring the
widespread existence ofholokinetic chromosomes, we also ignore the explanatory
power of their flexibility as features of karyotype evolution and sex determination
mechanisms.
Second, ho10kinetic systems may be fundamentally different from monocentric
ones in their constraints or permissiveness during early development, cell differen-
tiation, and gene regulation. For example, the greater repair ability of holokinetic
chromosomes should allow injured cells to survive many generations of replica-
tion. Thus they could tolerate damage that would be lethal in monocentric systems
(Evans and Pond 1964).
We believe further that there is a causal link between the type of chromosome
(holokinetic or monocentric) and the type of meiotic division (inverted or normal).
As noted earlier, numerous cytogeneticists (e.g. Rhoades 1961, John 1990) have
argued that inverted meiosis is possible only in holokinetic chromosomes. The
constraint upon monocentric bivalents to co-orient at metaphase I (i.e. have an
axial orientation relative to the spindle) appears to result from the dependence of
chromosomes upon kinetochores for orientation, and from the necessity in animals
for the linkage of kinetochores by microtubules to the centrioles (Peterson and
Berns 1980, Ba1czon and Brinkley 1990).
The phylogenetic consequences of such a causal linkage force a second hypoth-
esis: inverted meiosis could well be ancestral to "normal" meiosis (Halkka 1959,
Suomalainen and Hallcka 1963), and therefore normal meiosis may also have
evolved independently multiple times. This is not an outrageous idea. The evolu-
tionary path to complexity must start with simplicity, and in this context-
from a purely genetic perspective, ignoring the typically cytoplasmic events of
maturation and gamete differentiation-the first (equational) division of inverted
meiosis mimics mitosis. The second (reductional) division is then seen as the
evolutionary innovation, added to the end of an existing process in a parsimonious
manner. Intercalation of a reductional division between equational divisions (i.e.
the "normal" order of meiosis) is viewed as a further innovation. Since in this
case the latter would be the chronologically "inverted" order, we may need
to develop new terminology based on the relative position of the reductional
division.
4.3 Historical Inertia and the Monocentric Paradigm
If holokinetic chromosomes are so common, why are they so poorly appreciated?

Indeed, they virtually have been omitted from the evolutionary cytogenetic syn-
thesis. For example, White (1973) explicitly stated that we can generalize from
the karyology described for Drosophila, maize and humans to the rest of life,
because these organisms share the same key traits, despite their many differences.
He argued that not seeing a primary constriction was not proof of its absence,
leading most workers to identify any chromosomes with telokinetic behavior as
acrocentric. As Peterson and Berns (1980, 103) and Jones (1978, 134) have
noted, there has been remarkable tenacity among both animal and plant cytologists
to believe almost universally in a nonterminal, localized kinetic organization in
chromosomes.
White's three choices to represent life all happen to have a conspicuous centro-
mere that dominates the morphology and behavior of chromosomes in mitosis and
meiosis. Furthermore, each provides elegant genetic confirmation of cytological
behaviors that conform to the chromosomal theory of inheritance. So, White's
inference had added attractiveness: it was a reasonable generalization and it was
confirming the predictions of the most significant biological theory of the early
twentieth century.
Had the great morphological cytologists E. B. Wilson (e.g. 1928) or Franz
Schrader (e.g. 1953) been able to correlate their elegant observations on the
exclusively holokinetic Heteroptera with experimental genetic studies, perhaps
White would have been more circumspect. Although the chromosomes of the
Heteroptera are relatively easy to study, the merging of their cytology and heredity
never happened. Why? Bugs, scales, and aphids are not noted in the annals of
classical genetics because they are not useful model organisms; they do not
generate frequent, conspicuous mutations. Is this just a coincidence, or is there
a link between the type of chromosome system and the stability (i.e. immutability)
of the phenotype?
Consider this situation from an historical perspective. To study patterns of

inheritance, early geneticists had to be able to identify genes with relatively
conspicuous and simple phenotypic effects. The necessity of tracking the trans-
mission and expression of distinctive genotypes predisposed workers to select
organisms having genetic systems that revealed large, visible and viable muta-
tions. More relevant to our argument, these genetic systems had to expose discrete
and unique genetic variants at a relatively high frequency. The organisms selected
by geneticists, Drosophila, maize, mice or humans, possessed genetic systems
that were intrinsically likely to offer the geneticists what they sought. So, it is
no surprise that these chosen lifeforms shared a key trait-centromeres-that
dominated chromosomal movement during mitosis and meiosis.
With the developing body of knowledge about these organisms, the role of the
centromere in chromosome mobility and morphological cytology was seen as
central to mechanical orderliness, so much so that the alternative mechanisms
associated with holokinetic systems were less compelling. Furthermore, mono-
centric chromosomes are generally much larger, take up more stain, and occupy
cells with larger nuclei or have more nuclei undergoing division. As such, they
are simply more amenable to cytological investigation.
The effect of this history is significant. Referring to our earlier theme, there are
two central issues in the evolutionary cytogenetics of thelytokous and haplodiploid
organisms. One is the ability of a thelytoke's restoration mechanism to generate,
maintain, or eliminate heterozygosity (and thus cryptic genetic variability on
which selection could act). The other is the ability of males of haplodiploid
species (having no paternal DNA) to produce recombinant sperm. All applicable
cytogenetic models that could be used for these common reproductive modes are
developed for monocentric systems having normal meiosis (i.e. White 1973, Fig.
19.2). Also, White's (1973, 495) assumption that single-locus genetics should
be comparable in holokinetic systems has been adopted for nearly all organisms.
But his model is backwards for holokinetic organisms with inverted meiosis-the
system that most haplodiploids and thelytokes probably have. Thus, evolutionary
predictions for the genetic stability or flexibility of such organisms have an
erroneous footing-they are "upside-down."
5. Prospectus for Further Research
5.J Empirical Needs
Clearly our case for holokinetic chromosomes being important in the conservation
of mite genomes is based on a paucity of data. The first order of business will be
to document the distribution of holokinetic chromosomes in the major lineages
of parasitiform mites, and to survey the incidence of inverted meiosis (in both
oogenesis and spermatogenesis) in both orders.
Special attention must be paid to basal taxa, those commonly ignored because
they have no direct relevance to man. These include the parasitiform groups
Opilioacarida and Holothryida, as well as acariform groups such as the paraphy-
letic Endeostigmata, and the enarthronote and palaeosomatid Oribatida. Knowl-
edge of early derivative members of any stine and eupodine Prostigmata will also
be needed. Studies of sex determination in mites with similar male and female
karyotypes are also needed. Such information may help put in perspective the
origin of the many wholly thelytokous taxa of Endeostigmata and Oribatida and
the reversal to sexuality during the origin of Astigmata.
As is often noted, independently developed hypotheses of phylogenetic rela-
tionships among investigated taxa are critical to the analysis of any biological
pattern; for mites such hypotheses are developing, but are usually fragmentary
(Norton et al. 1993). Especially helpful will be a hypothesis of phylogeny within
the mesostigmatid taxon Dermanyssina; they have been a focal group for cytology
and reproductive biology, but we have no framework on which to hang the data.
For the big picture we are similarly constrained. Major gaps exist in our
knowledge of chromosome type, meiosis, and phylogenetic relationships of eu-
karyotes. Perhaps our initial attention should be directed toward groups already
known to include taxa with both holokinetic and monocentric chromosomes, such
as nematodes, annelids, beetles, and the entire group of panorpid insect orders.
A synthesis of cytological information and phylogenetic relationships among the
heteropteran insects will be illuminating; they exhibit many parallels with mites,
in both reproductive mode (e. g. parahaploidy, arrhenotoky, thelytoky) and cytol-
ogy. In addition, we need basic karyotype data from virtually all of the "minor"
taxa of lower eukaryotes.
The availability of several molecular tools makes some of these goals more
attainable than in the past. As examples, the CREST antibody, or probes for the
par locus of Escherichia coli, could be used to identify the presence of kineto-
chores (Balczon and Brinkley 1990). Not surprising, nothing is yet known about
the biochemistry of diffuse kinetochores, which reflects the general bias against
holokinetic systems. True sex chromosomes could be identified with the Bkm
satellite DNA technique (Jones 1985). Transposable elements such as mariner4
might be used to track segregation in progeny of thelytokous and sexual mothers
in species having no known sex-determining mechanism.
As an aside, we have noted a potentially important, but unexpected ecological
correlation of holokinetic chromosomes that should be closely examined. The
absence of kine to chores and centrioles, and the use ofkaryomeres and intranuclear
spindles, may be meaningfully related to nutritional regimes. Plants (and fungi)
produce antimitotics, such as caffeine and colchicine, as part of their defensive
arsenal. Caffeine causes the kinetochores of monocentric higher animal chromo-
4"The mariner transposable element is widespread in insects"; H. M. Robertson; Entomological

Society of America meeting, Baltimore, December 8, 1992. Note added in proof: see Nature 362:241-
245.
somes to drop off, leaving the chromosomes lost in a sea of cytoplasm (Balczon
and Brinkley 1990). Animals that suck the sap of plants or fungi are "pre adapted"
to these feeding modes if their genetic systems are unaffected by the antimitotics
generated by their meals. They include the many groups of plant-feeding mites
and homopteran insects that have holokinetic chromosomes. We suggest that
possession of such chromosomes should be an attribute shared by successful sap
feeders of any sort; testing this hypothesis may have economic significance.
5.2 Mending The Cytogenetic Synthesis
It has been more than a decade since Bell (1982) called for the emergence of a
new discipline, "metagenetics," to integrate theory concerning cytogenetics,
population genetics, popUlation ecology and life history. This emergence does
not seem to have occurred, perhaps due in part to the fact that the first of these
components has been incomplete.
Most cytogenetic theory-i.e. our perceptions of how the dynamic processes
of genomic repair and genomic change operate-is based on studies of organisms
having one of two major types of systems: (I) prokaryotes with a single circular
chromosome; or (2) diploid eukaryotes with monocentric chromosomes and nor-
mal meiosis. Clearly, we need to integrate a third type of organism, one having
holokinetic chromosomes and inverted meiosis. Also, we must deal with haplodi-
ploid systems and most forms of thelytoky as modifications of the third type,
rather than the second.
To be functional, a discipline such as "metagenetics" also requires a fifth
component, phylogenetic theory. For example, most models attempting to explain
the evolution of reproductive modes employ an ecological perspective to identify
selective advantages that drive the system. But the perceptions of the holokinetic
system discussed in this chapter have been influenced strongly by combining
cytological information with a phylogenetic perspective. Our belief is that these
perceptions will hold under the weight of badly-needed additional data; our
hope is that they will have heuristic value in unveiling the numerous additional
ramifications of holokinetic systems that must exist.
6. Summary
(1) Acari as a group seem to be characterized by a genetic system

featuring holokinetic chromosomes.
(2) Only holokinetic systems enable inverted meiosis, with equational
segregation of homologous chromatids at anaphase I. This inverted
pattern permits double-strand DNA repair while conserving the ma-
ternal genotype in secondary oocytes.
(3) The cytogenetic and evolutionary predictions for thelytokes with
monocentric systems are not applicable to those with holokinetic
chromosomes and inverted meiosis. When they restore diploidy

by the common mechanism of terminal fusion (or an equivalent),
organisms with inverted meiosis can both edit mutations and repair
adapted genomes, while maintaining the potential for variation.
Wholly thelytokous higher taxa can result; apparent examples of
which are various groups of endeostigmatid and oribatid mites, and
probably bdelloid rotifers.
(4) When functional crossingover is limited, thelytokous species with
terminal fusion automixy and inverted meiosis should faithfully
conserve maternal genome in progeny, and evidence of this is known
for nothroid oribatid mites. Cytogenetically such systems represent
"ideal thelytoky," but they also result in the near clonal reproduction
that is necessary for the evolution of general purpose genotypes
(sensu Lynch 1984).
(5) The restoration of sexuality within a thelytokous lineage-such as

the trhypochthonioid oribatid mites giving rise to Astigmata-is not
a major cytogenetic problem. Parallels are found in various cyclical
parthenogens.
(6) Holokinetic chromosomes and inverted meiosis appear to enable
arrhenotoky and parahaploidy. Haploid males produce just two
sperm per meiotic event and these carry identical halves of the
maternal genome.
(7) Haploid males permit facultative change in genetic recombination.
(8) Many other animals and plants appear to have holokinetic chromo-
somes and thus the potential for inverted meiosis.
(9) Much of the current cytogenetic paradigm is based on monocentric
systems (centromeres and normal meiosis), and ignores the real
possibility that holokinetic chromosomes and inverted meiosis are
ancestral in eukaryotes.
Acknowledgments
We wish to thank D. E. Johnston (The Ohio State University, Columbus; OSU)

and W. T. Atyeo and T. W. Kethley, Jr. (University of Georgia, Athens) for
facilitating this cooperative effort, and our editor, M. A. Houck, for her patience
and support. Constructive comment on the manuscript was provided by R. C.
Jackson (Texas Tech University, Lubbock), H. G. Nelson (FMNH, Chicago),
S. C. Palmer (Cazenovia College, Cazenovia, NY), and A. T. Peterson (FMNH,
Chicago). J. F. Downhower (OSU) provided ideas for Fig. 11.10, and Lavinia
Hales (OSU) helped in assembling references.
References
Alberti, G. 1991. Spermatology in the Acari: systematic and functional implications. In:
The Acari: Reproduction, Development and Life-History Strategies (R. Schuster and P.
W. Murphy eds.). Chapman and Hall Ltd., London. Pp. 77-105.
Ammermann, D. 1967. Die Cytologie der Parthenogenese bei dem Tardiagraden Hypsibius
dujardini. Chromosoma (Berl) 23:203-213.
Ansley, H. R. 1954. Alternative pathways of meiosis in Scutigera. Chromosoma 6:656-
695.
Asher, 1. H., Jr. 1970. Parthenogenesis and genetic variability II. One-locus models for
various diploid popultions. Genetics 66:369-391.
Baccetti, B. and B. A. Afzelius. 1976. The Biology of the Sperm Cell. Monographs in
Developmental Biology 10 (A. Wolsky ed.). S. Karger, NY. 254 pp.
Bacci, G. 1965. Sex Determination. Pergamon Press, NY.
Bacci, G., G. Cognetti and G. Vaccari. 1961. Endomeiosis and sex determination in
Daphnia pulex. Experientia (Basel) 17:505-506.
Bajer, A. E. Hansen-Melander, Y. Melander and J. Mole-Bajer. 1961. Meiosis in Cepea
nemoralis studies by microcinematography. Chromosoma (Berl) 12:374-381.
Balczon, R. D. and B. R. Brinkley. 1990. The kinetochore and its roles during cell
division. In: Chromosomes: Eukaryotic, Prokaryotic, and Viral, Vol. 1 (K. W. Adolph
ed.). CRC Press, Boca Raton. Pp. 167-189.
Battaglia, E. and J. W. Boyes. 1955. Post-reductional meiosis: its mechanism and causes.
Carylogia 8:87-134.
Bayreuther, K. 1955. Holokinetische Chromosomen bei Hematopinus suis (Anoplura,
Haematopinidae). Chromosoma (Berl) 7:260-270.
Beerman, S. 1977. The diminution of heterochromatic chromosomal segments in Cyclops
(Crustacea, Copepoda). Chromosoma (Berl) 60:297-344.
Bell, G. 1982. The Masterpiece of Nature. Univ. Calif. Press, Berkeley. 635 pp.
Benavente, R. and R. Wettstein. 1980. Ultrastructural characterization of the sex chromo-
somes during spermatogenesis of spiders having holocentric chromosomes and a long
diffuse stage. Chromosoma (Berl) 77:69-81.
Benazzi, M. and G. Benazzi Lenatati. 1976. Platyhelminthes. In: Animal Cytogenetics,
Vol. I (B. John ed.). Gebriider Borntraeger, Berlin-Stuttgart. 182 pp.
Bernstein, C. and H. Bernstein. 1991. Aging, Sex and DNA Repair. Academic Press,
Inc., NY. 382 pp.
Bertolani, R. 1975. Citology and systematics in Tardigrada. Mem. 1st. Ital. Idrobiol., 32
(Suppl.):17-35.
Birky, C. W. and J. J. Gilbert. 1971. Parthenogenesis in rotifers; the control of sexual
and asexual reproduction. Am. Zool. II :245-266.
Blackwelder, R. F. 1944. Checklist of the coleopterous insects of Mexico, Central
America, The West Indies, and South America. U.S. Nat. Mus. Bull. 185 (pt. 2):189-
341.
Brown, S. W. 1977. Adaptive status and genetic regulation in major evolutionary changes
of coccid chromosome systems. Nucleus 20: 145-157.
Brown, S. W. and C. Cleveland. 1968. Meiosis in the male of Puto albicans (Coccoidea-
Homoptera). Chromosoma (Bed) 24:210--232.
Brown, S. W. and G. DeLotto. 1959. Cytology and sex ratios of an African species of
armored scale insect (Coccoidea-Diaspididae). Am. Nat. 93:369-379.
Brown, S. W. and W. A. Nelson-Rees. 1961. Radiation analysis of a lecanoid genetic
system. Genetics 46:983-1007.
Brown, S. W. and U. Nur. 1964. Heterochromatic chromosomes in the coccids. Science
145: 130--136.
Brown, W. V. 1972. Textbook of Cytogenetics. C. V. Mosby, St. Louis. 346 pp.
Brusca, R. C. and G. 1. Brusca. 1990. Invertebrates. Sinauer, Sunderland, MA. 922 pp.
Bull, J. J. 1983. Evolution of Sex Determining Mechanisms. Benjamin/Cummings Publ.,
London. 316 pp.
Chandra, H. S. 1962. Inverse meiosis in triploid females of the mealy bug, Planoccus
citri. Genetics 47:1441-1454.
Chapman, R. F. 1969. The Insects. Structure and Function. Elsevier, NY. 919 pp.
Christiansen, B. 1980. Annelida. In: Animal Cytogenetics, Vol. 2 (B. John ed.). Gebriider
Bomtraeger, Berlin-Stuttgart. 81 pp.
Cooper, K. W. 1939. The nuclear cytology of the grass mite, Pediculopsis graminum
(Reut.), with special reference to karyomerokinesis. Chromosoma (Berl) 1:51-103.
Cooper, R. 1972. Experimental demonstration of holokinetic chromosomes, and of differ-
ential "radiosensitivity" during oogenesis in the grass mite, Siteroptes graminum (Reu-
ter). 1. Exp. Zool. 182:69-94.
Crow, J. F. 1992. An advantage of sexual reproduction in a rapidly changing environment.
1. Hered. 83:169-173.
Crozier, R. H. 1975. Hymenoptera. In: Animal Cytogenetics, Vol. 3: Insecta 7 (B. John
ed.). Gebriider Bomtraeger, Berlin-Stuttgart. 95 pp.
Cuellar, O. 1987. The evolution of parthenogenesis: a historical perspective. In: Meiosis
(P. B. Moens, ed.). Academic Press, NY.
Darlington, C. D. 1939. The Evolution of Genetic Systems, 1st Ed. Cambridge Univ.
Press, Cambridge. 149 pp.
Dawkics, R. 1976. The Selfish Gene. Oxford Univ. Press, NY. 352 pp.
de Lillo, E. 1991. Preliminary observations of ovoviviparity in the gall-forming mite,
Aceria caulobius (Nal.) (Eriophyoidea: Eriophyidae). In: The Acari: Reproduction,
Development and Life-history Strategies (R. Schuster and P. W. Murphy eds.). Chap-
man and Hall Ltd., London. Pp. 223-229.
Desch, C. R., Jr. 1984. The reproductive anatomy of Demodex folliculorum (Simon). In:
Acarology VI, Vol. 1 (D. A. Griffiths and C. E. Bowman eds.). Ellis Horwood,
Chichester. pp. 464--469.
Elbadry, E. A. and M. S. F. Tawkik. 1966. Life cycle of the mite Adactylidium sp.
334 I D. L. Wrensch, J. B. Kethley, and R. A. Norton
(Acarina: Pyemotidae), a predator of thrips eggs in the United Arab Republic. Ann.
Evans, H. J. and V. Pond. 1964. The influence ofthe centromere on chromosome fragment
frequency under chronic irradiation. Port. Acta Bioi. (Ser. A) 8: 125-146.
Feiertag-Koppen, C. C. M. and L. P. Pijnacker. 1985. Oogenesis. In: Spider Mites, Their
Biology, Natural Enemies and Control. World Crop Pests, Vol. IA (W. Helle and M.
Sabelis eds). Elsevier, NY. Pp. 117-127.
Flechtmann, C. H. W. and C. A. H. Flechtmann. 1984. Reproduction and chromosomes
in the Broad Mite, Polyphagotarsonemus latus (Banks, 1904) (Acari, Prostigmata,
Tarsonemidae). In: Acarology VI, Vol. I (D. A. Griffiths and C. E. Bowman eds.).
Ellis Horwood Ltd., Chichester. Pp. 455-456.
Friis, E. M., W. G. Chaloner and P. R. Crane. 1987. The Origins of Angiosperms and
their Biological Consequences. Cambridge Univ. Press, Cambridge.
Fujikawa, T. 1987. Biology of Oribatula sakamorii Aoki, a dominant species of the
oribatid fauna in nature farming field. In: Soil Fauna and Soil Fertility. Proc. 9th Int.
Congr. Soil. Zool. (B. R. Strigatova ed.). "Nauka," Moscow. Pp. 544-552.
Futuyma, D. 1. 1986. Evolutionary Biology, 2nd ed. Sinauer, Sunderland, MA. 600 pp.
Gao, Y-M., and Y. Natsukari. 1990. Karyological studies on seven cephalopods. Venus
49:126-145.
Ghiselin, M. T. 1974. The Economy of Nature and the Evolution of Sex. Univ. Calif.
Press, Berkeley. 346 pp.
Godward, M. B. E. 1954. The "diffuse" centromere or polycentric chromosomes in
Spirogyra. Ann. Bot. N.S. 18:143-156.
Godward, M. B. E. 1961. Meiosis in Spirogyra crassa. Heredity 16:53-62.
Goroshchenko, Y. L. 1962. Karyological evidence for the systematic subdivision of the
ticks belonging to the genus Argas Latr. (Ixodoidea, Argasidae), "reflexus" group. Zool.
Zh.41:358-363.
Grell, K. G. and A. Ruthman. 1964. Uber die Karyologie des Radiolars Aulacantha
scolymantha und die Feinstruktur seiner Chromosomen. Chromosoma (Ber!) 15: 185-
211.
Griffing, B. 1982. A theory of natural selection incorporating interaction among individu-
als. X. Use of groups consisting of a mating pair together with haploid and diploid caste
members. J. Theor. Bioi. 95:199-223.
Halkka, O. 1956. Studies on mitotic and meiotic cell division in certain Hemiptera under
normal and experimental conditions. Ann. Acad. Sci. Fenn. (Ser. A IV) 32:1-80.
Halkka, O. 1959. Chromosome studies on the Hemiptera, Homoptera, Auchenorrhyncha.
Ann. Acad. Sci. Fenn. (Ser. A IV) 43:1-72.
Hammer, M. 1965. Are low temperatures a species-preserving factor? Illustrated by the
oribatid mite Mucronothrus nasalis (Willm.). Acta Univ. Lund. (Sect. II) Med. Math.
Sci. Rerum Nat. 2:1-10.
Heath, B. 1980. Variant mitoses in lower eukaryotes: indicators of the evolution of

mitosis? Int. Rev. Cytol. 64:1-80.
Heinemann, R. L. and R. D. Hughes. 1969. The cytological basis for reproductive
variability in the Anoetidae (Sarcoptiformes: Acari). Chromosoma (Berl) 28:346-56.
Heinemann, R. L. and R. D. Hughes. 1970. Reproduction, reproductive organs, and
meiosis in the bisexual nonparthenogenetic mite Caloglyphus mycophagus, with refer-
ence to oocyte degeneration in virgins (Sarcoptiformes: Acaridae). J. Morphol. 130:93-
102.
Helenius, O. 1952. The mode of bivalent orientation in Hemiptera. Hereditas 38:420-
434.
Helle, W. 1985. Genetics. In: Spider Mites, Their Biology, Natural Enemies and Control.
World Crop Pests, Vol. lA (W. Helle and M. W. Sabelis eds.). Elsevier, NY. Pp.
185-192.
Helle, W., H. R. Bolland and W. R. B. Heitmans. 1980. Chromosomes and types of
parthenogenesis in the false spider mites (Acari: Tenuipalpidae). Genetica 54:45-50.
Helle, W., H. R. Bolland and W. R. B. Heitmans. 1981. A survey of chromosome
complements in the Tetranychidae. Int. J. Acarol. 7:147-155.
Helle, W., H. R. Bolland, S. H. M. Jeurissen and G. A. van Seventer. 1984. Chromosome
data on the Actinedida, Tarsonemida and Oribatida. In: Acarology VI, Vol. I (D. A.
Griffiths and C. E. Bowman eds.). Ellis Horwood, Chichester. Pp. 449-454.
Helle, W., H. R. Bolland, R. van Arendonk, R. De Boer, G. G. M. Schulten and V. M.
Russell. 1978. Genetic evidence for biparental males in haplo-diploid predator mites
(Acarina: Phytoseiidae). Genetica 49: 165-171.
Hill, R. 1948. Parthenogenesis beiNagara modesta Dolff (Isopodae). Chromosoma (Berl)
3:232-256.
Holmquist, G. and B. M. Dancis. 1980. A general model of karyotype evolution. Genetica
52/53: 151-163.
Hughes-Schrader, S. 1947. Reversion of XO to XY sex chromosome mechanisms in a
phasmid. Chromosoma 3:52-65.
Hughes-Schrader, S. 1948. Cytology of coccids (Coccoidea-Homoptera). Adv. Genet.
2:127-203.
Hughes-Schrader, S. 1955. The chromosomes of the giant scale Aspidoproctus maximus
Louns. (Coccoidea-Margarodidae) with special reference to asynapsis and sperm forma-
tion. Chromosoma 7:420-438.
Hughes-Schrader, S. 1963. Hermaphroditism in an African coccid, with notes on other
margarodids (Coccoidea-Homoptera). J. Morphol. 113:173-184.
Hughes-Schrader, S. 1980. Segregational mechanisms of sex chromosomes in Megaloptera
(Neuropterida). Chromosoma 8\:307-314.
Hughes-Schrader, S. and H. Ris. 1941. The diffuse spindle attachment of coccids, verified
by the mitotic behavior of induced chromosome fragments. J. Exp. Zool. 87:429-456.
Hughes-Schrader, S. and F. Schrader. 1961. The kinetochore of the Hemiptera. Chro-
mosoma (Berl) 12:327-350.
Husband, R. W. 1972. A new genus and species of mite (Acarina: Podapolipidae)

associated with the coccinellid Cycloneda sanguinea. Ann. Entomol. Soc. Am. 63: 1152-
1162.
Huxley, J. S. 1942. Evolution: The Modern Synthesis. Harper and Brothers, London. 645
pp.
Jenny, A. c., K. Jones and C. Colden. 1967. Cytomorphological variation in Selaginella.
1. Linn. Soc. (Bot.) 60:147.
John, B. 1983. The role of chromosome change in the evolution of orthopteroid insects.
In: Chromosomes in Evolution of Eukaryotic Groups, Vol. I (A. K. Shanna and A.
Shanna eds.). CRC Press, Boca Raton. Pp. 1-110.
John, B. 1990. Meiosis. Cambridge Univ. Press, Cambridge. 396 pp.
John, B. and K. R. Lewis. 1958. Studies on Periplaneta americana III. Selection for
heterozygosity. 1. Hered. 112:181-197.
John, B. and K. R. Lewis. 1965. The meiotic system. Protoplasmatologia 6:1-335.
Jones, G. H. 1987. Chiasmata. In: Meiosis (P. B. Moens ed.). Academic Press, NY. Pp.
213-244.
Jones, K. 1978. Aspects of chromosome evolution in higher plants. Adv. Bot Res. 6: 119-
193.
Jones, K. 1985. Bkm sequences and their conservation. In: The Origin and Evolution of
Sex (H. O. Halvorson and A. Monroy eds.). Alan R. Liss, Inc., NY. Pp. 213-244.
Kethley, 1. 1970. A revision of the family Syringophilidae (Prostigmata: Acarina). Con-
trib. Am. Entomol. Inst. (Ann Arbor) 5:1-76.
Kethley, J. 1971. Population regulation in quill mites (Acarina: Syringophilidae). Ecology
52:1113-1118.
Kethley, J. B. and D. E. Johnston. 1973. A numerical phenetic study of the quill mites
of the family Syringophilidae (Acari). 1. Parasitol. 59:520-530.
Keyl, H.-G. 1957. Zur Karyologie der Hydrachnellen (Acarina). Chromosoma (Berl)
8:719-729.
Khoshoo, T. N. 1990. The selected works of T. N. Khoshoo on Cytogenetics in Relation
to Plant Evolution and Improvement. Counc. Sci. Industr. Res., New Delhi. 728 pp.
Khoshoo, T. N. and M. R. Ahuja. 1963. The chromosomes and relationships of Wel-
witschia mirabilis. Chromosoma 14:522-533.
Kiauta, B. 1969. Some remarks on the evolution of the centromere, based upon the
distribution of centromere types in insects. Genen Phaenen 13:1-6.
Kiauta, B. and A. W. M. Mol. 1977. Behaviour of the spennatocyte chromosomes of the
mayfly, Cloeon dipterum (Linnaeus, 1761) s.l. (Ephemeroptera: Baetidae), with a note
on the cytology of the order. Genen Phaenen 19:31-39.
King, G. C. 1953. "Diffuse" centromeres, and other cytological observations on two
desmids. Nature 171:181.
Krivolutsky, D. A. and A. Va. Druk. 1986. Fossil oribatid mites. Annu. Rev. Entomol.
31:533-545.
Kubai, D. F. 1975. Evolution of the mitotic spindle. Int. Rev. Cytol. 43:167-227.
LaChance, L. E., M. Degrugillier and A. P. Leverich. 1970. Cytogenetics of inherited
partial sterility in three generations of the large milkweed bug as related to holokinetic
chromosomes. Chromosoma (Berl) 29:20-41.
Lamb, R. Y. and R. B. Willey. 1987. Cytological mechanisms ofthelytokous parthenogen-
esis in insects. Genome 29:367-369.
Lewis, K. R. and B. John. 1972. The Matter of Mendelian Heredity, 2nd ed. Longman
Group Ltd., London. 273 pp.
Lynch, M. 1984. Destabilizing hybridization, general-purpose genotypes and geographic
parthenogenesis. Q. Rev. Bioi. 59:257-290.
Manning, J. T. 1976. Is sex maintained to facilitate or minimize mutational advance?
Heredity 36:351-357.
Marchant, C. J. 1967. Evolution in Spartina (Gramineae). II. Chromosomes, basic rela-
tionships and problem of S. x. townsendii agg. J. Linn. Soc. (Bot.) 60:381-409.
Margulis, L., J. O. Corliss, M. Melkonian and D. J. Chapman. 1990. Handbook of
Protoctista. Jones and Bartlett, Boston. 914 pp.
Mather, K. 1953. The genetical structure of populations. In: Symposia of the Society for
Experimental Biology, Number VII. Cambridge Univ. Press, Cambridge. Pp. 66-95.
Matuszewski, B. 1961. Oogenesis in Mikiola fagi Hart. (Cecidomyiidae; Diptera). Chro-
mosoma (Berl) 12:741-811.
Maynard Smith, J. 1978. The Evolution of Sex. Cambridge Univ. Press, Cambridge. 222
pp.
Maynard Smith, J. 1986. Contemplating life without sex. Nature 324:300-301.
Michod, R. E. and B. R. Levin, eds. 1988. The Evolution of Sex. Sinauer, Sunderland,
MA. 342 pp.
Morton, J. K. 1967. The Commelinaceae of West Africa: a biosystematic survey. J. Linn.
Soc. (Bot.). 60:167-221.
Moss, W. W., 1. H. Oliver, Jr. and B. C. Nelson. 1968. Karyotypes and developmental
stages of Harpyrhynchus novoplumaris sp. n. (Acari: Cheyletoidea: Harpyrhynchidae),
a parasite of North American birds. J. Parasitol. 54:377-392.
Murdy, W. H. and H. L. Carson. 1959. Parthenogenesis in Drosophila managabeirai
Malog. Am. Nat. 93:355-363.
Nath, V. 1965. Animal Gametes (Male). Asia Pub!. House, NY. 162 pp.
Nelson-Rees, W. A., M. A. Hoy and R. T. Rousch. 1980. Heterochromatinization, chroma-
tin elimination and haploidization in the parahaploid mite Metaseiulus occidentalis (Nes-
bitt) (Acarina: Phytoseiidae). Chromosoma (Berl) 77:263-276.
Nieuwkoop, P. D. and L. A. Sutasurya. 1981. Primordial Germ Cells in the Invertebrates,
From Epigenesis to Preformation. Cambridge Univ. Press., Cambridge. 258 pp.
Nokkala, S. and C. Nokkala. 1984. Achiasmate mate meiosis in the heteropteran genus
Nabis (Nabidae, Hemiptera). Hereditas 99:131-134.
Nordenskiold, H. 1962. Studies of meiosis in Luzula pupurea. Hereditas 48:503-19.
338 ! D. L. Wrensch, 1. B. Kethley, and R. A. Norton
Norton, R. A., J. B. Kethley, D. E. Johnston and B. M. OConnor. 1993. Phylogenetic

Diversity of Sex Ratio in Insects and Mites (D. L. Wrensch and M. A. Ebbert eds.).
Chapman and Hall, NY. Pp. 8-99.
Norton, R. A. and S. C. Palmer. 1991. The distribution, mechanisms, and evolutionary
significance of parthenogenesis in oribatid mites. In: The Acari: Reproduction, Develop-
ment and Life-history Strategies (R. Schuster and P. W. Murphy eds.). Chapman and
Hall Ltd., London. Pp. 107-136.
Nunez, O. 1962. Cytology of Collembola. Nature 194:946-947.
Nur, U. 1971. Parthenogenesis in coccids (Homoptera). Am. Zool. 11:301-308.
Nuzzaci, G. and M. Solinas. 1984. An investigation into sperm formation, transfer,
storage, and utilization in Eriophyid mites. In: Acarology VI, Vol. I (D. A. Griffiths
and C. E. Bowman eds.). Ellis Horwood, Chichester. Pp. 491-503.
Oliver, J. H., Jr. 1964. Comments on karyotypes and sex determination in the Acari.
Oliver, J. H., Jr. 1965. Karyotypes and sex determination in some dermanyssid mites
(Acarina: Mesostigmata). Ann. Entomol. Soc. Am. 58:567-573.
Oliver, J. H., Jr. 1967. Cytogenetics of Acarines. In: Genetics ofInsect Vectors of Disease
(S. W. Wright and R. Pal eds.). Elsevier, Amsterdam. Pp. 417-439.
Oliver, J. H., Jr. 1977. Cytogenetics of mites and ticks. Annu. Rev. Entomol. 22:407-
429.
Oliver, J. H., Jr. and K. C. Bremner. 1968. Cytogenetics of ticks. 3. Chromosomes and
sex determination in some Australian hard ticks. Ann. Entomol. Soc. Am. 61:837-844.
Oliver, J. H., Jf. and B. C. Nelson. 1967. Mite chromosomes: an exceptionally small
number. Nature 214:809.
Oliver, J. H., Jr., K. Tanaka and M. Sawada. 1973. Cytogenetics of ticks (Acari:
Isodoidea) 12. Chromosome and hybridization studies of bisexual and parthenogenetic
Haemaphysalis iongicornis races from Japan and Korea. Chromosoma (Ber!) 42:209-
288.
Oppermann, E. 1935. Die Entstehung der Riesenspermien von Argas columbarum (Shaw)
(reflexus F.). Z. Mikrosk.-Anat. Forsch. (Leipz.) 37:538-560.
Palmer, S. C. and R. A. Norton. 1990. Further experimental proof of thel ytokous partheno-
genesis in oribatid mites (Acari: Oribatida: Desmonomata). Exp. Appl. Acarol. 8: 149-
159.
Palmer, S. C. and R. A. Norton. 1991. Taxonomic, geographic, and seasonal distribution
of thelytokous parthenogenesis in Desmonomata (Acari: Oribatida). Exp. Appl. Acarol.
12:67-81.
Palmer, S. C. and R. A. Norton. 1992. Genetic diversity in thelytokous oribatid mites
(Acari: Acariformes: Desmonomata). Biochem. Ecol. Syst. 20:219-231.
Piitau, K. 1936. Cytologische Untersuchungen an der haploid-parthenogenetischen Milbe
Pediculoides ventricosus Newpt. Zool. lahrb., Abt. Anat. u. Ontog. (Ber!) 56:277-
322.
Peterson, S. P. and M. W. Berns. 1980. The centriolar complex. Int. Rev. Cytol. 64:81-
105.
Phillips, D. M. 1970. Insect sperm: their structure and morphogenesis. 1. Cell Bioi.
44:243-77.
Pijnacker, L. P. 1985. Spermatogenesis. In: Spider Mites, Their Biology, Natural Enemies
and Control. World Crop Pests, Volume lA (W. Helle and M. Sabelis eds). Elsevier,
NY. Pp . 109-115.
Pijnacker, L. P., M. A. Ferwerda and W. Helle. 1981. Cytological investigations on the
female and male reproductive system of the parthenogenetic privet mite, Brevipalpus
obovatus (Donnadieu) (Phytoptipalpidae, Acari). Acarologia 22:157-163.
Piza, S. de T. 1958. Some interesting aspects of male meiosis in an elaterid beetle.
Caryologia 11:72-78.
Rack, G. and G. C. Eickwort. 1979. Biology and description of a new pygmephorid mite
(Acarina: Tarsonemida) associated with the soil-nesting bee Agapostemon nasutus
(Hymenoptera: Halictidae). Acarologia 21 :267-278.
Regev, S. 1974. Cytological and radioassay evidence of haploid parthenogenesis in
Cheyletus malaccensis. Genetica 45:125-132.
Resende, F. 1953. Consequiencias cito-geneticas do "kinetochoro difuso". Bol. Soc. Port.
Cienc. Nat. 4:252-264.
Reuter, E. 1909. Merokinesis, ein neuer Kemteilungsmodus. Acta Soc. Sci. Fenn. 37:1-
56.
Rhoades, M. M. 1961. Meiosis. In: The Cell. Biochemistry, Physiology, Morphology,
Vol. 1/1, Meiosis and Mitosis (J. Brachet and A. E. Mirsky eds.). Academic Press, NY.
Pp. 1-75.
Rieder, C. L. and R. Nowogrodzki. 1983. Intranuclear membranes and the formation of
the first meiotic spindle in Xenos peckii (Acroshismus wheeleri) oocytes. 1. Cell. Bioi.
97: 1144-1155.
Ris, H. 1942. A cytological and experimental analysis of the meiotic behavior of the
univalent X chromosome in the bearberry aphid Tamalia (= Phyllaphis) coweni (CklI.).
1. Exp. Zool. 90:267-330.
Sabelis, M. W. and C. J. Nagelkerke. 1987. Sex allocation strategies of pseudoarrhenoto-
kous phytoseiid mites. Neth. 1. Zool. 37:117-136.
Sabelis, M. W. and K. Nagelkerke. 1993. Sex allocation and pseudoarrhenotoky in
phytoseiid mites. In: Evolution and Diversity of Sex Ratio in Insects and Mites (D. L.
Wrensch and M. A. Ebbert eds.). Chapman and Hall, NY. Pp. 512-541.
Sarma, Y. S. R. K. 1983. Algal karyology and evolutionary trends. In: Chromosomes in
Evolution of Eukaryotic Groups, Vol 1 (A. K. Sharma and A. Sharma eds.). CRC
Press, Boca Raton. Pp. 177-223.
Scholl, H. 1955. Ein Beitrag zur Kenntnis der Spermatogenese der Mallophagen. Chro-
mosoma (BerI) 7:271-274.
Schrader, F. 1923. Haploidie bei einer Spinnmilbe. Arch. Mikrosk. Anat. 79:610-622.
340 I D. L. Wrensch, J. B. Kethley, and R. A. Norton
Schrader, F. 1935. Notes on the mitotic behavior of long chromosomes. Cytologia 6:422-
430.
Schrader, F. 1936. The kinetochore or spindle fibre in Amphiuma tridactylum. Bioi. Gull.
70:484-498.
Schrader, F. 1940. The formation of tetrads and the meiotic mitoses in the male Rhytiodo-
lomia senilis Say (Hemiptera, Heteroptera). J. Morphol. 67:123-142.
Schrader, F. 1953. Mitosis, 2nd Ed. Columbia Univ. Press, NY. 170 pp.
Seiler, J. 1948. Die Zytologie eines parthenogenetischen Riisselkafers, Otiorrhynchus
sulcatus F. Chromosoma (Berl) 3:88-109.
Shanahan, C. 1989. Cytogenetics of Australian scorpions. I. Interchange polymorphism
in the family Buthidae. Genome 32:882-889.
Sharma, A. K. and A. Sharma. 1984. Trends of chromosome evolution in the plant
kingdom. In: Chromosomes in Evolution of Eukaryotic Groups, Vol II (A. K. Sharma
and A. Sharma eds.). CRC Press, Boca Raton. pp. 227-239.
Shields, W. M. 1982. Philopatry, Inbreeding, and the Evolution of Sex. State Univ. NY
Press, Albany. 245 pp.
Smith, A. W. 1990. Population Dynamics and Chemical Ecology of the Honey Bee
Tracheal Mite, Acarapis woodi (Acari: Tarsonemidae), in Ohio. Ph.D. dissertation,
The Ohio State Univ. 130 pp.
Smith, S. G. and N. Virkki. 1978. Animal Cytogenetics, Vol. 3: Insecta 5. Coleoptera
(B. John ed.). Gebruder Bomtraeger, Berlin-Stuttgart. Pp. 366.
Sokolov, I. I. 1934. Untersuchungen uber die Spermatogenese bei den Arachniden. V.
Uber die Spermatogenese der Parasitidae. Z. ZellJorsch. 21:42-109.
Sokolov, I. I. 1945. Karyo1ogical study of some Acari and the problem of sex determination
in the group. Izv. Akad. Nauk, USSR 6:645-663. (In Russian).
Sokolov, I. I. 1954. The chromosome complex of mites and its importance for systematics
and phylogeny. Tr. O. Estestvoispyt. (Leningrad) 72:124-159. (In Russian).
Sokolov, I. I. 1958. Cytological studies of the development of the male germ cells in
Ornithodoros papillipes Bir. (Acari, Ixodoidea). Rev. Entomol. USSR 37:260-281.
Stebbins, G. L. 1971. Chromosomal Evolution in Higher Plants. Addison-Wesley Publ.,
Reading, MA. 216 pp.
Stefani, R. and G. Cadeddu. 1967. L'attivita centromeric a in Artemia salina. Leach.
Rend. Sem. Fac. Sci. Univ. Cagliari 37:287-291.
Stem, H. and Y. Hotta. 1987. The biochemistry of meiosis. In: Meiosis (P. B. Moens
ed.). Academic Press, NY. pp. 303-333.
Suomalainen, E. 1950. Parthenogenesis in animals. Adv. Genet. 3:193-253.
Suomalainen, E. 1953. The kinetochore and the bivalent structure in the Lepidoptera.
Hereditas 39:88-96.
Suoma1ainen, E. 1966. Achiasmatische Oogenese bei Trichopteran. Chromosoma (Berl)
18:201-207.
Suomalainen, E. and O. Hallcka. 1963. The mode of meiosis in the Psyllina. Chromosoma
(Berl) 14:498-510.
Suomalainen, E., A. Saura and J. Lokki. 1987. Cytology and Evolution in Parthenogene-
sis. CRC Press, Boca Raton.
Swan, D. C. 1934. The hay itch mite, Pediculoides ventricosus (Newport) (Acarina,
Pediculoididae) in South Australia. J. Agric. (S. Aust.) 37:1289-1299.
Swanson, C. 1957. Cytology and Cytogenetics. Prentice-Hall, Englewood Cliffs, NJ. 596
pp.
Sybenga, J. 1975. Meiotic Configurations, A Source of Informationfor Estimating Genetic
Parameters. Monographs on Theoretical and Applied Genetics l. Springer-Verlag,
Berlin. 251 pp.
Sybenga, J. 1981. Specialization in the behaviour of chromosomes on the meiotic spindle.
Genetica 57:143-15l.
Syren, R. M. and P. Luykx. 1977. Permanent segmental interchange complex in the
termite Incisitermes schwarzi. Nature 266:167-168.
Taberly, G. 1958. La cytologie de la parthenogenese chez Platynothrus pettifer (Koch)
(Acarien, Oribate). C. R. Ac. Sc. 147: 1655-1657.
Taberly, G. 1987. Recherches sur la parthenogenese thelytoque de deux especes d'acariens
oribates: Trhypochthonius tectorum (Berlese) et Platynothrus peltifer (Koch). III. Etude
anatomique, histologique et cytologique des femelles parthenogenetiques. Acarologia
28:389-403.
Takenouchi, Y., T. Shiitsu and S. Toshioka. 1970. A chromosome study on two partheno-
genetic ticks, Haemaphysalis bispinosa Newmann and H. longicornis Newmann (Aca-
rina: Ixodidae). J. Hokkaido Univ. Ed. (Sec. II B) 20:45-50.
Templaar, M. J. 1979a. Aberrations ofholokinetic chromosomes and associated lethality
after X-irradiation of meiotic stages in Tetranychus urticae Koch (Acari, Tetranychidae).
Mutat. Res. 61:259-274.
Templaar, M. J. 1979b. Fate offragments and properties of translocations of holokinetic
chromosomes after X-irradiation of mature sperm of Tetranychus urticae Koch (Acari,
Tetranychidae). Mutat. Res. 63:301-316.
Templaar, M. 1. 1980. Radiobiological and structural studies on the chromosomes of the
spider mite Tetranychus urticae Koch. Thesis, Univ. of Groningen (cited in Helle et al.
1984).
Templaar., M. J. 1985. Fine structure and related properties of the chromosomes. In:
Spider Mites, Their Biology, Natural Enemies and Control. World Crop Pests, Vol.
IA (W. Helle and M.W. Sabelis eds.). Elsevier, Amsterdam. Pp. 141-148.
Templaar, M. 1. and L. 1. Drenth-Diephuis. 1984. The nucleolar cycle in karyomeres of
Tetranychus urticae Koch (Acari, Tetranychidae) in relation to replication of fragments
of holokinetic chromosomes. Protoplasma 123:78-82.
Templeton, A. R. 1982. The prophecies of parthenogenesis. In: Evolution and Genetics
of Life Histories (H. Dingle and J. P. Hegmann eds.). Springer-Verlag, NY. pp. 75-
101.
Thoday, J. M. 1953. Components of fitness. In: Symposia of the Society for Experimental
Biology, VII. Cambridge Univ. Press, Cambridge. Pp. 96--113.
Treat, A. E. 1965. Sex-distinctive chromatin and the frequency of males in the moth ear
mite. 1. NY Entomol. Soc. 73:12-18.
Triantaphyllou, A. C. 1984. Chromosomes in evolution of nematodes. In: Chromosomes
in Evolution of Eukaryotic Groups, Vol II (A. K. Sharma and A. Sharma eds.). CRC
Tsurusaki, N. 1986. Parthenogenesis and geographic variation of sex ratio in two species
of Leiobunum (Arachnida, Opiliones). Zool. Sci. 3:517-532.
Tsurusaki, N. and J. C. Cokendolpher. 1990. Chromosomes of sixteen species of har-
vestmen (Arachnida, Opiliones, Caddidae and Phalangiidae). 1. Arachnol. 18: 151-166.
Tuzet, O. 1964. L'origine de la Iignee germinale et la gametogenese chez les Spongiaires.
In: L'Origine de La Lignee Germinale chez Les Vertebres et chez QueLqueLs Groups
d'Invertebres (E. Wolff ed.). Hermann, Paris. Pp. 79-111.
Ueshima, N. 1963. Chromosome behavior of the Cimex pilosellus complex (Cimicidae:
Hemiptera). Chromosoma 14:511-521.
Ueshima, N. 1979. Hemiptera II: Heteroptera. In: Animal Cytogenetics, Vol. 3: Insecta
6 (B. John ed.). Gebriider Bomtraeger, Berlin-Stuttgart. ll7 pp.
Uyenoyama, M. 1987. Genetic transmission and the evolution of reproduction: the signifi-
cance of parent-offspring relatedness to the "cost of meiosis." Evolution 38:87-102.
Vaarama, A. 1954. Cytological observations of Pleurozium schreberi, with special refer-
ence to centromere evolution. Ann. Bot. Soc. Zool. Bot. Fenn. 'Vanamo' 28:1-59.
Walker, T. G. 1984. Chromosomes and evolution in Pteridophytes. In: Chromosomes in
Evolution of Eukaryotic Groups, Vol II (A. K. Sharma and A. Sharma eds.). CRC
Warren, E. 1940. On the genital system of Dermanyssus gallinae and several other
Gamasidae. Ann. Natal. Mus. 9:409-459.
White, M. J. D. 1973. Animal Cytology and Evolution, 3rd ed. Cambridge Univ. Press,
Cambridge. 961 pp.
White, M. 1976. Blattodea, Mantodea, Isoptera, Grylloblattodea, Phasmatodea, Dermapt-
era and Embioptera. In: Animal Cytogenetics, Vol. 3: Insecta 2 (B. John ed.). Gebriider
Bomtraeger, Berlin-Stuttgart. 75 pp.
Whiting, P. W. 1945. The evolution of male haploidy. Q. Rev. Bioi. 20:231-260.
Wijsman, H. J. and M. Wijsman-Best. 1973. A note on the chromosomes of some
madreporian corals from the Mediterranean (Cnidaria, Anthozoa, Scleractinia: Dentro-
phylliidae, Caryophillidae, Faviidae). Genen Phaeen 16:61-64.
Williams, G. C. 1975. Sex and Evolution. Princeton Univ. Press, Princeton. 200 pp.
Wilson, E. B. 1928. Cell in Development and Heredity, 3rd edition. MacMillan, NY.
1232 pp.
Wrensch, D. L. 1993. Evolutionary flexibility through haploid males, or how chance
favors the prepared genome. In: Evolution and Diversity of Sex Ratio in Insects and
Mites (D. L. Wrensch and M. A. Ebbert eds.). Chapman and Hall, NY. Pp. 118-149.
Wrensch, D. L. and M. A. Ebbert, eds. 1993. Evolution and Diversity of Sex Ratio in
Insects and Mites. Chapman and Hall, NY. 630 pp.
Wysoki, M. and E. Swirski. 1968. Karyotypes and sex determination of ten species of
phytoseiid mites (Acarina: Mesostigmata). Genetics 39:220-228.
Young, S. S. Y., D. L. Wrensch and M. Kongchuensin. 1986. Control of sex ratio by
female spider mites. Entomol. Exp. Appl. 40:53-60.
Index *
Acarapis spp., 232 Afrocalvolia spp., 142, 146

Acaridae Afrocalvolia fraxini, 149
adaptation to human habitations, 144 Afrocalvolia natalie, 148
associations with bees, 220, 221, 222-223, Afrocypholaelaps spp., 234
228 Afrocypholaelaps africana, 242
decapod crustaceans as hosts to, 141 Afroxylocopa, 233
exploitation of parasitism, 253 Agapostemon nasutus, 231
habitats created by insects, 142, 143 Age
habitats created by mammals, 144 differential benefits of phoresy by class,
habitats created by plants, 138, 139 258-259
life span under laboratory culture, 147-148 relative survivorship and mortality by class,
soil and litter inhabiting species and demo- 259-261
graphics, 145-146 risks of dispersal by class, 263-264
Acariformes, genetic systems and reproductive simplified reproduction functions for Phyto-
modes, 284 seiidae, 83
Acarinaria, 238 Alaskozetes antarcticus, 107, 114-115
Acarus spp., 140 Aleuroglyphus, ISO
Acarus siro, 178 Algae, marine, 139
Achipteria holomonensis, 107 Algophagidae, 138, 139
Achipteria oudemansi, 107 Algophaginae, 150, 172
Acotyledon spp., 139, 140 Algophagus spp., 139
Acotyledon formosani, 178 Algophagus pennsylvanicus, 164-179
Adaptation Allocalvolia, 139
behavioral to phenology of individual flow- Allodynerus delphinalis, 149
ers, 26-28 Allodynerus rossi, 149
ecological in Poecilochirus carabi, 15-17 Amazilia tobaaci, 26
life-history and lineage success of Astig- Amblyseius idaeus, 72-73
mata, 154-155 Ameronothrus spp., 103
life-history and oribatid mite diversification, Amphiccalvolia hurdi, 271
100 Analgidae, 140
morphological of phoretic mites, 254-255 Ancistrocerus anti/ope, 149, 239
Aeroglyphidae, 139-140, 144, 145 Ancystropus, 197
* Page numbers printed in boldface type refer to tables or figures
345
346 / Index
Andrenidae, 246 associations with bees, 220, 221, 222, 226-

Androlaelaps spp., 195-196,201 230, 235
Androlaelaps casalis, 191 behavior of as treehole inhabitants, 164-172
Androlaelaps hirsti, 190 demographics of, 145-149
Animals description of group, 136-137
astigmid mites and habitats created by, 139- dispersal patterns of, 149-152
141,143-144 evolution of parasitism, 153-154,264-275
dispersal of astigmatid mites, 151 genetic systems and reproductive modes,
holokinetic chromosomes in, 313 284
Anoetus, 143,227-228, 237, 240, 243, 244 habitat associations, 137-143, 144-145
Anthophora, 231 host associations, 141, 143-145, 152-153
Anthophoridae, 224, 244 life-history adaptations and success of lin-
Anthophorinae, 224, 246 eage, 154-155
Antrozous pal/idus, 207 life-history aspects of origin of, 119-122
Ants, 143 life history and reproductive patterns in tree-
Apidae. See also Bees holes, 172-179
astigmatid mites associated with, 143 phoresy in, 254-264
Mesostigmata associated with, 232-234 phylogeny of Oribatida, 101, 102
phylogeny and mites, 244 sexual reproduction and thelytokous ances-
Apid bees, 222-223, 225 tors, 310-311
Apinae, 245 thelytoky and evolutionary relationship with
Apis spp., 227, 244 Trhypochthonioidea, 285-286
Apis cerana, 242 Atopmelidae, 140
Apis mellifera, 242, 307 Auricanoetus , 141
Apomixis, 304-305 Automixis, 305
Arabidopsis thaliana, 47 Axion, 277
Arawana, 277
Archegozetes spp., 124 Bacteria, 162
Archegozetes longisetosus, 108 Baloghella, 154
Arexenia, 141 Bats
Argas reflexus, 30 I as habitats for astigmatid mites, 140-141
Arrhenotoky (HIA) Laelapinae and line to Macronyssidae, 196-
definition of, 284-285 201
evolutionary theory and reproductive advan- Macronyssinae and first Macronyssid radia-
tages of, 286 tion on, 201-206
generational switch to thelytoky, 310-311 Bdelloid rotifers, 307
haplodiploidy and inverted meiosis, 318- Bdellonyssus, 297
319 Bees
reproduction in consecutive generations of evolutionary and phylogenetic considerations
spider mites, 323 in mites associated with, 240-246
sex determination in histiostomatid mites, as habitats for astigmatid mites, 142-143
171 life-history strategies of mites associated
Arthropods with, 234-240
dispersal of astigmatid mites, 151 mites associated with, 226-234
holokinetic chromosomes in species of, taxa of mite hosts, 219-226
313 Beetles, 151,265. See also Hemisarcoptes
as hosts to astigmatid mites, 141, 142 Behavior
as inhabitants of treeholes, 162-164 adaptation to phenology of individual flow-
parasitism and evolution of, 153 ers, 26-28
Askinasia, 141, 153 astigmatid inhabitants of treeholes, 164-172
Astigmata feeding of Proctolaelaps regalis, 57-58
Index I 347
Bet-hedging hypothesis, 118 Cheiromeles, 154

Birds Cheletophyes spp., 230--231, 236, 237
dispersal of astigmatid mites, lSI Cheletophyes apicola, 231
as focus of acarine parasitization, 253 Cheyletus malaccensis, 306
as habitats for astigmatid mites, 140, 141, Chi/oanoetus, 142
144-145 Chi/ocorus spp., Hemisarcoptes and
Rhinonyssidae and great endoparasitic radia- coevolution and future research, 275, 277
tion in,. 2W--211 defensive volley of counterreaction, 274
Sternostoma tracheacolum and contempo- host association, 152
rary Rhinonyssid radiation, 211 materials acquired from, 269, 271
Body size, flower size in relation to, 32--33, reflexed hemolymph and adaptation, 267
34 stenoxenic phoretic relationships, 265
Boletacarus, 139 Chi/ocorus cacti, 265, 266, 268, 270, 273,
Boletoglyphus, 139 276
Bombinae, 245 Chirodiscidae, 140
Bombus, 227, 237 Chiroptoglyphus, 154
Bostrichidae, 142 Chiroptonyssus robustipes, 206, 207, 208
Brachypylina, WI Chirorhynchobiidae, 140
Breeding-group size, 33, 35-38, 39 Chorioptes bovis, 147
Brevipalpus obovatus, 300, 305, 306 Chortoglyphidae, 145, 154
Bromeliaceae, 138 Chromosomes. See also Holokinetic chromo-
Bromeliaglyphus, 138 somes
Brumoides., 277 behavior of in mitosis, 288-292
Bumble bees, 225, 227 general contrast of holokinetic and mono-
centric, 287-296
Caenorhabditus elegans, 47 types of in mites, 297--30 I
Calaenosthanus, 234 Chrysomellidae, 274
Canestriniidae, 141, 153 Cimex, 293
Carabodes willmanni, 107 Cleptoparasitism, 235, 236
Carpenter bees, 226 Clones, oribatid mites, 123. See also
Carpoglyphidae, 145, 230 Thelytoky
Carpoglyphus spp., 138,236 Coccinellidae, 274
Carpoglyphus lactis, 151, 177, 178,230 Cockroaches, 141
Carrier preference, of Poecilochirus carabi, Coevolution
6--7,8-17 Chi/ocorus and Hemisarcoptes, 275, 277
Carrion, astigmatid mites, 140 hummingbird mites and hummingbird-flower
Central fusion, 306, 307, 308--309 mutualism, 23-24
Centrioles, holokinetic chromosomes and, 297 Proctolaelaps regalis and Drosophila, 58
Centromeres, 298-299 Cold environments, oribatid mites, 113-115
Centropogon spp., 27 Coleoglyphus, 273
Centropogon surinamensis, 33, 34 Coleoptera, 141, 142
Cephaelis muscosa, 26 Colletidae, 223
Ceratitis capitata, 261 Collohmannia, 105
Ceratozetes gracilis, 108 Commensalism. See Phoresy
Ceratozetes Iwnanaskis, 109, 112, 113 Comyianoetus, 144
Cerophagopsis, 228 Congovidia, 139
Cerophagus, 229 Conoppia palmicincta, 108
Chaetodactylidae, 143, 230 Corolla tube, 34, 35
Chaetodactylus spp., 143,230,235,243 Costus arabicus, 37
Chaetodactylus krombeini, 149 Courtship rituals, 105
Characteristic prey density, concept of, 86 Creutzeria, 138
348 / Index
Crustaceans, 141, 311 selection for characteristics in hypopus, 264

Cryptonyssus, 208-209 DNA, repair and evolutionary success, 301-
Ctenocolletacarus, 143, 228, 237, 242, 244 304
Ctenocolletes, 228, 242, 244 Draconyssus, 208
Ctenoglyphinae, 154 Drosophila bijasciata, 53
Curculanoetus, 142 Drosophilajunebris, 47
Cyta latirostris, 110 Drosophila mangabeirai, 307, 309
Cytoditidae, 140 Drosophila melanogaster
Cytogenetics, 286-287, 330 cultures of and observation of Proctolaelaps
Czenspinskia transversostriata, 151 regalis, 61-62
P element experiments with Proctolaelaps
Damaeus spp., 103, 104 regalis, 59-61
Damaeus onustus, 110 transposable elements in, 47-53
Daphnia, 311 Drosophila nebulosa, 52
Demographics, See also Age; Development Drosophila parthenogenetica, 307, 309
of astigmatid mites, 145-149 Drosophila willistoni, 50-51, 52
natural stabilizing selection of particular Dung, Histiostomatidae in cattle, 152. See
stage for phoresy, 258-264 also Guano accumulations
Dendrolimnetobionten, 163
Density-dependent population growth, 31, 32 Echimyopodidae, 145, 148, 154
Dermanyssoidea, 187, 188, 189-195 Echimyopus dasypus, 271
Dermanyssus grochovskae, 191 Ecological diversity, 16, 17
Dermanyssus quintus, 191 Ecology, phoresy in Astigmata, 255-257. See
Dermatophagoides, 147, 151-152 also Environment
Dermoglyphidae, 140 Edwardzetes elongatus, 114
Deserts, oribatid mites, 115-116 Egg retention, 103, 104
Desmonomata, 101 Emballonuridae, 205
Detritus, treehole communities, 162 Enarthronota, 10 I
Deutonymphs, 149-150, 153-154 Endoparasites, 210-211
Development. See also Ontogenesis Ensliniella spp., 146, 153
Astigmata in treehole environments, 177 Ensliniella kostylevi, 149
phoresy in Astigmata, 257-258 Ensliniella parasitica, 149
rates of in oribatid mites, 108-109 Ensliniellinae, 142
synchronization and mites associated with Entomophilous heteromorphs, 255
bees, 238-240 Environment, dispersal of astigmatid mites and
Diaspididae, 142 adverse changes in, 151-152. See also
Dinogamasus, 231, 233, 235, 237, 240, 242 Ecology; Habitat
Diplodiploidy Eobrachychthonius oudemansi, 114
as ancestral system in mite orders, 284 Epidamaeus kamaensis, 107
holokinetic chromosomes and kinetic flexi- Epidermoptidae, 140, 153
bility in, 316-317 Epilohmannia, 106
and inverted meiosis, 311, 315-317 Euglossinae, 225, 228
recombination index (RI) and, 321 Euglycyphagidae, 144
sex determination in Naiadacarus arbori- Eukaryotes
cola, 171-172 holokinetic chromosomes and evolution of,
spermatogenesis and sex determination, 324-328
315-316 organisms known and suggested to have ho-
Dispersal lokinetic chromosomes, 312-314
of astigmatid mites, 149-152, 168, 170-172 possibility of horizontal gene transfer
of oribatid mites, 112-113 among, 46-47
risks of by age class, 263-264 Eurog/yphus, 147
Index / 349
Evolution. See also Coevolution; Genetics adaptations of hummingbird flower mites to

association of Hemisarcoptes with seasonal, 24-26
Chi/ocorus, 275-277 behavioral adaptation of mites to phenology
Astigmata and parasitism, 153-154 of individual, 26-28
Dennanyssoid mites and parasitism, 195- size of and mite body size, 32-33, 34
211 size of and mite breeding-group size, 33, 35
genic models for female-biased sex ratios, Forest ecosystems, turnover time for treeholes,
37-38 171
holokinetic chromosomes and cytogenetics, Freshwater environments, oribatid mites in,
286-287 116-117
holokinetic chromosome systems and Fungi
eukaryotes, 324-328 astigmatid mites and habitats created by,
life history aspects of origin of Astigmata, 138-139, 144
119-122 holokinetic chromosomes in taxa, 312
of life history in oribatid mites, 118-119 water-filled treehole communities, 162
life-history patterns in Phytoseiidae, 83-86 Fusacarus, 150
model for life-history, 180 Fusohericia, 139
parasitism and unifying principles, 253
P elements in Drosophilidae, 50-51
Galumna fiabellifera, 107
phoresy in Astigmata and, 255-257
Gastronyssidae, 141
phoresy and transition into parasitism, 264-
Gaudiellidae, 229
275
Gaudoglyphidae, 140
recombination, DNA repair, and success,
Gene-cytotype incompatibility, 49-50
301-304
Generational synchrony, oribatid mites, III
reproductive advantages of arrhenotoky, 286
Genetics. See also Chromosomes; Evolution;
of sexual reproduction, 283-284
P elements; Recombinations; Repro-
of thelytoky, 285-286
duction
Ewingia, 141
horizontal gene transfer, 46-47, 52-53
Ewingiidae, 141
mutations and mobile transposable elements,
Exochromus, 277
47
Eylais setosa, 291
systems of and reproductive modes in mites,
284-285
Fagacarus, 139
Genomes, conservation of, 283-284, 306-310
Fahrenholz's Rule, 189
Glycacaridae, 144
Fecundity
Glycyphagidae, 140, 144, 148, 154
Astigmata and treehole environments, 177-
Glycyphagoidea, 144
178
Glycyphagus domesticus, 145, 150
demographics of astigmatid mites, 145-147
Glycyphagus (Lepidoglyphus) destructor, 150
life history of oribatid mites, 107-108
Glyphanoetus, 239
Feeding
Gohieria, 150
behavior and morphology of Astigmata in
Guano accumulations, 139-140
treehole communities, 166-168
Guanolichidae, 140
behavior of Proctolaelaps regalis, 57-58,
63
classification of the Dennanyssoidea, 188 Habitat
morphology of Proctolaelaps regalis, 54- Astigmata and associations, 137-143, 144-
57,63 145
Female-biased sex ratios, hummingbird flower astigmatid inhabitants of treeholes and niche
mites and breeding-group size, 36-38 breadth, 178-179
Fertilization, thelytoky in oribatid mites, 105 characteristics of water-filled treeholes, 161-
Flowers and flowering 164
350 I Index
life history of oribatid mites in apotypic, Histiostoma spp., 138-139, 142, 144
113-118 Histiostoma feroniarum, 305
phoresy and colonization of fresh, 256-257 Histiostoma laboratorium, 53, 60
Haemagamasus spp., 192, 196, 201 Histiostoma murchei, 146, 150
Haemagamasus ambulans, 190 Holokinetic chromosomes
Haemagamasus liponyssoides, 190, 201 and cytogenetics, 286-287
Haemagamasus pontiger, 192 evidence for in mites, 297-298
Haemagamasus reidi, 201 and evolution of eukaryotes, 324-328
Haemaphysalis spp., 297 kinetic flexibility in diplodiploids, 316-317
Haemaphysalis longicornis, 305 organisms known and suggested to have,
Halarachnidae, 193-195 312-314
Halictacarus, 229 properties of and distribution among mites,
Halictidae, 225, 244, 246 287-301
Halmus, 277 prospectus for future research, 328-330
Hamelia patens, 27-32 Honey bees, 225-226
Haplochthonius variabilis, 116 Hoogstralacarus, 141, 153
Haplodiploidy Horizontal gene transfer, 46-47, 52-53
definition of, 284 Hormosianoetus spp., 138, 139
facultative recombination through production Hormosianoetus mallotae, 164-179
of males, 320, 322, 324 Horstia spp., 228, 229, 235, 239, 243, 244
and inverted meiosis, 317-320 Horstia virginica, 149, 229
percent of eggs containing recombinant Horstiella, 228
chromosomes, 324 Horstiinae, 228-229
recombination index (RI) and, 321 Host-plant morphology, 32-40
Heliconia psittacorum, 27 Host-plant phenology, 24-32
H eliconia trinidatis, 27 Hosts
Hemisarcoptes spp., 142, 152, 153, 265, 275, astigmatid mites and associations, 141, 143-
277 145, 152-153
Hemisarcoptes cooremani, 256, 257, 258, bee taxa as, 219-226
265, 266-271 evolutionary implications of specificity in
Hemisarcoptidae, 142, 145, 229 bee mites, 241-243
Hericia, 139 plant morphology and, 32-40
Hermit crabs, 141 plant phenology and, 24-32
Heterocoptidae, 141, 153 sharing of, 25-26
Heterogony, 306 tracking of, 189
Heterostigmata, 231, 286 Host-sharing, 25-26
Hexanoetus, 144 Host-tracking, 189
Histiogaster spp., 142 Hot environments, oribatid mites, 115-116
Histiogaster arborsignis, 152 Humans
Histioplasma, 232 astigmatid mites and habitations of, 144-
Histiostomatidae 145
associations with bees, 227-228 as focus of acarine parasitization, 253
associations with beetles, 142 Hummingbird flower mites
demographics and humidity, 148 exploitation of bird-plant mutualism, 23-24
dung-breeding insects and dispersal patterns, host-plant morphology and, 32-40
152 host-plant phenology and, 24-32
guano accumulations and communities of, Hummingbirds, dispersal of mites, 26. See
140 also Hummingbird flower mites
habitats created by plants and fungi, 138 Hyadesiidae, 139
human habitations and, 145 Hydrodroma despiciens, 316
mammal hosts, 143 Hydrozetes spp., 103, 105,107,112-113
Index I 351
Hydrozetes lemnae, 109, 117 Lardoglyphus, 140

Hylaeinae, 223-224, 246 Lardophyphidae, 144, 145
Hylaeus, 243 Larviposition, 103, 104
Hymenoptera, 142, 143, 153 Lasioglossum, 227
Hypoaspidinae, 187, 195-196,233 Leafcutter bees, 226
Hypoaspis spp., 195-196,212 Leaves, water-filled treeholes, 162, 167-168
Hypoaspis aculeifer, 190 Lemna gibba, 117
Hypoaspis sensu lato, 233 Lemumyssidae, 141
Hypodectes propus, 271 Lepidacarus ornatissimus, 122
Hypoderatidae, 144, 154 Lepidoptera, 325
Hypopus, 168, 170-171,264. See also Leptus, 230
Astigmata Liacarus cidarus, 104-105
Life cycle
Icerya, 311 astigmatid mites and demographics, 145-
Imparipes spp., 231, 239 149
Imparipes apicola, 239 of Dermanyssoids, 189-195
Inflorescence, host phenology and population of Hormosianoetus mallotae, 169
growth and regulation, 28-32 oribatid mites and parity, 102-105
Insects role of sperm in, 311, 315
astigmatid mites and habitats created by, Life history
142-143 concept of trade-offs, 1-3
dispersal of astigmatid mites, 151 evolution of patterns in Phytoseiidae, 83-86
holokinetic chromosomes in taxa of, 314 of oribatid mites, 102-118
obligate fauna of treeholes, 163 origin of Astigmata, 119-122
Ischnopsyllidae, 197 and reproductive patterns of Astigmata in
Isoptera, 143 treeholes, 172-179
Iteroparity, 119 strategies of mites associated with bees,
Ixodida, 284 234-240
Ixodes ricinus, 206--207 studies on Phytoseiidae, 71-80, 90-94
Limnozetes spp., 103, 106
lornadia larrea, 116 Limnozetes sphagni, 104
loshuella striata, 116 Linobia spp., 141, 153
Jumping genes. See Transposable elements Linobia coccinellae, 141
Liodes, 103
Kanakobia, 141, 153 Liponyssus bacoti, 253
Kanoetus, 146 Listrophoridae, 140
Karyomeres, 297 Litomosoides carinii, 209
Kaszabanoetus, 142 Lobalgidae, 140
Kennethiella spp., 146, 153 Locustacarus spp., 232, 243
Kennethiella trisetosa, 149, 239, 240 Longevity
Konoglyphus, 229 Acaridae under laboratory culture, 147-148
Koptortosoma, 233 Astigmata in treehole environments, 177
K -selected species, 118, 172, 173 of oribatid mites, 109-111
Kuzinia spp., 228, 229 Long-tongued bees, 219, 221, 224-225
Kuzinia laevis, 146 Lophuromyopodinae, 154
Loxanoetus, 141, 154
Laelapinae, 195-201
Laelaps spp., 195-196, 199, 201 Macrocheles spp., 243
Laelaps echidninus, 201 Macrocheles praedafimetorum, 233
Laelaspoides, 233 Macrochelidae, 232-233
Laminosioptidae, 140 Macrochetes, 232-233
352 I Index
Macronyssidae, 193, 196-210 Mitosis, behavior of chromosomes in, 288-

Macronyssus, 202, 210 292
Maerkelotritia, 103 Mochloribatula, 105
Mallota spp., 152 Molossidae, 205
M allota bautias, 171 Molting, 261
M allota posticata, 171 Monobiacarus, 142
Mammals Montgaillardia, 105
dispersal of astigmatid mites, 151 Mormoopidae, 199
as exploitable microhabitats for astigmatid Morphology. See also Feeding
mites, 140--141, 143-144 adaptations of phoretic mites, 254-255
holokinetic chromosomes in, 313 changes in Chilocorus cacti associated with
Maternal genome, 306-310 beetles, 268
Medeus, 143 hummingbird flower mites and host-plant,
Medfly, 261 32-40
Megacanestrinia, 151,273 Mortality
Megachilidae, 142, 143, 224, 226, 229, 230, meaning of U-shaped curve, 262-263
245 in oribatid mites, 109-111
Megachilinae, 229, 246 and relative survivorship by age class, 259-
Megachiroptera, 147, 197-198 261
Megachilopus, 228 Mucronothrus spp., 124
Meiosis, inverted Mucronothrus nasalis, 104, 106, 117,310
diplodiploidy and, 311, 315-317 Mutualism, 23-24, 237-238
evidence of in mites, 299-30 I Myialges, 153
haplodiploidy and, 317-320 Myianoetus, 143
and holokinetic chromosomes in eukaryotes, Myocoptidae, 140--141
325-327 Mystacina spp., 204
normal compared to, 292-296 Mystacina tuberculata, 204-205
recombination index (RI) and, 320 Mystacinidae, 204
Melesodectinae, 154
Meliponapachys, 234 Nagara modesta, 308
Meliponinae, 229, 245 Naiacus, 138
Melissotydeus, 230 Naiadacarus arboricola, 146-147, 152, 164-
Melittiphis spp., 233 179
Melittiphis alvearius, 242 Nanacaroides, 139
Melliponocoptidae, 229-230 Nanacarus, 139
Meristaspis, 197 Necrophorus spp., 2
Mesostigmata Nectar flow rate, 33
Acari associated with bees, 220, 221, 222- Neocypholaelaps spp., 230, 234, 236
223 Neocypholaelaps malayensis, 234
cheliceral morphology and evolutionary Neocypholaelaps phooni, 234
success, 55-56 Neohorstia, 228
chromosome types in, 297 Neohypoaspis spp., 237
genetic systems and reproductive modes, Neohypoaspis ampliseta, 234
284 Neolaelaps spp., 196, 199-201
Mesotrichia, 233 Neolaelaps spinosus, 199,200, 201
Metalabidophorinae, 154 Neoribates gracilis, 110
Microchiroptera, 197 Neosomy, 206-207
Micronychites, 141, 153 Neottiglyphus, 143
Micronychitoides, 141, 153 Nepenthaceae, 138
M icrotritia, 106 Nepenthes, 150
Index / 353
N iadacarus arboricolus, 121 Ornithonyssus sylviarum, 207, 208, 209

Niche. See also Habitat Oromurcia sudetica, 109, 113
breadth of astigmatid inhabitants of tree- Osmia lignaria, 230
holes, 178-179 Otanoetus, 141, 154
functional role of general in animal commu- Oviposition
nity, 188 constraints on rate of egg production, 85
Nicrophorus spp., 3-4, 8-14 estimation of at various rates of, 84
Nidicoles, 144, 145 in phytoseiid mites, 75-78, 81
Nidicolous mites, 152
Nomia spp., 231, 232, 239 Palaeosomata, 10 I
Nomia melanderi, 239 Parahaploidy, 284-285, 319-320
Nothrus spp., 103, 104 . Parancistrocerus julvipes, 149
Nothrus bicilatus, 107 Parapygmephorus costaricanus, 231-232
Nothrus palustris, 104, 107, 305-306 Parapygmephorus (Sicilipes), 231
Notolaelaps spp., 196, 199-201 Parasitellus, 233, 237, 240, 242
Notolaelaps novaguinea, 199 Parasitengona, 284
Notolaelaps spinosus, 197 Parasitidae, 232-233
Nutrition, 234-237, 267. See also Starvation Parasitiformes, 284, 297-298
Nycteribiidae, 197 Parasitism
Nycteridocoptes, 147 Astigmata and evolution of, 153-154
Nycteriglyphus asiaticus, 154 definition of, 252-253
Nycterilichus, 153 evolution of phoresy and transition into,
264-275
Oconnoriidae, 140 multidisciplinary interest in origin of, 253
Ontogenesis, 26fr.267. See also Development origin and evolution of in Dermanyssoid
Oogenesis, 292-294 mites, 195-211
Ophionyssus spp., 297 Parhyposomata, 101
Ophionyssus natricis, 207 Passalozetes, 116
Opomyza germination is , 50 Pedetes capensis, 154
Oppia spp., 291 Pedetopodidae, 154
Oppia concolor, 107 P elements
Oppia nodosa, 107 detection of transmission events, 62-64
Oppiella nova, 107, 108, 109 evidence for horizontal gene transfer of, 52-
Oribatida 53
diversity and phylogeny of, 10 I gene-cytotype incompatibility, 49-50
evolution of life history in, 118-119 geographic distribution of in Drosophila,
genetic systems and reproductive modes, 51-52
284 horizontal gene transfer between Procto-
life history in apotypic habitats, 113-118 laelaps regalis and Drosophila melano-
life-history aspects of origin of Astigmata, gaster, 59-61
119-122 hypothesized origin of, 50-51
life history studies on, 99-101 potential vectors, 53-54
prospectus for future research on, 122-124 structure of, 48
review of life history traits, 102-113 transformations due to insertion of, 48-49
Oribatula sakamorii, 122, 311 Pellonyssus, 208, 210-211
Oribatula tibialis, 112 Pelzneria, 140, 146
Ornithonyssinae, 202, 205, 20fr.210 Pergalumna emarginata, 107
Ornithonyssus spp., 297 Phasmid insects, 307
Ornithonyssus bacoti, 207-208, 209 Phenology, host-plant and hummingbird mites,
Ornithonyssus bursa, 207, 209 24-32
354 I Index
Phoresy dynamics of Astigmatid mites, 176

definition of, 4-5 host phenology and growth and regulation
and developmental synchronization in bee of, 28-32
mites, 238-240 Prelaviposition, 103, 104
dispersal of Astigmata by deutonymphs, Prey, concept of characteristic densities, 86
149-150 Proctolaelaps spp., 23-24, 25-26, 234
evolutionary implications of in bee mites, Proctolaelaps bombophilus, 61
240--241 Proctolaelaps certator, 25, 27
and evolution of parasitism in Astigmata, Proctolaelaps contentiosus, 33, 34
254-258 Proctolaelaps glaucis, 27, 33, 34
evolution of and transition into parasitism, Proctolaelaps hypudaei, 61-62
264-275 Proctolaelaps kirmsei
natural stabilizing selection of particular behavioral adaptation to phenology of indi-
demographic stage for, 258-264 vidual flowers, 27-28
Phylogeny breeding-group size and corolla depth of
and diversity of oribatid mites, 10 I host plant, 35
and evolution of bee mites, 244-246 host plant and population structure and dy-
Phytoseiidae namics, 28-32
characteristics of reproductive schedule of, Proctolaelaps longisetosus, 61
88-89 Proctolaelaps nauphoetae, 61
evolution of life-history patterns in, 83-86 Proctolaelaps regalis
reproduction schedules and effect on intrin- feeding behavior, 57-58
sic rate of increase, 80--83 feeding morphology, 54-57
studies of life-history patterns, 70--80, 90- frequency of observation in Drosophila cul-
94 tures, 61-62
within-species, within-genus, and between- frequency of P element transmission, 63-64
genus trends, 80 incorporation of P elements into genome,
Phytoseiulus persimilis, 81, 85 62-63
Phytotelmata, 160--161. See also Treeholes P element experiments with Drosophila,
Pitcher plants, 138, 150 59-61
Plants. See also Flowers and flowering as potential P element vector. 53-54
astigmatid mites and habitats created by, Proctolaelaps spinosus, 27
138-139 Proctophyllodidae, 140
holokinetic chromosomes in, 312-313 Proctotydeus spp., 230
Platynothrus peltifer, 108, 112, 114, 123, Proctotydeus therapeutikos, 237
305-306 Pro stigmata
Platynothrus skoettsbergi, 113-114 associations with bees, 220, 221, 222, 230--
Pneumocoptidae, 141 232
Pneumolaelaps spp., 233, 240, 242 genetic systems and reproductive modes,
Pneumolaelaps machadoi, 243 284
Podapolipidae, 232 holokinetic chromosomes in, 297
Poecilochirus carabi Pseudacarapis indoapis, 232, 242
carrier preference, 6--7, 8-14 Psoroptes, 147
ecological adaptation, 15-17 Psoroptidid mites, 140, 154
life history traits of, 7 Psyllanoetus, 143
morphological analysis of, 7-8 Psylloglyphus, 143-144
natural history of, 4-6 Pteropus, 199
suitability for study of specialization, 2 Ptyssalgidae, 140
Polistes, 143 Pycnocerini, 142
Population Pyemotes ventricosus, 231
density and mortality rates, 261 Pygmephoridae, 231
Index I 355
Pyroglyphidae, 140, 144, 145 Rhizoglyphus echinopus, 310

Pyroglyphus moriani, 147 Rhizoglyphus robini, 177, 178-179
Pupa, feeding morphology of Proctoiaelaps Rhynchophorus, 142
regalis, 55 Rhyncoptidae, 141
Rhysotritia, 106
Quadroppia, 107 Rhyzobius, 277
Rosensteinia, 141, 153
Radfordiella, 202, 207 Rosensteiniidae, 139, 141, 153, 154
RaiIlietia spp., 194 Rostrozetes foveolatus, 117
Raillietia auris, 194 Rot-holes, tree, 161
Raillietiinae, 194 Roubikia, 230
Rapid-invasion hypothesis, 52 R-selection, 172, 173
Recent Loss Hypothesis, 51-52
Recombination, genetic Sancassania spp., 139, 140, 142, 149-150,
conservation of genomes, 283-284 228, 239
facultative through production of haploid Sancassania anomaIus, 177
males, 320, 322, 324 Sancassania boharti, 170
index (RI) as function of mode of reproduc- Sancassania rodriguezi, 177, 178
tion,321 Saproglyphus, 139
inverted meiosis and index (RI), 320 Saprophagy, 234-237
significance of inverted meiosis, 301-324 Sarcoptes scabiei, 147, lSI
Red velvet mites, 230 Sarcoptidae, 141
Reflexed hemolymph, 267 Sarraceniaceae, 138
Renealmia exaitata, 33, 34 Sarraceniopus, 138, 150
Reproduction Scale insects, 142
evolutionary advantages of arrhentoky, 286 Scarabaeidae, 142
evolution of sexual, 283-284 Scheloribates jijiensis, 104
generalized schedule for phytoseiid mites, Scheloribates Iatipes, 107
72-73, 88-89 Scheloribates paUiduIus, 112
genetic systems and modes of in mites, Schistosoma japonicum, 63
284-285 Schizoglyphidae, 149
and life history of Astigmata in treeholes, Schulzea, 229
172-179 Schwiebea spp., 138, 139, 142
mating position of Proctoiaelaps regalis, Schweibea rocketti, 178
57 Scolianoetus, 142, 146
net rates of in oribatid mites, 111-112 Scolytidae, 142
rate of increase in Phytoseiidae and Tetra- Scutacaridae, 231
nychidae, 80-83 Scutacarus spp., 232, 240, 242
recombination index (Rl) as function of Selection, survivorship curve and, 262
mode, 321 Sellea, 139
sexual from thelytokous ancestors, 310-311 Sennertia, 143, 230, 239, 243, 244
Resource-tracking, 189 Sennertionyx, 228
Rhinonyssidae, 193,210-211 Sex ratio, 35-40
Rhinoseius spp., 23, 25-26 Sexual dimorphism, 105
Rhinoseius chiriquensis, 25 Sexual reproduction. See Reproduction
Rhinoseius colwelli, 25, 27 Short-tongued bees, 219-220, 223-224
Rhinoseius epoecus, 25 Sigmodon hispidus, 209
Rhinoseius jidelis, 37 Siteroptes (=Pediculopsis) graminum, 300
Rhinoseius hirsutus, 26 Skin, mammalian, 147
Rhinoseius richardsoni, 25 Soils, temperate and oribatid mites, 102-113,
Rhizoglyphus spp., 138, 139 122
356 / Index
Solenobia triquetrella, 307 fertilization in oribatid mites, 105-107

Specialization, 2, 17-21 inverted meiosis as explanation for in higher
Speciation, 3, 17-21 taxa, 304-311
Sperm, role in life cycle, 311, 315 recombination index (RI) and, 321
Spermadactyl, of Proctolaelaps regalis, 56 Thyreophagus, 142
Spermatogenesis, 292, 315-316, 317-318 Tinaminyssus, 211
Sphecidae, 142 Tortonia spp., 143, 229
Sphexicozela, 143 Tortonia quadridens, 229
Spinanoetus, 140, 146 Trade-offs, 1-3, 16
Spinternix myoti, 192 Transposable elements
Spinturnicidae, 192 definition of, 46
Starvation, survival of Astigmata in treeholes in Drosophila, 47-53
during, 178 horizontal gene transfer and, 46--47
Steatonyssus spp., 203, 208, 210 potential P element vectors, 53-54
Steatonyssus antrozoi, 200, 203, 204, 207 Treeholes, water-filled
Steatonyssus leptus, 203 behavior of astigmatid inhabitants of, 164-
Steganacarus magnus, 103, 107, 108, 110 172
Sternostoma tracheacolum, 211 characteristics of as mite habitat, 161-164
Stingless bees, 225 habitats of astigmatid mites, 139
Streblidaae, 197 life-history and reproductive patterns of
Suidasia, 150 Astigmata in treeholes, 172-179
Suidasiidae, 144, 145, 229 Tree wounds, 139, 161
Survivorship Trhypochthonioidea, 285-286, 310-311
of Astigmata in treehole habitats, 172-173 Trhypochthonius spp., 124
and mortality by age class, 259-261 Trhypochthonius tecto rum , 305-306
in oribatid mites, 109-111 Trigona, 234
shifting selection pressures at ends of curve, Trimalaconothrus, 103
262 Trixoscelis frontalis, 50
Sweat bees, 225 Trochometridium spp., 239
Syconycteris, 199 Trochometridium tribulatum, 231
Syringobiidae, 140 Tropilaelaps, 234
Tropilichus, 150
Tadarida brasiliensis, 206 Trouessartiidae, 140
Tarsonemidae, 232 Trypoxylon, 229
Tectocepheus spp., 106 Turbinoptidae, 140
Tectocepheus velatus, 115, 123 Typhlodromus occidentalis, 81
Teffius, 151 Tyrolichus casei, 178
Telokinetic behavior, 298-299 Tyrophagus spp., 310
Tenebrionidae, 142 Tyrophagus longior, 151
Terminal fusion, 305-310 Tyrophagus putrescentiae, 177, 178
Tetranychidae (spider mites)
comparison of life history with Phytoseii- Uloma, 142
dae, 71-80
evidence of inverted meiosis in, 300 Varroa spp., 234
reproduction schedules and effect on intrin- Varroa jacobsoni, 242
sic rate of increase, 80-83 Varroa underwoodi, 242
Tetranychus urticae, 287 Vectors, genetic, 47, 53-54
Tetrapedia, 230 Vertebrates, life cycles in Dermanyssoidea as-
Thectochlora alaris, 229 sociated with, 190
Thelytoky Vespacarus spp., 146, 153
evolution of reproductive systems, 285-286 Vespacarus fulvipes, 149
Index / 357
Vespertillionidae, 205-206 Xenaria, 141

Vespidae, 143 Xolalgidae, 140
Vespula, 143 Xyleborus dispar, 325
Vidia spp., 142,229,235,243,244 Xylocopa spp., 226, 231, 233, 239, 242
Vidia undulata, 243 Xylocopa virginica, 229
Viruses, transfer of transposable elements, 47 Xylocopes latipes, 231
Voltinism, oribatid mites, III Xylocopinae, 143, 224-225, 230, 245,
246
Wasps, 229
Winterschmidtia, 142 Zachvatkinibates maritimus, 105
Winterschmidtiidae, 145, 148-149,229-230 Zwickia, 138

L0017 Houck 1994 Mites Ecological and Evolutionary Analyses of Life-History

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L0017 Houck 1994 Mites Ecological and Evolutionary Analyses of Life-History

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Ecological and Evolutionary

SPRINGER-SCIENCE+BUSINESS MEDIA, B.V

Library of Congress Cataloging in Publication Data

British Library Cataloguing in Publication Data available

In Recognition of their Creativity and Life-long

CHAPTER I: Poecilochirus carabi: Behavioral and Life-History

CHAPTER 2: Life-History Patterns of Hummingbird Flower Mites in

CHAPTER 3: Mites as Potential Horizontal Transfer Vectors of

CHAPTER 4: Evolution of Life-History Patterns in the Phytoseiidae. 70

CHAPTER 5: Evolutionary Aspects of Oribatid Mite Life Histories

CHAPTER 6: Life-History Modifications in Astigmatid Mites. 136

CHAPTER 7: Life-History Patterns of Astigmatid Inhabitants of

CHAPTER 8: The Evolution of Parasitism and the Distribution of

CHAPTER 9: Evolution and Life-History Patterns of Mites Associated

CHAPTER 10: Adaptation and Transition into Parasitism from

CHAPTER 11: Cytogenetics of Holokinetic Chromosomes

link generalists to the increasingly extensive and exciting acarologicalliterature

capture the imagination of the public with an understanding of the esthetic

and acknowledge that the

[Quotations extracted from the text of Dr. G. W. Wharton's Keynote Address to

Jonathan M. Brown John B. Kethley

Frank J. Radovsky David Sloan Wilson

Poecilochirus carabi: Behavioral and

The concept of trade-offs is central to many aspects of evolutionary biology.

Figure 1.1. Poecilochirus species clinging to a flying Necrophorus beetle.

2.1 The Beetles (Nicrophorus)

ers, N. orbicollis and N. defodiens. A large proportion of carcasses initially found

2.2 The Mites (Poecilochirus carabi)

families of insects (Hyatt 1980). We will argue that, as currently defined, P.

We have studied Poecilochirus carabi intensively at two sites in Michigan; the

3.J Carrier Preference of Poecilochirus carabi

3.2 Life-History Traits of Poecilochirus carabi

To measure differences in life-history traits that might correlate with carrier-

3.3 Morphological Analysis of Poecilochirus carabi

The analysis of morphological variation in P. carabi was performed on both field-

A principal components analysis (PCA) was performed on a set of log-trans-

4.1 1. Kellogg Biological Station (KBS)

Figure 1.2A (KBS) shows the results of a two-round choice-experiment test

(B) UMBS -- 8/85

"'' '< . . "'

from N. orbicollis are raised in association with N. tomentosus, their progeny

Beetle species N Mean N Mean

4.2 II. University of Michigan Biological Station (UMBS)

As previously stated, UMBS differs from KBS primarily in the addition of a

point of P. carabi, to prefer N. orbicollis is usually to be a latecomer. If arriving

4.3 1lI. The Region Between KBS and UMBS

To further document the relationship between the appearance of N. defodiens and

5.1 Ecological Adaptation in Poecilochirus carabi

Poecilochirus carabi is faced with a complex environment in the form of several

BEETLE COMMUNITY STRUCTURE

point of eliminating a well-adapted specialist from a community in which its

5.2 Specialization and Speciation in Poecilochirus carahi

existing in a mosaic of "one-niche" and "multiple-niche" patches. If species arise

Nt[123] 12114" No[88] 5111 ns

Beetle species preference tests using Poecilochirus carabi captured in: A)

PCI FROM (F) 0.007 0.97

may co-vary with life-history variation) of this group to be problematic. This is

Hyatt, K. H. 1980. Mites of the subfamily Parasitinae (Mesostigmata: Parasitidae) in the

Life-History Patterns of Hummingbird Flower

2. Effects of Host-Plant Phenology on Hummingbird Flower Mites

2.1 Adaptations of Mites to Seasonal Flowering

delimited host-plant repertoire of one to several species of hummingbird-polli-

Floral longevity profoundly affects the lives of hummingbird flower mites.

Remarkably, P. kirmsei repeated the same temporal pattern of behavior in a