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Published in the United States of America<br />
2013 • VOLUME 7 • NUMBER 1<br />
AMPHIBIAN & REPTILE<br />
<strong>CONSERVATION</strong><br />
SPECIAL MEXICO ISSUE<br />
amphibian-reptile-conservation.org<br />
ISSN: 1083-446X eISSN: 1525-9153
Raul E. Diaz<br />
University of Kansas, USA<br />
Editor<br />
Craig Hassapakis<br />
Berkeley, California, USA<br />
Associate Editors<br />
Howard O. Clark, Jr.<br />
Garcia and Associates, USA<br />
Erik R. Wild<br />
University of Wisconsin-Stevens Point, USA<br />
Alison R. Davis<br />
University of California, Berkeley, USA<br />
Assistant Editors<br />
Daniel D. Fogell<br />
Southeastern Community College, USA<br />
David C. Blackburn<br />
California Academy of Sciences, USA<br />
C. Kenneth Dodd, Jr.<br />
University of Florida, USA<br />
Harvey B. Lillywhite<br />
University of Florida, USA<br />
Peter V. Lindeman<br />
Edinboro University of Pennsylvania, USA<br />
Jaime E. Péfaur<br />
Universidad de Los Andes, VENEZUELA<br />
Jodi J. L. Rowley<br />
Australian Museum, AUSTRALIA<br />
Editorial Review Board<br />
Bill Branch<br />
Port Elizabeth Museum, SOUTH AFRICA<br />
Lee A. Fitzgerald<br />
Texas A&M University, USA<br />
Julian C. Lee<br />
Taos, New Mexico, USA<br />
Henry R. Mushinsky<br />
University of South Florida, USA<br />
Rohan Pethiyagoda<br />
Australian Museum, AUSTRALIA<br />
Peter Uetz<br />
Virginia Commonwealth University, USA<br />
Jelka Crnobrnja-Isailovć<br />
IBISS University of Belgrade, SERBIA<br />
Adel A. Ibrahim<br />
Ha’il University, SAUDIA ARABIA<br />
Rafaqat Masroor<br />
Pakistan Museum of Natural History, PAKISTAN<br />
Elnaz Najafımajd<br />
Ege University, TURKEY<br />
Nasrullah Rastegar-Pouyani<br />
Razi University, IRAN<br />
Larry David Wilson<br />
Instituto Regional de Biodiversidad, USA<br />
Allison C. Alberts<br />
Zoological Society of San Diego, USA<br />
Michael B. Eisen<br />
Public Library of Science, USA<br />
Russell A. Mittermeier<br />
Conservation International, USA<br />
Antonio W. Salas<br />
Environment and Sustainable Development, PERU<br />
Advisory Board<br />
Aaron M. Bauer<br />
Villanova University, USA<br />
James Hanken<br />
Harvard University, USA<br />
Robert W. Murphy<br />
Royal Ontario Museum, CANADA<br />
Dawn S. Wilson<br />
AMNH Southwestern Research Station, USA<br />
Walter R. Erdelen<br />
UNESCO, FRANCE<br />
Roy W. McDiarmid<br />
USGS Patuxent Wildlife Research Center, USA<br />
Eric R. Pianka<br />
University of Texas, Austin, USA<br />
Joseph T. Collins<br />
University of Kansas, USA<br />
Cover:<br />
Honorary Member<br />
Carl C. Gans<br />
(1923 – 2009)<br />
Upper left: Bolitoglossa franklini. Photo by Sean Rovito.<br />
Upper right: Diaglena spatulata. Photo by Oscar Medina Aguilar.<br />
Center left: Agkistrodon bilineatus. Photo by Chris Mattison.<br />
Center right: Trachemys gaigeae. Photo by Vicente Mata-Silva.<br />
Lower left: Heloderma horridum. Photo by Tim Burkhardt.<br />
Lower right: Cerro Mariana, Balsas-Tepalcatepec Depression, ca. 12 km NW of Caracuaro, Michoacán.<br />
Photo by Javier Alvarado-Díaz.<br />
Amphibian & Reptile Conservation—Worldwide Community-Supported Herpetological Conservation (ISSN: 1083-446X; eISSN: 1525-9153) is<br />
published by Craig Hassapakis/Amphibian & Reptile Conservation as full issues at least twice yearly (semi-annually or more often depending on<br />
needs) and papers are immediately released as they are finished on our website; http://amphibian-reptile-conservation.org; email:<br />
arc.publisher@gmail.com<br />
Amphibian & Reptile Conservation is published as an open access journal. Please visit the official journal website at:<br />
http://amphibian-reptile-conservation.org<br />
Instructions to Authors: Amphibian & Reptile Conservation accepts manuscripts on the biology of amphibians and reptiles, with emphasis on<br />
conservation, sustainable management, and biodiversity. Topics in these areas can include: taxonomy and phylogeny, species inventories, distribution,<br />
conservation, species profiles, ecology, natural history, sustainable management, conservation breeding, citizen science, social networking,<br />
and any other topic that lends to the conservation of amphibians and reptiles worldwide. Prior consultation with editors is suggested and<br />
important if you have any questions and/or concerns about submissions. Further details on the submission of a manuscript can best be obtained<br />
by consulting a current published paper from the journal and/or by accessing Instructions for Authors at the Amphibian and Reptile Conservation<br />
website: http://amphibian-reptile-conservation.org/submissions.html<br />
© Craig Hassapakis/Amphibian & Reptile Conservation
Copyright: © 2013 Wilson. This is an open-access article distributed under the terms of the Creative Commons Attribution–NonCommercial–NoDerivs<br />
3.0 Unported License, which permits unrestricted use for non-commercial<br />
and education purposes only provided the original author and source are credited.<br />
Amphibian & Reptile Conservation 7(1): i–ii.<br />
PREFACE<br />
AMPHIBIAN & REPTILE <strong>CONSERVATION</strong><br />
SPECIAL MEXICO ISSUE<br />
Citation: Wilson LD. 2013. Preface (Amphibian & Reptile Conservation Special Mexico Issue). Amphibian & Reptile Conservation 7(1): i–ii.<br />
The allure of Mexico first beckoned me in 1957, but only<br />
from across the border, as along with my parents and<br />
sister I was visiting family members in Mission, Texas.<br />
Mission is a bit west of McAllen, just north of the international<br />
border, with Reynosa located on the southern bank<br />
of the Río Bravo directly across from McAllen. We went<br />
to Reynosa just to say we had been in Mexico.<br />
My first herpetological trip to Mexico occurred in<br />
1966, when Ernest A. Liner kindly took me on one of his<br />
many journeys. We traveled as far south as Chiapas, and<br />
saw much of the country and plenty of amphibians and<br />
reptiles.<br />
In the ensuing years, I traveled south of the border on<br />
several occasions, and ultimately visited all but one of<br />
Mexico’s 31 states. Among several others, I took one of<br />
those trips with Louis Porras, the senior author of the paper<br />
on cantils in this issue. I made another extensive trip<br />
with my father, Ward Wendell Wilson, and visited many<br />
of the ancient ruins for which the country is well known.<br />
During my career I have always been interested in<br />
Mexico, although in recent years I spent much of my<br />
time in Central America. Nevertheless, I was delighted<br />
at the opportunity to work on the book Conservation of<br />
Mesoamerican Amphibians and Reptiles (2010), which<br />
dealt with all of Mexico and Central America. This massive<br />
undertaking presented me with the chance to work<br />
closely with two long-time friends, Jerry Johnson, one of<br />
my co-editors, and Louis Porras, the proprietor of Eagle<br />
Mountain Publishing, LC, and both are involved in this<br />
Special Mexico Issue.<br />
The herpetofauna of Mexico is impressive from a<br />
number of perspectives. At 1,227 species, it is almost<br />
twice the size of that of its northern neighbor (presently,<br />
the United States is known to contain 628 native species,<br />
according to the Center for North American Herpetology<br />
[naherpetology.org]; data accessed 17 March 2013);<br />
Mexico, however, is only about one-fifth the size of the<br />
United States. Mexico’s herpetofauna also is larger than<br />
that of the seven Central American nations combined<br />
(1,024 native species, according to Wilson and Johnson<br />
[2010], and my updating since), although the disparity between<br />
Mexico and its southern neighbors is much smaller.<br />
Notably, Central America’s land area is slightly over onefourth<br />
that of Mexico.<br />
The level of endemicity in Mexico also is spectacular.<br />
In this Special Mexico Issue, Wilson, Mata-Silva, and<br />
Johnson report that 482 species of reptiles (excluding<br />
the marine species) of a total of 849 (56.8%) are Mexican<br />
endemics; Wilson, Johnson, and Mata-Silva indicate<br />
that 253 species of amphibians of a total of 378 (66.9%)<br />
are not found outside of Mexico. The combined figure is<br />
736 endemics out of 1,227 species (60.0%), a percentage<br />
substantially higher than that for Central America.<br />
In Central America, 367 endemic species have been recorded<br />
to date (Wilson and Johnson [2010], and my updating<br />
since), which equates to 35.8%. According to the<br />
accounting at the Center for North American Herpetology<br />
website (www.cnah.org), however, compared to the<br />
figures for Mexico (see the two Wilson et al. papers indicated<br />
below), Canada (www.carcnet.ca) and the West<br />
Indies (Powell and Henderson 2012), of the 628 species<br />
listed, 335 are endemic to the United States, for which<br />
the resulting percentage (53.3%) is much closer to that<br />
of Mexico than for Central America. Because the United<br />
States is about five times the size of Mexico, when one<br />
compares the degree of endemism in these two countries<br />
with their respective land areas (area/number of endemics),<br />
the resulting figures (areas from the CIA World Factbook;<br />
www.cia.gov) are as follows: Mexico (1,943,945<br />
km 2 /736 = 2,641); and the United States (9,161,966<br />
km 2 /335 = 25,808). Thus, the area/endemism ratio for the<br />
United States is almost 10 times that of Mexico, indicating<br />
that endemism in Mexico is that much greater than<br />
that of its neighbor to the north. The comparable figure<br />
for Central America is 507,966 km 2 /367 = 1,384, which is<br />
even lower than that for Mexico, and this region already<br />
is regarded as a major source of herpetofaunal diversity<br />
(Wilson et al. 2010).<br />
The Mexican herpetofauna also is of immense importance<br />
and interest from a conservation standpoint. In both<br />
of the Wilson et al. papers indicated below, the authors<br />
applied the Environmental Vulnerability Score (EVS)<br />
measure to Mexico’s herpetofauna and found that 222<br />
of 378 amphibian species (58.7%) and 470 of 841 reptile<br />
species in (55.9%) were assigned an EVS that falls<br />
into the high vulnerability category. In total, 692 species<br />
(56.8%) fall into the highest category of susceptibility to<br />
environmental deterioration. The relatively small portion<br />
amphibian-reptile-conservation.org<br />
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June 2013 | Volume 7 | Number 1 | e62
Preface<br />
of humanity that recognizes the value and critical necessity<br />
of biodiversity is fighting an uphill battle to salvage<br />
as much biodiversity as possible before it disappears into<br />
extinction (Wilson 2006). Given the rate of human population<br />
growth and the commensurate rate of loss of natural<br />
habitats, populations of these unique components of<br />
the Mexican patrimony likely will decline steadily, as is<br />
happening over the remainder of the planet (Raven et al.<br />
2011).<br />
One of the most important imperatives we face, therefore,<br />
is to take appropriate steps to conserve the Mexican<br />
herpetofauna. Toward this end, five papers collectively<br />
written by 10 contributors are expected to appear in this<br />
Special Mexico Issue of Amphibian & Reptile Conservation.<br />
These papers are as follows:<br />
A conservation reassessment of the reptiles of Mexico<br />
based on the EVS measure by Larry David Wilson,<br />
Vicente Mata-Silva, and Jerry D. Johnson.<br />
A taxonomic reevaluation and conservation assessment<br />
of the common cantil, Agkistrodon bilineatus<br />
(Squamata: Viperidae): a race against time by<br />
Louis W. Porras, Larry David Wilson, Gordon W.<br />
Schuett, and Randall S. Reiserer.<br />
Patterns of physiographic distribution and conservation<br />
status of the herpetofauna of Michoacán, Mexico<br />
by Javier Alvarado-Díaz, Ireri Suazo-Ortuño,<br />
Larry David Wilson, and Oscar Medina-Aguilar.<br />
Taxonomic reevaluation and conservation of beaded<br />
lizards, Heloderma horridum (Squamata: Helodermatidae)<br />
by Randall S. Reiserer, Gordon W.<br />
Schuett, and Daniel D. Beck.<br />
A conservation reassessment of the amphibians of<br />
Mexico based on the EVS measure by Larry David<br />
Wilson, Jerry D. Johnson, and Vicente Mata-Silva.<br />
All of these papers deal with issues of herpetofaunal conservation,<br />
and range in coverage from the entire country<br />
of Mexico, through a single Mexican state, to what have<br />
been regarded as single species. Each study provides a set<br />
of recommendations.<br />
These five papers are gathered under this Preface and<br />
an issue cover. The concept behind the cover is to draw<br />
the papers into a coherent whole that reinforces the mission<br />
of the journal, which is to “support the sustainable<br />
management of amphibian and reptile biodiversity.”<br />
Thus, the photograph of Cerro Mariana, located in the<br />
Balsas-Tepalcatepec Depression between Huetamo and<br />
Morelia, in Michoacán, is intended to illustrate dry forest,<br />
the type of vegetation most heavily damaged in Mesoamerica<br />
(Janzen 1988), one of the major features of the<br />
state’s environment and in which a significant portion of<br />
the herpetofauna is found. This type of environment is<br />
inhabited by two of the reptiles featured in this issue, the<br />
common cantil (Agkistrodon bilineatus) and the beaded<br />
lizard (Heloderma horridum), as well as the shovel-headed<br />
treefrog (Diaglena spatulata); all three of these species<br />
are relatively broadly distributed in subhumid environments<br />
along the Pacific coastal region of Mexico, as well<br />
as in the extensive valley of the Balsas and Tepalcatepec<br />
rivers, of which the western portion lies in the state of<br />
Michoacán.<br />
Finally, our aim is to examine the conservation status<br />
of the amphibians and reptiles of Mexico, in general, and<br />
to focus more closely on a state herpetofauna (of Michoacán)<br />
and on two prominent and threatened Mexican flagship<br />
species, the common cantil and the beaded lizard.<br />
Thus, we hope to contribute to the ongoing effort to provide<br />
for a sustainable future for the world’s amphibians<br />
(Stuart et al. 2010) and reptiles (Böhm et al. 2013).<br />
Literature Cited<br />
Böhm M et al. 2013. The conservation status of the<br />
world’s reptiles. Biological Conservation 157: 372–<br />
385.<br />
Janzen DH. 1988. Tropical dry forests: the most endangered<br />
major tropical ecosystem. Pp. 130–137 In:<br />
Biodiversity. Editor, Wilson EO. National Academy<br />
Press, Washington, DC, USA.<br />
Powell R, Henderson RW (Editors). 2012. Island lists of<br />
West Indian amphibians and reptiles. Florida Museum<br />
of Natural History Bulletin 51: 85–166.<br />
Raven PH, Hassenzahl DM, Berg LR. 2011. Environment<br />
(8 th edition). John Wiley & Sons, Inc., Hoboken,<br />
New Jersey, USA.<br />
Stuart SN, Chanson JS, Cox NA, Young BE. 2010. The<br />
global decline of amphibians: current trends and future<br />
prospects. Pp. 2–15 In: Conservation of Mesoamerican<br />
Amphibians and Reptiles. Editors, Wilson<br />
LD, Townsend JH, Johnson JD. Eagle Mountain Publishing,<br />
LC, Eagle Mountain, Utah, USA.<br />
Wilson, EO. 2006. The Creation: An Appeal to Save Life<br />
on Earth. W. W. Norton & Company, New York, New<br />
York, USA.<br />
Wilson LD, Johnson JD. 2010. Distributional patterns<br />
of the herpetofauna of Mesoamerica, a biodiversity<br />
hotspot. Pp. 30–235 In: Conservation of Mesoamerican<br />
Amphibians and Reptiles. Editors, Wilson LD,<br />
Townsend JH, Johnson JD. Eagle Mountain Publishing,<br />
LC, Eagle Mountain, Utah, USA.<br />
Wilson LD, Townsend JH, Johnson JD. 2010. Conservation<br />
of Mesoamerican Amphibians and Reptiles. Eagle<br />
Mountain Publishing, LC, Eagle Mountain, Utah,<br />
USA.<br />
Larry David Wilson<br />
2 May 2013<br />
amphibian-reptile-conservation.org<br />
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June 2013 | Volume 7 | Number 1 | e62
Copyright: © 2013 Johnson et al. This is an open-access article distributed under the terms of the Creative Commons<br />
Attribution–NonCommercial–NoDerivs 3.0 Unported License, which permits unrestricted use for non-commercial<br />
and education purposes only provided the original author and source are credited.<br />
Amphibian & Reptile Conservation 7(1): iii–vi.<br />
DEDICATIONS<br />
Citation: Johnson JD, Porras LW, Schuett GW, Mata-Silva V, Wilson LD. 2013. Dedications (Amphibian & Reptile Conservation Special Mexico Issue).<br />
Amphibian & Reptile Conservation 7(1): iii–vi.<br />
With the publication of this Special Mexico Issue (SMI),<br />
the contributing authors were provided with an opportunity<br />
to dedicate it to herpetologists who have played a significant<br />
role in their lives, as well as the lives of other herpetologists<br />
past and present. Each of the 10 contributors<br />
was asked to identify the person who was most influential<br />
in their respective careers, especially with respect to what<br />
each of them has contributed to SMI. The dedicatees are:<br />
Miguel Álvarez del Toro.<br />
Miguel Álvarez del Toro (August 23, 1917–August 2,<br />
1996) was born in the city of Colima, Colima, México,<br />
according to an obituary in Herpetological Review by Oscar<br />
Flores-Villela and Wendy Hodges in 1999. He moved<br />
to Mexico City in 1932, where he attended and later graduated<br />
from high school. Although his formal education<br />
was limited, his repute as an avid naturalist spread rapidly<br />
and at the age of 21, while still in Mexico City, he began<br />
a long career devoted to a multitude of zoological and<br />
conservation related disciplines. He moved to Chiapas in<br />
1942, and after a short stint as keeper and curator became<br />
the Director of what then was known as the Instituto de<br />
Historia Natural located near downtown Tuxtla Gutiérrez.<br />
His reputation grew exponentially because of his tireless<br />
work at the Zoological Park and Natural History Museum,<br />
his publication record, including books and papers on<br />
numerous vertebrate and invertebrate groups, and his solemn<br />
activism on conservation issues. One of his greatest<br />
legacies was convincing several generations of politicians<br />
in Chiapas to help develop a system of natural protected<br />
areas, and also to expand the Zoological Park and move it<br />
to “El Zapotal,” a relatively pristine site on the southern<br />
edge of the city. That new and remarkable facility was<br />
named “Zoológico Regional Miguel Álvarez del Toro, or<br />
ZOOMAT as it is popularly called today. Because of his<br />
lifetime efforts, “Don Miguel,” as he was called respectfully,<br />
was justly awarded honorary doctoral degrees from<br />
the Universidad de Chapingo, in 1992, and from the Universidad<br />
Autónomo de Chiapas, in 1993. Over his long<br />
career he received a plethora of other awards, and also<br />
was involved in numerous conservation projects in conjunction<br />
with various local, state, national, and international<br />
organizations.<br />
Jerry D. Johnson, an avid “herper” since grade school<br />
and recently discharged from the Marine Corps after a<br />
stint in Viet Nam, enrolled in the 1971 wintermester<br />
course at Fort Hays State University (Kansas), and accompanied<br />
Dr. Charles A. Ely to Chiapas on a migratory<br />
bird study. Dr. Ely, after recognizing Johnson’s eagerness<br />
to search for amphibians and reptiles through all sorts<br />
of tropical and highland environments, included him on<br />
many return trips during the next several years. On that<br />
initial 1971 trip, Johnson briefly met Don Miguel at the<br />
old Zoological Park. In 1974, Dr. Ely arranged for he and<br />
Johnson to pitch tents in Don Miguel’s back yard, located<br />
near the Zoo. This initiated an opportunity to mingle with<br />
all sorts of interesting people, including the Álvarez del<br />
Toro family, their friends, and a continuous flow of traveling<br />
naturalists who were visiting the Zoo. During those<br />
times Johnson realized just how influential Don Miguel’s<br />
scientific and conservation work had become, in Chiapas<br />
and elsewhere. On a typical day, Don Miguel often would<br />
walk among the Zoological Park’s animal enclosures, and<br />
during those walks Jerry came to know him while discussing<br />
the status of herpetology in Chiapas, how conservation<br />
efforts were in dire straits, and pondering his<br />
doubts about the possibility that anything resembling a<br />
natural Chiapas would persist into the future. In 1985,<br />
Don Miguel published a book entitled ¡Asi Era Chiapas!<br />
that described how Chiapas had changed in the 40 years<br />
since he had arrived in the state. Even today, Johnson often<br />
thinks about how habitat destruction had altered the<br />
Chiapan environment since he began investigations there<br />
in 1971, as a college sophomore. He now realizes that<br />
his life and professional experiences have passed rather<br />
quickly, but sadly, environmental decay is accelerating<br />
at an even greater pace. Johnson now concentrates much<br />
of his professional efforts on conservation issues, hoping<br />
that humankind can avoid total environmental devastation.<br />
Jerry also is reasonably sure that Don Miguel really<br />
didn’t expect preservation efforts to be very successful,<br />
amphibian-reptile-conservation.org<br />
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June 2013 | Volume 7 | Number 1 | e64
Dedications<br />
but he didn’t give up his dream of a more conservationoriented<br />
populace by continually teaching people why<br />
preserving natural habitats is important to their own wellbeing,<br />
which probably is the only way conservation will<br />
ever succeed. With great pleasure, Johnson dedicates his<br />
contributions to this special Mexico edition of Amphibian<br />
and Reptile Conservation to Miguel Álvarez del Toro,<br />
who in his opinion was the leading advocate and pioneer<br />
of biodiversity conservation in 20 th century Mexico.<br />
book that set the standard for state herpetological publications.<br />
Roger perhaps is best known as the author of the<br />
best selling book in herpetological history, A Field Guide<br />
to the Reptiles and Amphibians of Eastern North America,<br />
which was illustrated by Isabelle. The book was published<br />
in 1958, and expanded versions followed in 1975,<br />
1991, and 1998. For the majority of amphibian and reptile<br />
enthusiasts and herpetologists living in the eastern part of<br />
the United States during those years, this book became<br />
their bible. In 1973, Roger retired early from the Philadelphia<br />
Zoo, after Isabelle had become ill. The Conants then<br />
moved to Albuquerque, where Roger became an adjunct<br />
professor at the University of New Mexico and devoted<br />
much of his time to herpetology. Isabelle passed away<br />
in 1976, and soon after Roger discovered that his close<br />
friend, Howard K. Gloyd, was terminally ill. Howard had<br />
been busy working on a project that he and Roger started<br />
in 1932, and because of Howard’s deteriorating condition<br />
Roger made an enormous commitment and assured<br />
Howard that the project would be completed. This hugely<br />
important contribution, entitled Snakes of the Agkistrodon<br />
Complex: a Monographic Review, was published<br />
by the Society for the Study of Amphibians and Reptiles<br />
(SSAR) in 1990. During this time Roger also was busy<br />
writing his memoirs, A Field Guide to the Life and Times<br />
of Roger Conant, which was published in 1997 by Selva,<br />
and details his remarkable life and illustrious career.<br />
Roger Conant in his early 20s.<br />
Roger Conant (May 6, 1909–December 19, 2003) was<br />
born in Mamaroneck, New York, USA. As a child he developed<br />
a passion for reptiles, especially snakes, and at<br />
the age of 19 became the Curator of Reptiles at the Toledo<br />
Zoo. After assembling a sizeable collection of reptiles<br />
for public display, he was promoted to General Curator.<br />
Because of the close proximity of Toledo to Ann Arbor,<br />
he occasionally would visit herpetologists at the University<br />
of Michigan and became close friends with a thengraduate<br />
student, Howard K. Gloyd. Eventually, Roger<br />
left Toledo to become the Curator of Herpetology at the<br />
Philadelphia Zoo, and in time became the zoo’s Director.<br />
Throughout his 38-year career at Philadelphia he participated<br />
in weekly radio shows, edited the zoo’s publications,<br />
and made frequent television appearances. During<br />
this time he also helped establish the Philadelphia Herpetological<br />
Society, served as President of the Association<br />
of Zoological Parks and Aquariums, and as President of<br />
the American Association of Ichthyologists and Herpetologists.<br />
In 1947 Roger married Isabelle Hunt Conant,<br />
an accomplished photographer and illustrator who had<br />
been working at the zoo for several years, and during the<br />
following two decades the couple made several collecting<br />
trips to Mexico. Roger’s first of 240 scientific publications<br />
(including 12 books) came at the age of 19; about a<br />
decade later he authored The Reptiles of Ohio, a landmark<br />
amphibian-reptile-conservation.org<br />
iv<br />
Roger Conant in Santa Rosa National Park,<br />
Costa Rica (1982).<br />
Louis W. Porras and Gordon W. Schuett, two very<br />
close friends of Roger’s, were involved at several levels<br />
with the Agkistrodon monograph and Roger’s autobiography.<br />
Because of their mutual interest in Agkistrodon, in<br />
January of 1982 the trio traveled to Costa Rica in search<br />
of cantils and although no individuals were found in the<br />
June 2013 | Volume 7 | Number 1 | e64
field, they managed to secure preserved specimens for<br />
study. In July of that year, Porras returned to Costa Rica<br />
with John Rindfleish and collected what became the holotype<br />
of Agkistrodon bilineatus howardgloydi. Additional<br />
information on the life of Roger Conant appears in an<br />
obituary published in the June 2004 issue of Herpetological<br />
Review. Among several solicited tributes indicating<br />
how Roger had affected his colleague’s lives and careers,<br />
Porras wrote the following summary:<br />
As a giant in herpetology, no doubt many will be writing<br />
about Roger Conant’s amazing organizational skills, attention<br />
to detail, literary contributions, lifelong productivity,<br />
and so on. From a personal perspective, however,<br />
Roger was my friend, mentor, and father figure. He enriched<br />
my life in so many ways, and it would warm his<br />
heart to know that by simply following his example, he<br />
will continue to do so.<br />
Schuett summarized his tribute as follows:<br />
Dedications<br />
In reflection, I have no doubt that Roger Conant possessed<br />
genius. His was not displayed in eccentric mannerisms<br />
and arrogant actions, but in a subtle and quiet<br />
ability to collect, organize, and process information for<br />
large-scale projects. In his research, each and every detail<br />
was painstakingly considered. Roger’s vast achievements<br />
are even more remarkable knowing that he was<br />
largely self-educated. If genius is measured by the degree<br />
to which one’s ideas and work influence others, Roger<br />
stands among the giants of knowledge…Cheers to you,<br />
Roger, to your remarkable and enviable life.<br />
Yes, Indeed!<br />
Aurelio Ramírez-Bautista in Chamela, Jalisco (2011).<br />
Aurelio Ramírez-Bautista was born in Xalapa, Veracruz,<br />
Mexico, and today is a professor and biological investigator<br />
at the Universidad Autónoma del Estado de Hidalgo.<br />
Dr. Ramírez-Bautista has authored or co-authored<br />
more than 100 publications, including five books and<br />
40 book chapters, made numerous presentations on the<br />
ecology and conservation of the Mexican herpetofauna,<br />
and has become one of the leading herpetologists in the<br />
country. During his many years as an educator and researcher,<br />
Dr. Ramírez-Bautista advised numerous bachelor,<br />
master, and doctoral students. Vicente Mata-Silva met<br />
Dr. Ramírez-Bautista in the summer of 1998, as an undergraduate<br />
student working on his thesis on the herpetofauna<br />
of a portion of the state of Puebla. They developed<br />
a friendship, and through Dr. Ramirez-Bautista’s mentoring<br />
Vicente developed a passion for Mexican herpetology,<br />
especially Chihuahuan Desert reptiles, that continued<br />
throughout his undergraduate studies and later through<br />
master’s, doctoral, and post-doctoral work in the Ecology<br />
and Evolutionary Biology program at the University of<br />
Texas at El Paso. They have continued to work on significant<br />
research projects on the conservation and ecology<br />
of the Mexican herpetofauna. Vicente is extremely grateful<br />
to Dr. Ramírez-Bautista for his farsighted and life-altering<br />
introduction to herpetology. Their association has<br />
led to a lifetime friendship, and a road of excitement and<br />
opportunities that Vicente never envisioned possible. Dr.<br />
Ramírez-Bautista is the epitome of what an educator and<br />
mentor should be, providing students the opportunity to<br />
become professional scientists working in a world sorely<br />
in need of commitment to environmental sustainability.<br />
Hobart M. Smith in Mexico (1930).<br />
Hobart Muir Smith (September 26, 1912–March 4,<br />
2013) was born Frederick William Stouffer in Stanwood,<br />
Iowa, USA. At the age of four, he was adopted by Charles<br />
and Frances Smith; both of his adoptive parents died,<br />
however, before Dr. Smith finished college at Kansas<br />
State University (KSU). In the engaging “historical perspective”<br />
written by David Chiszar, Edwin McConkey,<br />
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Dedications<br />
and Margaret M. Stewart and published in the 2004(2)<br />
issue of Copeia, the authors recount an amazing story indicating<br />
that when Dr. Smith (HMS) was in his senior<br />
year in high school he was plagued by tachycardia and<br />
an allergy to caffeine, which ended his interest in running<br />
and led to youthful resolution that they reported as follows:<br />
“If I’m gonna do anything worthwhile, I had better<br />
get to it, because I not gonna live very long” (!). Upon<br />
completing high school, he headed for KSU with expectations<br />
of a major in entomology. A fortunate meeting with<br />
Howard K. Gloyd, a somewhat older student who was<br />
majoring in herpetology, brought HMS a change of heart,<br />
however, and he became determined to study amphibians<br />
and reptiles. He made this decision after having traveled<br />
to the American West on collecting trips with Dr. Gloyd,<br />
whose association with Dr. Conant is discussed above.<br />
Gloyd and his major professor at the University of Michigan,<br />
Dr. Frank Blanchard, suggested that HMS contact<br />
Edward H. Taylor at the University of Kansas (KU). As<br />
noted by Chiszar et al. (2004: 419), “this was probably the<br />
act that cinched HMS to a herpetological orientation and<br />
kiboshed entomology.” In fact, these authors also claim<br />
that “HMS literally collected his BA and moments later<br />
hopped into Taylor’s car bound for Mexico,” and that “the<br />
rest is history.”<br />
Hobart M. Smith and Rozella B. Smith at the<br />
University of Wyoming (1960).<br />
In 1940 (Wilson’s birth year), at age 26, he married<br />
Rozella Pearl Beverly Blood, who he met while both<br />
were graduate students at KU. Their marriage endured<br />
until Rozella’s death in 1987. Dr. Smith began working<br />
in Mexico in 1932, before any of the SMI contributors<br />
was born, and those early collecting trips instilled a lifelong<br />
dedication for studying the Mexican herpetofauna.<br />
Other collecting ventures followed during the remainder<br />
of the decade. The material assembled during these trips<br />
allowed him to begin a life-long journey to record the<br />
composition, distribution, and systematics of the amazing<br />
Mexican herpetofauna. During his long life he authored<br />
more than 1,600 publications, including 29 books––the<br />
greatest output in the history of herpetology. Chiszar et al.<br />
(2004: 421–422) indicated that HMS was most proud of<br />
the three Mexican checklists, the Sceloporus monograph,<br />
the Handbook of Lizards, the comparative anatomy textbook<br />
(which Wilson used when he took the course under<br />
HMS), the Synopsis of the Herpetofauna of Mexico, the<br />
Pliocercus book, and the Candoia monograph. In 1947,<br />
HMS became a professor of zoology at the University of<br />
Illinois at Urbana-Champaign, and remained there until<br />
1968. During this period in his career, one of the SMI<br />
contributors came under his influence. In 1958, Larry David<br />
Wilson graduated from Stephen Decatur High School<br />
in Decatur, Illinois, and the following year enrolled at<br />
Millikin University in that city. After two years and having<br />
exhausted the coursework offered by the biology<br />
department at Millikin, Wilson decided to move to the<br />
U of I, which became a turning point in his life. There,<br />
he met HMS and managed to survive a number of his<br />
courses, including comparative anatomy. During the two<br />
years that led to his graduation, Wilson cemented his interest<br />
in zoology and, due to Smith’s influence, decided<br />
to attend graduate school and major in herpetology. Also,<br />
due to Smith’s interest in Mesoamerican amphibians and<br />
reptiles, Wilson was determined to specialize in studying<br />
these creatures, and in 1962 ventured south and never returned<br />
to live in the flatlands of the “Great Corn Desert.”<br />
In 1983, Wilson had the opportunity to acknowledge his<br />
gratitude to the Smiths by organizing a symposium on the<br />
Mexican herpetofauna in their honor, which was held in<br />
connection with the annual SSAR meeting in Salt Lake<br />
City, Utah. Although much of Wilson’s overall work has<br />
focused on the Honduran herpetofauna, this special issue<br />
on the Mexican herpetofauna provided him with an opportunity<br />
to reawaken his love for the country where his<br />
fieldwork outside the US began in 1966, and to again acknowledge<br />
his debt to Dr. Hobart Muir Smith, one of the<br />
most important people in the history of herpetology. As<br />
Wilson stated in a tribute to HMS on his centenary published<br />
last year in Herpetological Review, “I know I am<br />
only one of many people who are indebted to Dr. Smith<br />
in ways small and large. For me, however, his influence<br />
determined the direction of my career and, in a significant<br />
way, the nature of the contributions I have made to our<br />
field.”<br />
Acknowledgments.—The authors of the papers comprising<br />
the Special Mexico Issue are very grateful to Sally<br />
Nadvornik, who kindly supplied the photographs we used<br />
of her father, Hobart M. Smith, and Uriel Hernández-Salinas,<br />
who helpfully provided the image we used of Aurelio<br />
Ramírez-Bautista. Louis Porras provided the photographs<br />
of Roger Conant. The image of Miguel Álvarez del Toro<br />
was taken from the 3 rd edition of his book, Los Reptiles<br />
de Chiapas.<br />
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Xenosaurus tzacualtipantecus. The Zacualtipán knob-scaled lizard is endemic to the Sierra Madre Oriental of eastern Mexico.<br />
This medium-large lizard (female holotype measures 188 mm in total length) is known only from the vicinity of the type locality<br />
in eastern Hidalgo, at an elevation of 1,900 m in pine-oak forest, and a nearby locality at 2,000 m in northern Veracruz (Woolrich-<br />
Piña and Smith 2012). Xenosaurus tzacualtipantecus is thought to belong to the northern clade of the genus, which also contains X.<br />
newmanorum and X. platyceps (Bhullar 2011). As with its congeners, X. tzacualtipantecus is an inhabitant of crevices in limestone<br />
rocks. This species consumes beetles and lepidopteran larvae and gives birth to living young. The habitat of this lizard in the vicinity<br />
of the type locality is being deforested, and people in nearby towns have created an open garbage dump in this area. We determined<br />
its EVS as 17, in the middle of the high vulnerability category (see text for explanation), and its status by the IUCN and SEMAR-<br />
NAT presently are undetermined. This newly described endemic species is one of nine known species in the monogeneric family<br />
Xenosauridae, which is endemic to northern Mesoamerica (Mexico from Tamaulipas to Chiapas and into the montane portions of<br />
Alta Verapaz, Guatemala). All but one of these nine species is endemic to Mexico. Photo by Christian Berriozabal-Islas.<br />
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Copyright: © 2013 Wilson et al. This is an open-access article distributed under the terms of the Creative Commons<br />
Attribution–NonCommercial–NoDerivs 3.0 Unported License, which permits unrestricted use for non-commercial<br />
and education purposes only provided the original author and source are credited.<br />
Amphibian & Reptile Conservation 7(1): 1–47.<br />
A conservation reassessment of the reptiles of Mexico<br />
based on the EVS measure<br />
1<br />
Larry David Wilson, 2 Vicente Mata-Silva, and 3 Jerry D. Johnson<br />
1<br />
Centro Zamorano de Biodiversidad, Escuela Agrícola Panamericana Zamorano, Departamento de Francisco Morazán, HONDURAS 2,3 Department<br />
of Biological Sciences, The University of Texas at El Paso, El Paso, Texas 79968–0500, USA<br />
Abstract.—Mexico is the country with the most significant herpetofaunal diversity and endemism<br />
in Mesoamerica. Anthropogenic threats to Mexico’s reptiles are growing exponentially, commensurate<br />
with the rate of human population growth and unsustainable resource use. In a broad-based<br />
multi-authored book published in 2010 (Conservation of Mesoamerican Amphibians and Reptiles;<br />
CMAR), conservation assessment results differed widely from those compiled in 2005 by IUCN for<br />
a segment of the Mexican reptile fauna. In light of this disparity, we reassessed the conservation<br />
status of reptiles in Mexico by using the Environmental Vulnerability Score (EVS), a measure previously<br />
used in certain Central American countries that we revised for use in Mexico. We updated the<br />
total number of species for the Mexican reptile fauna from that reported in CMAR, which brought<br />
the new number to 849 (three crocodilians, 48 turtles, and 798 squamates). The 2005 assessment<br />
categorized a small percentage of species in the IUCN threat categories (Critically Endangered, Endangered,<br />
and Vulnerable), and a large number of species in the category of Least Concern. In view<br />
of the results published in CMAR, we considered their approach overoptimistic and reevaluated the<br />
conservation status of the Mexican reptile fauna based on the EVS measure. Our results show an<br />
inverse (rather than a concordant) relationship between the 2005 IUCN categorizations and the EVS<br />
assessment. In contrast to the 2005 IUCN categorization results, the EVS provided a conservation<br />
assessment consistent with the threats imposed on the Mexican herpetofauna by anthropogenic environmental<br />
degradation. Although we lack corroborative evidence to explain this inconsistency, we<br />
express our preference for use of the EVS measure. Based on the results of our analysis, we provide<br />
eight recommendations and conclusions of fundamental importance to individuals committed to<br />
reversing the trends of biodiversity decline and environmental degradation in the country of Mexico.<br />
Key words. EVS, lizards, snakes, crocodilians, turtles, IUCN categories, IUCN 2005 Mexican Reptile Assessment<br />
Resumen.—México es el país que contiene la diversidad y endemismo de herpetofauna más significativo<br />
en Mesoamérica. Las amenazas antropogénicas a los reptiles de México crecen exponencialmente<br />
acorde con la tasa de crecimiento de la población humana y el uso insostenible de los recursos.<br />
Un libro publicado por varios autores en 2010 (Conservation of Mesoamerican Amphibians and<br />
Reptiles; CMAR) produjo resultados sobre conservación ampliamente contrarios a los resultados<br />
de una evaluación de un segmento de los reptiles mexicanos conducida en 2005 por la UICN. A la<br />
luz de esta disparidad, se realizó una nueva evaluación del estado de conservación de los reptiles<br />
mexicanos utilizando una medida llamada el Cálculo de Vulnerabilidad Ambiental (EVS), revisado<br />
para su uso en México. Se actualizó el número de especies de reptiles mexicanos más allá del estudio<br />
de CMAR, por lo que el número total de especies se incrementó a 849 (tres cocodrílidos, 48<br />
tortugas, y 798 lagartijas y serpientes). La evaluación de 2005 de la UICN clasificó una proporción<br />
inesperadamente pequeña de especies en las categorías para especies amenazadas (En Peligro<br />
Crítico, En Peligro, y Vulnerable) y un porcentaje respectivamente grande en la categoría de Preocupación<br />
Menor. En vista de los resultados publicados en CMAR, consideramos que los resultados<br />
de este enfoque son demasiado optimistas, y reevaluamos el estado de conservación de todos los<br />
reptiles mexicanos basándonos en la medida de EVS. Nuestros resultados muestran una relación<br />
inversa (más que concordante) entre las categorizaciones de la UICN 2005 y EVS. Contrario a los<br />
resultados de las categorizaciones de la UICN 2005, la medida de EVS proporcionó una evaluación<br />
para la conservación de reptiles mexicanos que es coherente con las amenazas impuestas por la<br />
degradación antropogénica del medio ambiente. No tenemos la evidencia necesaria para proporcionar<br />
una explicación para esta inconsistencia, pero expresamos las razones de nuestra preferencia<br />
por el uso de los resultados del EVS. A la luz de los resultados de nuestro análisis, hemos<br />
Correspondence. Emails: 1 bufodoc@aol.com (Corresponding author), 2 vmata@utep.edu, 3 jjohnson@utep.edu<br />
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Wilson et al.<br />
construido ocho recomendaciones y conclusiones de importancia fundamental para las personas<br />
comprometidas en revertir las tendencias asociadas con la pérdida de biodiversidad y la degradación<br />
del medio ambiente.<br />
Palabras claves. EVS, lagartijas, culebras, cocodrílidos, tortugas, categorías de UICN, 2005 UICN valoración de<br />
reptiles mexicanos<br />
Citation: Wilson LD, Mata-Silva V, Johnson JD. 2013. A conservation reassessment of the reptiles of Mexico based on the EVS measure. Amphibian &<br />
Reptile Conservation 7(1): 1–47 (e61).<br />
The history of civilization is a history of human beings as<br />
they become increasingly knowledgeable about biological<br />
diversity.<br />
Introduction<br />
Beattie and Ehrlich 2004: 1.<br />
From a herpetofaunal standpoint, Mexico is the most<br />
significant center of diversity in the biodiversity hotspot<br />
of Mesoamerica (Mexico and Central America; sensu<br />
Wilson and Johnson [2010]). Of the 1,879 species of<br />
amphibians and reptiles listed by Wilson and Johnson<br />
(2010) for all of Mesoamerica, 1,203 (64.0%) occur in<br />
Mexico; reptiles are especially diverse in this country,<br />
with 830 species (72.3%) of the 1,148 species distributed<br />
throughout Mesoamerica.<br />
Wilson and Johnson (2010) also reported that the<br />
highest level of herpetofaunal endemism in Mesoamerica<br />
is found in Mexico (66.8% for amphibians, 57.2% for<br />
reptiles [60.2% combined]), with the next highest level<br />
in Honduras (36.2% for amphibians, 19.2% for reptiles<br />
[25.3% combined]). The reported level of herpetofaunal<br />
diversity and endemism in Mexico has continued to increase,<br />
and below we discuss the changes that have occurred<br />
since the publication of Wilson et al. (2010).<br />
Interest in herpetofaunal diversity and endemicity in<br />
Mexico dates back nearly four centuries (Johnson 2009).<br />
Herpetologists, however, only have become aware of the<br />
many threats to the survival of amphibian and reptile<br />
populations in the country relatively recently. The principal<br />
driver of these threats is human population growth<br />
(Wilson and Johnson 2010), which is well documented as<br />
exponential. “Any quantity that grows by a fixed percent<br />
at regular intervals is said to possess exponential growth”<br />
(www.regentsprep.org). This characteristic predicts that<br />
any population will double in size depending on the<br />
percentage growth rate. Mexico is the 11 th most populated<br />
country in the world (2011 Population Reference<br />
Bureau World Population Data Sheet), with an estimated<br />
mid-2011 total of 114.8 million people. The population<br />
of Mexico is growing at a more rapid rate (1.4% rate of<br />
natural increase) than the global average (1.2%), and at a<br />
1.4% rate of natural increase this converts to a doubling<br />
time of 50 years (70/1.4 = 50). Thus, by the year 2061<br />
the population of Mexico is projected to reach about 230<br />
million, and the population density will increase from 59<br />
to 118/km 2 (2011 PBR World Population Data Sheet).<br />
Given the widely documented threats to biodiversity<br />
posed by human population growth and its consequences<br />
(Chiras 2009; Raven et al. 2011), as well as the increasing<br />
reports of amphibian population declines in the late<br />
1980s and the 1990s (Blaustein and Wake 1990; Wake<br />
1991), the concept of a Global Amphibian Assessment<br />
(GAA) originated and was described as “a first attempt<br />
to assess all amphibians against the IUCN Red List Categories<br />
and Criteria” (Stuart et al. 2010). The results of<br />
this assessment were startling, and given broad press<br />
coverage (Conservation International 2004; Stuart et al.<br />
2004). Stuart et al. (2010) reported that of the 5,743 species<br />
evaluated, 1,856 were globally threatened (32.3%),<br />
i.e., determined to have an IUCN threat status of Critically<br />
Endangered (CR), Endangered (EN), or Vulnerable<br />
(VU). An additional 1,290 (22.5%) were judged as Data<br />
Deficient (DD), i.e., too poorly known for another determinable<br />
status. Given the nature of the Data Deficient<br />
category, eventually these species likely will be judged<br />
in one of the threat categories (CR, EN, or VU). Thus,<br />
by adding the Data Deficient species to those determined<br />
as globally threatened, the total comes to 3,146 species<br />
(54.8% of the world’s amphibian fauna known at the<br />
time of the GAA). Our knowledge of the global amphibian<br />
fauna has grown since the GAA was conducted, and<br />
a website (AmphibiaWeb) arose in response to the realization<br />
that more than one-half of the known amphibian<br />
fauna is threatened globally or too poorly known to conduct<br />
an evaluation. One of the functions of this website is<br />
to track the increasing number of amphibian species on a<br />
global basis. On 8 April 2013 we accessed this website,<br />
and found the number of amphibian species at 7,116, an<br />
increase of 23.9% over the number reported in Stuart et<br />
al. (2010).<br />
As a partial response to the burgeoning reports of<br />
global amphibian population decline, interest in the conservation<br />
status of the world’s reptiles began to grow<br />
(Gibbons et al. 2000). Some of this interest was due to<br />
the recognition that reptiles constitute “an integral part<br />
of natural ecosystems and […] heralds of environmental<br />
quality,” just like amphibians (Gibbons et al. 2000: 653).<br />
Unfortunately, Gibbons et al. (2000: 653) concluded that,<br />
“reptile species are declining on a global scale,” and further<br />
(p. 662) that, “the declines of many reptile populations<br />
are similar to those experienced by amphibians in<br />
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Conservation reassessment of Mexican reptiles<br />
Dermatemys mawii. The Central American river turtle is known from large river systems in Mexico, from central Veracruz southward<br />
into Tabasco and Chiapas and northeastward into southwestern Campeche and southern Quintana Roo, avoiding the northern<br />
portion of the Yucatan Peninsula. In Central America, it occurs in northern Guatemala and most of Belize. The EVS of this single<br />
member of the Mesoamerican endemic family Dermatemyidae has been calculated as 17, placing it in the middle of the high vulnerability<br />
category, and the IUCN has assessed this turtle as Critically Endangered. This image is of an individual emerging from its<br />
egg, with its egg tooth prominently displayed. The hatching took place at the Zoológico Miguel Álvarez del Toro in Tuxtla Gutiérrez,<br />
Chiapas, as part of a captive breeding program for this highly threatened turtle. The parents of this hatchling came from the<br />
hydrologic system of the Río Usumacinta and Playas de Catazajá. Photo by Antonio Ramírez Velázquez.<br />
Terrapene mexicana. The endemic Mexican box turtle is distributed from southern Tamaulipas southward to central Veracruz and<br />
westward to southeastern San Luis Potosí. Its EVS has been determined as 19, placing it in the upper portion of the high vulnerability<br />
category, but this turtle has not been evaluated by IUCN. This individual is from Gómez Farias, Tamaulipas, within the Reserva<br />
de la Biósfera El Cielo. Photo by Elí García Padilla.<br />
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Wilson et al.<br />
terms of taxonomic breath, geographic scope, and severity.”<br />
They also identified the following significant threats<br />
to reptile populations: habitat loss and degradation, introduced<br />
invasive species, environmental pollution, disease<br />
[and parasitism], unsustainable use, and global climate<br />
change. Essentially, these are the same threats identified<br />
by Vitt and Caldwell (2009) in the Conservation Biology<br />
chapter of their textbook Herpetology.<br />
In the closing chapter of Conservation of Mesoamerican<br />
Amphibians and Reptiles, Wilson and Townsend<br />
(2010: 774–777) provided six detailed and intensely<br />
critical recommendations for the conservation of the<br />
herpetofauna of this region, based on the premise that<br />
“problems created by humans … are not solved by treating<br />
only their symptoms.” Because of the nature of these<br />
recommendations, we consider it important to note that<br />
the IUCN conducted a conservation assessment of the<br />
Mexican reptiles in 2005, for which the results were made<br />
available in 2007 (see NatureServe Press Release, 12<br />
September 2007 at www.natureserve.org). The contents<br />
of this press release were startling and unexpected, however,<br />
as indicated by its title, “New Assessment of North<br />
American Reptiles Finds Rare Good News,” and contrast<br />
the conclusions of Wilson and Townsend (2010), which<br />
were based on the entire herpetofauna of Mesoamerica.<br />
The principal conclusion of the press release was that “a<br />
newly completed assessment of the conservation status<br />
of North American reptiles shows that most of the group<br />
is faring better than expected, with relatively few species<br />
at severe risk of extinction.” Wilson and Townsend<br />
(2010: 773) commented, however, that “conserving the<br />
Mesoamerican herpetofauna will be a major challenge<br />
for conservation biologists, in part, because of the large<br />
number of species involved and the considerable number<br />
that are endemic to individual countries, physiographic<br />
regions, and vegetation zones.”<br />
Given the contrast in the conclusions of these two<br />
sources, and because the 2005 Mexican reptile assessment<br />
was based on the IUCN categories and criteria<br />
without considering other measures of conservation status,<br />
herein we undertake an independent reassessment of<br />
the reptile fauna of Mexico based on the Environmental<br />
Vulnerability Score (EVS), a measure developed by<br />
Wilson and McCranie (2004) for use in Honduras, which<br />
was applied to the herpetofauna of certain Central American<br />
countries in Wilson et al. (2010), and modified in<br />
this paper for use in Mexico.<br />
The IUCN System of Conservation Status<br />
Categorization<br />
The 2005 Mexican reptile assessment was conducted<br />
using the IUCN system of conservation status categorization.<br />
This system is used widely in conservation biology<br />
and applied globally, and particulars are found at the<br />
IUCN Red List of Threatened Species website (www.<br />
iucnredlist.org). Specifically, the system is elaborated in<br />
the online document entitled “IUCN Red List of Categories<br />
and Criteria” (2010), and consists of nine categories,<br />
identified and briefly defined as follows (p. 9):<br />
Extinct (EX): “A taxon is Extinct when there is no reasonable<br />
doubt that the last individual has died.”<br />
Extinct in the Wild (EW): “A taxon is Extinct in the<br />
Wild when it is known only to survive in cultivation,<br />
in captivity or as a naturalized population (or populations)<br />
well outside the past range.”<br />
Critically Endangered (CR): “A taxon is Critically Endangered<br />
when the best available evidence indicates<br />
that it meets any of the criteria A to E for Critically<br />
Endangered, and it is therefore considered to be facing<br />
an extremely high risk of extinction in the wild.”<br />
Endangered (EN): “A taxon is Endangered when the<br />
best available evidence indicated that it meets any of<br />
the criteria A to E for Endangered, and is therefore<br />
considered to be facing a very high risk of extinction<br />
in the wild.”<br />
Vulnerable (VU): “A taxon is Vulnerable when the best<br />
available evidence indicates that it meets any of the<br />
criteria A to E for Vulnerable, and it is therefore considered<br />
to be facing a high risk of extinction in the<br />
wild.”<br />
Near Threatened (NT): “A taxon is Near Threatened<br />
when it has been evaluated against the criteria but<br />
does not quality for Critically Endangered, Endangered,<br />
or Vulnerable now, but is close to qualifying<br />
for or is likely to qualify for a threatened category in<br />
the near future.<br />
Least Concern (LC): “A taxon is Least Concern when<br />
it has been evaluated against the criteria and does not<br />
qualify for Critically Endangered, Endangered, Vulnerable<br />
or Near Threatened. Widespread and abundant<br />
taxa are included in this category.”<br />
Data Deficient (DD): “A taxon is Data Deficient when<br />
there is inadequate information to make a direct, or<br />
indirect, assessment of its risk of extinction based on<br />
its distribution and/or population status.”<br />
Not Evaluated (NE): “A taxon is Not Evaluated when<br />
it is has not yet been evaluated against the criteria.”<br />
As noted in the definition of the Near Threatened category,<br />
the Critically Endangered, Endangered, and Vulnerable<br />
categories are those with a threat of extinction in the<br />
wild. A lengthy discussion of criteria A to E mentioned<br />
in the definitions above is available in the 2010 IUCN<br />
document.<br />
A Revised EVS for Mexico<br />
In this paper, we revised the design of the EVS for Mexico,<br />
which differs from previous schemes in the components<br />
of geographic distribution and human persecution.<br />
Initially, the EVS was designed for use in instances<br />
where the details of a species’ population status (upon<br />
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Trachemys gaigeae. The Big Bend slider is distributed along the Rio Grande Valley in south-central New Mexico and Texas, as well<br />
as in the Río Conchos system in Chihuahua. Its EVS has been calculated as 18, placing it in the upper portion of the high vulnerability<br />
category, and the IUCN has assessed this turtle as Vulnerable. This individual is from the Rio Grande about 184 straight kilometers<br />
SE of Ciudad Juarez, Chihuahua. Although the picture was taken on the US side (about 44 km SSW of Van Horn, Hudspeth<br />
County, Texas), it was originally in the water. Photo by Vicente Mata-Silva.<br />
Kinosternon oaxacae. The endemic Oaxaca mud turtle occurs in southern Oaxaca and adjacent eastern Guerrero. Its EVS has been<br />
estimated as 15, placing it in the lower portion of the high vulnerability category, and the IUCN considers this kinosternid as Data<br />
Deficient. This individual was found in riparian vegetation along the edge of a pond in La Soledad, Tututepec, Oaxaca. Photo by<br />
Vicente Mata-Silva.<br />
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which many of the criteria for the IUCN status categorizations<br />
depend) are not available, so as to estimate its<br />
susceptibility to future environmental threats. In this<br />
regard, the EVS usually can be calculated as soon as a<br />
species is described, as it depends on information generally<br />
available when the species is discovered. Use of<br />
the EVS, therefore, does not depend on population assessments,<br />
which often are costly and time consuming.<br />
Nonetheless, its use does not preclude the implementation<br />
of other measures for assessing the conservation status<br />
of a species, when these measures can be employed.<br />
After all, conservation assessment measures are only a<br />
guide for designing conservation strategies, and constitute<br />
an initial step in our effort to protect wildlife.<br />
The version of the EVS algorithm we developed for<br />
use in Mexico consists of three scales, for which the values<br />
are added to produce the Environmental Vulnerability<br />
Score. The first scale deals with geographic distribution,<br />
as follows:<br />
1 = distribution broadly represented both inside<br />
and outside Mexico (large portions of range are<br />
both inside and outside Mexico)<br />
2 = distribution prevalent inside Mexico, but<br />
limited outside Mexico (most of range is inside<br />
Mexico)<br />
3 = distribution limited inside Mexico, but prevalent<br />
outside Mexico (most of range is outside<br />
Mexico)<br />
4 = distribution limited both inside and outside<br />
Mexico (most of range is marginal to areas<br />
near border of Mexico and the United States or<br />
Central America)<br />
5 = distribution only within Mexico, but not restricted<br />
to vicinity of type locality<br />
6 = distribution limited to Mexico in the vicinity of<br />
type locality<br />
The second scale deals with ecological distribution<br />
based on the number of vegetation formations occupied,<br />
as follows:<br />
1 = occurs in eight or more formations<br />
2 = occurs in seven formations<br />
3 = occurs in six formations<br />
4 = occurs in five formations<br />
5 = occurs in four formations<br />
6 = occurs in three formations<br />
7 = occurs in two formations<br />
8 = occurs in one formation<br />
The third scale relates to the degree of human persecution<br />
(a different measure is used for amphibians), as follows:<br />
1 = fossorial, usually escape human notice<br />
2 = semifossorial, or nocturnal arboreal or aquatic,<br />
nonvenomous and usually non-mimicking,<br />
sometimes escape human notice<br />
3 = terrestrial and/or arboreal or aquatic, generally<br />
ignored by humans<br />
4 = terrestrial and/or arboreal or aquatic, thought to<br />
be harmful, might be killed on sight<br />
5 = venomous species or mimics thereof, killed on<br />
sight<br />
6 = commercially or non-commercially exploited<br />
for hides, meat, eggs and/or the pet trade<br />
The score for each of these three components is added to<br />
obtain the Environmental Vulnerability Score, which can<br />
range from 3 to 20. Wilson and McCranie (2004) divided<br />
the range of scores for Honduran reptiles into three categories<br />
of vulnerability to environmental degradation, as<br />
follows: low (3–9); medium (10–13); and high (14–19).<br />
We use a similar categorization here, with the high category<br />
ranging from 14–20.<br />
For convenience, we utilized the traditional classification<br />
of reptiles, so as to include turtles and crocodilians,<br />
as well as lizards and snakes (which in a modern context<br />
comprise a group).<br />
Recent Changes to the Mexican Reptile<br />
Fauna<br />
Our knowledge of the composition of the Mexican reptile<br />
fauna keeps changing due to the discovery of new<br />
species and the systematic adjustment of certain known<br />
species, which adds or subtracts from the list of taxa that<br />
appeared in Wilson et al. (2010). Since that time, the following<br />
nine species have been described:<br />
Gopherus morafkai: Murphy et al. (2011). ZooKeys<br />
113: 39–71.<br />
Anolis unilobatus: Köhler and Vesely (2010). Herpetologica<br />
66: 186–207.<br />
Gerrhonotus farri: Bryson and Graham (2010). Herpetologica<br />
66: 92–98.<br />
Scincella kikaapoda: García-Vásquez et al. (2010).<br />
Copeia 2010: 373–381.<br />
Lepidophyma cuicateca: Canseco-Márquez et al.<br />
(2008). Zootaxa 1750: 59–67.<br />
Lepidophyma zongolica: García-Vásquez et al.<br />
(2010). Zootaxa 2657: 47–54.<br />
Xenosaurus tzacualtipantecus: Woolrich-Piña and<br />
Smith (2012). Herpetologica 68: 551–559.<br />
Coniophanes michoacanensis: Flores-Villela and<br />
Smith (2009). Herpetologica 65: 404–412.<br />
Geophis occabus: Pavón-Vázquez et al. (2011). Herpetologica<br />
67: 332–343.<br />
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Abronia smithi. Smith’s arboreal alligator lizard is endemic to the Sierra Madre de Chiapas, in the southeastern portion of this<br />
state. Its EVS has been determined as 17, placing it in the middle of the high vulnerability category; the IUCN, however, lists this<br />
lizard as of Least Concern. This individual was found in cloud forest in the Reserva de la Biósfera El Triunfo, Chiapas. Photo by<br />
Elí García-Padilla.<br />
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The following 18 taxa either have been resurrected from<br />
the synonymy of other taxa or placed in the synonymy of<br />
other taxa, and thus also change the number of species in<br />
the CMAR list:<br />
Phyllodactylus nocticolus: Blair et al. (2009). Zootaxa<br />
2027: 28–42. Resurrected as a distinct species<br />
from P. xanti.<br />
Sceloporus albiventris: Lemos-Espinal et al. (2004).<br />
Bulletin of the Chicago Herpetological Society 39:<br />
164–168. Resurrected as a distinct species from S.<br />
horridus.<br />
Sceloporus bimaculatus: Leaché and Mulcahy (2007).<br />
Molecular Ecology 16: 5216–5233. Returned to<br />
the synonymy of S. magister.<br />
Plestiodon bilineatus: Feria-Ortiz et al. (2011). Herpetological<br />
Monographs 25: 25–51. Elevated to<br />
full species from P. brevirostris.<br />
Plestiodon dicei: Feria-Ortiz et al. (2011). Herpetological<br />
Monographs 25: 25–51. Elevated to full<br />
species from P. brevirostris.<br />
Plestiodon indubitus: Feria-Ortiz et al. (2011). Herpetological<br />
Monographs 25: 25–51. Elevated to full<br />
species from P. brevirostris.<br />
Plestiodon nietoi: Feria-Ortiz and García-Vázquez<br />
(2012). Zootaxa 3339: 57–68. Elevated to full species<br />
from P. brevirostris.<br />
Aspidoscelis stictogramma: Walker and Cordes<br />
(2011). Herpetological Review 42: 33–39. Elevated<br />
to full species from A. burti.<br />
Xenosaurus agrenon: Bhullar (2011). Bulletin of the<br />
Museum of Comparative Zoology 160: 65–181. Elevated<br />
to full species from X. grandis.<br />
Xenosaurus rackhami: Bhullar (2011). Bulletin of the<br />
Museum of Comparative Zoology 160: 65–181. Elevated<br />
to full species from X. grandis.<br />
Lampropeltis californiae: Pyron and Burbrink (2009).<br />
Zootaxa 2241: 22–32. Elevated to full species from<br />
L. getula.<br />
Lampropeltis holbrooki: Pyron and Burbrink (2009).<br />
Zootaxa 2241: 22–32. Elevated to full species from<br />
L. getula.<br />
Lampropeltis splendida: Pyron and Burbrink (2009).<br />
Zootaxa 2241: 22–32. Elevated to full species from<br />
L. getula.<br />
Sonora aequalis: Cox et al. (2012). Systematics and<br />
Biodiversity 10: 93–108. Placed in synonymy of S.<br />
mutabilis.<br />
Coniophanes taylori: Flores-Villela and Smith (2009).<br />
Herpetologica 65: 404–412. Resurrected as a distinct<br />
species from C. piceivittis.<br />
Leptodeira maculata: Daza et al. (2009). Molecular<br />
Phylogenetics and Evolution 53: 653–667. Synonymized<br />
with L. cussiliris. The correct name of the<br />
taxon, however, contrary to the decision of Daza et<br />
al. (2009), is L. maculata, inasmuch as this name<br />
was originated by Hallowell in 1861, and thus has<br />
priority. Leptodeira cussiliris, conversely, originally<br />
was named as a subspecies of L. annulata by<br />
Duellman (1958), and thus becomes a junior synonym<br />
of L. maculata.<br />
Crotalus ornatus: Anderson and Greenbaum (2012).<br />
Herpetological Monographs 26: 19–57. Resurrected<br />
as a distinct species from the synonymy of<br />
C. molossus.<br />
Mixcoatlus browni: Jadin et al. (2011). Zoological<br />
Journal of the Linnean Society 163: 943–958. Resurrected<br />
as a distinct species from M. barbouri.<br />
The following species have undergone status changes,<br />
including some taxa discussed in the addendum to Wilson<br />
and Johnson (2010):<br />
Anolis beckeri: Köhler (2010). Zootaxa 2354: 1–18.<br />
Resurrected as a distinct species from A. pentaprion,<br />
which thus no longer occurs in Mexico.<br />
Marisora brachypoda: Hedges and Conn (2012). Zootaxa<br />
3288: 1–244. Generic name originated for a<br />
group of species formerly allocated to Mabuya.<br />
Sphaerodactylus continentalis: McCranie and Hedges<br />
(2012). Zootaxa 3492: 65–76. Resurrection from<br />
synonymy of S. millepunctatus, which thus no longer<br />
occurs in Mexico.<br />
Holcosus chaitzami, H. festivus, and H. undulatus:<br />
Harvey et al. (2012). Zootaxa 3459: 1–156. Generic<br />
name originated for a group of species formerly<br />
allocated to Ameiva.<br />
Lampropeltis knoblochi: Burbrink et al. (2011). Molecular<br />
and Phylogenetic Evolution. 60: 445–454.<br />
Elevated to full species from L. pyromelana, which<br />
thus no longer is considered to occur in Mexico.<br />
Leptodeira cussiliris: Mulcahy. 2007. Biological<br />
Journal of the Linnean Society 92: 483–500. Removed<br />
from synonymy of L. annulata, which thus<br />
no longer occurs in Mexico. See Leptodeira maculata<br />
entry above.<br />
Leptodeira uribei: Reyes-Velasco and Mulcahy<br />
(2010). Herpetologica 66: 99–110. Removed from<br />
the genus Pseudoleptodeira.<br />
Rhadinella godmani: Myers. 2011. American Museum<br />
Novitates 3715: 1–33. Species placed in new<br />
genus from Rhadinaea.<br />
Rhadinella hannsteini: Myers (2011). American Museum<br />
Novitates 3715: 1–33. Species placed in new<br />
genus from Rhadinaea.<br />
Rhadinella kanalchutchan: Myers (2011). American<br />
Museum Novitates 3715: 1–33. Species placed in<br />
new genus from Rhadinaea.<br />
Rhadinella kinkelini: Myers (2011). American Museum<br />
Novitates 3715: 1–33. Species placed in new<br />
genus from Rhadinaea.<br />
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Barisia ciliaris. The widespread Sierra alligator lizard is endemic to Mexico, and is part of a complex that still is undergoing systematic<br />
study. Its distribution extends along the Sierra Madre Occidental from southern Chihuahua southward through western Durango<br />
and into central Jalisco, and thence into northern Guanajuato and central Querétaro and northward in the Sierra Madre Oriental to<br />
central Nuevo León. Its EVS has been calculated as 15, placing it in the lower portion of the high vulnerability category. The IUCN<br />
does not recognize this taxon at the species level, so it has to be considered as Not Evaluated. This individual is from 10.1 km WNW<br />
of La Congoja, Aguascalientes. Photo by Louis W. Porras.<br />
Lampropeltis mexicana. The endemic Mexican gray-banded kingsnake is distributed from the Sierra Madre Occidental in southern<br />
Durango and the Sierra Madre Oriental in extreme southeastern Coahuila southward to northern Guanajuato. Its EVS has been<br />
gauged as 15, placing it in the lower portion of the high vulnerability category, but its IUCN status, however, was determined as of<br />
Least Concern. This individual was found at Banderas de Aguila (N of Coyotes), Durango. Photo by Ed Cassano.<br />
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Rhadinella lachrymans: Myers (2011). American Museum<br />
Novitates 3715: 1–33. Species placed in new<br />
genus from Rhadinaea.<br />
Rhadinella posadasi: Myers (2011). American Museum<br />
Novitates 3715: 1–33. Species placed in new<br />
genus from Rhadinaea.<br />
Rhadinella schistosa: Myers (2011). American Museum<br />
Novitates 3715: 1–33. Species placed in new<br />
genus from Rhadinaea.<br />
Sonora aemula: Cox et al. (2012). Systematics and<br />
Biodiversity 10: 93–108. Generic name changed<br />
from Procinura, which thus becomes a synonym<br />
of Sonora.<br />
Epictia goudotii: Adalsteinsson et al. (2009). Zootaxa<br />
2244: 1–50. Species placed in a new genus from<br />
Leptotyphlops.<br />
Rena boettgeri: Adalsteinsson et al. (2009). Zootaxa<br />
2244: 1–50. Species placed in a new genus from<br />
Leptotyphlops.<br />
Rena bressoni: Adalsteinsson et al. (2009). Zootaxa<br />
2244: 1–50. Species placed in a new genus from<br />
Leptotyphlops.<br />
Rena dissecta: Adalsteinsson et al. (2009). Zootaxa<br />
2244: 1–50. Species placed in a new genus from<br />
Leptotyphlops.<br />
Rena dulcis: Adalsteinsson et al. (2009). Zootaxa<br />
2244: 1–50. Species placed in a new genus from<br />
Leptotyphlops.<br />
Rena humilis: Adalsteinsson et al. (2009). Zootaxa<br />
2244: 1–50. Species placed in a new genus from<br />
Leptotyphlops.<br />
Rena maxima: Adalsteinsson et al. (2009). Zootaxa<br />
2244: 1–50. Species placed in a new genus from<br />
Leptotyphlops.<br />
Rena myopica: Adalsteinsson et al. (2009). Zootaxa<br />
2244: 1–50. Species placed in a new genus from<br />
Leptotyphlops.<br />
Mixcoatlus barbouri: Jadin et al. (2011). Zoological<br />
Journal of the Linnean Society 163: 943–958. New<br />
genus for species removed from Cerrophidion.<br />
Mixcoatlus melanurus: Jadin et al. (2011). Zoological<br />
Journal of the Linnean Society 163: 943–958. New<br />
genus for species removed from Ophryacus.<br />
Results of the 2005 Mexican Reptile<br />
Assessment<br />
The 2005 Mexican Reptile Assessment “was carried out<br />
by zoologists from the non-profit conservation group<br />
NatureServe, working in partnership with reptile experts<br />
from universities, the World Conservation Union<br />
(IUCN), and Conservation International” (NatureServe<br />
Press Release; available at natureserve.org/aboutUS/<br />
PressReleases). This study dealt with “721 species of<br />
lizards and snakes found in Mexico, the United States,<br />
and Canada.” Turtles and crocodilians previously were<br />
assessed. The press release indicated that, “about one<br />
in eight lizards and snakes (84 species) were found to<br />
be threatened with extinction [i.e., judged as Critically<br />
Endangered, Endangered, or Vulnerable], with another<br />
23 species labeled Near Threatened. For 121 lizards and<br />
snakes, the data are insufficient to allow a confident estimate<br />
of their extinction risk [i.e., judged as Data Deficient],<br />
while 493 species (about two-thirds of the total)<br />
are at present relatively secure [i.e., judged as Least Concern].”<br />
Thus, the percentages of species that fall into the<br />
standard IUCN assessment categories are as follows: CR,<br />
EN, and VU (11.7); NT (3.2); DD (16.8); and LC (68.4).<br />
Inasmuch as the above results include species that<br />
occur in the United States, Canada, and also those not<br />
evaluated in the survey, we extracted information from<br />
the IUCN Red List website on the ratings provided for<br />
Mexican species alone, and also used the “NE” designation<br />
for species not included in the 2005 assessment. We<br />
list these ratings in Appendix 1.<br />
Critique of the 2005 Results<br />
Our primary reason for writing this paper is to critique<br />
the results of the Mexican reptile assessment, as reported<br />
in the above press release, and to reassess the conservation<br />
status of these organisms using another conservation<br />
assessment tool. We begin our critique with the data<br />
placed in Appendix 1, which we accessed at the IUCN<br />
Red List website up until 26 May 2012. The taxa listed<br />
in this appendix are current to the present, based on the<br />
changes to the Mexican reptile fauna indicated above.<br />
The data on the IUCN ratings are summarized by family<br />
in Table 1 and discussed below.<br />
We based our examination on the understanding that<br />
the word “critique” does not necessarily imply an unfavorable<br />
evaluation of the results of the Mexican reptile<br />
assessment, as conducted using the IUCN categories and<br />
criteria. “Critique,” in the strict sense, implies neither<br />
praise nor censure, and is neutral in context. We understand,<br />
however, that the word sometimes is used in a negative<br />
sense, as noted in the 3 rd edition of The American<br />
Heritage Dictionary (1992: 443). Nonetheless, our usage<br />
simply means to render a careful analysis of the results.<br />
Presently, we recognize 849 species of reptiles in<br />
Mexico, including three crocodilians, 48 turtles, 413 lizards<br />
and amphisbaenians, and 385 snakes, arrayed in 42<br />
families. This total represents an increase of 19 species<br />
(14 lizards, five snakes) over the totals listed by Wilson<br />
and Johnson (2010). The number and percentage of each<br />
of these 849 species allocated to the IUCN categories,<br />
or not evaluated, are as follows: CR = 9 (1.1%); EN =<br />
38 (4.5%); VU = 45 (5.3%); NT = 26 (3.1%); LC = 424<br />
(49.9%); DD = 118 (13.9%); and NE (not evaluated) =<br />
189 (22.2%). The number and percentage of species collectively<br />
allocated to the three threat categories (CR, EN,<br />
and VU) are 92 and 10.8%, respectively. This number is<br />
exceeded by the 118 species placed in the DD category,<br />
and is slightly less than one-half of the 189 species not<br />
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Anolis dollfusianus. The coffee anole is distributed on the Pacific versant from southern Chiapas to western Guatemala. Its EVS has<br />
been determined as 13, placing it at the upper end of the medium vulnerability category, and its IUCN status is undetermined. This<br />
individual was found in cloud forest in Reserva de la Biósfera El Triunfo, Chiapas. Photo by Elí García-Padilla.<br />
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Table 1. IUCN Red List categorizations for the Mexican reptile families (including crocodilians, turtles, lizards, and snakes).<br />
Families<br />
Number of<br />
species<br />
IUCN Red List categorizations<br />
Critically<br />
Endangered Endangered Vulnerable Near<br />
Threatened<br />
Least<br />
Concern<br />
Data<br />
Deficient<br />
Not<br />
Evaluated<br />
Alligatoridae 1 — — — — 1 — —<br />
Crocodylidae 2 — — 1 — 1 — —<br />
Subtotals 3 — — 1 — 2 — —<br />
Cheloniidae 5 2 2 1 — — — —<br />
Chelydridae 1 — — 1 — — — —<br />
Dermatemydidae 1 1 — — — — — —<br />
Dermochelyidae 1 1 — — — — — —<br />
Emydidae 15 — 2 4 2 2 1 4<br />
Geoemydidae 3 — — — 2 — — 1<br />
Kinosternidae 17 — — — 6 6 3 2<br />
Testudinidae 3 — — 1 — 1 — 1<br />
Trionychidae 2 — — — — 1 — 1<br />
Subtotals 48 4 4 7 10 10 4 9<br />
Biporidae 3 — — — — 3 — —<br />
Anguidae 48 — 10 4 1 17 10 6<br />
Anniellidae 2 — 1 — — 1 — —<br />
Corytophanidae 6 — — — — 1 — 5<br />
Crotaphytidae 10 — 1 1 8<br />
Dactyloidae 50 — 3 2 — 16 12 17<br />
Dibamidae 1 — — — — 1 — —<br />
Eublepharidae 7 — — — — 6 — 1<br />
Gymnophthalmidae<br />
1 — — — — — — 1<br />
Helodermatidae 2 — — — 1 1 — —<br />
Iguanidae 19 1 — 2 2 3 — 11<br />
Mabuyidae 1 — — — — — — 1<br />
Phrynosomatidae 135 1 5 8 6 89 6 20<br />
Phyllodactylidae 15 — — — 1 10 1 3<br />
Scincidae 23 — — 1 — 12 5 5<br />
Sphaerodactylidae 4 — — — — — — 4<br />
Sphenomorphidae 6 — — — — 3 — 3<br />
Teiidae 46 — — 3 1 35 2 5<br />
Xantusiidae 25 — 1 2 — 6 8 8<br />
Xenosauridae 9 — 2 1 — 2 1 3<br />
Subtotals 413 2 23 24 12 214 45 93<br />
Boidae 2 — — — — 1 — 1<br />
Colubridae 136 2 3 1 3 77 18 32<br />
Dipsadidae 115 — 3 3 — 44 38 27<br />
Elapidae 19 — — 1 — 13 4 1<br />
Leptotyphlopidae 8 — — — — 5 1 2<br />
Loxocemidae 1 — — — — — — 1<br />
Natricidae 33 — 2 3 — 20 3 5<br />
Typhlopidae 2 — — — — 2 — —<br />
Ungaliophiidae 2 — — 1 — — — 1<br />
Viperidae 59 1 3 4 1 33 4 13<br />
Xenodontidae 8 — — — — 3 1 4<br />
Subtotals 385 3 11 13 4 198 69 87<br />
Totals 849 9 38 45 26 424 118 189<br />
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Mastigodryas cliftoni. The endemic Clifton’s lizard eater is found along the Pacific versant from extreme southeastern Sonora<br />
southward to Jalisco. Its EVS has been determined as 14, placing it at the lower end of the high vulnerability category, and its IUCN<br />
status has not been assessed. This individual is from El Carrizo, Sinaloa. Photo by Ed Cassano.<br />
Geophis dugesi. The endemic Dugès’ earthsnake occurs from extreme southwestern Chihuahua along the length of the Sierra<br />
Madre Occidental southward to Michoacán. Its EVS has been assessed as 13, placing it at the upper end of the medium vulnerability<br />
category, and its IUCN status has been determined as of Least Concern. This individual was found at El Carrizo, Sinaloa.<br />
Photo by Ed Cassano.<br />
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evaluated on the website. Thus, of the total of 849 species,<br />
307 (36.2%) are categorized either as DD or NE.<br />
As a consequence, only 542 (63.8%) of the total number<br />
are allocated to one of the other five categories (CR, EN,<br />
VU, NT, or LC).<br />
These results provided us with a substantially incomplete<br />
picture of the conservation status of reptiles<br />
in Mexico, which sharply contrasts the picture offered<br />
for Central American reptiles (the other major portion<br />
of Mesoamerica), as recorded in Wilson et al. (2010).<br />
This situation is underscored by the relatively low species<br />
numbers of Mexican reptiles placed in any of the<br />
three IUCN threat categories. In addition, a substantial<br />
proportion (13.9%) of the Mexican species are assessed<br />
as DD, indicating that insufficient information exists for<br />
the IUCN rating system to be employed. Finally, 189<br />
species (22.3%) are not evaluated, largely because they<br />
also occur in Central America (and in some cases, also<br />
in South America) and will be assessed presumably in<br />
future workshops, which was the case for most of these<br />
species when they were assessed in a Central American<br />
workshop held on May 6–10, 2012; as yet, the results of<br />
that assessment are not available.<br />
Given that only 10.8% of the Mexican species were<br />
allocated to one of the three IUCN threat categories<br />
and that about six in 10 species in the country are endemic,<br />
we examined the IUCN ratings reported for species<br />
inhabiting five of the countries in Central America<br />
(see Wilson et al. 2010). For Guatemala, Acevedo et al.<br />
(2010) reported that 56 reptile species (23.0%) of a total<br />
of 244 then recognized were assigned to one of the three<br />
threat categories. Of 237 Honduran reptiles assessed by<br />
Townsend and Wilson (2010), 74 (31.2%) were placed in<br />
one of the threat categories. Sunyer and Köhler (2010)<br />
listed 165 reptile species from Nicaragua, a country with<br />
only three endemic reptiles known at the time, but judged<br />
10 of them (6.1%) as threatened. Of 231 reptile species<br />
assessed by Sasa et al. (2010) for Costa Rica, 36 (15.6%)<br />
were placed in a threat category. Finally, Jaramillo et<br />
al. (2010) placed 22 of 248 Panamanian reptile species<br />
(8.9%) in the threat categories. Collectively, 17% of the<br />
reptile species in these countries were assessed in one of<br />
the three threat categories.<br />
The number of species in Central America placed<br />
into one of the threat categories apparently is related to<br />
the number allocated to the DD category. Although the<br />
DD category is stated explicitly as a non-threat category<br />
(IUCN Red List Categories and Criteria 2010), its use<br />
highlights species so poorly known that one of the other<br />
IUCN categories cannot be applied. The percentage of<br />
DD species in the reptile faunas of each of the five Central<br />
American countries discussed above ranges from 0.9<br />
in Honduras to 40.3 in Panama. Intermediate figures are<br />
as follows: Nicaragua = 1.2; Guatemala = 5.3; Costa Rica<br />
= 34.2. These data apparently indicate that the conservation<br />
status of the Costa Rican and Panamanian reptile<br />
faunas are by far more poorly understood than those of<br />
Guatemala, Honduras, and Nicaragua.<br />
The length of time for placing these DD species into<br />
another category is unknown, but a reassessment must<br />
await targeted surveys for the species involved. Given<br />
the uncertainty implied by the use of this category supplemented<br />
by that of NE species in Mexico, we believe<br />
there is ample reason to reassess the conservation status<br />
of the Mexican reptiles using the Environmental Vulnerability<br />
Score (EVS).<br />
EVS for Mexican Reptiles<br />
The EVS provides several advantages for assessing the<br />
conservation status of amphibians and reptiles. First, this<br />
measure can be applied as soon as a species is described,<br />
because the information necessary for its application<br />
generally is known at that point. Second, the calculation<br />
of the EVS is an economical undertaking and does not<br />
require expensive, grant-supported workshops, such as<br />
those held in connection with the Global Reptile Assessment<br />
sponsored by the IUCN. Third, the EVS is predictive,<br />
because it provides a measure of susceptibility to<br />
anthropogenic pressure, and can pinpoint taxa in need of<br />
immediate attention and continuing scrutiny. Finally, this<br />
measure is simple to calculate and does not “penalize”<br />
species that are poorly known. One disadvantage of the<br />
EVS, however, is that it was not designed for use with<br />
marine species. So, the six species of marine turtles and<br />
two of marine snakes occurring on the shores of Mexico<br />
could not be assessed. Nevertheless, given the increasing<br />
rates of human population growth and environmental<br />
deterioration, an important consideration for a given species<br />
is to have a conservation assessment measure that<br />
can be applied simply, quickly, and economically.<br />
We calculated the EVS for each of the 841 species<br />
of terrestrial reptiles occurring in Mexico (Wilson and<br />
Johnson 2010, and updated herein; see Appendix 1). In<br />
this appendix, we listed the scores alongside the IUCN<br />
categorizations from the 2005 Mexican Reptile Assessment,<br />
as available on the IUCN Red List website (www.<br />
iucnredlist.org) and as otherwise determined by us (i.e.,<br />
as NE species).<br />
Theoretically, the EVS can range from 3 to 20. A score<br />
of 3 is indicative of a species that ranges widely both<br />
within and outside of Mexico, occupies eight or more<br />
forest formations, and is fossorial and usually escapes<br />
human notice. Only one such species (the leptotyphlopid<br />
snake Epictia goudotii) is found in Mexico. At the<br />
other extreme, a score of 20 relates to a species known<br />
only from the vicinity of the type locality, occupies a<br />
single forest formation, and is exploited commercially or<br />
non-commercially for hides, meat, eggs and/or the pet<br />
trade. Also, only one such species (the trionychid turtle<br />
Apalone atra) occurs in Mexico. All of the other scores<br />
fall within the range of 4–19. We summarized the EVS<br />
for reptile species in Mexico by family in Table 2.<br />
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Rhadinaea laureata. The endemic crowned graceful brownsnake is distributed along the Sierra Madre Occidental from west-central<br />
Durango southward into the Tranverse Volcanic Axis as far as central Michoacán, Morelos, and the Distrito Federal. Its EVS has<br />
been calculated as 12, placing it in the upper portion of the medium vulnerability category, and its IUCN status has been determined<br />
as Least Concern. This individual is from Rancho Las Canoas, Durango. Photo by Louis W. Porras.<br />
Thamnophis mendax. The endemic Tamaulipan montane gartersnake is restricted to a small range in the Sierra Madre Oriental in<br />
southwestern Tamaulipas. Its EVS has been determined as 14, placing it at the lower end of the high vulnerability category, and its<br />
IUCN status has been assessed as Endangered. This individual came from La Gloria, in the Gómez Farías region of Tamaulipas.<br />
Photo by Ed Cassano.<br />
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Families<br />
Number<br />
of<br />
species<br />
Environmental Vulnerability Scores<br />
3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20<br />
Alligatoridae 1 — — — — — — — — — — — — — 1 — — — —<br />
Crocodylidae 2 — — — — — — — — — — 1 1 — — — — — —<br />
Subtotals 3 — — — — — — — — — — 1 1 — 1 — — — —<br />
Subtotal % — — — — — — — — — — — 33.3 33.3 — 33.3 — — — —<br />
Chelydridae 1 — — — — — — — — — — — — — — 1 — — —<br />
Wilson et al.<br />
Table 2. Environmental Vulnerability Scores for the Mexican reptile species (including crocodilians, turtles, lizards, and snakes, but excluding the<br />
marine species), arranged by family. Shaded area to the left encompasses low vulnerability scores, and to the right high vulnerability scores.<br />
1 — — — — — — — — — — — — — — 1 — — —<br />
Emydidae 15 — — — — — — — — — — 1 1 1 2 1 4 5 —<br />
Geoemydidae 3 — — — — — 1 — — — — 1 1 — — — — — —<br />
Kinosternidae 17 — — — — — — — 3 1 1 1 6 3 2 — — — —<br />
Testudinidae 3 — — — — — — — — — — — — 1 — — 1 1 —<br />
Trionychidae 2 — — — — — — — — — — — — 1 — — — — 1<br />
Subtotals 42 — — — — — 1 — 3 1 1 3 8 6 4 3 5 6 1<br />
Subtotal % — — — — — — 2.4 — 7.1 2.4 2.4 7.1 19.0 14.3 9.5 7.1 11.9 14.3 2.4<br />
Bipedidae 3 — — — — — — — — — 1 — 2 — — — — — —<br />
Anguidae 48 — — — 1 — — 1 2 — 1 3 6 11 7 8 8 — —<br />
Anniellidae 2 — — — — — — — — — 1 1 — — — — — — —<br />
Dermatemydidae<br />
Corytophanidae<br />
6 — — — — 1 1 1 — 2 — 1 — — — — — — —<br />
Crotaphytidae<br />
10 — — — — — — 1 — 1 2 2 — — 4 — — —<br />
Dactyloidae 50 — — — — 1 2 3 3 — 3 8 3 8 15 4 — — —<br />
Dibamidae 1 — — — — — — — 1 — — — — — — — — — —<br />
Eublepharidae<br />
7 — — — — — — 1 — 1 — — 2 1 — 1 1 — —<br />
Gymnophthalmidae<br />
1 — — — — — — 1 — — — — — — — — — — —<br />
Helodermatidae<br />
2 — — — — — — — — 1 — — — 1 — — — — —<br />
Iguanidae 19 — — — — — 1 — — 1 2 1 1 4 4 2 1 2 —<br />
Mabuyidae 1 — — — 1 — — — — — — — — — — — — — —<br />
Phrynosomatidae<br />
135 — — 1 1 2 1 3 3 11 18 22 16 23 23 11 — — —<br />
Phyllodactylidae<br />
15 — — — — — 1 — 2 — — 1 1 4 5 1 — — —<br />
Scincidae 23 — — — — — — — 1 4 5 2 4 4 2 1 — — —<br />
Sphaerodactylidae<br />
4 — — — — — — — 1 1 1 1 — — — — — — —<br />
Sphenomorphidae<br />
6 — — — — 1 1 — — 1 1 1 — — — 1 — — —<br />
Teiidae 46 — — — — 1 2 1 1 2 2 3 14 7 6 7 — — —<br />
Xantusiidae 25 — — — — — 2 — — 2 1 3 4 3 9 1 — — —<br />
Xenosauridae 9 — — — — — — 1 — 1 1 — 1 1 3 1 — — —<br />
Subtotals 413 — — 1 3 6 11 13 14 28 39 49 54 67 78 38 10 2 —<br />
Subtotal % — — — 0.2 0.7 1.5 2.7 3.1 3.4 6.8 9.4 11.9 13.1 16.2 18.9 9.2 2.4 0.5 —<br />
Boidae 2 — — — — — — — 2 — — — — — — — — — —<br />
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Table 2. Continued.<br />
Colubridae 136 — — 4 7 3 6 10 15 8 8 18 22 14 16 5 — — —<br />
Dipsadidae 115 — 1 3 3 3 8 4 7 6 13 14 13 19 15 6 — — —<br />
Elapidae 17 — — — — — 2 — — 2 — 2 2 3 — 2 3 1 —<br />
Leptotyphlopidae<br />
8 1 — — — — 1 — — 2 — 2 2 — — — — — —<br />
Loxocemidae 1 — — — — — — — 1 — — — — — — — — — —<br />
Natricidae 33 — — — — 3 1 — 2 2 2 3 6 7 4 2 1 — —<br />
Typhlopidae 2 — — — — — — — — 1 1 — — — — — — — —<br />
Ungaliophiidae<br />
2 — — — — — — — 1 — — — — 1 — — — — —<br />
Viperidae 59 — — — — — 1 2 1 3 7 5 6 6 9 8 5 6 —<br />
Xenodontidae 8 — — — — — — 1 1 1 — 3 1 — — 1 — — —<br />
Subtotals 383 1 1 7 10 9 19 17 30 25 31 47 52 50 44 24 9 7 —<br />
Subtotal % — 0.3 0.3 1.8 2.6 2.3 5.0 4.4 7.8 6.5 8.1 12.3 13.6 13.1 11.5 6.3 2.3 1.8 —<br />
Totals 841 1 1 8 13 15 31 30 47 54 71 100 115 123 127 65 24 15 1<br />
Total % — 0.1 0.1 1.0 1.5 1.8 3.7 3.6 5.6 6.4 8.4 11.9 13.7 14.6 15.1 7.7 2.9 1.8 0.1<br />
The range and average EVS for the major reptile<br />
groups are as follows: crocodilians = 13–16 (14.3); turtles<br />
= 8–20 (15.3); lizards = 5–19 (13.8); and snakes =<br />
3–19 (12.8). On average, turtles are most susceptible and<br />
snakes least susceptible to environmental degradation,<br />
with lizards and crocodilians falling in between. The average<br />
scores either are at the upper end of the medium<br />
category, in the case of snakes and lizards, or at the lower<br />
end of the high category, in the case of crocodilians and<br />
turtles. The average EVS for all the reptile species is<br />
13.4, a value close to the lower end of the high range of<br />
vulnerability.<br />
Nineteen percent of the turtle species were assigned<br />
an EVS of 14, at the lower end of the high vulnerability<br />
category. For lizards, the respective figures are 18.9%<br />
and 16, about midway through the range for the high vulnerability<br />
category; for snakes, the values are 13.6% and<br />
14.<br />
The total EVS values generally increase from the low<br />
end of the scale (3) to about midway through the high end<br />
(16), with a single exception (a decrease from 31 to 29<br />
species at scores 8 and 9), then decrease thereafter to the<br />
highest score (20). The peak number of taxa (127) was<br />
assigned an EVS of 16, a score that falls well within the<br />
range of high vulnerability.<br />
Of the 841 total taxa that could be scored, 99 (11.8%)<br />
fall into the low vulnerability category, 272 (32.3%) in<br />
the medium category, and 470 (55.9%) in the high category.<br />
Thus, more than one-half of the reptile species<br />
in Mexico were judged as having the highest degree of<br />
vulnerability to environmental degradation, and slightly<br />
more than one-tenth of the species the lowest degree.<br />
This increase in absolute and relative numbers from<br />
the low portion, through the medium portion, to the high<br />
portion varies somewhat with the results published for<br />
both the amphibians and reptiles for some Central American<br />
countries (see Wilson et al. 2010). Acevedo et al.<br />
(2010) reported 89 species (23.2%) with low scores, 179<br />
(46.7%) with medium scores, and 115 (30.0%) with high<br />
scores for Guatemala. The same trend is seen in Honduras,<br />
where Townsend and Wilson (2010) indicated the<br />
following absolute and relative figures in the same order,<br />
again for both amphibians and reptiles: 71 (19.7%); 169<br />
(46.8%); and 121 (33.5%). Comparable figures for the<br />
Panamanian herpetofauna (Jaramillo et al. 2010) are: 143<br />
(33.3%); 165 (38.4%); and 122 (28.4%).<br />
The principal reason that EVS values are relatively<br />
high in Mexico is because of the high level of endemism<br />
and the relatively narrow range of habitat occurrence.<br />
Of the 485 endemic species in Mexico (18 turtles, 264<br />
lizards, 203 snakes), 124 (25.6%) were assigned a geographic<br />
distribution score of 6, signifying that these creatures<br />
are known only from the vicinity of their respective<br />
type localities; the remainder of the endemic species (361<br />
[74.4%]) are more broadly distributed within the country<br />
(Appendix 1). Of the 841 terrestrial Mexican reptile species,<br />
212 (25.2%) are limited in ecological distribution to<br />
one formation (Appendix 1). These features of geographic<br />
and ecological distribution are of tremendous significance<br />
for efforts at conserving the immensely important<br />
Mexican reptile fauna.<br />
Comparison of IUCN Categorizations and<br />
EVS Values<br />
Since the IUCN categorizations and EVS values both<br />
measure the degree of environmental threat impinging on<br />
a given species, a certain degree of correlation between<br />
the results of these two measures is expected. Townsend<br />
and Wilson (2010) demonstrated this relationship with<br />
reference to the Honduran herpetofauna, by comparing<br />
the IUCN and EVS values for 362 species of amphibians<br />
and terrestrial reptiles in their table 4. Perusal of the data<br />
in this table indicates, in a general way, that an increase in<br />
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Crotalus catalinensis. The endemic Catalina Island rattlesnake is restricted in distribution to Santa Catalina Island in the Gulf of<br />
California. Its EVS has been determined as 19, placing it in the upper portion of the high vulnerability category, and its IUCN status<br />
as Critically Endangered. Photo by Louis W. Porras.<br />
Crotalus stejnegeri. The endemic Sinaloan long-tailed rattlesnake is restricted to a relatively small range in western Mexico, where<br />
it is found in the western portion of the Sierra Madre Occidental in western Durango and southeastern Sinaloa. Its EVS has been<br />
determined as 17, placing it in the middle of the high vulnerability category, and its IUCN status as Vulnerable. This individual came<br />
from Plomosas, Sinaloa. Photo by Louis W. Porras.<br />
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Table 3. Comparison of the Environmental Vulnerability Scores (EVS) and IUCN categorizations for terrestrial Mexican reptiles.<br />
Shaded area on top encompasses the low vulnerability category scores, and at the bottom high vulnerability category scores.<br />
IUCN categories<br />
EVS Critically<br />
Near Least Data Not Totals<br />
Endangered Vulnerable<br />
Endangered<br />
Threatened Concern Deficient Evaluated<br />
3 — — — — — — 1 1<br />
4 — — — — 1 — — 1<br />
5 — — — — 3 — 5 8<br />
6 — — — — 5 — 8 13<br />
7 — — — — 5 — 10 15<br />
8 — — — — 20 — 11 31<br />
9 — — 1 — 16 — 13 30<br />
10 — — — — 25 1 21 47<br />
11 — — 1 1 36 2 14 54<br />
12 — 1 1 — 49 4 16 71<br />
13 — 2 5 3 66 5 19 100<br />
14 — 5 6 8 65 15 16 115<br />
15 — 13 11 7 54 25 13 123<br />
16 — 8 3 6 48 38 24 127<br />
17 4 3 11 1 21 14 11 65<br />
18 — 2 2 — 4 12 4 24<br />
19 2 2 3 — 4 2 2 15<br />
20 — — — — — — 1 1<br />
Totals 6 36 44 26 422 118 189 841<br />
EVS values is associated with a corresponding increase<br />
in the degree of threat, as measured by the IUCN categorizations.<br />
If average EVS values are determined for the<br />
IUCN categories in ascending degrees of threat, the following<br />
figures result: LC (206 spp.) = 10.5; NT (16 spp.)<br />
= 12.9; VU (18 spp.) = 12.5; EN (64 spp.) = 14.1; CR<br />
(50 spp.) = 15.1; and EX (2 spp.) = 16.0. The broad correspondence<br />
between the two measures is evident. Also<br />
of interest is that the average EVS score for the six DD<br />
species listed in the table is 13.7, a figure closest to that<br />
for the EN category (14.1), which suggests that if and<br />
when these species are better known, they likely will be<br />
judged as EN or CR.<br />
In order to assess whether such a correspondence exists<br />
between these two conservation measures for the<br />
Mexican reptiles, we constructed a table (Table 3) similar<br />
to table 4 in Townsend and Wilson (2010). Important<br />
similarities and differences exist between these tables.<br />
The most important similarity is in general appearance,<br />
i.e., an apparent general trend of decreasing EVS values<br />
with a decrease in the degree of threat, as indicated by the<br />
IUCN categorizations. This similarity, however, is more<br />
apparent than real. Our Table 3 deals only with Mexican<br />
reptiles, excludes the IUCN category EX (because<br />
presently this category does not apply to any Mexican<br />
species), and includes a NE category that we appended<br />
to the standard set of IUCN categories. Apart from these<br />
obvious differences, however, a closer examination of<br />
the data distribution in our Table 3 reveals more significant<br />
differences in the overall picture of the conservation<br />
status of the Mexican reptiles when using the IUCN<br />
categorizations, as opposed to the EVS, especially when<br />
viewed against the backdrop of results in Townsend and<br />
Wilson (2010: table 4).<br />
1. Nature of the IUCN categorizations in<br />
Table 3<br />
Unlike the Townsend and Wilson (2010) study, we introduced<br />
another category to encompass the Mexican<br />
reptile species that were not evaluated in the 2005 IUCN<br />
study. The category is termed “Not Evaluated” (IUCN<br />
2010) and a large proportion of the species (189 of 841<br />
Mexican terrestrial reptiles [22.5%]) are placed in this<br />
category. Thus, in the 2005 study more than one-fifth of<br />
the species were not placed in one of the standard IUCN<br />
categories, leaving their conservation status as undetermined.<br />
In addition, a sizable proportion of species (118<br />
[14.0%]) were placed in the DD category, meaning their<br />
conservation status also remains undetermined. When<br />
the species falling into these two categories are added,<br />
evidently 307 (36.5%) of the 841 Mexican terrestrial reptiles<br />
were not placed in one of the IUCN threat assessment<br />
categories in the 2005 study. This situation leaves<br />
less than two-thirds of the species as evaluated.<br />
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Xantusia sanchezi. The endemic Sanchez’s night lizard is known only from extreme southwestern Zacatecas to central Jalisco. This<br />
lizard’s EVS has been assessed as 16, placing it in the middle of the high vulnerability category, but its IUCN status has been determined<br />
as Least Concern. This individual was discovered at Huaxtla, Jalisco. Photo by Daniel Cruz-Sáenz.<br />
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2. Pattern of mean EVS vs. IUCN categorizations<br />
In order to more precisely determine the relationship between<br />
the IUCN categorizations and the EVS, we calculated<br />
the mean EVS for each of the IUCN columns in Table<br />
3, including the NE species and the total species. The<br />
results are as follows: CR (6 spp.) = 17.7 (range 17–19);<br />
EN (36 spp.) = 15.4 (12–19); VU (44 spp.) = 15.3 (10–<br />
19); NT (26 spp.) = 14.6 (11–17); LC (422 spp.) = 13.0<br />
(4–19); DD (118 spp.) = 15.5 (10–19); and NE (189 spp.)<br />
= 12.0 (3–20); and Total (841 spp.) = 13.3 (3–20). The<br />
results of these data show that the mean EVS decreases<br />
from the CR category (17.7) through the EN category<br />
(15.4) to the VU category (15.3), but only slightly between<br />
the EN and VU categories. They also continue to<br />
decrease from the NT category (14.6) to the LC category<br />
(13.0). This pattern of decreasing values was expected.<br />
In addition, as with the Townsend and Wilson (2010)<br />
Honduran study, the mean value for the DD species<br />
(15.5) is closest to that for the EN species (15.4). To us,<br />
this indicates what we generally have suspected about the<br />
DD category, i.e., that the species placed in this category<br />
likely will fall either into the EN or the CR categories<br />
when (and if) their conservation status is better understood.<br />
Placing species in this category is of little benefit<br />
to determining their conservation status, however, since<br />
once sequestered with this designation their significance<br />
tends to be downplayed. This situation prevailed once the<br />
results of the 2005 assessment were reported, given that<br />
the 118 species evaluated as DD were ignored in favor of<br />
the glowing report that emerged in the NatureServe press<br />
release (see above). If the data in Table 3 for the DD species<br />
is conflated with that for the 86 species placed in one<br />
of the three threat categories, the range of EVS values<br />
represented remains the same as for the threat categories<br />
alone, i.e., 10–19, and the mean becomes 15.5; the same<br />
as that indicated above for the DD species alone and only<br />
one-tenth of a point from the mean score for EN species<br />
(15.4). On the basis of this analysis, we predict that if<br />
a concerted effort to locate and assess the 118 DD species<br />
were undertaken, that most or all of them would be<br />
shown to qualify for inclusion in one of the three IUCN<br />
threat categories. If that result were obtained, then the<br />
number of Mexican reptile species falling into the IUCN<br />
threat categories would increase from 86 to 204, which<br />
would represent 24.3% of the reptile fauna.<br />
Based on the range and mean of the EVS values, the<br />
pattern for the LC species appears similar to that of the<br />
NE species, as the ranges are 4–19 and 3–20 and the<br />
means are 13.0 and 12.0, respectively. If these score distributions<br />
are conflated, then the EVS range becomes the<br />
broadest possible (3–20) and the mean becomes 12.7,<br />
which lies close to the upper end of the medium vulnerability<br />
category. While we cannot predict what would<br />
happen to the NE species once they are evaluated (presumably<br />
most species were evaluated during the Central<br />
American reptile assessment of May, 2012), because they<br />
were evaluated mostly by a different group of herpetologists<br />
from those present at the 2005 Mexican assessment,<br />
we suspect that many (if not most) would be judged as<br />
LC species. A more discerning look at both the LC and<br />
NE species might demonstrate that many should be partitioned<br />
into other IUCN categories, rather than the LC.<br />
Our reasoning is that LC and NE species exhibit a range<br />
of EVS values that extend broadly across low, medium,<br />
and high categories of environmental vulnerability. The<br />
number and percentage of LC species that fall into these<br />
three EVS categories are as follows: Low (range 3–9)<br />
= 50 spp. (11.8%); Medium (10–13) = 176 (41.7); and<br />
High (14–20) = 196 (46.5). For the NE species, the following<br />
figures were obtained: Low = 48 (25.8); Medium<br />
= 68 (36.6); and High = 70 (37.6). The percentage values<br />
are reasonably similar to one another, certainly increasing<br />
in the same direction from low through medium to<br />
high.<br />
Considering the total number of species, 99 (11.8%)<br />
fall into the low vulnerability category, 272 (32.3%) into<br />
the medium vulnerability category, and 470 (55.9%) into<br />
the high vulnerability category. These results differ significantly<br />
from those from the 2005 study. If the three<br />
IUCN threat categories can be considered most comparable<br />
to the high vulnerability EVS category, then 86 species<br />
fall into these three threat categories, which is 16.1%<br />
of the total 534 species in the CR, EN, VU, NT, and LC<br />
categories. If the NT category can be compared with the<br />
medium vulnerability EVS category, then 26 species fall<br />
into this IUCN category (4.9% of the 534 species). Finally,<br />
if the LC category is comparable to the low vulnerability<br />
EVS category, then 422 species (79.0%) fall<br />
into this IUCN category. Clearly, the results of the EVS<br />
analysis are nearly the reverse of those obtained from the<br />
IUCN categorizations discussed above.<br />
Discussion<br />
In the Introduction we indicated that our interest in conducting<br />
this study began after the publication of Wilson<br />
et al. (2010), when we compared the data resulting from<br />
that publication with a summary of the results of a 2005<br />
Mexican reptile assessment conducted under the auspices<br />
of the IUCN, and later referenced in a 2007 press<br />
release by NatureServe, a supporter of the undertaking.<br />
Our intention was not to critique the IUCN system of<br />
conservation assessment (i.e., the well-known IUCN categorizations),<br />
but rather to critique the results of the 2005<br />
assessment. We based our critique on the use of the Environmental<br />
Vulnerability Score (EVS), a measure used<br />
by Wilson and McCranie (2004) and in several Central<br />
American chapters in Wilson et al. (2010).<br />
Since the IUCN assessment system uses a different<br />
set of criteria than the EVS measure, we hypothesized<br />
that the latter could be used to test the results of the former.<br />
On this basis, we reassessed the conservation status<br />
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of the reptiles of Mexico, including, by our definition of<br />
convenience, crocodilians, turtles, lizards, and snakes,<br />
by determining the EVS value for each terrestrial species<br />
(since the measure was not designed for use with<br />
marine species). Based on our updating of the species<br />
list in Wilson and Johnson (2010), our species list for<br />
this study consisted of 841 species. We then developed<br />
an EVS measure applicable to Mexico, and employed it<br />
to calculate the scores indicated in Appendix 1.<br />
Our analysis of the EVS values demonstrated that<br />
when the scores are arranged in low, medium, and high<br />
vulnerability categories, the number and percentage<br />
of species increases markedly from the low category,<br />
through the medium category, to the high category (Table<br />
2). When these scores (Table 3) are compared to the<br />
IUCN categorizations documented in Table 1, however,<br />
an inverse correlation essentially exists between the results<br />
obtained from using the two methods. Since both<br />
methods are designed to render conservation status assessments,<br />
the results would be expected to corroborate<br />
one another.<br />
We are not in a position to speculate on the reason(s)<br />
for this lack of accord, and simply are offering a reassessment<br />
of the conservation status of Mexico’s reptile species<br />
based on another measure (EVS) that has been used<br />
in a series of studies since it was introduced by Wilson<br />
and McCranie (1992), and later employed by McCranie<br />
and Wilson (2002), Wilson and McCranie (2004), and<br />
several chapters in Wilson et al. (2010). Nonetheless, we<br />
believe our results provide a significantly better assessment<br />
of the conservation status Mexico’s reptiles than<br />
those obtained in the 2005 IUCN assessment. We consider<br />
our results more consonant with the high degree of<br />
reptile endemism in the country, and the restricted geographic<br />
and ecological ranges of a sizable proportion of<br />
these species. We also believe that our measure is more<br />
predictive, and reflective of impact expected from continued<br />
habitat fragmentation and destruction in the face<br />
of continuing and unregulated human population growth.<br />
Conclusions and Recommendations<br />
Our conclusions and conservation recommendations<br />
draw substantially from those promulgated by Wilson<br />
and Townsend (2010), which were provided for the entire<br />
Mesoamerican herpetofauna; thus, we refined them<br />
specifically for the Mexican reptile fauna, as follows:<br />
1. In the introduction we noted the human population<br />
size and density expected for Mexico in half a century,<br />
and no indication is available to suggest that<br />
this trend will be ameliorated. Nonetheless, although<br />
66% of married women in Mexico (ages 15–49) use<br />
modern methods of contraception, the current fertility<br />
rate (2.3) remains above the replacement level (2.0)<br />
and 29% of the population is below the age of 15, 1%<br />
above the average for Latin America and the Caribbean<br />
(2011 PRB World Population Data Sheet).<br />
2. Human population growth is not attuned purposefully<br />
to resource availability, and the rate of regeneration<br />
depends on the interaction of such societal factors as<br />
the level of urbanization; in Mexico, the current level<br />
is 78%, and much of it centered in the Distrito Federal<br />
(2011 PRB World Population Data Sheet). This<br />
statistic is comparable to that of the United States<br />
(79%) and Canada (80%), and indicates that 22% of<br />
Mexico’s population lives in rural areas. Given that<br />
the level of imports and exports are about equal (in<br />
2011, imports = 350.8 billion US dollars, exports =<br />
349.7 billion; CIA World Factbook 2012), the urban<br />
population depends on the basic foodstuffs that the<br />
rural population produces. An increase in human population<br />
demands greater agricultural production and/<br />
or efficiency, as well as a greater conversion of wild<br />
lands to farmlands. This scenario leads to habitat loss<br />
and degradation, and signals an increase in biodiversity<br />
decline.<br />
3. Although the rate of conversion of natural habitats to<br />
agricultural and urban lands varies based on the methods<br />
and assumptions used for garnering this determination,<br />
most estimates generally are in agreement.<br />
The Secretaría del Medio Ambiente y Recursos Naturales<br />
(SEMARNAT; Secretariat of Environment and<br />
Natural Resources; semarnat.gob.mx) has attempted<br />
to measure the rate of deforestation from 1978 to<br />
2005, with estimates ranging from about 200,000 to<br />
1,500,000 ha/yr. Most estimates, however, range from<br />
about 200,000 to 400,000 ha/yr. A study conducted<br />
for the years 2000 to 2005 reported an average rate of<br />
260,000 ha/yr. Another source of information (www.<br />
rainforests.mongabay.com) reports that from 1990 to<br />
2010 Mexico lost an average of 274,450 ha (0.39% of<br />
the total 64,802,000 ha of forest in the country), and<br />
during that period lost 7.8% of its forest cover (ca.<br />
5,489,000 ha). No matter the precise figures for forest<br />
loss, this alarming situation signifies considerable<br />
endangerment for organismic populations, including<br />
those of reptiles. About one-third of Mexico is (or<br />
was) covered by forest, and assuming a constant rate<br />
of loss all forests would be lost in about 256 years<br />
(starting from 1990), or in the year 2246. Forest loss<br />
in Mexico, therefore, contributes significantly to the<br />
global problem of deforestation.<br />
4. As a consequence, no permanent solution to the problem<br />
of biodiversity decline (including herpetofaunal<br />
decline) will be found in Mexico (or elsewhere in the<br />
world) until humans recognize overpopulation as the<br />
major cause of degradation and loss of humankind’s<br />
fellow organisms. Although this problem is beyond<br />
the scope of this investigation, solutions will not be<br />
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available until humanity begins to realize the origin,<br />
nature, and consequences of the mismatch between<br />
human worldviews and how our planet functions. Wilson<br />
(1988) labeled this problem “the mismanagement<br />
of the human mind.” Unfortunately, such realignment<br />
is only envisioned by a small cadre of humans, so<br />
crafting provisional solutions to problems like biodiversity<br />
decline must proceed while realizing the ultimate<br />
solution is not available, and might never be.<br />
5. Mexico is the headquarters of herpetofaunal diversity<br />
and endemism in Mesoamerica, which supports<br />
the conclusions of Ochoa-Ochoa and Flores-Villela<br />
(2006), Wilson and Johnson (2010), and the authors<br />
of four chapters on the Mexican herpetofauna in Wilson<br />
et al. (2010). Furthermore, field research and systematic<br />
inquiry in Mexico will continue to augment<br />
the levels of diversity and endemicity, which are of<br />
immense conservation significance because reptiles<br />
are significant contributors to the proper functioning<br />
of terrestrial and aquatic ecosystems (Gibbons et al.<br />
2000). From a political and economic perspective,<br />
diversity and endemism are important components<br />
of Mexico’s patrimony, as well as a potential source<br />
of income from ecotourism and related activities. Investing<br />
in such income sources should appeal to local<br />
stakeholders, as it provides an incentive for preserving<br />
natural habitats (Wilson 2011).<br />
6. Given that the ultimate solutions to biodiversity decline<br />
are unlikely to be implemented in any pertinent<br />
time frame, less effective solutions must be found.<br />
Vitt and Caldwell (2009) discussed a suite of approaches<br />
for preserving and managing threatened<br />
species, including the use of reserves and corridors<br />
to save habitats, undertaking captive management<br />
initiatives, and intentionally releasing individuals to<br />
establish or enlarge populations of target species. Unquestionably,<br />
preserving critical habitat is the most<br />
effective and least costly means of attempting to rescue<br />
threatened species. Captive management is less<br />
effective, and has been described as a last-ditch effort<br />
to extract a given species from the extinction vortex<br />
(Campbell et al. 2006). Efforts currently are underway<br />
in segments of the herpetological community to<br />
develop programs for ex situ and in situ captive management<br />
of some of the most seriously threatened herpetofaunal<br />
species, but such efforts will succeed only<br />
if these species can be reproduced in captivity and<br />
reintroduced into their native habitats. In the case of<br />
Mexico, Ochoa-Ochoa, et al. (2011: 2710) commented<br />
that, “given the current speed of land use change,<br />
we cannot expect to save all species from extinction,<br />
and so must decide how to focus limited resources to<br />
prevent the greatest number of extinctions,” and for<br />
amphibians proposed “a simple conservation triage<br />
method that: evaluates the threat status for 145 microendemic<br />
Mexican amphibian species; assesses current<br />
potential threat abatement responses derived from<br />
existing policy instruments and social initiatives; and<br />
combines both indicators to provide broad-scale conservation<br />
strategies that would best suit amphibian<br />
micro-endemic buffered areas (AMBAs) in Mexico.”<br />
These authors concluded, however, that a quarter of<br />
the micro-endemic amphibians “urgently need fieldbased<br />
verification to confirm their persistence due to<br />
the small percentage of remnant natural vegetation<br />
within the AMBAs, before we may sensibly recommend”<br />
a conservation strategy. Their tool also should<br />
apply to Mexican reptiles, and likely would produce<br />
similar results.<br />
7. The preferred method for preserving threatened species<br />
is to protect habitats by establishing protected<br />
areas, both in the public and private sectors. Habitat<br />
protection allows for a nearly incalculable array of relationships<br />
among organisms. Like most countries in<br />
the world, Mexico, has developed a governmentally<br />
established system of protected areas. Fortunately,<br />
studies have identified “critical conservation zones”<br />
(Ceballos et al. 2009), as well as gaps in their coverage<br />
(Koleff et al. 2009). The five reserves of greatest<br />
conservation importance for reptiles are the Los<br />
Tuxtlas Biosphere Reserve, the islands of the Gulf of<br />
California in the UNESCO World Heritage Site, the<br />
Sierra Gorda Biosphere Reserve, the Tehuacán-Cuicatlán<br />
Biosphere Reserve, and the Chamela-Cuixmala<br />
Biosphere Reserve. Significantly, all of these areas<br />
are part of the UNESCO World Network of Biosphere<br />
Reserves, but attainment of this status does not guarantee<br />
that these reserves will remain free from anthropogenic<br />
damage. Ceballos et al. (2009, citing Dirzo<br />
and García 1992) indicated that although the Los<br />
Tuxtlas is the most important reserve in Mexico for<br />
amphibians and reptiles, a large part of its natural vegetation<br />
has been lost. This example of deforestation is<br />
only one of many, but led Ceballos et al. (2009: 597)<br />
to conclude (our translation of the original Spanish)<br />
that, “The determination of high risk critical zones has<br />
diverse implications for conservation in Mexico. The<br />
distribution of critical zones in the entire country confirms<br />
the problem of the loss of biological diversity<br />
is severe at the present time, and everything indicates<br />
it will become yet more serious in future decades.<br />
On the other hand, the precise identification of these<br />
zones is a useful tool to guide political decisions concerning<br />
development and conservation in the country,<br />
and to maximize the effects of conservation action.<br />
Clearly, a fundamental linchpin for the national conservation<br />
strategy is to direct resources and efforts to<br />
protect the high-risk critical zones. Finally, it also is<br />
evident that tools for management of production and<br />
development, such as the land-use planning and environmental<br />
impact, should be reinforced in order to<br />
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fully comply with their function to reconcile development<br />
and conservation.” We fully support this recommendation.<br />
8. Humans have developed an amazing propensity for<br />
living in an unsustainable world. Organisms only can<br />
persist on Earth when they live within their environmental<br />
limiting factors, and their strategy is sustainability,<br />
i.e., in human terms, living over the long term<br />
within one’s means, a process made allowable by organic<br />
evolution. Homo sapiens is the only extant species<br />
with the capacity for devising another means for<br />
securing its place on the planet, i.e., a strategy of unsustainability<br />
over the short term, which eventually is<br />
calculated to fail. Conservation biology exists because<br />
humans have devised this unworkable living strategy.<br />
What success it will have in curbing biodiversity loss<br />
remains to be seen.<br />
Acknowledgments.—We are grateful to the following<br />
individuals for improving the quality of this contribution:<br />
Irene Goyenechea, Pablo Lavín-Murcio, Julio<br />
Lemos-Espinal, and Aurelio Ramírez-Bautista. We are<br />
especially thankful to Louis W. Porras, who applied his<br />
remarkable editorial skills to our work.<br />
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Ithaca, New York, USA.<br />
Mulcahy DG. 2007. Molecular systematics of Neotropical<br />
cat-eyed snakes: A test of the monophyly of Leptodeirini<br />
(Colubridae: Dipsadinae) with implications<br />
for character evolution and biogeography. Biological<br />
Journal of the Linnean Society 92: 483–500.<br />
Murphy RW, Berry KH, Edwards T, Leviton AE, Lathrop<br />
A, Riedle JD. 2011. The dazed and confused identity<br />
of Agassiz’s land tortoise, Gopherus agassizii (Testudines,<br />
Testudinidae) with the description of a new species,<br />
and its consequences for conservation. ZooKeys<br />
113: 39–71.<br />
Myers CW. 2011. A new genus and new tribe for Enicognathus<br />
melanauchen Jan, 1863, a neglected South<br />
American snake (Colubridae, Xenodontinae), with<br />
taxonomic notes on some Dipsadinae. American Museum<br />
Novitates 3715: 1–33.<br />
NatureServe Press Release. 2007. New assessment of<br />
North American reptiles finds rare good news. Available:<br />
www.natureserve.org [Accessed: 21 May 2012].<br />
Ochoa-Ochoa LM, Bezaury-Creel JE, Vázquez L-B,<br />
Flores-Villela O. 2011. Choosing the survivors? A<br />
GIS-based triage support tool for micro-endemics: application<br />
to data for Mexican amphibians. Biological<br />
Conservation 144: 2710–2718.<br />
Ochoa-Ochoa LM, Flores-Villela OA. 2006. Áreas de<br />
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Diversidad y Endemismo de la Herpetofauna Mexicana.<br />
Universidad Nacional Autónoma de México-<br />
Comisión Nacional para el Conocimiento y Uso de la<br />
Biodiversidad, México, DF, Mexico.<br />
Pavón-Vázquez CJ, García-Vázquez UO, Blancas-<br />
Hernández JC, Nieto-Montes A. 2011. A new species<br />
of the Geophis sieboldi group (Squamata: Colubridae)<br />
exhibiting color pattern polymorphism from Guerrero,<br />
Mexico. Herpetologica 67: 332–343.<br />
Population Reference Bureau. 2011. World Population<br />
Data Sheet. Available: www.prb.org [Accessed: 27<br />
January 2012].<br />
Pyron RA, Burbrink FT. 2009. Systematics of the common<br />
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and the burden of heritage in taxonomy. Zootaxa<br />
2241: 22–32.<br />
Raven PH, Hassenzahl DM, Berg LR. 2009. Environment<br />
(8 th edition). John Wiley & Sons, Inc. Hoboken,<br />
New Jersey, USA.<br />
Reyes-Velasco J, Mulcahy DG. 2010. Additional taxonomic<br />
remarks on the genus Pseudoleptodeira (Serpentes:<br />
Colubridae) and the phylogenetic placement<br />
of “P. uribei.” Herpetologica 66: 99–110.<br />
Sasa M, Chaves G, Porras LW. 2010. The Costa Rican<br />
herpetofauna: conservation status and future perspectives.<br />
Pp. 510–603 In: Conservation of Mesoamerican<br />
Amphibians and Reptiles. Editors, Wilson LD,<br />
Townsend JH, Johnson JD. Eagle Mountain Publishing,<br />
LC, Eagle Mountain, Utah, USA.<br />
Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues<br />
ASL, Fischman DL, Waller RW. 2004. Status and<br />
trends of amphibian declines and extinctions worldwide.<br />
Science 306(5702): 1783–1786.<br />
Stuart SN, Chanson JS, Cox NA, Young BE. 2010. The<br />
global decline of amphibians: Current trends and future<br />
prospects. Pp. 2–15 In: Conservation of Mesoamerican<br />
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LD, Townsend JH, Johnson JD. Eagle Mountain Publishing,<br />
LC, Eagle Mountain, Utah, USA.<br />
Sunyer J, Köhler G. 2010. Conservation status of the<br />
herpetofauna of Nicaragua. Pp. 488–509 In: Conservation<br />
of Mesoamerican Amphibians and Reptiles.<br />
Editors, Wilson LD, Townsend JH, Johnson JD. Eagle<br />
Mountain Publishing, LC, Eagle Mountain, Utah,<br />
USA.<br />
Townsend JH, Wilson LD. 2010. Conservation of the<br />
Honduran herpetofauna: issues and imperatives. Pp.<br />
460–487 In: Conservation of Mesoamerican Amphibians<br />
and Reptiles. Editors, Wilson LD, Townsend JH,<br />
Johnson JD. Eagle Mountain Publishing, LC, Eagle<br />
Mountain, Utah, USA.<br />
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Academic Press, Burlington, Maine, USA.<br />
Wake DB. 1991. Declining amphibian populations. Science<br />
253(5022): 860.<br />
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Review 42: 33–39.<br />
Wilson EO (Editor). 1988. Biodiversity. National Academy<br />
Press, Washington, DC, USA.<br />
Wilson LD. 2011. Imperatives and opportunities: reformation<br />
of herpetology in the age of amphibian decline.<br />
Herpetological Review 42: 146–150.<br />
Wilson LD, Johnson JD. 2010. Distributional patterns<br />
of the herpetofauna of Mesoamerica, a biodiversity<br />
hotspot. Pp. 30–235 In: Conservation of Mesoamerican<br />
Amphibians and Reptiles. Editors, Wilson LD,<br />
Townsend JH, Johnson JD. Eagle Mountain Publishing,<br />
LC, Eagle Mountain, Utah, USA.<br />
Wilson LD, McCranie JR. 1992. Status of amphibian<br />
populations in Honduras. Unpublished Report to the<br />
Task Force on Declining Amphibian Population, 15<br />
August 1992. 14 p.<br />
Wilson LD, McCranie JR. 2004. The conservation status<br />
of the herpetofauna of Honduras. Amphibian & Reptile<br />
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Mesoamerica: biodiversity significance, conservation<br />
status, and future challenges. Pp. 760–812 In: Conservation<br />
of Mesoamerican Amphibians and Reptiles.<br />
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Mountain Publishing, LC, Eagle Mountain, Utah,<br />
USA.<br />
Wilson LD, Townsend JH, Johnson JD. 2010. Conservation<br />
of Mesoamerican Amphibians and Reptiles. Eagle<br />
Mountain Publishing, LC, Eagle Mountain, Utah,<br />
USA.<br />
Woolrich-Piña, GA, Smith GR. 2012. A new species of<br />
Xenosaurus from the Sierra Madre Oriental, Mexico.<br />
Herpetologica 68: 551–559.<br />
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WWF International, Gland, Switzerland.<br />
Received: 18 Feb 2013<br />
Accepted: 24 April 2013<br />
Published: 09 June 2013<br />
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Larry David Wilson is a herpetologist with lengthy experience in Mesoamerica, totaling six collective years<br />
(combined over the past 47). Larry is the senior editor of the recently published Conservation of Mesoamerican<br />
Amphibians and Reptiles and a co-author of seven of its chapters. He retired after 35 years of<br />
service as Professor of Biology at Miami-Dade College in Miami, Florida. Larry is the author or co-author<br />
of more than 290 peer-reviewed papers and books on herpetology, including the 2004 Amphibian & Reptile<br />
Conservation paper entitled “The conservation status of the herpetofauna of Honduras.” His other<br />
books include The Snakes of Honduras, Middle American Herpetology, The Amphibians of Honduras,<br />
Amphibians & Reptiles of the Bay Islands and Cayos Cochinos, Honduras, The Amphibians and Reptiles<br />
of the Honduran Mosquitia, and Guide to the Amphibians & Reptiles of Cusuco National Park, Honduras.<br />
He also served as the Snake Section Editor for the Catalogue of American Amphibians and Reptiles for<br />
33 years. Over his career, Larry has authored or co-authored the descriptions of 69 currently recognized<br />
herpetofaunal species and six species have been named in his honor, including the anuran Craugastor<br />
lauraster and the snakes Cerrophidion wilsoni, Myriopholis wilsoni, and Oxybelis wilsoni.<br />
Vicente Mata-Silva is a herpetologist interested in ecology, conservation, and the monitoring of amphibians<br />
and reptiles in Mexico and the southwestern United States. His bachelor’s thesis compared herpetofaunal<br />
richness in Puebla, México, in habitats with different degrees of human related disturbance. Vicente’s<br />
master’s thesis focused primarily on the diet of two syntopic whiptail species of lizards, one unisexual<br />
and the other bisexual, in the Trans-Pecos region of the Chihuahuan Desert. Currently, he is a postdoctoral<br />
research fellow at the University of Texas at El Paso, where his work focuses on rattlesnake populations<br />
in their natural habitat. His dissertation was on the ecology of the rock rattlesnake, Crotalus lepidus, in<br />
the northern Chihuahuan Desert. To date, Vicente has authored or co-authored 34 peer-reviewed scientific<br />
publications.<br />
Jerry D. Johnson is Professor of Biological Sciences at The University of Texas at El Paso, and has extensive<br />
experience studying the herpetofauna of Mesoamerica. He is the Director of the 40,000 acre “Indio<br />
Mountains Research Station,” was a co-editor on the recently published Conservation of Mesoamerican<br />
Amphibians and Reptiles, and is Mesoamerica/Caribbean editor for the Geographic Distribution section<br />
of Herpetological Review. Johnson has authored or co-authored over 80 peer-reviewed papers, including<br />
two 2010 articles, “Geographic distribution and conservation of the herpetofauna of southeastern<br />
Mexico” and “Distributional patterns of the herpetofauna of Mesoamerica, a biodiversity hotspot.”<br />
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Appendix 1. Comparison of the IUCN Ratings from the 2005 Mexican Assessment (updated to the present time) and the Environmental Vulnerability<br />
Scores for 849 Mexican reptile species (crocodilians, turtles, lizards, and snakes). See text for explanation of the IUCN and EVS rating systems.<br />
* = species endemic to Mexico. 1 = IUCN status needs updating. 2 = Not rated because not recognized as a distinct species. 3 = not described<br />
at the time of assessment.<br />
Species<br />
IUCN<br />
Ratings<br />
Geographic<br />
Distribution<br />
Environmental Vulnerability Scores<br />
Ecological<br />
Distribution<br />
Degree of Human<br />
Persecution<br />
Order Crocodylia (3 species)<br />
Family Alligatoridae (1 species)<br />
Caiman crocodilus LC 1 3 7 6 16<br />
Family Crocodylidae (2 species)<br />
Crocodylus acutus VU 3 5 6 14<br />
Crocodylus moreletii LC 2 5 6 13<br />
Order Testudines (48 species)<br />
Family Cheloniidae (5 species)<br />
Caretta caretta EN — — — —<br />
Chelonia mydas EN — — — —<br />
Eretmochelys imbricata CR — — — —<br />
Lepidochelys kempii CR — — — —<br />
Lepidochelys olivacea VU — — — —<br />
Family Chelydridae (1 species)<br />
Chelydra rossignonii VU 4 7 6 17<br />
Family Dermatemydidae (1 species)<br />
Dermatemys mawii CR 4 7 6 17<br />
Family Dermochelyidae (1 species)<br />
Dermochelys coriacea CR — — — —<br />
Family Emydidae (15 species)<br />
Actinemys marmorata VU 3 8 6 17<br />
Chrysemys picta LC 3 8 3 14<br />
Pseudemys gorzugi NT 4 6 6 16<br />
Terrapene coahuila* EN 5 8 6 19<br />
Terrapene mexicana* NE 5 8 6 19<br />
Terrapene nelsoni* DD 5 7 6 18<br />
Terrapene ornata NT 3 6 6 15<br />
Terrapene yucatana* NE 5 7 6 18<br />
Trachemys gaigeae VU 4 8 6 18<br />
Trachemys nebulosa* NE 5 7 6 18<br />
Trachemys ornata* VU 5 8 6 19<br />
Trachemys scripta LC 3 7 6 16<br />
Trachemys taylori* EN 5 8 6 19<br />
Trachemys venusta NE 3 4 6 13<br />
Trachemys yaquia* VU 5 8 6 19<br />
Family Geoemydidae (3 species)<br />
Rhinoclemmys areolata NT 4 6 3 13<br />
Rhinoclemmys pulcherrima NE 1 4 3 8<br />
Rhinoclemmys rubida* NT 5 6 3 14<br />
Family Kinosternidae (17 species)<br />
Claudius angustatus NT 1 4 7 3 14<br />
Kinosternon acutum NT 1 4 7 3 14<br />
Total<br />
Score<br />
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Kinosternon alamosae* DD 5 6 3 14<br />
Kinosternon arizonense LC 4 8 3 15<br />
Kinosternon chimalhuaca* LC 5 8 3 16<br />
Kinosternon creaseri* LC 5 7 3 15<br />
Kinosternon durangoense* DD 5 8 3 16<br />
Kinosternon flavescens LC 3 6 3 12<br />
Kinosternon herrerai* NT 5 6 3 14<br />
Kinosternon hirtipes LC 2 5 3 10<br />
Kinosternon integrum* LC 5 3 3 11<br />
Kinosternon leucostomum NE 3 4 3 10<br />
Kinosternon oaxacae* DD 5 7 3 15<br />
Kinosternon scorpioides NE 3 4 3 10<br />
Kinosternon sonoriense NT 4 7 3 14<br />
Staurotypus salvinii NT 1 4 6 3 13<br />
Staurotypus triporcatus NT 1 4 7 3 14<br />
Family Testudinidae (3 species)<br />
Gopherus berlandieri LC 1 4 8 6 18<br />
Gopherus flavomarginatus* VU 5 8 6 19<br />
Gopherus morafkai NE 3 4 5 6 15<br />
Family Trionychidae (2 species)<br />
Apalone atra* NE 6 8 6 20<br />
Apalone spinifera LC 3 6 6 15<br />
Order Squamata (798 species)<br />
Family Bipedidae (3 species)<br />
Bipes biporus* LC 5 8 1 14<br />
Bipes canaliculatus* LC 5 6 1 12<br />
Bipes tridactylus* LC 5 8 1 14<br />
Family Anguidae (48 species)<br />
Abronia bogerti* DD 6 8 4 18<br />
Abronia chiszari* EN 6 7 4 17<br />
Abronia deppii* EN 6 6 4 16<br />
Abronia fuscolabialis* EN 6 8 4 18<br />
Abronia graminea* EN 5 6 4 15<br />
Abronia leurolepis* DD 6 8 4 18<br />
Abronia lythrochila* LC 6 7 4 17<br />
Abronia martindelcampoi* EN 5 6 4 15<br />
Abronia matudai EN 4 7 4 15<br />
Abronia mitchelli* DD 6 8 4 18<br />
Abronia mixteca* VU 6 8 4 18<br />
Abronia oaxacae* VU 6 7 4 17<br />
Abronia ochoterenai DD 4 8 4 16<br />
Abronia ornelasi* DD 6 8 4 18<br />
Abronia ramirezi* DD 6 8 4 18<br />
Abronia reidi* DD 6 8 4 18<br />
Abronia smithi* LC 6 7 4 17<br />
Abronia taeniata* VU 5 6 4 15<br />
Anguis ceroni* NE 5 7 2 14<br />
Anguis incomptus* NE 5 8 2 15<br />
Barisia ciliaris* NE 5 7 3 15<br />
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Barisia herrerae* EN 5 7 3 15<br />
Barisia imbricata* LC 5 6 3 14<br />
Barisia jonesi* NE 2 6 7 3 16<br />
Barisia levicollis* DD 5 7 3 15<br />
Barisia planifrons* NE 2 5 7 3 15<br />
Barisia rudicollis* EN 5 7 3 15<br />
Celestus enneagrammus* LC 5 6 3 14<br />
Celestus ingridae* DD 6 8 3 17<br />
Celestus legnotus* LC 5 6 3 14<br />
Celestus rozellae NT 4 6 3 13<br />
Elgaria cedrosensis* LC 5 8 3 16<br />
Elgaria kingii LC 2 5 3 10<br />
Elgaria multicarinata LC 3 4 3 10<br />
Elgaria nana* LC 5 8 3 16<br />
Elgaria paucicarinata* VU 5 5 3 13<br />
Elgaria velazquezi* LC 5 6 3 14<br />
Gerrhonotus farri* NE 3 6 8 3 17<br />
Gerrhonotus infernalis* LC 5 5 3 13<br />
Gerrhonotus liocephalus LC 2 1 3 6<br />
Gerrhonotus lugoi* LC 6 8 3 17<br />
Gerrhonotus ophiurus* LC 5 4 3 12<br />
Gerrhonotus parvus* EN 6 8 3 17<br />
Mesaspis antauges* DD 6 7 3 16<br />
Mesaspis gadovii* LC 5 6 3 14<br />
Mesaspis juarezi* EN 5 7 3 15<br />
Mesaspis moreleti LC 3 3 3 9<br />
Mesaspis viridiflava* LC 5 8 3 16<br />
Family Anniellidae (2 species)<br />
Anniella geronimensis* EN 5 7 1 13<br />
Anniella pulchra LC 3 8 1 12<br />
Family Corytophanidae (6 species)<br />
Basiliscus vittatus NE 1 3 3 7<br />
Corytophanes cristatus NE 3 5 3 11<br />
Corytophanes hernandesii NE 4 6 3 13<br />
Corytophanes percarinatus NE 4 4 3 11<br />
Laemanctus longipes NE 1 5 3 9<br />
Laemanctus serratus LC 2 3 3 8<br />
Family Crotaphytidae (10 species)<br />
Crotaphytus antiquus* EN 5 8 3 16<br />
Crotaphytus collaris LC 3 7 3 13<br />
Crotaphytus dickersonae* LC 5 8 3 16<br />
Crotaphytus grismeri* LC 5 8 3 16<br />
Crotaphytus insularis* LC 6 7 3 16<br />
Crotaphytus nebrius LC 2 7 3 12<br />
Crotaphytus reticulatus VU 4 5 3 12<br />
Crotaphytus vestigium LC 3 3 3 9<br />
Gambelia copeii LC 2 6 3 11<br />
Gambelia wislizenii LC 3 7 3 13<br />
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Family Dactyloidae (50 species)<br />
Anolis allisoni NE 3 7 3 13<br />
Anolis alvarezdeltoroi* DD 6 8 3 17<br />
Anolis anisolepis* LC 5 7 3 15<br />
Anolis barkeri* VU 5 7 3 15<br />
Anolis beckeri NE 3 3 6 3 12<br />
Anolis biporcatus NE 3 4 3 10<br />
Anolis breedlovei* EN 6 7 3 16<br />
Anolis capito NE 3 6 3 13<br />
Anolis compressicauda* LC 5 7 3 15<br />
Anolis crassulus NE 3 4 3 10<br />
Anolis cristifer DD 4 6 3 13<br />
Anolis cuprinus* LC 6 7 3 16<br />
Anolis cymbops* DD 6 8 3 17<br />
Anolis dollfusianus NE 4 6 3 13<br />
Anolis duellmani* DD 6 8 3 17<br />
Anolis dunni* LC 5 8 3 16<br />
Anolis forbesi* DD 6 7 3 16<br />
Anolis gadovi* LC 5 8 3 16<br />
Anolis hobartsmithi* EN 6 6 3 15<br />
Anolis isthmicus* DD 5 8 3 16<br />
Anolis laeviventris NE 3 3 3 9<br />
Anolis lemurinus NE 3 2 3 8<br />
Anolis liogaster* LC 5 6 3 14<br />
Anolis macrinii* LC 5 8 3 16<br />
Anolis matudai NE 4 6 3 13<br />
Anolis megapholidotus* LC 5 8 3 16<br />
Anolis microlepidotus* LC 5 7 3 15<br />
Anolis milleri* DD 5 6 3 14<br />
Anolis naufragus* VU 5 5 3 13<br />
Anolis nebuloides* LC 5 6 3 14<br />
Anolis nebulosus* LC 5 5 3 13<br />
Anolis omiltemanus* LC 5 7 3 15<br />
Anolis parvicirculatus* LC 6 7 3 16<br />
Anolis petersii NE 2 4 3 9<br />
Anolis polyrhachis* DD 5 8 3 16<br />
Anolis pygmaeus* EN 5 8 3 16<br />
Anolis quercorum* LC 5 8 3 16<br />
Anolis rodriguezii NE 4 3 3 10<br />
Anolis sagrei NE 2 7 3 12<br />
Anolis schiedii* DD 5 8 3 16<br />
Anolis schmidti* LC 5 8 3 16<br />
Anolis sericeus NE 2 3 3 8<br />
Anolis serranoi NE 4 5 3 12<br />
Anolis simmonsi* DD 5 7 3 15<br />
Anolis subocularis* DD 5 7 3 15<br />
Anolis taylori* LC 5 8 3 16<br />
Anolis tropidonotus NE 4 2 3 9<br />
Anolis uniformis NE 4 6 3 13<br />
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Anolis unilobatus NE 3 1 3 3 7<br />
Anolis utowanae* DD 6 8 3 17<br />
Family Dibamidae (1 species)<br />
Anelytropsis papillosus* LC 5 4 1 10<br />
Family Eublepharidae (7 species)<br />
Coleonyx brevis LC 4 6 4 14<br />
Coleonyx elegans NE 2 3 4 9<br />
Coleonyx fasciatus* LC 5 8 4 17<br />
Coleonyx gypsicolus* LC 6 8 4 18<br />
Coleonyx reticulatus LC 4 7 4 15<br />
Coleonyx switaki LC 4 6 4 14<br />
Coleonyx variegatus LC 4 3 4 11<br />
Family Gymnophthalmidae (1 species)<br />
Gymnophthalmus speciosus NE 3 3 3 9<br />
Family Helodermatidae (2 species)<br />
Heloderma horridum LC 2 4 5 11<br />
Heloderma suspectum NT 4 6 5 15<br />
Family Iguanidae (19 species)<br />
Ctenosaura acanthura NE 2 4 6 12<br />
Ctenosaura alfredschmidti NT 4 8 3 15<br />
Ctenosaura clarki* VU 5 7 3 15<br />
Ctenosaura conspicuosa* NE 5 8 3 16<br />
Ctenosaura defensor* VU 5 7 3 15<br />
Ctenosaura hemilopha* NE 5 7 6 18<br />
Ctenosaura macrolopha* NE 5 8 6 19<br />
Ctenosaura nolascensis* NE 6 8 3 17<br />
Ctenosaura oaxacana* CR 5 8 6 19<br />
Ctenosaura pectinata* NE 5 4 6 15<br />
Ctenosaura similis LC 1 4 3 8<br />
Dipsosaurus catalinensis* NE 6 8 3 17<br />
Dipsosaurus dorsalis LC 4 4 3 11<br />
Iguana iguana NE 3 3 6 12<br />
Sauromalus ater LC 4 6 3 13<br />
Sauromalus hispidus* NT 5 6 3 14<br />
Sauromalus klauberi* NE 6 7 3 16<br />
Sauromalus slevini* NE 5 8 3 16<br />
Sauromalus varius* NE 5 8 3 16<br />
Family Mabuyidae (1 species)<br />
Marisora brachypoda NE 1 2 3 6<br />
Family Phrynosomatidae (135 species)<br />
Callisaurus draconoides LC 4 5 3 12<br />
Cophosaurus texanus LC 4 7 3 14<br />
Holbrookia approximans* NE 5 6 3 14<br />
Holbrookia elegans LC 4 6 3 13<br />
Holbrookia lacerata NT 4 7 3 14<br />
Holbrookia maculata LC 1 6 3 10<br />
Holbrookia propinqua LC 4 8 3 15<br />
Petrosaurus mearnsi LC 4 5 3 12<br />
Petrosaurus repens* LC 5 5 3 13<br />
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Petrosaurus slevini* LC 5 8 3 16<br />
Petrosaurus thalassinus* LC 5 5 3 13<br />
Phrynosoma asio NE 2 6 3 11<br />
Phrynosoma blainvillii NE 3 7 3 13<br />
Phrynosoma braconnieri* LC 5 7 3 15<br />
Phrynosoma cerroense* NE 6 7 3 16<br />
Phrynosoma cornutum LC 1 7 3 11<br />
Phrynosoma coronatum* LC 5 4 3 12<br />
Phrynosoma ditmarsi* DD 5 8 3 16<br />
Phrynosoma goodei NE 4 6 3 13<br />
Phrynosoma hernandesi LC 3 7 3 13<br />
Phrynosoma mcallii NT 4 8 3 15<br />
Phrynosoma modestum LC 4 5 3 12<br />
Phrynosoma orbiculare* LC 5 4 3 12<br />
Phrynosoma platyrhinos LC 3 7 3 13<br />
Phrynosoma solare LC 4 7 3 14<br />
Phrynosoma taurus* LC 5 4 3 12<br />
Phrynosoma wigginsi* NE 5 8 3 16<br />
Sceloporus acanthinus NE 3 7 3 13<br />
Sceloporus adleri* LC 5 7 3 15<br />
Sceloporus aeneus* LC 5 5 3 13<br />
Sceloporus albiventris* NE 5 8 3 16<br />
Sceloporus anahuacus* LC 5 7 3 15<br />
Sceloporus angustus* LC 5 8 3 16<br />
Sceloporus asper* LC 5 6 3 14<br />
Sceloporus bicanthalis* LC 5 5 3 13<br />
Sceloporus bulleri* LC 5 7 3 15<br />
Sceloporus carinatus LC 4 5 3 12<br />
Sceloporus cautus* LC 5 7 3 15<br />
Sceloporus chaneyi* EN 5 7 3 15<br />
Sceloporus chrysostictus LC 4 6 3 13<br />
Sceloporus clarkii LC 2 5 3 10<br />
Sceloporus couchii* LC 5 7 3 15<br />
Sceloporus cowlesi NE 4 6 3 13<br />
Sceloporus cozumelae* LC 5 7 3 15<br />
Sceloporus cryptus* LC 5 6 3 14<br />
Sceloporus cupreus* NE 5 8 3 16<br />
Sceloporus cyanogenys* NE 6 7 3 16<br />
Sceloporus cyanostictus* EN 5 8 3 16<br />
Sceloporus druckercolini* NE 5 6 3 14<br />
Sceloporus dugesii* LC 5 5 3 13<br />
Sceloporus edwardtaylori* LC 5 6 3 14<br />
Sceloporus exsul* CR 6 8 3 17<br />
Sceloporus formosus* LC 5 7 3 15<br />
Sceloporus gadoviae* LC 5 3 3 11<br />
Sceloporus goldmani* EN 5 7 3 15<br />
Sceloporus grammicus LC 2 4 3 9<br />
Sceloporus grandaevus* LC 6 7 3 16<br />
Sceloporus halli* DD 6 8 3 17<br />
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Sceloporus heterolepis* LC 5 6 3 14<br />
Sceloporus horridus* LC 5 3 3 11<br />
Sceloporus hunsakeri* LC 5 6 3 14<br />
Sceloporus insignis* LC 5 8 3 16<br />
Sceloporus internasalis LC 4 4 3 11<br />
Sceloporus jalapae* LC 5 5 3 13<br />
Sceloporus jarrovii LC 2 6 3 11<br />
Sceloporus lemosespinali* DD 5 8 3 16<br />
Sceloporus licki* LC 5 5 3 13<br />
Sceloporus lineatulus* LC 6 8 3 17<br />
Sceloporus lineolateralis* NE 5 8 3 16<br />
Sceloporus lundelli LC 4 7 3 14<br />
Sceloporus macdougalli* LC 5 8 3 16<br />
Sceloporus maculosus* VU 5 8 3 16<br />
Sceloporus magister LC 1 5 3 9<br />
Sceloporus marmoratus NE 2 6 3 11<br />
Sceloporus megalepidurus* VU 5 6 3 14<br />
Sceloporus melanorhinus LC 2 4 3 9<br />
Sceloporus merriami LC 4 6 3 13<br />
Sceloporus minor* LC 5 6 3 14<br />
Sceloporus mucronatus* LC 5 5 3 13<br />
Sceloporus nelsoni* LC 5 5 3 13<br />
Sceloporus oberon* VU 5 6 3 14<br />
Sceloporus occidentalis LC 3 6 3 12<br />
Sceloporus ochoterenae* LC 5 4 3 12<br />
Sceloporus olivaceus LC 4 6 3 13<br />
Sceloporus orcutti LC 2 2 3 7<br />
Sceloporus ornatus* NT 5 8 3 16<br />
Sceloporus palaciosi* LC 5 7 3 15<br />
Sceloporus parvus* LC 5 7 3 15<br />
Sceloporus poinsetti LC 4 5 3 12<br />
Sceloporus prezygus NE 4 8 3 15<br />
Sceloporus pyrocephalus* LC 5 4 3 12<br />
Sceloporus salvini* DD 5 7 3 15<br />
Sceloporus samcolemani* LC 5 7 3 15<br />
Sceloporus scalaris* LC 5 4 3 12<br />
Sceloporus serrifer LC 2 1 3 6<br />
Sceloporus shannonorum* NE 5 7 3 15<br />
Sceloporus siniferus LC 2 6 3 11<br />
Sceloporus slevini LC 2 6 3 11<br />
Sceloporus smaragdinus LC 4 5 3 12<br />
Sceloporus smithi* LC 5 7 3 15<br />
Sceloporus spinosus* LC 5 4 3 12<br />
Sceloporus squamosus NE 3 5 3 11<br />
Sceloporus stejnegeri* LC 5 5 3 13<br />
Sceloporus subniger* NE 5 7 3 15<br />
Sceloporus subpictus* DD 6 7 3 16<br />
Sceloporus sugillatus* LC 5 8 3 16<br />
Sceloporus taeniocnemis LC 4 5 3 12<br />
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Sceloporus tanneri* DD 6 7 3 16<br />
Sceloporus teapensis LC 4 6 3 13<br />
Sceloporus torquatus* LC 5 3 3 11<br />
Sceloporus uniformis NE 3 7 3 13<br />
Sceloporus utiformis* LC 5 7 3 15<br />
Sceloporus vandenburgianus LC 4 7 3 14<br />
Sceloporus variabilis NE 1 1 3 5<br />
Sceloporus virgatus LC 4 8 3 15<br />
Sceloporus zosteromus* LC 5 4 3 12<br />
Uma exsul* EN 5 8 3 16<br />
Uma notata NT 4 8 3 15<br />
Uma paraphygas* NT 6 8 3 17<br />
Uma rufopunctata* NT 5 8 3 16<br />
Urosaurus auriculatus* EN 6 7 3 16<br />
Urosaurus bicarinatus* LC 5 4 3 12<br />
Urosaurus clarionensis* VU 6 8 3 17<br />
Urosaurus gadovi* LC 3 6 3 12<br />
Urosaurus graciosus LC 3 8 3 14<br />
Urosaurus lahtelai* LC 5 8 3 16<br />
Urosaurus nigricaudus LC 3 2 3 8<br />
Urosaurus ornatus LC 2 5 3 10<br />
Uta encantadae* VU 6 8 3 17<br />
Uta lowei* VU 6 8 3 17<br />
Uta nolascensis* LC 6 8 3 17<br />
Uta palmeri* VU 6 8 3 17<br />
Uta squamata* LC 6 8 3 17<br />
Uta stansburiana LC 3 1 3 7<br />
Uta tumidarostra* VU 6 8 3 17<br />
Family Phyllodactylidae (15 species)<br />
Phyllodactylus bordai* LC 5 5 3 13<br />
Phyllodactylus bugastrolepis* LC 6 8 3 17<br />
Phyllodactylus davisi* LC 5 8 3 16<br />
Phyllodactylus delcampoi* LC 5 8 3 16<br />
Phyllodactylus duellmani* LC 5 8 3 16<br />
Phyllodactylus homolepidurus* LC 5 7 3 15<br />
Phyllodactylus lanei* LC 5 7 3 15<br />
Phyllodactylus muralis* LC 5 6 3 14<br />
Phyllodactylus nocticolus NE 2 5 3 10<br />
Phyllodactylus partidus* LC 5 8 3 16<br />
Phyllodactylus paucituberculatus* DD 6 7 3 16<br />
Phyllodactylus tuberculosus NE 1 4 3 8<br />
Phyllodactylus unctus* NT 5 7 3 15<br />
Phyllodactylus xanti* LC 5 7 3 15<br />
Thecadactylus rapicauda NE 3 4 3 10<br />
Family Scincidae (23 species)<br />
Mesoscincus altamirani* DD 5 6 3 14<br />
Mesoscincus schwartzei LC 2 6 3 11<br />
Plestiodon bilineatus* NE 5 5 3 13<br />
Plestiodon brevirostris* LC 5 3 3 11<br />
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Plestiodon callicephalus LC 2 7 3 12<br />
Plestiodon colimensis* DD 5 6 3 14<br />
Plestiodon copei* LC 5 6 3 14<br />
Plestiodon dicei* NE 5 4 3 12<br />
Plestiodon dugesi* VU 5 8 3 16<br />
Plestiodon gilberti LC 3 6 3 12<br />
Plestiodon indubitus* NE 5 7 3 15<br />
Plestiodon lagunensis* LC 6 6 3 15<br />
Plestiodon lynxe* LC 5 2 3 10<br />
Plestiodon multilineatus* DD 5 8 3 16<br />
Plestiodon multivirgatus LC 3 8 3 14<br />
Plestiodon nietoi* NE 6 8 3 17<br />
Plestiodon obsoletus LC 3 5 3 11<br />
Plestiodon ochoterenae* LC 5 5 3 13<br />
Plestiodon parviauriculatus* DD 5 7 3 15<br />
Plestiodon parvulus* DD 5 7 3 15<br />
Plestiodon skiltonianus LC 3 5 3 11<br />
Plestiodon sumichrasti NE 4 5 3 12<br />
Plestiodon tetragrammus LC 4 5 3 12<br />
Family Sphaerodactylidae (4 species)<br />
Aristelliger georgeensis NE 3 7 3 13<br />
Gonatodes albogularis NE 3 5 3 11<br />
Sphaerodactylus continentalis NE 4 3 3 10<br />
Sphaerodactylus glaucus NE 4 5 3 12<br />
Family Sphenomorphidae (6 species)<br />
Scincella gemmingeri* LC 5 3 3 11<br />
Scincella kikaapoda* NE 3 6 8 3 17<br />
Scincella lateralis LC 3 7 3 13<br />
Scincella silvicola* LC 5 4 3 12<br />
Sphenomorphus assatus NE 2 2 3 7<br />
Sphenomorphus cherriei NE 3 2 3 8<br />
Family Teiidae (46 species)<br />
Aspidoscelis angusticeps LC 4 6 3 13<br />
Aspidoscelis bacata* LC 6 8 3 17<br />
Aspidoscelis burti LC 4 8 3 15<br />
Aspidoscelis calidipes* LC 5 6 3 14<br />
Aspidoscelis cana* LC 5 8 3 16<br />
Aspidoscelis carmenensis* LC 6 8 3 17<br />
Aspidoscelis catalinensis* VU 6 8 3 17<br />
Aspidoscelis celeripes* LC 5 7 3 15<br />
Aspidoscelis ceralbensis* LC 6 8 3 17<br />
Aspidoscelis communis* LC 5 6 3 14<br />
Aspidoscelis costata* LC 5 3 3 11<br />
Aspidoscelis cozumela* LC 5 8 3 16<br />
Aspidoscelis danheimae* LC 6 7 3 16<br />
Aspidoscelis deppii LC 1 4 3 8<br />
Aspidoscelis espiritensis* LC 5 8 3 16<br />
Aspidoscelis exanguis LC 4 7 3 14<br />
Aspidoscelis franciscensis* LC 6 8 3 17<br />
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Aspidoscelis gularis LC 2 4 3 9<br />
Aspidoscelis guttata* LC 5 4 3 12<br />
Aspidoscelis hyperythra LC 2 5 3 10<br />
Aspidoscelis inornata LC 4 7 3 14<br />
Aspidoscelis labialis* VU 5 7 3 15<br />
Aspidoscelis laredoensis LC 4 7 3 14<br />
Aspidoscelis lineattissima* LC 5 6 3 14<br />
Aspidoscelis marmorata NE 4 7 3 14<br />
Aspidoscelis martyris* VU 6 8 3 17<br />
Aspidoscelis maslini LC 4 8 3 15<br />
Aspidoscelis mexicana* LC 5 6 3 14<br />
Aspidoscelis motaguae LC 4 5 3 12<br />
Aspidoscelis neomexicana LC 4 8 3 15<br />
Aspidoscelis opatae* DD 5 8 3 16<br />
Aspidoscelis parvisocia* LC 5 7 3 15<br />
Aspidoscelis picta* LC 6 8 3 17<br />
Aspidoscelis rodecki* NT 5 8 3 16<br />
Aspidoscelis sackii* LC 5 6 3 14<br />
Aspidoscelis semptemvittata LC 3 7 3 13<br />
Aspidoscelis sexlineata LC 3 8 3 14<br />
Aspidoscelis sonorae LC 4 6 3 13<br />
Aspidoscelis stictogramma NE 4 7 3 14<br />
Aspidoscelis tesselata LC 4 7 3 14<br />
Aspidoscelis tigris LC 3 2 3 8<br />
Aspidoscelis uniparens LC 4 8 3 15<br />
Aspidoscelis xanthonota NE 4 7 3 14<br />
Holcosus chaitzami DD 4 7 3 14<br />
Holcosus festiva NE 3 5 3 11<br />
Holcosus undulatus NE 2 2 3 7<br />
Family Xantusiidae (25 species)<br />
Lepidophyma chicoasense* DD 6 8 2 16<br />
Lepidophyma cuicateca* NE 3 6 8 2 16<br />
Lepidophyma dontomasi* DD 6 6 2 14<br />
Lepidophyma flavimaculatum NE 1 5 2 8<br />
Lepidophyma gaigeae* VU 5 6 2 13<br />
Lepidophyma lineri* DD 5 8 2 15<br />
Lepidophyma lipetzi* EN 6 8 2 16<br />
Lepidophyma lowei* DD 6 8 2 16<br />
Lepidophyma micropholis* VU 5 8 2 15<br />
Lepidophyma occulor* LC 5 7 2 14<br />
Lepidophyma pajapanense* LC 5 6 2 13<br />
Lepidophyma radula* DD 6 5 2 13<br />
Lepidophyma smithii NE 2 4 2 8<br />
Lepidophyma sylvaticum* LC 5 4 2 11<br />
Lepidophyma tarascae* DD 5 7 2 14<br />
Lepidophyma tuxtlae* DD 5 4 2 11<br />
Lepidophyma zongolica* NE 3 6 8 2 16<br />
Xantusia bolsonae* DD 6 8 3 17<br />
Xantusia extorris* LC 5 7 3 15<br />
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Xantusia gilberti* NE 5 8 3 16<br />
Xantusia henshawi LC 4 5 3 12<br />
Xantusia jaycolei* NE 5 8 3 16<br />
Xantusia sanchezi* LC 5 8 3 16<br />
Xantusia sherbrookei* NE 5 8 3 16<br />
Xantusia wigginsi NE 4 7 3 14<br />
Family Xenosauridae (9 species)<br />
Xenosaurus agrenon* NE 5 4 3 12<br />
Xenosaurus grandis* VU 5 1 3 9<br />
Xenosaurus newmanorum* EN 5 7 3 15<br />
Xenosaurus penai* LC 6 7 3 16<br />
Xenosaurus phalaroanthereon* DD 5 8 3 16<br />
Xenosaurus platyceps* EN 5 6 3 14<br />
Xenosaurus rackhami NE 4 4 3 11<br />
Xenosaurus rectocollaris* LC 5 8 3 16<br />
Xenosaurus tzacualtipantecus* NE 6 8 3 17<br />
Family Boidae (2 species)<br />
Boa constrictor NE 3 1 6 10<br />
Charina trivirgata LC 4 3 3 10<br />
Family Colubridae (136 species)<br />
Arizona elegans LC 1 1 3 5<br />
Arizona pacata* LC 5 5 4 14<br />
Bogertophis rosaliae LC 2 5 3 10<br />
Bogertophis subocularis LC 4 7 3 14<br />
Chilomeniscus savagei* LC 6 7 2 15<br />
Chilomeniscus stramineus LC 4 2 2 8<br />
Chionactus occipitalis LC 4 6 2 12<br />
Chionactus palarostris LC 4 7 2 13<br />
Coluber constrictor LC 1 6 3 10<br />
Conopsis acuta* NE 5 7 2 14<br />
Conopsis amphisticha* NT 5 8 2 15<br />
Conopsis biserialis* LC 5 6 2 13<br />
Conopsis lineata* LC 5 6 2 13<br />
Conopsis megalodon* LC 5 7 2 14<br />
Conopsis nasus* LC 5 4 2 11<br />
Dendrophidion vinitor LC 3 7 3 13<br />
Drymarchon melanurus LC 1 1 4 6<br />
Drymobius chloroticus LC 1 3 4 8<br />
Drymobius margaritiferus NE 1 1 4 6<br />
Ficimia hardyi* EN 5 6 2 13<br />
Ficimia olivacea* NE 5 2 2 9<br />
Ficimia publia NE 4 3 2 9<br />
Ficimia ramirezi* DD 6 8 2 16<br />
Ficimia ruspator* DD 6 8 2 16<br />
Ficimia streckeri LC 3 7 2 12<br />
Ficimia variegata* DD 5 7 2 14<br />
Geagras redimitus* DD 5 7 2 14<br />
Gyalopion canum LC 4 3 2 9<br />
Gyalopion quadrangulare LC 3 6 2 11<br />
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Lampropeltis alterna LC 4 7 3 14<br />
Lampropeltis californiae NE 2 3 4 3 10<br />
Lampropeltis catalinensis* DD 6 8 3 17<br />
Lampropeltis herrerae* CR 6 8 3 17<br />
Lampropeltis holbrooki NE 2 3 8 3 14<br />
Lampropeltis knoblochi NE 2 2 5 3 10<br />
Lampropeltis mexicana* LC 5 7 3 15<br />
Lampropeltis ruthveni* NT 5 8 3 16<br />
Lampropeltis splendida NE 2 4 5 3 12<br />
Lampropeltis triangulum NE 1 1 5 7<br />
Lampropeltis webbi* DD 5 8 3 16<br />
Lampropeltis zonata LC 3 7 5 15<br />
Leptophis ahaetulla NE 3 3 4 10<br />
Leptophis diplotropis* LC 5 5 4 14<br />
Leptophis mexicanus LC 1 1 4 6<br />
Leptophis modestus VU 3 7 4 14<br />
Liochlorophis vernalis LC 3 8 3 14<br />
Masticophis anthonyi* CR 6 8 3 17<br />
Masticophis aurigulus* LC 5 4 4 13<br />
Masticophis barbouri* DD 6 8 3 17<br />
Masticophis bilineatus LC 2 5 4 11<br />
Masticophis flagellum LC 1 3 4 8<br />
Masticophis fuliginosus NE 2 3 4 9<br />
Masticophis lateralis LC 3 3 4 10<br />
Masticophis mentovarius NE 1 1 4 6<br />
Masticophis schotti LC 4 5 4 13<br />
Masticophis slevini* LC 6 8 3 17<br />
Masticophis taeniatus LC 1 5 4 10<br />
Mastigodryas cliftoni* NE 5 6 3 14<br />
Mastigodryas melanolomus LC 1 1 4 6<br />
Opheodrys aestivus LC 3 7 3 13<br />
Oxybelis aeneus NE 1 1 3 5<br />
Oxybelis fulgidus NE 3 2 4 9<br />
Pantherophis bairdi NE 4 7 4 15<br />
Pantherophis emoryi LC 3 6 4 13<br />
Phyllorhynchus browni LC 4 7 2 13<br />
Phyllorhynchus decurtatus LC 4 5 2 11<br />
Pituophis catenifer LC 4 1 4 9<br />
Pituophis deppei* LC 5 5 4 14<br />
Pituophis insulanus* LC 6 6 4 16<br />
Pituophis lineaticollis LC 2 2 4 8<br />
Pituophis vertebralis* LC 5 3 4 12<br />
Pseudelaphe flavirufa LC 2 4 4 10<br />
Pseudelaphe phaescens* NE 5 7 4 16<br />
Pseudoficimia frontalis* LC 5 5 3 13<br />
Pseustes poecilonotus LC 3 4 3 10<br />
Rhinocheilus antonii* NE 5 8 3 16<br />
Rhinocheilus etheridgei* DD 6 7 3 16<br />
Rhinocheilus lecontei LC 1 3 4 8<br />
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Salvadora bairdi* LC 5 6 4 15<br />
Salvadora deserticola NE 4 6 4 14<br />
Salvadora grahamiae LC 4 2 4 10<br />
Salvadora hexalepis LC 4 2 4 10<br />
Salvadora intermedia* LC 5 7 4 16<br />
Salvadora lemniscata* LC 5 6 4 15<br />
Salvadora mexicana* LC 5 6 4 15<br />
Scaphiodontophis annulatus NE 1 5 5 11<br />
Senticolis triaspis NE 2 1 3 6<br />
Sonora aemula* NT 5 6 5 16<br />
Sonora michoacanensis* LC 5 6 3 14<br />
Sonora mutabilis* LC 5 6 3 14<br />
Sonora semiannulata LC 1 1 3 5<br />
Spilotes pullatus NE 1 1 4 6<br />
Stenorrhina degenhardtii NE 3 3 3 9<br />
Stenorrhina freminvillii NE 1 2 4 7<br />
Symphimus leucostomus* LC 5 6 3 14<br />
Symphimus mayae LC 4 7 3 14<br />
Sympholis lippiens* NE 5 6 3 14<br />
Tantilla atriceps LC 2 7 2 11<br />
Tantilla bocourti* LC 5 2 2 9<br />
Tantilla briggsi* DD 6 8 2 16<br />
Tantilla calamarina* LC 5 5 2 12<br />
Tantilla cascadae* DD 6 8 2 16<br />
Tantilla ceboruca* NE 6 8 2 16<br />
Tantilla coronadoi* LC 6 7 2 15<br />
Tantilla cuniculator LC 4 7 2 13<br />
Tantilla deppei* LC 5 6 2 13<br />
Tantilla flavilineata* EN 5 7 2 14<br />
Tantilla gracilis LC 3 8 2 13<br />
Tantilla hobartsmithi LC 3 6 2 11<br />
Tantilla impensa LC 3 5 2 10<br />
Tantilla johnsoni* DD 6 8 2 16<br />
Tantilla moesta LC 4 7 2 13<br />
Tantilla nigriceps LC 3 6 2 11<br />
Tantilla oaxacae* DD 6 7 2 15<br />
Tantilla planiceps LC 4 3 2 9<br />
Tantilla robusta* DD 6 8 2 16<br />
Tantilla rubra LC 2 1 2 5<br />
Tantilla schistosa NE 3 3 2 8<br />
Tantilla sertula* DD 6 8 2 16<br />
Tantilla shawi* EN 5 8 2 15<br />
Tantilla slavensi* DD 5 7 2 14<br />
Tantilla striata* DD 5 7 2 14<br />
Tantilla tayrae* DD 6 7 2 15<br />
Tantilla triseriata* DD 5 6 2 13<br />
Tantilla vulcani NE 4 6 2 12<br />
Tantilla wilcoxi LC 2 6 2 10<br />
Tantilla yaquia LC 2 6 2 10<br />
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Tantillita brevissima LC 4 3 2 9<br />
Tantillita canula LC 4 6 2 12<br />
Tantillita lintoni LC 4 6 2 12<br />
Trimorphodon biscutatus NE 2 1 4 7<br />
Trimorphodon lambda NE 4 5 4 13<br />
Trimorphodon lyrophanes NE 4 2 4 10<br />
Trimorphodon paucimaculatus* NE 5 6 4 15<br />
Trimorphodon tau* LC 5 4 4 13<br />
Trimorphodon vilkinsonii LC 4 7 4 15<br />
Family Dipsadidae (115 species)<br />
Adelphicos latifasciatum* DD 6 7 2 15<br />
Adelphicos newmanorum* NE 5 5 2 12<br />
Adelphicos nigrilatum* LC 5 7 2 14<br />
Adelphicos quadrivirgatum DD 4 4 2 10<br />
Adelphicos sargii LC 4 6 2 12<br />
Amastridium sapperi NE 4 4 2 10<br />
Chersodromus liebmanni* LC 5 5 2 12<br />
Chersodromus rubriventris* EN 5 7 2 14<br />
Coniophanes alvarezi* DD 6 8 3 17<br />
Coniophanes bipunctatus NE 1 5 3 10<br />
Coniophanes fissidens NE 1 3 3 7<br />
Coniophanes imperialis LC 2 3 3 8<br />
Coniophanes lateritius* DD 5 5 3 13<br />
Coniophanes melanocephalus* DD 5 6 3 14<br />
Coniophanes meridanus* LC 5 7 3 15<br />
Coniophanes michoacanensis* NE 3 6 8 3 17<br />
Coniophanes piceivittis LC 1 3 3 7<br />
Coniophanes quinquevittatus LC 4 6 3 13<br />
Coniophanes sarae* DD 5 7 3 16<br />
Coniophanes schmidti LC 4 6 3 13<br />
Coniophanes taylori* NE 5 7 4 16<br />
Cryophis hallbergi* DD 5 7 2 14<br />
Diadophis punctatus LC 1 1 2 4<br />
Dipsas brevifacies LC 4 7 4 15<br />
Dipsas gaigeae* LC 5 8 4 17<br />
Enulius flavitorques NE 1 1 3 5<br />
Enulius oligostichus* DD 5 7 3 15<br />
Geophis anocularis* LC 6 8 2 16<br />
Geophis bicolor* DD 5 8 2 15<br />
Geophis blanchardi* DD 5 8 2 15<br />
Geophis cancellatus LC 4 6 2 12<br />
Geophis carinosus LC 2 4 2 8<br />
Geophis chalybeus* DD 6 7 2 15<br />
Geophis dubius* LC 5 6 2 13<br />
Geophis duellmani* LC 5 8 2 15<br />
Geophis dugesi* LC 5 6 2 13<br />
Geophis immaculatus LC 4 8 2 14<br />
Geophis incomptus* DD 6 8 2 16<br />
Geophis isthmicus* DD 6 8 2 16<br />
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Geophis juarezi* DD 6 8 2 16<br />
Geophis juliai* VU 5 6 2 13<br />
Geophis laticinctus* LC 5 4 2 11<br />
Geophis laticollaris* DD 6 8 2 16<br />
Geophis latifrontalis* DD 5 7 2 14<br />
Geophis maculiferus* DD 6 8 2 16<br />
Geophis mutitorques* LC 5 6 2 13<br />
Geophis nasalis LC 4 3 2 9<br />
Geophis nigrocinctus* DD 5 8 2 15<br />
Geophis occabus* NE 3 6 8 2 16<br />
Geophis omiltemanus* LC 5 8 2 15<br />
Geophis petersi* DD 5 8 2 15<br />
Geophis pyburni* DD 6 8 2 16<br />
Geophis rhodogaster LC 3 7 2 12<br />
Geophis russatus* DD 6 8 2 16<br />
Geophis sallei* DD 6 7 2 15<br />
Geophis semidoliatus* LC 5 6 2 13<br />
Geophis sieboldi* DD 5 6 2 13<br />
Geophis tarascae* DD 5 8 2 15<br />
Heterodon kennerlyi NE 3 4 4 11<br />
Hypsiglena affinis* NE 5 7 2 14<br />
Hypsiglena chlorophaea NE 1 5 2 8<br />
Hypsiglena jani NE 1 3 2 6<br />
Hypsiglena ochrorhyncha NE 2 4 2 8<br />
Hypsiglena slevini* NE 5 4 2 11<br />
Hypsiglena tanzeri* DD 5 8 2 15<br />
Hypsiglena torquata* LC 5 1 2 8<br />
Imantodes cenchoa NE 1 3 2 6<br />
Imantodes gemmistratus NE 1 3 2 6<br />
Imantodes tenuissimus NE 4 7 2 13<br />
Leptodeira frenata LC 4 4 4 12<br />
Leptodeira maculata LC 2 1 4 7<br />
Leptodeira nigrofasciata LC 1 3 4 8<br />
Leptodeira punctata* LC 5 8 4 17<br />
Leptodeira septentrionalis NE 2 2 4 8<br />
Leptodeira splendida* LC 5 5 4 14<br />
Leptodeira uribei* LC 5 8 4 17<br />
Ninia diademata LC 4 3 2 9<br />
Ninia sebae NE 1 1 2 5<br />
Pliocercus elapoides LC 4 1 5 10<br />
Pseudoleptodeira latifasciata* LC 5 5 4 14<br />
Rhadinaea bogertorum* DD 6 8 2 16<br />
Rhadinaea cuneata* DD 6 7 2 15<br />
Rhadinaea decorata NE 1 6 2 9<br />
Rhadinaea forbesi* DD 5 8 2 15<br />
Rhadinaea fulvivittis* VU 5 4 2 11<br />
Rhadinaea gaigeae* DD 5 5 2 12<br />
Rhadinaea hesperia* LC 5 3 2 10<br />
Rhadinaea laureata* LC 5 5 2 12<br />
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Rhadinaea macdougalli* DD 5 5 2 12<br />
Rhadinaea marcellae* EN 5 5 2 12<br />
Rhadinaea montana* EN 5 7 2 14<br />
Rhadinaea myersi* DD 5 5 2 12<br />
Rhadinaea omiltemana* DD 5 8 2 15<br />
Rhadinaea quinquelineata* DD 5 8 2 15<br />
Rhadinaea taeniata* LC 5 6 2 13<br />
Rhadinella godmani NE 3 5 2 10<br />
Rhadinella hannsteini DD 4 5 2 11<br />
Rhadinella kanalchutchan* DD 6 8 2 16<br />
Rhadinella kinkelini LC 4 6 2 12<br />
Rhadinella lachrymans LC 4 2 2 8<br />
Rhadinella posadasi NE 4 8 2 14<br />
Rhadinella schistosa* LC 5 6 2 13<br />
Rhadinophanes monticola* DD 6 7 2 15<br />
Sibon dimidiatus LC 1 5 4 10<br />
Sibon linearis* DD 6 8 2 16<br />
Sibon nebulatus NE 1 2 2 5<br />
Sibon sanniolus LC 4 6 2 12<br />
Tantalophis discolor* VU 5 6 3 14<br />
Tropidodipsas annulifera* LC 5 4 4 13<br />
Tropidodipsas fasciata* NE 5 4 4 13<br />
Tropidodipsas fischeri NE 4 3 4 11<br />
Tropidodipsas philippi* LC 5 5 4 14<br />
Tropidodipsas repleta* DD 5 8 4 17<br />
Tropidodipsas sartorii NE 2 2 5 9<br />
Tropidodipsas zweifeli* NE 5 7 4 16<br />
Family Elapidae (19 species)<br />
Laticauda colubrina LC — — — —<br />
Micruroides euryxanthus LC 4 6 5 15<br />
Micrurus bernadi* LC 5 5 5 15<br />
Micrurus bogerti* DD 5 7 5 17<br />
Micrurus browni LC 2 1 5 8<br />
Micrurus diastema LC 2 1 5 8<br />
Micrurus distans* LC 5 4 5 14<br />
Micrurus elegans LC 4 4 5 13<br />
Micrurus ephippifer* VU 5 5 5 15<br />
Micrurus laticollaris* LC 5 4 5 14<br />
Micrurus latifasciatus LC 4 4 5 13<br />
Micrurus limbatus* LC 5 7 5 17<br />
Micrurus nebularis* DD 5 8 5 18<br />
Micrurus nigrocinctus NE 3 3 5 11<br />
Micrurus pachecogili* DD 6 7 5 18<br />
Micrurus proximans* LC 5 8 5 18<br />
Micrurus tamaulipensis* DD 6 8 5 19<br />
Micrurus tener LC 1 5 5 11<br />
Pelamis platura LC — — — —<br />
Family Leptotyphlopidae (8 species)<br />
Epictia goudotii NE 1 1 1 3<br />
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Rena boettgeri* NE 5 8 1 14<br />
Rena bressoni* DD 5 8 1 14<br />
Rena dissecta LC 4 6 1 11<br />
Rena dulcis LC 4 8 1 13<br />
Rena humilis LC 4 3 1 8<br />
Rena maxima* LC 5 5 1 11<br />
Rena myopica* LC 5 7 1 13<br />
Family Loxocemidae (1 species)<br />
Loxocemus bicolor NE 1 5 4 10<br />
Family Natricidae (33 species)<br />
Adelophis copei* VU 5 8 2 15<br />
Adelophis foxi* DD 6 8 2 16<br />
Nerodia erythrogaster LC 3 4 4 11<br />
Nerodia rhombifer LC 1 5 4 10<br />
Storeria dekayi LC 1 4 2 7<br />
Storeria hidalgoensis* VU 5 6 2 13<br />
Storeria storerioides* LC 5 4 2 11<br />
Thamnophis bogerti* NE 5 7 4 16<br />
Thamnophis chrysocephalus* LC 5 5 4 14<br />
Thamnophis conanti* NE 5 8 4 17<br />
Thamnophis cyrtopsis LC 2 1 4 7<br />
Thamnophis elegans LC 3 7 4 14<br />
Thamnophis eques LC 2 2 4 8<br />
Thamnophis errans* LC 5 7 4 16<br />
Thamnophis exsul* LC 5 7 4 16<br />
Thamnophis fulvus LC 4 5 4 13<br />
Thamnophis godmani* LC 5 5 4 14<br />
Thamnophis hammondii LC 4 5 4 13<br />
Thamnophis lineri* NE 5 8 4 17<br />
Thamnophis marcianus NE 1 5 4 10<br />
Thamnophis melanogaster* EN 5 6 4 15<br />
Thamnophis mendax* EN 5 5 4 14<br />
Thamnophis nigronuchalis* DD 5 3 4 12<br />
Thamnophis postremus* LC 5 6 4 15<br />
Thamnophis proximus NE 1 2 4 7<br />
Thamnophis pulchrilatus* LC 5 6 4 15<br />
Thamnophis rossmani* DD 6 8 4 18<br />
Thamnophis rufipunctatus LC 4 7 4 15<br />
Thamnophis scalaris* LC 5 5 4 14<br />
Thamnophis scaliger* VU 5 6 4 15<br />
Thamnophis sirtalis LC 3 7 4 14<br />
Thamnophis sumichrasti* LC 5 6 4 15<br />
Thamnophis validus* LC 5 3 4 12<br />
Family Typhlopidae (2 species)<br />
Typhlops microstomus LC 4 7 1 12<br />
Typhlops tenuis LC 4 6 1 11<br />
Family Ungaliophiidae (2 species)<br />
Exiliboa placata* VU 5 8 2 15<br />
Ungaliophis continentalis NE 3 5 2 10<br />
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Family Viperidae (59 species)<br />
Agkistrodon bilineatus NT 1 5 5 11<br />
Agkistrodon contortrix LC 3 6 5 14<br />
Agkistrodon taylori* LC 5 7 5 17<br />
Atropoides mexicanus NE 3 4 5 12<br />
Atropoides nummifer* LC 5 3 5 13<br />
Atropoides occiduus NE 4 6 5 15<br />
Atropoides olmec LC 4 6 5 15<br />
Bothriechis aurifer VU 3 6 5 14<br />
Bothriechis bicolor LC 4 5 5 14<br />
Bothriechis rowleyi* VU 5 6 5 16<br />
Bothriechis schlegelii NE 3 4 5 12<br />
Bothrops asper NE 3 4 5 12<br />
Cerrophidion godmani NE 3 3 5 11<br />
Cerrophidion petlalcalensis* DD 5 8 5 18<br />
Cerrophidion tzotzilorum* LC 6 8 5 19<br />
Crotalus angelensis* LC 6 7 5 18<br />
Crotalus aquilus* LC 5 6 5 16<br />
Crotalus atrox LC 1 3 5 9<br />
Crotalus basiliscus* LC 5 6 5 16<br />
Crotalus catalinensis* CR 6 8 5 19<br />
Crotalus cerastes LC 4 7 5 16<br />
Crotalus culminatus* NE 5 5 5 15<br />
Crotalus enyo* LC 5 3 5 13<br />
Crotalus ericsmithi* NE 5 8 5 18<br />
Crotalus estebanensis* LC 6 8 5 19<br />
Crotalus helleri NE 4 3 5 12<br />
Crotalus intermedius* LC 5 5 5 15<br />
Crotalus lannomi* DD 6 8 5 19<br />
Crotalus lepidus LC 2 5 5 12<br />
Crotalus lorenzoensis* LC 6 8 5 19<br />
Crotalus mitchellii LC 4 3 5 12<br />
Crotalus molossus LC 2 1 5 8<br />
Crotalus muertensis* LC 6 8 5 19<br />
Crotalus ornatus NE 4 4 5 13<br />
Crotalus polystictus* LC 5 6 5 16<br />
Crotalus pricei LC 2 7 5 14<br />
Crotalus pusillus* EN 5 8 5 18<br />
Crotalus ravus* LC 5 4 5 14<br />
Crotalus ruber LC 2 2 5 9<br />
Crotalus scutulatus LC 2 4 5 11<br />
Crotalus simus NE 3 2 5 10<br />
Crotalus stejnegeri* VU 5 7 5 17<br />
Crotalus tancitarensis* DD 6 8 5 19<br />
Crotalus tigris LC 4 7 5 16<br />
Crotalus totonacus* NE 5 7 5 17<br />
Crotalus transversus* LC 5 7 5 17<br />
Crotalus triseriatus* LC 5 6 5 16<br />
Crotalus tzabcan NE 4 7 5 16<br />
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Crotalus viridis LC 1 6 5 12<br />
Crotalus willardi LC 2 6 5 13<br />
Mixcoatlus barbouri* EN 5 5 5 15<br />
Mixcoatlus browni* NE 5 7 5 17<br />
Mixcoatlus melanurus* EN 5 7 5 17<br />
Ophryacus undulatus* VU 5 5 5 15<br />
Porthidium dunni* LC 5 6 5 16<br />
Porthidium hespere* DD 5 8 5 18<br />
Porthidium nasutum LC 3 6 5 14<br />
Porthidium yucatanicum* LC 5 7 5 17<br />
Sistrurus catenatus LC 3 5 5 13<br />
Family Xenodontidae (8 species)<br />
Clelia scytalina NE 4 5 4 13<br />
Conophis lineatus LC 2 3 4 9<br />
Conophis morai* DD 6 7 4 17<br />
Conophis vittatus LC 2 5 4 11<br />
Manolepis putnami* LC 5 5 3 13<br />
Oxyrhopus petolarius NE 3 6 5 14<br />
Tretanorhinus nigroluteus NE 3 5 2 10<br />
Xenodon rabdocephalus NE 3 5 5 13<br />
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Cantils (genus Agkistrodon) are some of the most feared snakes in Mesoamerica, as their bite and powerful venom have caused<br />
numerous human fatalities. Equipped with a large and strikingly-marked head, a stout body, and a nervous attitude that often is mistaken<br />
for aggression, these snakes usually are killed on sight. Cantils primarily are found in tropical forests that undergo a prolonged<br />
dry season, but occasionally inhabit savannas and areas that flood seasonally after heavy rains. Pictured here is a cantil from Parque<br />
Nacional Santa Rosa, in northwestern Costa Rica. Photo by Louis W. Porras.<br />
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Copyright: © 2013 Porras et al. This is an open-access article distributed under the terms of the Creative Commons<br />
Attribution–NonCommercial–NoDerivs 3.0 Unported License, which permits unrestricted use for non-commercial<br />
and education purposes only provided the original author and source are credited.<br />
Amphibian & Reptile Conservation 7(1): 48–73.<br />
A taxonomic reevaluation and conservation assessment of<br />
the common cantil, Agkistrodon bilineatus (Squamata:<br />
Viperidae): a race against time<br />
1<br />
Louis W. Porras, 2 Larry David Wilson, 3,4 Gordon W. Schuett,<br />
and 4 Randall S. Reiserer<br />
1<br />
7705 Wyatt Earp Avenue, Eagle Mountain, Utah, 84005, USA 2 Centro Zamorano de Biodiversidad, Escuela Agrícola Panamericana Zamorano, Francisco<br />
Morazán, HONDURAS; 16010 S.W. 207th Avenue, Miami, Florida, 33187, USA 3 Department of Biology and Center for Behavioral Neuroscience,<br />
Georgia State University, Atlanta, Georgia, 30303, USA 4 The Copperhead Institute, P.O. Box 6755, Spartanburg, South Carolina 29304, USA<br />
Abstract.—Several lines of evidence suggest that numerous populations of cantils (Agkistrodon bilineatus,<br />
A. taylori), New World pitvipers with a distribution in Mesoamerica, are in rapid decline. We<br />
examined the IUCN conservation status for A. bilineatus, assessed for the entire range of the species,<br />
as well as the Environmental Vulnerability Scores (EVS) provided for certain countries along<br />
its distribution. Because of pronounced disparities in these conservation assessments and notable<br />
phenotypic differences that coincide with the geographic distribution of certain cantil populations,<br />
we conduct a taxonomic reassessment of the common cantil, Agkistrodon bilineatus (Günther<br />
1863), to determine if the recognized subspecies of A. bilineatus merit specific status. Based on<br />
our morphological assessment, biogeographical evidence, and the results of previous DNA-based<br />
studies, we elevate the three previously recognized subspecies of A. bilineatus to full species (A.<br />
bilineatus, A. russeolus, and A. howardgloydi). Given this taxonomic reassessment, we examine the<br />
conservation status of the newly elevated taxa, suggest avenues for future studies within this complex<br />
of pitvipers, and provide conservation recommendations.<br />
Key words. Character evolution, evolutionary species, Mesoamerica, subspecies concept<br />
Resumen.—Varias líneas de evidencia sugieren que numerosas poblaciones de cantiles (Agkistrodon<br />
bilineatus, A. taylori), víboras de foseta del Nuevo Mundo con una distribución en Mesoamérica, están<br />
en rápido declive. Examinamos los resultados sobre el estado de conservación propuestos por<br />
la UICN para A. bilineatus, que fueron evaluados para la distribución total de la especie, así como<br />
los resultados de los Índices de Vulnerabilidad Ambiental (en inglés, Environmental Vulnerability<br />
Scores [EVS]) que fueron determinados para esta especie en algunos países a lo largo de su distribución.<br />
Por haber disparidades pronunciadas en estas evaluaciones de conservación y diferencias<br />
fenotípicas notables que coinciden con la distribución geográfica de ciertas poblaciones de cantiles,<br />
en este trabajo realizamos una reevaluación taxonómica del cantil común, Agkistrodon bilineatus<br />
(Günther 1863), para determinar si las subespecies reconocidas de A. bilineatus merecen el<br />
estatus de especie. Basado en nuestro análisis morfológico, evidencia biogeográfica y los resultados<br />
de anteriores estudios basados en ADN, elevamos las tres subespecies de A. bilineatus previamente<br />
reconocidas al nivel de especie (A. bilineatus, A. russeolus y A. howardgloydi). Tomando en<br />
cuenta esta nueva evaluación taxonómica, examinamos el estado de conservación de los taxones<br />
aquí elevados, hacemos sugerencias para estudios futuros dentro de este complejo de víboras de<br />
foseta y ofrecemos recomendaciones para su conservación.<br />
Palabras claves. Evolución de caracteres, especies evolutivas, Mesoamérica, concepto de subespecies<br />
Citation: Porras LW, Wilson LD, Schuett GW, Reiserer RS. 2013. A taxonomic reevaluation and conservation assessment of the common cantil,<br />
Agkistrodon bilineatus (Squamata: Viperidae): a race against time. Amphibian & Reptile Conservation 7(1): 48–73 (e63).<br />
Correspondence. Emails: 1 empub@msn.com (Corresponding author) 2 bufodoc@aol.com 3,4 gwschuett@yahoo.com<br />
4<br />
rreiserer@gmail.com<br />
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Porras et al.<br />
Although the restoration of tropical dry forest is still possible,<br />
humanity will not give the globe back to its wildland<br />
denizens, and old-growth tropical dry forest will<br />
never again cover large areas.<br />
Introduction<br />
Janzen 2004: 80.<br />
The common cantil (Agkistrodon bilineatus) is a polytypic<br />
species of North American pitviper with a variably<br />
fragmented distribution extending from extreme southwestern<br />
Chihuahua and southern Sonora, Mexico, to<br />
northwestern Costa Rica, on the Pacific versant, and parts<br />
of the Yucatan Peninsula, northern Belize, Guatemala,<br />
and extreme western Honduras on the Atlantic versant;<br />
it also occurs in Las Islas Marías, an archipelago of four<br />
islands located about 100 km west of the state of Nayarit,<br />
Mexico (Gloyd and Conant 1990; Campbell and Lamar<br />
2004; Lemos-Espinal and Smith 2007; Babb and Dugan<br />
2008; García-Grajales and Buenorostro-Silva 2011;<br />
McCranie 2011). With few exceptions, the dominant<br />
vegetation zones occupied by A. bilineatus are dry forest,<br />
deciduous forest, thorn scrub, and savanna, primarily<br />
areas of low relief that have been exploited heavily for<br />
irrigated agriculture and where this species mostly has<br />
become a rare snake; the elevational range of A. bilineatus<br />
extends from near sea level to about 1,500 m (Gloyd<br />
and Conant 1990; Conant 1992). Along the Pacific coast<br />
of Mesoamerica, tropical dry forests were reported as the<br />
most endangered of the major tropical ecosystems, with<br />
only 0.09% of that region afforded official conservation<br />
status (Janzen 1988). A quarter of a century after Janzen’s<br />
elucidative paper, aside from protected areas, dry forests<br />
throughout this region have continued to deteriorate.<br />
In a monographic study of the Agkistrodon complex,<br />
Gloyd and Conant (1990) provided an extensive review<br />
of the cantils, including information on their taxonomy,<br />
morphology, distribution, and aspects of their natural<br />
history. Based on multiple lines of evidence, Parkinson<br />
et al. (2002) conducted a phylogeographic analysis of<br />
the cantils and elevated A. b. taylori to the rank of full<br />
species, emphasizing that the loss of forested areas in<br />
the habitat of this species underscored the need for its<br />
conservation. More recently, Wilson et al. (2010) compiled<br />
an extensive conservation assessment for the entire<br />
Mesoamerican herpetofauna, in which numerous<br />
authorities provided information on the status of cantils.<br />
Although the methodological approaches of these<br />
authors varied, it was clear from the outcome that the<br />
conservation status of A. bilineatus showed dramatic<br />
differences when analyzed on a country by country or<br />
regional basis, since the reported or estimated IUCN<br />
rankings for this species extended the gamut from Least<br />
Concern to Critically Endangered (Lavin-Murcio and<br />
Lazcano 2010; Sasa et al. 2010). Some authors also<br />
provided Environmental Vulnerability Scores (EVS; a<br />
conservation measure developed and used by Wilson and<br />
McCranie 1992, 2004, and McCranie and Wilson 2002)<br />
for certain countries, and their results were more informative.<br />
This measure provides a rough gauge of the theoretical<br />
degree that herptofaunal species are vulnerable to<br />
environmental degradation; the scores at the upper end<br />
of the scale (ranging from 14 to 20) indicate a greater degree<br />
of concern (Wilson et al. 2013), and the EVS for A.<br />
bilineatus was reported as 15 for Honduras, Nicaragua,<br />
and Costa Rica, and as 16 for Belize (Sasa et al. 2010;<br />
Stafford et al. 2010; Sunyer and Köhler 2010; Townsend<br />
and Wilson 2010).<br />
Based on our field experiences, recent discussions<br />
with several colleagues working in regions where cantils<br />
occur, and information from the published literature, we<br />
echo the statements of several of the aforementioned authorities<br />
that in many regions A. bilineatus has declined<br />
significantly, largely as a result of human activities.<br />
Our principal goal in this paper is to reexamine the<br />
conservation status of A. bilineatus, inasmuch as the<br />
available information suggests that certain populations<br />
are declining or imperiled. In conservation biology the<br />
threat status of an organism typically is evaluated at the<br />
species level, so first we reevaluate the taxonomic status<br />
of the three subspecies of A. bilineatus (bilineatus, russeolus,<br />
and howardgloydi) to determine if any (or all) of<br />
them shows sufficient lineage divergence to warrant full<br />
species recognition. Accordingly, our conservation assessment<br />
develops from our taxonomic conclusions.<br />
Morphological Assessment<br />
Gloyd and Conant (1990) and Campbell and Lamar<br />
(2004) provided an extensive amount of biological information<br />
on cantils, including excellent drawings of the<br />
scalation and pattern of the relevant taxa discussed in<br />
this paper, so we relied largely on these sources for our<br />
morphological assessment. Unlike previous views (see<br />
Gloyd and Conant 1990), the genus Agkistrodon now is<br />
restricted to the New World (see Molecular Assessment).<br />
As in other pitviper genera, Agkistrodon (sensu<br />
stricto) is characterized by the presence of a deep facial<br />
pit, a vertically elliptical pupil, a large venom<br />
gland in the temporal region, and a canaliculated fang<br />
on the maxilla followed by a series of smaller replacement<br />
fangs. In Agkistrodon, however, the scales on the<br />
crown generally are large and plate-like, although often<br />
they are fragmented or contain partial sutures, and the<br />
skull is relatively broad and equipped with short fangs.<br />
Other characters include a pronounced canthus rostralis,<br />
the presence of a loreal scale in all members except<br />
A. piscivorus, a robust (or relatively robust) body, and a<br />
moderate to long tail. Scale characters such as supralabials,<br />
infralabials, and dorsal scale rows at midbody show<br />
little variation among the species, although the last of<br />
these characters is slightly higher in A. piscivorus. The<br />
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number of ventral scales is lower in A. bilineatus and A.<br />
taylori than in A. contortrix and A. piscivorus, and the<br />
number of subcaudals is slightly lower in the latter two<br />
species. In Agkistrodon, some or most of the subcaudal<br />
scales are divided, and the terminal spine on the tail tip<br />
is turned downward in all the taxa except A. piscivorus.<br />
Moderate hemipenial differences have been reported<br />
among the taxa, but the similarities are more pronounced<br />
when comparing A. contortrix and A. piscivorus to A. bilineatus<br />
and A. taylori (Gloyd and Conant 1990; Malnate<br />
1990). The tail tip of neonates and juveniles of all species<br />
of Agkistrodon is brightly colored and typically is<br />
yellow, white, or pink (Gloyd and Conant 1990). The<br />
coloration of the tail tip changes as animals mature, to a<br />
faded yellow, green, gray, black, or sometimes to match<br />
the color of the dorsum. Young individuals often use their<br />
tail to lure prey (e.g., anurans, lizards) by way of vertical<br />
undulations and waving, a behavior termed “caudal luring”<br />
(reviewed by Strimple 1988, 1992; Carpenter and<br />
Gillingham 1990).<br />
1. The cantils<br />
Commonly known as cantils, A. bilineatus and A. taylori<br />
are thick-bodied pitvipers (Serpentes: Viperidae) with a<br />
large head and a moderately long and slender tail, and<br />
their maximum total lengths are similar. As in the other<br />
species of Agkistrodon, the scale characters of cantils<br />
only show a moderately low range of variation (Table 1).<br />
A wide range of color pattern variation is evident in<br />
Agkistrodon, and these characters were used to diagnose<br />
the three subspecies of A. bilineatus (Burger and<br />
Robertson 1951; Gloyd 1972; Conant 1984), as well to<br />
elevate A. taylori to the rank of full species (Parkinson<br />
et al. 2000). The coloration of the head is distinctive, as<br />
cantils are adorned with five conspicuous pale stripes,<br />
one vertically on the front of the snout and two laterally<br />
on each side of the head. The dorsal color pattern consists<br />
of crossbands, at least in juveniles, and this character<br />
shows a notable degree of geographic and ontogenetic<br />
variation. The chin color and ventral coloration also<br />
demonstrate considerable geographic variation.<br />
2. Color and pattern characteristics of the<br />
ornate cantil<br />
Among the cantils, the color pattern of A. taylori is the<br />
most vivid (Fig.1). The lower facial stripe is broad and<br />
extends to cover the lower edge of the supralabials, the<br />
dorsal pattern is composed of pronounced black crossbands<br />
separated by gray or pale brown areas that often<br />
contain yellowish brown or orange, the chin is patterned<br />
with bold markings with wide white or yellow elements,<br />
and the venter contains dark gray or black markings<br />
Fig. 1. Adult female Agkistrodon taylori from Aldamas, Tamaulipas, Mexico. The ornate cantil often is vividly marked.<br />
Photo by Tim Burkhardt.<br />
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Table 1. Maximum total length and selected scale characters in the three subspecies of Agkistrodon bilineatus and in A. taylori.<br />
Min-max values are followed by the mean (in parentheses). Data derived from Gloyd and Conant (1990).<br />
Character A. b. bilineatus A. b. russeolus A. b. howardgloydi A. taylori<br />
Total length 1,090 mm 1,050 mm* 960 mm 960 mm<br />
Ventrals 127–143 (134.5) 131–141 (136.1) 128–135 (131.1) 127–138 (133.7)<br />
Subcaudals 52–71 (61.6) 46–62 (55.4) 54–61 (58.8) 40–56 (48.3)<br />
Supralabials 5–9 (8.1) 8–9 (8.0) 7–9 (8.0) 7–9 (8.0)<br />
Infralabials 9–13 (10.7) 8–12 (10.8) 9–12 (10.9) 9–12 (10.4)<br />
Dorsal scale rows<br />
21–25 (22.9) 23–25 (23.1) 23–25 (23.4) 21–23 (22.9)<br />
(midbody)<br />
*Specimen with an incomplete tail.<br />
arranged in a somewhat checkerboard pattern. In contrast<br />
to juveniles, adults exhibit a subdued pattern that contains<br />
brighter colors, but older individuals of both sexes<br />
tend to become melanistic, and sexual color dimorphism<br />
is present in all age classes (Burchfield 1982). The tail tip<br />
of young individuals has been reported as sulphur yellow,<br />
ivory white, or salmon pink (Burchfield 1982; Gloyd and<br />
Conant 1990); the tail tip of most young individuals,<br />
however, is sulphur yellow (LWP, GWS, pers. observ.;<br />
Fig. 2).<br />
Fig. 2. Neonate female Agkistrodon taylori born in captivity<br />
from adults collected in the state of Tamaulipas, Mexico. Sexual<br />
color pattern dimorphism is evident in all age classes, except in<br />
very old individuals that sometimes darken with age. In young<br />
males, the rhombs on the dorsum tend to form bands and the<br />
interstitial pattern is reduced. Photo by Breck Bartholomew.<br />
3. Color and pattern characteristics of the<br />
common cantil<br />
In A. b. bilineatus, both the upper and lower facial stripes<br />
are relatively broad, and the lower stripe is continuous<br />
and bordered below by dark pigment along the mouth<br />
line. From a frontal view, the vertical stripe along the<br />
rostral and mental and the lateral head stripes often meet<br />
on the tip of the snout. In adults, the dorsal ground color<br />
ranges from very dark brown to black, and if crossbands<br />
are present often they are difficult to distinguish. The<br />
dorsal pattern consists of small white spots or streaks.<br />
The chin and throat are dark brown or black with a pattern<br />
of narrow white lines or markings, and the venter is<br />
dark brown or black with pale markings. The coloration<br />
of neonates and juveniles is some shade of brown, and<br />
consists of brown or chestnut crossbands separated by a<br />
paler ground color, with the lateral edges of the crossbands<br />
flecked with white. The crossbands gradually fade<br />
with maturity, however, as the overall dorsal coloration<br />
darkens (Fig. 3). The tail tip of neonates and juveniles<br />
has been reported in numerous publications as bright yellow<br />
(e.g., Allen 1949; Gloyd and Conant 1990). Sexual<br />
color dimorphism has not been reported in any age class.<br />
In A. b. russeolus, the upper facial stripe is narrow<br />
and sometimes is intermittent posterior to the eye, and<br />
the lower stripe is broader and continuous and separated<br />
from the commissure by a band of dark pigment. From a<br />
frontal view, the vertical stripe along the rostral and mental<br />
and the two upper lateral head stripes typically meet<br />
on the tip of the snout. The dorsal ground color of adults<br />
generally is pale reddish brown, and the pattern consists<br />
of broad, deep reddish brown to brown crossbands that<br />
are separated dorsally by areas of paler coloration, and<br />
often are edged irregularly with white. The crossbands<br />
remain apparent, even in older adults. Laterally, the centers<br />
of the crossbands are paler and usually contain one<br />
or two dark spots. The pattern on the chin and throat often<br />
is reduced, with small whitish spots or lines present<br />
on a darker background. Approximately the median third<br />
of the venter lacks a pattern or contains a few markings.<br />
The coloration of a neonate (150 to 175 mm TL) collected<br />
near Mérida, Yucatán, was described from life<br />
by Howard K. Gloyd (Gloyd and Conant 1990: 83) as<br />
showing a velvety appearance, and its pattern consisted<br />
of rich chestnut-brown crossbands with rufous brown<br />
interspaces, which were edged with blackish brown and<br />
interrupted lines of white, “and the tip of the tail gray.”<br />
A neonate from Dzibilchaltún, Yucatán, showed a similar<br />
coloration except that the banding was edged intermittently<br />
only with white, and the tail tip was pale gray with<br />
faint white banding (Fig. 4). This individual was maintained<br />
in captivity and by the time it had grown to a total<br />
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Fig. 3. Young adult Agkistrodon b. bilineatus from Apatzingán, Michoacan, Mexico, at an elevation of 330 m. Adult individuals<br />
from much of the west coast of Mexico often lose the dorsal banding (see cover of this issue). Photo by Javier Alvarado.<br />
Fig. 4. Neonate Agkistrodon bilineatus russeolus from<br />
Dzibilchaltún,Yucatán, Mexico. Note the pale gray tail tip with<br />
faint white banding, and the overall dorsal color pattern.<br />
Photo by Javier Ortiz.<br />
length of ca. 400 mm, a marked transformation in color<br />
pattern had taken place (Fig. 5). With growth, the inner<br />
portion of the crossbands gradually turned the same pale<br />
color as the interspaces and the individual’s pattern developed<br />
a more fragmented appearance; the color of the<br />
tail tip also shifted to include darker gray tones (Fig. 5).<br />
Henderson (1978) reported the dorsal pattern of a preserved<br />
young individual (ca. 380 mm) from Orange Walk<br />
Town, Orange Walk District, Belize, as faintly banded,<br />
and the tail as grayish-yellow with faint narrow bands.<br />
Although Gloyd and Conant (1990: 83) reported the tail<br />
Fig. 5. Juvenile (ca. 400 mm TL) Agkistrodon bilineatus russeolus<br />
from Dzibilchaltún,Yucatán, Mexico (same individual as in<br />
Fig. 4). With growth, the inner portion of the crossbands turned<br />
the same color as the interspaces, and the snake’s pattern developed<br />
a more fragmented appearance. Photo by Javier Ortiz.<br />
tip of an individual from the same locality as “bright<br />
green,” they did not indicate the total length of the snake<br />
and an ontogenetic color shift might have occurred. The<br />
fragmentation of the banding in A. b. russeolus is apparent<br />
in the photograph of an adult collected in the outskirts<br />
of Consejo, Corozal, Belize (Fig. 6). Sexual color dimorphism<br />
has not been reported in juveniles or adults of A.<br />
b. russeolus.<br />
In A. b. howardgloydi, the upper facial stripe is narrow<br />
and the posterior part often is absent in adults, and the<br />
lower facial stripe is broader and usually divided into two<br />
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Fig. 6. Adult Agkistrodon bilineatus russeolus from the outskirts of Consejo, Corozal, Belize. Note the fragmented color pattern.<br />
Photo by Kevin Zansler, courtesy of Robert A. Thomas.<br />
Fig. 7. Adult Agkistrodon bilineatus howardgloydi from Volcán Telica, León,<br />
Nicaragua. The color pattern of individuals from this volcanic region often contains<br />
black pigment. Photo by Nony Sonati, courtesy of Javier Sunyer.<br />
components that sometimes meet at the suture between<br />
the second and third suprlabials, and below is bordered<br />
by a dark line; the lower edges of the supralabials also are<br />
pale in color. From a frontal view, of the five facial stripes<br />
only the top two generally meet on<br />
the tip of the snout, but in some<br />
individuals all five stripes are connected.<br />
The dorsal ground color of<br />
adults generally is reddish brown or<br />
brown. Adults with black pigment,<br />
however, are known from Reserva<br />
Natural Volcán Telica in northwestern<br />
Nicaragua, with a pattern consisting<br />
of darker crossbands that<br />
contrast moderately with the dorsal<br />
ground color, and along this volcanic<br />
area adults sometimes show a dark<br />
coloration (J. Sunyer, pers. comm.;<br />
Figs. 7, 8). A cantil also was sighted<br />
on the eastern shore of Laguna de<br />
Xiloá, north of Managua (R. Earley,<br />
pers. comm.). The chin and throat<br />
are orange yellow, bright orange, or<br />
brownish orange with a pattern of a<br />
few small white spots, but this coloration<br />
terminates abruptly after the<br />
first few ventrals. The venter usually<br />
is dark reddish brown. The dorsal coloration of juveniles<br />
is tan to reddish orange, or reddish, with distinguishable<br />
reddish brown crossbands that are edged intermittently<br />
with white and/or black, especially as they approach<br />
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Fig. 8. Young Agkistrodon bilineatus howardgloydi from Volcán Masaya, Masaya,<br />
Nicaragua. The color pattern of adults from this area sometimes darkens with age.<br />
Photo by Javier Sunyer.<br />
the venter. The tail tip of juveniles<br />
is banded with a sequential pattern<br />
that ranges from very dark gray anteriorly<br />
to paler gray toward the tip,<br />
with the interspaces alternating from<br />
pale gray to white (Fig. 9). Although<br />
Villa (1984: 19) indicated that in<br />
Nicaragua “the bright sulphuryellow<br />
tail of the young becomes<br />
dark in the adult,” and a photograph<br />
of a “juvenile individual” of A. b.<br />
howardgloydi with what is indicated<br />
as a “yellowish tail” appears on the<br />
frontispiece, the robust body features<br />
of the snake clearly show that it is<br />
not a juvenile and its tail is not yellow.<br />
We question, therefore, whether<br />
Villa might not have assumed that<br />
the tail color of A. b. howardgloydi<br />
would be yellow, as this information<br />
long was entrenched in literature regarding<br />
A. b. bilineatus. With regard<br />
to sexual color dimorphism, unlike<br />
the other subspecies of A. bilineatus,<br />
sub-adults and adults of A. b. howardgloydi<br />
show a moderate degree<br />
of sexual color dimorphism; in individuals<br />
from Costa Rica, females are<br />
distinctly banded and paler in overall<br />
coloration, whereas males tend to be<br />
darker, with their banding obscured<br />
(Figs. 10, 11). Metachrosis, the ability<br />
to change color at will or under<br />
external stimuli (such as light), was<br />
observed in the holotype of A. b.<br />
howardgloydi (Conant 1984). The<br />
coloration of this individual was<br />
paler at night (LWP, pers. observ.).<br />
Fig 9. Juvenile (311 mm TL) Agkistrodon bilineatus howardgloydi from Parque<br />
Nacional Santa Rosa, Guanacaste, Costa Rica. Note the color pattern of the tail tip,<br />
which anteriorly to posteriorly turns from very dark to pale gray with corresponding<br />
pale gray to white interspaces. Photo by Alejandro Solórzano.<br />
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Fig. 10. Adult female Agkistrodon bilineatus howardgloydi from Colonia Jobo de la Cruz, Guanacaste, Costa Rica. The color pattern<br />
of subadults and adults is paler in females. Photo by Louis W. Porras.<br />
Fig. 11. Adult male A. b. howardgloydi (holotype) from 0.8 kilimeters north of Mirador Cañon del Tigre, Parque Nacional Santa<br />
Rosa, Guanacaste, Costa Rica. The color pattern of subadults and adults is darker in males. Photo by Louis W. Porras.<br />
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Molecular Assessment<br />
Gloyd and Conant (1990) recognized 33 taxa (species<br />
and subspecies) in Agkistrodon (sensu lato), with a<br />
distribution in the Old World and the New World, but<br />
subsequent studies using molecular (mtDNA) methods<br />
partitioned Agkistrodon and demonstrated that the name<br />
applies to a monophyletic group of species restricted to<br />
the New World (Knight et al. 1992; Kraus et al. 1996;<br />
Parkinson et al. 1997, 2002; Parkinson 1999; Castoe and<br />
Parkinson 2006; Malhotra et al. 2010). Agkistrodon currently<br />
is viewed as containing four species, A. bilineatus,<br />
A. contortrix, A. piscivorus, and A. taylori (Parkinson et<br />
al. 2000; Campbell and Lamar 2004), although one subspecies<br />
of A. piscivorus and two of A. contortrix appear<br />
to constitute distinct species (Guiher and Burbrink 2008;<br />
Douglas et al. 2009).<br />
1. Molecular studies of cantils<br />
Parkinson et al. (2000) provided the first phylogeographic<br />
(mtDNA) analysis of cantils, and tested all of the<br />
recognized subspecies (bilineatus, howardgloydi, russeolus,<br />
and taylori). Using maximum parsimony (MP)<br />
and maximum likelihood (ML) methods, these authors<br />
recovered the clades (taylori + (bilineatus (howardgloydi<br />
+ russeolus))). Furthermore, based on additional lines<br />
of evidence (e.g., biogeography, morphology) they recommended<br />
the elevation of taylori to full species status,<br />
whereas the remaining subspecies were thought to be<br />
more recently diverged (i.e., having shallower relationships).<br />
Using other mtDNA regions (ATPase 8 and 6),<br />
and both ML and Bayesian methods of analyses, Douglas<br />
et al. (2009) corroborated the results of Knight et al.<br />
(1992) and Parkinson et al. (2000) with respect to New<br />
World Agkistrodon, including the relationships of cantils,<br />
although in their study they lacked DNA samples of A. b.<br />
russeolus.<br />
2. Current views of cantil systematics and<br />
taxonomy<br />
Despite efforts by the various aforementioned authorities,<br />
a considerable gap in our understanding of the taxonomy<br />
and phylogeography of cantils remains. We attribute<br />
this outcome largely to insufficient sampling,<br />
based on the number of specimens used in their analyses<br />
and the number of localities sampled. For example,<br />
Knight et al. (1992) included only two samples of cantils<br />
(bilineatus and taylori) and both lacked locality information,<br />
although their samples of taylori presumably<br />
were collected in Tamaulipas, Mexico (A. Knight, pers.<br />
comm.). Similarly, Parkinson et al. (2000) reported on<br />
only seven samples of cantils, of which two lacked locality<br />
data, and their respective samples of taylori (n =<br />
2) and howardgloydi (n = 2) each came from the same<br />
locality (see Parkinson et al. 2000: table 2). In testing<br />
phylogeographic hypotheses in Agkistrodon, Guiher and<br />
Burbrink (2008) and Douglas et al. (2009) used extensive<br />
sampling of A. contortrix and A. piscivorus, and both<br />
studies used cantils as an outgroup. No new localities for<br />
cantils, however, were sampled.<br />
Presently, only limited mtDNA-based sequence data<br />
(no nuclear genes have been tested) are available for a<br />
handful of specimens of cantils. No definitive molecular<br />
information exists for the nominate form, A. b. bilineatus<br />
(i.e., no study has provided precise locality information)<br />
and only one specimen of A. b. russeolus (Yucatán,<br />
Mexico) has been subjected to a DNA-based inquiry<br />
(Parkinson et al. 2000). Given the extensive range of cantils,<br />
the limited number of specimens sampled and tested<br />
thus far (Mexico: Tamaulipas [no specific locality],<br />
Yucatán, [no specific locality]; Costa Rica: Guanacaste<br />
Province, Santa Rosa) is inadequate to provide a robust<br />
view of their phylogeography. Nonetheless, despite these<br />
deficiencies, the available molecular (mtDNA) evidence<br />
suggests that the three subspecies of cantils (A. b. bilineatus,<br />
A. b. howardgloydi, and A. b. russeolus) can be<br />
diagnosed as separate evolutionary entities (per Wiley<br />
1978, 1981).<br />
Character Mapping<br />
Character mapping is a powerful analytical procedure<br />
for producing information and gaining insights into<br />
character evolution, particularly with respect to origin,<br />
direction, and frequency (Brooks and McLennan 1991;<br />
Harvey and Pagel 1991; Martins 1996; Fenwick et al.<br />
2011; Maddison and Maddison 2011). Ideally, characters<br />
(traits) should be traced onto trees constructed from an<br />
explicitly independent data set (Harvey and Pagel 1991;<br />
Maddison and Maddison 2011), such as morphological<br />
characters mapped onto trees constructed using molecules<br />
(e.g., proteins, DNA).<br />
1. Methods<br />
We conducted a character mapping analysis (CMA) of<br />
the cantils by using morphological data derived from the<br />
literature (Gloyd and Conant 1990; Campbell and Lamar<br />
2004), new information presented in this paper, and unpublished<br />
personal data on all species of Agkistrodon<br />
(sensu stricto) (see Appendix 1). All characters were<br />
coded as binary (i.e., 0, 1) or multi-state (e.g., 0, 1, 2).<br />
Non-discrete multi-state characters (e.g., color pattern)<br />
were ordered from lowest to highest values. Character<br />
polarity was established by using two congeners (A. contortrix<br />
and A. piscivorus) as outgroups. The cottonmouth<br />
(A. piscivorus) is confirmed as the sister group to cantils<br />
(Douglas et al. 2009). Ten characters were selected as<br />
potential apomorphies (shared-derived traits) and were<br />
traced onto a fully resolved tree (six taxa) based on the<br />
mtDNA-markers used in Parkinson et al. (2000) and<br />
Douglas et al. (2009). Character tracing was performed<br />
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separately for each of the 10 traits using outgroup analysis<br />
and parsimony procedures in Mesquite (Madison and<br />
Madison 2011), and then combining the individual results<br />
onto a global tree.<br />
2. Results and discussion<br />
We found 10 morphological characters (scutellation,<br />
color pattern traits) selected for the CMA useful in providing<br />
broad support for the topology of the molecular<br />
tree, as well as robust evidence for the distinctiveness of<br />
the taxa, in particular the three subspecies of A. bilineatus<br />
(Table 2). We thus assign these characters as putative<br />
synapomorphies and autapomorphies for Agkistrodon<br />
(Fig. 12). Although we had a priori knowledge of specific<br />
and unique traits used to originally diagnose each of<br />
the subspecies, the CMA presents them in a phylogenetic<br />
and temporal framework. Accordingly, we show trait<br />
evolution with respect to origin, direction, and frequency.<br />
For example, we recovered dark dorsal coloration (dark<br />
brown or black) as the putative ancestral condition of<br />
Agkistrodon (Outgroup 1), which is retained in the basalmost<br />
cantils (A. taylori and A. b. bilineatus), but evolved<br />
to reddish-brown in the sister clade A. b. howardgloydi +<br />
A. b. russeolus. These types of data can be used in CMA<br />
to test explicit hypotheses concerning adaptation, such<br />
as seeking correlations of body color to climate, habitat<br />
types, and a range of other variables (e.g., Martins 1996).<br />
Allopatry in A. bilineatus<br />
In prioritizing a list of vipers for future conservation measures,<br />
Greene and Campbell (1992: 423) considered A.<br />
bilineatus (sensu lato) a taxon of special interest because<br />
of its “highly fragmented and biogeographically interesting<br />
distribution.” Parkinson et al. (2002) also commented<br />
on the relictual nature of the distribution of cantils, and<br />
used allopatry as one of their criteria for elevating A. b.<br />
taylori to species level.<br />
As presently understood, the distribution of A. b.<br />
bilineatus extends along the Pacific coast of Mexico<br />
(including the offshore Las Islas Marías) and northern<br />
Central America, from extreme southwestern Chihuahua<br />
and southern Sonora to central El Salvador; inland in<br />
Mexico, this species has been recorded in northwestern<br />
and extreme southeastern Morelos, as well as in the<br />
Río Grijalva Valley (Central Depression; Johnson et al.<br />
2010) of Chiapas (Gloyd and Conant 1990; Campbell<br />
and Lamar 2004; Castro-Franco and Bustos Zagal 2004;<br />
Herrera et al. 2006; Lemos-Espinal and Smith 2007;<br />
García-Grajales and Buenorostro-Silva 2011). McCranie<br />
(2011) included a photograph of a cantil from extreme<br />
western Honduras (Copán, Copán). Based on that photograph,<br />
and others provided to us by the collector (R.<br />
Garrado, pers. comm.) taken after the animal had reached<br />
maturity, the color pattern characteristics of this individual<br />
are most similar to those of A. b. bilineatus (Fig. 13).<br />
Table 2. Morphological characters used in the character mapping<br />
analysis (Fig. 12). See text for details.<br />
Character State Designation<br />
Facial striping absent A0<br />
present<br />
A1<br />
Upper facial stripe absent B0<br />
variable<br />
B1<br />
broad<br />
narrow<br />
Adult coloration tan C0<br />
black/dark brown C1<br />
Adult dorsal band<br />
(same as ground color)<br />
Adult dorsal band<br />
color (when present)<br />
reddish-brown<br />
no<br />
yes<br />
brown<br />
black/dark brown<br />
multi-colored<br />
reddish-brown<br />
Throat color ground-color F0<br />
cream/white<br />
F1<br />
Juvenile to adult<br />
color ontogeny<br />
multi-colored<br />
dark<br />
brown<br />
yellow-orange<br />
slight<br />
pronounced<br />
moderate<br />
Neonate tail-tip color yellow H0<br />
gray<br />
H1<br />
Neonate tail pattern slight I0<br />
moderate<br />
I1<br />
Sexual color<br />
dimorphism<br />
pronounced<br />
absent<br />
present<br />
A photograph of what appears to be A. b. bilineatus, with<br />
a locality of Honduras, also appears in Köhler (2001: fig.<br />
264). The distribution of A. b. russeolus primarily extends<br />
along the outer part of the Yucatan Peninsula, from westcentral<br />
Campeche and the northern portion of Yucatán and<br />
Quintana Roo on the Gulf side, and in northern Belize on<br />
the Caribbean side, although isolated records are available<br />
from extreme southeastern Campeche and central<br />
Petén, Guatemala (Gloyd and Conant 1990; Campbell<br />
1998; Campbell and Lamar 2004; Köhler 2008). The<br />
southernmost population of cantil (A. b. howardgloydi)<br />
B2<br />
B3<br />
C2<br />
D0<br />
D1<br />
E0<br />
E1<br />
E2<br />
E3<br />
F2<br />
F3<br />
F4<br />
F5<br />
G0<br />
G1<br />
G2<br />
I2<br />
J0<br />
J1<br />
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Fig. 12. Character mapping analysis of morphological traits in cantils (A. b. bilineatus,<br />
A. b. howardgloydi, A. b. russeolus, and A. taylori). Outgroup 1 = A. piscivorus;<br />
Outgroup 2 = A. contortrix. See Table 2 and Appendix 1.<br />
Fig. 13. Young adult Agkistrodon b. bilineatus from La Chorcha Lodge, Copán,<br />
Honduras at an elevation of 610 m (2,000 feet). Two sighting of this species have<br />
occurred at the lodge, in 2003 and 2008. Photo by Robert Gallardo.<br />
occurs along the Pacific coast of<br />
Central America from Isla Zacate<br />
Grande, in the Golfo de Fonseca,<br />
and the adjacent mainland of southern<br />
Honduras to the southern limit<br />
of Parque Nacional Santa Rosa Park<br />
in northwestern Costa Rica (Sasa<br />
and Solórzano 1995).<br />
The taxonomic assignment of<br />
certain populations of A. bilineatus,<br />
however, remains problematical. A<br />
single individual of cantil was reported<br />
from north of Palma Sola,<br />
in central coastal Veracruz, an area<br />
disjunct from that of all other populations<br />
(Blair et al. 1997). Smith<br />
and Chiszar (2001) described the<br />
specimen as a new subspecies (A.<br />
b. lemosespinali), but Campbell and<br />
Lamar (2004: 266) indicated that<br />
this taxon “was diagnosed by several<br />
characteristics, all of which are<br />
within the normal range of variation<br />
for A. taylori or might be artifacts<br />
in a specimen preserved for more<br />
than 30 years.” After examining<br />
additional specimens of A. taylori<br />
from Hidalgo and Veracruz, however,<br />
Bryson and Mendoza-Quijano<br />
(2007) concluded that the specimen<br />
was most closely related to, if<br />
not conspecific with, A. b. bilineatus,<br />
but that it also differed from all<br />
of the subspecies of A. bilineatus<br />
in its tail length to total length ratio.<br />
Bryson and Mendoza-Quijano<br />
(2007) further commented that the<br />
presence of A. bilineatus in coastal<br />
Veracruz lends corroboration to the<br />
transcontinental dispersal hypothesis<br />
presented by Parkinson et al.<br />
(2002).<br />
Another isolated population is<br />
known from the Atlantic versant<br />
of central Guatemala, from the Río<br />
Chixoy (Negro) Valley (Campbell<br />
and Lamar 1989). Gloyd and Conant<br />
(1990) commented that two specimens<br />
from this area show similarities<br />
in color pattern to each of the<br />
three populations of A. bilineatus<br />
occurring in Central America. Until<br />
additional specimens and/or molecular<br />
data are available, however, the<br />
taxonomic status of this allopatric<br />
population is uncertain and remains<br />
for future investigation. Similarly,<br />
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the population in the Central Depression of Chiapas,<br />
Mexico, and adjacent western Guatemala merits further<br />
examination.<br />
In summary, the distribution of A. bilineatus is disjunct<br />
or fragmented throughout its extensive range, and thus<br />
we contend that three identifiable areas of its distribution<br />
are biogeographically distinct. Except for certain issues<br />
that remain unresolved (see Discussion), these regions of<br />
allopatry constitute the ranges of A. b. bilineatus, A. b.<br />
russeolus, and A. b. howardgloydi (see Distribution Map<br />
[Fig. 14] below).<br />
Our Taxonomic Position<br />
Six decades ago, Wilson and Brown (1953) discussed the<br />
recognition of subspecies in biology and were among the<br />
first to advocate, with compelling academic vigor, to halt<br />
the use of trinomials in taxonomy. Since their provocative<br />
paper was published, a flurry of literally hundreds of<br />
papers on the utility of infraspecific categories has appeared,<br />
of which many applauded the insights of Wilson<br />
and Brown (1953) and supported abandoning the recognition<br />
of subspecies (e.g., Edwards 1954; Donoghue 1985;<br />
Ball and Avise 1992; Douglas et al. 2002; Zink 2004),<br />
whereas others criticized their views as biologically short<br />
sighted (e.g., Sibley 1954; Durrant 1955; Crusz 1986;<br />
Mallet 1995). Even with the application of an integrative<br />
taxonomic approach (reviewed by Padial and de la Riva<br />
2010), a unified concept of species and consequences<br />
for solving the problems of species delimitation (see de<br />
Queiroz 2007), or a general species concept approach as<br />
presented by Hausdorf (2011), no perfect solutions are<br />
available to resolve all of the conflicting viewpoints.<br />
Nevertheless, Padial and de la Riva (2010: 748) argued<br />
that on the basis of the evolutionary species concept, “the<br />
point of separation from [a] sister lineage is what marks<br />
the origin of a species…and neither subspecies nor ‘subspeciation’<br />
are logically needed.” Importantly, this statement<br />
implies that there are no “stages of speciation,” i.e.,<br />
subspecies are not “on their way” to becoming species.<br />
We also share the opinion of Johnson et al. (2010: 327),<br />
who asserted that the species level is “the lowest evolutionary<br />
lineage segment that should be used in a formal<br />
phylogenetically based taxonomy…In this modern taxonomic<br />
hierarchy, all taxa except for subspecies are hypothesized<br />
to consist of separate evolutionary lineages,<br />
and thus subspecies should not be recognized as a formal<br />
taxonomic unit.” Moreover, today new subspecies rarely<br />
are described in most major zoological journals, although<br />
many authors retain already-recognized subspecies as a<br />
provisional measure (e.g., Oatley et al. 2011). Here, we<br />
adopt the position on subspecies outlined by Wilson and<br />
Brown (1953) and subsequently supported by hundreds<br />
of biologists (reviewed by Burbrink et al. 2000; Douglas<br />
et al. 2002; Johnson et al. 2010).<br />
Taxonomic Conclusions<br />
The taxonomic overview and analysis we provide for<br />
the three putative subspecies of the common cantil (A.<br />
b. bilineatus, A. b. russeolus, and A. b. howardgloydi)<br />
substantiates that sufficient morphological (color and<br />
pattern), molecular (mtDNA), and ecological (biogeographical)<br />
data are available to consider these taxa as<br />
separate and diagnosable entities with their own evolutionary<br />
trajectories (see Wiley 1981; Wiley and Mayden<br />
2000; Douglas et al. 2002). As we view it necessary to<br />
adopt and identify a species concept (Padial and de la<br />
Riva 2010), we used the evolutionary species concept<br />
(ESC) introduced by Wiley (1978, 1981). We agree with<br />
others that the ESC is preferred among the species hypotheses,<br />
since it best accommodates both morphological<br />
and molecular information (Wiley and Mayden 2000;<br />
Schwentner et al. 2011).<br />
Accordingly, we elevate the three subspecies of A.<br />
bilineatus to full species and suggest the following common<br />
names: Agkistrodon bilineatus (common cantil),<br />
A. russeolus (Yucatecan cantil), and A. howardgloydi<br />
(southern cantil). We indicate the reported localities for<br />
all the cantils, including A. taylori, in a distribution map<br />
(Fig. 14).<br />
Conservation Assessment<br />
Up to 2006, the conservation status of Agkistrodon bilineatus<br />
(sensu lato) was judged by the IUCN as Least<br />
Concern, but in 2007, presumably as a result of the reptile<br />
assessment undertaken in September 2005, in Jalisco,<br />
Mexico, the status was changed to Near Threatened<br />
(IUCN Red List website; accessed 20 February 2013).<br />
Given that we elevated each of the three subspecies of A.<br />
bilineatus to full species, we will assess their conservation<br />
status individually.<br />
1. Application of the IUCN rankings<br />
The IUCN categories for assigning conservation status<br />
are the most widely used scheme for attempting to assess<br />
the degree of extinction risk for taxa at the species<br />
level (www.iucnredlist.org). The criteria used for this<br />
assessment are stipulated in the Guidelines for Using<br />
the IUCN Red List Categories and Criteria (Version<br />
8.1; August 2010). Those with the greatest application<br />
to Mesoamerican reptile populations involve the extent<br />
of occurrence (i.e., geographic range), and at least two<br />
criteria regarding the degree of range fragmentation, the<br />
degree of decline in one of a number of distributional or<br />
populational characteristics, or the degree of fluctuations<br />
in any of these characteristics. The extent of occurrence<br />
is related to the threat categories as follows: Critically<br />
Endangered (< 100 km 2 ); Endangered (< 5,000 km 2 ); and<br />
Vulnerable (< 20,000 km 2 ).<br />
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Fig. 14. Distribution map of the reported localities for cantils, including some indicated in this paper. Green is used to designate<br />
localities from where we regard the systematic status of cantils as undetermined.<br />
Under our new taxonomic arrangement, the distribution<br />
of A. bilineatus (sensu stricto) is extended to include<br />
extreme western Honduras, in the vicinity of the city of<br />
Copán on the Caribbean versant (McCranie 2011). Thus,<br />
its extent of distribution well exceeds the 20,000 km 2<br />
that forms the upper cutoff for a Vulnerable species; it<br />
also is greater than the 250,000 km 2 indicated by García<br />
(2006) as the combined extent of the six dry forest ecoregions<br />
in Pacific coastal Mexico, in addition to its range<br />
in Central America. Given its approximate geographic<br />
distribution, it clearly lies outside of the upper size limits<br />
for any of the IUCN threat categories. In addition, this<br />
species does not appear to qualify as Near Threatened,<br />
given that “the taxon should be close to qualifying for<br />
the Vulnerable category. The estimates of population size<br />
or habitat should be close to the Vulnerable thresholds,<br />
especially when there is a high degree of uncertainty”<br />
(IUCN 2010: 63). If, however, A. bilineatus cannot be<br />
judged as Near Threatened, only three other categories<br />
are available, viz., Extinct, Least Concern, and Data<br />
Deficient. The species is not Extinct, or as we maintain<br />
in this paper not of Least Concern, and also does not classify<br />
as Data Deficient because enough information was<br />
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available for it to be judged as Near Threatened (Lee and<br />
Hammerson 2007). In light of this information, we contend<br />
that A. bilineatus (sensu stricto) should be judged<br />
as Near Threatened. A broad-scale assessment of this<br />
snake’s conservation status throughout its distribution<br />
is extremely critical, however, since much of its area of<br />
occurrence has been subjected to considerable human<br />
population growth.<br />
In Mexico, A. bilineatus primarily occurs in the<br />
coastal portion of nine states from Sonora to Chiapas, as<br />
well as in Morelos. According to information obtained<br />
from Wikipedia (www.wikipedia.org), here and elsewhere<br />
in this section, these 10 states have a combined<br />
human population of 33,432,935 (29.0% of the 2012<br />
population of Mexico). With a growth rate of 1.4% for<br />
the country (Population Reference Bureau 2010) and<br />
an estimated doubling time of 50 years, if these growth<br />
rates remain comparable the population of these states<br />
will reach 66,865,870 by the year 2063. Although these<br />
figures and projections apply to an area greater than the<br />
total range of A. bilineatus in Mexico, they signal grave<br />
concern for the survival of these populations.<br />
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The prospects for the future of A. bilineatus in<br />
Guatemala and El Salvador are equally as disturbing.<br />
Guatemala is the most rapidly growing country in Central<br />
America, with a human population 13,824,463 in 2011,<br />
a growth rate of 2.8%, and an estimated doubling time of<br />
25 years, and El Salvador already has become the most<br />
densely populated region in Mesoamerica. These statistics,<br />
therefore, portend a gloomy picture for the flora and<br />
fauna of these countries.<br />
Consequently, in light of these data, we consider A.<br />
bilineatus as Near Threatened, while conceding that future<br />
population analyses might demonstrate a threatened<br />
status.<br />
The distribution of A. russeolus is much greater<br />
than 100 km 2 (the upper cutoff point for a Critically<br />
Endangered species), but significantly less than 5,000<br />
km 2 (the upper cutoff point for an Endangered species).<br />
Thus, based on the extent of occurrence, A. russeolus<br />
should be judged as an Endangered species. According<br />
to the maps in Gloyd and Conant (1990), Lee (1996),<br />
Campbell and Lamar (2004), and Köhler (2008), A. russeolus<br />
is known from up to twelve localities, depending<br />
on the level of discrimination. Most of these localities<br />
are from the state of Yucatán, from the vicinity of<br />
Mérida, Motul, and Pisté. Given this number of locations<br />
(n = 12), A. russeolus should be assessed as Vulnerable,<br />
since the criterion for this category is ≤ 10, as opposed to<br />
Endangered, which is ≤ 5. These records are historical,<br />
however, with some dating prior to 1895 (sensu Gloyd<br />
and Conant 1990), and to our knowledge no modern survey<br />
has been undertaken to ascertain the viability of cantil<br />
populations in these regions.<br />
The human population of the three Mexican states<br />
occupying the Yucatan Peninsula, Campeche, Yucatán,<br />
and Quintana Roo, is over 4,000,000 (Population Reference<br />
Bureau 2010). Most of the historical records for<br />
A. russeolus are from the state of Yucatán, the most<br />
populous of the three with a current population of about<br />
2,000,000. Specimens assigned to A. russeolus have been<br />
reported from seasonally dry forest in northern Belize,<br />
from Corozal and northern Belize Districts (Stafford<br />
and Meyer 2000), and the savanna area of central Petén,<br />
Guatemala (Campbell 1998).<br />
Lee and Hammerson (2007) indicated that the major<br />
factor affecting the long-term viability of populations of<br />
A. bilineatus (sensu lato) is “the extreme pressure from<br />
persecution leading to population reductions of close<br />
to 30% over the last 15 to 30 years…” According to<br />
J. Lee (pers. comm.), this evaluation cannot be applied<br />
precisely to A. russeolus, but would point to a Critically<br />
Endangered status based on criterion C1, i.e., an estimate<br />
of continuing decline of at least 25% in 3 years or one<br />
generation (IUCN 2010). Lee (1996: 399) commented<br />
that, “Agkistrodon bilineatus [sensu lato] is a dangerously<br />
venomous snake that is widely feared by the native<br />
people of Yucatán. It is believed to be capable of<br />
prodigious jumps and to deliver venom both through<br />
its bite and with its tail, which is thought to act as a<br />
stinger…” Lee (1996: 416) also discussed the historical<br />
and the modern attitude toward snakes in general and A.<br />
russeolus (as A. bilineatus) in particular, in his chapter<br />
on ethnoherpetology in the Yucatan Peninsula, indicating<br />
that the cantil or uolpoch (the Mayan name) “is considered<br />
by many contemporary Maya to be the most dangerous<br />
of all Yucatecan snakes.” This attitude translates into<br />
this snake being killed on sight (J. Lee, pers. comm.).<br />
Consequently, based on the available information on the<br />
conservation status of A. russeolus, we consider this species<br />
as Endangered. A conservation assessment needs to<br />
be undertaken, however, to determine if this categorization<br />
is appropriate, or whether the category of Critically<br />
Endangered would be more applicable.<br />
Agkistrodon howardgloydi is distributed in apparently<br />
fragmented populations that extend from Isla<br />
Zacate Grande in the Golfo de Fonseca and the adjacent<br />
mainland of southern Honduras (McCranie 2011),<br />
western Nicaragua in the area west of Río Tipitapa and<br />
the northwestern shore of Lago de Nicaragua (Köhler<br />
1999, 2001), and in extreme northwestern Costa Rica<br />
from Bahía Salinas, near the Nicaraguan border, to the<br />
sectors of Santa Rosa and Guanacaste, both in Área de<br />
Conservación Guanacaste (Conant 1984; Solórzano<br />
2004). Gloyd and Conant (1990: 92) discussed additional<br />
Nicaraguan localities that would extend the distribution<br />
northeastward into the southwestern tip of Departamento<br />
Jinotega, but this record is one of several supplied to the<br />
authors by Jaime Villa. Unfortunately, these specimens<br />
were in Villa’s “personal collection that was destroyed<br />
during the earthquake and fire that devastated Managua<br />
beginning on December 23, 1972.” Like Köhler (1999,<br />
2001), we discounted these records until museum specimens<br />
are available from those areas to provide verification.<br />
The extent of this species’ range, therefore, apparently<br />
is greater than 100 km 2 but less than 5,000 km 2 ,<br />
so on the basis of its extent of occurrence it would be<br />
assessed as Endangered. With respect to the number of<br />
localities, three have been reported for Honduras, including<br />
one based on a photograph in Köhler et al. (2006),<br />
five from Nicaragua (Köhler 2001; a sight record in this<br />
paper), and five from Costa Rica (Conant 1984; Savage<br />
2002); most of these localities in Costa Rica, however, fall<br />
within Parque Nacional Santa Rosa, so their total number<br />
could be considered as few as two. Thus the total number<br />
of localities would range from 10 to 13, which technically<br />
would place this species in the Near Threatened category,<br />
but again historical records (Nicaragua) date back<br />
to 1871 (Gloyd and Conant 1990). As a consequence, this<br />
species would appear to fall in the Vulnerable category.<br />
Furthermore, given the localized distribution of A. howardgloydi<br />
in Costa Rica, it is noteworthy that this species<br />
was not reported from the country until 1970 (Bolaños<br />
and Montero 1970).<br />
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Agkistrodon howardgloydi occurs in disjunct populations<br />
in Honduras, Nicaragua, and Costa Rica, in lowland<br />
dry forest––the most endangered of the major forest<br />
types in Mesoamerica (Janzen 2004). In Honduras,<br />
nearly all of this forest has been removed from the Pacific<br />
coastal plain. A telling feature in McCranie (2011: table<br />
22) is that of the protected areas in Honduras currently<br />
supporting “some good forest,” not one contains lowland<br />
dry forest. Based on figures from 2001, the departments<br />
of Choluteca and Valle each rank among the top five in<br />
human population density in the country. As noted by<br />
Solórzano et al. (1999), M. Sasa was unsuccessful in<br />
finding this species at several localities in the Golfo de<br />
Fonseca and indicated that most of the locals were unaware<br />
of its existence. These disturbing reports and observations<br />
suggest that low population densities (or local<br />
extirpation) might be the trend. Similarly, McCranie<br />
(2011) noted that professional collectors in Choluteca<br />
failed to identify this species from photographs. Also,<br />
three of us (LWP, LDW, GWS) have been unsuccessful<br />
in finding this species on Isla Zacate Grande, in the Golfo<br />
de Fonseca, and on the adjacent mainland.<br />
According to Sunyer and Köhler (2010: 494), similar<br />
population trends prevail in Nicaragua, since A. howardgloydi<br />
(as A. bilineatus) is restricted to lowland dry<br />
forest in the western part of the country, and “this formation<br />
has undergone severe human alteration.” Although<br />
A. howardgloydi apparently occurs in at least three protected<br />
areas, 75% of the protected areas in Nicaragua<br />
“contain less than 50% of their original forest cover…”<br />
(Sunyer and Köhler 2010: 505). The five known localities<br />
for this species in Nicaragua (Köhler 2001; this paper)<br />
all are from the most heavily populated region in<br />
the country, an area that likely harbored more extensive<br />
populations of this species in the past.<br />
In Costa Rica, the conservation of A. howardgloydi<br />
is more promising, as most of the restricted range of<br />
this species is located within the Área de Conservación<br />
Guanacaste. In this region, populations have been reported<br />
as “relatively stable and protected” (Solórzano<br />
2004: 622). At Parque Nacional Santa Rosa, for example,<br />
21 individuals were obtained for study from 1993<br />
to 1996 (Solórzano et al. 1999). Nonetheless, Sasa et al.<br />
(2010: table 8) indicated that although the distribution of<br />
this species has been reduced by slightly more than 20%<br />
from a potential distribution of 6,883 km 2 , only a little<br />
more than 13% of that reduced distribution (5,465 km 2 )<br />
is located within reserves. Like other venomous snakes,<br />
we can assume that this species is killed on sight in the<br />
87% of the reduced range outside of protected areas. An<br />
important factor in this species’ favor is that the human<br />
population growth rate of Costa Rica (1.2%) is the lowest<br />
in Central America, and that Guanacaste Province, which<br />
encompasses the snake’s entire range in Costa Rica, is<br />
the most sparsely populated of all the provinces.<br />
Although the population of A. howardgloydi in protected<br />
areas of Costa Rica apparently remains stable,<br />
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throughout most of the range populations have been extirpated<br />
(or are nearing extirpation). Thus, in light of the<br />
conservation prospects for A. howardgloydi, we consider<br />
this species as Endangered with the understanding that<br />
a range-wide conservation assessment is required, especially<br />
in Honduras and Nicaragua.<br />
2. Application of the EVS<br />
The conservation status algorithm known as the<br />
Environmental Vulnerability Score (EVS) was developed<br />
by Wilson and McCranie (1992) for use with amphibians<br />
in Honduras and subsequently applied to both amphibians<br />
and reptiles in this country (Wilson and McCranie<br />
2004). The EVS was utilized in a broader fashion in most<br />
of the chapters dealing with Central American countries<br />
in Wilson et al. (2010), and in all cases used at the country<br />
level. As noted in the Introduction of this paper, the EVS<br />
for A. bilineatus (sensu lato) in four Central American<br />
countries fell within the upper end of the vulnerability<br />
scale (Wilson and McCranie 2004).<br />
Originally, the EVS algorithm was constructed for<br />
use strictly within Honduras, and thus had limited utility<br />
outside of that country. For example, the scale used for<br />
Honduras was as follows:<br />
1 = widespread in and outside of Honduras<br />
2 = distribution peripheral to Honduras, but widespread<br />
elsewhere<br />
3 = distribution restricted to Nuclear Middle America<br />
(exclusive of Honduran endemics)<br />
4 = distribution restricted to Honduras<br />
5 = known only from the vicinity of the type locality<br />
In its original form, four of the five levels of this scale<br />
could not be used outside of Honduras. For the EVS to<br />
have a broader application, therefore, it required reconstruction<br />
and this recently was accomplished for Belize<br />
(Stafford et al. 2010), Nicaragua (Sunyer and Köhler<br />
2010), and Costa Rica (Sasa et al. 2010).<br />
In order to use the EVS measure independent of country<br />
divisions, it requires additional reconstruction, as<br />
follows:<br />
1 = distribution extending from North America (United<br />
States and Canada) to South America<br />
2 = distribution extending from North America to<br />
Mesoamerica or from Mesoamerica to South America<br />
3 = distribution restricted to Mesoamerica<br />
4 = distribution restricted to a single physiographic<br />
region within Mesoamerica<br />
5 = known only from the vicinity of the type locality<br />
The other components of the gauge require only minimal<br />
reconstruction. The ecological distribution component<br />
can be revised as follows:<br />
1 = occurs in eight or more formations<br />
2 = occurs in seven formations<br />
3 = occurs in six formations<br />
4 = occurs in five formations<br />
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5 = occurs in four formations<br />
6 = occurs in three formations<br />
7 = occurs in two formations<br />
8 = occurs in one formation<br />
The only modification of this component is that the first<br />
level was changed from “occurs in eight formations” to<br />
“occurs in eight or more formations” (see Wilson and<br />
McCranie 2004). This change appears acceptable, since<br />
very few species in Mesoamerica occupy more than eight<br />
formations (see Wilson and Johnson 2010: table 16).<br />
The component for the degree of human persecution<br />
in reptiles (a different measure was used for amphibians)<br />
is the same as used by Wilson and McCranie (2004), as<br />
follows:<br />
1 = fossorial, usually escape human notice<br />
2 = semifossorial, or nocturnal arboreal or aquatic,<br />
non-venomous and usually non-mimicking, sometimes<br />
escape human notice<br />
3 = terrestrial and/or arboreal or aquatic, generally ignored<br />
by humans<br />
4 = terrestrial and/or arboreal or aquatic, thought to be<br />
harmful, might be killed on sight<br />
5 = venomous species or mimics thereof, killed on<br />
sight<br />
6 = commercially or non-commercially exploited for<br />
hides and/or meat and/or eggs<br />
Based on these changes to the EVS, the calculated scores<br />
for the three species of cantils are as follows:<br />
A. bilineatus: 3 + 5 + 5 = 13<br />
A. russeolus: 4 + 6 + 5 = 15<br />
A. howardgloydi: 4 + 8 + 5 = 17<br />
Consequently, the value for A. bilineatus falls at the upper<br />
end of the medium vulnerability category, and the<br />
values for A. russeolus and A. howardgloydi fall into the<br />
high vulnerability category.<br />
In summary, the IUCN categorizations and EVS values<br />
for these three taxa are as follows: A. bilineatus (Near<br />
Threatened and 13); A. russeolus (Endangered and 15);<br />
and A. howardgloydi (Endangered and 17). Interestingly,<br />
the IUCN has assessed A. taylori as a species of Least<br />
Concern (Lavin et al. 2007), whereas the EVS for this<br />
taxon is reported as 17 (Wilson et al. 2013).<br />
Discussion<br />
We provided a substantive review of the taxonomy and<br />
conservation status of the common cantil (A. bilineatus,<br />
sensu lato). Our taxonomic assessment led us to elevate<br />
the three subspecies of A. bilineatus to full species (A.<br />
bilineatus, A. howardgloydi, and A. russeolus), based on<br />
multiple lines of evidence. Nonetheless, we are not confident<br />
that this arrangement necessarily captures the full<br />
diversity of this widely distributed group of pitvipers.<br />
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Accordingly, we identified several regions where additional<br />
sampling must be accomplished, but overall<br />
we recommend a thorough phylogeographic analysis<br />
employing morphological analyses and the use of both<br />
mtDNA and nuclear (e.g., introns, microsatellites) markers.<br />
Owing largely to the isolation of certain populations,<br />
we suspect that additional species will be discovered<br />
within this complex.<br />
The population of A. bilineatus in southern Sonora<br />
and adjacent southwestern Chihuahua, Mexico, for example,<br />
occurs in a distinctive habitat (“Sonoran-Sinaloan<br />
transition subtropical dry forest” according to the WWF<br />
[see García 2006]), the color pattern of adults differs<br />
somewhat from that of typical A. bilineatus (Fig. 15), and<br />
a moderate hiatus exists from the closest-known population<br />
to the south (49 miles [78.8 kilometers] south of<br />
Culiacán, Sinaloa, Mexico; Hardy and McDiarmid 1969;<br />
Campbell and Lamar 2004).<br />
Another example is the insular population on Las Islas<br />
Marías. On this offshore group of islands, two specimens<br />
collected in 1881 were reported from the “Tres<br />
Marías” (without naming a specific island), and one<br />
specimen from Isla María Grande was collected in 1897<br />
(Boulenger 1896; Stejneger 1899; see Zweifel 1960).<br />
Interestingly, Gloyd and Conant (1990) indicated that the<br />
cantil with the greatest total length is among these specimens,<br />
as well as the A. b. bilineatus (sensu lato) with<br />
the lowest number of subcaudals. Gloyd and Conant<br />
(1990), however, considered this latter specimen as aberrant,<br />
but commented (p. 69) that “Whether other aberrant<br />
specimens occurred on the islands probably will never<br />
be known, inasmuch as the species may now have been<br />
extirpated from the archipelago.” Casas-Andreu (1992)<br />
indicated the presence of A. bilineatus on other islands<br />
of the Las Islas Marías chain (on Isla San Juanito and<br />
Isla María Magdalena). According to G. Casas-Andreu<br />
(pers. comm.), however, these records were not based<br />
on new material, as no cantils were encountered during<br />
his survey in 1986, but rather they were obtained<br />
from the literature. Inasmuch as no literature citations or<br />
museum numbers for these specimens appear in Casas-<br />
Andreu (1992), our knowledge of the distribution of A.<br />
bilineatus on Las Islas Marías remains sketchy. Although<br />
some areas of “good habitat” were present in the archipelago<br />
in 1986 (G. Casas-Andreu, pers. comm.), habitat<br />
destruction, a growing human population (including a<br />
large penal colony), the presence of agricultural camps<br />
and domestic animals, the outright killing of fauna, and<br />
the introduction of rats and feral cats all had become a<br />
significant problem (Casas-Andreu 1992). In 2000, the<br />
archipelago and its surrounding waters were declared an<br />
international protected area (Reserva de la Biósfera Islas<br />
Marías). In spite of the lack of information on A. bilineatus<br />
from these islands, the only reptiles protected under<br />
the Secretaría del Medio Ambiente y Recursos Naturales<br />
(SEMARNAT) are Crocodylus acutus (special protection),<br />
Iguana iguana (special protection), Ctenosaura<br />
June 2013 | Volume 7 | Number 1 | e63
pectinata (threatened), and Eretmochelys imbricata (in<br />
danger of extinction) (Anonymous 2007). A determination<br />
of the actual distribution and population status of A.<br />
bilineatus on Las Islas Marías, therefore, is a conservation<br />
priority.<br />
The taxonomic status of A. b. lemosespinali, which<br />
tentatively was assigned to A. b. bilineatus by Bryson<br />
and Mendoza-Quijano (2007), remains unresolved.<br />
Known from a single specimen from Palma Sola, in<br />
coastal central Veracruz, Mexico, this area was noted<br />
Porras et al.<br />
Fig. 15. Adult Agkistrodon bilineatus found by Larry Jones and Thomas Skinner in<br />
August of 2005, ca. 12 km NW of Alamos, Sonora, Mexico. This individual later was<br />
released. Photo by James C. Rorabaugh.<br />
Fig. 16. Young cantil from Aldea La Laguna, Nentón, Huehuetenango, Guatemala.<br />
The specific allocation of this population remains uncertain (see Fig. 14).<br />
Photo by Manuel Acevedo.<br />
by Smith and Chizar (2001: 133) as<br />
highly agricultural and located next<br />
to a nuclear power plant regarded by<br />
“many local residents and environmentalists<br />
in general as having contaminated<br />
the surrounding area with<br />
radioactivity.” These authors further<br />
indicated that if “A. b. lemosespinali<br />
ever occurred in that area, it is likely<br />
now to be extinct, or it likely would<br />
have been found [again] long ago.”<br />
Other disjunct populations of<br />
cantils merit a closer examination<br />
at both morphological and molecular<br />
levels, such as those from the<br />
Central Depression of Chiapas and<br />
the headwaters of the Río Grijalva<br />
that extend into northwestern<br />
Guatemala (Fig. 16), the Río Chixoy<br />
and Motagua valleys of Guatemala,<br />
as well as isolated populations of<br />
A. russeolus (Gloyd and Conant<br />
1990; Campbell and Lamar 2004;<br />
McCranie 2011).<br />
Assigning protected areas for the<br />
conservation of cantil populations is<br />
not simply a matter of determining<br />
regions that exist within the range<br />
of the three species, as these have<br />
been shown to vary in their level of<br />
protection. Jaramillo et al. (2010:<br />
650) presented a model that could<br />
be used to analyze systems of protected<br />
areas in Mesoamerica, and<br />
based on six requisites concluded<br />
that the system of protected areas<br />
in Panama is impressive due to the<br />
number of areas included and their<br />
collective territory; a detailed examination<br />
of the features, however,<br />
demonstrated that all but one of the<br />
97 areas failed, to some degree, “in<br />
meeting the necessary requirements<br />
for the long-term protection of its<br />
biotic resources.” In Honduras,<br />
McCranie (2011) indicated that, “at<br />
first glance, Honduras appears to have in place a robust<br />
system of protected areas, especially when compared to<br />
nearby countries. However, most of those areas exist on<br />
paper only.” Similarly, Acevedo et al. (2010) stated that,<br />
“the existing system of protected areas in Guatemala is<br />
insufficient to protect the country’s herpetofauna, because<br />
most of the legally designated areas must be considered<br />
as ‘paper parks’.” Essentially the same story can<br />
be told about systems of protected areas in other countries<br />
where cantils occur (see various chapters in Wilson<br />
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Taxonomy and conservation of the common cantil<br />
et al. 2010), an unfortunate aspect of reality in ongoing<br />
efforts to conserve biodiversity.<br />
Unfortunately, because of the continuing destruction<br />
of natural habitats and the potential for the extirpation of<br />
cantil populations, the answers to some of the aforementioned<br />
questions are on the brink of being lost forever, if<br />
not lost already. This problem is critical, and we view it<br />
as a race against time to generate the necessary information<br />
that could help set aside protected areas to conserve<br />
disjunct and relictual populations of cantils for posterity.<br />
Conservation Recommendations<br />
Our recommendations for the long-term conservation of<br />
A. bilineatus, A. howardgloydi, A. russeolus, and A. taylori<br />
are as follows:<br />
1. In light of the paucity of information regarding the<br />
relative health of populations of these species, it will<br />
be essential to undertake population assessments for<br />
all the cantils at or near localities where they have<br />
been recorded, most critically for A. howardgloydi<br />
and A. russeolus because of their relatively limited<br />
geographic ranges.<br />
2. Once these surveys are completed, a conservation<br />
management plan should be developed to ascertain<br />
if populations of all four species are located within<br />
established protected areas, or if new areas should<br />
be considered. Such a plan is critical to the survival<br />
of cantils, especially since outside of protected areas<br />
these snakes generally are killed on sight or otherwise<br />
threatened by persistent habitat destruction or<br />
degradation.<br />
3. Inasmuch as not all protected areas can be expected to<br />
provide adequate levels of protection to support viable<br />
populations of cantils, long-term population monitoring<br />
will be essential.<br />
4. Given the elevation of these taxa to full species,<br />
conservation agencies can now use these vipers as<br />
“flagship species” in efforts to publicize conservation<br />
efforts in their respective countries at all levels<br />
of interest and concern, including education and<br />
ecotourism.<br />
5. We recommend the establishment of zoo conservation<br />
(e.g., AZA) and outreach programs, such as those<br />
currently in progress for the venomous Guatemalan<br />
beaded lizard (e.g., www.ircf.org; see Domínguez-<br />
Vega et al. 2012) and a wide variety of highly endangered<br />
anuran species (e.g., www.zooatlanta.org).<br />
Captive assurance colonies might help maximize future<br />
options for the recovery of wild populations.<br />
6. One major conclusion of this paper is that our knowledge<br />
of the taxonomy and phylogeography of cantils<br />
remains at an elementary level. Thus, as conservation<br />
assessments proceed, it will be important to obtain tissue<br />
samples from a sufficiently broad array of populations<br />
to allow for more robust molecular analyses.<br />
Similarly, we need more detailed morphological assessments<br />
and more sophisticated levels of analyses,<br />
such as geometric morphometric approaches (Davis<br />
2012).<br />
Acknowledgments.—We thank the following people<br />
for submitting or helping us obtain photographs<br />
for this paper: Manuel Acevedo, Javier Alvarado Días,<br />
Breck Bartholomew, Tim Burkhardt, Eric Dugan,<br />
Robert Gallardo (La Chorcha Lodge), Javier Ortiz,<br />
James C. Rorabaugh, Alejandro Solórzano, Ireri Suazo-<br />
Ortuño, Javier Sunyer, Robert A. Thomas, R. Wayne<br />
Van Devender, and Kevin Zansler. Additionally, Chris<br />
Mattison graciously provided a photo of Agkistrodon<br />
bilinatus for the cover of this issue. We also are grateful<br />
to the following individuals for providing regional<br />
biological information on cantils: Gustavo Casas-Andreu<br />
(Las Islas Marías), Alec Knight (Tamaulipas), Javier<br />
Ortiz (Yucatán), Julian C. Lee (Yucatan Peninsula),<br />
Manuel Acevedo (Guatemala), Ryan Earley and Javier<br />
Sunyer (Nicaragua), and Mahmood Sasa and Alejandro<br />
Solórzano (Costa Rica). For other courtesies, we appreciate<br />
the efforts and cooperation provided by Vicente<br />
Mata-Silva, Robert A. Thomas, and Josiah H. Townsend.<br />
Fran Platt assisted with image cleanup and the layout of<br />
this paper. The molecular work we discussed was made<br />
possible through the courtesy of Michael Douglas and<br />
Marlis Douglas. Several anonymous reviewers provided<br />
valuable insights that helped to improve this paper. Over<br />
the years, numerous people have accompanied one or<br />
more of the authors into the field in search of cantils,<br />
and we reminisce about the good times spent with Ed<br />
Cassano, the late Roger Conant, W. W. Lamar, James R.<br />
McCranie, John Rindfleish, Alejandro Solórzano, and<br />
Mahmood Sasa. Of these, we are especially indebted to<br />
Roger Conant, for without his encouragement and inspiration<br />
this paper might never have come to fruition.<br />
Beyond this, we wish to dedicate this paper to this remarkable<br />
man, whose influence has been so broadly felt<br />
in our own lives and among herpetologists far and wide.*<br />
*This paper is part of a special issue of Amphibian & Reptile<br />
Conservation that deals with the herpetofauna of Mexico. In addition<br />
to Dr. Conant’s seminal work on Agkistrodon (with Dr.<br />
Howard K. Gloyd), readers should be reminded that he also produced<br />
important works on this country’s Nerodia (then Natrix)<br />
and Thamnophis.<br />
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Porras et al.<br />
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Received: 18 March 2013<br />
Accepted: 24 May 2013<br />
Published: 20 June 2013<br />
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Taxonomy and conservation of the common cantil<br />
Louis W. Porras is President of Eagle Mountain Publishing, LC, a company that has published Biology of<br />
the Vipers (2002), Biology of the Boas and Pythons (2007), Amphibians, Reptiles, and Turtles in Kansas<br />
(2010), Conservation of Mesoamerican Amphibians and Reptiles (2010), and Amphibians and Reptiles of<br />
San Luis Potosí (2013). For many years Louis served as Vice-President and President of the International<br />
Herpetological Symposium, and during his tenure was instrumental (along with Gordon W. Schuett) in<br />
launching the journal Herpetological Natural History. A native of Costa Rica, Porras has authored or<br />
co-authored over 50 papers in herpetology. During the course of his studies he has traveled extensively<br />
throughout the Bahamas and Latin America. Two taxa, Sphaerodactylus nigropunctatus porrasi, from the<br />
Ragged Islands, and Porthidium porrasi, from Costa Rica, have been named in his honor.<br />
Larry David Wilson is a herpetologist with lengthy experience in Mesoamerica, totaling six collective<br />
years (combined over the past 47). Larry is the senior editor of the recently published Conservation of<br />
Mesoamerican Amphibians and Reptiles and a co-author of seven of its chapters. He retired after 35 years<br />
of service as Professor of Biology at Miami-Dade College in Miami, Florida. Larry is the author or coauthor<br />
of more than 290 peer-reviewed papers and books on herpetology, including the 2004 Amphibian &<br />
Reptile Conservation paper entitled “The conservation status of the herpetofauna of Honduras.” His other<br />
books include The Snakes of Honduras, Middle American Herpetology, The Amphibians of Honduras,<br />
Amphibians & Reptiles of the Bay Islands and Cayos Cochinos, Honduras, The Amphibians and Reptiles<br />
of the Honduran Mosquitia, and Guide to the Amphibians & Reptiles of Cusuco National Park, Honduras.<br />
He also served as the Snake Section Editor for the Catalogue of American Amphibians and Reptiles for<br />
33 years. Over his career, Larry has authored or co-authored the descriptions of 69 currently recognized<br />
herpetofaunal species and six species have been named in his honor, including the anuran Craugastor<br />
lauraster and the snakes Cerrophidion wilsoni, Myriopholis wilsoni, and Oxybelis wilsoni.<br />
Gordon W. Schuett is an evolutionary biologist and herpetologist who has conducted extensive research<br />
on reptiles. His work has focused primarily on venomous snakes, but he has also published on turtles,<br />
lizards, and amphibians. His most significant contributions to date have been studies of winner-loser effects<br />
in agonistic encounters, mate competition, mating system theory, hormone cycles and reproduction,<br />
caudal luring and mimicry, long-term sperm storage, and as co-discoverer of facultative parthenogenesis<br />
in non-avian reptiles. He served as chief editor of the peer-reviewed book Biology of the Vipers and<br />
is presently serving as chief editor of an upcoming peer-reviewed book The Rattlesnakes of Arizona<br />
(rattlesnakesofarizona.org). Gordon is a Director and scientific board member of the newly founded nonprofit<br />
The Copperhead Institute (copperheadinstitute.org). He was the founding Editor of the journal<br />
Herpetological Natural History. Dr. Schuett is an adjunct professor in the Department of Biology at<br />
Georgia State University.<br />
Randall S. Reiserer is an integrative biologist whose research focuses on understanding the interrelationships<br />
among ecology, morphology, and behavior. Within the broad framework of evolutionary biology,<br />
he studies cognition, neuroscience, mimicry, life-history evolution, and the influence of niche dynamics<br />
on patterns of evolutionary change. His primary research centers on reptiles and amphibians, but his<br />
academic interests span all major vertebrate groups. His studies of behavior are varied and range from<br />
caudal luring and thermal behavior in rattlesnakes to learning and memory in transgenic mice. His studies<br />
of caudal luring in snakes established methods for studying visual perception and stimulus control. He<br />
commonly employs phylogenetic comparative methods and statistics to investigate and test evolutionary<br />
patterns and adaptive hypotheses. Dr. Reiserer is an editor of the upcoming peer-reviewed book, The<br />
Rattlesnakes of Arizona.<br />
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Porras et al.<br />
Appendix 1. Morphological characters of the subspecies of Agkistrodon bilineatus (ingroup) and two outgroups (A. contortrix and A.piscivorus)<br />
used for character mapping analysis in this study. Unless otherwise indicated, characters are based on adult stages. *Not used in analysis.<br />
Ingroup (cantils)<br />
Agkistrodon bilineatus bilineatus<br />
Upper facial stripe (lateral view): relatively broad and white.<br />
Lower facial stripe (lateral view): relatively broad and continuous with dark pigment below; white.*<br />
Dorsal coloration of adults: very dark brown to black; crossbands usually absent; if present, difficult to distinguish;<br />
pattern composed of small white spots or streaks.<br />
Chin and throat: dark brown or black, with narrow white lines or markings.<br />
Venter: dark brown or black with pale markings.*<br />
Coloration of neonates/juveniles: some shade of brown with crossbands separated by a paler ground color; lateral<br />
edges of crossbands flecked with white.<br />
Tail tip of neonates: bright yellow.<br />
Sexual color dimorphism: absent.<br />
Agkistrodon bilineatus howardgloydi<br />
Upper facial stripe (lateral view): narrow and white; posterior portion often absent in adults.<br />
Lower facial stripe (lateral view): broader than upper stripe, and divided into two components; stripe bordered<br />
below by dark line, followed by pale pigment to lower edge of supralabials; white.*<br />
Dorsal coloration of adults: reddish brown or brown; pattern of dark crossbands contrasts moderately with dorsal<br />
ground color.<br />
Chin and throat: orange yellow, bright orange, or brownish orange with few white spots.<br />
Venter: dark reddish brown.*<br />
Coloration of neonates/juveniles: tan to reddish orange, or reddish, with reddish brown crossbands edged intermittently<br />
with white and/or black, especially as they approach venter.<br />
Tail tip of neonates/juveniles: banded with sequential pattern ranging from very dark gray anteriorly to paler gray<br />
toward the tip, with interspaces alternating from pale gray to white.<br />
Sexual color dimorphism: moderate sexual color dimorphism present in sub-adults and adults.<br />
Agkistrodon bilineatus russeolus<br />
Upper facial stripe (lateral view): narrow and white; sometimes intermittent posterior to eye.<br />
Lower facial stripe (lateral view): broader than upper stripe and continuous, with narrow band of dark pigment<br />
below; white.*<br />
Dorsal coloration of adults: pale reddish brown; broad deep reddish brown to brown crossbands separated by paler<br />
areas, and strongly edged irregularly with white; crossbands remain apparent, even in older adults; laterally, centers<br />
of crossbands paler and usually contain one or two dark spots.<br />
Chin and throat: pattern often reduced; small whitish spots or lines evident on a darker background.<br />
Venter: approximately the median third is not patterned.*<br />
Coloration of neonates/juveniles: pattern of brown crossbands with paler brown interspaces; banding intermittently<br />
edged with white; with growth, inner portion of crossbands turns same color as interspaces, thereby developing a<br />
highly fragmented pattern.<br />
Tail tip of neonates/juveniles: pale gray with faint white banding; darker gray tones evident with growth.<br />
Sexual color dimorphism: absent.<br />
Agkistrodon taylori<br />
Upper facial stripe (lateral view): relatively broad and white.<br />
Lower facial stripe (lateral view): broad and continuous, and extends to lower edge of supralabials.<br />
Dorsal coloration of adults: pronounced black crossbands separated by gray, pale brown, or lavender areas that<br />
often contain yellow-brown or orange.*<br />
Chin and throat: bold markings, with white, yellow and or orange elements.<br />
Venter: dark gray or black markings arranged in a somewhat checkerboard pattern.<br />
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Coloration of neonates/juveniles: strongly patterned, but with markings like those of adults but less intense.<br />
Tail tip of neonates/juveniles: yellow (rarely, white).<br />
Sexual color dimorphism: present in all age classes; sometimes difficult to detect in older adults that darken.<br />
Outgroups<br />
Agkistrodon piscivorus (outgroup 1)<br />
Upper facial stripe (lateral view): variable in size and appearance; pale but not white.<br />
Lower facial stripe (lateral view): relatively broad and continuous with dark pigment below.*<br />
Dorsal coloration of adults: very dark brown to black; crossbands present in some populations, difficult to distinguish;<br />
pattern composed of small white spots or streaks.<br />
Chin and throat: pale, cream to white.<br />
Venter: dark brown or black with pale markings.*<br />
Coloration of neonates/juveniles: pale ground color with pronounced bands; strong ontogenetic change<br />
Tail tip of neonates: bright yellow.<br />
Sexual color dimorphism: absent.<br />
Agkistrodon contortrix (outgroup 2)<br />
Taxonomy and conservation of the common cantil<br />
Upper facial stripe (lateral view): absent.<br />
Lower facial stripe (lateral view): absent.*<br />
Dorsal coloration of adults: light tan ground color; brown crossbands of varying size present.<br />
Chin and throat: tan; typically same as ground color of face and dorsum.<br />
Venter: pale tan with dark tan markings.*<br />
Coloration of neonates/juveniles: ground color pale tan; similar to adults but subdued.<br />
Tail tip of neonates: bright yellow.<br />
Sexual color dimorphism: absent.<br />
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Dr. Daniel D. Beck (right) with Martin Villa at the Centro Ecologia de Sonora, in Hermosillo, Mexico. Dr. Beck is holding a nearrecord<br />
length Río Fuerte beaded lizard (Heloderma horridum exasperatum). Photo by Thomas Wiewandt.<br />
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Copyright: © 2013 Reiserer et al. This is an open-access article distributed under the terms of the Creative Commons<br />
Attribution–NonCommercial–NoDerivs 3.0 Unported License, which permits unrestricted use for non-commercial<br />
and education purposes only provided the original author and source are credited.<br />
Amphibian & Reptile Conservation 7(1): 74–96.<br />
Taxonomic reassessment and conservation status<br />
of the beaded lizard, Heloderma horridum<br />
(Squamata: Helodermatidae)<br />
1<br />
Randall S. Reiserer, 1,2 Gordon W. Schuett, and 3 Daniel D. Beck<br />
1<br />
The Copperhead Institute, P. O. Box 6755, Spartanburg, South Carolina 29304, USA 2 Department of Biology and Center for Behavioral Neuroscience,<br />
Georgia State University, 33 Gilmer Street, SE, Unit 8, Atlanta, Georgia, 30303-3088, USA 3 Department of Biological Sciences, Central<br />
Washington University, Ellensburg, Washington 98926, USA<br />
Abstract.—The beaded lizard (Heloderma horridum) and Gila monster (H. suspectum) are large,<br />
highly venomous, anguimorph lizards threatened by human persecution, habitat loss and degradation,<br />
and climate change. A recent DNA-based phylogenetic analysis of helodermatids (Douglas et<br />
al. 2010. Molecular Phylogenetics and Evolution 55: 153–167) suggests that the current infraspecific<br />
taxonomy (subspecies) of beaded lizards underestimates their biodiversity, and that species status<br />
for the various subspecies is warranted. Those authors discussed “conservation phylogenetics,”<br />
which incorporates historical genetics in conservation decisions. Here, we reassess the taxonomy<br />
of beaded lizards utilizing the abovementioned molecular analysis, and incorporate morphology by<br />
performing a character mapping analysis. Furthermore, utilizing fossil-calibrated sequence divergence<br />
results, we explore beaded lizard diversification against a backdrop of the origin, diversification,<br />
and expansion of seasonally dry tropical forests (SDTFs) in Mexico and Guatemala. These forests<br />
are the primary biomes occupied by beaded lizards, and in Mesoamerica most are considered<br />
threatened, endangered, or extirpated. Pair-wise net sequence divergence (%) values were greatest<br />
between H. h. charlesbogerti and H. h. exasperatum (9.8%), and least between H. h. alvarezi and H. h.<br />
charlesbogerti (1%). The former clade represents populations that are widely separated in distribution<br />
(eastern Guatemala vs. southern Sonora, Mexico), whereas in the latter clade the populations<br />
are much closer (eastern Guatemala vs. Chiapas, Mexico). The nominate subspecies (Heloderma h.<br />
horridum) differed from the other subspecies of H. horridum at 5.4% to 7.1%. After diverging from a<br />
most-recent common ancestor ~35 mya in the Late Eocene, subsequent diversification (cladogenesis)<br />
of beaded lizards occurred during the late Miocene (9.71 mya), followed by a lengthy stasis of<br />
up to 5 my, and further cladogenesis extended into the Pliocene and Pleistocene. In both beaded<br />
lizards and SDTFs, the tempo of evolution and diversification was uneven, and their current distributions<br />
are fragmented. Based on multiple lines of evidence, including a review of the use of trinomials<br />
in taxonomy, we elevate the four subspecies of beaded lizards to full species: Heloderma alvarezi<br />
(Chiapan beaded lizard), H. charlesbogerti (Guatemalan beaded lizard), H. exasperatum Río Fuerte<br />
beaded lizard), and H. horridum (Mexican beaded lizard), with no changes in their vernacular names.<br />
Finally, we propose a series of research programs and conservation recommendations.<br />
Key words. mtDNA, ATPase, nuclear genes, character mapping, genomics, seasonally dry tropical forests, reptiles<br />
Resumen.—El escorpión (Heloderma horridum) y el monstruo de Gila (H. suspectum) son lagartijas<br />
grandes, anguimorfas, y muy venenosas que están sufriendo diversas amenazas como resultado de<br />
la persecución humana, degradación y pérdida del hábitat y el cambio climático global. Un análisis<br />
filogenético reciente basado en ADN de este grupo (Douglas et al. 2010. Molecular Phylogenetics<br />
and Evolution 55: 153–167) sugiere que la actual taxonomía intraespecífica (subespecies) del escorpión<br />
está subestimando la diversidad biológica, y el reconocimiento de especies es justificable.<br />
Estos autores discuten la utilidad del enfoque denominado “conservación filogenética”, que hace<br />
hincapié en la incorporación de la genética histórica en las decisiones de conservación. En este<br />
estudio, reevaluamos la taxonomía del escorpión utilizando el análisis molecular antes mencionado<br />
e incorporamos la morfología en un análisis de mapeo de caracteres. Así mismo, con los resultados<br />
de la secuencia de divergencia calibrada con fósiles, se explora la diversificación del escorpión en<br />
forma yuxtapuesta al origen, la diversificación y la expansión de los bosques tropicales estacionalmente<br />
secos (SDTFs) en México y Guatemala. Estos bosques son los principales biomas ocupados<br />
por los escorpiones, y en Mesoamérica la mayoria son considerados amenazados, en peligro o<br />
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Reiserer et al.<br />
biome in Mesoamerica owing to persistent deforestation<br />
for agriculture, cattle ranching, and a burgeoning<br />
human population (Janzen 1988; Myers et al. 2000; Trejo<br />
and Dirzo 2000; Hoekstra et al. 2005; Miles et al. 2006;<br />
Stoner and Sánchez-Azofeifa, 2009; Williams-Linera<br />
and Lorea 2009; Beck 2005; Pennington et al. 2006;<br />
Wilson et al. 2010, 2013; Dirzo et al. 2011; De-Nova et<br />
al. 2012; Domínguez-Vega et al. 2012; Golicher et al.<br />
2012). Furthermore, drought and fires escalate the above<br />
threats (Beck 2005; Miles et al. 2006), and recent predictive<br />
models of climate change show that the persistence<br />
of SDTFs in this region is highly dubious (Trejo and<br />
Dirzo 2000; Miles et al. 2006; Golicher et al. 2012).<br />
Despite its large size and charismatic nature, our<br />
knowledge of the ecology, geographical distribution,<br />
and status of populations of H. horridum remains limited<br />
(Beck and Lowe 1991; Beck 2005; Ariano-Sánchez<br />
2006; Douglas et al. 2010; Domiguez-Vega et al. 2012).<br />
Furthermore, based on multiple lines of evidence, a taxonomic<br />
reevaluation of this group of lizards is long overdue<br />
(Beck 2005; Douglas et al. 2010).<br />
Here, we continue the dialogue concerning the infraspecifc<br />
(subspecific) taxonomy and conservation status<br />
of beaded lizards. We reviewed recent publications by<br />
Beck (2005) and Domínguez-Vega et al. (2012), and augment<br />
their conclusions based on personal (DDB) field research<br />
in Mexico. We reassess the taxonomic status of<br />
the populations of H. horridum using morphology, biogeography,<br />
and a recent molecular-based (mtDNA,<br />
nDNA) analysis conducted by Douglas et al. (2010).<br />
Although Douglas et al. (2010) commented on the moextirpados.<br />
Los valores de la secuencia de divergencia neta por pares (%) fueron mayores entre H.<br />
h. charlesbogerti y H. h. exasperatum (9,8%) y menores entre H. h. alvarezi y H. h. charlesbogerti<br />
(1%). El primer grupo representa a poblaciones que están muy distantes una de la otra en su distribución<br />
(este de Guatemala vs. sur de Sonora, México), mientras que las poblaciones en el segundo<br />
grupo están mucho más relacionadas (este de Guatemala vs. Chiapas, México). La subespecie denominada<br />
(Heloderma h. horridum) difirió de las otras subespecies de H. horridum entre un 5,4% a<br />
7,1%. Después de la separación de un ancestro común más reciente, ~35 mda a finales del Eoceno,<br />
ocurrió una diversificación (cladogénesis) posterior de Heloderma a finales del Mioceno tardío (9,71<br />
mda), seguida de un estancamiento prolongado de hasta 5 mda, con una cladogénesis posterior<br />
que se extendió hasta el Plioceno y Pleistoceno. En ambos grupos, escorpiones y bosques tropicales<br />
estacionalmente secos, los procesos de evolución y diversificación fueron desiguales, y su<br />
distribución fue fragmentada. Hoy en día, el escorpión está distribuido de manera irregular a lo<br />
largo de su amplio rango geográfico. Basándonos en varias líneas de evidencia, incluyendo una revisión<br />
del uso de trinomios taxonómicos, elevamos las cuatro subespecies del escorpión al nivel de<br />
especie: Heloderma alvarezi (escorpión de Chiapas), H. charlesbogerti (escorpión Guatemalteco),<br />
H. exasperatum (escorpión del Río Fuerte), y H. horridum (escorpión Mexicano), sin cambios en los<br />
nombres vernáculos. Por último, proponemos una serie de programas de investigación y recomendaciones<br />
para su conservación.<br />
Palabras claves. ADNmt, ATPasas, genes nucleares, mapeo de caracteres, genómica, bosque tropical estacionalmente<br />
seco, reptiles<br />
Citation: Reiserer RS, Schuett GW, Beck DD. 2013. Taxonomic reassessment and conservation status of the beaded lizard, Heloderma horridum<br />
(Squamata: Helodermatidae). Amphibian & Reptile Conservation 7(1): 74–96 (e67).<br />
The century-long debate over the meaning and utility of<br />
the subspecies concept has produced spirited print but<br />
only superficial consensus. I suggest that genuine consensus<br />
about subspecies is an impossible goal ... the subspecies<br />
concept itself is simply too heterogeneous to be<br />
classified as strict science.<br />
Introduction<br />
Fitzpatrick 2010: 54.<br />
The beaded lizard (Heloderma horridum) is a large, highly<br />
venomous, anguimorph (Helodermatidae) squamate<br />
with a fragmented distribution in Mesoamerica that extends<br />
from northwestern Mexico (Sonora, Chihuahua) to<br />
eastern Guatemala (Bogert and Martín del Campo 1956;<br />
Campbell and Vannini 1988; Campbell and Lamar 2004;<br />
Beck 2005; Beaman et al. 2006; Anzueto and Campbell<br />
2010; Wilson et al. 2010, 2013; Domínguez-Vega et<br />
al. 2012). Among the reptilian fauna of this region, the<br />
beaded lizard (in Spanish, known as the “escorpión”) is<br />
well known to local inhabitants, yet its natural history<br />
is surrounded by mystery, notoriety and misconception.<br />
Consequently, it is frequently slaughtered when encountered<br />
(Beck 2005).<br />
Adding to this anthropogenic pressure, beaded lizard<br />
populations, with rare exceptions (Lemos-Espinal et al.<br />
2003; Monroy-Vilchis et al. 2005), occur primarily in<br />
seasonally dry tropical forests, SDTFs (Campbell and<br />
Lamar 2004; Beck 2005; Campbell and Vannini 1988;<br />
Domínguez-Vega et al. 2012), the most endangered<br />
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lecular diversity of Heloderma, especially in H. horridum,<br />
they did not provide explicit taxonomic changes.<br />
In this paper, therefore, we reevaluate and expand upon<br />
their conclusions. To gain insights into phenotypic (morphological)<br />
evolution of extant Heloderma, with emphasis<br />
on H. horridum, we conduct a character mapping<br />
analysis (Brooks and McLennan 1991; Harvey and Pagel<br />
1991; Martins 1996; Maddison and Maddison 2011), utilizing<br />
the phylogenetic information (trees) recovered by<br />
Douglas et al. (2010).<br />
Overview of Morphology and Molecules<br />
in the genus Heloderma<br />
1. Morphological assessment<br />
Published over half a century ago, Bogert and Martín del<br />
Campo’s (1956) detailed and expansive monograph of<br />
extant and fossil helodermatid lizards remains the definitive<br />
morphological reference (reviewed in Campbell and<br />
Lamar, 2004; Beck, 2005), and it contains the diagnoses<br />
and descriptions of two new subspecies (Heloderma<br />
horridum alvarezi and H. h. exasperatum). Thirty-two<br />
years later, Campbell and Vannini (1988) described a<br />
new subspecies (H. h. charlesbogerti), from the Río Motagua<br />
Valley in eastern Guatemala, in honor of Charles<br />
Bogert’s pioneering work on these lizards. With few exceptions,<br />
such as Conrad et al. (2010) and Gauthier et al.<br />
(2012), who examined higher-level relationships of the<br />
Helodermatidae and other anguimorphs, a modern phylogeographic<br />
analysis of morphological diversity for extant<br />
helodermatids is lacking. However, as we illustrate<br />
in our character mapping analysis, the morphological<br />
characters used by Bogert and Martín del Campo (1956)<br />
in diagnosing and describing the subspecies of beaded<br />
lizards, though somewhat incomplete, remains useful in<br />
analyzing phenotypic variation.<br />
2. Diagnosis, description, and distribution<br />
of Heloderma horridum<br />
Diagnosis and description. —Bogert and Martín del<br />
Campo (1956) and Campbell and Vannini (1988) provided<br />
diagnoses and descriptions of the subspecies of<br />
Heloderma horridum. Recent information on the biology,<br />
systematics, and taxonomy of H. horridum and H.<br />
suspectum is summarized and critiqued by Campbell and<br />
Lamar (2004) and Beck (2005), and Beaman et al. (2006)<br />
provided a literature reference summary of the Helodermatidae.<br />
Presently, four subspecies of H. horridum are<br />
recognized (Figs. 1–5).<br />
Mexican beaded lizard: H. h. horridum (Wiegmann<br />
1829)<br />
Río Fuerte beaded lizard: H. h. exasperatum Bogert<br />
and Martín del Campo 1956<br />
Chiapan beaded lizard: H. h. alvarezi Bogert and Martín<br />
del Campo 1956<br />
Guatemalan beaded lizard: H. h. charlesbogerti<br />
Campbell and Vannini 1988<br />
The four subspecies of H. horridum were diagnosed<br />
and described on the basis of scutellation, color pattern,<br />
and geographical distribution, and we refer the reader to<br />
the aforementioned works for detailed descriptions and<br />
taxonomic keys. The characters used by Bogert and Martín<br />
del Campo (1956) and Campbell and Vannini (1988)<br />
to diagnose the subspecies have been reevaluated as to<br />
their stability, albeit informally (Campbell and Lamar<br />
2004; Beck 2005). Poe and Wiens (2000) and Douglas<br />
et al. (2007) discussed the problem of character stability<br />
in phylogenetic analyses. Kraus (1988), for example,<br />
commented that reasonable evidence for character stability,<br />
and thus its usefulness as a shared-derived character<br />
(apomorphy), was the occurrence of a discrete trait in<br />
adults at a frequency of 80% or greater. In our character<br />
mapping analysis using published morphological characters<br />
(discussed below), character stability was a major<br />
assumption. Consequently, further research is warranted<br />
for substantiation.<br />
Geographic distribution. —The geographic distribution<br />
of Heloderma horridum extends from southern Sonora<br />
and adjacent western Chihuahua, in Mexico, southward<br />
to eastern and southern Guatemala (Campbell and<br />
Lamar 2004; Beck 2005; Anzueto and Campbell 2010;<br />
Domiguez-Vega et al. 2012).<br />
The Río Fuerte Beaded Lizard (H. h. exasperatum) inhabits<br />
the foothills of the Sierra Madre Occidental, within<br />
the drainage basins of the Río Mayo and Río Fuerte of<br />
the Sonoran-Sinaloan transition subtropical dry forest in<br />
southern Sonora, extreme western Chihuahua, and northern<br />
Sinaloa (Campbell and Lamar 2004; Beck 2005). Its<br />
distribution closely matches the fingers of SDTFs within<br />
this region, but it has also been encountered in pine-oak<br />
forest at 1,400 m near Alamos, Sonora (Schwalbe and<br />
Lowe 2000). Bogert and Martín del Campo (1956) commented<br />
that as far as their records indicated, a considerable<br />
hiatus existed between the distribution of H. h. exasperatum<br />
(to the north) and H. h. horridum (to the south),<br />
but owing to the narrow contact between the supranasal<br />
and postnasal in H. h. horridum from Sinaloa, intergradation<br />
might be found in populations north of Mazatlán.<br />
Based on this information, Beck (2005: 24) stated, “…in<br />
tropical dry forest habitats north of Mazatlan, Sinaloa, H.<br />
h. exasperatum likely intergrades with H. h. horridum.”<br />
Definitive data on intergradation remains unreported,<br />
however, and published distribution maps have incorporated<br />
that assumption (e.g., Campbell and Lamar 2004;<br />
Beck 2005). Campbell and Lamar (2004, p. 104) show<br />
a single example of H. suspectum from El Dorado in<br />
west-central Sinaloa, Mexico (deposited in the American<br />
Museum of Natural History [90786]), a locality 280 km<br />
south from northern records in Río del Fuerte, Sinaloa.<br />
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Fig. 1. A. Adult Río Fuerte beaded lizard (Heloderma horridum exasperatum) in a defensive display (Alamos, Sonora). B. Adult<br />
Río Fuerte beaded lizard raiding a bird nest (Alamos, Sonora). Photos by Thomas Wiewandt.<br />
Fig. 2. Adult Mexican beaded lizard (H. h. horridum) observed on 11 July 2011 at Emiliano Zapata, municipality of La Huerta,<br />
coastal Jalisco, Mexico. Photo by Javier Alvarado.<br />
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Fig. 3. Adult Chiapan beaded lizard (Heloderma horridum alvarezi) from Sumidero Canyon in the Río Grijalva Valley, east of<br />
Tuxtla Gutiérrez, Chiapas, Mexico. Photo by Thomas Wiewandt.<br />
Fig. 4. Adult Guatemalan beaded lizard (Heloderma horridum charlesbogerti) from the Motagua Valley, Guatemala.<br />
Photo by Daniel Ariano-Sánchez.<br />
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A<br />
C<br />
Fig. 5. A. Juvenile Heloderma horridum exasperatum (in situ,<br />
Álamos, Sonora, Mexico). Photo by Stephanie Meyer.<br />
B. Neonate Heloderma h. horridum (wild-collected July 2011,<br />
Chamela, Jalisco). Photo by Kerry Holcomb.<br />
C. Neonate Heloderma horridum alvarezi (Río Lagartero<br />
Depression, extreme western Guatemala).<br />
Photo by Quetzal Dwyer.<br />
D. Neonate Heloderma horridum charlesbogerti (hatched at<br />
Zoo Atlanta in late 2012). Photo by David Brothers, courtesy<br />
of Zoo Atlanta.<br />
D<br />
B<br />
Owing to this unusual location, we suggest a re-examination<br />
of this museum specimen to verify its identity. Neonates<br />
and juveniles of H. h. exasperatum resemble adults<br />
in color pattern (Fig. 5a), but they show greater contrast<br />
(i.e., a pale yellow to nearly white pattern on a ground<br />
color of brownish-black). Also, their color pattern can be<br />
distinguished from that of adults (e.g., no yellow speckling<br />
between the tail bands), and an ontogenetic increase<br />
in yellow pigment occurs (Bogert and Martín del Campo<br />
1956; Beck 2005).<br />
The Mexican beaded lizard (H. h. horridum), the<br />
subspecies with the most extensive distribution, occurs<br />
primarily in dry forest habitats from southern Sinaloa<br />
southward to Oaxaca, including the states of Jalisco,<br />
Nayarit, Colima, Michoacán, and Guerrero, and inland<br />
into the states of México and Morelos (Campbell and<br />
Lamar 2004; Beck 2005). Monroy-Vilchis et al. (2005)<br />
recorded an observation of this taxon at mid elevations<br />
(e.g., 1861 m) in pine-oak woodlands in the state<br />
of México. Campbell and Vannini (1988), citing Álvarez<br />
del Toro (1983), indicated the probability of areas<br />
of intergradation between H. h. horridum and H. h. alvarezi,<br />
in the area between the Isthmus of Tehuantepec<br />
and Cintalapa, Chiapas. Nonetheless, Álvarez del Toro<br />
(1983) stated that individuals of beaded lizards with yellow<br />
markings (a coloration character present in H. h.<br />
horridum) are found in the region from Cintalapa to the<br />
Isthmus of Tehuantepec, as well as in dry areas along the<br />
coast from Arriaga (near the Isthmus of Tehuantepec) to<br />
Huixtla (near the Guatemalan border). Literature information<br />
on intergradation between these two subspecies<br />
is inconclusive and, therefore, will require further investigation.<br />
Neonates and juveniles of H. h. horridum, like<br />
those of H. h. exasperatum, resemble adults in color pattern<br />
(Fig. 5b), but their color contrast is greater (Bogert<br />
and Martín del Campo 1956; Beck 2005).<br />
The Chiapan beaded lizard (H. h. alvarezi) inhabits<br />
dry forests in the Central Depression (Río Grijalva<br />
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Depression) of central Chiapas and the Río Lagartero<br />
Depression in extreme western Guatemala (Campbell<br />
and Lamar 2004; Beck 2005; Johnson et al. 2010; Wilson<br />
et al. 2010: p. 435). This taxon is unique among the<br />
subspecies in that it undergoes an ontogenetic increase<br />
in melanism, whereby it tends to lose the juvenile color<br />
pattern (Bogert and Martín del Campo 1956; Beck 2005).<br />
Neonates and juveniles often are distinctly marked with<br />
yellow spots and bands, including on the tail (Fig. 5c),<br />
whereas the color pattern of adults gradually transforms<br />
to an almost uniform dark brown or gray. Black individuals,<br />
however, are uncommon. Yellow banding on the tail,<br />
a characteristic typical of the other subspecies of beaded<br />
lizards, (Fig. 2), is essentially absent in adults (Bogert<br />
and Martín del Campo 1956; Beck 2005).<br />
The Guatemalan beaded lizard (H. h. charlesbogerti)<br />
inhabits the Río Motagua Valley, in the Atlantic versant<br />
of eastern Guatemala (Campbell and Vannini 1988). Recently,<br />
however, Anzueto and Campbell (2010) reported<br />
three specimens from two disjunct populations on the<br />
Pacific versant of Guatemala, to the southwest of the<br />
Motagua Valley. Neonates resemble adults in color pattern,<br />
though they tend to be paler (Fig. 5d).<br />
In summary, the distribution of H. horridum is fragmented<br />
throughout its extensive range and corresponds<br />
closely with the patchy distribution of SDTFs in Mexico<br />
and Guatemala (Beck 2005; Miles et al. 2006; Domínguez-Vega<br />
et al. 2012). The distribution of the Guatemalan<br />
beaded lizard (H. h. charlesbogerti) is distinctly<br />
allopatric (Campbell and Vannini 1988; Beck 2005;<br />
Ariano-Sánchez 2006; Anzueto and Campbell 2010).<br />
3. Molecular assessment<br />
Douglas et al. (2010) provided the first detailed molecular-based<br />
(mtDNA, nDNA) analysis of the phylogeographic<br />
diversity of helodermatid lizards, which is available<br />
at www.cnah.org/cnah_pdf.asp. Two authors (GWS,<br />
DDB) of this paper were co-authors. Specifically, Douglas<br />
et al. (2010) used a “conservation phylogenetics”<br />
approach (Avise 2005, 2008; Avise et al. 2008), which<br />
combines and emphasizes the principles and approaches<br />
of genetics and phylogeography and how they can be applied<br />
to describe and interpret biodiversity.<br />
Methods. —Douglas et al. (2010) sampled 135 localityspecific<br />
individuals of Heloderma (48 H. horridum, 87 H.<br />
suspectum) from throughout their range (their ingroup).<br />
The outgroup taxa included multiple lineages of lizards<br />
and snakes, with an emphasis on anguimorphs. Based on<br />
both morphological and DNA-based analyses, all authorities<br />
have recognized the extant helodermatid lizards as<br />
monotypic (a single genus, Heloderma), and as members<br />
of a larger monophyletic assemblage of lizards termed<br />
the Anguimorpha (Pregill et al. 1986; Estes et al. 1988;<br />
Townsend et al. 2004; Wiens et al. 2010, 2012; Gauthier<br />
et al. 2012). This lineage includes the well-known varanids<br />
(Varanus), alligator lizards and their relatives<br />
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(Anguidae), as well as such relatively obscure taxa as the<br />
Old World Lanthanotidae (Lanthanotus) and Shinisauridae<br />
(Shinisaurus), and the New World Xenosauridae (Xenosaurus).<br />
The mtDNA analyses in Douglas et al. (2010)<br />
were rooted with the tuatara (Sphenodon punctatus), and<br />
Bayesian and maximum parsimony (MP) analyses were<br />
conducted using Mr. Bayes (Hulsenbeck and Rohnquist<br />
2001).<br />
Douglas et al. (2010) used sequence data from both mitochondrial<br />
(mt) DNA and nuclear (n) DNA as molecular<br />
markers in their phylogenetic analyses. Specifically, they<br />
discussed reasons for selecting mtDNA regions ATPase<br />
8 and 6, and the nDNA introns alpha-enolase (ENOL)<br />
and ornithine decarboxylase (OD). The utility of combining<br />
mt- and nDNAs (supertree) in recovering phylogenetic<br />
signals has been discussed (Douglas et al. 2007,<br />
2010), yet each of these markers and the procedure of<br />
combining sequence data have both benefits and pitfalls<br />
(Wiens 2008; Castoe et al. 2009). Long-branch attraction<br />
and convergence, for example, can result in misleading<br />
relationships (Bergsten 2005; Wiens 2008; Castoe et al.<br />
2009). The tools for detecting and potentially correcting<br />
these problems have been discussed (e.g., Castoe et al.<br />
2009; Assis and Rieppel 2011).<br />
Results and discussion. —Douglas et al. (2010) recovered<br />
the genus Heloderma as monophyletic (Helodermatidae),<br />
with H. horridum and H. suspectum as sister<br />
taxa. In a partitioned Bayesian analysis of mtDNA, Helodermatidae<br />
was recovered as sister to the anguimorph<br />
clade (Shinisaurus (Abronia + Elgaria)), which in turn<br />
was sister to the clade Lanthanotus + Varanus. Recent<br />
molecular studies of squamates by Wiens et al. (2012, see<br />
references therein) recovered a similar topology to that<br />
of Douglas et al. (2010). However, an extensive morphological<br />
analysis by Gauthier et al. (2012) supported a traditional<br />
topology of Heloderma as sister to varanids and<br />
Lanthanotus borneensis (see Estes et al. 1986; Pregill et<br />
al. 1988). In Douglas et al. (2010), a partitioned Bayesian<br />
analysis of the nuclear marker alpha-enolase (intron 8<br />
and exon 8 and 9), however, recovered Heloderma as sister<br />
to a monophyletic Varanus. Using a combined analysis<br />
of morphology (extant and fossil data), mitochondrial,<br />
and nuclear markers, Lee (2009) recovered Varanidae as<br />
sister to the clade Helodermatidae + Anguidae. In a combined<br />
approach, Wiens et al. (2010) recovered results that<br />
were similar to those of Lee (2009). A recent DNA-based<br />
analysis of Squamata by Pyron et al. (2013) examined<br />
4151 species (lizards and snakes), and they recovered<br />
Helodermatidae as sister to the clade Anniellidae + Anguidae.<br />
Moreover, they recovered the clade Varanidae +<br />
Lanthanotidae as sister to Shinisauridae.<br />
How do systematists deal with this type of incongruity<br />
(discordance) in studies that use different types<br />
(e.g., morphology vs. molecular) of phylogenetic markers?<br />
Recently, Assis and Rieppel (2011) and Losos et al.<br />
(2012) discussed the common occurrence of discordance<br />
between molecular and morphological phylogenetic<br />
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Reiserer et al.<br />
analyses. Specifically, with respect to discordance, Assis<br />
and Rieppel (2011) stated that, “...the issue is not to<br />
simply let the molecular signal override the morphological<br />
one. The issue instead is to make empirical evidence<br />
scientific by trying to find out why such contrastive<br />
signals are obtained in the first place.” We concur with<br />
their opinions, and thus further research is warranted to<br />
resolve such conflicts in the phylogeny of anguimorph<br />
squamates.<br />
Relationships among the four subspecies of H. horridum<br />
recovered in the analysis by Douglas et al. (2010,<br />
p. 158–159, fig. 3a, b) are depicted in Fig. 6. This topology<br />
was derived from a partitioned Bayesian analysis of<br />
the mtDNA regions ATPase 8 and 6. The Gila monster<br />
(H. suspectum) was the immediate outgroup. Two sets of<br />
sister pairs of beaded lizards were recovered: H. h. exasperatum<br />
(HHE) + H. h. horridum (HHH), and H. h. alvarezi<br />
(HHA) + H. h. charlesbogerti (HHC). The current<br />
subspecific designations for H. horridum were robustly<br />
supported (concordant) by these genetic analyses. Unlike<br />
results obtained for Gila monsters (H. suspectum),<br />
haplotype and genotype data for H. horridum were both<br />
diverse and highly concordant with the designated subspecies<br />
and their respective geographic distributions.<br />
Douglas et al. (2010) generated pair-wise net sequence<br />
divergence (%) values based on their recovered relationships<br />
(Table 1, Fig. 6). The greatest divergence was between<br />
HHE and HHC (9.8%), and the least between HHA<br />
and HHC (1%). The former pair represents populations<br />
widely separated in distribution (southern Sonora, Mexico<br />
vs. eastern Guatemala), whereas the latter are much<br />
more closely distributed (Chiapas, Mexico vs. eastern<br />
Guatemala). The nominate subspecies (Heloderma h.<br />
horridum) differed from the other three subspecies of<br />
beaded lizards, from 5.4% to 7.1%.<br />
Table 1. Pair-wise net sequence divergence (%) values between<br />
the four subspecies of the beaded lizard (Heloderma horridum)<br />
derived from a partitioned Bayesian analysis of the mtDNA regions<br />
ATPase 8 and 6 (modified from Douglas et al. 2010, pp.<br />
157–159, 163; fig. 3a, b, tables 1 and 3). Values in parentheses<br />
denote evolutionary divergence times, which represent mean<br />
age. Mean age is the time in millions of years (mya) since the<br />
most-recent common ancestor (tree node) and is provided for<br />
the sister clades HHE-HHH and HHA-HHC (Fig. 6). Beaded<br />
lizards and Gila monsters (H. suspectum) are hypothesized<br />
to have diverged from a most-recent common ancestor in the<br />
late Eocene ~35 mya (Douglas et al. 2010, p. 163). Percent sequence<br />
divergence was greatest for HHC-HHE, and was lowest<br />
for HHA-HHC. See text for further details.<br />
HHA HHC HHE HHH<br />
HHA —<br />
HHC 1% (3.02) —<br />
HHE 9.3% 9.8% —<br />
HHH 5.4% 6.2% 7.1% (4.42) —<br />
HHA = H. h. alvarezi; HHC = H. h. charlesbogerti; HHE = H. h. exasperatum;<br />
HHH = H. h. horridum.<br />
Fig. 6. Character mapping analysis. Tree topology and node dates based on Douglas et al. (2010). Morphological characters (Table<br />
2) were mapped via parsimony and outgroup methods using the software program Mesquite (Maddison and Maddison 2011). Node<br />
1 = Late Eocene (~35 million years ago, mya); Node 2 = 9.71 mya; Node 3 = 4.42 mya; and Node 4 = 3.02 mya (see Table 1). See<br />
text for details of the analysis.<br />
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Table 2. Morphological characters used for the character mapping analysis (see Table 1, Fig. 6). See text for details.<br />
Character State Designation<br />
Tail length 41–55% of snout-to-vent length A0<br />
≥ 65% of snout-to-vent length<br />
A1<br />
Number of caudal vertebrae 25–28 B0<br />
40 B1<br />
Number of transverse rows of ventromedial absent C0<br />
caudal scales (vent to tail tip) greater than 62 present C1<br />
Usually one pair of enlarged preanal scales present D0<br />
absent<br />
D1<br />
First pair of infralabials usually in contact with present E0<br />
chin shields absent E1<br />
Number of maxillary teeth 8–9 F0<br />
6–7 F1<br />
Upper posterior process of splenial bone overlaps inner surface of coronoid G0<br />
does not overlap coronoid<br />
G1<br />
Number of black tail bands (including black 4–5 H0<br />
terminus on tail of juveniles) 6–7 H1<br />
Adult total length < 570 mm I0<br />
> 600 mm I1<br />
Tongue color black or nearly so J0<br />
pink<br />
J1<br />
Supranasal-postnasal association in contact K0<br />
separated by first canthal<br />
K1<br />
Association of second supralabial and in contact L0<br />
prenasal/nasal plates separated by lorilabial L1<br />
Shape of mental scute shield-shaped (elongate and triangular) M0<br />
wedge-shaped (twice as long as wide)<br />
M1<br />
Dominant adult dorsal coloration orange, pink N0<br />
black or dark brown<br />
N1<br />
yellow<br />
N2<br />
Adult dorsal yellow spotting absent O0<br />
extremely low<br />
O1<br />
low<br />
O2<br />
med<br />
O3<br />
high<br />
O4<br />
Mental scute scalloped edges absent P0<br />
moderately scalloped edges<br />
P1<br />
Enlarged preanal scutes in some females absent Q0<br />
present<br />
Q1<br />
Ontogenetic melanism absent R0<br />
present<br />
R1<br />
Spots on tail in adults absent S0<br />
present<br />
S1<br />
Bands on tail black T0<br />
yellow<br />
T1<br />
absent<br />
T2<br />
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4. Character mapping analysis<br />
A character mapping analysis (CMA) is one of several robust<br />
tools used in comparative biology to comprehend the<br />
distribution of traits (e.g., morphology), often by explicitly<br />
utilizing molecular phylogenetic information (Brooks<br />
and McLennan 1991; Harvey and Pagel 1991; Martins<br />
1996; Freeman and Herron 2004; Maddison and Maddison<br />
2011; for a critique, see Assis and Rieppel 2011).<br />
Specifically, the CMA aims to provide insights to the origin,<br />
frequency, and distribution of selected traits formally<br />
expressed onto a tree (e.g., Schuett et al. 2001, 2009; Fenwick<br />
et al. 2011). These procedures also are potentially<br />
useful in disentangling homology from homoplasy (Freeman<br />
and Herron 2004). Furthermore, the CMA provides<br />
a framework for testing hypotheses of adaptive evolution<br />
and the identification of species (Harvey and Pagel 1991;<br />
Futuyma 1998; Freeman and Herron 2004; Schuett et al.<br />
2001, 2009; Maddison and Maddison 2011). However,<br />
CMA does not replace a strict phylogenetic analysis of<br />
morphological traits (Assis and Rieppel 2011).<br />
Here, we used character mapping to investigate the<br />
morphological traits of the four subspecies of H. horridum,<br />
to gain insights on the distribution, divergence, and<br />
homology (e.g., shared-derived traits, such as possible<br />
autapomorphies) of these traits.<br />
Methods. —We used published morphological data on<br />
Heloderma (Bogert and Martín del Campo 1956; Campbell<br />
and Vannini 1988; Campbell and Lamar 2004; Beck<br />
2005) and selected 20 morphological characters for the<br />
CMA (Table 2). All characters were coded as binary (i.e.,<br />
0, 1) or multi-state (e.g., 0, 1, 2). Non-discrete multi-state<br />
characters (e.g., color pattern) were ordered from lowest<br />
to highest values. Character polarity was established<br />
by using H. suspectum as the outgroup. The CMA traced<br />
each character independently by using the outgroup analysis<br />
and parsimony procedures in Mesquite (Maddison<br />
and Maddison 2011), and we combined the individual<br />
results onto a global tree.<br />
Results and discussion. —The CMA results (Fig. 6)<br />
show that multiple morphological traits are putative apomorphies<br />
or autapomorphies (traits unique to a single<br />
taxon) for the various H. horridum clades (subspecies)<br />
delimited in the molecular tree recovered by Douglas et<br />
al. (2010). Although we had a priori knowledge of specific<br />
and unique traits (presumptive autapomorphies)<br />
used to diagnose each of the subspecies, the CMA presents<br />
them in a phylogenetic and temporal framework.<br />
Our results show trends in scutellation (e.g., presenceabsence,<br />
relative positions), relative tail length, and body<br />
color pattern, including ontogenetic melanism. Are the<br />
characters we used in the CMA stable in the subspecies?<br />
That question remains for future investigation; however,<br />
we have no evidence to the contrary. Indeed, we anticipate<br />
that these characters, and others likely to be revealed<br />
through detailed studies, will exhibit stability.<br />
Importantly, each of these traits is amenable to further<br />
investigation and formal tests. For examples, what is<br />
the evolutionary and ecological significance of tongue<br />
color differences in beaded lizards (always pink) and<br />
Gila monsters (always black), the extreme differences in<br />
adult dorsal color pattern in H. h. exasperatum (yellow<br />
is predominant) vs. H. h. alvarezi (dark brown and patternless<br />
predominate), and ontogenetic melanism in H. h.<br />
alvarezi? As we discussed, beaded lizards occupy similar<br />
seasonally dry tropical forests, yet each of the subspecies<br />
exhibits pronounced molecular and morphological<br />
differentiation.<br />
Similar types of questions concerning adaptation have<br />
used a CMA to explore social systems and sexual dimorphisms<br />
in lizards (Carothers 1984), male fighting and<br />
prey subjugation in snakes (Schuett et al. 2001), types<br />
of bipedalism in varanoids (Schuett et al. 2009), and direction<br />
of mode of parity (oviparous vs. viviparous) in<br />
viperids (Fenwick et al. 2011).<br />
Subspecies and the Taxonomy of Beaded<br />
Lizards<br />
Introduced in the late 19 th century by ornithologists to describe<br />
geographic variation in avian species, the concept<br />
of subspecies and trinomial taxonomy exploded onto the<br />
scene in the early 20 th century (Bogert et al. 1943), but<br />
not without controversy. The use of subspecies has been<br />
both exalted and condemned by biologists (see perspectives<br />
by Mallet 1995; Douglas et al. 2002; Zink 2004;<br />
Fitzpatrick 2010). Thousands of papers have been published<br />
in an attempt to either bolster the utility and promulgation<br />
of subspecies, or to denounce the concept as<br />
meaningless and misleading in evolutionary theory (Wilson<br />
and Brown 1953; Zink 2004). What is the problem?<br />
One common critical response is that the subspecies concept<br />
lacks coherence in meaning, and hence is difficult<br />
to comprehend (Futuyma 1998; Zink 2004). Moreover,<br />
the use of subspecies often masks real diversity (cryptic<br />
species, convergence) or depicts diversity that is non-existent<br />
or only trivial (e.g., lack of support in DNA-based<br />
analyses; Zink 2004). Indeed, as John Fitzpatrick attests<br />
(2010, p. 54), “The trinomial system cannot accurately<br />
represent the kind of information now available about genetic<br />
and character variation across space. Instead, even<br />
more accurate tools are being perfected for quantitative,<br />
standardized descriptions of variation. These analyses—<br />
not subspecies classifications—will keep providing new<br />
scientific insights into geographic variation.”<br />
Even with the identification of a variety of problems,<br />
many authors recommend that complete abandonment<br />
of the trinomial category in taxonomy is not necessary<br />
nor advised (e.g., Mallett 1995, Hawlitschek et al. 2012).<br />
Unfortunately, a consensus among biologists concerning<br />
the use of subspecies is not likely to emerge (Fitzpatrick<br />
2010). In step with Fitzpatrick’s (2010) comments, we<br />
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Taxonomy and conservation of beaded lizards<br />
contend that the plethora of variation detected in organisms<br />
must be approached in a modern sense that does<br />
not rely upon a cumbersome and outdated taxonomic<br />
system. Indeed, we anticipate that the description of<br />
geographic variation in organisms, once emancipated<br />
from infraspecific taxonomy, will actually accelerate our<br />
understanding of variation and its complexities. In our<br />
view, the confusion in recognizing subspecies can also<br />
mislead conservation planning, and it has on more than<br />
one occasion (e.g., the dusky seaside sparrow, see Avise<br />
and Nelson 1989). We thus agree with Wilson and Brown<br />
(1953), Douglas et al. (2002), Zink (2004), Fitzpatrick<br />
(2010) and others in their insightful criticisms leveled at<br />
the subspecies concept and the use of trinomials in taxonomy.<br />
Other authors have echoed similar views (Burbrink<br />
et al., 2000; Burbrink 2001; Douglas et al. 2007; Tobias<br />
et al. 2010; Braby et al. 2011; Hoisington-Lopez 2012;<br />
Porras et al. 2013).<br />
Given our reassessment of molecular (mt- and<br />
nDNAs), phylogeographic, morphological, and biogeographic<br />
evidence, we elevate the subspecies of Heloderma<br />
horridum to the rank of full species (Wiley, 1978;<br />
Zink 2004; Tobias et al. 2010; Braby et al. 2011; Porras<br />
et al. 2013). Indeed, Douglas et al. (2010, p. 164) stated<br />
that, “… unlike H. suspectum, our analyses support the<br />
subspecific designations within H. horridum. However,<br />
these particular lineages almost certainly circumscribe<br />
more than a single species … Thus, one benefit of a conservation<br />
phylogenetic perspective is that it can properly<br />
identify biodiversity to its correct (and thus manageable)<br />
taxonomic level.” Accordingly, based on multiples lines<br />
of concordant evidence, we recognize four species of<br />
beaded lizards. They are:<br />
Mexican beaded lizard: Heloderma horridum (Wiegmann<br />
1829)<br />
Río Fuerte beaded lizard: Heloderma exasperatum<br />
(Bogert and Martín del Campo 1956)<br />
Chiapan beaded lizard: Heloderma alvarezi (Bogert<br />
and Martín del Campo 1956)<br />
Guatemalan beaded lizard: Heloderma charlesbogerti<br />
(Campbell and Vannini, 1988)<br />
In the above arrangement, we do not recognize subspecies<br />
and vernacular names remain unchanged. The geographic<br />
distribution of the four species of beaded lizards<br />
is presented in Fig. 7. Locality data for the map were<br />
derived from Bogert and Martín del Campo (1956),<br />
Campbell and Vannini (1988), Schwalbe and Lowe<br />
(2000), Lemos-Espinal et al. (2003), Campbell and Lamar<br />
(2004), Beck (2005), Monroy-Vilchis et al. (2005),<br />
Ariano-Sánchez and Salazar (2007), Anzueto and Campbell<br />
(2010), Domiguez-Vega et al. (2012), and Sánchez-<br />
De La Vega et al. (2012). The “?” on the map (coastal<br />
Oaxaca, municipality: San Pedro Tututepec) denotes a<br />
jet-black adult specimen photographed by Vicente Mata-<br />
Silva (pers. comm.) in December 2010. The validity of<br />
this record is questionable owing to its striking coloration<br />
resemblance to H. alvarezi from the Central Depression<br />
(Río Grijalva Depression) of Chiapas and extreme western<br />
Guatemala, rather than to H. horridum. Although the<br />
individual might represent an isolated population of H.<br />
alvarezi, further study in this area of Oaxaca is required<br />
to rule out human activity as an agent (e.g., displacement).<br />
Beaded Lizards and Seasonally Dry<br />
Tropical Forests<br />
The key to understanding the evolution and biogeography<br />
of beaded lizards and the prospects for implementing<br />
meaningful conservation measures is through a recognition<br />
of the biomes they occupy, which we emphasize are<br />
the widely but patchily distributed low elevation seasonally<br />
dry tropical forests (SDTFs; see Trejo and Dirzo<br />
2000; Campbell and Lamar 2004; Beck 2005; Ariano-<br />
Sánchez 2006; Miles et al. 2006; Pennington et al. 2006;<br />
Dirzo et al. 2011; Domiguez-Vega et al. 2012).<br />
The evolution of SDTFs in Mesoamerica is a complex<br />
evolutionary scenario (Stuart 1954, 1966), and our understanding<br />
of their origin and temporal diversification<br />
is in its infancy (Janzen, 1988; Becerra 2005; Pennington<br />
et al. 2006; Dirzo et al. 2011; De-Nova et al. 2012). One<br />
approach to grapple with complex issues such as the origin<br />
and historical construction of SDTFs in Mesoamerica<br />
has been to examine a single but highly diverse plant taxon<br />
within a phylogenetic (phylogenomic) backdrop. This<br />
approach, accomplished by Becerra (2005) and more recently<br />
by De-Nova et al. (2012), uses the woody plant<br />
(tree) Bursera (Burseracae, Sapindales), a highly diverse<br />
genus (> 100 species) with a distribution in the New<br />
World and emblematic of most dry forest landscapes<br />
(De-Nova et al. 2012). Owing to this diversity, coupled<br />
with extensive endemism, this taxon has yielded valuable<br />
information that serves as a reasonable proxy for diversification<br />
and expansion of the SDTF biomes (Dick and<br />
Pennington 2012). Hence, plant (angiosperm) species<br />
richness and expansion of SDTF biomes in Mesoamerica<br />
is hypothesized to parallel the diversification of Bursera<br />
(Dick and Wright 2005).<br />
Based on both plastid and nuclear genomic markers<br />
that were analyzed using fossil-calibrated techniques and<br />
ancestral habitat reconstruction, the origin of Bursera in<br />
Mesoamerica is hypothesized to be in northwestern Mexico<br />
in the earliest Eocene (~50 mya), with subsequent extensive<br />
diversification and southern expansion along the<br />
Mexican Transvolcanic Belt in the Miocene, especially<br />
~7–10 mya (De-Nova et al. 2012). Accelerated clade diversification<br />
of Bursera and its sister genus Commiphora<br />
occurred during the Miocene, a period of increased aridity<br />
likely derived from seasonal cooling and rain shadow<br />
effects (Dick and Wright 2005). Although causal connections<br />
are complex, they include global tectonic pro-<br />
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Fig. 7. The distribution of beaded lizards in Mexico and Guatemala. Colored dots represent verified sightings (populations) and<br />
museum records. Note the fragmented populations of all four species, which closely approximates the patchy distribution of seasonal<br />
dry tropical forests (see map in Brown and Lowe [1980]). See text for explanation of question marks (“?”) and other details.<br />
cesses, orogenic activities (uplifting of the Sierra Madre<br />
Occidental and Sierra Made Oriental) and local volcanism<br />
(Dick and Wright 2005; De-Nova et al. 2012). De-<br />
Nova et al. (2012) concluded by emphasizing that their<br />
phylogenomic analysis of Bursera points to high species<br />
diversity of SDTFs in Mesoamerica that derives from<br />
within-habitat speciation rates that occurred in the envelope<br />
of increasing aridity from the early Miocene to the<br />
present. Furthermore, they stated (p. 285), “This scenario<br />
agrees with previous suggestions that [angiosperm] lineages<br />
mostly restricted to dry environments in Mexico<br />
resulted from long periods of isolated evolution rather<br />
than rapid species generation....”<br />
Beaded Lizard Evolution and Diversification<br />
The phylogenetic analyses of Heloderma horridum<br />
(sensu lato) by Douglas et al (2010) provided fossilcalibrated<br />
estimates of divergence times, which allow us<br />
to draw connections to the origin and diversification of<br />
SDTFs in Mesoamerica (Table 1, Fig. 6). Based on those<br />
analyses, H. horridum (sensu lato) and H. suspectum are<br />
hypothesized to have diverged from a most-recent common<br />
ancestor in the late Eocene (~35 mya), which corresponds<br />
to the establishment of Bursera in northwestern<br />
Mexico. Subsequent diversification (cladogenesis) of the<br />
beaded lizards occurred during the late Miocene (9.71<br />
mya), followed by a lengthy period of stasis of up to 5<br />
my, with subsequent cladogenesis extending into the<br />
Pliocene and Pleistocene. Of particular interest is that<br />
this scenario approximately parallels the diversification<br />
and southern expansion of SDTFs (Dick and Wright<br />
2005; De-Nova et al. 2012). Accordingly, based on the<br />
above discussion of SDTFs and phylogenetic analyses,<br />
we suggest that beaded lizard lineage diversification<br />
resulted from long periods of isolated (allopatric) evolution<br />
in SDTFs. Douglas et al. (2010) referred to the<br />
fragmented tropical dry forests of western Mexico as<br />
“engines” for diversification. The extralimital distribution<br />
of H. exasperatum and H. horridum into adjacent<br />
pine-oak woodland and thorn scrub biomes appears to be<br />
relatively uncommon (Schwalbe and Lowe 2000; Beck<br />
2005; Monroy-Vilchis et al. 2005).<br />
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Taxonomy and conservation of beaded lizards<br />
Conservation of Beaded Lizards<br />
A primary aim of this paper is to provide a useful and<br />
accurate synthesis of information on the taxonomy of<br />
beaded lizards that will lead to informed decisions regarding<br />
their conservation (see Douglas et al., 2010).<br />
Until recently, H. horridum (sensu lato) was designated<br />
as Vulnerable on the World Conservation Union (IUCN)<br />
Red List. In 2007, that designation was changed to Least<br />
Concern based on more stringent criteria (Canseco-<br />
Marquez and Muñoz 2007; categories and criteria version<br />
3.1). The 2007 IUCN Red List also determined that,<br />
“Additional research is needed into the taxonomic status,<br />
distribution and threats to this species” (Canseco-Marquez<br />
and Muñoz 2007). The critically endangered status<br />
of H. h. charlesbogerti (sensu lato) in Guatemala (Ariano-Sánchez<br />
2006; Ariano-Sánchez and Salazar 2007)<br />
has not altered the current IUCN Red List designation<br />
of this taxon, because population trends of other beaded<br />
lizards in Mexico remain “unknown” (www.iucnredlist.<br />
org/search; see International Reptile Conservation Foundation,<br />
IRCF; www.ircf.org). As more information on the<br />
population status of the newly elevated beaded lizards<br />
becomes available, in view of their fragmented distributions<br />
and threats to their habitats, the IUCN likely will<br />
designate these taxa as Vulnerable or a higher threat category<br />
(see our EVS analysis below). For example, H. exasperatum,<br />
H. alvarezi, and H. charlesbogerti all occupy<br />
limited areas of SDTF (Beck 2005).<br />
In Mexico, helodermatid lizards are listed as “threatened”<br />
(amenazadas) under the Mexican law (NOM-<br />
059-SEMARNAT-2010), legislation comparable to that<br />
in the United States Endangered Species Act. The threatened<br />
category from Mexican law coincides, in part, with<br />
the “Vulnerable” category of the IUCN Red List. This<br />
document defines “threatened” as species or populations<br />
that could become at risk of extinction in a short to medium<br />
period if negative factors continue to operate that<br />
reduce population sizes or alter habitats. Heloderma h.<br />
charlesbogerti (sensu lato) is listed on the Guatemalan<br />
Lista Roja (Red List) as “endangered,” with approximately<br />
200–250 adult individuals remaining in under<br />
26,000 ha of its natural habitat of SDTF and thorn scrub,<br />
(Ariano-Sánchez 2006).<br />
Furthermore, H. h. charlesbogerti (sensu lato) is listed<br />
on CITES Appendix I, a designation that includes species<br />
threatened with extinction (see CITES document<br />
appended to Ariano-Sánchez and Salazar 2007). Trade<br />
in CITES Appendix I species is prohibited except under<br />
exceptional circumstances, such as for scientific research<br />
(CITES 2007). The remaining taxa of Heloderma horridum<br />
(sensu lato) (H. h. alvarezi, H. h. exasperatum,<br />
and H. h. horridum) are listed on Appendix II of CITES<br />
(CITES 2007). International trade in Appendix II species<br />
might be authorized under an export permit, issued by<br />
the originating country only if conditions are met that<br />
show trade will not be detrimental to the survival of the<br />
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species in the wild. The United States Fish & Wildlife<br />
Service issues permits only if documentation is provided<br />
proving legal origin, including a complete paper trail<br />
back to legal founder animals. This procedure allows the<br />
importation of beaded lizards into the United States to<br />
be tightly regulated (in theory), and also subjects such<br />
imports to provisions of the Lacey Act that control commerce<br />
in illegally obtained fish and wildlife (Beck 2005).<br />
Beaded Lizards: Denizens of Endangered<br />
SDTFs<br />
Although occasional sightings of beaded lizards have<br />
been reported from mid elevation pine-oak woodlands, all<br />
four species primarily inhabit lowland SDTFs and rarely<br />
in associated thorn scrub, in both Mexico and Guatemala<br />
(Schwalbe and Lowe 2000; Lemos-Espinal et al. 2003;<br />
Campbell and Lamar 2004; Beck 2005; Monroy-Vilchis<br />
et al. 2005; Ariano and Salazar 2007; Domiguez-Vega et<br />
al. 2012). Thus, the optimal measure to reduce threats to<br />
beaded lizards is to maintain the integrity of their tropical<br />
dry forest habitats. Current threats to beaded lizards<br />
throughout their range include habitat loss, road mortality,<br />
poaching, and illegal trade (Beck 2005; Miles et<br />
al. 2006; Golicher et al. 2012). Habitat loss takes many<br />
forms, from the conversion of SDTFs to areas of agriculture<br />
and cattle ranching, to forest fragmentation owing<br />
to roads and other forms of development (Pennington et<br />
al. 2006). Degradation from human-introduced invasive<br />
(exotic) organisms and fire also are contributing factors<br />
(Beck 2005).<br />
When the Spaniards arrived in the Western Hemisphere,<br />
Mesoamerican SDTFs covered a region stretching<br />
from Sonora (Mexico) to Panama, an area roughly the<br />
size of France (~550,000 km 2 ). Today, only 0.1% of that<br />
region (under 500 km 2 ) has official conservation status,<br />
and less than 2% remains sufficiently intact to attract the<br />
attention of conservationists (Janzen 1988; Hoekstra et<br />
al. 2005). Of all 13 terrestrial biomes analyzed by Hoekstra<br />
et al. (2005), the SDTF biome has the third highest<br />
conservation risk index (ratio of % land area converted<br />
per % land area protected), far above tropical wet forest<br />
and temperate forest biomes (Miles et al. 2006).<br />
Mexico ranks among the most species rich countries<br />
in the world (García 2006; Urbina-Cardona and Flores-<br />
Villela 2010; Wilson and Johnson 2010; Wilson et al.<br />
2010, 2013). Nearly one-third of all the Mexican herpetofaunal<br />
species are found in SDTFs (García 2006; De-<br />
Nova et al. 2012). Neotropical dry forests span over 16<br />
degrees of latitude in Mexico, giving way to variation<br />
in climatic and topography that results in a diversity of<br />
tropical dry forest types, and a concurrent high proportion<br />
of endemism of flora and fauna (García 2006; De-<br />
Nova et al. 2012; Wilson et al. 2010; 2013). Mexican<br />
seasonally tropical dry forest, classified into seven ecoregions<br />
that encompass about 250,000 km 2 , has enormous<br />
conservation value and has been identified as a hotspot<br />
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Reiserer et al.<br />
for conservation priorities (Myers et al. 2000; Sánchez-<br />
Azofeifa et al. 2005; García 2006; Urbina-Cardona and<br />
Flores-Villela, 2010; Wilson et al. 2010, Mittermeier et<br />
al. 2011). The vast majority (98%) of this region, however,<br />
lies outside of federally protected areas (De-Nova<br />
et al. 2012). With few exceptions, most of the protected<br />
areas in Mexico occur in the states of Chiapas and Jalisco,<br />
leaving much of the region (e.g., Nayarit and Sinaloa)<br />
without government (federal) protection (García 2006).<br />
In Guatemala, less than 10% of an estimated 200,000<br />
ha of original suitable habitat have been established as<br />
protected critical habitat in the Motagua Valley for the<br />
endangered H. charlesbogerti (Nájera Acevedo 2006). A<br />
strong effort led by local citizens, conservation workers,<br />
biologists, government officials, NGOs, and conservation<br />
organizations (e.g., The Nature Conservancy, International<br />
Reptile Conservation Association, Zoo Atlanta,<br />
and Zootropic) negotiated to have H. h. charlesbogerti<br />
(sensu lato) placed on CITES Appendix I, to purchase<br />
habitat, conduct research, employ local villagers in monitoring<br />
the lizards, and promote environmental education<br />
(Lock 2009). Similar efforts for beaded lizards have been<br />
underway for many years in Chiapas (Mexico), spearheaded<br />
at ZooMAT (Ramírez-Velázquez 2009), and in<br />
Chamela, Jalisco (www.ibiologia.unam.mx/ebchamela/<br />
www/reserva.html). Such efforts will need to expand in<br />
the years ahead and will doubtless play a crucial role if<br />
we hope to retain the integrity of existing SDTFs inhabited<br />
by beaded lizards throughout their range.<br />
Discussion<br />
In this paper, we reassessed the taxonomy of Heloderma<br />
horridum (sensu lato) using both published information<br />
and new analyses (e.g., CMA). We concluded that diversity<br />
in beaded lizards is greater than explained by infraspecific<br />
differences and that the recognition of subspecies<br />
is not warranted, as it obscures diversity. Our decision to<br />
elevate the four subspecies of H. horridum to full species<br />
status is not entirely novel (Beck 2005; Douglas et al.<br />
2010). Furthermore, our taxonomic changes are based on<br />
integrative information (i.e., morphology, mt- and nDNA<br />
sequence information, biogeography) and changing perspectives<br />
on the utility of formally recognizing infraspecific<br />
diversity using a trinomial taxonomy (Wilson and<br />
Brown 1953; Douglas et al. 2002; Zink 2004; Porras et<br />
al. 2013). This decision not only adds to a better understanding<br />
of the evolution of helodermatids, but also provides<br />
an important evolutionary framework from which<br />
to judge conservation decisions with prudence (Douglas<br />
et al. 2002).<br />
Below, we delineate and discuss prospective research<br />
and conservation recommendations for beaded lizards<br />
based on our present review. Borrowing some of the<br />
guidelines and recommendations for future research and<br />
conservation for cantils, also inhabitants of SDTFs, by<br />
Porras et al. (2013), we outline similar ones for the four<br />
species of beaded lizards (H. alvarezi, H. charlesbogerti,<br />
H. exasperatum, and H. horridum).<br />
Future Research and Conservation<br />
Recommendations<br />
1. Throughout this paper we emphasized the importance<br />
of SDTFs in the distribution of beaded lizards, yet most<br />
SDTFs within their distribution are not Protected Natural<br />
Areas (PNAs; Beck 2005; Urbina-Cardona and Flores-<br />
Villela 2009; Domiguez-Vega et al. 2012). Accordingly,<br />
emphasis should be placed on those areas of SDTFs for<br />
prospective research, new conservation projects, and for<br />
establishing new PNAs. The protection of beaded lizards<br />
must be placed into a larger context of conservation<br />
planning. Proper stewardship of SDTFs and other biomes<br />
must include meaningful (scientific) protective measures<br />
for all of the flora and fauna, rather than piecemeal (e.g.,<br />
taxon-by-taxon) approaches that lack a cohesive conservation<br />
plan (Douglas et al. 2010).<br />
We applaud the efforts of Domíguez-Vega et al.<br />
(2012) in identifying conservation areas for beaded lizards;<br />
however, we do not agree with all of their conclusions.<br />
In particular, based on field experiences by one<br />
of us (DDB), we contend that the potential (predicted)<br />
range of H. exasperatum in Sonora (Mexico) based on<br />
the results of their habitat suitability modeling, appears<br />
exaggerated and thus may be misleading. In our opinion,<br />
their distribution maps (figs. 2 and 3) overestimate<br />
the extent of true SDTFs in Sonora, showing their occurrence<br />
in a type of biome that is more accurately classified<br />
as Sinaloan Thorn Scrub (see the excellent maps in<br />
Brown and Lowe 1980; Robichaux and Yetman 2000).<br />
In Sonora, beaded lizards (H. exasperatum) are rarely<br />
found in association with pure thorn scrub, while Gila<br />
monsters, in contrast, are frequently encountered in that<br />
type of habitat (Schwalbe and Lowe 2000; Beck 2005).<br />
2. With few exceptions, the population viability of beaded<br />
lizards is largely unknown (Beck 2005; Ariano-Sánchez<br />
2006; Ariano-Sánchez et al. 2007; Domíguez-Vega et al.<br />
2012). We highly recommend that modern assessments<br />
of the four species occur at or near localities where they<br />
have been recorded (e.g., Jiménez-Valverde and Lobo<br />
2007). Whereas H. charlesbogerti, and to a lesser degree<br />
H. alvarezi (Ramírez-Velázquez 2009), are receiving international<br />
conservation attention, we feel that similar<br />
consideration is necessary for H. exasperatum owing<br />
to its relatively limited geographic range (Sonora, Chihuahua,<br />
Sinaloa), the large extent of habitat destruction<br />
and fragmentation (Fig. 8), and limited areas receiving<br />
protection (Trejo and Dirzo 2000; Domíguez-Vega et<br />
al. 2012; see http://www.conanp.gob.mx/regionales/). In<br />
1996, about 92, 000 hectares in the Sierra de Álamos and<br />
the upper drainage of the Río Cuchujaqui were declared<br />
a biosphere reserve by the Secretary of the Environment<br />
and Natural Resources (SEMARNAT 2010), called the<br />
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y Río Cuchujaqui (Martin and Yetman 2000; S. Meyer,<br />
pers. comm.). Efforts continue in Sonora to set aside additional<br />
habitat for conservation, but, other than Alamos,<br />
no other areas with true SDTFs presently exist (Robichaux<br />
and Yetman 2000; S. Meyer, pers. comm.).<br />
3. Conservation management plans for each of the species<br />
of beaded lizards should be developed from an<br />
integrative perspective based on modern population<br />
assessments, genetic information, and ecological (e.g.,<br />
soil, precipitation, temperature) and behavioral data<br />
(e.g., social structure, mating systems, home range size).<br />
Taxonomy and conservation of beaded lizards<br />
Fig. 8. Destruction of seasonally dry tropical forest near Alamos, Sonora, Mexico.<br />
Photo by Daniel D. Beck.<br />
Such a conservation plan is in place for the Guatemalan<br />
beaded lizard (H. charlesbogerti) by CONAP-Zootropic<br />
(www.ircf.org/downloads/PCHELODERMA-2Web.<br />
pdf). Also, aspects of burgeoning human population<br />
growth must be considered, since outside of PNAs these<br />
large slow-moving lizards generally are slaughtered on<br />
sight, killed on roads by vehicles (Fig. 9), and threatened<br />
by persistent habitat destruction primarily for agriculture<br />
and cattle ranching (Fig. 10). For discussions on conservation<br />
measures in helodermatid lizards, see Sullivan et<br />
al. (2004), Beck (2005), Kwiatkowski et al. (2008), Douglas<br />
et al. (2010), Domíguez-Vega et al. (2012), and Ariano-<br />
Sánchez and Salazar (2013).<br />
In Mexico, the IUCN lists<br />
Heloderma horridum (sensu<br />
lato) under the category of Least<br />
Concern. Recently, Wilson et al.<br />
(2013) reported the Environmental<br />
Vulnerability Score (EVS)<br />
for H. horridum (sensu lato) as<br />
11. Briefly, an EVS analysis assesses<br />
the potential threat status<br />
of a given species based on<br />
multiple criteria and provides a<br />
single score or index value (Wilson<br />
and McCranie 2004; Porras<br />
et al. 2013; Wilson et al. 2013).<br />
High EVS scores (e.g., 17), for<br />
example, signify vulnerability.<br />
With the taxonomic changes we<br />
proposed for beaded lizards, an<br />
EVS assessment is thus required<br />
for each species. Using the new<br />
criteria developed by Wilson et<br />
al. (2013; see Porras et al. 2013),<br />
we recalculated the EVS for the<br />
species of beaded lizards, which<br />
are presented below:<br />
H. horridum: 5 + 4 + 5 = 14<br />
H. exasperatum: 5 + 7 + 5 = 17<br />
H. alvarezi: 4 + 6 + 5 = 15<br />
H. charlesbogerti: 4 + 8 + 5 = 17<br />
Fig. 9. A dead-on-the-road (DOR) H. exasperatum (sensu stricto) near Álamos, Sonora,<br />
Mexico. Vehicles on paved roads are an increasing threat to beaded lizards, Gila monsters,<br />
and other wildlife. Photo by Thomas Wiewandt.<br />
These recalculated values fall into<br />
the high vulnerability category<br />
(Wilson et al. 2013; Porras et al.<br />
2013), underscoring the urgency<br />
for the development of conservation<br />
management plans and longterm<br />
population monitoring of all<br />
species of beaded lizards. These<br />
values thus need to be reported<br />
to the appropriate IUCN committees,<br />
so immediate changes in status<br />
can be made and conservation<br />
actions implemented.<br />
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Fig. 10. Agave cultivation in Mexico results in the destruction of seasonally dry tropical<br />
forests. Photo by Thomas Wiewandt.<br />
natural habitat, small population<br />
size (200–250 adults) and endangered<br />
status, H. charlesbogerti is<br />
currently listed as CITES Appendix<br />
I (Ariano-Sánchez and Salazar<br />
2007). Given the taxonomic<br />
elevation of these taxa, conservation<br />
agencies can use these charismatic<br />
lizards as flagship species<br />
in efforts to publicize conservation<br />
efforts in their respective<br />
countries at all levels of interest<br />
and concern, including education<br />
and ecotourism (Beck 2005).<br />
Eli Lilly Co., Disney Worldwide<br />
Conservation Fund and The Nature<br />
Conservancy support the<br />
conservation of H. charlesbogerti<br />
(Ariano-Sánchez and Salazar<br />
2012). Such corporate involvement<br />
provides funds and positive<br />
public exposure (e.g., social network<br />
advertising) that otherwise<br />
would not be possible.<br />
Fig. 11. Antonio Ramirez Ramírez-Velázquez, a herpetologist, discusses the beauty and<br />
importance of beaded lizards (H. alvarezi, sensu stricto) to a group of enthusiastic children<br />
and their teacher at Zoo Miguel Álvarez del Toro (ZooMAT) in Tuxtla Gutiérrez, Chiapas,<br />
Mexico. The zoo was named in honor of its founding director, Señor Miguel Alvarez del<br />
Toro, who had a keen academic and conservation interest in beaded lizards. He collected<br />
the type specimen of H. alvarezi (described in Bogert and Martín del Campo, 1956), which<br />
was named in his honor. ZooMAT offers hands-on environmental education programs to<br />
schoolchildren and other citizens of southern Mexico. Photo by Thomas Wiewandt.<br />
4. We recommend the establishment of zoo conservation<br />
(AZA) educational outreach programs, both ex situ and<br />
in situ, such as those currently in progress for H. charlesbogerti<br />
(www.IRCF.org;www.zooatlanta.org) and for<br />
H. alvarezi in Chiapas (Ramírez-Velázquez, 2009, see<br />
Fig. 11). Because of its limited range, destruction of its<br />
5. One of the major conclusions<br />
of this paper is that our knowledge<br />
of the taxonomy and phylogeography<br />
of beaded lizards<br />
remains at an elementary level.<br />
As discussed, a robust phylogeographic<br />
analysis using morphological<br />
characters is not available.<br />
Our character mapping<br />
exercise, for various reasons, is<br />
not a substitute procedure for<br />
detailed phylogenetic analyses<br />
using morphology (Assis 2009;<br />
Assis and Rieppel 2011). Other<br />
authors have made similar pleas<br />
concerning the importance of<br />
morphology, including fossils, in<br />
phylogenetic reconstruction (Poe<br />
and Wiens 2000; Wiens 2004,<br />
2008; Gauthier et al. 2012).<br />
Moreover, further studies on the<br />
historical biogeography of helodermatids<br />
(e.g., ancestral area<br />
reconstruction) are needed (e.g.,<br />
Ronquist 1997, 2001; Ree and<br />
Smith 2008). Detailed morphological<br />
analyses can be conducted with new tools such as<br />
computed tomography (CT) scans of osteological characters<br />
of both extant and fossil specimens (Gauthier et al.<br />
2012), and geometric morphometric approaches to external<br />
characters (Davis 2012). Furthermore, in the expanding<br />
field of “venomics” new venom characters in beaded<br />
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lizards will likely be discovered, which might prove useful<br />
in phylogenetic analyses (Fry et al. 2009, 2010).<br />
As we progress into the “Age of Genomics” with<br />
ever-growing computational advancements (e.g., bioinformatics;<br />
Horner et al. 2009), new and exciting methods<br />
to explore organismal diversity are opening, including<br />
such next-generation approaches as pyrosequencing<br />
(microsatellite isolation), establishing transcriptome<br />
databases, and whole-genome sequencing (Wiens 2008;<br />
Castoe et al. 2011; Culver et al. 2011). Currently, plans<br />
are underway to apply pyrosequencing methods to helodermatids<br />
to generate a nearly inexhaustible supply of<br />
microsatellite markers for a variety of proposed analyses<br />
(W. Booth and T. Castoe, pers. comm.). Standing on<br />
the shoulders of The Human Genome Project (Culver et<br />
al. 2011), and reaping the success of genome projects in<br />
other reptilian taxa (Castoe et al. 2011), it is now possible<br />
to establish a “Helodermatid Genome Project.” Beaded<br />
lizards and the Gila monster are especially good candidates<br />
for such an investment, especially given the importance<br />
of their venom components in medical research and<br />
recent pharmaceutical applications (Beck 2005; Douglas<br />
et al. 2010; Fry et al. 2009, 2010).<br />
6. An important take-home message from Douglas et al.<br />
(2010) is that future conservation efforts will require a<br />
robust understanding of phylogenetic diversity (e.g.,<br />
conservation phylogenetics) to make sensible (logical)<br />
and comprehensive conservation plans. For example, the<br />
range of H. horridum (sensu stricto) is the most expansive<br />
of the species of beaded lizards and has not been fully<br />
explored with respect to genetic diversity. Accordingly,<br />
sampling throughout its range may yield cryptic genetic<br />
diversity, perhaps even new species. We emphasize that<br />
viable conservation planning must incorporate all intellectual<br />
tools available, including those that incorporate<br />
old methods (e.g., paleoecological data) but viewed<br />
through a new lens (Douglas et al. 2007, 2009; Willis<br />
et al. 2010). Wisely, Greene (2005) reminds us that we<br />
are still grappling with understanding basic and essential<br />
issues concerning the natural history of most organisms.<br />
To that end, we must continue in our efforts to educate<br />
students and the public of the need for and importance of<br />
this branch of science.<br />
7. The new taxonomic arrangement of beaded lizards<br />
we proposed will affect other fields of science, such as<br />
conservation biology and human medicine (Beck, 2005;<br />
Douglas et al., 2010). In Fry et al. (2010, p. 396, table 1),<br />
toxins are matched to the subspecies of beaded lizards<br />
and Gila monsters. Yet as noted by Beck (2005) and<br />
Douglas et al. (2010), the banded Gila monster (H. s.<br />
cinctum) is not a valid subspecies, which is based on<br />
several levels of analysis (i.e., morphology, geographic<br />
distribution, and haplotype data). Individuals assigned to<br />
H. s. cinctum based on color and pattern, for example,<br />
have been found in southwestern Arizona near the Mexican<br />
border and in west-central New Mexico (Beck 2005).<br />
Furthermore, most venom researchers, including those<br />
who study helodermatids, often obtain samples from captive<br />
subjects in private collections and zoological institutions.<br />
Many of these animals have been bred in captivity<br />
and result from crossing individuals of unknown origin<br />
or from different populations (D. Boyer, pers. comm).<br />
Among other negative outcomes, such “mutts” will confound<br />
results of the true variation of venoms. Geographic<br />
and ontogenetic variation in venom constituents is well<br />
established in other squamates (Minton and Weinstein<br />
1986; Alape-Girón et al. 2008; Gibbs et al. 2009), which<br />
is apparently the case in helodermatids (Fry et al. 2010).<br />
Thus, we strongly encourage researchers investigating<br />
helodermatid venoms for molecular analysis and pharmaceutical<br />
development to use subjects with detailed locality<br />
information, as well as age, gender, and size, and<br />
to provide those data in their publications.<br />
8. Owing to problems that many scientists, their students,<br />
and other interested parties from Mesoamerica<br />
have in gaining access to primary scientific literature,<br />
we highly recommend that authors seek Open Access<br />
peer-reviewed journals as venues for their publications<br />
on beaded lizards, an important factor in our choice for<br />
selecting the present journal (www.redlist-ARC.org) as a<br />
venue for our data and conservation message.<br />
Acknowledgments.—We thank Larry David Wilson<br />
for inviting us to participate in the Special Mexico Issue.<br />
A Heritage Grant from the Arizona Game and Fish<br />
Department and a Research Incentive Award/Scholarly<br />
Research and Creative Activities Award (Arizona State<br />
University) awarded to GWS funded parts of this research.<br />
Zoo Atlanta (Dwight Lawson, Joe Mendelson III)<br />
and Georgia State University (Department of Biology)<br />
provided various levels of support. Warren Booth, Donal<br />
Boyer, Dale DeNardo, Andrés García, Stephanie Meyer,<br />
and Tom Wiewandt were always willing to discuss<br />
beaded lizard and tropical dry forest biology with us. We<br />
thank Brad Lock, Louis Porras, and Larry David Wilson<br />
for their suggestions and valuable insights in improving<br />
an earlier version of this manuscript. Also, three reviewers,<br />
including Daniel Ariano-Sánchez, provided key<br />
information and sharpened our focus, though we bear<br />
the burden of any blunders. We thank Javier Alvarado,<br />
Daniel Ariano-Sánchez, David Brothers, Quetzal Dwyer,<br />
Kerry Holcomb, Vicente Mata-Silva, Stephanie Meyer,<br />
Adam Thompson, and Tom Wiewandt for graciously<br />
supplying us with images. Vicente Mata-Silva kindly assisted<br />
us in preparing the resumen and locating literature<br />
on Heloderma.<br />
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Received: 23 May 2013<br />
Accepted: 12 June 2013<br />
Published: 29 July 2013<br />
Randall S. Reiserer is an integrative biologist whose research focuses on understanding the interrelationships<br />
among ecology, morphology, and behavior. Within the broad framework of evolutionary biology, he studies<br />
cognition, neuroscience, mimicry, life-history evolution, and the influence of niche dynamics on patterns of<br />
evolutionary change. His primary research centers on reptiles and amphibians, but his academic interests<br />
span all major vertebrate groups. His studies of behavior are varied and range from caudal luring and thermal<br />
behavior in rattlesnakes to learning and memory in transgenic mice. Randall established methods for studying<br />
visual perception and stimulus control in is studies of caudal luring in snakes. He commonly employs<br />
phylogenetic comparative methods and statistics to investigate and test evolutionary patterns and adaptive<br />
hypotheses. Dr. Reiserer is an editor of the upcoming peer-reviewed book, The Rattlesnakes of Arizona.<br />
Gordon W. Schuett is an evolutionary biologist and herpetologist who has conducted extensive research on reptiles.<br />
His work has focused primarily on venomous snakes, but he has also published on turtles, lizards, and<br />
amphibians. Among his most significant contributions are studies of winner-loser effects in agonistic encounters,<br />
mate competition, mating system theory, hormone cycles and reproduction, caudal luring and mimicry,<br />
long-term sperm storage, phylogeographic analyses of North American pitvipers, and as a co-discoverer of<br />
facultative parthenogenesis in non-avian reptiles. He served as chief editor of the peer-reviewed book Biology<br />
of the Vipers and is presently serving as chief editor of an upcoming peer-reviewed book The Rattlesnakes of<br />
Arizona (rattlesnakesofarizona.org). Gordon is a Director and scientific board member of the newly founded<br />
non-profit The Copperhead Institute (copperheadinstitute.org). He was the founding Editor of the journal<br />
Herpetological Natural History. Dr. Schuett resides in Arizona and is an adjunct professor in the Department<br />
of Biology at Georgia State University.<br />
Daniel D. Beck is an ecologist and herpetologist who has conducted research on the ecology, physiology, and behavior<br />
of rattlesnakes and helodermatid lizards. He has pioneered many of the field studies on helodermatid<br />
lizards in the past 30 years, including topics ranging from energy metabolism and habitat use to combat and<br />
foraging behaviors in locations ranging from the deserts of Utah, Arizona, and New Mexico, to the tropical<br />
dry forests of Sonora and Jalisco, Mexico. His book, Biology of Gila Monsters and Beaded Lizards (2005),<br />
presents a synthesis of much of our knowledge of these charismatic reptiles. Dr. Beck is Professor of Biology<br />
at Central Washington University, in Ellensburg, Washington, where he lives in a straw bale house with his<br />
wife, biologist Kris Ernest, and their two teenage children.<br />
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Pseudoeurycea naucampatepetl. The Cofre de Perote salamander is endemic to the Sierra Madre Oriental of eastern Mexico. This<br />
relatively large salamander (reported to attain a total length of 150 mm) is recorded only from, “a narrow ridge extending east from<br />
Cofre de Perote and terminating [on] a small peak (Cerro Volcancillo) at the type locality,” in central Veracruz, at elevations from<br />
2,500 to 3,000 m (Amphibian Species of the World website). Pseudoeurycea naucampatepetl has been assigned to the P. bellii<br />
complex of the P. bellii group (Raffaëlli 2007) and is considered most closely related to P. gigantea, a species endemic to the La<br />
<br />
specimens and has not been seen for 20 years, despite thorough surveys in 2003 and 2004 (EDGE; www.edgeofexistence.org), and<br />
thus it might be extinct. The habitat at the type locality (pine-oak forest with abundant bunch grass) lies within Lower Montane Wet<br />
Forest (Wilson and Johnson 2010; IUCN Red List website [accessed 21 April 2013]). The known specimens were “found beneath<br />
the surface of roadside banks” (www.edgeofexistence.org) along the road to Las Lajas Microwave Station, 15 kilometers (by road)<br />
south of Highway 140 from Las Vigas, Veracruz (Amphibian Species of the World website). This species is terrestrial and presumed<br />
to reproduce by direct development.<br />
Pseudoeurycea naucampatepetl is placed as number 89 in the top 100 Evolutionarily Distinct and Globally Endangered amphibians<br />
(EDGE; www.edgeofexistence.org). We calculated this animal’s EVS as 17, which is in the middle of the high vulnerability<br />
category (see text for explanation), and its IUCN status has been assessed as Critically Endangered. Of the 52 species in the genus<br />
Pseudoeurycea, all but four are endemic to Mexico (see Appendix of this paper and Acevedo et al. 2010). Photo by James Hanken.<br />
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Copyright: © 2013 Wilson et al. This is an open-access article distributed under the terms of the Creative Commons<br />
Attribution–NonCommercial–NoDerivs 3.0 Unported License, which permits unrestricted use for non-commercial<br />
and education purposes only provided the original author and source are credited.<br />
Amphibian & Reptile Conservation 7(1): 97–127.<br />
A conservation reassessment of the amphibians of<br />
Mexico based on the EVS measure<br />
1<br />
Larry David Wilson, 2 Jerry D. Johnson, and 3 Vicente Mata-Silva<br />
1<br />
Centro Zamorano de Biodiversidad, Escuela Agrícola Panamericana Zamorano, Departamento de Francisco Morazán, HONDURAS 2,3 Department<br />
of Biological Sciences, The University of Texas at El Paso, El Paso, Texas 79968-0500, USA<br />
Key words. EVS, anurans, salamanders, caecilians, IUCN categorizations, survival prospects<br />
Abstract.—Global amphibian population decline is one of the better documented symptoms of biodiversity<br />
loss on our planet, and one of the environmental super-problems humans have created.<br />
<br />
we are part of the natural world and depend on it for our survival. As a consequence, humans keep<br />
unraveling Earth’s life-support systems, and to reverse this trend must begin to develop a sustainable<br />
existence. Given this reality, we examine the conservation status of the 378 species of amphibians<br />
in Mexico, by using the Environmental Vulnerability Score (EVS) algorithm. We summarize and<br />
critique the IUCN Red List Assessments for these creatures, calculate their EVS, and compare the<br />
results of both conservation assessments. We also compare the EVS for Mexican amphibians with<br />
those recently reported for Mexican reptiles, and conclude that both groups are highly imperiled,<br />
especially the salamanders, lizards, and turtles. The response of humans to these global imperatives<br />
has been lackluster, even though biological scientists worldwide have called attention to the<br />
grave prospects for the survival of life on our planet. As part of the global community, Mexico must<br />
realize the effects of these developments and the rapid, comprehensive need to conserve the coun-<br />
mendations.<br />
Resumenmentados<br />
sobre la pérdida de biodiversidad en nuestro planeta, que a su vez es uno de los super-<br />
<br />
der<br />
que somos parte y dependemos de ella misma. Como consecuencia de ello, estamos desarticulando<br />
los sistemas biológicos del planeta, y para revertir esta tendencia debemos desarrollar una<br />
existencia sostenible. Ante esta realidad, examinamos el estado de conservación de las 378 espe-<br />
<br />
<br />
EVS, y comparamos los resultados con los resultados de la categorización de la UICN. También<br />
<br />
-<br />
<br />
sido mediocre, a pesar de que la comunidad mundial de biólogos se une al llamado de atención<br />
sobre las perspectivas graves que amenazan la supervivencia de la vida en nuestro planeta. Como<br />
<br />
<br />
<br />
Palabras claves. EVS, anuros, salamandras, cecilios, categorización de UICN, perspectivas de supervivencia<br />
Citation: Wilson LD, Johnson JD, Mata-Silva V. 2013. A conservation reassessment of the amphibians of Mexico based on the EVS measure. Amphibian<br />
& Reptile Conservation 7(1): 97–127(e69).<br />
Correspondence. Emails: 1 bufodoc@aol.com (Corresponding author) 2 jjohnson@utep.edu 3 vmata@utep.edu<br />
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Wilson et al.<br />
How will humans react to an increased awareness that<br />
Earth’s biodiversity is diminishing? What are these losses<br />
telling us about our place on the planet, our role in the<br />
biosphere? What is our role in conserving biodiversity as<br />
we become custodians of a planet that has clear limitations?<br />
And how can we pass to future generations the<br />
wisdom needed to make sound environmental decisions?<br />
The answers to these questions will tell us much about<br />
ourselves, and science will take us only part of the way<br />
along that journey.<br />
Collins and Crump 2009: 205.<br />
Introduction<br />
Global amphibian population decline is a well-known<br />
environmental issue to conservation biologists and herpetologists<br />
(Collins and Crump 2009; Stuart et al. 2010).<br />
This issue, however, often does not make it onto lists<br />
<br />
European Union citizens conducted in the fall of 2011<br />
<br />
(1) poverty, hunger and lack of drinking water (28% of<br />
those surveyed); (2) climate change (20%); (3) the economic<br />
situation (16%); (4) international terrorism (11%);<br />
(5) the availability of energy (7%); (6) the increasing<br />
global population (5%); (7) the spread of infectious dis-<br />
<br />
nuclear weapons (3%); and (10) don’t know (2%).<br />
Such surveys expose several underlying concerns.<br />
One is that amphibian population decline is not on the<br />
list, but neither is the larger issue of biodiversity decline.<br />
Another concern is that this “pick the biggest problem”<br />
approach does not acknowledge that all of these issues<br />
are intertwined and capable of creating “environmental<br />
super-problems,” as explained by Bright (2000). Further,<br />
with respect to the natural world Bright (2000: 37) indicated<br />
that “we will never understand it completely, it will<br />
not do our bidding for free, and we cannot put it back the<br />
way it was.” These features are characteristic of biodiversity<br />
and biodiversity decline, and indicative of how little<br />
we know about the current status of biodiversity. Mora<br />
et al. (2011) provided an estimate of the total amount of<br />
biodiversity, which they indicated at approximately 8.7<br />
million (±1.3 million SE), with about 86% of the existing<br />
land species and 91% of the oceanic species still awaiting<br />
description. The description of new taxa is only the<br />
initial step toward understanding how the natural world<br />
works. The world will not do our bidding for free, since<br />
we cannot obtain an appreciable quantity of anything<br />
<br />
<br />
we have destroyed the habitats of countless creatures (including<br />
amphibians) that also have evolved over time.<br />
We cannot reverse this damage, as evidenced by the fact<br />
that we have been unable to provide permanent solutions<br />
<br />
the case with biodiversity decline, since no retreat from<br />
species extinction is possible.<br />
Biodiversity decline is an environmental super-prob-<br />
<br />
fragmentation, and loss, pollution and disease, over-harvesting,<br />
exotic species, and extinction (Vitt and Caldwell<br />
2009). These problems interact to enmesh species into<br />
<br />
spiral in which inbreeding and genetic drift combine to<br />
cause a small population to shrink and, unless the spiral<br />
is reversed, to become extinct” (Campbell et al. 2008:<br />
pact<br />
species with narrower distributions.<br />
The extent of biodiversity decline is unknown, although<br />
most estimates indicate that we know very little<br />
about this topic. With respect to animals, we know substantially<br />
more about the diversity of vertebrates than invertebrates.<br />
Among the vertebrates subjected to a global<br />
analysis, a greater proportion of amphibians have been<br />
documented as threatened than birds or mammals (Stuart<br />
sessed.<br />
The data presented in Stuart et al. (2010) essentially<br />
were the same as in Stuart (2004). The number of amphibians<br />
known globally now exceeds 7,000 (7,139;<br />
www.amphibiaweb.org [accessed 8 June 2013]), which<br />
is 24.3% greater than the one cited by Stuart et al. (2010).<br />
The description of new species of amphibians obviously<br />
is a “growth industry,” and the rate of discovery does not<br />
appear to be slowing. Thus, we expect that the number<br />
of new amphibian taxa from Mexico will continue to increase.<br />
Another major fault with assessing the “world’s great-<br />
<br />
noted by Wilson et al. (2013: 23), “no permanent solution<br />
to the problem of biodiversity decline (including herpetofaunal<br />
decline) will be found in Mexico (or elsewhere<br />
in the world) until humans recognize overpopulation as<br />
the major cause of degradation and loss of humankind’s<br />
fellow organisms.” Further, they stated (Pp. 23–24) that,<br />
“solutions will not be available until humanity begins to<br />
realize the origin, nature, and consequences of the mismatch<br />
between human worldviews and how our planet<br />
<br />
“planetary management worldview” as maintaining that<br />
“we are separate from and in charge of nature, that nature<br />
exists mainly to meet our needs and increasing wants,<br />
and that we can use our ingenuity and technology to<br />
manage the earth’s life-support systems, mostly for our<br />
<br />
Unfortunately, over the span of about 10,000 years,<br />
humans have dismantled the planet’s life-support systems,<br />
and today we are living unsustainably (Miller and<br />
Spoolman 2012). So, until and unless we develop an environmentally<br />
sustainable society, no lasting, workable<br />
solutions to environmental problems will be found, including<br />
that of biodiversity decline.<br />
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Incilius pisinnus. The Michoacán toad, a state endemic, is known only from the Tepalcatepec Depression. This toad’s EVS has<br />
<br />
individual came from Apatzingán. Photo by Iván Trinidad Ahumada-Carrillo.<br />
Craugastor hobartsmithi. The distribution of the endemic Smith’s pygmy robber frog is along the southwestern portion of the Mexican<br />
Plateau, from Nayarit and Jalisco to Michoacán and the state of México. Its EVS has been determined as 15, placing it in the<br />
lower portion of the high vulnerability category, and its IUCN status as Endangered. This individual is from the Sierra de Manantlán<br />
in Jalisco. Photo by Iván Trinidad Ahumada-Carrillo.<br />
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Nonetheless, building a sustainable society requires<br />
steps that only a few people appear willing to take. Thus,<br />
efforts by conservation biologists to reverse biodiversity<br />
decline, including amphibian population decline, must<br />
proceed with the realization that we will only be designing<br />
short-term solutions that deal with the symptoms of<br />
the problems rather than their causes. Within this realization,<br />
we undertake the following reassessment of the<br />
conservation status of the amphibians of Mexico.<br />
A Revised Environmental Vulnerability<br />
Measure<br />
In conducting a conservation reassessment of Mexican<br />
reptiles, Wilson et al. (2013) revised the Environmental<br />
Vulnerability Score (EVS) from that used in various<br />
<br />
the EVS measure for use with Mexican amphibians, especially<br />
by substituting the human persecution scale used<br />
for reptiles with a reproductive mode scale, as did Wilson<br />
and McCranie (2004) and other authors who used this<br />
measure with Central American amphibians (see Wilson<br />
et al. 2010).<br />
Wilson et al. (2013) indicated that the EVS measure<br />
originally was designed for use in cases where the details<br />
of the population status of a species, upon which many<br />
of the criteria for IUCN status categorization depend,<br />
were not available, as well as to provide an estimate of<br />
the susceptibility of amphibians and reptiles to future environmental<br />
threats. The advantages for using the EVS<br />
measure are indicated below (see EVS for Mexican amphibians).<br />
The EVS algorithm we developed for use with Mexican<br />
amphibians consists of three scales, for which the<br />
values are added to produce the Environmental Vulner-<br />
bution,<br />
as follows:<br />
1 = distribution broadly represented both inside and<br />
outside Mexico (large portions of range are both<br />
inside and outside Mexico)<br />
2 = distribution prevalent inside Mexico, but limited<br />
outside Mexico (most of range is inside Mexico)<br />
3 = distribution limited inside Mexico, but prevalent<br />
outside Mexico (most of range is outside Mexico)<br />
4 = distribution limited both inside and outside Mexico<br />
(most of range is marginal to areas near border<br />
of Mexico and the United States or Central<br />
America)<br />
5 = distribution within Mexico only, but not restricted<br />
to vicinity of type locality<br />
6 = distribution limited to Mexico in the vicinity of<br />
type locality<br />
The second scale deals with ecological distribution, as<br />
follows:<br />
1 = occurs in eight or more formations<br />
2 = occurs in seven formations<br />
3 = occurs in six formations<br />
<br />
5 = occurs in four formations<br />
6 = occurs in three formations<br />
7 = occurs in two formations<br />
8 = occurs in one formation<br />
The third scale is concerned with the type of reproductive<br />
mode, as follows:<br />
1 = both eggs and tadpoles in large to small bodies of<br />
lentic or lotic water<br />
2 = eggs in foam nests, tadpoles in small bodies of<br />
lentic or lotic water<br />
3 = tadpoles occur in small bodies of lentic or lotic<br />
water, eggs outside of water<br />
4 = eggs laid in moist situation on land or moist arboreal<br />
situations, direct development, or viviparous<br />
5 = eggs and tadpoles in water-retaining arboreal bro-<br />
<br />
Once these three components are added, their EVS can<br />
range from 3 to 19. Wilson and McCranie (2004) allocated<br />
the range of scores for Honduran amphibians into<br />
three categories of vulnerability to environmental degradation,<br />
as follows: low (3–9); medium (10–13); and high<br />
(14–19). We use the same categorization.<br />
Recent Changes to the Mexican Amphibian<br />
Fauna<br />
Our knowledge of the composition of the Mexican amphibian<br />
fauna keeps changing due to discovery of new<br />
species and the systematic adjustment of certain known<br />
species, which adds or subtracts from the list of taxa that<br />
appeared in Wilson et al. (2010). Since that time, the following<br />
seven species have been described or resurrected:<br />
Incilius aurarius: Mendelson et al. 2012. Journal of<br />
Herpetology 46: 473–479. New species.<br />
Incilius mccoyi: Santos-Barrera and Flores Villela.<br />
2011. Journal of Herpetology 45: 211–215. New species.<br />
Craugastor saltator: Hedges et al. 2008. Zootaxa<br />
1737: 1–182. Resurrected from synonymy of C. mexicanus.<br />
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Eleutherodactylus modestus. The endemic blunt-toed chirping frog is known from Colima and southwestern Jalisco. Its EVS has<br />
been calculated at 16, placing it in the middle portion of the high vulnerability category, and its IUCN status as Vulnerable. This<br />
individual is from the Sierra de Manantlán in Jalisco. Photo by Iván Trinidad Ahumada-Carrillo.<br />
Dendropsophus sartori. <br />
EVS has been determined as 14, at the lower end of the high vulnerability category, and its IUCN status as of Least Concern. This<br />
individual came from the Municipality of Minatitlán, Colima. Photo by Jacobo Reyes-Velasco.<br />
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Charadrahyla tecuani: Campbell et al. 2009. Copeia<br />
2009: 287–295. New species.<br />
Gastrophryne mazatlanensis: Streicher et al. 2012.<br />
Molecular Phylogenetics and Evolution 64: 645–653.<br />
Resurrected from synonymy of G. olivacea.<br />
Bolitoglossa chinanteca: Rovito et al. 2012. ZooKeys<br />
185: 55–71. New species.<br />
Pseudoeurycea cafetalera: Parra-Olea et al. 2010.<br />
Zootaxa 2725: 57–68. New species.<br />
This represents an increase of 2.0% over the 373 species<br />
listed by Wilson and Johnson (2010).<br />
The following species have undergone status changes,<br />
and include some taxa discussed in the addendum to Wilson<br />
and Johnson (2010):<br />
Diaglena spatulata: Smith et al. 2007. Evolution 61:<br />
2075–2085. Transfer from genus Triprion.<br />
Hypopachus ustus: Streicher et al. 2012. Molecular<br />
Phylogenetics and Evolution 64: 645–653. Transfer<br />
from genus Gastrophryne<br />
corrected by Frost (2013).<br />
Trachycephalus typhonius: Lavilla et al. 2010. Zootaxa<br />
2671: 17–30. New name for T. venulosus.<br />
Ixalotriton niger: Wake. 2012. Zootaxa 3484: 75–82.<br />
Resurrection of genus.<br />
Ixalotriton parva: Wake. 2012. Zootaxa 3484: 75–82.<br />
Resurrection of genus.<br />
IUCN Red List Assessment of Mexican<br />
Amphibians<br />
The IUCN assessment of Mexican amphibians was conducted<br />
as part of a Mesoamerican Workshop held in 2002<br />
at the La Selva Biological Station in Costa Rica (see foreword<br />
in Köhler 2011). The results of this workshop were<br />
incorporated into a general worldwide overview called<br />
the Global Amphibian Assessment (Stuart et al. 2004;<br />
Stuart et al. 2008; Stuart et al. 2010). This overview uncovered<br />
startling conclusions, of which the most important<br />
was that nearly one-third (32.3%) of the world’s amphibian<br />
species are threatened with extinction, i.e., were<br />
assessed as Critically Endangered, Endangered, or Vulnerable.<br />
This proportion did not include 35 species considered<br />
as Extinct or Extinct in the Wild, and by adding<br />
them 1,891 of 5,743 species (32.9%) were considered as<br />
Table 1. IUCN Red List categorizations for Mexican amphibian families.<br />
Families<br />
Number of<br />
species<br />
Critically<br />
Endangered<br />
Endangered<br />
IUCN Red List categorizations<br />
Vulnerable<br />
Near<br />
Threatened<br />
Least<br />
Concern<br />
Data<br />
<br />
Not<br />
Evaluated<br />
35 1 7 2 3 19 1 2<br />
Centrolenidae 1 — — — — 1 — —<br />
Craugastoridae 39 7 8 7 3 6 6 2<br />
Eleutherodactylidae 23 2 4 7 — 4 5 1<br />
Hylidae 97 29 18 10 4 25 8 3<br />
Leiuperidae 1 — — — — 1 — —<br />
Leptodactylidae 2 — — — — 2 — —<br />
Microhylidae 6 — — 1 — 4 — 1<br />
Ranidae 28 4 2 5 2 12 2 1<br />
Rhinophrynidae 1 — — — — 1 — —<br />
Scaphiopodidae 4 — — — — 2 — 2<br />
Subtotals 237 43 39 31 12 77 22 12<br />
Ambystomatidae 18 9 2 — — 2 3 2<br />
Plethodontidae 118 36 37 11 9 10 12 3<br />
Salamandridae 1 — 1 — — — — —<br />
Sirenidae 2 — — — — 2 — —<br />
Subtotals 139 45 40 11 9 14 15 5<br />
Dermophiidae 2 — — 1 — — 1 —<br />
Subtotals 2 — — 1 — — 1 —<br />
Totals 378 88 79 44 21 91 38 17<br />
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Smilisca dentata. The endemic upland burrowing treefrog occurs only in southwestern Aguascalientes and adjacent northern Jalisco.<br />
Its EVS has been assessed as 14, placing it at the lower end of the high vulnerability category, and its IUCN status as Endangered.<br />
This individual was found in the Municipality of Ixtlahuacán del Río, Jalisco. Photo by Jacobo Reyes-Velasco.<br />
Lithobates johni. Moore’s frog is an endemic anuran whose distribution is limited to southeastern San Luis Potosí, eastern Hidalgo,<br />
and northern Puebla. Its EVS has been assessed as 14, placing it at the lower end of the high vulnerability category, and its IUCN<br />
status as Endangered. This individual came from Río Claro, Municipality of Molango, Hidalgo. Photo by Uriel Hernández-Salinas.<br />
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threatened, near extinction, or extinct. Notably, another<br />
<br />
i.e., too poorly known to allocate to any of the other<br />
IUCN categories. By adding these species to the previous<br />
cies<br />
(3,181 [55.4%]) known at that time were considered<br />
threatened, near extinction, extinct, or too poorly known<br />
<br />
worldwide cottage industry that continues to evaluate the<br />
state of amphibian population decline, as registered in<br />
a number of websites, most prominently AmphibiaWeb<br />
and the Global Amphibian Assessment.<br />
The IUCN Red List website lists the current categorizations<br />
for the world’s amphibians using the standard<br />
IUCN system. We accessed this website in order to summarize<br />
the current situation for Mexican amphibians<br />
(Table 1). The data in this table are more complete than<br />
those for reptiles, as reported by Wilson et al. (2013). All<br />
but 17 of the current 378 known Mexican amphibian species<br />
have been assigned to an IUCN category, and as for<br />
the reptiles (see Wilson et al. 2013) we placed these 17<br />
amphibian taxa (4.5%) in a Not Evaluated (NE) category.<br />
The remaining categorizations are: Critically Endangered<br />
(CR; 88; 23.2%); Endangered (EN; 79; 20.8%); Vulnerable<br />
(VU; 44; 11.6%); Near Threatened (NT; 21; 5.5%);<br />
<br />
38; 10.0%). Thus, 211 species (55.7%) are placed in one<br />
of the three threat categories (CR, EN, or VU), a propor-<br />
egories<br />
on a global scale (CR+EN+VU = 1,856 species,<br />
32.3%; Stuart et al., 2010). If the DD species are added to<br />
those in the threat categories, then 249 (65.7%) are either<br />
threatened with extinction or too poorly known to allow<br />
<br />
the global situation (CR+EN+VU+DD = 3,146 species;<br />
54.8%; Stuart et al. 2010).<br />
The largest proportion of threatened species are in<br />
the anuran families Craugastoridae (22 of 39 species;<br />
56.4%), Eleutherodactylidae (13 of 24 species; 54.2%),<br />
and Hylidae (57 of 97 species; 58.8%), and the salamander<br />
families Ambystomatidae (11 of 19 species; 57.9%)<br />
and Plethodontidae (84 of 118 species; 71.2%). Collec-<br />
<br />
78.4% of the amphibian taxa in Mexico, and the 187<br />
threatened species in these families comprise 88.6% of<br />
the 211 total.<br />
Table 2. Environmental Vulnerability Scores for Mexican amphibian species, arranged by family. Shaded area to left encompasses low vulnerability<br />
scores, and to the right high vulnerability scores.<br />
Families<br />
Number<br />
of species<br />
Environmental Vulnerability Scores<br />
3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19<br />
35 1 — 1 2 2 2 3 2 6 4 5 5 2 — — — —<br />
Centrolenidae 1 — — — — — — — 1 — — — — — — — — —<br />
Craugastoridae 39 — — — — — 1 1 1 1 1 4 4 10 3 5 8 —<br />
Eleutherodactylidae 23 — — — — — — — — 2 3 — — 3 4 8 3 —<br />
Hylidae 97 1 2 — — 4 4 7 5 9 11 16 22 12 1 1 1 1<br />
Leiuperidae 1 — — — — 1 — — — — — — — — — — — —<br />
Leptodactylidae 2 — — 1 1 — — — — — — — — — — — — —<br />
Microhylidae 6 — 1 — — 1 2 1 1 — — — — — — — — —<br />
Ranidae 28 1 — 1 — 1 2 2 2 2 5 4 5 3 — — — —<br />
Rhinophrynidae 1 — — — — — 1 — — — — — — — — — — —<br />
Scaphiopodidae 4 1 — — 1 — — — 1 — 1 — — — — — — —<br />
Subtotals 237 4 3 3 4 9 12 14 13 20 25 29 36 30 8 14 12 1<br />
Subtotals % — 1.7 1.3 1.3 1.7 3.8 5.1 5.9 5.4 8.4 10.5 12.2 15.2 12.7 3.4 5.9 5.1 0.4<br />
Ambystomatidae 18 — — — — — — — 2 — — 4 5 7 — — — —<br />
Plethodontidae 118 — — — — — — 1 — 2 3 3 8 16 13 36 36 —<br />
Salamandridae 1 — — — — — — — — — 1 — — — — — — —<br />
Sirenidae 2 — — — — — — — — — 2 — — — — — — —<br />
Subtotals 139 — — — — — — 1 2 2 6 7 13 23 13 36 36 —<br />
Subtotals % — — — — — — — 0.7 1.4 1.4 4.3 5.0 9.4 16.6 9.4 25.9 25.9 —<br />
Dermophiidae 2 — — — — — — — — 1 1 — — — — — — —<br />
Subtotals 2 — — — — — — — — 1 1 — — — — — — —<br />
Subtotals % — — — — — — — — — 50.0 50.0 — — — — — — —<br />
Totals 378 4 3 3 4 9 12 15 15 23 32 36 49 53 21 50 48 1<br />
Totals % — 1.1 0.8 0.8 1.1 2.3 3.2 4.0 4.0 6.1 8.4 9.5 12.9 14.0 5.6 13.2 12.7 0.3<br />
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Triprion petasatus. The Yucatecan casque-headed treefrog is restricted primarily to the Yucatan Peninsula, occurring in the Mexican<br />
states of Yucatán, Campeche, and Quintana Roo, as well as in northern Guatemala and northern Belize. A disjunct population also<br />
has been recorded from Santa Elena, Departamento de Cortés, Honduras. Its EVS has been calculated as 10, placing it at the lower<br />
end of the medium vulnerability category, and its IUCN status is of Least Concern. Although this treefrog is broadly distributed in<br />
the Yucatan Peninsula, it usually is found only during the rainy season when males and females congregate around restricted bodies<br />
<br />
tree holes and rock crevices, and sometimes use their head to plug the opening. This individual is from the state of Yucatán. Photo<br />
by Ed Cassano.<br />
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These data from the IUCN Red List show a frightening<br />
picture for the amphibian fauna of Mexico, acknowledged<br />
as a major herpetodiversity hotspot in the world<br />
on the basis of its diversity and endemism (Wilson and<br />
Johnson 2010). Mexico’s level of amphibian endemism<br />
(66.8%) also has been reported as greater than that for<br />
the country’s reptiles (57.2%; Wilson and Johnson 2010).<br />
Even more frightening is the fact that Mexican salamanders<br />
are more threatened than anurans (Table 1). Of the<br />
139 recognized species of salamanders, 96 (69.1%) were<br />
assessed into one of the threat categories, as compared<br />
to anurans (114 of 236 [48.3%]). In addition, a much<br />
smaller proportion of salamander species were judged as<br />
Least Concern (14 [10.1%]), as compared to anurans (78<br />
[33.1%]).<br />
Critique of the IUCN Assessment<br />
Although the conservation status of amphibians in Mexico<br />
is better understood than that for reptiles (see Wilson<br />
et al. 2013), a need for reassessment still is required<br />
for several reasons. About 10% of Mexico’s amphib-<br />
<br />
conservation status remains undetermined. In addition,<br />
because certain species have been described recently<br />
(see above), 4.5% have not been evaluated (see www.<br />
iucnredlist.org; accessed 08 May 2013). Also, by adding<br />
the DD and NE species, 55 (14.5%) of Mexico’s amphibians<br />
presently are not assigned to any of the other IUCN<br />
categories. Thus, we consider it worthwhile to subject the<br />
Mexican amphibians to the same assessment measure applied<br />
by Wilson et al. (2013) for reptiles, to allow for a<br />
comparison between these two groups. For these reasons,<br />
we will reassess the Mexican amphibian fauna using the<br />
Environmental Vulnerability Score (EVS).<br />
EVS for Mexican Amphibians<br />
The EVS provides several advantages for assessing the<br />
conservation status of amphibians and reptiles. First, this<br />
measure can be applied as soon as a species is named,<br />
because the information necessary for its application<br />
generally is known at that point. Second, calculating the<br />
EVS is economical because it does not require expensive,<br />
grant-supported workshops, such as those undertaken<br />
for the Global Amphibian Assessment (sponsored by<br />
the IUCN). Third, the EVS is predictive, as it measures<br />
susceptibility to anthropogenic pressure and can pinpoint<br />
taxa with the greatest need of immediate attention and<br />
continued scrutiny. Finally, it is simple to calculate and<br />
does not “penalize” poorly known species. Thus, given<br />
the geometric pace at which environmental threats worsen,<br />
since they are commensurate with the rate of human<br />
population growth, it is important to use a conservation<br />
assessment measure that can be applied simply, quickly,<br />
and economically.<br />
We calculated the EVS using the above-mentioned<br />
methodology. This step allowed us to determine the conservation<br />
status of all the currently recognized Mexican<br />
amphibian species (378), including the 55 species placed<br />
in the DD category or not evaluated by the IUCN (www.<br />
iucnredlist.org; see Appendix 1, Table 2).<br />
Theoretically, the EVS can range from 3 to 20 (in<br />
Mexico, from 3 to 19). A score of 3 is indicative of a species<br />
that ranges widely both within and outside of Mexico,<br />
occupies eight or more forest formations, and lays its<br />
eggs in small to large lentic or lotic bodies of water. Four<br />
such species (one each in the families Bufonidae, Hylidae,<br />
Ranidae, and Scaphiopodidae) are found in Mexico.<br />
At the other extreme, a score of 20 relates to a species<br />
that is known only from the vicinity of the type locality,<br />
occupies a single forest formation, and its eggs and tadpoles<br />
are found in water-retaining arboreal bromeliads or<br />
ico).<br />
Thus, all the scores fall within the range of 4–19.<br />
In the Introduction, we expressed an interest in attempting<br />
to determine the impact of small populations<br />
on amphibian species survival in Mexico. The data in<br />
Appendix 1 allow us to approximate an answer to this<br />
question, inasmuch as one of the components of the EVS<br />
assesses the extent of geographic distribution on a sliding<br />
scale (1–6), on which higher numbers signify increasingly<br />
smaller geographic ranges. Using this range, the<br />
distribution of the 378 Mexican species is as follows: 1 =<br />
13 species (3.4%); 2 = 20 (5.3%); 3 = 28 (7.4%); 4 = 64<br />
(16.9%); 5 = 126 (33.3%); and 6 = 127 (33.6%). Obviously,<br />
the higher the value of the geographic range, the<br />
higher the number and percentage of the taxa involved.<br />
ian<br />
species in Mexico are known only from the vicinity<br />
of their respective type localities. The range of another<br />
one-third is somewhat broader, but still limited to the<br />
pects<br />
of about two-thirds of Mexico’s amphibians are<br />
tied to changes in their natural environment, as well as to<br />
the conservation atmosphere in this nation.<br />
We summarized the EVS for Mexican amphibians by<br />
family in Table 2. The EVS range falls into the following<br />
three portions: low (3–9), medium (10–13), and high<br />
(14–19).<br />
The range and average EVS for the major amphibian<br />
groups are as follows: anurans = 3–19 (12.4); salamanders<br />
= 9–18 (15.9); and caecilians = 11–12 (11.5).<br />
<br />
than anurans to environmental degradation and caecilians<br />
somewhat less susceptible than anurans (although<br />
only two caecilian species are involved). The average<br />
scores either fall in the medium category, in the case of<br />
anurans and caecilians, or in the middle portion of the<br />
high category, in the case of salamanders. The average<br />
EVS for all amphibian species is 13.7, a value near the<br />
lower end of the high range of vulnerability.<br />
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Ambystoma velasci. The endemic Plateau tiger salamander, as currently recognized, is distributed widely from northwestern Chihuahua<br />
southward along the eastern slopes of the Sierra Madre Oriental, and from southern Nuevo León in the Sierra Madre Oriental,<br />
westward to Zacatecas and southward onto the Transverse Volcanic Axis of central Mexico. Its EVS has been determined<br />
as 10, placing it at the lower end of the medium vulnerability category, and its IUCN status is of Least Concern. Even though this<br />
species does not appear threatened, this is likely an artifact of the composite nature of this taxon. This individual was found at Santa<br />
Cantarina, Hidalgo. Photo by Raciel Cruz-Elizalde.<br />
Bolitoglossa franklini. <br />
south-central Guatemala. Its EVS has been determined as 14, placing it at the lower end of the high vulnerability category, and its<br />
IUCN status as Endangered. This individual came from Cerro Mototal, in the Municipality of Motozintla, Chiapas. Photo by Sean<br />
M. Rovito.<br />
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An EVS of 14, at the lower end of the high vulnerability<br />
category, was found in the highest percentage (15.2)<br />
of anuran species. For salamanders, the respective values<br />
are 25.9% for an EVS of both 17 and 18, near the upper<br />
end of the range for the high vulnerability category, and<br />
for caecilians 50.0% for an EVS of both 11 and 12.<br />
The total EVS scores generally increased from the<br />
low end of the scale (3) through most of the high end<br />
(14–18), with a single exception (a decrease from 53 to<br />
21 species at scores 15 and 16). An EVS of 15 was found<br />
in the peak number of taxa (53), a score that falls within<br />
the high range of vulnerability.<br />
Of the 378 total taxa, 50 (13.2%) fall into the low<br />
vulnerability category, 106 (28.0%) into the medium<br />
category, and 222 (58.7%) into the high category. Thus,<br />
six of every 10 Mexican amphibian species were judged<br />
as having the highest degree of vulnerability to environmental<br />
degradation, and slightly more than one-seventh<br />
the lowest degree.<br />
This considerable increase in the absolute and relative<br />
numbers from the low portion, through the medium<br />
portion, to the high portion differs somewhat from the<br />
results published for amphibians and reptiles for several<br />
Central American countries in Wilson et al. (2010).<br />
Acevedo et al. (2010) reported 89 species (23.2%) with<br />
low scores, 179 (46.7%) with medium scores, and 115<br />
(30.0%) with high scores for Guatemala. The same trend<br />
was reported for Honduras, where Townsend and Wilson<br />
(2010) indicated the corresponding values for amphibians<br />
and reptiles as 71 (19.7%), 169 (46.8%), and 121<br />
(33.5%). The comparable data for the Panamanian herpetofauna<br />
in Jaramillo et al. (2010) are 143 (33.3%), 165<br />
(38.4%), and 122 (28.4%).<br />
The principal reason that EVS scores are relatively<br />
high in Mexico is because of the high level of endemism<br />
and the concomitantly narrow range of geographical and<br />
ecological occurrence (Appendix 1). Of the 253 endemic<br />
amphibian species (139 anurans, 113 salamanders, and<br />
one caecilian), 125 (49.4%) were allocated a geographic<br />
distribution score of 6, signifying that these creatures<br />
are known only from the vicinity of their respective type<br />
localities; the remainder of the endemic species (128<br />
[50.6%]) are more broadly distributed within the country<br />
(Appendix 1).<br />
Of the 378 Mexican amphibian species, 128 (33.9%)<br />
are limited in ecological distribution to one formation<br />
(Appendix 1). Therefore, we emphasize that close to onehalf<br />
of the country’s endemic amphibian species are not<br />
known to occur outside of the vicinity of their type localities.<br />
In addition, essentially one-third are not known to<br />
occur outside of a single forest formation. This situation<br />
imposes serious challenges in our attempt to conserve the<br />
endemic component of the strikingly important Mexican<br />
amphibian fauna.<br />
Comparison of IUCN Categorizations and<br />
EVS Values<br />
Table 3. Comparison of Environmental Vulnerability Scores (EVS) and IUCN categorizations for Mexican amphibians. Shaded<br />
area at the top encompasses low vulnerability category scores, and that at the bottom high vulnerability category scores.<br />
EVS<br />
Critically<br />
Endangered<br />
Endangered<br />
Vulnerable<br />
IUCN categories<br />
Near<br />
Threatened<br />
Least<br />
Concern<br />
Data<br />
<br />
Not<br />
Evaluated<br />
3 — — — — 4 — — 4<br />
4 — — — — 3 — — 3<br />
5 — — — — 3 — — 3<br />
6 — — — — 3 — 1 4<br />
7 1 — — — 8 — — 9<br />
8 — — 2 2 6 — 2 12<br />
9 1 1 1 1 10 — 1 15<br />
10 1 2 1 — 9 — 2 15<br />
11 1 2 7 — 13 — — 23<br />
12 5 4 3 4 13 2 1 32<br />
13 4 12 5 5 6 3 1 36<br />
14 12 11 7 2 8 6 3 49<br />
15 22 8 5 2 3 10 3 53<br />
16 4 9 4 2 1 1 — 21<br />
17 15 17 6 2 1 7 2 50<br />
18 21 13 3 1 — 9 1 48<br />
19 1 — — — — — — 1<br />
Totals 88 79 44 21 91 38 17 378<br />
Totals<br />
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Ixalotriton niger. The black jumping salamander is known only from the immediate vicinity of the type locality in northwestern<br />
Chiapas. Its EVS has been calculated as 18, placing it in the upper portion of the high vulnerability category, and its IUCN status<br />
as Critically Endangered. This individual came from the type locality and was used as part of the type series in the description of<br />
the species by Wake and Johnson (1989). The genus Ixalotriton is endemic to Mexico, and contains one other species (I. parvus).<br />
Photo by David B. Wake.<br />
Pseudoeurycea longicauda. The endemic long-tailed false brook salamander is distributed in the Transverse Volcanic Axis of eastern<br />
Michoacán and adjacent areas in the state of México. Its EVS has been determined as 17, placing it in the middle of the high<br />
vulnerability category, and its IUCN status as Endangered. This individual came from Zitácuaro, Michoacán, near the border with<br />
the state of México. Photo by Iván Trinidad Ahumada-Carrillo.<br />
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We noted in Wilson et al. (2013: 18) that, “Since the<br />
IUCN categorizations and EVS values both measure the<br />
degree of environmental threat impinging on a given species,<br />
a certain degree of correlation between the results,<br />
using the two measures, is expected.” They further indicated<br />
that Townsend and Wilson (2010) demonstrated<br />
this to be the case with the Honduran herpetofauna. Wilson<br />
et al. (2013: 22) concluded, however, that, “the results<br />
of the EVS analysis are nearly the reverse of those<br />
obtained from the IUCN categorizations.”<br />
We compared the results of these two conservation<br />
measures in Table 3, expecting that our results for the<br />
Mexican amphibians would be more consistent with those<br />
obtained for the Honduran herpetofauna (Townsend and<br />
Wilson 2010) than those garnered for the Mexican reptiles<br />
(Wilson et al. 2013).<br />
1. Nature of the IUCN categorizations in<br />
Table 3<br />
Like Wilson et al. (2013), we used the “Not Evaluated”<br />
category (IUCN 2010), since 17 species (4.5%) have<br />
not been evaluated at the IUCN Red List website, and<br />
<br />
iucnredlist.org; accessed 08 May 2013). Thus, the IUCN<br />
conservation status of 55 (14.6%) of the total amphibian<br />
species remained undetermined. A greater proportion of<br />
the Mexican amphibians, however, were assessed based<br />
on the IUCN categorizations (323 species [85.4%]) than<br />
the Mexican reptiles (Wilson et al. 2013).<br />
2. Pattern of mean EVS vs. IUCN<br />
categorizations<br />
In order to more precisely determine the relationship between<br />
the IUCN categorizations and the EVS, we calculated<br />
the mean EVS for each of the IUCN columns<br />
in Table 3, including for the NE species and the total<br />
species. The results are as follows: CR (88 spp.) = 15.5<br />
(range 7–19); EN (79 spp.) = 15.1 (9–18); VU (44 spp.)<br />
= 13.8 (8–18); NT (21 spp.) = 13.3 (8–18); LC (91 spp.)<br />
= 10.0 (3–17); DD (38 spp.) = 15.6 (12–18); NE (17 spp.)<br />
= 12.6 (6–18); and total (378 spp.) = 13.7 (3–19). The<br />
results of these data show that the mean EVS decreases<br />
steadily from the CR category (15.5) through the EN<br />
(15.1), VU (13.8), and NT (13.3) categories to the LC<br />
category (10.0). This pattern of decreasing values was<br />
expected. In addition, the mean value for the DD species<br />
(15.6) is closest to that for the CR species. As we stated<br />
with regard to Mexican reptiles (Wilson et al. 2013: 22),<br />
“this indicates what we generally have suspected about<br />
the DD category, i.e., that the species placed in this category<br />
likely will fall into the EN or CR categories when<br />
(and if) their conservation status is better understood.<br />
termining<br />
their conservation status, however, since once<br />
<br />
to be downplayed.” Wilson et al. (2013) demonstrated<br />
<br />
reptiles, given that 118 species were evaluated as DD,<br />
which provided the impetus to work on the 38 amphibian<br />
Table 4. Comparison of Environmental Vulnerability Scores for Mexican amphibian and reptile species, arranged by major groups. Shaded area to the<br />
left encompasses low vulnerability scores, and to the right high vulnerability scores.<br />
<br />
Number of<br />
Environmental Vulnerability Scores<br />
species 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20<br />
Anurans 237 4 3 3 4 9 12 14 13 20 25 29 36 30 8 14 12 1 —<br />
Percentages — 1.7 1.3 1.3 1.7 3.8 5.1 5.9 5.4 8.4 10.5 12.2 15.2 12.7 3.4 5.9 5.1 0.4 —<br />
Salamanders 139 — — — — — — 1 2 2 6 7 13 23 13 36 36 — —<br />
Percentages — — — — — — — 0.7 1.4 1.4 4.3 5.0 9.4 16.6 9.4 25.9 25.9 — —<br />
Caecilians 2 — — — — — — — — 1 1 — — — — — — — —<br />
Percentages — — — — — — — — — 50.0 50.0 — — — — — — — —<br />
Amphibian Totals 378 4 3 3 4 9 12 15 15 23 32 36 49 53 21 50 48 1 —<br />
Percentages — 1.0 0.8 0.8 1.0 2.4 3.2 4.0 4.0 6.1 8.5 9.5 13.0 14.0 5.5 13.2 12.7 0.3 —<br />
Crocodilians 3 — — — — — — — — — — 1 1 — 1 — — — —<br />
Percentages — — — — — — — — — — — 33.3 33.3 — 33.3 — — — —<br />
Turtles 42 — — — — — 1 — 3 1 1 3 8 6 4 3 5 6 1<br />
Percentages — — — — — — 2.4 — 7.1 2.4 2.4 7.1 19.0 14.3 9.5 7.1 11.9 14.3 2.4<br />
Lizards 409 — — 1 3 6 11 12 15 26 39 49 54 67 77 37 10 2 —<br />
Percentages — — — 0.2 0.7 1.5 2.7 2.9 3.7 7.1 9.5 12.0 13.2 16.4 18.8 9.0 2.4 0.5 —<br />
Snakes 382 1 1 7 10 9 19 17 30 25 31 46 52 50 44 24 9 7 —<br />
Percentages — 0.3 0.3 1.8 2.6 2.4 5.0 4.5 7.9 6.5 8.1 12.0 13.6 13.1 11.5 6.3 2.4 1.8 —<br />
Reptile Totals 836 1 1 8 13 15 31 30 46 53 71 99 115 123 126 64 24 15 1<br />
Percentages — 0.1 0.1 1.0 1.6 1.8 3.7 3.6 5.5 6.3 8.5 11.8 13.8 14.7 15.1 7.8 2.9 1.8 0.1<br />
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Dermophis oaxacae. The endemic Oaxacan caecilian is distributed in Colima, Jalisco, Michoacán, Guerrero, Oaxaca, and Chiapas.<br />
Its EVS has been calculated as 12, placing it in the middle portion of the medium vulnerability category, and its IUCN status as Data<br />
Photo by Jacobo Reyes-Velasco.<br />
species assessed as DD with those occupying the threat<br />
categories (CR, EN, and VU) to arrive at a total of 249<br />
species (65.9% of the total amphibian fauna). The EVS<br />
range for these DD species (12–18) falls within that for<br />
the threat species as a whole (7–19) and the mean for all<br />
the four categories becomes 15.1, the same as that for the<br />
EN species alone. So, if the DD species can be considered<br />
“threat species in disguise,” then close to two-thirds<br />
of the Mexican amphibian species would be considered<br />
under the threat of extinction.<br />
The EVS for the 17 Mexican amphibian species that<br />
have not been evaluated by the IUCN range from 6 to 18<br />
tion<br />
interest, inasmuch as the EVS of nine of them falls<br />
into the range of high vulnerability.<br />
Based on the pattern of relationships between the LC<br />
species and their corresponding EVS, this IUCN category<br />
apparently has become a “dumping ground” for a<br />
sizable number of Mexican amphibians (91; 24.1% of the<br />
amphibian fauna) and like Wilson et al. (2013: 22) concluded<br />
for Mexican reptiles, we concur that “A more discerning<br />
look at both the LC and NE species might demonstrate<br />
that many should be partitioned into other IUCN<br />
categories, rather than the LC.” The range of EVS values<br />
for this category (3–17) is almost as broad as the range<br />
of EVS (3–19) for amphibians as a whole; 37 (40.7%)<br />
of these 91 species are relegated to the low vulnerability<br />
range (3–9), 41 (45.0%) to the medium vulnerability<br />
range, and 13 (14.3%) to the high vulnerability range.<br />
Again, these results indicate that the LC category likely<br />
has been used rather indiscriminately and that the EVS<br />
algorithm provides a more useful conservation measure<br />
than the IUCN system of categories.<br />
Comparison of EVS Values for Mexican<br />
Amphibians and Reptiles<br />
One of our major reasons for writing this paper was to<br />
determine the EVS values for Mexican amphibians, so<br />
they could be compared to those calculated for Mexican<br />
reptiles in Wilson et al. (2013). Thus, we summarized<br />
the data in Table 2, and reduced them to the major group<br />
level in Table 4. We also reduced the data in Wilson et al.<br />
(2013: table 2) and placed them in our Table 4.<br />
The data in this table indicate that the range of EVS<br />
values are comparable for amphibians (3–19) and reptiles<br />
(3–20). The EVS for the number of amphibian species<br />
essentially increases until a score of 15 is reached<br />
(53 species), and at 16 drops considerably (21 species)<br />
only to spike back up at 17 and 18 (50 and 48 species,<br />
respectively). The highest EVS value (19) was assigned<br />
to a single species (the fringe-limbed hylid Ecnomiohyla<br />
echinata). For the reptiles, the numbers and percentages<br />
also increase, with the peak (126 [15.1%]) reached at an<br />
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EVS of 16, and decreasing rapidly thereafter. As with<br />
amphibians, only a single species (the soft-shelled turtle<br />
Apalone atra) was assigned the highest EVS (20).<br />
When the EVS values are arranged into low, medium,<br />
and high categories, the numbers and percentages of species<br />
are as follows (amphibians, followed by reptiles):<br />
low = 50 (13.2%), 99 (11.8%); medium = 106 (28.0%),<br />
269, (32.2%); and high = 222 (58.8%), 468, (56.0%).<br />
The percentages for these two groups are comparable and<br />
arranged in the same order. The greatest concern is that<br />
in both amphibians and reptiles more than one-half of the<br />
species fall into the upper portion of the high vulnerability<br />
category, indicating that the Mexican herpetofauna is<br />
seriously imperiled.<br />
Of the major groups of amphibians and reptiles, Mexican<br />
salamanders were judged the most imperiled. Of the<br />
139 species known from the country, 121 (87.1%) were<br />
assessed in the high vulnerability category. The compa-<br />
<br />
half of that for salamanders. Among the reptiles, lizards<br />
were judged more threatened than snakes. Of the lizards,<br />
247 (60.4%) fall within the high vulnerability category;<br />
<br />
Turtles, although fewer in numbers, are more threatened<br />
than other reptiles, with 33 species (78.6%) in the high<br />
vulnerability category.<br />
knowledged<br />
widely as threatened on a global basis, a fair<br />
accounting of the worldwide conservation status of most<br />
reptiles remains unavailable. Our use of the EVS measure<br />
for Mexican amphibians and reptiles demonstrates<br />
that both groups are in grave peril, and we expect that<br />
this situation will worsen exponentially in the coming<br />
decades.<br />
Discussion<br />
Global amphibian population decline has occupied the<br />
attention of herpetologists since the late 1980s (Gascon<br />
et al. 2007). In the years that followed, the Global<br />
Amphibian Assessment (GAA) was undertaken (Stuart<br />
et al. 2004), which uncovered the startling conclusions<br />
discussed in the Introduction. As noted in the foreword<br />
<br />
the breadth of amphibian losses worldwide and made it<br />
clear that business as usual—the customary conservation<br />
approaches and practices—were not working.” As<br />
a result, an Amphibian Conservation Summit was convened<br />
in September 2005, which resulted in a putatively<br />
comprehensive Amphibian Conservation Action Plan<br />
(ACAP; Gascon et al. 2007). The ACAP declaration proposed<br />
(p. 59) that, “Four kinds of intervention are needed<br />
to conserve amphibians, all of which need to be started<br />
immediately:<br />
1. Expanded understanding of the causes of declines<br />
and extinctions<br />
2. Ongoing documentation of amphibian diversity,<br />
and how it is changing<br />
3. Development and implementation of long-term<br />
conservation programmes<br />
4. Emergency responses to immediate crises.”<br />
We maintain that the ACAP does an admirable job of examining<br />
many of the issues directly related to amphibian<br />
decline, but this examination essentially stops after considering<br />
the proximate symptoms of the problem. Nonetheless,<br />
as noted by Wilson and Townsend (2010: 774),<br />
“problems created by humans, i.e., overpopulation and<br />
its sequelae, are not solved by treating only their symptoms,<br />
e.g., organismic endangerment.” Consequently,<br />
trying to deal with a symptom of overpopulation and<br />
resource overuse and abuse, such as amphibian decline,<br />
will create only limited short-term responses, instead of<br />
lasting solutions to the fundamental problems tied to the<br />
impact of humans. Thus, ultimately, amphibian decline<br />
will not be successfully addressed.<br />
The fundamental problem is that humans have not<br />
created a sustainable existence for themselves. Understanding<br />
why not is simple through examination of the<br />
principles of sustainability elaborated by Miller and<br />
Spoolman (2012: 6), as follows:<br />
<br />
relying on solar energy, biodiversity, and nutrient cycling.<br />
<br />
the sun and on natural resources and natural services<br />
(natural capital) provided by the earth.<br />
<br />
and degrading more of the earth’s natural capital.<br />
tion<br />
growth, wasteful and unsustainable resource use,<br />
poverty, and not including the harmful environmental<br />
costs of resource use in the market prices of goods<br />
and services.<br />
<br />
determining whether we live unsustainably or more<br />
sustainably.<br />
ral<br />
income without depleting or degrading the natural<br />
capital that supplies it.”<br />
Living unsustainably is a consequence of unregulated<br />
human population growth that generates the overuse and<br />
abuse of renewable and non-renewable resources, and<br />
dependence on a cost-accounting system that ignores<br />
factoring in clean up expenses in determining how goods<br />
and services are priced. Life-sustaining resources are not<br />
distributed equitably among people, but along a scale<br />
ranging from very high to very low. Poverty is the consequence<br />
of existing at the low end of the scale, where people<br />
are unable to meet their basic needs for adequate food<br />
and water, clothing, or shelter (Raven and Berg 2004).<br />
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Environmental scientists use the concept of ecological<br />
footprint to express “the average amount of land and<br />
ocean needed to supply an individual with food, energy,<br />
water, housing, transportation, and waste disposal” (Raven<br />
and Berg 2004: G-5). The global ecological footprint<br />
has increased over the years to the point that the Global<br />
Footprint Network calculated it would take “1.5 years to<br />
generate the renewable resources used in 2008” (WWF<br />
Living Planet Report 2012: 40). “Humanity’s annual demand<br />
on the natural world has exceeded what the Earth<br />
can renew in a year since the 1970s,” which has created<br />
a so-called “ecological overshoot” (WWF Living Planet<br />
Report 2012: 40). Thus, Earth’s capital (its biocapacity)<br />
is being depleted on a continually growing basis, and the<br />
planet is becoming less capable of supporting life in general,<br />
and human life in particular. Estimates indicate that<br />
by the year 2050, under a “business as usual” scenario, it<br />
would require an equivalent of 2.9 planets to support the<br />
amount of humanity expected to exist at that time (WWF<br />
Living Planet Report 2012: 101).<br />
The World Wildlife Fund promulgated its “One Planet<br />
perspective,” which “explicitly proposes to manage, govern<br />
and share natural capital within the Earth’s ecological<br />
boundaries. In addition to safeguarding and restoring<br />
this natural capital, WWF seeks better choices along the<br />
entire system of production and consumption, supported<br />
<br />
governance. All of this, and more, is required to decouple<br />
human development from unsustainable consumption<br />
(moving away from material and energy-intensive<br />
commodities), to avoid greenhouse gas emissions, to<br />
maintain ecosystem integrity, and to promote pro-poor<br />
growth and development” (WWF Living Planet Report<br />
2012: 106).<br />
Only within this context will the provisions of ACAP<br />
have the desired effects, i.e., to preserve the portion of<br />
natural capital represented by amphibians. Thus, in writing<br />
about the conservation status of the amphibians of<br />
Mexico, we are constructing our conclusions and recommendations<br />
in light of these global imperatives.<br />
Conclusions and Recommendations<br />
We structured our conclusions and recommendations after<br />
those of Wilson and Townsend (2010) for the entire<br />
<br />
for the Mexican amphibian fauna, as follows:<br />
1. Given that Mexico contains the highest level of<br />
amphibian diversity and endemicity in the Mesoamerican<br />
biodiversity hotspot, our most fundamental<br />
recommendation is that protection of this<br />
aspect of the Mexican patrimony should be made<br />
a major component of the management strategy of<br />
the Secretaría de Medio Ambiente y Recursos Naturales<br />
(SEMARNAT). In turn, that strategy needs<br />
to be incorporated into an overall plan for a sustainable<br />
future for Mexico, of which the most critical<br />
component is to “explicitly integrate population<br />
dynamics (size, growth rate, composition, location<br />
and migration) and per capita consumption trends<br />
into national planning policies to support a better<br />
balance between population and available resources”<br />
(WWF Living Planet Report 2012: 121).<br />
2. All organisms have intrinsic and extrinsic value,<br />
especially as components of healthily functioning<br />
ecosystems, but we believe that although conservation<br />
efforts should extend to all species in a given<br />
area, most interest should be focused on species<br />
with a limited distribution (i.e., endemic species).<br />
The rationale for this position is that funds to support<br />
conservation initiatives have remained scarce,<br />
although this situation will have to change in the<br />
near future. The principal regions of Mexican amphibian<br />
endemism are the Sierra Madre Oriental,<br />
the Sierra Madre del Sur, and the Mesa Central,<br />
in the order listed. Unfortunately, about 39% of<br />
Mexico’s population occupies the Mesa Central<br />
(Flores-Villela et al. 2010). Inasmuch as this concentrated<br />
population will continue to grow into the<br />
foreseeable future, not only as a consequence of<br />
the rate of natural increase (1.4% in Mexico), but<br />
also because of the increase in the percentage of<br />
the population attracted to the large cities of the<br />
Mesa Central (Guadalajara, León, México, Morelia,<br />
Salamanca, and others; Flores-Villela et al.<br />
2010), it is critically important to make the amphibian<br />
fauna of the Mesa Central a fundamental<br />
component of the national plan for biodiversity<br />
protection by SEMARNAT.<br />
3. Oscar Flores-Villela and his colleagues produced<br />
<br />
Villela 1993; Flores-Villela and Gerez 1994;<br />
Ochoa-Ochoa and Flores-Villela 2006; Flores-Villela<br />
et al. 2010) that have documented the centers<br />
of diversity and endemism of the Mexican herpetofauna.<br />
Given the large disparity between these<br />
centers and the placement of protected areas in<br />
the country, we can only echo the conclusions of<br />
Flores-Villela et al. (2010: 313) that, “Given the<br />
great importance of the herpetofauna of the Central<br />
Highlands of Mexico, both in terms of its diversity<br />
and endemicity, appropriate steps need to be taken<br />
quickly to establish protected areas around the center<br />
of herpetofaunal endemism in the Sierra Madre<br />
del Sur, and to reassess the ability of the protected<br />
areas already established in the Mesa Central to<br />
encompass their centers of endemism.” A similar<br />
recommendation can be made with respect to<br />
the other centers, e.g., the Sierra Madre Oriental,<br />
which has been even more ignored than areas in the<br />
Central Highlands (Lavín et al. 2010).<br />
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Wilson et al.<br />
4. Finding ways to use biodiversity sustainably must<br />
become a fundamental goal for all humanity. The<br />
<br />
to envision; the problem lies in marshaling the paradigm<br />
shift necessary to make the transition. The<br />
major steps involve: (a) creating a reality-based<br />
educational system that will prepare people for the<br />
world as it is and will come to be, instead of the<br />
way people wish it were; (b) integrating educational<br />
reform into a broad-based plan for governmental<br />
and economic reform founded on principles of<br />
equality, shared responsibility, and commitment to<br />
a sustainable future for humanity and the natural<br />
world; (c) using governmental and economic reform<br />
to design a global society structured to exist<br />
within the limits of nature; and (d) basing a society<br />
on the notion that everyone must work toward<br />
this end. Within such overarching goals, the task<br />
of learning the best way to catalogue, protect, and<br />
make sustainable use of the world’s organisms is a<br />
huge undertaking. New molecular-based technology,<br />
however, is allowing for a better understanding<br />
of biological diversity, which is much greater<br />
than we previously envisioned. Because of the accelerating<br />
rate at which we are losing biological diversity,<br />
biologists are faced with helping humanity<br />
adopt a worldview in which all species matter, and<br />
that the sustainability of humans will depend on<br />
reforming our society based on the framework for<br />
survival tested by the process of natural selection<br />
over the last 3.5 billion years life has occupied our<br />
planet (Beattie and Ehrlich 2004).<br />
5. In 2012, the United Nations Secretary-General’s<br />
High-level Panel on Global Sustainability produced<br />
a seminal report entitled “Resilient People,<br />
Resilient Planet: A Future Worth Choosing.” In a<br />
vision statement (p. 13), the panel introduced the<br />
concept of “tipping points,” as follows: “The current<br />
global development model is unsustainable.<br />
We can no longer assume that our collective actions<br />
will not trigger tipping points as environmental<br />
thresholds are breached, risking irreversible<br />
damage to both ecosystems and human communities.<br />
At the same time, such thresholds should not<br />
be used to impose arbitrary growth ceilings on developing<br />
countries seeking to lift their people out<br />
of poverty. Indeed, if we fail to resolve the sustainable<br />
development dilemma, we run the risk of<br />
condemning up to 3 billion members of our human<br />
family to a life of endemic poverty. Neither of<br />
<br />
new way forward.” The panel also pointed out (p.<br />
14) that “it is time for bold global efforts, includ-<br />
<br />
to strengthen the interface between science and<br />
entists<br />
refer to as ‘planetary boundaries,’ ‘environmental<br />
thresholds,’ and ‘tipping points.” On p. 23,<br />
they emphasize that, “awareness is growing of the<br />
potential for passing ‘tipping points’ beyond which<br />
environmental change accelerates, has the potential<br />
to become self-perpetuating, and may be dif-<br />
tal<br />
scientists have warned of this eventuality for<br />
decades; most of the world’s people just have not<br />
listened. The Stockholm Resilience Centre (www.<br />
stockholmresilience.org), however, has exposed<br />
<br />
certain thresholds or tipping points beyond which<br />
there is the “risk of irreversible and abrupt environmental<br />
change” (Box 2 on p. 24 of the UN panel report).<br />
The Stockholm Resilience Centre sponsored<br />
a group of scientists (Rockström et al. 2009) that<br />
<br />
“climate change, rate of biodiversity loss, biogeo-<br />
<br />
<br />
global freshwater use, change in land use, atmospheric<br />
aerosol loading and chemical pollution.”<br />
The scientists estimated that “human activity appears<br />
to have already transgressed the [planetary]<br />
boundaries associated with climate change, rate of<br />
biodiversity loss and changes to the global nitrogen<br />
cycle.” Furthermore, “humanity may soon be approaching<br />
the boundaries for interference with the<br />
global phosphorous cycle, global freshwater use,<br />
<br />
Finally, they concluded that, “the boundaries are<br />
strongly interlinked, so that crossing one may shift<br />
others and even cause them to be overstepped.”<br />
As a consequence of these realities, governments<br />
across the globe are faced with the choice of continuing<br />
to do “business as usual,” ultimately spilling<br />
over all the planetary boundaries and ending up<br />
in a world in which all of our options have been exhausted<br />
except for the last one…the option to fail,<br />
or to pull together to develop a human existence<br />
<br />
a “safe operating space for humanity.” Our chances<br />
to avoid the one and succeed with the other will<br />
depend on how well humanity is able to embrace<br />
new ways of thinking about our problems and enlist<br />
the help of groups of people who traditionally<br />
have been marginalized—especially women and<br />
the young. These words apply to Mexico, as they<br />
do to all other countries in the world.<br />
The three authors of this work are herpetologists who<br />
specialize in research on amphibians and reptiles in Mesoamerica.<br />
This paper focuses on the conservation status<br />
of the amphibians of Mexico, and follows a similar effort<br />
on the reptiles (Wilson et al. 2013). We demonstrated by<br />
using both the IUCN categorizations and EVS measure<br />
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Conservation reassessment of Mexican amphibians<br />
that the Mexican amphibian fauna is one of the most seriously<br />
threatened of any existing in the world. All indications<br />
suggest that humans have transgressed the planetary<br />
boundaries associated with biodiversity loss, and<br />
there is no time to lose to reverse this dismantling trend<br />
or our descendants will be left to conclude that our generation<br />
condemned them to an environmentally impover-<br />
<br />
manity’s<br />
job now is to survive the one of its own making.<br />
Acknowledgments.—We are thankful to the following<br />
individuals for improving the quality of this contribution:<br />
Javier Alvarado-Díaz, Irene Goyenechea, and Louis<br />
W. Porras. We are most grateful to Louis, who applied<br />
his amazing editing skills to the job of making our work<br />
better than what we initially produced.<br />
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Received: 05 March 2013<br />
Accepted: 26 April 2013<br />
Published: 02 August 2013<br />
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Conservation reassessment of Mexican amphibians<br />
Larry David Wilson is a herpetologist with lengthy experience in Mesoamerica, totaling six collective years<br />
(combined over the past 47). Larry is the senior editor of the recently published Conservation of Mesoamerican<br />
Amphibians and Reptiles and a co-author of seven of its chapters. He retired after 35 years of service as<br />
Professor of Biology at Miami-Dade College in Miami, Florida. Larry is the author or co-author of more than<br />
290 peer-reviewed papers and books on herpetology, including the 2004 Amphibian & Reptile Conservation<br />
paper entitled “The conservation status of the herpetofauna of Honduras.” His other books include The<br />
Snakes of Honduras, Middle American Herpetology, The Amphibians of Honduras, Amphibians & Reptiles<br />
of the Bay Islands and Cayos Cochinos, Honduras, The Amphibians and Reptiles of the Honduran Mosquitia,<br />
and Guide to the Amphibians & Reptiles of Cusuco National Park, Honduras. He also served as the Snake<br />
Section Editor for the Catalogue of American Amphibians and Reptiles for 33 years. Over his career, Larry<br />
has authored or co-authored the descriptions of 69 currently recognized herpetofaunal species and six species<br />
have been named in his honor, including the anuran Craugastor lauraster and the snakes Cerrophidion<br />
wilsoni, Myriopholis wilsoni, and Oxybelis wilsoni.<br />
Jerry D. Johnson is Professor of Biological Sciences at The University of Texas at El Paso, and has extensive<br />
experience studying the herpetofauna of Mesoamerica. He is the Director of the 40,000 acre “Indio<br />
Mountains Research Station,” was a co-editor on the recently published Conservation of Mesoamerican<br />
Amphibians and Reptiles, and is Mesoamerica/Caribbean editor for the Geographic Distribution section of<br />
Herpetological Review. Johnson has authored or co-authored over 80 peer-reviewed papers, including two<br />
2010 articles, “Geographic distribution and conservation of the herpetofauna of southeastern Mexico” and<br />
“Distributional patterns of the herpetofauna of Mesoamerica, a biodiversity hotspot.”<br />
Vicente Mata-Silva is a herpetologist interested in ecology, conservation, and the monitoring of amphibians and<br />
reptiles in Mexico and the southwestern United States. His bachelor’s thesis compared herpetofaunal richness<br />
in Puebla, México, in habitats with different degrees of human related disturbance. Vicente’s master’s thesis<br />
focused primarily on the diet of two syntopic whiptail species of lizards, one unisexual and the other bisexual,<br />
in the Trans-Pecos region of the Chihuahuan Desert. Currently, he is a postdoctoral research fellow at the<br />
University of Texas at El Paso, where his work focuses on rattlesnake populations in their natural habitat. His<br />
dissertation was on the ecology of the rock rattlesnake, Crotalus lepidus, in the northern Chihuahuan Desert.<br />
<br />
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Species<br />
Wilson et al.<br />
Appendix 1. Comparison of the IUCN Ratings from the Red List Website (updated to 08 May 2013) and Environmental<br />
Vulnerability Scores for 378 Mexican Amphibians. See text for explanations of the IUCN and EVS rating systems. * =<br />
species endemic to Mexico.<br />
IUCN<br />
rating<br />
Geographic<br />
Distribution<br />
Environmental Vulnerability Score<br />
Ecological<br />
Distribution<br />
Reproductive<br />
Mode<br />
Total Score<br />
Order Anura (237 species)<br />
<br />
Anaxyrus boreus NT 3 4 1 8<br />
Anaxyrus californicus EN 4 7 1 12<br />
Anaxyrus cognatus LC 3 5 1 9<br />
Anaxyrus compactilis* LC 5 8 1 14<br />
Anaxyrus debilis LC 1 5 1 7<br />
Anaxyrus kelloggi* LC 5 8 1 14<br />
Anaxyrus mexicanus* NT 5 7 1 13<br />
Anaxyrus punctatus LC 1 3 1 5<br />
Anaxyrus retiformis LC 4 7 1 12<br />
Anaxyrus speciosus LC 4 7 1 12<br />
Anaxyrus woodhousii LC 3 6 1 10<br />
Incilius alvarius LC 4 6 1 11<br />
Incilius aurarius NE 4 8 1 13<br />
Incilius bocourti LC 4 6 1 11<br />
Incilius campbelli NT 4 8 1 13<br />
Incilius canaliferus LC 4 3 1 8<br />
Incilius cavifrons* EN 5 7 1 13<br />
Incilius coccifer LC 3 5 1 9<br />
Incilius cristatus* CR 5 8 1 14<br />
Incilius cycladen* VU 5 8 1 14<br />
Incilius gemmifer* EN 6 8 1 15<br />
Incilius luetkenii LC 3 3 1 7<br />
Incilius macrocristatus VU 4 6 1 11<br />
Incilius marmoreus* LC 5 5 1 11<br />
Incilius mazatlanensis* LC 5 6 1 12<br />
Incilius mccoyi* NE 5 8 1 14<br />
Incilius nebulifer LC 1 4 1 6<br />
Incilius occidentalis* LC 5 5 1 11<br />
Incilius perplexus* EN 5 5 1 11<br />
Incilius pisinnus* DD 6 8 1 15<br />
Incilius spiculatus* EN 5 7 1 13<br />
Incilius tacanensis EN 4 4 1 9<br />
Incilius tutelarius EN 4 5 1 10<br />
Incilius valliceps LC 3 2 1 6<br />
Rhinella marina LC 1 1 1 3<br />
Family Centrolenidae (1 species)<br />
LC 3 4 3 10<br />
Family Craugastoridae (39 species)<br />
Craugastor alfredi VU 2 5 4 11<br />
Craugastor amniscola DD 4 6 4 14<br />
Craugastor augusti LC 2 2 4 8<br />
Craugastor batrachylus* DD 6 8 4 18<br />
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Craugastor berkenbuschii* NT 5 5 4 14<br />
Craugastor brocchi VU 4 6 4 14<br />
Craugastor decoratus* VU 5 6 4 15<br />
Craugastor galacticorhinis* NE 6 8 4 15<br />
Craugastor glaucus* CR 6 8 4 18<br />
Craugastor greggi CR 4 7 4 15<br />
Craugastor guerreroensis* CR 6 8 4 18<br />
Craugastor hobartsmithi* EN 5 6 4 15<br />
Craugastor laticeps NT 4 4 4 12<br />
Craugastor lineatus CR 4 7 4 15<br />
Craugastor loki LC 2 4 4 10<br />
Craugastor matudai VU 4 7 4 15<br />
Craugastor megalotympanum* CR 6 8 4 18<br />
Craugastor mexicanus* LC 5 7 4 16<br />
Craugastor montanus* EN 6 8 4 18<br />
Craugastor occidentalis* DD 5 4 4 13<br />
Craugastor omiltemanus* EN 5 7 4 16<br />
Craugastor palenque DD 4 7 4 15<br />
Craugastor pelorus* DD 5 6 4 15<br />
Craugastor polymniae* CR 6 8 4 18<br />
Craugastor pozo* CR 6 7 4 17<br />
Craugastor pygmaeus VU 2 3 4 9<br />
Craugastor rhodopis* VU 5 5 4 14<br />
Craugastor rugulosus* LC 5 4 4 13<br />
Craugastor rupinius LC 4 5 4 13<br />
Craugastor saltator* NE 5 6 4 15<br />
Craugastor silvicola* EN 6 8 4 18<br />
Craugastor spatulatus* EN 5 7 4 16<br />
Craugastor stuarti EN 4 7 4 15<br />
Craugastor tarahumaraensis* VU 5 8 4 17<br />
Craugastor taylori* DD 6 8 4 18<br />
Craugastor uno* EN 5 8 4 17<br />
Craugastor vocalis* LC 5 4 4 13<br />
Craugastor vulcani* EN 6 7 4 17<br />
Craugastor yucatanensis* NT 5 8 4 17<br />
Family Eleutherodactylidae (23 species)<br />
Eleutherodactylus albolabris* NE 6 7 4 17<br />
Eleutherodactylus angustidigitorum* VU 5 8 4 17<br />
Eleutherodactylus cystignathoides LC 2 6 4 12<br />
Eleutherodactylus dennisi* EN 6 8 4 18<br />
Eleutherodactylus dilatus* EN 5 8 4 17<br />
Eleutherodactylus grandis* CR 6 8 4 18<br />
Eleutherodactylus guttilatus LC 2 5 4 11<br />
Eleutherodactylus interorbitalis* DD 5 6 4 15<br />
Eleutherodactylus leprus VU 2 6 4 12<br />
Eleutherodactylus longipes* VU 5 6 4 15<br />
Eleutherodactylus maurus* DD 5 8 4 17<br />
Eleutherodactylus modestus* VU 5 7 4 16<br />
Eleutherodactylus nitidus* LC 5 3 4 12<br />
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Eleutherodactylus nivicolimae* VU 6 7 4 17<br />
Eleutherodactylus pallidus* DD 5 8 4 17<br />
Eleutherodactylus pipilans LC 2 5 4 11<br />
Eleutherodactylus rubrimaculatus VU 4 7 4 15<br />
Eleutherodactylus rufescens* CR 6 7 4 17<br />
Eleutherodactylus saxatilis* EN 5 8 4 17<br />
Eleutherodactylus syristes* EN 5 7 4 16<br />
Eleutherodactylus teretistes* DD 5 7 4 16<br />
Eleutherodactylus verrucipes* VU 5 7 4 16<br />
Eleutherodactylus verruculatus* DD 6 8 4 18<br />
Family Hylidae (97 species)<br />
Acris blanchardi NE 3 8 1 12<br />
Agalychnis callidryas LC 3 5 3 11<br />
Agalychnis dacnicolor* LC 5 5 3 13<br />
Agalychnis moreletii CR 1 3 3 7<br />
Anotheca spinosa LC 3 6 5 14<br />
Bromeliohyla bromeliacia EN 4 7 5 16<br />
Bromeliohyla dendroscarta* CR 5 7 5 17<br />
Charadrahyla altipotens* CR 5 6 1 12<br />
Charadrahyla chaneque* EN 5 7 1 13<br />
Charadrahyla nephila* VU 5 7 1 13<br />
Charadrahyla taeniopus* VU 5 7 1 13<br />
Charadrahyla tecuani* NE 6 8 1 15<br />
Charadrahyla trux* CR 6 7 1 14<br />
Dendropsophus ebraccatus LC 3 6 3 10<br />
Dendropsophus microcephalus LC 3 3 1 7<br />
Dendropsophus robertmertensi LC 4 4 1 9<br />
Dendropsophus sartori* LC 5 8 1 14<br />
Diaglena spatulata* LC 5 7 1 13<br />
Duellmanohyla chamulae* EN 6 7 1 13<br />
Duellmanohyla ignicolor* EN 6 7 1 14<br />
Duellmanohyla schmidtorum VU 4 3 1 8<br />
Ecnomiohyla echinata* CR 6 8 5 19<br />
Ecnomiohyla miotympanum* NT 5 3 1 9<br />
Ecnomiohyla valancifer* CR 6 7 5 18<br />
Exerodonta abdivita* DD 6 8 1 15<br />
Exerodonta bivocata* DD 6 8 1 15<br />
Exerodonta chimalapa* EN 6 5 1 12<br />
Exerodonta juanitae* VU 5 8 1 14<br />
Exerodonta melanomma* VU 5 5 1 11<br />
Exerodonta pinorum* VU 5 7 1 13<br />
Exerodonta smaragdina* LC 5 6 1 12<br />
Exerodonta sumichrasti* LC 5 3 1 9<br />
Exerodonta xera* VU 5 8 1 14<br />
Hyla arboricola* DD 5 6 1 12<br />
Hyla arenicolor LC 2 4 1 7<br />
Hyla euphorbiacea* NT 5 7 1 13<br />
Hyla eximia* LC 5 4 1 10<br />
Hyla plicata* LC 5 5 1 11<br />
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Hyla walkeri VU 4 6 1 11<br />
Hyla wrightorum LC 2 6 1 9<br />
Megastomatohyla mixe* CR 6 8 1 15<br />
Megastomatohyla mixomaculata* EN 5 8 1 14<br />
Megastomatohyla nubicola* EN 5 8 1 14<br />
Megastomatohyla pellita* CR 6 7 1 14<br />
Plectrohyla acanthodes CR 4 7 1 12<br />
Plectrohyla ameibothalame* DD 6 8 1 15<br />
Plectrohyla arborescandens* EN 5 5 1 11<br />
Plectrohyla avia CR 4 8 1 13<br />
Plectrohyla bistincta* LC 5 3 1 9<br />
Plectrohyla calthula* CR 5 8 1 14<br />
Plectrohyla calvicollina* CR 6 7 1 14<br />
Plectrohyla celata* CR 6 7 1 14<br />
Plectrohyla cembra* CR 5 8 1 14<br />
Plectrohyla charadricola* EN 5 8 1 14<br />
Plectrohyla chryses* CR 6 7 1 14<br />
Plectrohyla crassa* CR 5 8 1 14<br />
Plectrohyla cyanomma* CR 5 8 1 14<br />
Plectrohyla cyclada* EN 5 8 1 14<br />
Plectrohyla ephemera* CR 6 8 1 15<br />
Plectrohyla guatemalensis CR 4 4 1 9<br />
Plectrohyla hartwegi CR 4 5 1 10<br />
Plectrohyla hazelae* CR 5 6 1 12<br />
Plectrohyla ixil CR 4 7 1 12<br />
Plectrohyla labedactyla* DD 6 8 1 15<br />
Plectrohyla lacertosa* EN 5 8 1 14<br />
Plectrohyla matudai VU 4 6 1 11<br />
Plectrohyla miahuatlanensis* DD 6 8 1 15<br />
Plectrohyla mykter* EN 5 7 1 13<br />
Plectrohyla pachyderma* CR 6 8 1 15<br />
Plectrohyla pentheter* EN 5 7 1 13<br />
Plectrohyla psarosema* CR 6 8 1 15<br />
Plectrohyla pychnochila* CR 6 8 1 15<br />
Plectrohyla robertsorum* EN 5 7 1 13<br />
Plectrohyla sabrina* CR 5 8 1 14<br />
Plectrohyla sagorum EN 4 5 1 10<br />
Plectrohyla siopela* CR 6 8 1 15<br />
Plectrohyla thorectes* CR 5 7 1 13<br />
Pseudacris cadaverina LC 4 6 1 11<br />
Pseudacris clarki LC 3 8 1 12<br />
Pseudacris hypochondriaca NE 4 4 1 9<br />
Ptychohyla acrochorda* DD 6 7 1 14<br />
Ptychohyla erythromma* EN 5 7 1 13<br />
Ptychohyla euthysanota NT 4 3 1 8<br />
Ptychohyla leonhardschultzei* EN 5 6 1 12<br />
Ptychohyla macrotympanum CR 4 6 1 11<br />
Ptychohyla zophodes* DD 5 7 1 13<br />
Scinax staufferi LC 2 1 1 4<br />
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Smilisca baudinii LC 1 1 1 3<br />
Smilisca cyanosticta NT 4 7 1 12<br />
Smilisca dentata* EN 5 8 1 14<br />
Smilisca fodiens LC 2 5 1 8<br />
Tlalocohyla godmani* VU 5 7 1 13<br />
Tlalocohyla loquax LC 3 3 1 7<br />
Tlalocohyla picta LC 2 5 1 8<br />
Tlalocohyla smithii* LC 5 5 1 11<br />
Trachycephalus typhonius LC 1 2 1 4<br />
Triprion petasatus LC 4 5 1 10<br />
Family Leiuperidae (1 species)<br />
Engystomops pustulosus LC 3 2 2 7<br />
Family Leptodactylidae (2 species)<br />
Leptodactylus fragilis LC 1 2 2 5<br />
Leptodactylus melanonotus LC 1 3 2 6<br />
Family Microhylidae (6 species)<br />
Gastrophryne elegans LC 2 5 1 8<br />
Gastrophryne mazatlanensis NE 2 5 1 8<br />
Gastrophryne olivacea LC 3 5 1 9<br />
Hypopachus barberi VU 4 5 1 10<br />
Hypopachus ustus LC 2 4 1 7<br />
Hypopachus variolosus LC 2 1 1 4<br />
Family Ranidae (28 species)<br />
Lithobates berlandieri LC 4 2 1 7<br />
Lithobates brownorum NE 4 3 1 8<br />
Lithobates catesbeianus LC 3 6 1 10<br />
Lithobates chichicuahutla* CR 6 8 1 15<br />
Lithobates chiricahuensis VU 4 6 1 11<br />
Lithobates dunni* EN 5 8 1 14<br />
Lithobates forreri LC 1 1 1 3<br />
Lithobates johni* EN 5 8 1 14<br />
Lithobates lemosespinali* DD 5 8 1 14<br />
Lithobates macroglossa VU 4 7 1 12<br />
Lithobates maculatus LC 3 1 1 5<br />
Lithobates magnaocularis* LC 5 6 1 12<br />
Lithobates megapoda* VU 5 8 1 14<br />
Lithobates montezumae* LC 5 7 1 13<br />
Lithobates neovolcanicus* NT 5 7 1 13<br />
Lithobates omiltemanus* CR 5 7 1 13<br />
Lithobates psilonota* DD 5 8 1 14<br />
Lithobates pueblae* CR 6 8 1 15<br />
Lithobates pustulosus* LC 5 3 1 9<br />
Lithobates sierramadrensis* VU 5 7 1 13<br />
Lithobates spectabilis* LC 5 6 1 12<br />
Lithobates tarahumarae VU 2 5 1 8<br />
Lithobates tlaloci* CR 6 8 1 15<br />
Lithobates vaillanti LC 3 5 1 9<br />
Lithobates yavapaiensis LC 4 7 1 12<br />
Lithobates zweifeli* LC 5 5 1 11<br />
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Rana boylii NT 3 8 1 12<br />
Rana draytonii LC 3 6 1 10<br />
Family Rhinophrynidae (1 species)<br />
Rhinophrynus dorsalis LC 2 5 1 8<br />
Family Scaphiopodidae (4 species)<br />
Scaphiopus couchii LC 1 1 1 3<br />
Spea bombifrons NE 3 6 1 10<br />
Spea hammondii LC 3 8 1 12<br />
Spea multiplicata NE 1 4 1 6<br />
Order Caudata (139 species)<br />
Family Ambystomatidae (18 species)<br />
Ambystoma altamirani* EN 5 7 1 13<br />
Ambystoma amblycephalum* CR 6 6 1 13<br />
Ambystoma andersoni* CR 6 8 1 15<br />
Ambystoma bombypellum* CR 6 8 1 15<br />
Ambystoma dumerilii* CR 6 8 1 15<br />
DD 6 7 1 14<br />
Ambystoma granulosum* CR 6 7 1 14<br />
Ambystoma leorae* CR 6 8 1 15<br />
Ambystoma lermaense* CR 6 8 1 15<br />
Ambystoma mavortium NE 3 6 1 10<br />
Ambystoma mexicanum* CR 6 8 1 15<br />
Ambystoma ordinarium* EN 5 7 1 13<br />
Ambystoma rivulare* DD 5 7 1 13<br />
Ambystoma rosaceum* LC 5 8 1 14<br />
Ambystoma silvense* DD 5 8 1 14<br />
Ambystoma subsalsum* NE 5 8 1 14<br />
Ambystoma taylori* CR 6 8 1 15<br />
Ambystoma velasci* LC 5 4 1 10<br />
Family Plethodontidae (118 species)<br />
Aneides lugubris LC 3 7 4 14<br />
Batrachoseps major LC 4 6 4 14<br />
Bolitoglossa alberchi* LC 6 5 4 15<br />
Bolitoglossa chinanteca NE 6 8 4 18<br />
Bolitoglossa engelhardti EN 4 7 4 15<br />
EN 4 7 4 15<br />
EN 4 5 4 13<br />
Bolitoglossa franklini EN 4 6 4 14<br />
Bolitoglossa hartwegi NT 4 4 4 12<br />
Bolitoglossa hermosa* NT 5 7 4 16<br />
Bolitoglossa lincolni NT 4 5 4 13<br />
Bolitoglossa macrinii* NT 5 6 4 15<br />
Bolitoglossa mexicana LC 4 3 4 11<br />
Bolitoglossa mulleri VU 4 7 4 15<br />
Bolitoglossa oaxacensis* DD 5 8 4 17<br />
Bolitoglossa occidentalis LC 4 3 4 11<br />
Bolitoglossa platydactyla* NT 5 6 4 15<br />
Bolitoglossa riletti* EN 6 6 4 16<br />
Bolitoglossa rostrata VU 4 6 4 14<br />
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Bolitoglossa rufescens LC 1 4 4 9<br />
Bolitoglossa stuarti DD 4 7 4 15<br />
Bolitoglossa veracrucis* EN 6 7 4 17<br />
Bolitoglossa yucatana LC 4 7 4 15<br />
Bolitoglossa zapoteca* DD 6 8 4 18<br />
Chiropterotriton arboreus* CR 6 8 4 18<br />
Chiropterotriton chiropterus* CR 6 6 4 16<br />
Chiropterotriton chondrostega* EN 5 8 4 17<br />
Chiropterotriton cracens* EN 6 7 4 17<br />
Chiropterotriton dimidiatus* EN 6 7 4 17<br />
Chiropterotriton lavae* CR 6 8 4 18<br />
Chiropterotriton magnipes* CR 6 6 4 16<br />
Chiropterotriton mosaueri* DD 6 8 4 18<br />
Chiropterotriton multidentatus* EN 5 6 4 15<br />
Chiropterotriton orculus* VU 6 8 4 18<br />
Chiropterotriton priscus* NT 6 6 4 16<br />
Chiropterotriton terrestris* CR 6 8 4 18<br />
Cryptotriton alvarezdeltoroi* EN 6 8 4 18<br />
Dendrotriton megarhinus* VU 6 7 4 17<br />
Dendrotriton xolocalcae* VU 6 8 4 18<br />
Ensatina eschscholtzii LC 3 7 4 14<br />
Ensatina klauberi NE 4 6 4 14<br />
Ixalotriton niger* CR 6 8 4 18<br />
Ixalotriton parvus* CR 6 8 4 18<br />
Nyctanolis pernix EN 4 7 4 15<br />
Oedipina elongata LC 4 7 4 15<br />
Parvimolge townsendi* CR 5 7 4 16<br />
Pseudoeurycea ahuitzotl* CR 6 8 4 18<br />
Pseudoeurycea altamontana* EN 5 8 4 17<br />
Pseudoeurycea amuzga* DD 6 8 4 18<br />
Pseudoeurycea anitae* CR 6 8 4 18<br />
Pseudoeurycea aquatica* CR 6 8 4 18<br />
Pseudoeurycea aurantia* VU 6 8 4 18<br />
Pseudoeurycea bellii* VU 5 3 4 12<br />
Pseudoeurycea boneti* VU 6 7 4 17<br />
Pseudoeurycea brunnata CR 4 7 4 15<br />
Pseudoeurycea cafetalera NE 6 7 4 17<br />
Pseudoeurycea cephalica* NT 5 5 4 14<br />
Pseudoeurycea cochranae* EN 6 7 4 17<br />
Pseudoeurycea conanti* EN 5 7 4 16<br />
EN 6 8 4 18<br />
Pseudoeurycea gadovii* EN 5 4 4 13<br />
Pseudoeurycea galaenae* NT 6 8 4 18<br />
Pseudoeurycea gigantea* CR 5 7 4 16<br />
Pseudoeurycea goebeli CR 4 7 4 15<br />
Pseudoeurycea juarezi* CR 6 7 4 17<br />
Pseudoeurycea leprosa* VU 5 7 4 16<br />
Pseudoeurycea lineola* EN 5 5 4 14<br />
Pseudoeurycea longicauda* EN 5 8 4 17<br />
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Pseudoeurycea lynchi* CR 5 8 4 17<br />
Pseudoeurycea maxima* DD 5 8 4 17<br />
Pseudoeurycea melanomolga* EN 6 6 4 16<br />
Pseudoeurycea mixcoatl* DD 6 8 4 17<br />
Pseudoeurycea mixteca* LC 5 8 4 17<br />
Pseudoeurycea mystax* EN 6 8 4 18<br />
Pseudoeurycea naucampatepetl* CR 6 7 4 17<br />
Pseudoeurycea nigromaculata* CR 5 8 4 17<br />
Pseudoeurycea obesa* DD 6 8 4 18<br />
Pseudoeurycea orchileucos* EN 6 8 4 18<br />
Pseudoeurycea orchimelas* EN 6 7 4 17<br />
Pseudoeurycea papenfussi* NT 6 7 4 17<br />
Pseudoeurycea praecellens* CR 6 8 4 18<br />
Pseudoeurycea quetzalanensis* DD 6 7 4 17<br />
Pseudoeurycea rex CR 4 4 4 12<br />
Pseudoeurycea robertsi* CR 6 8 4 18<br />
DD 6 8 4 18<br />
Pseudoeurycea saltator* CR 6 8 4 18<br />
Pseudoeurycea scandens* VU 6 7 4 17<br />
Pseudoeurycea smithi* CR 5 6 4 15<br />
Pseudoeurycea tenchalli* EN 6 7 4 17<br />
Pseudoeurycea teotepec* EN 6 8 4 18<br />
Pseudoeurycea tlahcuiloh* CR 6 7 4 17<br />
Pseudoeurycea tlilicxitl* DD 5 8 4 17<br />
Pseudoeurycea unguidentis* CR 6 7 4 17<br />
Pseudoeurycea werleri* EN 6 7 4 17<br />
Thorius adelos* EN 6 8 4 18<br />
Thorius arboreus* EN 6 8 4 18<br />
Thorius aureus* CR 6 7 4 17<br />
Thorius boreas* EN 6 8 4 18<br />
Thorius dubitus* EN 5 7 4 16<br />
Thorius grandis* EN 6 5 4 15<br />
Thorius infernalis* CR 6 8 4 18<br />
Thorius insperatus* DD 6 8 4 18<br />
Thorius lunaris* EN 6 8 4 18<br />
Thorius macdougalli* VU 6 6 4 16<br />
Thorius magnipes* CR 6 7 4 17<br />
Thorius minutissimus* CR 6 7 4 17<br />
Thorius minydemus* CR 6 8 4 18<br />
CR 6 8 4 18<br />
Thorius narismagnus* CR 6 8 4 18<br />
Thorius narisovalis* CR 6 7 4 17<br />
Thorius omiltemi* EN 6 8 4 18<br />
Thorius papaloae* EN 6 7 4 17<br />
Thorius pennatulus* CR 5 6 4 15<br />
Thorius pulmonaris* EN 6 7 4 17<br />
Thorius schmidti* EN 6 7 4 17<br />
Thorius smithi* CR 6 7 4 17<br />
Thorius spilogaster* CR 6 7 4 17<br />
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Thorius troglodytes* EN 6 6 4 16<br />
Family Salamandridae (1 species)<br />
Notophthalmus meridionalis EN 2 8 1 12<br />
Family Sirenidae (2 species)<br />
Siren intermedia LC 3 8 1 12<br />
Siren lacertina LC 3 8 1 12<br />
Order Gymnophiona (2 species)<br />
Family Dermophiidae (2 species)<br />
Dermophis mexicanus VU 4 3 4 11<br />
Dermophis oaxacae* DD 5 3 4 12<br />
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Crotalus tancitarensis. The Tancítaro cross-banded mountain rattlesnake is a small species (maximum recorded total length = 434<br />
mm) known only from the upper elevations (3,220–3,225 m) of Cerro Tancítaro, the highest mountain in Michoacán, Mexico,<br />
where it inhabits pine-fir forest (Alvarado and Campbell 2004; Alvarado et al. 2007). Cerro Tancítaro lies in the western portion of<br />
the Transverse Volcanic Axis, which extends across Mexico from Jalisco to central Veracruz near the 20°N latitude. Its entire range<br />
is located within Parque Nacional Pico de Tancítaro (Campbell 2007), an area under threat from manmade fires, logging, avocado<br />
culture, and cattle raising. This attractive rattlesnake was described in 2004 by the senior author and Jonathan A. Campbell, and<br />
placed in the Crotalus intermedius group of Mexican montane rattlesnakes by Bryson et al. (2011). We calculated its EVS as 19,<br />
which is near the upper end of the high vulnerability category (see text for explanation), its IUCN status has been reported as Data<br />
Deficient (Campbell 2007), and this species is not listed by SEMARNAT. More information on the natural history and distribution<br />
of this species is available, however, which affects its conservation status (especially its IUCN status; Alvarado-Díaz et al. 2007).<br />
We consider C. tancitarensis one of the pre-eminent flagship reptile species for the state of Michoacán, and for Mexico in general.<br />
Photo by Javier Alvarado-Díaz.<br />
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Copyright: © 2013 Alvarado-Díaz et al. This is an open-access article distributed under the terms of the Creative<br />
Commons Attribution–NonCommercial–NoDerivs 3.0 Unported License, which permits unrestricted use for<br />
non-commercial and education purposes only provided the original author and source are credited.<br />
Amphibian & Reptile Conservation 7(1): 128–170.<br />
Patterns of physiographic distribution and conservation<br />
status of the herpetofauna of Michoacán, Mexico<br />
1<br />
Javier Alvarado-Díaz, 2 Ireri Suazo-Ortuño,<br />
3<br />
Larry David Wilson, and 4 Oscar Medina-Aguilar<br />
1,2,4<br />
Instituto de Investigaciones sobre los Recursos Naturales, Universidad Michoacana de San Nicolás de Hidalgo, Av. San Juanito Itzícuaro s/n<br />
Col. Nva. Esperanza, Morelia, Michoacán, MÉXICO, 58337 3 Centro Zamorano de Biodiversidad, Escuela Agrícola Panamericana Zamorano,<br />
Departamento de Francisco Morazán, HONDURAS<br />
Abstract.—At their respective levels, the country of Mexico and the state of Michoacán are major centers<br />
of herpetofaunal diversity and endemicity. Three of us (JAD, ISO, OMA) conducted extensive<br />
fieldwork in Michoacán from 1998 to 2011, and recorded 169 herpetofaunal species. With additional<br />
species reported in the literature and specimens available in scientific collections, the number of<br />
species in Michoacán has grown to 215. We examined the distribution of these species within the<br />
framework of the five physiographic provinces within the state, i.e., the Coastal Plain, the Sierra<br />
Madre del Sur, the Balsas-Tepalcatepec Depression, the Transverse Volcanic Axis, and the Central<br />
Plateau, which briefly are characterized geomorphologically and climatically. The herpetofauna<br />
consists of 54 amphibians and 161 reptiles (17.5% of the total for Mexico), classified in 38 families<br />
and 96 genera. Almost one-half of Michoacán’s herpetofaunal species occur in a single physiographic<br />
province, and the percentage of species decreases with an increase in the number of provinces.<br />
The province with the most species is the Sierra Madre del Sur, with slightly fewer numbers<br />
in the Balsas-Tepalcatepec Depression and the Transverse Volcanic Axis. An intermediate number<br />
is found in the Coastal Plain, and the lowest in the Central Plateau province. We constructed a Coefficient<br />
of Biogeographic Resemblance matrix and found the greatest degree of herpetofaunal resemblance<br />
between the Balsas-Tepalcatepec Depression and the Sierra Madre del Sur. The greatest<br />
resemblance of the Coastal Plain herpetofauna is to that of Balsas-Tepalcatepec Depression, that<br />
of the Transverse Volcanic Axis to that of the Central Plateau, and vice versa. Of the species limited<br />
to one physiographic province, 47 occur only in the Transverse Volcanic Axis, 23 in the Coastal<br />
Plain, 15 in the Balsas-Tepalcatepec, 14 in the Sierra Madre del Sur, and one in the Central Plateau.<br />
We employed three systems for determining the conservation status of the herpetofauna of Michoacán:<br />
SEMARNAT, IUCN, and EVS. Almost one-half of the species in the state are not assessed by<br />
the SEMARNAT system, with the remainder allocated to the Endangered (four species), Threatened<br />
(31), and Special Protection (79) categories. The IUCN system provides an assessment for 184 of<br />
the 212 native species, allocating them to the Critically Endangered (five species), Endangered (10),<br />
Vulnerable (12), Near Threatened (four), Least Concern (127), and Data Deficient (26) categories.<br />
The EVS system provides a numerical assessment for all of the native non-marine species (four marine<br />
species occur in the state), with the values ranging from three to 19. The resulting 208 species<br />
were placed in low, medium, and high categories of vulnerability, as follows: low (17 amphibians,<br />
39 reptiles); medium (23 amphibians, 45 reptiles); and high (13 amphibians, 71 reptiles). The EVS<br />
system is the only one that provides an assessment for all the species (except for the four marine<br />
taxa), as well as the only one that considers the distributional status of Michoacán’s herpetofauna<br />
(state-level endemic, country-level endemic, and non-endemic). Furthermore, the values indicate<br />
that ca. 40% of the state’s herpetofauna is categorized at the highest level of environmental vulnerability.<br />
Based on these conclusions, we provide recommendations for protecting Michoacán’s<br />
herpetofauna in perpetuity.<br />
Key words. Amphibians, reptiles, physiographic provinces, conservation status, recommendations<br />
Correspondence. Emails: 1 jvr.alvarado@gmail.com (Corresponding author) 2 ireri.suazo@gmail.com<br />
3<br />
bufodoc@aol.com 4 mineo_osc@hotmail.com<br />
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Physiographic distribution and conservation of Michoacán herpetofauna<br />
Resumen.—México es un importante centro de diversidad y endemismo herpetofaunistico y el estado<br />
de Michoacán también presenta estas características. Durante el período de 1998–2011, tres<br />
de nosotros (JAD, ISO, OMA) conducimos un extenso trabajo de campo en Michoacán, registrando<br />
169 especies de anfibios y reptiles. Con la adición de especies reportadas en la literatura y los<br />
registros disponibles en colecciones científicas, el número total de especies de la herpetofauna<br />
michoacana es de 215. Examinamos la distribución de estas especies en Michoacán, considerando<br />
las cinco provincias fisiográficas representadas en el Estado: la Llanura Costera, la Sierra Madre<br />
del Sur, la Depresión del Balsas-Tepalcatepec, el Eje Volcánico Transversal, y la Meseta Central,<br />
las que de manera resumida son caracterizadas en base a su geomorfología y clima. La herpetofauna<br />
consiste de 54 anfibios y 161 reptiles (17.5% del total de México), clasificadas en 38 familias<br />
y 96 géneros. Casi la mitad de las especies de la herpetofauna de Michoacán ocurre en una sola<br />
provincia fisiográfica, con un cada vez menor porcentaje de especies a medida que el número de<br />
provincias se incrementa. El mayor número de especies se encuentra en la Sierra Madre del Sur,<br />
con cifras ligeramente menores en la Depresión del Balsas-Tepalcatepec y el Eje Volcánico Transversal.<br />
Un número intermedio de especies se encuentra en la provincia Planicie Costera y el menor<br />
número se encuentra en la provincia Meseta Central. Implementamos una matriz del Coeficiente de<br />
Semejanza Biogeográfica, la que muestra que el mayor grado de semejanza herpetofaunistica se<br />
encuentra entre la Depresión del Balsas-Tepalcatepec y la Sierra Madre del Sur. La mayor similitud<br />
de la herpetofauna de la Planicie Costera es con la herpetofauna de la Depresión Balsas-Tepalcatepec,<br />
la del Eje Volcánico Transversal con la de la Meseta Central y viceversa. De las especies<br />
restringidas a una sola provincia fisiográfica, 47 ocurren solamente en el Eje Volcánico Transversal,<br />
23 en la Planicie Costera, 15 en la Depresión del Balsas-Tepalcatepec, 14 en la Sierra Madre del<br />
Sur, y una en la Meseta Central. Usamos tres sistemas para determinar el estado de conservación:<br />
SEMARNAT, UICN, y EVS. Casi la mitad de las especies de Michoacán no han sido evaluadas por<br />
el sistema de SEMARNAT, y las evaluadas han sido asignadas a las categorías de Peligro (cuatro<br />
especies), Amenazadas (31), y Protección Especial (79). El sistema de la UICN ha evaluado 184 de<br />
las 212 especies nativas de Michoacán, asignadas a las siguientes categorías: Peligro Crítico (cinco<br />
especies), En Peligro (10), Vulnerable (12), Casi Amenazado (cuatro), Preocupación Menor (127), y<br />
Datos Insuficientes (26). El sistema EVS proporciona una evaluación numérica para todas las especies<br />
nativas que no son marinas (cuatro especies marinas ocurren en el estado), con valores de tres<br />
a 18. Las 209 especies evaluadas mediante el EVS fueron asignadas a las categorías de baja, media<br />
y alta vulnerabilidad de la siguiente manera: baja (17 anfibios, 39 reptiles); media (23 anfibios, 45<br />
reptiles); y alta (13 anfibios, 71 reptiles). El sistema EVS es el único de los tres que proporciona una<br />
evaluación de todas las especies (excepto para los cuatro taxa marinos) y el único que considera<br />
el estado distribucional de los componentes de la herpetofauna de Michoacán (endémico a nivel<br />
estatal, endémico a nivel de país, y no endémico). Además, los valores muestran que cerca del 40%<br />
de la herpetofauna del estado se encuentra en la categoría más alta de vulnerabilidad ambiental.<br />
En base a estas conclusiones, proponemos recomendaciones para la protección a perpetuidad de<br />
la herpetofauna de Michoacán.<br />
Palabras claves. Anfibios, reptiles, provincias fisiográficas, estatus de conservación, recomendaciones<br />
Citation: Alvarado-Díaz J, Suazo-Ortuño I, Wilson LD, Medina-Aguilar O. 2013. Patterns of physiographic distribution and conservation status of the<br />
herpetofauna of Michoacán, Mexico. Amphibian & Reptile Conservation 7(1): 128–170(e71).<br />
The publication of On the Origin of Species in 1859 is<br />
a recognized watershed in biological science. Perhaps<br />
the greatest threat to Western ideology was not the common<br />
origin of all beings, as is assumed, but rather the<br />
possibility of a common ending: that all beings, humans<br />
among them were subjected to the same forces and vulnerabilities.<br />
Chernela 2012: 22.<br />
Introduction<br />
Mesoamerica is one of the principal biodiversity hotspots<br />
in the world (Wilson and Johnson 2010), and the country<br />
of Mexico comprises about 79% of the land surface<br />
of Mesoamerica (CIA World Factbook). The documented<br />
amphibian fauna of Mexico currently consists of<br />
379 species, including 237 anurans, 140 salamanders,<br />
and two caecilians (Wilson et al. 2013b). Based on this<br />
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Alvarado-Díaz et al.<br />
Incilius pisinnus. The Michoacán toad is a state endemic, with a distribution in the Balsas-Tepalcatepec Depression and the Sierra<br />
Madre del Sur. Its EVS was estimated as 15, which is unusually high for a bufonid anuran, its IUCN ranking has been judged as<br />
Data Deficient, and a SEMARNAT status has not been provided. This individual is from Apatzingán, Michoacán.<br />
Photo by Oscar Medina-Aguilar.<br />
Eleutherodactylus rufescens. The blunt-toed chirping frog is endemic to the Sierra de Coalcomán region of the Sierra Madre del<br />
Sur. Its EVS has been assessed as 17, placing this species in the middle of the high vulnerability category, this frog is considered as<br />
Critically Endangered by IUCN, and as a Special Protection species by SEMARNAT. This individual was found at Dos Aguas in<br />
the Sierra de Coalcomán (Sierra Madre del Sur) in Michoacán. Photo by Oscar Medina-Aguilar.<br />
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Physiographic distribution and conservation of Michoacán herpetofauna<br />
figure, Mexico is the country with the 5 th largest number<br />
of amphibian species in the world (Llorente-Bousquets<br />
and Ocegueda 2008; Stuart et al. 2010a), after Brazil,<br />
Colombia, Ecuador, and Peru. The country also is inhabited<br />
by 849 species of reptiles, including 798 squamates,<br />
48 turtles, and three crocodylians (Wilson et<br />
al. 2013a), which globally is the second largest reptile<br />
fauna (Llorente-Bousquets and Ocegueda 2008), after<br />
Australia. The total number of 1,227 species makes the<br />
Mexican herpetofauna the second largest in the world<br />
(Llorente-Bousquets and Ocegueda 2008), comprising<br />
7.3% of the global herpetofauna (7,044 amphibian species,<br />
according to the Amphibian Species of the World<br />
website, accessed 21 February 2013, and 9,766 reptile<br />
species, according to the Reptile Database website, also<br />
accessed 21 February 2013, for a total of 16,810).<br />
Beyond its highly significant herpetofaunal diversity,<br />
Mexico also contains an amazing amount of endemicity.<br />
Currently, 254 of 379 (67.0%) of the known amphibian<br />
species and 480 of 849 (56.5%) of the known reptile<br />
species are endemic (Wilson et al. 2013a,b). The combined<br />
figure for both groups is 734 species (59.8%), a<br />
percentage 2.4 times as high as the next highest rate of<br />
endemicity for the Central American countries (24.8%<br />
for Honduras; Townsend and Wilson 2010).<br />
Michoacán (the formal name is Michoacán de Ocampo)<br />
is the 16 th largest state in Mexico, with an area of<br />
58,599 km 2 (www.en.wikipedia.org/wiki/List_of_Mexican_states_by_area),<br />
which comprises about 3.0% of the<br />
country’s land surface. The state is located in southwestern<br />
Mexico between latitudes 20°23'44" and 18°09'49"<br />
N and longitudes 100°04'48" and 103°44'20" W, and<br />
is bounded to the northwest by Colima and Jalisco, to<br />
the north by Guanajuato and Querétaro, to the east by<br />
México, and to the southeast by Guerrero. Michoacán is<br />
physiographically and vegetationally diverse, inasmuch<br />
as elevations range from sea level to 3,840 m (at the top<br />
of Volcán Tancítaro). The state encompasses a portion of<br />
the Pacific coastal plain, a long stretch of the Balsas-Tepalcatepec<br />
Depression, a segment of the Sierra Madre<br />
del Sur called the Sierra de Coalcomán, and a significant<br />
portion of the Transverse Volcanic Axis.<br />
Mexico is known for its high level of herpetofaunal<br />
endemism, but compared with the country the herpetofauna<br />
of Michoacán is several percentage points higher,<br />
with a number of the country endemics limited in distribution<br />
to the state (see below). Any attempt to assess the<br />
conservation status of a herpetofaunal group depends on<br />
an accurate accounting of the distribution and composition<br />
of the species involved. Thus, our objectives with<br />
this study are to update the list of amphibians and reptiles<br />
in Michoacán, to discuss their distribution among<br />
the physiographic provinces, and to use these data to<br />
gauge the conservation status of the entire herpetofauna<br />
using various measures. Finally, based on our conservation<br />
assessment, we provide recommendations to<br />
enhance current efforts to protect the state’s amphibians<br />
and reptiles.<br />
Diaglena spatulata. The shovel-headed treefrog is distributed along the Pacific coastal lowlands from Sinaloa to Oaxaca, and thus<br />
is a Mexican endemic hylid anuran. In Michoacán, it occurs in the Balsas-Tepalcatepec Depression and along the Coastal Plain. Its<br />
EVS was gauged as 13, placing it at the upper end of the medium vulnerability category, IUCN has assessed this anuran as Least<br />
Concern, and it is not listed by SEMARNAT. This individual was photographed at the Reserva de la Biosfera Chamela-Cuixmala<br />
on the coast of Jalisco. Photo by Oscar Medina-Aguilar.<br />
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Materials and Methods<br />
1. Sampling procedures<br />
From 1998 to 2011, three of us (JAD, ISO, OMA) conducted<br />
fieldwork in 280 localities (58 municipalities) of<br />
Michoacán, representing all of the state’s physiographic<br />
provinces, with significant attention paid to poorly sampled<br />
areas, as part of the “Diversidad Herpetofaunística<br />
del Estado de Michoacán” project undertaken by personnel<br />
from the Laboratorio de Herpetología of the Instituto<br />
de Investigaciones sobre los Recursos Naturales (INI-<br />
RENA) of the Universidad Michoacana de San Nicolás<br />
de Hidalgo (UMSNH). Importantly, due to unsafe<br />
conditions in certain parts of the state in recent years,<br />
large areas have not been explored. During each visit<br />
to the sampling sites, we used visual encounter surveys<br />
(Crump and Scott 1994) to locate amphibians and reptiles<br />
during the day and at night. This work was conducted<br />
under scientific collecting permits (DGVS/FAUT-<br />
0113), and used the collection techniques described by<br />
Casas et al. (1991). In cases where we could not identify<br />
individuals in the field, they were sacrificed and subsequently<br />
deposited in the herpetological collections of<br />
INIRENA-UMSNH. We identified specimens by using<br />
taxonomic keys and other information in Smith and Taylor<br />
(1945, 1948, 1950), Duellman (1961, 1965, 2001),<br />
Casas-Andréu and McCoy (1979), Ramírez-Bautista<br />
(1994), Flores-Villela et al. (1995), and Huacuz (1995),<br />
and updated scientific names by using Flores-Villela and<br />
Canseco-Márquez (2004), Faivovich et al. (2005), Wilson<br />
and Johnson (2010), and Wilson et al. (2013a,b).<br />
2. Updating the herpetofaunal list<br />
In addition to the specimens recorded during the fieldwork,<br />
the list of species was augmented using material<br />
donated by others. We also used records from the Colección<br />
Nacional de Anfibios y Reptiles-UNAM (CNAR),<br />
the California Academy of Sciences (CAS), the University<br />
of Colorado Museum of Natural History, Herpetology<br />
Collection (CUMNH), the Museum of Natural Sciences,<br />
Louisiana State University (LSUMZ), the Field Museum<br />
of Natural History (FMNH), and the Royal Ontario<br />
Museum (ROM). Additionally, we included records for<br />
Michoacán from the Catálogo de la Biodiversidad en<br />
Michoacán (SEDUE [Secretaría de Desarrollo Urbano y<br />
Ecología], UMSNH 2000), la Biodiversidad en Michoacán<br />
Estudio de Estado (Villaseñor 2005), various distribution<br />
notes published in Herpetological Review and<br />
otherwise posted at the IUCN Red List website, as well<br />
as data presented by Flores-Villela and Canseco-Márquez<br />
(2004), Vargas-Santamaría and Flores-Villela (2006),<br />
González-Hernández and Garza-Castro (2006), Medina-Aguilar<br />
et al. (2011), and Torres (2011). We follow the<br />
taxonomy used in Wilson (2013a, b), with the exception<br />
of the deletion of the nominal species Anolis schmidti,<br />
which recently was synonymized by Nieto et al. (2013).<br />
3. Systems for determining<br />
conservation status<br />
We used the following three systems to determine the<br />
conservation status of the 212 native species of amphibians<br />
and reptiles in Michoacán: SEMARNAT, IUCN, and<br />
EVS. The SEMARNAT system, established by the Secretaría<br />
de Medio Ambiente y Recursos Naturales, employs<br />
three categories––Endangered (P), Threatened (A),<br />
and Subject to Special Protection (Pr). The results of the<br />
application of this system are reported in the NORMA<br />
Oficial Mexicana NOM-059-SEMARNAT-2010 (www.<br />
semarnat.gob.mx). For species not assessed by this system,<br />
we use the designation “No Status.”<br />
The IUCN system is utilized widely to assess the conservation<br />
status of species on a global basis. The categories<br />
used are explained in the document IUCN Red List<br />
of Categories and Criteria (2010), and include Extinct<br />
(EX), Extinct in the Wild (EW), Critically Endangered<br />
(CR), Endangered (EN), Vulnerable (VU), Near Threatened<br />
(NT), Least Concern (LC), Data Deficient (DD),<br />
and Not Evaluated (NE). The categories Critically Endangered,<br />
Endangered, and Vulnerable collectively are<br />
termed “threat categories,” to distinguish them from the<br />
other six.<br />
The EVS system was developed initially for use in<br />
Honduras by Wilson and McCranie (2004), and subsequently<br />
was used in several chapters on Central American<br />
countries in Wilson et al. (2010). Wilson et al. (2013a,b)<br />
modified this system and explained its use for the amphibians<br />
and reptiles of Mexico, and we follow their prescriptions.<br />
The EVS measure is not designed for use with<br />
marine species (e.g., marine turtles and sea snakes), and<br />
generally is not applied to non-native species.<br />
Physiography and Climate<br />
1. Physiographic provinces<br />
Based on geological history, morphology, structure, hydrography,<br />
and soils, five physiographic provinces can<br />
be recognized within the state of Michoacán, including<br />
the Pacific Coastal Plain, the Sierra Madre del Sur, the<br />
Balsas-Tepalcatepec Depression, the Transverse Volcanic<br />
Axis, and the Central Plateau (Fig. 1). The Coastal Plain<br />
province comprises a narrow strip of land between the Pacific<br />
Ocean and the Sierra Madre del Sur, and consists of<br />
small alluvial plains extending from the mouth of the Río<br />
Balsas to the east and the Río Coahuayana to the west.<br />
The Sierra Madre del Sur (Sierra de Coalcomán) lies<br />
between the Coastal Plain and the Balsas-Tepalcatepec<br />
Depression, extends for over 100 km in a northwest-southeast<br />
direction, and contains elevations reaching<br />
about 2,200 m. The Balsas-Tepalcatepec Depression<br />
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Fig. 1. Physiographic provinces in Michoacán.<br />
is located between the Sierra Madre del Sur to the southwest<br />
and the Transverse Volcanic Axis to the northeast.<br />
This intermontane area is a broad structural basin that<br />
lies at elevations ranging from 200 to 700 m. As noted<br />
by Duellman (1961:10), “the western part of this basin…<br />
is the valley of the Río Tepalcatepec, a major tributary<br />
of the Río Balsas. The eastern part of the basin is the<br />
valley of the Río Balsas.” The Transverse Volcanic Axis<br />
is located to the south of the Central Plateau and crosses<br />
Mexico at about the 20 th parallel. The region is composed<br />
of volcanic ejecta and is volcanically active. This area is<br />
home to Mexico’s highest mountains, such as Pico de<br />
Orizaba (5,636 m) and Popocatépetl (5,426 m), which<br />
in Michoacán is represented by Pico de Tancítaro, with<br />
an elevation of 3,850 m. In addition, several endorheic<br />
lakes are located in this province, including Pátzcuaro,<br />
Zirahuén, and Cuitzeo. The Central Plateau is a vast tableland<br />
bordered on the south by the Transverse Volcanic<br />
Axis, on the west by the Sierra Madre Occidental, on<br />
the east by the Sierra Madre Oriental, and on the north<br />
by the Río Bravo (Rio Grande). Elevations in this province<br />
range from 1,100 m in the northern portion of the<br />
country to 2,000 m. In Michoacán, this province is represented<br />
by a relatively small area (3,905 km 2 ) along the<br />
northern border of the state; the Río Lerma flows from<br />
it, and empties into the Pacific Ocean (Duellman 1961).<br />
2. Climate<br />
Given its location in the tropical region of Mexico, south<br />
of the Tropic of Cancer, temperatures in Michoacán vary<br />
as a consequence of differences in elevation and the effects<br />
of prevailing winds. To illustrate variation in ambient<br />
temperatures in the state, we extracted data for one<br />
locality from each of the five physiographic provinces<br />
from the Servicio Meteorológico Nacional, Michoacán,<br />
and placed them in Table 1. These data are organized in<br />
the table from top to bottom based on the elevation of the<br />
localities (from low to high). As expected, a decrease in<br />
the mean annual temperature occurs from lower to higher<br />
elevations. The same pattern is seen for annual minimum<br />
and maximum temperatures, except for the Coastal<br />
Plain compared to the Balsas-Tepalcatepec Depression<br />
(33.0 vs. 34.4 °C).<br />
As expected in the tropics, relatively little temperature<br />
variation occurs throughout the year. The differences<br />
between the low and high mean monthly temperatures<br />
(in °C) for the localities in the five physiographic provinces<br />
are as follows: Coastal Plain (Lázaro Cárdenas,<br />
50 m) = 1.9; Balsas-Tepalcatepec Depression (Apatzingán,<br />
320 m) = 5.5; Sierra Madre del Sur (Coalcomán, 1,100 m)<br />
= 5.2; Central Plateau (Morelia, 1,915 m) = 5.9; and<br />
Transverse Volcanic Axis (Pátzcuaro, 2,035 m) = 6.6.<br />
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The lowest mean monthly temperatures are for January,<br />
and the highest for May or June. Essentially the same<br />
pattern occurs with minimum and maximum monthly<br />
temperatures, except for minor departures in a few areas<br />
(Table 1).<br />
The highest mean monthly temperature (34.4 °C) is<br />
at Apatzingán in the Balsas-Tepalcatepec Depression.<br />
Duellman (1961) stated that the highest mean annual<br />
temperatures (29.3 °C) in this depression have been<br />
recorded at Churumuco (251 m), as reported by Contreras<br />
(1942). More recent data at the Servicio Meteorológico<br />
Nacional website for Michoacán indicates that<br />
the highest daily temperature of 46 °C was recorded at<br />
this locality on 9 April 1982. At the other extreme are<br />
temperatures on the peak of Volcán Tancítaro, where the<br />
mean annual temperature is less than 10 °C and it snows<br />
during the winter.<br />
In tropical locales, heavy or light precipitation typically<br />
occurs during the rainy and dry seasons, respectively.<br />
In Michoacán, the rainy season extends from June<br />
to October, when 80% or more of the annual precipitation<br />
is deposited. As with temperature data, we extracted<br />
information on mean annual precipitation and variation<br />
in monthly precipitation recorded at one locality<br />
for each of the five physiographic provinces, and placed<br />
the data in Table 2. The results demonstrate that at each<br />
locality the highest amount of precipitation occurs from<br />
June to October. The percentage of annual precipitation<br />
Table 1. Monthly minimum, mean (in parentheses), maximum, and annual temperature data (in °C) for the physiographic provinces<br />
of Michoacán, Mexico. Localities and their elevation for each of the provinces are as follows: Coastal Plain (Lázaro Cárdenas, 50<br />
m); Balsas-Tepalcatepec Depression (Apatzingán, 320 m); Sierra Madre del Sur (Coalcomán de Vázquez Pallares, 1,100 m); Central<br />
Plateau (Morelia, 1,915 m); Transverse Volcanic Axis (Pátzcuaro, 2,035 m). Data (1971–2000) from the Sistema Meteorológico Nacional,<br />
Michoacán (smn.cna.gob.mx/index).<br />
Physiographic<br />
Province<br />
Coastal Plain<br />
Balsas-<br />
Tepalcatepec<br />
Depression<br />
Sierra Madre<br />
del Sur<br />
Jan. Feb. March April May June July Aug. Sept. Oct. Nov. Dec. Annual<br />
20.6<br />
(26.6)<br />
32.6<br />
16.7<br />
(24.6)<br />
32.5<br />
10.2<br />
(19.9)<br />
29.7<br />
Central Plateau 6.8<br />
(15.8)<br />
24.7<br />
Transverse<br />
Volcanic Axis<br />
3.3<br />
(12.9)<br />
22.5<br />
20.6<br />
(26.8)<br />
33.1<br />
17.6<br />
(25.9)<br />
34.1<br />
10.7<br />
(20.8)<br />
30.9<br />
7.6<br />
(17.0)<br />
26.4<br />
4.0<br />
(14.1)<br />
24.1<br />
20.8<br />
(27.0)<br />
33.2<br />
19.1<br />
(27.7)<br />
36.3<br />
11.6<br />
(22.1)<br />
32.7<br />
9.6<br />
(19.0)<br />
28.4<br />
5.4<br />
(16.0)<br />
26.6<br />
21.2<br />
(27.3)<br />
33.5<br />
20.7<br />
(29.2)<br />
37.6<br />
12.3<br />
(23.5)<br />
34.6<br />
11.1<br />
(20.4)<br />
29.7<br />
7.3<br />
(17.8)<br />
28.2<br />
22.8<br />
(28.3)<br />
33.8<br />
22.3<br />
(30.3)<br />
38.3<br />
14.3<br />
(24.8)<br />
35.3<br />
12.6<br />
(21.7)<br />
30.9<br />
9.4<br />
(19.1)<br />
28.7<br />
23.9<br />
(28.5)<br />
33.1<br />
22.7<br />
(29.1)<br />
35.6<br />
17.9<br />
(25.1)<br />
32.4<br />
13.3<br />
(21.2)<br />
29.1<br />
12.5<br />
(19.5)<br />
26.4<br />
23.4<br />
(28.0)<br />
32.7<br />
21.6<br />
(27.3)<br />
33.1<br />
18.2<br />
(24.1)<br />
30.1<br />
12.8<br />
(19.6)<br />
26.5<br />
12.0<br />
(18.0)<br />
23.9<br />
23.7<br />
(28.1)<br />
32.6<br />
21.6<br />
(27.3)<br />
33.1<br />
17.4<br />
(23.8)<br />
30.2<br />
13.1<br />
(19.8)<br />
26.4<br />
11.9<br />
(18.0)<br />
24.1<br />
23.3<br />
(27.7)<br />
32.0<br />
21.7<br />
(27.3)<br />
33.0<br />
17.7<br />
(23.8)<br />
30.0<br />
12.9<br />
(19.4)<br />
26.0<br />
11.5<br />
(17.7)<br />
23.9<br />
23.5<br />
(28.1)<br />
32.6<br />
21.5<br />
(27.7)<br />
33.8<br />
16.7<br />
(23.7)<br />
30.8<br />
11.3<br />
(18.7)<br />
26.1<br />
9.2<br />
(16.7)<br />
24.1<br />
22.7<br />
(27.9)<br />
33.2<br />
19.5<br />
(26.4)<br />
33.3<br />
13.9<br />
(22.2)<br />
30.4<br />
9.3<br />
(17.7)<br />
26.2<br />
5.9<br />
(14.8)<br />
23.7<br />
21.1<br />
(27.1)<br />
33.2<br />
17.7<br />
(25.1)<br />
32.5<br />
11.9<br />
(21.0)<br />
30.0<br />
7.3<br />
(16.4)<br />
25.5<br />
4.3<br />
(13.4)<br />
22.6<br />
22.3<br />
(27.6)<br />
33.0<br />
20.2<br />
(27.3)<br />
34.4<br />
14.4<br />
(22.9)<br />
31.4<br />
10.6<br />
(18.9)<br />
27.2<br />
8.1<br />
(16.5)<br />
24.9<br />
Table 2. Monthly and annual precipitation data (in mm.) for the physiographic provinces of Michoacán, Mexico. Localities and<br />
their elevation for each of the provinces are as follows: Coastal Plain (Lázaro Cárdenas, 50 m); Sierra Madre del Sur (Coalcomán<br />
de Vázquez Pallares, 1,100 m); Balsas-Tepalcatepec Depression (Apatzingán, 320 m); Transverse Volcanic Axis (Pátzcuaro, 2,035<br />
m); Central Plateau (Morelia, 1,915 m). The shaded area indicates the months of the rainy season. Data taken from Servicio<br />
Meteorológico Nacional, Michoacán (smn.cna.gob.mx/index).<br />
Physiographic Jan. Feb. March Apr. May June July Aug. Sept. Oct. Nov. Dec. Annual<br />
Province<br />
Coastal Plain 7.5 0.4 1.0 0.0 17.0 240.4 269.0 257.0 374.2 150.1 23.7 34.0 1,374.3<br />
Balsas-<br />
Tepalcatepec 19.8 22.0 9.0 2.5 24.1 138.0 167.9 160.8 133.6 78.8 36.9 15.3 808.7<br />
Depression<br />
Sierra Madre del 33.7 42.8 24.8 7.8 37.2 272.2 284.1 258.0 225.7 166.8 93.0 42.1 1,488.2<br />
Sur<br />
Central Plateau 15.8 5.6 7.5 9.9 37.9 146.5 166.1 167.8 131.6 51.6 10.4 4.2 754.9<br />
Transverse<br />
Volcanic Axis 27.1 5.0 5.1 9.7 37.8 150.3 219.6 204.1 157.9 71.2 17.6 13.4 918.8<br />
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during this period ranges from 81.1% at Coalcomán in<br />
the Sierra Madre del Sur to 93.9% at Lázaro Cárdenas<br />
on the Coastal Plain (mean 86.9%). Generally, the driest<br />
month is April (except on the Central Plateau, where it<br />
is December) and the wettest month is July (except on<br />
the Central Plateau, where it is August). Annual precipitation<br />
is lowest on the Central Plateau, with 754.9 mm<br />
for the capital city of Morelia, and highest at Coalcomán<br />
in the Sierra Madre del Sur, with 1,488.2 mm (Table 2).<br />
Composition of the Herpetofauna<br />
Field surveys and a review of the published literature and<br />
databases yielded a total of 215 species of amphibians<br />
and reptiles for the state of Michoacán (54 amphibians,<br />
161 reptiles). Of the amphibians, 44 are anurans (81.1%,<br />
including the non-native Lithobates catesbeianus), nine<br />
are salamanders (17.0%), and one is a caecilian (1.9%).<br />
Of the 161 reptiles, 153 are squamates (95.0%, including<br />
the non-native Hemidactylus frenatus and Ramphotyphlops<br />
braminus), seven are turtles (4.4%), and one is a<br />
crocodylian (0.6%). The number of species occurring in<br />
Michoacán is 17.5% of the total for the Mexican herpetofauna<br />
(1,227 species; Wilson et al. 2013a,b; Table 3).<br />
Table 3. Composition of the amphibians and reptiles of Mexico<br />
and the state of Michoacán. In each column, the number to the<br />
left is that indicated in Wilson et al. (2013a,b) for the country<br />
of Mexico; the number to the right is that recorded in this study<br />
for the state of Michoacán. These numbers include the marine<br />
and non-native taxa.<br />
Taxa Families Genera Species<br />
Anura 11/9 35/19 237/44<br />
Caudata 4/2 15/2 139/9<br />
Gymnophiona 1/1 1/1 2/1<br />
Subtotals 16/12 51/22 378/54<br />
Squamata 31/21 139/68 798/153<br />
Testudines 9/4 18/5 48/7<br />
Crocodylia 2/1 2/1 3/1<br />
Subtotals 42/26 159/74 849/161<br />
Totals 58/38 210/96 1,227/215<br />
1. Families<br />
The herpetofauna of Michoacán (215 species) is classified<br />
in 38 families (65.5% of the number in Mexico),<br />
with the 54 species of amphibians in 12 of the 16 families<br />
known from the country (75.0%; Wilson et al. 2013a,<br />
b; Table 3). About one-half of the amphibian species are<br />
classified in one of three families (Hylidae, Ranidae, and<br />
Ambystomatidae). The 161 species of reptiles are classified<br />
in 26 families (including the family Gekkonidae,<br />
occupied by a single non-native species, H. frenatus, and<br />
the family Typhlopidae, occupied by a single non-native<br />
species, R. braminus), 61.9% of the 42 families found in<br />
Mexico (Wilson et al. 2013a; Table 3). One-half of the<br />
species of reptiles in the state are classified in one of three<br />
families (Phrynosomatidae, Colubridae, and Dipsadidae).<br />
2. Genera<br />
The herpetofauna of Michoacán is represented by 96<br />
genera (45.7% of the 210 known from Mexico; Wilson et<br />
al. 2013a,b), with the amphibians composed of 22 genera<br />
(43.1% of the 51 known from the country). The reptiles<br />
consist of 74 genera (46.5% of the country total of 159).<br />
The largest amphibian genera are Incilius (four species),<br />
Craugastor (five), Eleutherodactylus (five), Lithobates<br />
(11), and Ambystoma (seven). Together, these 32 species<br />
comprise 59.3% of the amphibians known from the state<br />
(Table 3). The most sizable reptilian genera are Sceloporus<br />
(16), Geophis (nine), Thamnophis (nine), Crotalus<br />
(eight), Aspidoscelis (seven), Phyllodactylus (five),<br />
Plestiodon (five), Coniophanes (five), and Leptodeira<br />
(five). These 69 species constitute 42.9% of the reptiles<br />
known from the state (Table 3).<br />
3. Species<br />
Mexico is home to 378 amphibian species, of which<br />
54 (14.3%) occur in Michoacán (Table 3). Anurans are<br />
better represented in the state (18.6% of 237 Mexican<br />
species) than salamanders (6.5% of 139). Only two caecilian<br />
species are known from Mexico, and one occurs<br />
in Michoacán (50.0%). Mexico also is inhabited by 849<br />
reptile species, of which 161 (19.0%) are found in Michoacán.<br />
Squamates are somewhat better represented in<br />
the state (19.2% of 798) than turtles (14.6% of 48). Only<br />
three crocodylian species occur in Mexico, and one is<br />
found in Michoacán (Table 3).<br />
Patterns of Physiographic Distribution<br />
We recognize five physiographic provinces in Michoacán<br />
(Fig. 1), and their herpetofaunal distribution is indicated<br />
in Table 4 and summarized by family in Table 5.<br />
Of the 215 species recorded from the state, 100<br />
(46.5%, 24 amphibians, 76 reptiles) are limited in distribution<br />
to a single physiographic province. In addition,<br />
64 (29.8%, 15 amphibians, 49 reptiles) are known<br />
from two provinces, 37 (17.2%, eight amphibians, 29<br />
reptiles) from three, 11 (5.1%, seven amphibians, four<br />
reptiles) from four, and only three (1.4%, 0 amphibians,<br />
three reptiles) from all five provinces (Table 4). In both<br />
amphibians and reptiles, the number of species steadily<br />
drops from the lowest to the highest occupancy figures.<br />
This distributional feature is significant to conservation<br />
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efforts, inasmuch as the more restricted their distribution<br />
the more difficult it will be to provide species with<br />
effective protective measures. This feature is obvious<br />
when examining the mean occupancy figure, which is<br />
2.0 for amphibians and 1.8 for reptiles, indicating that<br />
on average both groups occupy two or slightly fewer<br />
physiographic provinces. The three most broadly distributed<br />
species (i.e., occurring in all five provinces) all<br />
are reptiles and include the anole Anolis nebulosus, the<br />
whipsnake Masticophis mentovarius, and the mud turtle<br />
Kinosternon integrum (Table 4). The most broadly<br />
distributed amphibians all are anurans and include the<br />
following seven species: the toad Rhinella marina, the<br />
chirping frog Eleutherodactylus nitidus, the treefrogs<br />
Exerodonta smaragdina and Hyla arenicolor, the whitelipped<br />
frog Leptodactylus fragilis, the sheep frog Hypopachus<br />
variolosus, and the leopard frog Lithobates neovolcanicus<br />
(Table 4).<br />
Similar numbers of species have been recorded from<br />
the Balsas-Tepalcatepec Depression, the Sierra Madre<br />
del Sur, and the Transverse Volcanic Axis. A smaller<br />
number occupies the Coastal Plain and the smallest<br />
number is found on the Central Plateau. The distinction<br />
between the species numbers in the higher-species areas<br />
(Balsas-Tepalcatepec Depression, Sierra Madre del Sur,<br />
and the Transvese Volcanic Axis) and the lower-species<br />
areas (Coastal Plain and Central Plateau) is more marked<br />
for amphibians than for reptiles (Table 5).<br />
Table 4. Distribution of the native and non-native amphibian and reptiles of Michoacán, Mexico, by physiographic province.<br />
Taxa<br />
Coastal<br />
Plain<br />
(COP)<br />
Balsas-<br />
Tepalcatepec<br />
Depression<br />
(BTD)<br />
Physiographic Provinces<br />
SierraMadre<br />
del Sur<br />
(SMS)<br />
Transverse<br />
Volcanic Axis<br />
(TVA)<br />
Central<br />
Plateau<br />
(CEP)<br />
Amphibia (54 species)<br />
Anura (44 species)<br />
Bufonidae (6 species)<br />
Anaxyrus compactilis + +<br />
Incilius marmoreus + + +<br />
Incilius occidentalis + +<br />
Incilius perplexus + +<br />
Incilius pisinnus + +<br />
Rhinella marina + + + +<br />
Craugastoridae (5 species)<br />
Craugastor augusti + +<br />
Craugastor hobartsmithi +<br />
Craugastor occidentalis +<br />
Craugastor pygmaeus + + +<br />
Craugastor vocalis + + +<br />
Eleutherodactylidae (5 species)<br />
Eleutherodactylus angustidigitorum +<br />
Eleutherodactylus maurus +<br />
Eleutherodactylus modestus +<br />
Eleutherodactylus nitidus + + + +<br />
Eleutherodactylus rufescens +<br />
Hylidae (11 species)<br />
Agalychnis dacnicolor + + +<br />
Diaglena spatulata + +<br />
Exerodonta smaragdina + + + +<br />
Hyla arenicolor + + + +<br />
Hyla eximia + +<br />
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Hyla plicata +<br />
Plectrohyla bistincta + +<br />
Smilisca baudinii + + +<br />
Smilisca fodiens + +<br />
Tlalocohyla smithii + + +<br />
Trachycephalus typhonius +<br />
Leptodactylidae (2 species)<br />
Leptodactylus fragilis + + + +<br />
Leptodactylus melanonotus + + +<br />
Microhylidae (2 species)<br />
Hypopachus ustus +<br />
Hypopachus variolosus + + + +<br />
Ranidae (11 species)<br />
Lithobates berlandieri +<br />
Lithobates catesbeianus +<br />
Lithobates dunni +<br />
Lithobates forreri + +<br />
Lithobates magnaocularis +<br />
Lithobates megapoda + +<br />
Lithobates montezumae + +<br />
Lithobates neovolcanicus + + + +<br />
Lithobates pustulosus + + +<br />
Lithobates spectabilis +<br />
Lithobates zweifeli + +<br />
Rhinophrynidae (1 species)<br />
Rhinophrynus dorsalis +<br />
Scaphiopodidae (1 species)<br />
Spea multiplicata + +<br />
Caudata (9 species)<br />
Ambystomatidae (6 species)<br />
Ambystoma amblycephalum +<br />
Ambystoma andersoni +<br />
Ambystoma dumerilii +<br />
Ambystoma ordinarium +<br />
Ambystoma rivulare +<br />
Ambystoma velasci +<br />
Plethodontidae (3 species)<br />
Pseudoeurycea bellii +<br />
Pseudoeurycea leprosa +<br />
Pseudoeurycea longicauda +<br />
Gymnophiona (1 species)<br />
Caeciliidae (1 species)<br />
Dermophis oaxacae + +<br />
Reptilia (161 species)<br />
Crocodylia (1 species)<br />
Crocodylidae (1 species)<br />
Crocodylus acutus +<br />
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Squamata (153 species)<br />
Bipedidae (1 species)<br />
Bipes canaliculatus +<br />
Anguidae (6 species)<br />
Abronia deppii +<br />
Barisia imbricata +<br />
Barisia jonesi +<br />
Barisia rudicollis +<br />
Elgaria kingii +<br />
Gerrhonotus liocephalus +<br />
Corytophanidae (1 species)<br />
Basiliscus vittatus + + +<br />
Dactyloidae (2 species)<br />
Anolis dunni + +<br />
Anolis nebulosus + + + + +<br />
Eublepharidae (1 species)<br />
Coleonyx elegans + +<br />
Gekkonidae (1 species)<br />
Hemidactylus frenatus + + +<br />
Helodermatidae (1 species)<br />
Heloderma horridum + + +<br />
Iguanidae (3 species)<br />
Ctenosaura clarki +<br />
Ctenosaura pectinata + + +<br />
Iguana iguana + + +<br />
Mabuyidae (1 species)<br />
Marisora brachypoda + +<br />
Phrynosomatidae (20 species)<br />
Phrynosoma asio + +<br />
Phrynosoma orbiculare +<br />
Sceloporus aeneus +<br />
Sceloporus asper + + +<br />
Sceloporus bulleri +<br />
Sceloporus dugesii + +<br />
Sceloporus gadoviae + +<br />
Sceloporus grammicus +<br />
Sceloporus heterolepis + +<br />
Sceloporus horridus + + + +<br />
Sceloporus insignis +<br />
Sceloporus melanorhinus + + +<br />
Sceloporus pyrocephalus + + +<br />
Sceloporus scalaris + +<br />
Sceloporus siniferus + +<br />
Sceloporus spinosus + +<br />
Sceloporus torquatus + +<br />
Sceloporus utiformis + + + +<br />
Urosaurus bicarinatus + + + +<br />
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Urosaurus gadovi + +<br />
Phyllodactylidae (5 species)<br />
Phyllodactylus davisi +<br />
Phyllodactylus duellmani + +<br />
Phyllodactylus homolepidurus +<br />
Phyllodactylus lanei + + + +<br />
Phyllodactylus paucituberculatus +<br />
Scincidae (6 species)<br />
Mesoscincus altamirani + +<br />
Plestiodon colimensis + +<br />
Plestiodon copei +<br />
Plestiodon dugesii +<br />
Plestiodon indubitus + +<br />
Plestiodon parvulus +<br />
Sphenomorphidae (1 species)<br />
Scincella assata + + +<br />
Teiidae (8 species)<br />
Aspidoscelis calidipes + +<br />
Aspidoscelis communis + + +<br />
Aspidoscelis costata + +<br />
Aspidoscelis deppei + + +<br />
Aspidoscelis gularis + +<br />
Aspidoscelis lineatissima + + +<br />
Aspidoscelis sacki +<br />
Holcosus undulatus + + +<br />
Xantusiidae (1 species)<br />
Lepidophyma tarascae + +<br />
Boidae (1 species)<br />
Boa constrictor + + +<br />
Colubridae (28 species)<br />
Conopsis biserialis +<br />
Conopsis lineatus + +<br />
Conopsis nasus +<br />
Drymarchon melanurus + + +<br />
Drymobius margaritiferus + + +<br />
Geagras redimitus +<br />
Gyalopion canum +<br />
Lampropeltis ruthveni +<br />
Lampropeltis triangulum +<br />
Leptophis diplotropis + + +<br />
Masticophis flagellum + +<br />
Masticophis mentovarius + + + + +<br />
Masticophis taeniatus + +<br />
Mastigodryas melanolomus + +<br />
Oxybelis aeneus + + +<br />
Pituophis deppei + +<br />
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Pituophis lineaticollis + +<br />
Pseudoficimia frontalis + + +<br />
Salvadora bairdi + +<br />
Salvadora mexicana + +<br />
Senticolis triaspis + +<br />
Sonora michoacanensis + +<br />
Symphimus leucostomus +<br />
Tantilla bocourti +<br />
Tantilla calamarina + + +<br />
Tantilla cascadae +<br />
Trimorphodon biscutatus + + +<br />
Trimorphodon tau + + +<br />
Dipsadidae (33 species)<br />
Coniophanes fissidens + +<br />
Coniophanes lateritius + +<br />
Coniophanes michoacanensis +<br />
Coniophanes piceivittis +<br />
Coniophanes sarae +<br />
Diadophis punctatus +<br />
Dipsas gaigeae +<br />
Enulius flavitorques + +<br />
Enulius oligostichus +<br />
Geophis bicolor +<br />
Geophis dugesii +<br />
Geophis incomptus +<br />
Geophis maculiferus +<br />
Geophis nigrocinctus +<br />
Geophis petersii + +<br />
Geophis pyburni +<br />
Geophis sieboldi +<br />
Geophis tarascae +<br />
Hypsiglena torquata + +<br />
Imantodes gemmistratus +<br />
Leptodeira maculata + + +<br />
Leptodeira nigrofasciata +<br />
Leptodeira septentrionalis +<br />
Leptodeira splendida + + +<br />
Leptodeira uribei +<br />
Pseudoleptodeira latifasciata + +<br />
Rhadinaea hesperia + +<br />
Rhadinaea laureata +<br />
Rhadinaea taeniata +<br />
Sibon nebulata + +<br />
Tropidodipsas annulifera +<br />
Tropidodipsas fasciata +<br />
Tropidodipsas philippii + +<br />
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Elapidae (4 species)<br />
Micrurus distans + +<br />
Micrurus laticollaris +<br />
Micrurus tener +<br />
Pelamis platura +<br />
Leptotyphlopidae (4 species)<br />
Epictia goudotii + +<br />
Rena bressoni +<br />
Rena humilis +<br />
Rena maxima +<br />
Loxocemidae (1 species)<br />
Loxocemus bicolor + +<br />
Natricidae (11 species)<br />
Adelophis copei +<br />
Storeria storerioides + +<br />
Thamnophis cyrtopsis + +<br />
Thamnophis eques + +<br />
Thamnophis melanogaster +<br />
Thamnophis postremus +<br />
Thamnophis proximus +<br />
Thamnophis pulchrilatus +<br />
Thamnophis scalaris +<br />
Thamnophis scaliger + +<br />
Thamnophis validus +<br />
Typhlopidae (1 species)<br />
Ramphotyphlops braminus + + +<br />
Viperidae (10 species)<br />
Agkistrodon bilineatus + + +<br />
Crotalus aquilus +<br />
Crotalus basiliscus + + +<br />
Crotalus culminatus +<br />
Crotalus molossus +<br />
Crotalus polystictus +<br />
Crotalus pusillus + +<br />
Crotalus tancitarensis +<br />
Crotalus triseriatus +<br />
Porthidium hespere +<br />
Xenodontidae (2 species)<br />
Conophis vittatus + + +<br />
Manolepis putnami + +<br />
Testudines (7 species)<br />
Cheloniidae (2 species)<br />
Chelonia mydas +<br />
Lepidochelys olivacea +<br />
Dermochelyidae (1 species)<br />
Dermochelys coriacea +<br />
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Geoemydidae (2 species)<br />
Rhinoclemmys pulcherrima +<br />
Rhinoclemmys rubida + + +<br />
Kinosternidae (2 species)<br />
Kinosternon hirtipes + +<br />
Kinosternon integrum + + + + +<br />
Table 5. Summary of the distributional occurrence of families of amphibians and reptiles in Michoacán by physiographic province.<br />
Families<br />
Number<br />
of<br />
Species<br />
Coastal<br />
Plain<br />
(COP)<br />
Balsas-<br />
Tepalcatepec<br />
Depression<br />
(BTD)<br />
Distributional Occurrence<br />
Sierra Madre<br />
del Sur<br />
(SMS)<br />
Transverse<br />
Volcanic Axis<br />
(TVA)<br />
Central<br />
Plateau<br />
(CEP)<br />
Bufonidae 6 2 4 5 2 2<br />
Craugastoridae 5 — 2 3 5 —<br />
Eleutherodactylidae 5 — 2 3 2 1<br />
Hylidae 11 5 7 6 5 4<br />
Leptodactylidae 2 2 2 2 1 —<br />
Microhylidae 2 1 1 1 1 1<br />
Ranidae 11 — 6 4 7 3<br />
Rhinophrynidae 1 — 1 — — —<br />
Scaphiopodidae 1 — — — 1 1<br />
Subtotals 44 10 25 24 24 12<br />
Ambystomatidae 6 — — — 6 —<br />
Plethodontidae 3 — — — 3 —<br />
Subtotals 9 — — — 9 —<br />
Caeciliidae 1 1 — — 1 —<br />
Subtotals 1 1 — — 1 —<br />
Totals 54 11 25 24 34 12<br />
Crocodylidae 1 1 — — — —<br />
Subtotals 1 1 — — — —<br />
Cheloniidae 2 2 — — — —<br />
Dermochelyidae 1 1 — — — —<br />
Geoemydidae 2 2 1 1 — —<br />
Kinosternidae 2 1 1 1 2 2<br />
Subtotals 7 6 2 2 2 2<br />
Bipedidae 1 — 1 — — —<br />
Anguidae 6 — — 2 4 —<br />
Corytophanidae 1 1 1 1 — —<br />
Dactyloidae 2 1 2 2 1 1<br />
Eublepharidae 1 1 1 — — —<br />
Gekkonidae 1 1 1 1 — —<br />
Helodermatidae 1 1 1 1 — —<br />
Iguanidae 3 2 3 2 — —<br />
Mabuyidae 1 1 1 — — —<br />
Phrynosomatidae 20 6 9 13 12 4<br />
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Phyllodactylidae 5 3 3 2 1 —<br />
Scincidae 6 2 1 3 3 —<br />
Sphenomorphidae 1 1 1 1 — —<br />
Teiidae 8 4 7 6 1 1<br />
Xantusiidae 1 1 1 — — —<br />
Subtotals 58 25 33 34 22 6<br />
Boidae 1 1 1 1 — —<br />
Colubridae 28 11 13 13 15 6<br />
Dipsadidae 33 8 10 19 9 —<br />
Elapidae 4 1 2 1 1 —<br />
Leptotyphlopidae 4 — 4 1 — —<br />
Loxocemidae 1 — 1 1 — —<br />
Natricidae 11 2 1 2 7 3<br />
Typhlopidae 1 — 1 1 1 —<br />
Viperidae 10 3 3 3 6 —<br />
Xenodontidae 2 2 2 1 — —<br />
Subtotals 95 28 38 43 39 9<br />
Totals 161 60 73 79 63 17<br />
Sum Totals 215 71 98 103 97 29<br />
Anurans are more broadly represented in the Balsas-Tepalcatepec Depression, where 25 species classified in all but<br />
one of the nine families occurring in the state are found. These anurans are represented most narrowly on the Coastal<br />
Plectrohyla bistincta. The Mexican fringe-limbed treefrog is<br />
distributed from Durango and Veracruz southward to México<br />
and Oaxaca. Its EVS has been assessed as 9, placing at the<br />
upper end of the low vulnerability category, this species<br />
is considered as Least Concern by IUCN, and as a Special<br />
Protection species by SEMARNAT. This individual came from<br />
San José de las Torres, near Morelia, in Michoacán.<br />
Photo by Javier Alvarado-Díaz.<br />
Plain, where only 10 species assigned to four families<br />
occur. One or more species in the families Bufonidae,<br />
Hylidae, and Microhylidae are distributed in each of the<br />
five provinces (Table 5). As expected, the family Hylidae<br />
is best represented in each of the provinces except for<br />
the Transverse Volcanic Axis, where more ranids (seven<br />
species) than hylids (five) occur. All nine species of<br />
salamanders are limited in occurrence to the Transverse<br />
Volcanic Axis and the single caecilian to the Transverse<br />
Volcanic Axis and the Coastal Plain (Table 5).<br />
Lizards are best represented in the Sierra Madre del<br />
Sur, with 34 species, but the Balsas-Tepalcatepec Depression<br />
falls only one behind, with 33 (Table 5). Both<br />
of these figures comprise more than one-half of the 58<br />
species of lizards known from the state. Fewer than onehalf<br />
of this number occurs on the Coastal Plain (25) and<br />
the Transverse Volcanic Axis (22). Only a few species<br />
(six) occur on the Central Plateau. In the families Dactyloidae,<br />
Phrynosomatidae, and Teiidae, one or more species<br />
is distributed in each of the five provinces (Table 5).<br />
Due to the size of the Phrynosomatidae in Michoacán<br />
(20 species), this family is the best represented in each<br />
of the provinces. Several lizard families are represented<br />
by a single species in each of the provinces, but only<br />
one with a single species (the Bipedidae) is limited to a<br />
single province (Table 5).<br />
The largest number of snake species is known from<br />
the Sierra Madre del Sur, with 43 species. Fewer numbers<br />
are found in the Transverse Volcanic Axis (39), Balsas-Tepalcatepec<br />
Depression (38), Coastal Plain (28),<br />
and the Central Plateau (nine). One or more representatives<br />
of only two snake families, the Colubridae and<br />
Natricidae, are found in each of the five provinces (Table<br />
5). Interestingly, although the Colubridae in Michoacán<br />
is represented by five fewer species than the Dipsadidae,<br />
it is the best-represented family in all of the provinces<br />
except for the Sierra Madre del Sur, in which the Dip-<br />
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Ambystoma velasci. The plateau tiger salamander is found along the Transverse Volcanic Axis in Michoacán and elsewhere, thence<br />
northward into both the Sierra Madre Occidental to northwestern Chihuahua and the Sierra Madre Oriental to southern Nuevo<br />
León. Its EVS has been assigned a value of 10, placing it at the lower end of the medium vulnerability category, its status has been<br />
judged as Least Concern by IUCN, and it is considered a Special Protection species by SEMARNAT. This individual came from<br />
Los Azufres, in the Tranverse Volcanic Axis. Photo by Javier Alvarado-Díaz.<br />
sadidae is the best represented. Only three snake families<br />
are represented by a single species (including the<br />
Typhlopidae, containing the non-native blindsnake Ramphotyphlops<br />
braminus), but in all three cases they occur<br />
in two or three provinces (Table 5).<br />
Relatively few species of turtles have been recorded<br />
in Michoacán, and given that three of the seven are sea<br />
turtles, most of them (six) are known from the Coastal<br />
Plain (obviously, sea turtles come on land for egg deposition).<br />
Only two species of the families Geoemydidae<br />
and/or Kinosternidae are found in the remaining four<br />
provinces (Table 5). The single crocodylian species is<br />
found only in the Coastal Plain (Table 5).<br />
We constructed a Coefficient of Biogeographic Resemblance<br />
(CBR) matrix to examine the herpetofaunal<br />
relationships among the five physiographic provinces<br />
(Table 6). The data in this table demonstrate that the<br />
greatest degree of resemblance (74 species shared, CBR<br />
value of 0.74) occurs between the Balsas-Tepalcatepec<br />
Depression and the Sierra Madre del Sur (Table 6).<br />
Whereas this fact might be considered counterintuitive,<br />
given the elevational distinction between the two areas,<br />
these two provinces broadly contact one another along<br />
the northern and eastern face of the mountain mass (Fig.<br />
1). A greater degree of resemblance might be expected<br />
between the Balsas-Tepalcatepec Depression and the<br />
Coastal Plain, inasmuch as these are relatively low-elevation<br />
areas, but they only contact one another where<br />
the Río Balsas flows onto the coastal plain prior to entering<br />
the Pacific Ocean. As a consequence, these two<br />
provinces share only 44 species and their CBR value is<br />
0.52 (Table 6). Nonetheless, these values are the highest<br />
that the Coastal Plain shares with any of the other four<br />
provinces, with the exception of the Sierra Madre del Sur<br />
(44 species and 0.51). For a similar reason, it might be<br />
expected that the Balsas-Tepalcatepec Depression would<br />
share a relatively large number of species with the Transverse<br />
Volcanic Axis to the north, but this is not the case.<br />
Only 21 species are shared and the CBR value is only<br />
0.22 (Table 6).<br />
One might also presume that the Transverse Volcanic<br />
Axis and the Sierra Madre del Sur would share a sizable<br />
number of montane-distributed species, but the two<br />
provinces only share 29 species and their CBR value is<br />
0.29. The Central Plateau is adjacent to the Transverse<br />
Volcanic Axis and the data in Table 6 demonstrate that<br />
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Table 6. CBR matrix of herpetofaunal relationships for the five physiographic provinces in Michoacán. N = species in each<br />
province; N = species in common between two provinces; N = Coefficients of Biogeographic Resemblance. The formula for this<br />
algorithm is CBR = 2C/N1 + N2, where C is the number of species in common to both provinces, N1 is the number of species in<br />
the first province, and N2 is the number of species in the second province.<br />
COP BTD SMS TVA CEP<br />
COP 71 44 44 9 4<br />
BTD 0.52 98 74 21 11<br />
SMS 0.51 0.74 103 29 9<br />
TVA 0.11 0.22 0.29 97 26<br />
CEP 0.08 0.17 0.14 0.41 29<br />
26 of the 29 species found in the Central Plateau also are<br />
recorded from the Transverse Volcanic Axis, but because<br />
of the disparity in the size of their respective herpetofaunas<br />
their CBR value is only 0.41. Nonetheless, this<br />
is the Central Plateau’s greatest degree of resemblance<br />
with any of the other four provinces.<br />
As opposed to species shared between or among<br />
physiographic provinces, the distribution of some species<br />
is confined to a single province (Table 4), although<br />
sometimes these are more broadly distributed outside the<br />
state. In the Coastal Plain, the following 22 species are<br />
involved:<br />
Trachycephalus typhonius<br />
Hypopachus ustus<br />
Crocodylus acutus<br />
Phyllodactylus davisi<br />
Phyllodactylus homolepidurus<br />
Plestiodon parvulus<br />
Geagras redimitus<br />
Symphimus leucostomus<br />
Coniophanes michoacanensis<br />
Coniophanes piceivittis<br />
Enulius oligostichus<br />
Leptodeira nigrofasciata<br />
Leptodeira uribei<br />
Pelamis platura<br />
Thamnophis proximus<br />
Thamnophis validus<br />
Porthidium hespere<br />
Plestiodon parvulus<br />
Chelonia mydas<br />
Lepidochelys olivacea<br />
Dermochelys coriacea<br />
Rhinoclemmys pulcherrima<br />
In the Balsas-Tepalcatepec Depression, the following<br />
16 species are confined to this province:<br />
Eleutherodactylus maurus<br />
Lithobates berlandieri<br />
Lithobates magnaocularis<br />
Rhinophrynus dorsalis<br />
Bipes canaliculatus<br />
Ctenosaura clarki<br />
Phyllodactylus paucituberculatus<br />
Aspidoscelis sacki<br />
Imantodes gemmistratus<br />
Leptodeira septentrionalis<br />
Micrurus laticollaris<br />
Rena bressoni<br />
Rena humilis<br />
Rena maxima<br />
Thamnophis postremus<br />
Crotalus culminatus<br />
The following 14 species are limited to the Sierra<br />
Madre del Sur, within the state:<br />
Eleutherodactylus modestus<br />
Eleutherodactylus rufescens<br />
Barisia jonesi<br />
Elgaria kingii<br />
Sceloporus bulleri<br />
Sceloporus insignis<br />
Coniophanes sarae<br />
Dipsas gaigeae<br />
Geophis incomptus<br />
Geophis nigrocinctus<br />
Geophis pyburni<br />
Geophis sieboldi<br />
Tropidodipsas annulifera<br />
Tropidodipsas fasciata<br />
The herpetofauna of the Transverse Volcanic Axis in<br />
Michoacán contains the following 47 single-province<br />
species (Lithobates catesbeianus, a non-native species,<br />
is not listed):<br />
Craugastor hobartsmithi<br />
Craugastor occidentalis<br />
Eleutherodactylus angustidigitorum<br />
Hyla plicata<br />
Lithobates dunni<br />
Lithobates spectabilis<br />
Ambystoma amblycephalum<br />
Ambystoma andersoni<br />
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Ambystoma dumerilii<br />
Ambystoma ordinarium<br />
Ambystoma rivulare<br />
Ambystoma velasci<br />
Pseudoeurycea bellii<br />
Pseudoeurycea leprosa<br />
Pseudoeurycea longicauda<br />
Abronia deppii<br />
Barisia imbricata<br />
Barisia rudicollis<br />
Gerrhonotus liocephalus<br />
Phrynosoma orbiculare<br />
Sceloporus aeneus<br />
Sceloporus grammicus<br />
Plestiodon copei<br />
Plestiodon dugesii<br />
Conopsis biserialis<br />
Conopsis nasus<br />
Gyalopion canum<br />
Lampropeltis ruthveni<br />
Lampropeltis triangulum<br />
Tantilla bocourti<br />
Tantilla cascadae<br />
Diadophis punctatus<br />
Geophis bicolor<br />
Geophis dugesii<br />
Geophis maculiferus<br />
Geophis tarascae<br />
Rhadinaea laureata<br />
Rhadinaea taeniata<br />
Micrurus tener<br />
Thamnophis melanogaster<br />
Thamnophis pulchrilatus<br />
Thamnophis scalaris<br />
Crotalus aquilus<br />
Crotalus molossus<br />
Crotalus polystictus<br />
Crotalus tancitarensis<br />
Crotalus triseriatus<br />
Finally, the Central Plateau herpetofauna includes<br />
only one species limited to this province, as follows:<br />
Adelophis copei<br />
In total, of the 212 native species, 100 (47.2%) are<br />
confined to a single physiographic province within the<br />
state. Organizing these single-province species by their<br />
distributional status (Table 7) indicates the following<br />
(listed in order of state endemics, country endemics, and<br />
non-endemic species): Coastal plain (22 total species)<br />
= 1 (4.5%), 10 (45.5%), 11 (50.0%); Balsas-Tepalcate-<br />
Pseudoeurycea bellii. Bell’s false brook salamander occurs from southern Tamaulipas and southern Nayarit southward to Tlaxcala<br />
and Guerrero, Mexico, with a disjunct population found in east-central Sonora and adjacent Chihuahua. Its EVS has been gauged<br />
as 12, placing it in the upper portion of the medium vulnerability category, its status has been judged as Vulnerable by IUCN, and it<br />
is regarded as Threatened by SEMARNAT. This individual was found and photographed on Cerro Tancítaro, Michoacán.<br />
Photo by Javier Alvarado-Díaz.<br />
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pec Depression (16 species) = 3 (18.8%), 7 (43.8%), 6<br />
(37.4%); Sierra Madre del Sur (14 species) = 5 (35.7%), 8<br />
(57.2%), 1 (7.1%); Transverse Volcanic Axis = 8 (17.0%),<br />
32 (68.1%), 7 (14.9%); Central Plateau = 0 (0.0%), 1<br />
(100%), 0 (0.0%). Most of these single-province species<br />
are country-level endemics (58 [58.0%]); and the remaining<br />
are non-endemics (25 [25.0%]) or state-level endemics<br />
(17 [17.0%]).<br />
Conservation Status<br />
system), another developed for use in Central America<br />
(the EVS system, Wilson and Johnson 2010) and later<br />
applied to Mexico (Wilson et al. 2013a,b), and a third<br />
developed for use on a global basis (the IUCN system).<br />
We discuss the application of these systems to the herpetofauna<br />
of Michoacán below.<br />
We employed three systems in creating a comprehensive<br />
view of the conservation status of the amphibians and reptiles<br />
of Michoacán (see Materials and Methods), of which<br />
one was developed for use in Mexico (the SEMARNAT<br />
Table 7. Distributional and conservation status measures for members of the herpetofauna of Michoacán, Mexico. Distributional<br />
Status: SE = endemic to state of Michoacán; CE = endemic to country of Mexico; NE = not endemic to state or country; NN<br />
= non-native. Environmental Vulnerability Score (taken from Wilson et al. 2013a,b): low vulnerability species (EVS of 3–9);<br />
medium vulnerability species (EVS of 10–13); high vulnerability species (EVS of 14–20). IUCN Categorization: CR = Critically<br />
Endangered; EN = Endangered; VU = Vulnerable; NT = Near Threatened; LC = Least Concern; DD = Data Deficient; NE =<br />
Not Evaluated. SEMARNAT Status: A = Threatened; P = Endangered; Pr = Special Protection; NS = No Status. See text for<br />
explanations of the EVS, IUCN, and SEMARNAT rating systems.<br />
Taxa<br />
Distributional<br />
Status<br />
Environmental<br />
Vulnerability<br />
Score<br />
IUCN<br />
Categorization<br />
SEMARNAT<br />
Status<br />
Amphibia (54 species)<br />
Anura (44 species)<br />
Bufonidae (6 species)<br />
Anaxyrus compactilis CE 14 LC NS<br />
Incilius marmoreus CE 11 LC NS<br />
Incilius occidentalis CE 11 LC NS<br />
Incilius perplexus CE 11 EN NS<br />
Incilius pisinnus SE 15 DD NS<br />
Rhinella marina NE 3 LC NS<br />
Craugastoridae (5 species)<br />
Craugastor augusti NE 8 LC NS<br />
Craugastor hobartsmithi CE 15 EN NS<br />
Craugastor occidentalis CE 13 DD NS<br />
Craugastor pygmaeus NE 9 VU NS<br />
Craugastor vocalis CE 13 LC NS<br />
Eleutherodactylidae (5 species)<br />
Eleutherodactylus angustidigitorum SE 17 VU Pr<br />
Eleutherodactylus maurus CE 17 DD Pr<br />
Eleutherodactylus modestus CE 16 VU Pr<br />
Eleutherodactylus nitidus CE 12 LC NS<br />
Eleutherodactylus rufescens SE 17 CR Pr<br />
Hylidae (11 species)<br />
Agalychnis dacnicolor CE 13 LC NS<br />
Diaglena spatulata CE 13 LC NS<br />
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Exerodonta smaragdina CE 12 LC Pr<br />
Hyla arenicolor NE 7 LC NS<br />
Hyla eximia NE 10 LC NS<br />
Hyla plicata CE 11 LC A<br />
Plectrohyla bistincta CE 9 LC Pr<br />
Smilisca baudinii NE 3 LC NS<br />
Smilisca fodiens NE 8 LC NS<br />
Tlalocohyla smithii CE 11 LC NS<br />
Trachycephalus typhonius NE 4 LC NS<br />
Leptodactylidae (2 species)<br />
Leptodactylus fragilis NE 5 LC NS<br />
Leptodactylus melanonotus NE 6 LC NS<br />
Microhylidae (2 species)<br />
Hypopachus ustus NE 7 LC Pr<br />
Hypopachus variolosus NE 4 LC NS<br />
Ranidae (11 species)<br />
Lithobates berlandieri NE 7 LC Pr<br />
Lithobates catesbeianus NN — — —<br />
Lithobates dunni SE 14 EN Pr<br />
Lithobates forreri NE 3 LC Pr<br />
Lithobates magnaocularis CE 12 LC NS<br />
Lithobates megapoda CE 14 VU Pr<br />
Lithobates montezumae CE 13 LC Pr<br />
Lithobates neovolcanicus CE 13 NT A<br />
Lithobates pustulosus CE 9 LC Pr<br />
Lithobates spectabilis CE 12 LC NS<br />
Lithobates zweifeli CE 11 LC NS<br />
Rhinophrynidae (1 species)<br />
Rhinophrynus dorsalis NE 8 LC Pr<br />
Scaphiopodidae (1 species)<br />
Spea multiplicata NE 6 LC NS<br />
Caudata (9 species)<br />
Ambystomatidae (6 species)<br />
Ambystoma amblycephalum SE 13 CR Pr<br />
Ambystoma andersoni SE 15 CR Pr<br />
Ambystoma dumerilii SE 15 CR Pr<br />
Ambystoma ordinarium CE 13 EN Pr<br />
Ambystoma rivulare CE 13 DD A<br />
Ambystoma velasci CE 10 LC Pr<br />
Plethodontidae (3 species)<br />
Pseudoeurycea bellii CE 12 VU A<br />
Pseudoeurycea leprosa CE 16 VU A<br />
Pseudoeurycea longicauda CE 17 EN Pr<br />
Gymnophiona (1 species)<br />
Caeciliidae (1 species)<br />
Dermophis oaxacae CE 12 DD Pr<br />
Reptilia (161 species)<br />
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Crocodylia (1 species)<br />
Crocodylidae (1 species)<br />
Crocodylus acutus NE 14 VU Pr<br />
Squamata (153 species)<br />
Bipedidae (1 species)<br />
Bipes canaliculatus CE 12 LC Pr<br />
Anguidae (6 species)<br />
Abronia deppii CE 16 EN A<br />
Barisia imbricata CE 14 LC Pr<br />
Barisia jonesi SE 16 NE NS<br />
Barisia rudicollis CE 15 EN P<br />
Elgaria kingii NE 10 LC Pr<br />
Gerrhonotus liocephalus NE 6 LC Pr<br />
Corytophanidae (1 species)<br />
Basiliscus vittatus NE 7 NE NS<br />
Dactyloidae (2 species)<br />
Anolis dunni CE 16 LC A<br />
Anolis nebulosus CE 13 LC NS<br />
Eublepharidae (1 species)<br />
Coleonyx elegans NE 9 NE A<br />
Gekkonidae (1 species)<br />
Hemidactylus frenatus NN — — —<br />
Helodermatidae (1 species)<br />
Heloderma horridum NE 11 LC A<br />
Iguanidae (3 species)<br />
Ctenosaura clarki CE 15 VU A<br />
Ctenosaura pectinata CE 15 NE A<br />
Iguana iguana NE 12 NE Pr<br />
Mabuyidae (1 species)<br />
Marisora brachypoda NE 6 NE NS<br />
Phrynosomatidae (20 species)<br />
Phrynosoma asio NE 11 NE Pr<br />
Phrynosoma orbiculare CE 12 LC A<br />
Sceloporus aeneus CE 13 LC NS<br />
Sceloporus asper CE 14 LC Pr<br />
Sceloporus bulleri CE 15 LC NS<br />
Sceloporus dugesii CE 13 LC NS<br />
Sceloporus gadoviae CE 11 LC NS<br />
Sceloporus grammicus NE 9 LC Pr<br />
Sceloporus heterolepis CE 14 LC NS<br />
Sceloporus horridus CE 11 LC NS<br />
Sceloporus insignis CE 16 LC Pr<br />
Sceloporus melanorhinus NE 9 LC NS<br />
Sceloporus pyrocephalus CE 12 LC NS<br />
Sceloporus scalaris NE 12 LC NS<br />
Sceloporus siniferus NE 11 LC NS<br />
Sceloporus spinosus CE 12 LC NS<br />
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Sceloporus torquatus CE 11 LC NS<br />
Sceloporus utiformis CE 15 LC NS<br />
Urosaurus bicarinatus CE 12 LC NS<br />
Urosaurus gadovi CE 12 LC NS<br />
Phyllodactylidae (5 species)<br />
Phyllodactylus davisi CE 16 LC A<br />
Phyllodactylus duellmani SE 16 LC Pr<br />
Phyllodactylus homolepidurus CE 15 LC Pr<br />
Phyllodactylus lanei CE 15 LC NS<br />
Phyllodactylus paucituberculatus SE 16 DD A<br />
Scincidae (6 species)<br />
Mesoscincus altamirani CE 14 DD Pr<br />
Plestiodon colimensis CE 14 DD Pr<br />
Plestiodon copei CE 14 LC Pr<br />
Plestiodon dugesii CE 16 VU Pr<br />
Plestiodon indubitus CE 15 LC NS<br />
Plestiodon parvulus CE 15 DD NS<br />
Sphenomorphidae (1 species)<br />
Sphenomorphus assatus NE 7 NE NS<br />
Teiidae (8 species)<br />
Aspidoscelis calidipes SE 14 LC Pr<br />
Aspidoscelis communis CE 14 LC Pr<br />
Aspidoscelis costata CE 11 LC Pr<br />
Aspidoscelis deppei NE 8 LC NS<br />
Aspidoscelis gularis NE 9 LC NS<br />
Aspidoscelis lineatissima CE 14 LC Pr<br />
Aspidoscelis sacki CE 14 LC NS<br />
Holcosus undulatus NE 7 NE NS<br />
Xantusiidae (1 species)<br />
Lepidophyma tarascae CE 14 DD A<br />
Boidae (1 species)<br />
Boa constrictor NE 10 NE A<br />
Colubridae (28 species)<br />
Conopsis biserialis CE 13 LC A<br />
Conopsis lineata CE 13 LC NS<br />
Conopsis nasus CE 11 LC NS<br />
Drymarchon melanurus NE 6 LC NS<br />
Drymobius margaritiferus NE 6 NE NS<br />
Geagras redimitus CE 14 DD Pr<br />
Gyalopion canum NE 9 LC NS<br />
Lampropeltis ruthveni CE 16 NT A<br />
Lampropeltis triangulum NE 7 NE A<br />
Leptophis diplotropis CE 14 LC A<br />
Masticophis flagellum NE 8 LC A<br />
Masticophis mentovarius NE 6 NE A<br />
Masticophis taeniatus NE 10 LC NS<br />
Mastigodryas melanolomus NE 6 LC NS<br />
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Oxybelis aeneus NE 5 NE NS<br />
Pituophis deppei CE 14 LC A<br />
Pituophis lineaticollis NE 8 LC NS<br />
Pseudoficimia frontalis CE 13 LC Pr<br />
Salvadora bairdi CE 15 LC Pr<br />
Salvadora mexicana CE 15 LC Pr<br />
Senticolis triaspis NE 6 NE NS<br />
Sonora michoacanensis CE 14 LC NS<br />
Symphimus leucostomus CE 14 LC Pr<br />
Tantilla bocourti CE 9 LC NS<br />
Tantilla calamarina CE 12 LC Pr<br />
Tantilla cascadae SE 16 DD A<br />
Trimorphodon biscutatus NE 7 NE NS<br />
Trimorphodon tau CE 13 LC NS<br />
Dipsadidae (33 species)<br />
Coniophanes fissidens NE 7 NE NS<br />
Coniophanes lateritius CE 13 DD NS<br />
Coniophanes michoacanensis SE 17 NE NS<br />
Coniophanes piceivittis NE 7 LC NS<br />
Coniophanes sarae SE 16 DD NS<br />
Diadophis punctatus NE 4 LC NS<br />
Dipsas gaigeae CE 17 LC Pr<br />
Enulius flavitorques NE 5 NE NS<br />
Enulius oligostichus CE 15 DD Pr<br />
Geophis bicolor CE 15 DD Pr<br />
Geophis dugesii CE 13 LC NS<br />
Geophis incomptus SE 16 DD Pr<br />
Geophis maculiferus SE 16 DD Pr<br />
Geophis nigrocinctus CE 15 DD Pr<br />
Geophis petersii CE 15 DD Pr<br />
Geophis pyburni SE 16 DD Pr<br />
Geophis sieboldi CE 13 DD Pr<br />
Geophis tarascae CE 15 DD Pr<br />
Hypsiglena torquata NE 8 LC Pr<br />
Imantodes gemmistratus NE 6 NE Pr<br />
Leptodeira maculata CE 7 LC Pr<br />
Leptodeira nigrofasciata NE 8 LC NS<br />
Leptodeira septentrionalis NE 8 NE NS<br />
Leptodeira splendida CE 14 LC NS<br />
Leptodeira uribei CE 17 LC Pr<br />
Pseudoleptodeira latifasciata CE 14 LC Pr<br />
Rhadinaea hesperia CE 10 LC Pr<br />
Rhadinaea laureata CE 12 LC NS<br />
Rhadinaea taeniata CE 13 LC NS<br />
Sibon nebulatus NE 5 NE NS<br />
Tropidodipsas annulifera CE 13 LC Pr<br />
Tropidodipsas fasciata CE 13 NE NS<br />
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Tropidodipsas philippii CE 14 LC Pr<br />
Elapidae (4 species)<br />
Micrurus distans CE 14 LC Pr<br />
Micrurus laticollaris CE 14 LC Pr<br />
Micrurus tener NE 11 LC NS<br />
Pelamis platura NE — LC NS<br />
Leptotyphlopidae (4 species)<br />
Epictia goudotii NE 3 NE NS<br />
Rena bressoni SE 14 DD Pr<br />
Rena humilis NE 8 LC NS<br />
Rena maxima CE 11 LC NS<br />
Loxocemidae (1 species)<br />
Loxocemus bicolor NE 10 NE Pr<br />
Natricidae (11 species)<br />
Adelophis copei CE 15 VU Pr<br />
Storeria storerioides CE 11 LC NS<br />
Thamnophis cyrtopsis NE 7 LC A<br />
Thamnophis eques NE 8 LC A<br />
Thamnophis melanogaster CE 15 EN A<br />
Thamnophis postremus SE 15 LC NS<br />
Thamnophis proximus NE 7 NE NS<br />
Thamnophis pulchrilatus CE 15 LC NS<br />
Thamnophis scalaris CE 14 LC A<br />
Thamnophis scaliger CE 15 VU A<br />
Thamnophis validus CE 12 LC NS<br />
Typhlopidae (1 species)<br />
Ramphotyphlops braminus NN — — —<br />
Viperidae (10 species)<br />
Agkistrodon bilineatus NE 11 NT Pr<br />
Crotalus aquilus CE 16 LC Pr<br />
Crotalus basiliscus CE 16 LC Pr<br />
Crotalus culminatus CE 15 NE NS<br />
Crotalus molossus NE 8 LC Pr<br />
Crotalus polystictus CE 16 LC Pr<br />
Crotalus pusillus CE 18 EN A<br />
Crotalus tancitarensis SE 19 DD NS<br />
Crotalus triseriatus CE 16 LC NS<br />
Porthidium hespere CE 18 DD Pr<br />
Xenodontidae (2 species)<br />
Conophis vittatus CE 11 LC NS<br />
Manolepis putnami CE 13 LC NS<br />
Testudines (7 species)<br />
Cheloniidae (2 species)<br />
Chelonia mydas NE — EN P<br />
Lepidochelys olivacea NE — VU P<br />
Dermochelyidae (1 species)<br />
Dermochelys coriacea NE — CR P<br />
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Geoemydidae (2 species)<br />
Rhinoclemmys pulcherrima NE 8 NE A<br />
Rhinoclemmys rubida CE 14 NT Pr<br />
Kinosternidae (2 species)<br />
Kinosternon hirtipes NE 10 LC Pr<br />
Kinosternon integrum CE 11 LC Pr<br />
Pseudoeurycea leprosa. The leprous false brook salamander occurs in Veracruz, Puebla, Distrito Federal, México, Morelos,<br />
Guerrero, and Oaxaca. Its EVS has been judged as 16, placing it in the middle of the high vulnerability category, IUCN has assessed<br />
this species as Vulnerable, and it is considered as Threatened by SEMARNAT. This individual was encountered on Cerro Cacique,<br />
near Zitacuaro, in Michoacán. Photo by Oscar Medina-Aguilar.<br />
Abronia deppii. Deppe’s arboreal alligator lizard is found in the mountains of the Transverse Volcanic Axis in Michoacán, México,<br />
and Jalisco. Its EVS has been judged as 16, placing it in the middle of the high vulnerability category, IUCN considers this species<br />
as Endangered, and it has been provided a Threatened status by SEMARNAT. This individual came from San José de las Torres,<br />
near Morelia, in Michoacán. Photo by Javier Alvarado-Díaz.<br />
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Barisia imbricata. In Michoacán, the imbricate alligator lizard occurs in the Transverse Volcanic Axis. The systematics of this<br />
species, however, is currently in flux, and based on indications in recent molecular work this taxon likely will be divided into a<br />
number of species. Its EVS has been estimated as 14, placing it at the lower end of the high vulnerability category, this species has<br />
been judged as Least Concern by IUCN, and given a Special Protected status by SEMARNAT. This individual is from Tacámbaro,<br />
in the Transverse Volcanic Axis of Michoacán. Photo by Oscar Medina-Aguilar.<br />
1. The SEMARNAT system<br />
The application of the SEMARNAT system appears in<br />
NOM-059-SEMARNAT-2010 (available at www.semarnat.gob.mx),<br />
and uses three categories: Endangered (P),<br />
Threatened (A), and Special Protection (Pr). In addition<br />
to these categories, we considered the species left untreated<br />
in the SEMARNAT system as having “No status.” We<br />
listed the SEMARNAT categorizations in Table 7 and<br />
summarized the results of the partitioning of the 212 native<br />
species in Table 8.<br />
Perusal of the tabular data reveals one important conclusion––almost<br />
one-half of the species in Michoacán (98<br />
[46.2%]) are not considered in the SEMARNAT system<br />
(Table 8). The missing species include 27 anurans, 27 lizards,<br />
and 44 snakes, and include the following: all six of<br />
the bufonids, of which five are Mexican endemic species<br />
(one is endemic to Michoacán); all five of the craugastorids,<br />
of which three are Mexican endemics; eight of<br />
11 hylids, of which three are Mexican endemics; one of<br />
two dactyloids, which one is a Mexican endemic; 15 of<br />
20 phrynosomatids, of which 12 are Mexican endemics;<br />
one-half of the 28 colubrids, of which five are Mexican<br />
endemics; 15 of 33 dipsadids, of which eight are Mexican<br />
endemics (two also are state endemics); four of 11 natricids,<br />
of which four are Mexican endemics (one also is a<br />
state endemic); and two of 10 viperids, of which two are<br />
Mexican endemics (one also is a state endemic).<br />
Of the 212 total species, only four (1.9%) are judged<br />
as Endangered (three are sea turtles from the coastal waters<br />
of the state and one is the anguid Abronia deppii).<br />
Thirty-one species (14.6%) are considered as Threatened<br />
and 79 (37.1%) as needing Special Protection (Table 8).<br />
In the end, any system purporting to at least identify<br />
species in need of conservation attention is better than no<br />
system at all. The SEMARNAT system, however, is seriously<br />
deficient because a high percentage of species are<br />
not provided with a conservation status, and a significant<br />
portion of these taxa are state or country level endemics.<br />
We address our concerns in the Conclusions and Recommendations<br />
section.<br />
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Table 8. SEMARNAT categorizations for amphibians and reptiles in Michoacán arranged by families. Non-native species are<br />
excluded.<br />
Families<br />
Number<br />
of<br />
Species<br />
SEMARNAT Categorizations<br />
Endangered (P) Threatened (A) Special<br />
Protection (Pr)<br />
No Status<br />
Bufonidae 6 — — — 6<br />
Craugastoridae 5 — — — 5<br />
Eleutherodactylidae 5 — — 4 1<br />
Hylidae 11 — 1 2 8<br />
Leptodactylidae 2 — — — 2<br />
Microhylidae 2 — — 1 1<br />
Ranidae 10 — 1 6 3<br />
Rhinophrynidae 1 — — 1 —<br />
Scaphiopodidae 1 — — — 1<br />
Subtotals 43 — 2 14 27<br />
Ambystomatidae 6 — 1 5 —<br />
Plethodontidae 3 — 2 1 —<br />
Subtotals 9 — 3 6 —<br />
Caeciliidae 1 — — 1 —<br />
Subtotals 1 — — 1 —<br />
Totals 53 — 5 21 27<br />
Crocodylidae 1 — — 1 —<br />
Subtotals 1 — — 1 —<br />
Cheloniidae 2 2 — — —<br />
Dermochelyidae 1 1 — — —<br />
Geoemydidae 2 — 1 1 —<br />
Kinosternidae 2 — — 2 —<br />
Subtotals 7 3 1 3 —<br />
Bipedidae 1 — — 1 —<br />
Anguidae 6 1 1 3 1<br />
Corytophanidae 1 — — — 1<br />
Dactyloidae 2 — 1 — 1<br />
Eublepharidae 1 — 1 — —<br />
Helodermatidae 1 — 1 — —<br />
Iguanidae 3 — 2 1 —<br />
Mabuyidae 1 — — — 1<br />
Phrynosomatidae 20 — 1 4 15<br />
Phyllodactylidae 5 — 2 2 1<br />
Scincidae 6 — — 4 2<br />
Sphenomorphidae 1 — — — 1<br />
Teiidae 8 — — 4 4<br />
Xantusiidae 1 — 1 — —<br />
Subtotals 57 1 10 19 27<br />
Boidae 1 — 1 — —<br />
Colubridae 28 — 8 6 14<br />
Dipsadidae 33 — — 18 15<br />
Elapidae 4 — — 2 2<br />
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Leptotyphlopidae 4 — — 1 3<br />
Loxocemidae 1 — — 1 —<br />
Natricidae 11 — 5 1 5<br />
Viperidae 10 — 1 6 3<br />
Xenodontidae 2 — — — 2<br />
Subtotals 94 — 15 35 44<br />
Totals 159 4 26 58 71<br />
Sum Totals 212 4 31 79 98<br />
2. The IUCN system<br />
Coleonyx elegans. The elegant banded gecko is broadly distributed on both versants, from southern Nayarit and Veracruz in Mexico<br />
southward to Guatemala and Belize. In Michoacán, it inhabits the Coastal Plain and Balsas-Tepalcatepec Depression physiographic<br />
provinces. Its EVS has been indicated as 9, placing it at the upper end of the low vulnerability category, its IUCN status has not<br />
been assessed, and this gecko is regarded as Threatened by SEMARNAT. This individual came from Colola, on the coast of<br />
Michoacán. Photo by Javier Alvarado-Díaz.<br />
Ctenosaura clarki. The Balsas armed lizard is endemic to the Balsas-Tepalcatepec Depression. Its EVS has been gauged as<br />
15, placing it in the lower portion of the high vulnerability category, this species has been judged as Vulnerable by IUCN, and<br />
considered as Threatened by SEMARNAT. This individual is from Nuevo Centro, Reserva de la Biósfera Infiernillo-Zicuirán, near<br />
the Presa Infiernillo on the Río Balsas in southeastern Michoacán. Photo by Javier Alvarado-Díaz.<br />
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The IUCN system is the most widely used system for categorizing<br />
the conservation status of the world’s organisms,<br />
although it is skewed heavily toward chordate animals,<br />
as assessed by Stuart et al. (2010b). Of the 64,788<br />
described chordate species, 27,882 (43.0%) had been assessed<br />
on the IUCN Red List by the year 2009; comparatively,<br />
only 7,615 of 1,359,365 species of other described<br />
animals had been assessed, a miniscule 0.56%. In fact,<br />
if all of the 1,424,153 animal species treated in Stuart<br />
et al. (2010b) are considered, only 2.5% have been assessed<br />
on the IUCN Red List. This extant situation is not<br />
so much of a criticism of the effectiveness of the IUCN<br />
system, but rather a criticism of the lack of attention given<br />
to conservation of the world’s organisms by humanity<br />
at large (Wilson 2002). As a case in point, Stuart et al.<br />
(2010b) reported that if a provisional target number of<br />
106,979 animal species (only 7.5% of the total number<br />
of described species) were established in attempting to<br />
develop a broader taxonomic base of threatened animal<br />
species, the estimated cost to complete would be about<br />
$36,000,000. Completion of a threatened species assessment,<br />
however, is only the first step toward providing a<br />
given species adequate protection for perpetuity.<br />
We listed the current IUCN Red List categorizations<br />
for the Michoacán herpetofauna in Table 7 and summarized<br />
the results in Table 9. The allocations of the 212<br />
species assessed to the seven IUCN categories are as follows:<br />
Critically Endangered (CR) = 5 species (2.3%); Endangered<br />
(E) = 10 (4.7%); Vulnerable (VU) = 12 (5.6%);<br />
Near Threatened (NT) = 4 (1.9%); Least Concern (LC)<br />
= 127 (60.0%); Data Deficient (DD) = 26 (12.3%); and<br />
Not Evaluated (NE) = 28 (13.2%). These results are typical<br />
of those allocated for all Mexican amphibians and<br />
reptiles (see Wilson et al. 2013a,b). As a consequence,<br />
only 27 of the 213 species (12.7%) occupy the threatened<br />
categories (CR, EN, or VU). Six of every 10 species are<br />
judged at the lowest level of concern (LC). Finally, 54<br />
species (25.5%) have been assessed either as DD or have<br />
not been assessed (NE).<br />
Table 9. IUCN Red List categorizations for amphibian and reptile families in Michoacán. Non-native species are excluded.<br />
Families<br />
Number<br />
of<br />
Species<br />
Critically<br />
Endangered<br />
IUCN Red List categorizations<br />
Endangered Vulnerable Near<br />
Threatened<br />
Least<br />
Concern<br />
Data<br />
Deficient<br />
Not<br />
Evaluated<br />
Bufonidae 6 — 1 — — 4 1 —<br />
Craugastoridae 5 — 1 1 — 2 1 —<br />
Eleutherodactylidae 5 1 — 2 — 1 1 —<br />
Hylidae 11 — — — — 11 — —<br />
Leptodactylidae 2 — — — — 2 — —<br />
Microhylidae 2 — — — — 2 — —<br />
Ranidae 10 — 1 1 1 7 — —<br />
Rhinophrynidae 1 — — — — 1 — —<br />
Scaphiopodidae 1 — — — — 1 — —<br />
Subtotals 43 1 3 4 1 31 3 —<br />
Ambystomatidae 6 3 1 — — 1 1 —<br />
Plethodontidae 3 — 1 2 — — — —<br />
Subtotals 9 3 2 2 — 1 1<br />
Caeciliidae 1 — — — — — 1 —<br />
Subtotals 1 — — — — — 1 —<br />
Totals 53 4 5 6 1 32 5 —<br />
Crocodylidae 1 — — 1 — — — —<br />
Subtotals 1 — — 1 — — — —<br />
Cheloniidae 2 — 1 1 — — — —<br />
Dermochelyidae 1 1 — — — — — —<br />
Geoemydidae 2 — — — 1 — — 1<br />
Kinosternidae 2 — — — — 2 — —<br />
Subtotals 7 1 1 1 1 2 — 1<br />
Bipedidae 1 — — — — 1 — —<br />
Anguidae 6 — 2 — — 3 — 1<br />
Corytophanidae 1 1<br />
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Corytophanidae 1 1<br />
Dactyloidae 2 — — — — 2 — —<br />
Eublepharidae 1 — — — — — — 1<br />
Helodermatidae 1 — — — — 1 — —<br />
Iguanidae 3 — — 1 — — — 2<br />
Mabuyidae 1 — — — — — — 1<br />
Phrynosomatidae 20 — — — — 19 — 1<br />
Phyllodactylidae 5 — — — — 4 1 —<br />
Scincidae 6 — — 1 — 2 3 —<br />
Sphenomorphidae 1 — — — — — — 1<br />
Teiidae 8 — — — — 7 — 1<br />
Xantusiidae 1 — — — — — 1 —<br />
Subtotals 57 — 2 2 — 39 5 9<br />
Boidae 1 — — — — — — 1<br />
Colubridae 28 — — — 1 19 2 6<br />
Dipsadidae 33 — — — — 15 11 7<br />
Elapidae 4 — — — — 4 — —<br />
Leptotyphlopidae 4 — — — — 2 1 1<br />
Loxocemidae 1 — — — — — — 1<br />
Natricidae 11 — 1 2 — 7 — 1<br />
Viperidae 10 — 1 — 1 5 2 1<br />
Xenodontidae 2 — — — — 2 — —<br />
Subtotals 94 — 2 2 2 54 16 19<br />
Totals 151 1 5 6 3 96 21 28<br />
Sum Totals 212 5 10 12 4 127 26 28<br />
Phyllodactylus duellmani. Duellman’s pigmy leaf-toed gecko is endemic to Michoacán, where it is found in the Balsas-Tepalcatepec<br />
Depression and the Sierra Madre del Sur. Its EVS has been assigned a value of 16, placing it in the middle of the high vulnerability<br />
category, this species has been judged as Least Concern by IUCN, and accorded a Special Protection status by SEMARNAT. This<br />
individual was photographed at Nuevo Centro, Reserva de la Biósfera Infiernillo-Zicuirán, near the Presa Infiernillo on the Río<br />
Balsas in southeastern Michoacán. Photo by Oscar Medina-Aguilar.<br />
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Leptodeira uribei. Uribe’s cat-eyed snake is distributed along the coastal plain in<br />
Michoacán, and northward through the lowlands to Jalisco and southward to Oaxaca. Its<br />
EVS has been gauged as 17, placing it in the middle of the high vulnerability category, its<br />
IUCN status has been assessed as Least Concern, and it is considered a Special Protection<br />
species by SEMARNAT. This individual was found at San Mateo, near the Reserva de la<br />
Biosfera Chamela-Cuixmala on the coast of Jalisco. Photo by Javier Alvarado-Díaz.<br />
Thamnophis postremus. The Michoacán gartersnake is a state endemic. Its EVS has been<br />
allocated as 15, placing it in the lower portion of the high vulnerability category, it has<br />
been judged as Least Concern by IUCN, and this species has not been provided a status by<br />
SEMARNAT. This individual came from San Lucas in the Balsas-Tepalcatepec Depression<br />
in Michoacán. Photo by Javier Alvarado-Díaz.<br />
Based on the application of<br />
this system, only a small percentage<br />
of the species in the<br />
state would be scheduled to<br />
receive the greatest amount of<br />
attention. These 27 species include<br />
eight anurans, seven salamanders,<br />
one crocodylian, three<br />
turtles, four lizards, and four<br />
snakes. Whereas most of these<br />
species appear to merit a threatened<br />
status, inasmuch as 16 of<br />
the 27 species are country-level<br />
endemics and six are state-level<br />
endemics (22 species, 81.5%<br />
of the 27), the herpetofauna of<br />
Michoacán is characterized by<br />
a higher level of endemism than<br />
for the entire country of Mexico<br />
(140 of 212 species [66.0%] vs.<br />
736 of 1,227 species [60.0%]).<br />
If endemism can be considered<br />
an important criterion for listing<br />
a species as threatened under the<br />
IUCN system (which it is not, as<br />
this system exists), then a substantial<br />
number of other candidates<br />
are available for choosing<br />
(Table 10), a significant issue<br />
that needs to be addressed.<br />
A similar issue is the number<br />
of species judged as Data<br />
Deficient (Table 9). Of these 26<br />
species, 17 are country and nine<br />
are state level endemics. Assignment<br />
of the DD status leaves<br />
these species in limbo, and requires<br />
additional fieldwork before<br />
applying for a change in a<br />
species’ status. Other papers in<br />
this special Mexico issue have<br />
criticized the use of the DD category,<br />
with Wilson et al. (2013b)<br />
labeling these species as “threat<br />
species in disguise.” The significance<br />
of such species can be ignored<br />
in the “rush to judgment”<br />
that sometimes accompanies<br />
assessments conducted using<br />
the IUCN system (NatureServe<br />
Press Release 2007).<br />
Another problem with the<br />
use of the IUCN system is discussed<br />
in the lead-in paragraph<br />
to this section, i.e., that some<br />
species have not been evaluated<br />
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(the NE species). Given the average cost of producing an<br />
IUCN threat assessment for a single species ($534.12,<br />
according to the figures in Stuart et al. 2010b), it takes a<br />
considerable investment to assign a species to a category<br />
other than NE. Nonetheless, one is left with relegating<br />
such species to a “wastebasket of neglect.” In the case<br />
of the Michoacán herpetofauna, 28 species fall into this<br />
category, including nine lizards and 19 snakes (Table<br />
9). To be fair, the distributions of most of these species<br />
(21) extends outside of Mexico and thus were assessed<br />
in a Central American Workshop held in May of 2012 in<br />
Costa Rica (Rodríguez et al. 2013). At that workshop,<br />
most of these species were assigned an LC status.<br />
Adding more species to the LC category is not necessarily<br />
a beneficial step, inasmuch as this category<br />
was described as a “dumping ground” by Wilson et<br />
al. (2013b), who opined that “a more discerning look<br />
would demonstrate that many of these species should be<br />
partitioned into IUCN categories other than LC,” e.g.,<br />
the threat categories and NT. Currently, 127 of the 212<br />
native species of amphibians and reptiles (59.9%) are<br />
placed in the LC category (Table 9), which includes 31<br />
anurans, one salamander, two turtles, 39 lizards, and 54<br />
snakes. We question these assignments on the basis that<br />
83 of these species are country-level endemics, and three<br />
(Phyllodactylus duellmani, Aspidoscelis calidipes, and<br />
Thamnophis postremus) also are state-level endemics<br />
(Table 7).<br />
Table 10. Summary of the distributional status of amphibian and reptile families in Michoacán.<br />
Families<br />
Number<br />
of<br />
Species<br />
Non-endemic<br />
(NE)<br />
Distributional Status<br />
Country<br />
Endemic (CE)<br />
State Endemic<br />
(SE)<br />
Non-native<br />
(NN)<br />
Bufonidae 6 1 4 1 —<br />
Craugastoridae 5 2 3 — —<br />
Eleutherodactylidae 5 — 3 2 —<br />
Hylidae 11 5 6 — —<br />
Leptodactylidae 2 2 — — —<br />
Microhylidae 2 2 — — —<br />
Ranidae 11 2 7 1 1<br />
Rhinophrynidae 1 1 — — —<br />
Scaphiopodidae 1 1 — — —<br />
Subtotals 44 16 23 4 1<br />
Ambystomatidae 6 — 3 3 —<br />
Plethodontidae 3 — 3 — —<br />
Subtotals 9 — 6 3<br />
Caeciliidae 1 — 1 — —<br />
Subtotals 1 — 1 — —<br />
Totals 54 16 30 7 1<br />
Crocodylidae 1 1 — — —<br />
Subtotals 1 1 — — —<br />
Cheloniidae 2 2 — — —<br />
Dermochelyidae 1 1 — — —<br />
Geoemydidae 2 1 1 — —<br />
Kinosternidae 2 1 1 — —<br />
Subtotals 7 5 2 —<br />
Bipedidae 1 — 1 — —<br />
Anguidae 6 2 3 1 —<br />
Corytophanidae 1 1 — — —<br />
Dactyloidae 2 — 2 — —<br />
Eublepharidae 1 1 — — —<br />
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Gekkonidae 1 — — — 1<br />
Helodermatidae 1 1 — — —<br />
Iguanidae 3 1 2 — —<br />
Mabuyidae 1 1 — — —<br />
Phrynosomatidae 20 5 15 — —<br />
Phyllodactylidae 5 — 3 2 —<br />
Scincidae 6 — 6 — —<br />
Sphenomorphidae 1 1 — — —<br />
Teiidae 8 3 4 1 —<br />
Xantusiidae 1 — 1 — —<br />
Subtotals 58 16 37 4 1<br />
Boidae 1 1 — — —<br />
Colubridae 28 12 15 1 —<br />
Dipsadidae 33 9 19 5 —<br />
Elapidae 4 2 2 — —<br />
Leptotyphlopidae 4 2 1 1 —<br />
Loxocemidae 1 1 — — —<br />
Natricidae 11 3 7 1 —<br />
Typhlopidae 1 — — — 1<br />
Viperidae 10 2 7 1 —<br />
Xenodontidae 2 — 2 — —<br />
Subtotals 95 32 53 9 1<br />
Totals 161 54 92 13 2<br />
Sum Totals 215 70 122 20 3<br />
3. The EVS system<br />
Rena bressoni. The Michoacán slender blindsnake is a state endemic, and its distribution is limited to the Balsas-Tepalcatepec<br />
Depression. Its EVS has been estimated as 14, placing it at the lower end of the high vulnerability category, it has been judged as<br />
Data Deficient by IUCN, and SEMARNAT considers it a Special Protection species. This individual was found in the municipality<br />
of Tacámbaro in Michoacán. Photo by Oscar Medina-Aguilar.<br />
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Crotalus basiliscus. The west coast Mexican rattlesnake is distributed from southern<br />
Sonora to northwestern Michoacán. In Michoacán, it is found in the Coastal Plain, Sierra<br />
Madre del Sur, and the Balsas-Tepalcatepec Depression physiographic provinces. Its EVS<br />
has been reported as 16, placing it in the middle of the high vulnerability category, it has<br />
been assessed as Least Concern by IUCN, and it is regarded as a Special Protection species<br />
by SEMARNAT. This individual is from San Mateo, on the coast of Jalisco.<br />
Photo by Oscar Medina-Aguilar.<br />
Crotalus pusillus. The Tancitaran dusky rattlesnake is found in the Sierra de Coalcomán<br />
region of the Sierra Madre del Sur and the western portion of the Transverse Volcanic Axis.<br />
Its EVS has been estimated as 18, placing it in the upper portion of the high vulnerability<br />
category, it has been assessed as Endangered by IUCN, and it is considered as Threatened<br />
by SEMARNAT. This individual came from Cerro Tancítaro, the highest mountain in<br />
Michoacán, located in the west-central portion of the state. Photo by Javier Alvarado-Díaz.<br />
The EVS (Environmental Vulnerability<br />
Score) system of conservation<br />
assessment first was<br />
applied to the herpetofauna of<br />
Honduras by Wilson and Mc-<br />
Cranie (2004). Since that time,<br />
this system has been applied<br />
to the herpetofaunas of Belize<br />
(Stafford et al. 2010), Guatemala<br />
(Acevedo et al. 2010),<br />
Nicaragua (Sunyer and Köhler<br />
2010), Costa Rica (Sasa et al.<br />
2010), and Panama (Jaramillo et<br />
al. 2010). In this special Mexico<br />
issue, the EVS measure also<br />
has been applied to the herpetofauna<br />
of Mexico (Wilson et al.<br />
2013a,b).<br />
In this paper, we utilized the<br />
scores computed by Wilson et al<br />
(2013a,b), which are indicated<br />
in Table 7 and summarized in<br />
Table 11 for the 208 species for<br />
which the scores are calculable.<br />
We arranged the resultant scores<br />
into three categories (low, medium,<br />
and high vulnerability),<br />
which were established by Wilson<br />
and McCranie (2004).<br />
The EVS for members of the<br />
Michoacán herpetofauna range<br />
from 3 to 19 (Table 11). The<br />
lowest score of 3 was calculated<br />
for three anurans (the bufonid<br />
Rhinella marina, the hylid<br />
Smilisca baudinii, and the ranid<br />
Lithobates forreri) and one<br />
snake (the leptotyphlopid Epictia<br />
goudotii). The highest value<br />
of 19 was assigned to the viperid<br />
Crotalus tancitarensis.<br />
The summed scores for the<br />
entire herpetofauna vascillate<br />
over the range, but still generally<br />
rise from the lower scores<br />
of 3 through 5 to peak at 14 and<br />
decline thereafter (Table 11).<br />
Similar patterns are seen for amphibians<br />
and reptiles separately,<br />
although the species numbers<br />
for amphibians peak at an EVS<br />
of 13 instead of 14, as is the case<br />
for reptiles.<br />
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Table 11. Environmental Vulnerability Scores (EVS) for amphibian and reptile species in Michoacán, arranged by family. Shaded area to<br />
the left encompasses low vulnerability scores, and to the right high vulnerability scores.<br />
Families<br />
Number<br />
of<br />
Environmental Vulnerability Scores<br />
Species<br />
3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19<br />
Bufonidae 6 1 — — — — — — — 3 — — 1 1 — — — —<br />
Craugastoridae 5 — — — — — 1 1 — — — 2 — 1 — — — —<br />
Eleutherodactylidae 5 — — — — — — — — — 1 — — — 1 3 — —<br />
Hylidae 11 1 1 — — 1 1 1 1 2 1 2 — — — — — —<br />
Leptodactylidae 2 — — 1 1 — — — — — — — — — — — — —<br />
Microhylidae 2 — 1 — — 1 — — — — — — — — — — — —<br />
Ranidae 10 1 — — — 1 — 1 — 1 2 2 2 — — — — —<br />
Rhinophrynidae 1 — — — — — 1 — — — — — — — — — — —<br />
Scaphiopodidae 1 — — — 1 — — — — — — — — — — — — —<br />
Subtotals 43 3 2 1 2 3 3 3 1 6 4 6 3 2 1 3 — —<br />
Subtotals % — 7.0 4.6 2.3 4.6 7.0 7.0 7.0 2.3 14.0 9.3 14.0 7.0 4.6 2.3 7.0 — —<br />
Ambystomatidae 6 — — — — — — — 1 — — 3 — 2 — — — —<br />
Plethodontidae 3 — — — — — — — — — 1 — — — 1 1 — —<br />
Subtotals 9 — — — — — — — 1 — 1 3 — 2 1 1 — —<br />
Subtotals % — — — — — — — — 11.1 — 11.1 33.3 — 22.2 11.1 11.1 — —<br />
Caeciliidae 1 — — — — — — — — — 1 — — — — — — —<br />
Subtotals 1 — — — — — — — — — 1 — — — — — — —<br />
Subtotals % — — — — — — — — — — 100 — — — — — — —<br />
Totals 53 3 2 1 2 3 3 3 2 6 6 9 3 4 2 4 — —<br />
Totals % — 5.7 3.8 1.9 3.8 5.7 5.7 5.7 3.8 11.3 11.3 16.8 5.7 7.5 3.8 7.5 — —<br />
Crocodylidae 1 — — — — — — — — — — — 1 — — — — —<br />
Subtotals — — — — — — — — — — — 1 — — — — —<br />
Subtotal % — — — — — — — — — — — — 100 — — — — —<br />
Geoemydidae 2 — — — — — 1 — — — — — 1 — — — — —<br />
Kinosternidae 2 — — — — — — — 1 1 — — — — — — — —<br />
Subtotals 4 — — — — — 1 — 1 1 — — 1 — — — — —<br />
Subtotal % — — — — — — 25.0 — 25.0 25.0 — — 25.0 — — — — —<br />
Bipedidae 1 — — — — — — — — — 1 — — — — — — —<br />
Anguidae 6 — — — 1 — — — 1 — — — 1 1 2 — — —<br />
Corytophanidae 1 — — — — 1 — — — — — — — — — — — —<br />
Dactyloidae 2 — — — — — — — — — — 1 — — 1 — — —<br />
Eublepharidae 1 — — — — — — 1 — — — — — — — — — —<br />
Helodermatidae 1 — — — — — — — — 1 — — — — — — — —<br />
Iguanidae 3 — — — — — — — — — 1 — — 2 — — — —<br />
Mabuyidae 1 — — — 1 — — — — — — — — — — — — —<br />
Phrynosomatidae 20 — — — — — — 2 — 5 6 2 2 2 1 — — —<br />
Phyllodactylidae 5 — — — — — — — — — — — 2 3 — — —<br />
Scincidae 6 — — — — — — — — — — — 3 2 1 — — —<br />
Sphenomorphidae 1 — — — — 1 — — — — — — — — — — — —<br />
Teiidae 8 — — — — 1 1 1 — 1 — — 4 — — — — —<br />
Xantusiidae 1 — — — — — — — — — — — 1 — — — — —<br />
Subtotals 57 — — — 2 3 1 4 1 7 8 3 11 9 8 — — —<br />
Subtotal % — — — — 3.5 5.3 1.8 7.0 1.8 12.3 14.0 5.3 19.3 15.7 14.0 — — —<br />
Boidae 1 — — — — — — — 1 — — — — — — — — —<br />
Colubridae 28 — — 1 5 2 2 2 1 1 1 4 5 2 2 — — —<br />
Dipsadidae 33 — 1 2 1 3 3 — 1 — 1 6 3 5 4 3 — —<br />
Elapidae 3 — — — — — — — — 1 — — 2 — — — — —<br />
Leptotyphlopidae 4 1 — — — — 1 — — 1 — — 1 — — — — —<br />
Loxocemidae 1 — — — — — — — 1 — — — — — — — — —<br />
Natricidae 11 — — — — 2 1 — — 1 1 — 1 5 — — — —<br />
Viperidae 10 — — — — — 1 — — 1 — — — 1 4 — 2 1<br />
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Xenodontidae 2 — — — — — — — — 1 — 1 — — — — — —<br />
Subtotals 93 1 1 3 6 7 8 2 4 6 3 11 12 13 10 3 2 1<br />
Subtotal % — 1.1 1.1 3.2 6.4 7.5 8.6 2.2 4.3 6.4 3.2 11.8 12.9 14.0 10.8 3.2 2.2 1.1<br />
Totals 155 1 1 3 8 10 10 6 6 14 11 14 25 22 18 3 2 1<br />
Total % — 0.6 0.6 1.9 5.2 6.5 6.5 3.9 3.9 9.0 7.1 9.0 16.1 14.2 11.6 1.9 1.3 0.6<br />
Sum Totals 208 4 3 4 10 13 13 9 8 20 17 23 28 26 20 7 2 1<br />
Sum Totals % — 1.9 1.4 1.9 4.8 6.3 6.3 4.3 3.8 9.6 8.2 11.1 13.5 12.5 9.6 3.3 1.0 0.5<br />
After organizing the EVS into low, medium, and high categories, a number of conclusions of conservation significance<br />
are apparent. The absolute and relative numbers for each of these categories, from low to high arranged<br />
by major herpetofaunal group, are as follows: anurans<br />
= 17 (39.5%), 17 (39.5%), 9 (21.0%); salamanders = 0<br />
(0.0%), 5 (55.6%), 4 (44.4%); caecilians = 0 (0.0%), 1<br />
(100%), 0 (0.0%); crocodylians = 0 (0.0%), 0 (0.0%), 1<br />
(100%); turtles = 1 (25.0%), 2 (50.0%), 1 (25.0%); lizards<br />
= 10 (17.6%), 19 (33.3%), 28 (49.1%); and snakes<br />
= 28 (30.1%), 25 (26.9%), 40 (43.0%). The highest absolute<br />
and relative numbers for each of the amphibian<br />
groups fall into the medium range, evident when these<br />
numbers are added, as follows: 17 (32.1); 23 (43.4); and<br />
13 (24.5). For the reptile groups, the pattern is different<br />
in that the largest absolute and relative numbers for all<br />
groups, except for turtles, fall into the high range. Summing<br />
these numbers illustrates the general trend for reptiles,<br />
in which numbers increase from low to high: 39<br />
(25.2); 46 (29.7); and 70 (45.1).<br />
The trend seen for reptiles also applies to the herpetofauna<br />
as a whole. Of the 208 total species, 56 (26.9%)<br />
are assigned to the low category, 69 (33.2%) to the medium<br />
category, and 83 (39.9%) to the high category.<br />
In summary, application of the EVS measure to the<br />
members of the herpetofauna of Michoacán demonstrates<br />
starkly that the absolute and relative numbers<br />
increase dramatically from the low category of scores<br />
through the medium category to the high category.<br />
4. Comparing the results of the three<br />
systems<br />
When we compared the results of the three conservation<br />
assessment systems, it was obvious that the EVS is the<br />
only one for which the entire land herpetofauna of Michoacán<br />
can be assessed. The EVS also is the only system<br />
that provides a fair accounting of the distributional<br />
status of species (state-level endemic, country-level<br />
endemic, and non-endemic). Furthermore, this system<br />
is cost-effective, as the authors of this paper and those<br />
of the two on the Mexican herpetofauna in this special<br />
Mexico issue assembled these contributions from their<br />
homes, simply by using the communicative ability of<br />
the Internet. The only disadvantage of the EVS is that<br />
it does not apply to marine species; today, however, a<br />
sizable number of conservation champions at least are<br />
working with marine turtles. Thus, as noted by Wilson<br />
et al. (2013b), “given the geometric pace at which environmental<br />
threats worsen, since they are commensurate<br />
with the rate of human population growth, it is important<br />
to have a conservation assessment measure that can be<br />
applied simply, quickly, and economically to the species<br />
under consideration.” The EVS is the only one of the<br />
three systems we examined with this capacity.<br />
Conclusions and Recommendations<br />
1. Conclusions<br />
A broad array of habitat types are found in Michoacán,<br />
ranging from those at relatively lower elevations along<br />
the Pacific coastal plain and in the Balsas-Tepalcatepec<br />
Depression to those at higher elevations in the Sierra<br />
Madre del Sur, the Transverse Volcanic Axis, and<br />
the Central Plateau. In total, 215 species of amphibians<br />
and reptiles are recorded from the state, including 212<br />
native and three non-native species (Lithobates catesbeianus,<br />
Hemidactylus frenatus, and Ramphotyphlops<br />
braminus). The native amphibians comprise 43 anurans,<br />
nine salamanders, and one caecilian. The native reptiles<br />
constitute 151 squamates (including the marine Pelamis<br />
platura), seven turtles (including the marine Chelonia<br />
mydas, Dermochelys coriacea, and Lepidochelys olivacea),<br />
and one crocodylian.<br />
With respect to the number of physiographic provinces<br />
inhabited, the numbers drop consistently from the<br />
lowest to the highest occupancy figures (i.e., one through<br />
five). The number of taxa in each of the provinces, in<br />
decreasing order, is as follows: Sierra Madre del Sur (103<br />
species); Balsas-Tepalcatepec Depression (98); Transverse<br />
Volcanic Axis (97); Coastal Plain (71); and Central<br />
Plateau (29). Among the five provinces, the representation<br />
of the major herpetofaunal groups is as follows:<br />
anurans = Balsas-Tepalcatepec Depression; salamanders<br />
= Transverse Volcanic Axis (all species limited here);<br />
caecilians = Sierra Madre del Sur and Transverse Volcanic<br />
Axis (single species limited to these two provinces);<br />
lizards = Sierra Madre del Sur; snakes = Sierra Madre del<br />
Sur; turtles = Coastal Plain; and crocodylians = Coastal<br />
Plain (single species limited here). The degree of herpetofaunal<br />
resemblance is greatest between the Balsas-Te-<br />
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palcatepec Depression and the Sierra Madre del Sur. The<br />
greatest resemblance of the Coastal Plain herpetofauna<br />
also is to that of the Balsas-Tepalcatepec Depression.<br />
Finally, the greatest resemblance of the herpetofauna<br />
of the Transverse Volcanic Axis is to that of the Central<br />
Plateau, and vice versa. Within Michoacán, close to onehalf<br />
of the native herpetofauna is limited in distribution<br />
to a single physiographic province, in the following decreasing<br />
order: Transverse Volcanic Axis, Coastal Plain,<br />
Balsas-Tepalcatepec Depression, Sierra Madre del Sur,<br />
and Central Plateau. Most of these single-province species<br />
also are country-level endemics.<br />
We employed three systems for assessing the conservation<br />
status of members of the Michoacán herpetofauna<br />
(SEMARNAT, IUCN, and EVS). The SEMARNAT system<br />
was developed for use in Mexico by the Secretaría<br />
de Medio Ambiente y Recursos Naturales. Although<br />
widely used in Mexico, when this system is applied to<br />
the herpetofauna of Michoacán it leaves almost onehalf<br />
of the species unassessed (i.e., having “no status”).<br />
Nevertheless, we documented and analyzed the results<br />
applying this system to the herpetofauna of Michoacán.<br />
Given the significantly incomplete coverage of the<br />
SEMARNAT system, we found it insufficiently useful<br />
for our purposes.<br />
The IUCN system is applied and used globally. Its<br />
categories are broadly recognized (e.g., Critically Endangered,<br />
Endangered, and Vulnerable, the three socalled<br />
threat categories). Although this system presently<br />
has been applied to a greater proportion of the herpetofauna<br />
of Michoacán (compared to the SEMARNAT<br />
system), it has not been applied to about 13% of the<br />
species. Furthermore, we question the applicability of<br />
some aspects of this system, especially with regard to<br />
the significant use of the Data Deficient category and<br />
the overuse of the Least Concern category. In addition,<br />
the expense of creating IUCN threat assessments and the<br />
manner in which they are created (e.g., workshops that<br />
bring together workers from far-flung areas of the world<br />
to a single location within the area of evaluation for several<br />
days) often is cost-prohibitive. We also found this<br />
system deficient in presenting a useful appraisal of the<br />
conservation status of Michoacán’s herpetofauna.<br />
The EVS system originally was developed for use<br />
with amphibians and reptiles in Honduras, but later was<br />
expanded for use elsewhere in Central America. In this<br />
Special Mexico Issue of Amphibian & Reptile Conservation,<br />
it was applied to all of the native amphibians and<br />
non-marine reptiles of Mexico (Wilson et al. 2013a,b).<br />
We adopted the scores developed in these two papers for<br />
use with the Michoacán herpetofauna, and analyzed the<br />
results. We discovered that once all of the species were<br />
evaluated using the EVS system and allocated to low,<br />
medium, and high score categories, the number of species<br />
increases strikingly from the low through the medium<br />
to the high category.<br />
2. Recommendations<br />
Porthidium hespere. The western hog-nosed viper inhabits the coastal plain of western<br />
Mexico, from southeastern Colima to central Michoacán. Its EVS has been reported as<br />
18, placing it in the upper portion of the high vulnerability category, it has been judged as<br />
Data Deficient by IUCN, and assigned a Special Protection status by SEMARNAT. This<br />
individual is from Coahuayana on the coast of Michoacán. Photo by Oscar Medina-Aguilar.<br />
Based on our conclusions, a<br />
number of recommendations<br />
follow:<br />
1. Given that the degree of herpetofaunal<br />
endemism in Michoacán<br />
is greater than that for the<br />
country of Mexico, and that a<br />
substantial number of those endemic<br />
species are known only<br />
from the state, the level of protection<br />
afforded to the state’s<br />
herpetofauna is of major conservation<br />
interest. One hundred and<br />
twenty-one species are endemic<br />
at the country level and an additional<br />
20 are endemic at the state<br />
level. Thus, the total for these<br />
two groups is 141 (66.5% of the<br />
total native herpetofauna), a figure<br />
6.5% higher than that for the<br />
country (Wilson et al. 2013a,b).<br />
The species with the most conservation<br />
significance are the 20<br />
state endemics, and we recommend<br />
a conservation assessment<br />
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of the state’s herpetofauna that focuses on the<br />
state- and country-level endemic species.<br />
2. Michoacán contains a sizable number of protected<br />
areas at the global, national, state, and local levels.<br />
Because the distribution of the herpetofauna<br />
in these areas only is being determined, we recommend<br />
that this work be accelerated to form a database<br />
for creating a state-level conservation plan.<br />
3. An evaluation of the level of protection afforded<br />
to the state’s herpetofauna in protected areas<br />
is critical for determining areas with high species<br />
richness, a high number of endemic species, or<br />
species at risk, as well as the degree of overlap<br />
within the various protected areas.<br />
4. We recommend an evaluation of all the protected<br />
areas in the state, based on their ability to support<br />
viable populations of the resident herpetofauna.<br />
5. Once a distributional database is assembled for<br />
the state’s herpetofauna in protected areas, and a<br />
capacity analysis completed, a robust conservation<br />
plan needs to be developed and implemented.<br />
6. Considering that agriculture, logging, and cattle<br />
ranching are the leading factors in the local extirpation<br />
and extinction of ecosystems and their<br />
resident species, and that human-modified environments<br />
now are the dominant landscapes in<br />
the state, the potential for the conservation of the<br />
herpetofauna in these environments needs to be<br />
evaluated. Management strategies that allow for<br />
the maximal numbers of herpetofaunal species to<br />
survive and thrive in these altered landscapes also<br />
need to be defined.<br />
7. Ultimately, humans protect only what they appreciate,<br />
and thus a conservation management<br />
plan must encompass environmental education<br />
programs for all groups of people, especially the<br />
young, as well as the involvement of local people<br />
in implementing these programs.<br />
Acknowledgments.—We are indebted to our colleagues<br />
Jerry D. Johnson and Vicente Mata-Silva for<br />
generously sharing the data accumulated for their papers<br />
on Mexican amphibians and reptiles in this Special Mexico<br />
Issue. We extend our gratitude to Louis W. Porras for<br />
kindly offering his counsel and assistance on a number<br />
of issues that arose while preparing this paper, and to<br />
he and Donald E. Hahn for providing needed literature.<br />
Louis was especially helpful in providing us a remarkable<br />
job of copy-editing our work. We also are grateful<br />
to Craig Hassapakis, the editor of this journal, for his<br />
unflagging encouragement, enthusiasm, and support of<br />
our work on this paper. In addition, we thank Jonatan<br />
Torres for his help in updating the list of amphibians and<br />
reptiles of Michoacán. Finally, we are grateful to Uri<br />
García-Vazquez and Aurelio Ramírez-Bautista for their<br />
helpful reviews of our work. Funding for fieldwork was<br />
provided by the Consejo de Investigación Cientifica,<br />
UMSNH.<br />
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Acevedo M, Wilson LD, Cano EB, Vásquez-Almazán C.<br />
2010. Diversity and conservation status of the Guatemalan<br />
herpetofauna. Pp. 406–435 In: Conservation<br />
of Mesoamerican Amphibians and Reptiles. Editors,<br />
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Addendum<br />
After this paper was placed in proof, we discovered a<br />
report of a new Michoacán record for Coniophanes melanocephalus<br />
(Carbajal-Márquez RA, Quintero-Díaz<br />
GE, and Domínguez-De La Riva MA. 2011. Geographic<br />
distribution. Coniophanes melanocephalus [Black-headed<br />
Stripeless Snake] Herpetological Review 42: 242).<br />
The specimen was found in “subtropical dry forest” at<br />
Hoyo del Aire, Municipality of Taretan, at an elevation<br />
of 887 m. This locality lies within the northernmost finger<br />
of the Balsas-Tepalcatepec Depression in central Michoacán.<br />
The EVS of Coniophanes melanocephalus has<br />
been assessed as 14, placing it in the high vulnerability<br />
category, its IUCN status reported as DD (Wilson et al.<br />
2013), and no status is available in the SEMARNAT system<br />
(www.semarnat.gob.mx).<br />
Received: 26 March 2013<br />
Accepted: 04 June 2013<br />
Published: 03 September 2013<br />
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Physiographic distribution and conservation of Michoacán herpetofauna<br />
Javier Alvarado-Díaz is a herpetologist and professor of vertebrate zoology and herpetology<br />
at the Universidad de Michoacán, México. His main interest in herpetology<br />
is the conservation of Mexican amphibians and reptiles, from sea turtles to montane<br />
snakes. He is a member of the Sistema Nacional de Investigadores and has published<br />
a number of peer-reviewed papers and books on conservation and ecology of<br />
the Mexican herpetofauna.<br />
Ireri Suazo Ortuño is a herpetologist and professor of zoology and herpetology at<br />
the Universidad de Michoacán, México. Her principal interest in herpetology is<br />
the conservation of amphibians and reptiles in human modified landscapes. She<br />
is a member of the Sistema Nacional de Investigadores, and has published peerreviewed<br />
papers on the ecology of tropical herpetofaunal assemblages. She is also<br />
the director of the Instituto de Investigaciones sobre los Recursos Naturales de la<br />
Universidad Michoacana de San Nicolás de Hidalgo.<br />
Larry David Wilson is a herpetologist with lengthy experience in Mesoamerica, totaling<br />
six collective years (combined over the past 47). Larry is the senior editor<br />
of the recently published Conservation of Mesoamerican Amphibians and Reptiles<br />
and a co-author of seven of its chapters. He retired after 35 years of service as<br />
Professor of Biology at Miami-Dade College in Miami, Florida. Larry is the author<br />
or co-author of more than 290 peer-reviewed papers and books primarily on herpetology,<br />
including the 2004 Amphibian & Reptile Conservation paper entitled “The<br />
conservation status of the herpetofauna of Honduras.” His other books include The<br />
Snakes of Honduras, Middle American Herpetology, The Amphibians of Honduras,<br />
Amphibians & Reptiles of the Bay Islands and Cayos Cochinos, Honduras, The<br />
Amphibians and Reptiles of the Honduran Mosquitia, and Guide to the Amphibians<br />
& Reptiles of Cusuco National Park, Honduras. He also served as the Snake Section<br />
Editor for the Catalogue of American Amphibians and Reptiles for 33 years.<br />
Over his career, Larry has authored or co-authored the description of 69 currently<br />
recognized herpetofaunal species and six species have been named in his honor,<br />
including the anuran Craugastor lauraster and the snakes Cerrophidion wilsoni,<br />
Myriopholis wilsoni, and Oxybelis wilsoni.<br />
Oscar Medina-Aguilar graduated from the Facultad de Biología of the Universidad<br />
Michoacana de San Nicolás de Hidalgo in 2011. He studied the herpetofauna of<br />
Tacámbaro, Michoacán, as part of his degree requirements. His interests include the<br />
systematics and distribution of the amphibians and reptiles of México. In 2011, the<br />
results of his study of the herpetofauna of Tacámbaro were published in the Revista<br />
Mexicana de Biodiversidad.<br />
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CONTENTS<br />
Administration, journal information (Instructions to Authors), and copyright notice. ……….…...… Inside front cover<br />
Larry David Wilson—Preface (Amphibian & Reptile Conservation Special Mexico Issue). ..…….………………. i<br />
Jerry D. Johnson, Louis W. Porras, Gordon W. Schuett, Vincente Mata-Silva, and Larry David Wilson.—<br />
Dedications (Amphibian& Reptile Conservation Special Mexico Issue). ………………………………………… iii<br />
Larry David Wilson, Vicente Mata-Silva, and Jerry D. Johnson—A conservation reassessment of the reptiles<br />
of Mexico based on the EVS measure. ……..………………………………………………………..……….. 1<br />
Louis W. Porras, Larry David Wilson, Gordon W. Schuett, and Randall S. Reiserer—A taxonomic reevaluation<br />
and conservation assessment of the common cantil, Agkistrodon bilineatus (Squamata: Viperidae):<br />
a race against time. …………………………………………………………………………………………….<br />
SUPPORTING THE SUSTAINABLE MANAGEMENT<br />
48<br />
Randall S. Reiserer, Gordon W. Schuett, and Daniel D. Beck—Taxonomic reassessment and conservation<br />
OF status AMPHIBIAN of the beaded lizard, Heloderma AND horridum REPTILE (Squamata: Helodermatidae). BIODIVERSITY<br />
……………………………… 74<br />
Larry David Wilson, Jerry D. Johnson, and Vicente Mata-Silva—A conservation reassessment of the amphibians<br />
of Mexico based on the EVS measure. …………………………………………………………………<br />
Javier Alvarado Díaz, Ireri Suazao-Ortuño, Larry David Wilson, and Oscar Medina-Aguilar—Patterns<br />
of physiographic distribution and conservation status of the herpetofauna of Michoacán, Mexico. ………… 128<br />
Table …………………………………………………………………………………………………………………………<br />
of Contents. .…………………………………………………………………………………………….….. Back cover<br />
97<br />
VOLUME 7 2013<br />
NUMBER 1