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Alexander Kieneke and Andreas Schmidt-Rhaesa
1 Gastrotricha
1.1Introduction
The microscopically small gastrotrichs are abundant in
diverse aquatic habitats. Gastrotrichs must have been
among the first small animals studied with early micro-
scopes. Remane (1936) lists some reports from the 18th
century, which likely represent gastrotrich specimens.
At first, gastrotrichs were treated, together with pro-
tozoans, rotifers, and other tiny animals, as “infuso-
rians”, until Ehrenberg (1830) separated gastrotrichs
and rotifers from protozoans. Ehrenberg treated gast-
rotrichs as part of rotifers and only subsequently
researchers recognized the differences between these
two groups. Mečnikow (1865) introduced the name
Gastrotricha.
Originally, gastrotrichs were only found in fresh-
water, until Schultze (1853) found the first marine
species, Turbanella hyalina, in sandy samples from
the island Neuwerk (North Sea). Soon after, Claparéde
(1867) described Hemidasys agaso from the harbour in
Naples (Mediterranean Sea). The main era of the disco-
very of marine species started with Remane’s intensive
investigations of marine sediments in the Kiel Bight
(Baltic Sea) (Remane 1924, 1925a, 1926a, b, 1927a, b,
see also 1927c, 1929, 1936). Today, we know about 780
species, a number that is constantly growing. Still, the
gastrotrich fauna of many places is unknown or has
been sampled only superficially. Gastrotrichs occur in
a variety of freshwater habitats and in the sea, from
the littoral region to the deep sea. In the marine envi-
ronment, gastrotrichs are part of the mesopsammon,
the community of animals living in the pore system
between sand grains. In freshwater, gastrotrichs are
either benthic (mesopsammic or epipelic, respectively)
or live among vegetation, some species are swimming
in the free water.
The first broad account to gastrotrich morphology
was made by Zelinka (1889). Because of the minute
size of gastrotrichs, transmission electron microscopy
(TEM) played an important role to understand their
internal anatomy (see, e.g., Ruppert 1991). The position
of gastrotrichs in the phylogenetic system has changed
several times and still is not solved convincingly.
1.2Morphology
1.2.1General and external morphology
Most gastrotrich species are microscopically small animals
in the size range of a few hundred micrometers. Especially
among Paucitubulatina, there are very small species with
about 70 µm length. The longest gastrotrichs belong to the
macrodasyid genus Megadasys and reach up to 3.5mm in
length (Schmidt 1974). The body form varies quite a bit.
Almost all species in the taxon Paucitubulatina are more
or less tenpin-shaped with a clearly defined head region,
a narrowing neck, and a slightly bulbous trunk (Fig. 1.1
A). Species of Macrodasyida vary much more in shape. A
head and neck region is present in several species, but
often not very distinct. The trunk is usually of equal dia-
meter throughout, giving the animals a shape that is often
called “strap-shaped” (Fig. 1.1 B). Some species are short
and broad and can best be termed “tongue-shaped”. The
chaetonotid genus Neodasys resembles the strap-shaped
macrodasyids in body outline.
In the posterior end, many gastrotrichs have paired
extensions often called feet or, in paucitubulatinans, furca
(Fig. 1.1 A, B). The feet carry one or more pairs of adhesive
tubes (see below). In Paucitubulatina, only one pair of
adhesive tubes is present on the furca. The exceptions are
the absence of feet in swimming chaetonotids in the taxa
Neogosseidae and Dasydytidae as well as reported two
pairs in the genera Dichaetura and Diuronotus (see, e.g.,
Schwank 1990, Todaro etal. 2005). A recent description of
Dichaetura filispina (Suzuki etal. 2013) found one adhesive
tube and a solid spine on each foot, making a reinvestiga-
tion of the other species of the genus desirable. In mac-
rodasyidan species, there is usually more than one adhe-
sive tube on each foot (Fig. 1.1 B). When feet are absent,
the posterior end is rounded or an unpaired tail is present.
This tail is most conspicuous and several times as long
as the trunk in species of the genus Urodasys (e.g., Wilke
1954, Schoepfer-Sterrer 1974). Based on their parsimonious
character optimization, Kieneke etal. (2008a) reconstruc-
ted the stem species of Gastrotricha as an elongate (worm-
shaped), dorsoventrally flattened, benthic-marine animal
with a rounded frontal and a bilobed caudal trunk end.
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2 1Gastrotricha
Further appendage-like extensions of the body wall
occur in some species, such extensions either act as a
basal structure for adhesive tubes or as sensory structu-
res in the head region (see chapter Sensory Structures and
descriptions of genera).
Adhesive tubes are slender extensions, often accom-
panied by a cilium. They have a secretory function (see
below). In chaetonotids of the subtaxon Paucitubula-
tina, they are restricted to the feet, but in macrodasy-
ids and in Neodasys, adhesive tubes occur on various
body regions (Fig. 1.1 A, B). Usually, adhesive tubes are
divided into three major groups (see Fig. 1.1 B). Anterior
adhesive tubes (usually abbreviated TbA) are the tubes
in the head region. Often, they are concentrated in
paired clusters on the ventral side; in some cases, they
originate from a common basis. This basis is sometimes
called “hand” or “fleshy base”. The lateral adhesive
tubes (TbL) are positioned along the body in a lateral
position; they may be few (e.g., in Dactylopodola) or
very many (e.g., in different species of Turbanella). Pos-
terior adhesive tubes (TbP) are those tubes present on
feet or, when feet are absent, on the posterior end of
the animals. In addition to the TbL, there may also be
dorsal (TbD), dorsolateral (TbDL), ventrolateral (TbVL),
or even ventral (TbV) adhesive tubes arranged along the
entire body or restricted to certain regions of the trunk.
The stem species of Gastrotricha at least had adhesive
tubes in the lateral (TbL) and posterior (TbP) arrange-
ments (Kieneke etal. 2008a).
The mouth opening is terminal or subterminal on the
anterior tip of the animal. In some species, it leads to a
funnel- or barrel-shaped buccal cavity. In some species
(e.g., from the genera Diplodasys, Oregodasys, Ptychos-
tomella, and Tetranchyroderma), the mouth opens very
broad and occupies almost the entire anterior end, dor-
sally shielded by the so-called oral hood.
Very characteristic and important for determination
is the covering of the body by cilia and cuticular struc-
tures. The restriction of locomotory cilia to the ventral
side of the animals is the name-giving feature of gast-
rotrichs (Fig. 1.2 D–H). Cilia occur as a broad field,
as transverse rows, as isolated paired patches, or as
paired longitudinal bands in the trunk region (Remane
1936). In the head region, they usually cover the entire
ventral surface. An exception occurs in species of the
Xenotrichulidae; here, cilia in the anterior region and in
the midtrunk region are tightly packed together and form
so-called cirri (Fig. 1.1 A). Further, isolated and often stiff
100 µm
50 µm
AB
TbA
cir
TbP
TbP
TbL
fu
Fig. 1.1: Gross body organization of Gastro-
tricha. (A) Xenotrichula velox (Paucitubula-
tina) from Tulip Beach, Lee Stocking Island
(Bahamas), ventral view. (B) Turbanella
hyalina (Macrodasyida) from the intertidal
at Schillig, Northern Germany, ventral view.
(A and B) differential interference contrast
(DIC). Abbreviations: cir, ventral locomotorc
cirri; fu, furca; TbA, anterior adhesive tubes;
TbL, lateral adhesive tubes; TbP, posterior
adhesive tubes.
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1.2Morphology 3
50 µm
50 µm25 µm
25 µm
25 µm
100 µm
100 µm100 µm
AB
lci
C
D
EF GH
lci
lci
sp
sci sci
lci
lci
sci
Fig. 1.2: Epidermis and external cilia of Gastrotricha. (A) Neodasys uchidai (Multitubulatina). Dorsal view of anterior end. Light microscopic
bright field (BF) image. (B) Macrodasys sp. Horizontal view of anterior end. (C) Dorsal view of a juvenile Macrodasys. Note the vacuolated
epidermis cells in A–C (white triangles). (D) Anterior end of a marine Aspidiophorus sp., lateral view. Cilia are restricted to the ventral
side. (B–D) DIC. (E–G) Maximum projections of confocal image stacks. In all 3 species, α-tubulin was stained with fluorescence-labeled
antibodies thereby making visible locomotor and sensory cilia. (E) Pseudostomella roscovita. (F) Thaumastoderma ramuliferum.
(G) Tetranchyroderma sp. (H) Scanning electron microscopic (SEM) image of the ventral surface of a Turbanella subterranea. Note the paired
columns of locomotory cilia. Abbreviations: lci, locomotory cilia; sci, sensory cilia; sp, cilia of spermatozoa.
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4 1Gastrotricha
cilia may be seen in different locations, particularly in
the anterior end. Such cilia are assumed to have sensory
functions (see chapter Sensory Structures).
The entire body is covered by a cuticle, and this
cuticle may form various structures covering the body,
especially on the dorsal side. Such coverings are spines,
scales, or mixtures of these forms. In macrodasyids, scales
occur, for example, in genera such as Lepidodasys and
Diplodasys and spines occur in Acanthodasys. However,
species of Diplodasys additionally possess spines at
the lateral margins while species of Acanthodasys may
display a spiny surface interspersed with tiny scales. Very
conspicuous are cuticular structures in which three to five
curved and pointed branches originate from a common
base. Such structures are called triancres, tetrancres,
and pentancres, and occur in the genera Pseudostomella,
Thaumastoderma, and Tetranchyroderma. In chaetono-
tids, the variability of spines and scales is more diverse
and characteristic for the genera. Spines can originate
from scales (spined scales) or scales can be stalked, i.e.,
they rest on a cuticular rod that is basally connected to
the cuticle that directly lines the epidermis. There are,
however, also many species with a rather thin cuticle
without any of the above-mentioned differentiations. This
condition was probably also present in the last common
ancestor of Gastrotricha (Kieneke etal. 2008a).
1.2.2Integument
The integument of gastrotrichs is composed of a layer of
epidermal cells, the cuticle, and the basal extracellular
matrix (ECM). Also described here are glandular structu-
res associated with the epidermis, in particular the adhe-
sive tubes and epidermal glands.
The epidermis is cellular, and the cells differ in
their structure between the dorsal and the ventral sides
of the animal. The ventral cells are usually cuboidal
ciliated cells; the dorsal cells are flatter, contain less
cytoplasm, and lack cilia (Ruppert 1991). Epidermal
cells are connected to each other by adhaerens junc-
tions and septate junctions (Ruppert 1991). Adhaerens
junctions are mechanical cell-cell connections, and
they occur in various types, of which desmosomes and
hemidesmosomes are the most well-known ones (see
Schmidt-Rhaesa 2007). At least in species of Macroda-
sys, the dorsal epidermal cells are large and contain
a vacuole (Teuchert 1978, Ruppert 1991; Fig. 1.2 A–C),
this condition suggests either a skeletal function during
locomotion (Teuchert 1978) or possibly an adaptation
to the interstitial habitat (Ax 1966). To our knowledge,
gap junctions have not been shown in gastrotrichs but
should be present because they are broadly distributed
among eumetazoans (see, e.g., Schmidt-Rhaesa 2007).
The basal lamina (ECM) is very thin or may even be
absent in gastrotrichs (Ruppert 1991).
The name-giving feature of gastrotrichs is the pre-
sence of locomotory cilia on the ventral side of the
animals (Fig. 1.2 D). Their action allows ciliary gliding,
which is the most important form of locomotion (see
chapter Musculature for muscle-aided locomotion). The
ventral cells have either one cilium per cell (monocili-
ated; Fig. 1.3 A) or more cilia per cell (few up to about
40; multiciliated; Fig. 1.3 B). Monociliated cells occur
in several macrodasyids and in Neodasys, multiciliated
cells in all Paucitubulatina and several macrodasyids
(Rieger 1976, Boaden 1985, Ruppert 1991).
Cilia have the usual axonemal pattern of internal
microtubules (nine peripheral duplets and two single
central ones) and the usual basal structure of nine peri-
pheral triplets of microtubuli (Fig. 1.3 E). An accessory cen-
triole is present and a pair of ciliary rootlets anchors the
cilia in the epidermal cells (Rieger 1976, Ruppert 1991; Fig.
1.3 A, B). In most species, a rostral and a caudal rootlet are
present (see Rieger 1976 for length measurements), only
in the investigated species of Lepidodasys and Xenotri-
chula is the rostral rootlet absent (Rieger 1976). Species of
Xenotrichulidae are peculiar in possessing cirri, which are
bundles of cilia that act as a functional unit (Ruppert 1979;
Fig. 1.3 B). In Xenotrichula, each cirrus as a whole is sur-
rounded by epicuticle (Rieger 1976, Ruppert 1991; Fig. 1.3
B), wheraes this is not the case in the xenotrichulid genus
Draculiciteria (Ruppert 1991). The rootlets of all cilia from
one cirrus form a bundle that is anchored in the epider-
mal cell (Rieger 1976, Ruppert 1991; Fig. 1.3 B). Cirri also
occur in species of the genus Oregodasys, but these have
not been investigated ultrastructurally to date.
The epidermis is covered by a cuticle, and the
pharynx also has a cuticular lining. Further cuticu-
lar structures are rare; in some species of Urodasys, a
cuticular stylet is present in the reproductive system
(Schoepfer-Sterrer 1974). A further presumably cuti-
cular hard part of the reproductive system may be the
recently discovered sclerotic canal inside the caudal
organ of Tetranchyroderma bronchostylus (Atherton &
Hochberg 2012). The body cuticle is composed of two
layers, the endocuticle and the epicuticle. Please note
that the outer layer is often called “exocuticle”, but for
comparative reasons explained below, we prefer the
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1.2Morphology 5
term “epicuticle”. The epicuticle covers the entire body,
including the sensory and locomotory cilia (Fig. 1.3
D, E), which is a very peculiar feature among animals
and much likely an autapomorphy of the Gastrotricha
(Kieneke et al. 2008a). Sensory cilia in Tetranchyro-
derma adelae are more complex; in these case, both
cuticular layers, endocuticle and epicuticle, surround
each cilium (Hochberg 2008). Within the endocuticular
layer, 10 microvilli are embedded (Hochberg 2008).
Among gastrotrich species, the cuticle varies in
thickness and may be smooth or sculptured. The fine
structure of the cuticle was extensively investigated
by Rieger & Rieger (1977) and Ruppert (1991); if not
otherwise indicated, the following data refer to these
sources.
The thickness of the cuticle ranges from 100nm
up to 4 µm. The two layers, epicuticle and endocuticle,
can always be distinguished. The epicuticle is com-
posed of a varying number of layers. Each such layer
is usually trilaminate, which means that it is compo-
sed of an electron-dark outer and inner sublayer and
an electron-lucent middle sublayer. In some species,
this trilaminate substructure of the individual layers
has not been recognized and appears to be a thin
monolayer (observed in representatives of Crasiella,
Dactylopodola, and Urodasys) or a thicker monolayer
(observed in Neodasys, Fig. 1.3 A, E). The number of
layers ranges from 1 to 25, species with an unsculptu-
red (smooth) cuticle have 2 to 25 layers, species with a
sculptured cuticle have 1–18 layers (see, e.g., Balsamo
et al. 2010a for one layer of epicuticle in Diuronotus
aspetos and Musellifer delamarei). The endocuticle is
granular or fibrous in fine structure, and sometimes, a
subdivision is observed. In this case, there is an outer
striated, a middle finely fibrous, and an inner loosely
fibrous substructure.
Especially in species of Paucitubulatina, there are
local thickenings of the cuticle in the head region that have
the appearance of cuticular plates (cephalion, pleura,
hypostomium) (Fig. 1.4 J, K). The presence and shape of
these plates is of taxonomic importance. Ultrastructural
sections through these regions are not available, but there
is a peculiar surface structure of curved ridges on the
cuticular plates on the head of Lepidodermella squamata
observable with the scanning electron microscope (SEM)
(Hochberg 2001).
0.5 µm
1 µm
2 µm
0.5 µm
0.25 µm
AB
CD
E
lci
ve
nu
*
**
*
cir
epc
enc
epc
enc
ve
mi
epc
epc
Fig. 1.3: Ultrastructure of epidermis,
external cilia and cuticle of Gastrotricha.
(A) Neodasys chaetonotoideus
(Multitubulatina), ventral epidermis with
monociliated epithelial cells. Note the
cellular junctions/belt desmosomes
(asterisks) and the basal bodies of 2
cilia (white triangles). (B) Xenotrichula
carolinensis (Paucitubulatina), multiciliary
ventral epidermis cell forming a locomotory
cirrus. Note the bundle of ciliary rootlets
(white triangle). (C) Dorsal epidermis of
Tetranchyroderma sp. (Macrodasyida)
with a pentancre formed by endocuticle
and epicuticle. (D and E) Cross sections of
locomotory cilia covered by epicuticle: (D)
Chaetonotus maximus and (E) Neodasys
chaetonotoideus. (A–E) TEM images of
cross-sectioned specimens. Abbreviations:
cir, locomotory cirrus (compound cilium);
enc, endocuticle; epc, epicuticle; lci,
locomotory cilium; mi, mitochondrium; nu,
nucleus of epidermis cell; ve, electron-dark
vesicles.
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6 1Gastrotricha
When cuticular structures such as spines or scales are
present (Fig. 1.4 A–I), these are formations of the endocu-
ticle. Rieger & Rieger (1977) and Ruppert (1991) recognized
three different types of such structures. In Xenodasys,
the cuticular structures are hollow and include processes
of the epidermis. In all other cases, structures are only
made of cuticular material, and no epidermal compo-
nents extend into them. In macrodasyids (Lepidodasys
and Thaumastodermatidae), cuticular structures are solid
local thickenings in the endocuticle (see Hochberg 2008 as
one example; Fig. 1.3 C). Sometimes a substructure such as
a fine striation or a honeycomb pattern can be observed.
In representatives of Paucitubulatina, cuticular structu-
res are derivates of the outer sublayer of the endocuticle;
they have a homogeneous or finely striated substructure.
In Diuronotus aspetos and Musellifer delamarei, the solid
scales are made up of two electron-dense, homogeneous
layers (Balsamo etal. 2010a). Sometimes scales and spines
of Paucitubulatina are hollow structures, but in contrast
to Xenodasys, they never include epidermal extensions.
The gastrotrich cuticle does not contain chitin
(Neuhaus et al. 1996), and is not molted during deve-
lopment (Ruppert 1991). Despite the fact that molecular
analyses do not favor a close relationship between gast-
rotrichs and cycloneuralians (nematodes and related
groups, see Schmidt-Rhaesa 2013), the structure of the
cuticle appears comparable to some extent. Cycloneu-
ralians probably have an ancestral cuticular structure
composed of three layers, a proteinaceous endocuticle,
a chitinous exocuticle, and a trilaminate epicuticle (see
Schmidt-Rhaesa etal. 1998). The trilaminate epicuticle
and the proteinaceous endocuticle appear comparable
and could argue for a common ancestor of Cycloneuralia
and Gastrotricha. During gastrotrich evolution, the epi-
cuticle becomes multiplied; during cycloneuralian evolu-
tion, an additional layer, the chitinous exocuticle, occurs
(Schmidt-Rhaesa 2002).
In macrodasyids, the epidermis often contains glan-
dular cells (glandulocytes), the so-called epidermal
glands (Fig. 1.5 A–D). Epidermal glands may be arranged
in paired longitudinal rows along the dorsal side of the
animals. Each epidermal gland is composed of a single,
flask-shaped glandulocyte and acts as an individual unit.
Beside the sparsely arranged organelles and a rather big,
10 µm 4 µm 2 µm 5 µm
50 µm 25 µm 50 µm
10 µm
8 µm20 µm 4 µm
AB
CD
E
ce
ep
FGJ
K
HI
hp
ce
Fig. 1.4: Cuticular differentiations of
Gastrotricha. (A) Dorsal tile-like scales
of Diplodasys rothei (Macrodasyida).
(B) Spined scales of Chaetonotus schulzei
(Paucitubulatina). Note the pair of denticles
slightly proximal to the tip of each spine.
(C) Dorsal keeled scales of Aspidiophorus
sp. (Paucitubulatina) (D) Pentancres of
Tetranchyroderma sp. (Macrodasyida).
(E) Another species of Tetranchyroderma
with tetrancres. (F) Keeled scales of
Lepidodasys sp. (Macrodasyida). (G) Slightly
polygonal scales of Draculiciteria tesselata
(Paucitubulatina). (H) Heterolepidoderma
sp. (Paucilubulatina) with keeled scales,
lateral view. (I) Lateral thorn of Diplodasys
rothei. (J) Head region of Chaetonotus
maximus (Paucitubulatina), dorsal view.
(K) Head region of another species of
Chaetonotus, lateral view. Note the “mouth
basket” around the mouth opening.
(A–D and H–K) SEM images. (E–G) DIC
images. Abbreviations: ce, cephalion; ep,
epipleurion; hp, hypopleurion.
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1.2Morphology 7
100 µm
50 µm
20 µm
4 µm
AB C
D
at
eg
eg
eg
eg
eg
mg
Fig. 1.5: Epidermal glands of Macrodasyida.
(A) Diplodasys sp., habitus. Note the slightly
colored epidermal glands. (B) Different
types of epidermal glands of Diplodasys
cf. meloriae. (C) Epidermal glands and
adhesive tubes within the vacuolated
epidermis of Turbanella bocqueti.
(D) Elevated pore of an epidermal gland
of Tetranchyroderma sp. (A) BF-image
(B and C) DIC Images. (D) SEM image.
Abbreviations: at, adhesive tube; eg,
epidermal gland; mg, midgut.
basally positioned nucleus, there are few big secretion
granules with irregularly staining content (Fig. 1.6). Secre-
tion products are released through an apical pore within
the cuticle (Teuchert 1977a, Ruppert 1991). In Turbanella
cornuta, the apical neck of the glandulocyte is formed by
a cellular protrusion that is surrounded by up to 50 micro-
villi, which do not penetrate the cuticle. Further proximal,
10 rings of short microvilli surround the neck of the epider-
mal gland (Fig. 1.6). It is hypothesized that these microvilli
serve as a mechanic protection against pressure from the
surrounding epidermis cells (Teuchert 1977a). In Orego-
dasys katharinae, the glandular system is more complex,
it comprises at least three types of papillae beneath the
cuticle, blunt, triangle-shaped and sensory ones (Hoch-
berg 2010a). Furthermore, insunk glandulocytes are
present. Until now, there is no convincing hypothesis
for the functional role of the epidermal gland system
in macrodasyidan gastrotrichs (Ruppert 1991, but see
Hochberg 2010b).
Conspicuous glandular structures of the Gast-
rotricha are the adhesive tubes (Fig. 1.7), which are
present in different body regions in macrodasyids
and on the posterior end in paucitubulatinan chae-
tonotids. These structures are tube-like extensions of
the body cuticle containing two types of glandulocy-
tes (all information in this section from Tyler & Rieger
1980 and Ruppert 1991. These glandulocytes are basal
to the tubes and extend through the tube to open at
its apical end where the cuticle is broken by one or
more pores. Two different types of glandulocytes are
distinguished (Fig. 1.8 A–B). One produces a secretion
made up of larger, electron-dense vesicles, and this is
called “viscid gland cell” and is assumed to have an
adhesive function. The other glandulocyte produces
smaller vesicles, this is called “releasing gland cell”
and is assumed to dissolve the adhesive secretion
and release the attachment. In the investigated cases,
one releasing gland cell and one to few viscid gland
cells have been observed. They usually open through
one apical pore, but in Tetranchyroderma sp., each
of the two viscid cells has its own pore. The structure
of the adhesive tubes corresponds to the definition of
the “duo-gland adhesive system” (see, e.g., Tyler
1988). Further, glandulocytes (epidermal glands) or
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8 1Gastrotricha
cells, and the releasing gland cell is derived from the
associated sensory cell. Such a scenario also supports
the hypothesis of Neodasys as the earliest branch within
the phylogenetic system of Gastrotricha as proposed by
Kieneke etal. (2008a). The posterior adhesive organs of
Neodasys are also of peculiar structure. The paired caudal
feet include adhesive tubes similar in ultrastructure to the
lateral ones but additionally possess a distal pore lined
by a microvillar border of a specialized myoepithelial cell
(Tyler etal. 1980, Ruppert 1991).
1.2.3Musculature
Solely based on light microscopic investigations, Remane
(1936) already provided a quite detailed understanding of
the muscular system in different species of the Gastrotri-
cha, for instance, in Macrodasys sp., Turbanella cornuta,
Dactylopodola baltica, Chaetonotus sp., Chaetonotus sim-
rothi, Aspidiophorus paradoxus, and Dasydytes ornatus.
Although he was not able to present any data on circular
muscles in Gastrotricha in his slightly earlier monograph
(Remane 1929), the occurrence of this muscle component
could be demonstrated a few years later in taxa such as
Polymerurus, Dactylopodola, Pleurodasys, and Oregoda-
sys (Remane 1936). He concluded that Gastrotricha are
characterized by a musculature consisting of a system of
separate strands of longitudinal and circular muscles in
contrast to the nearly closed muscular sheath below the
epidermis composed of outer circular muscle layer and
inner longitudinal muscle layer in many other vermiform
taxa of the Bilateria, a consideration that is currently
up-to-date. However, some of Remane’s (1936) findings
had to be revised or complemented as well, as new tech-
niques and methods provided a much more detailed view
on muscle arrangement of microscopic animals. The
resolving power of electron microscopy, primarily TEM,
gave a first insight to the ultrastructure and cytomorpho-
logy of single muscle cells of Gastrotricha. Muscle ult-
rastructure was intensely studied in Turbanella cornuta by
Teuchert (1974) and will be reviewed below. Then, the
combination of specific fluorescence staining methods
(e.g., staining of f-actin with fluorochrome-labeled phal-
loidin) with three dimensionally resolving confocal laser
scanning microscopy (or initially conventional epifluore-
scence microscopy) provided a holistic look on the myo-
anatomy of many microscopic invertebrate taxa inclu-
ding the Gastrotricha. Richard Hochberg and Marian K.
Litvaitis were the first to demonstrate the diversity of
muscle arrangement among several gastrotrich species
monociliated sensory cells can be associated with the
adhesive tubes (see chapter Sensory Structures).
A peculiar exception to the structure described above
occurs in the genus Neodasys (Tyler etal. 1980, see also
Ruppert 1991; Fig. 1.7 E). Neodasys has, from a general
appearance, a distribution of adhesive tubes compara-
ble to macrodasyidan species (however, anterior adhe-
sive tubes are absent in Neodasys), but the fine structure
of these tubes is not comparable. The papilliform lateral
tubes in Neodasys contain only one glandulocyte per
tube, this cell has a rudimentary cilium. A ciliated sensory
cell is closely associated with this glandulocyte (Fig. 1.8
C). Tyler etal. (1980) interpret this structure as a kind of
forerunner of the duo-gland adhesive tubes of other gast-
rotrichs. According to this model, the viscid gland cell(s)
of the adhesive tubes are derived from ciliated epidermal
2 µm
mv
di
mv
ed
gc
po
cut
nu
ed
er
sg
sg
mi
gn
cj
Fig. 1.6: Epidermal gland of Turbanella cornuta, schematic. Note
the circularly arranged microvilli on the surface of the neck of the
gland cell. The proximal extension of the gland cell leads to the
basal matrix. Abbreviations: cj, cellular junction (adhaerens
junction and septate junction); cut, cuticle; di, dictyosome;
ed, epidermis; er, endoplasmic reticulum; gc, gland cell;
gn, neck of the gland cell; mi, mitochondria; mv, microvilli;
nu, nucleus; po, pore of the epidermal gland; sg, secretory
granule. (According to figure 5 of Teuchert 1977).
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1.2Morphology 9
100 µm
100 µm
50 µm 50 µm
50 µm
50 µm
30 µm
50 µm
4 µm 4 µm
50 µm
ABCD
E
TbA
TbP
TbVL eg
mo
FG
H
IJ
K
*
*
TbA
TbP
TbVL
Fig. 1.7: Different arrangements of adhesive tubes in Gastrotricha. (A) Tetranchyroderma sp., ventral view of the head.
(B) Posterior trunk end of Macrodasys sp., ventral view. (C) Ventral view of Xenodasys riedli showing the peculiar adhesive
organs or pedicles (asterisks). (D) Rear trunk end of Macrodasys caudatus that is tightly glued to the microscopic slide
(white triangle). (E) Neodasys chaetonotoideus that vigorously adheres to the glass slide and to sediment particles
(triangles). (F) Anterior and posterior end of Megadasys sp., ventral view. (G) Caudal furca of Draculiciteria tesselata
(Paucitubulatina), ventral view. (H) Underside of Diplodasys sp. with ventrolateral adhesive tubes. (I) Ventral side of the
head of Cephalodasys maximus with hand-like arranged anterior adhesive tubes on a “fleshy base”. (J) Posterior lateral
adhesive tubes of Dactylopodola baltica. (K) Posterior adhesive tubes of Tetranchyroderma sp. on a pedicle. (A–C and F–H)
DIC images. (D and E) BF images. (I–K) SEM images. Abbreviations: mo, mouth opening; TbA, anterior adhesive tubes; TbP,
posterior adhesive tubes; TbVL, ventrolateral adhesive tubes.
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10 1Gastrotricha
representing various taxa (Hochberg & Litvaitis 2001a–d,
2003a,Hochberg 2005). Among other findings, these
studies comprise the discovery of helicoidally arranged
muscles that partially enwrap the gut tube (pharynx plus
midgut) and represent a unique character (autapomorphy)
of the Gastrotricha (Hochberg & Litvaitis 2001a). Further-
more, quite a high abundance of circular muscles (in visce-
ral as well as somatic positions) was observed in macroda-
syidan species and in Neodasys (e.g., Hochberg & Litvaitis
2001b, Hochberg 2005), unlike what was anticipated
before by Remane (1936). Hochberg & Litvaitis (2001b) also
tested and demonstrated the phylogenetic value of muscle
characters of Gastrotricha and established a species-
character-matrix. This matrix, which has been expan-
ded by current data since, provides a thorough survey of
general muscle patterns of the Macrodasyida (Tab. 1.1).
Taking the muscular characters of several species
of Macrodasyida and Paucitubulatina and those of two
investigated species of the phylogenetically important
taxon Neodasys (see chapter Phylogeny) into account,
Hochberg (2005) suggests a “primitive organization” of
the gastrotrich musculature, i.e., the character pattern
that was probably present in the last common ancestor
(stem species) of Gastrotricha. According to this scena-
rio, the stem species was provided with muscle strands
in three different orientations, longitudinal, circular, and
helicoidal (Figs. 1.9 and 1.10). The myoepithelial sucking
pharynx (for details of the contractile elements of the
pharynx see below) is surrounded by numerous consecu-
tive visceral muscle rings followed by visceral longitudi-
nal muscle fibers that accompany the whole gut tube from
the terminal mouth opening to the ventral anus. These
visceral longitudinal muscles are located dorsal, lateral,
and ventral to the gut tube. In the intestinal region poste-
rior to the pharynx, the visceral longitudinal muscle fibers
are surrounded by aligned visceral muscle rings. Hence,
the spatial arrangement of visceral longitudinal and vis-
ceral circular muscles is inverted form the pharynx to the
intestine (inner circulars and outer longitudinals versus
inner longitudinals and outer circulars, see Figs. 1.9 B–C,
1.11 C–D). Both circular and longitudinal muscle com-
ponents of the gut tube are enwrapped with a muscu-
lar double helix. Such fibers are crossing on the dorsal,
ventral, and lateral sides of the gut tube (Figs. 1.9 A, 1.10,
1.11 A–B, 1.12 B). The helicoidally arranged muscles do not
span the whole intestine down to the anus but only reach
the midtrunk region in most species (e.g., Hochberg & Lit-
vaitis 2001b, 2003a). Such a pattern can also be assumed
for the stem species of Gastrotricha. In a somatic, ventro-
lateral position, there is a pair of massive longitudinally
arranged muscle bands composed of several closely arran-
3 µm
1 µm
A
vg
B
Cnb
cil
mv
vg
rg
nb
ed
ed
cut cut
cr
bb
cut
gc sc
er
di
nu
mi
nu
Fig. 1.8: Adhesive organs (adhesive tubes) of Gastrotricha.
(A) Longitudinal section (schematic) of a dorsolateral
adhesive tube of Tetranchyroderma sp. consisting of 2
viscid glands and 1 releasing gland. (B) Cross section
of that tube (level indicated by bold line in A). Note the
larger and electron-dark vesicles of the viscid glands and
the smaller and lighter vesicles of the releasing gland. In
Tetranchyroderma sp., each gland cell has its own cuticular
pore. (C) Longitudinal section (schematic) of a lateral
adhesive tube of Neodasys sp. A sensory cell, probably
mechanoreceptive in function, is closely associated with
the single gland cell. A releasing gland is missing in
Neodasys. Abbreviations: bb, basal body; cil, cilium of the
sensory cell; cr, ciliary rootlet; cut, cuticle; di, dictyosome;
ed, epidermis; er, endoplasmic reticulum; gc, gland cell;
mi, mitochondria; mv, microvilli; nb, neurite bundle; nu,
nucleus; rg, releasing gland; sc, sensory cell; vg, viscid
gland. (A and B, According to a TEM micrograph of Tyler &
Rieger 1980; C, modified from Tyler etal. 1980.)
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1.2Morphology 11
Tab. 1.1: Characters related with musculature and muscle arrangement in Macrodasyida.
Character-number according to Hochberg & Litvaitis (b) Source
Somatic
circular
muscles
Visceral
circular
muscles
on
pharynx
Semicircu-
lar muscle
band on
ventral
side of
pharynx
Visceral
circular
muscles
on
intestine
(midgut)
Visceral
longi-
tudinal
muscles
on dorsal
side of
gut tube
Visceral
longi-
tudinal
muscles
on ventral
side of
gut tube
Somatic longi-
tudinal muscle
bands in ventro-
lateral position
(musculus princi-
palis according
to Remane )
Splitting
of mus-
culus
princi-
palis in
midtrunk
region
Anterior
inser-
tion of
musculus
principalis
Cross-
over
muscles
in
caudal
region
Bran-
ches of
musculus
principa-
lis supply
head
region
Heli-
coidal
muscles
enwrap
pharynx
Heli-
coidal
muscles
enwrap
intes-
tine
(midgut)
Muscle
striation
pattern
(see also
Tab. .)
Dactylopo-
dola baltica
At level of
TbA
Cross-
striated
Hochberg
& Litvaitis
(b)
Dolichodasys
elongatus
At level of
TbA
Oblique
striation
Hochberg
& Litvaitis
(b)
Paradasys
sp.
At level of
TbA
aOblique
striation
Leasi etal.
()
Lepidodasys
ligni
? On mouth
rim
Oblique
striation
Hochberg
etal.
()
Macrodasys
caudatus
? On mouth
rim
Oblique
striation
Hochberg
& Litvaitis
(b)
Turbanella
ambronensis
At level of
TbA
b Oblique
striation
Hochberg
& Litvaitis
(b)
Turbanella
sp.
At level of
TbA
Oblique
striation
Leasi etal.
()
Acanthodasys
aculeatus
On mouth
rim
Oblique
striation
Hochberg
& Litvaitis
(b)
Pseudos-
tomella
roscovita
On mouth
rim
Oblique
striation
Hochberg
& Litvaitis
(b)
Tetranchyro-
derma papii
On mouth
rim
Oblique
striation
Hochberg
& Litvaitis
(b)
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12 1Gastrotricha
Character-number according to Hochberg & Litvaitis (b) Source
Somatic
circular
muscles
Visceral
circular
muscles
on
pharynx
Semicircu-
lar muscle
band on
ventral
side of
pharynx
Visceral
circular
muscles
on
intestine
(midgut)
Visceral
longi-
tudinal
muscles
on dorsal
side of
gut tube
Visceral
longi-
tudinal
muscles
on ventral
side of
gut tube
Somatic longi-
tudinal muscle
bands in ventro-
lateral position
(musculus princi-
palis according
to Remane )
Splitting
of mus-
culus
princi-
palis in
midtrunk
region
Anterior
inser-
tion of
musculus
principalis
Cross-
over
muscles
in
caudal
region
Bran-
ches of
musculus
principa-
lis supply
head
region
Heli-
coidal
muscles
enwrap
pharynx
Heli-
coidal
muscles
enwrap
intes-
tine
(midgut)
Muscle
striation
pattern
(see
also Tab.
...)
Tetranchy-
roderma
megastoma
On mouth
rim
Oblique
striation
Hochberg
& Litvaitis
(b)
Thaumas-
toderma
heideri
On mouth
rim
Oblique
striation
Hochberg
& Litvaitis
(b)
Oregodasys
cirratus
? ? On mouth
rim
Oblique
striation
Rothe &
Schmidt-
Rhaesa
()
Neodasys
cirritus
? On mouth
rim
Cross-
striated
Hochberg
()
Modified and amended from Hochberg & Litvaitis (b). A question mark (?) indicates an unknown character state; , absence; , presence; TbA, anterior adhesive tubes.
a There is only one crossing of the helicoidal muscle on the intestine in Paradasys sp. (see Leasi etal. 2006).
b Hochberg & Litvaitis (2001b) code the crossover muscle as “present” for T. ambronensis, although in the text, they report its absence.
Tab. 1.1 (Continued)
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1.2Morphology 13
A
B
C
ph
br
in
sc
sc
sc
vc
vc
vc
vc
in
ph
go
go
hm
vlm
vlm
vlm
vl
vl
hm
vl
hm
Fig. 1.9: Muscular system (schematic) of
the last common ancestor of Gastrotricha.
(A) Myoanatomy, dorsal view. (B and C)
Trunk cross sections at different levels
(indicated by bold lines). Note the reversal
of the sequence of visceral circular and
longitudinal muscles from pharyngeal
(B) to intestinal (C) region. It is not sure
if the stem species, like many extant
gastrotrichs, possessed a splitting of
the ventrolateral muscle bands in the
midtrunk region (left body side in A and
C). Abbreviations: br, brain; go, gonads;
hm, helicoidal muscle; in, intestine;
ph, pharynx; sc, somatic circular muscle;
vc, visceral circular muscle; vl, visceral
longitudinal muscles; vlm, ventrolateral
muscle bands (musculi principales).
ph
in
sc vc
vc hm
vlm
vl
vl
Fig. 1.10: Muscular system (schematic) of the last common ancestor of Gastrotricha, lateral view. Note the reversal of the sequence of
visceral circular and longitudinal muscles from pharyngeal to intestinal region. Abbreviations: hm, helicoidal muscle; in, intestine;
ph, pharynx; sc, somatic circular muscles; vc, visceral circular muscles; vl, visceral longitudinal muscles; vlm, ventrolateral muscle band
(musculus principalis).
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14 1Gastrotricha
ged muscle fibers (Fig. 1.12 A–D). These paired musculi
principales (according to Remane 1936, but see the notes
on this terminology in Teuchert 1974) or ventrolateral
muscle bands insert anteriorly close to the mouth rim and
reach the caudal lobes that bear the posterior adhesive
tubes (the stem species of Gastrotricha was characterized
by a bilobed caudal trunk end according to Kieneke etal.
2008a). Along the whole body, there are separate somatic
circular muscles that surround the ventrolateral muscle
bands and probably all other muscular components (Figs.
1.9 and 1.10). Yet, it is not clear if these somatic circular
muscles of the stem species of Gastrotricha represent
closed rings. In many species of the Macrodasyida, the
somatic circular muscles are reported to enclose the ven-
trolateral muscle bands “on either side of the midgut”.
Such a description, in addition with the presented data,
indicates the presence of incomplete muscle rings at least
in these species (e.g., Hochberg & Litvaitis 2001b, Leasi
et al. 2006). In Neodasys, the somatic circular muscles
are branches of the visceral circular muscles that line the
gut tube (Hochberg 2005). Such a condition is generally
regarded to demonstrate the evolutionary origin of the
somatic circular muscles (see Leasi & Todaro 2008 and
references therein). As for the stem species, there are not
data on the exact numbers concerning different muscular
components such as the number of visceral and somatic
circular muscles, of visceral longitudinal muscles, of
crossings of the helicoidal muscles, and of muscle fibers
per ventrolateral muscle band. It remains to mention
that there are diverse modifications (e.g., reductions,
losses, branching patterns, additional muscle compo-
nents) from the previously described ancestral muscular
character pattern in extant species of Gastrotricha (see
Tab. 1.1). These include, for instance, the presence of a
peculiar semicircular muscle band on the ventral side of
the pharynx in taxa such as Dactylopodola baltica, Parada-
sys sp., or Turbanella (Hochberg & Litvaitis 2001b, Leasi
etal. 2006). When present, this muscle connects both ven-
trolateral muscle bands (musculi principales) close to the
level of the anterior adhesive tubes (see Fig. 1.24 C). A com-
parable (homologous?) muscle is also present in the basal
paucitubulatinan species Musellifer delamarei (Leasi &
Todaro 2008, see Tab. 1.2). Additionally, there might be
one or two so-called crossover muscles connecting both
parts of musculi principales in the caudal region of many
but not all species with a bilobed caudal end (Hochberg &
Litvaitis 2001b, c, Tab. 1.1). The crossover muscle results
from a splitting of one or few fibers of the ventrolate-
ral muscle band passing over to the other side and vice
versa (Hochberg & Litvaitis 2001c). There is a splitting of
each ventrolateral muscle band in the midtrunk region in
several species with paired testes: Some fibers run more
laterally (pars lateralis according to Remane 1936), while
others are located more medially (pars ventrolateralis
according to Remane 1936). Further posterior, all fibers
converge forming a common muscle band (e.g., in Dacty-
lopodola baltica, Paradasys sp., Turbanella sp., or in Cra-
siella fonseci, see Hochberg & Litvaitis 2001b, Leasi etal.
2006, Hochberg 2014). Such kind of splitting is mostly
absent in members of the Thaumastodermatinae that only
possess one single testis (Hochberg & Litvaitis 2001b, but
see Rothe & Schmidt-Rhaesa 2010 for the situation in Ore-
godasys cirratus). This taxon is further characterized by
complete absence of somatic circular muscles (Hochberg
& Litvaitis 2001b, c). An exception to this pattern is Orego-
dasys cirratus (Rothe & Schmidt-Rhaesa 2010, Tab. 1.1). A
peculiarity of whole Thaumastodermatidae is the forma-
tion of anterior branches of dorsal visceral longitudinal
muscles that spread out into the oral hood (Remane 1936,
Hochberg & Litvaitis 2001b, c). These muscle branches
facilitate the withdrawal of the oral hood (Remane 1936).
Additional variation in muscle organization concerns the
anterior insertion of the ventrolateral muscle bands. In
species that possess distinct, frequently hand-like ante-
rior adhesive organs composed of several closely arran-
ged adhesive tubes (e.g., taxa Turbanella and Paradasys),
the musculi principales terminate in close proximity to
these organs and hence a certain distance posterior to the
anterior end. In species that do not possess those ante-
rior adhesive organs but instead have separately arran-
ged adhesive tubes close to the anterior trunk end (e.g.,
Lepidodasys, Macrodasys, Thaumastodermatidae), the
ventrolateral muscle bands insert close to the mouth rim
(Tab. 1.1). Species such as Dactylopodola baltica and
species of Turbanella and Neodasys have thin branches of
the ventrolateral muscle bands in the anterior region that
supply the head (Hochberg & Litvaitis 2001b, Hochberg
2005, Tab. 1.1). These are different from the muscle bran-
ches within the head region (oral hood) of the Thaumas-
todermatidae, which are formations of the dorsal visceral
longitudinal muscles (see above).
Severe evolutionary modifications of the muscular
system occurred both along the stem lineage of the gast-
rotrich subtaxon Paucitubulatina and within this clade.
Through fluorescence staining and confocal or epifluo-
rescence microscopy, the musculature of several species
of this group has been studied so far (Hochberg & Litvai-
tis 2001d, 2003a, Leasi etal. 2006, Kieneke etal. 2008b,
Kieneke & Ostmann 2012, Leasi & Todaro 2008, 2009). In
contrast to the Macrodasyida and Neodasys, the number
and arrangement of longitudinal muscles, somatic and
visceral, is much more determined in Paucitubulatina.
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1.2Morphology 15
Fig. 1.11: Muscular system (schematic) of the
last common ancestor of Paucitubulatina.
Myoanatomy in (A) dorsal and (B) ventral
views. (C and D) Trunk cross sections
at different levels (sectional plains
indicated by bold lines). Note the reversal
of the sequence of visceral circular and
longitudinal muscles from pharyngeal
(C) to intestinal (D) region. Abbreviations:
br, brain; ddm, dorsodermal muscle;
go, gonads; hm, helicoidal muscle; in,
intestine; md, musculus dorsalis; ml,
musculus lateralis; mv, musculus ventralis;
mvl, musculus ventrolateralis; ph, pharynx;
sc, somatic circular muscle; vc, visceral
circular muscle.
A B
C
ph br
sc
vc
vc
vc
in
ph
go
hm
ml
hm
hm
D
go
hm
in
ml
mv
mvl
mv
mvl
sc
md
ddm
ddm md
md
Pairs of potentially homologous longitudinal muscles that
have been detected in all hitherto investigated species of
the Paucitubulatina are the musculi ventrales, m. ventro-
laterales, m. laterales, m. dorsales, and one or two pairs
of dorsodermal muscles that are branches of musculi dor-
sales (Hochberg & Litvaitis 2001d, 2003a, Leasi & Todaro
2008, Tab. 1.2, Figs. 1.11, 1.12 E, F). Although this is not
based on a thorough phylogenetic reconstruction, we con-
clude that these five to six longitudinal muscle pairs pro-
bably belong to the character pattern of the stem species
of Paucitubulatina (this clade is most likely a monophy-
letic group, see chapter Phylogeny). As most investigated
basal species of Paucitubulatina (Musellifer delamarei,
Draculiciteria tesselata, and most species of Xenotrichuli-
nae) possess only one dorsodermal branch of musculi dor-
sales (“Rückenhautmuskel” according to Zelinka 1889, see
Hochberg & Litvaitis 2003a), we suspect that this repre-
sents the ancestral condition (Figs. 1.11 and 1.12 F). Owing
to their more peripheral position in the body, musculi late-
rales and dorsodermal muscles are considered to repre-
sent somatic components, whereas all other longitudinal
muscles are visceral components (Hochberg & Litvaitis
2001d, 2003a). However, the assignment to one or the
other group of musculature – visceral or somatic – is not
always that explicit, and it seems that in different members
of the Xenotrichulidae, the musculi ventrolaterales
rather belong to the somatic musculature (see results of
Leasi & Todaro 2008). Similar names imply a homology
of these muscles, which may not always be the case. For
example, it is likely that the musculi ventrolaterales of
Paucitubulatina are not homologous to the ventrolateral
muscle bands (musculi principales) in Macrodasyida and
Neodasys. It is more likely that the somatic musculi latera-
les of Paucitubulatina are homologous to the ventrolateral
muscle bands of Macrodasyida and Neodasys or at least to
one or two of their fibers.
In addition to the aforementioned five to six pairs
of longitudinal muscles, there may be further pairs. In
Xenotrichulinae, for instance, there is always a visce-
ral pair of musculi ventromediales that spans between
m. ventrales and m. ventrolaterales for most of its course
(Hochberg & Litvaitis 2003a, Leasi & Todaro 2008, 2009).
In Draculiciteria tesselata, there is another somatic (?)
longitudinal muscle pair, the musculi paralaterales. This
muscle spans between m. laterales and m. ventrolate-
rales (Hochberg & Litvaitis 2001d). The basal paucitu-
bulatinan species Musellifer delamarei has additional
somatic longitudinal muscles: There are two pairs of broad
muscle bands running along the body wall in dorsal and
ventral positions (Leasi & Todaro 2008). Further differen-
ces between species can be found in the specific course
of certain longitudinal muscles. Especially the musculi
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16 1Gastrotricha
50 µm
75 µm
50 µm
100 µm
50 µm
50 µm
AB
CD
E
ph
pp
mlv
F
*
*
hm
vlm
mcv
vlm
vlm
mcv
mlv
ph om ml
ph
ml
md
ddm
dvm
*
Fig. 1.12: Muscular system of Gastrotricha. Maximum projections of confocal image stacks. F-actin was stained with fluorescence-labeled
phalloidin. (A) Turbanella ambronensis (Macrodasyida), horizontal view. (B–D) Turbanella hyalina, horizontal views. Note the stained
filaments inside the adhesive tubes. (B) Anterior end. Note the sphincter-like circular muscles at the anterior and posterior end of the
pharynx (asterisks). (C) Rear trunk end. (D) Whole specimen. (E) Dasydytes goniathrix (Paucitubulatina) with a highly derived somatic
musculature consisting of oblique and segmented longitudinal muscles that are used for moving the long cuticular spines (asterisk,
autofluorescence). Lateral view, specimen slightly tilted. (F) Xenotrichula velox, a rather primitive species of the Paucitubulatina that still
has dorsoventral muscles in a visceral and somatic position, lateral view. Abbreviations: ddm, dorsodermal muscle; dvm, dorsoventral
muscles; hm, helicoidal muscles; mcv, visceral circular muscles; md, musculus dorsalis; ml, musculus lateralis (of Paucitubulatina);
mlv, visceral longitudinal muscles; om, oblique muscles; ph, myoepithelial pharynx; pp, pharyngeal pore; vlm, ventrolateral muscle
blocks of Macrodasyida (musculi principales).
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1.2Morphology 17
Tab. 1.2: Characters related with musculature and muscle arrangement in Paucitubulatina.
Character-number according to Leasi & Todaro ()
Number of myocytes
(fibers) per somatic
longitudinal musclea
Anterior insertion
of somatic longitu-
dinal musclesa
Muscles in the
furca/caudal lobes
Visceral musculi
paralaterales
Visceral musculi
ventrolaterales
Visceral musculi
ventromediales
Visceral
musculi
ventrales
Visceral
musculus
dorsalis
Dactylopodola baltica > Distant to mouth – – – – –
Neodasys cirritus > Close to mouthb – – – – –
Draculiciteria tesselata – Close to mouth
Heteroxenotrichula squamosa – Close to mouth
Xenotrichula intermedia – Close to mouth
Xenotrichula punctata – Close to mouth
Aspidiophorus marinus – Close to mouth
Chaetonotus sp. – Close to mouth
Halichaetonotus sp. /H. aculifer – Close to mouth
Lepidodermella squamata – Close to mouth
Musellifer delamarei > Distant to mouth
Polymerurus nodicaudus – Close to mouth
Character-number according to Leasi & Todaro ()
+
Dorsodermal muscle
(branch of visceral
musculus dorsalis)
Posterior branching of musculus
dorsalis with crossing
Striation pattern Extent of helicoidal muscles Visceral muscles in the
intestinal region
Dactylopodola baltica Cross-striation Longer than one third of intestine Complete circular
Neodasys cirritus Atypical cross-striation To one third of intestine Complete circular
Draculiciteria tesselata Atypical cross-striation Longer than one third of intestine Complete dorsoventral
Heteroxenotrichula squamosa Oblique striation Longer than one third of intestine Complete dorsoventral
Xenotrichula intermedia Oblique striation Longer than one third of intestine Incomplete circular
Xenotrichula punctata Oblique striation To one third of intestine Incomplete dorsoventral
Aspidiophorus marinus Oblique striation To one third of intestine Absent
Chaetonotus sp. Oblique striation To one third of intestine Absent
Halichaetonotus sp. /H. aculifer Oblique striation To one third of intestine Absent
Lepidodermella squamata Oblique striation To one third of intestine Absent
Musellifer delamarei Atypical cross-striation To the base of pharynx Incomplete circular
Polymerurus nodicaudus Oblique striation To one third of intestine Complete dorsoventral
(Continued)
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18 1Gastrotricha
Character-number according to Leasi & Todaro () Source
+
Termination of circular or
dorsoventral muscles in the
intestinal region
Semicircular muscle
band(s) on ventral
side of pharynx
Somatic muscles in the
intestinal region
Somatic dorsoventral musclee
pairs close to the pharyngeointes-
tinal junction
Dactylopodola baltica – Circular Hochberg & Litvaitis (b)
Neodasys cirritus – Circular Hochberg ()
Draculiciteria tesselata Branched Complete dorsoventral Hochberg & Litvaitis (d)
Heteroxenotrichula squamosa Branched Complete dorsoventral Leasi & Todaro ()
Xenotrichula intermedia Branched Incomplete dorsoventral Hochberg & Litvaitis (a), Leasi &
Todaro ()
Xenotrichula punctata Branched Incomplete dorsoventral Leasi & Todaro ()
Aspidiophorus marinus – Absent Hochberg & Litvaitis (a)
Chaetonotus sp. – Absent Leasi & Todaro ()
Halichaetonotus sp. /H. aculifer – Absent Hochberg & Litvaitis (a)
Lepidodermella squamata – Absent Hochberg & Litvaitis (a)
Musellifer delamarei Not branched Incomplete dorso-ventralc Leasi & Todaro ()
Polymerurus nodicaudus Branched Absent Leasi etal. ()
Modied and amended from Leasi & Todaro (2008). Dactylopodola baltica and Neodasys cirritus were used for the outgroup comparison. A question mark (?) indicates an unknown character
state; dash (–), inapplicable character state; 0, absence; 1, presence.
a The “somatic longitudinal muscles” are the ventrolateral muscle bands (musculus principalis) in Macrodasyida and Neodasys, called musculi laterales in Paucitubulatina according to
Hochberg & Litvaitis (2003a).
b Leasi & Todaro () coded the longitudinal muscle insertion in N. cirritus distant to the mouth, although original data (Hochberg ) demonstrate a different pattern.
c Leasi & Todaro () coded the somatic muscles in the intestinal region of M. delamarei as “incomplete dorsoventral”, although they are later treated as “incomplete circular” (see, e.g.,
their figure ).
Tab. 1.2: (Continued)
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1.2Morphology 19
Other taxa of the Chaetonotidae like Aspidiophorus, Chae-
tonotus, Halichaetonotus, and Lepidodermella completely
lack circular or dorsoventral muscles apart from a tiny
single pair close to the anus (Hochberg & Litvaitis 2003a,
Leasi & Todaro 2008). Also, species of the exclusively
freshwater-dwelling Dasydytidae lack any circular muscle
components in the intestinal region (Kieneke etal. 2008b,
Kieneke & Ostmann 2012), a result that partially revises
the muscular description of Dasydytes ornatus by Remane
(1936), who suspected the presence of incomplete circular
muscles in that species. The Paucitubulatina are another
example for muscular diversity: The muscle endings are
simple in M. delamarei, whereas all investigated Xenotri-
chulidae and P. nodicaudus have branched muscle endings
(Tab. 1.2). We can deduce from the evolutionary scenario
of circular muscle evolution in Paucitubulatina developed
by Leasi & Todaro (2008), that the last common ancestor
of Paucitubulatina could have had a system of incomplete
circular muscles in visceral and somatic positions in its
intestinal region in addition to the longitudinal muscle
pairs discussed above (Fig. 1.11). The presence of incom-
plete circular muscles in a somatic position, however, is
purely hypothetical and has never been observed in any
extant species of the Paucitubulatina (Leasi & Todaro
2008). Because a visceral helicoidal musculature is present
in all investigated species of Paucitubulatina studied so
far (Hochberg & Litvaitis 2001d, 2003a, Leasi etal. 2006,
Kieneke etal. 2008b, Kieneke & Ostmann 2012, Leasi &
Todaro 2008, 2009), this muscular component is an ances-
tral paucitubulatinan character, too.
The taxon Dasydytidae is a highly derived group of
freshwater-dwelling planktonic gastrotrichs (almost all
other species of Paucitubulatina have an endobenthic, epi-
benthic, or periphytic lifestyle, see chapter Ecology), which
have paired groups of motile cuticular spines. These spines
are actively movable and can be abducted and adducted
serving either for supporting locomotion (species such as
Haltidytes crassus may perform short “jumps” in the water
column) or for performing defensive positions at which the
animals take a strong ventral flexion of the trunk and abduct
their spines to a maximum. Spine movement is brought
about by a highly specialized musculature consisting of
serially arranged somatic oblique muscles and segments
of the partitioned musculi laterales (Kieneke etal. 2008b,
Kieneke & Ostmann 2012; Fig. 1.12 E). Although it was ini-
tially supposed that oblique and segmented longitudinal
muscles represent elements of an antagonistically working
system (Kieneke et al. 2008b), it is more likely that both
muscle components work synergistically to facilitate the
spine abduction-adduction cycle (Kieneke & Ostmann 2012).
It is not likely that the oblique musculature of Dasydytidae
laterales and m. ventrolaterales may run in close proximity
to the pharynx in certain species, whereas in others, they
follow the contours of the anterior body or continuously
diverge toward the anterior end (compare reconstructions
of Aspidiophorus marinus, Chaetonotus spp., Halichaetono-
tus spp., and Lepidodermella spp. in Hochberg & Litvaitis
2003a). In Xenotrichula intermedia, musculi ventrales are
reported to cross over in the region of the anus (Hochberg
& Litvaitis 2003a). However, such a crossover was not con-
firmed for X. intermedia and other members of the Xenotri-
chulinae (Leasi & Todaro 2008). Meanwhile, a peculiar
x-shaped connection between the paired musculi dorsales
in the posterior trunk region was detected in all species of
Xenotrichulidae (Xenotrichulinae plus Draculiciteria tesse-
lata) studied so far (Leasi & Todaro 2008, Tab. 1.2).
In the pharyngeal region of Paucitubulatina, like
in Macrodasyida and Neodasys, there are densely piled
complete circular muscles that line the pharynx inward
the visceral longitudinal muscle components. However,
such muscle rings could not be detected with certainty in
species of the derived paucitubulatinan taxon Dasydyti-
dae (see Kieneke etal. 2008b, Kieneke & Ostmann 2012).
In Musellifer delamarei, a semicircular muscle band on the
ventral side of the pharynx was found, which is compara-
ble to those muscles discovered in Dactylopodola baltica
and other species of Macrodasyida (Leasi & Todaro 2008,
compare Tab. 1.1 with Tab. 1.2). Even more structural diver-
sity can be observed among the “circular” muscle compo-
nents in the intestinal region of Paucitubulatina (Hoch-
berg & Litvaitis 2001d, 2003a, Leasi & Todaro 2008, 2009,
Tab. 1.2). In the assumed basal species M. delamarei, there
are incomplete visceral circular muscles plus somatic dor-
soventral muscles. “Incomplete” refers to the fact that
these circular muscles do not represent closed rings but
have a median gap dorsally and ventrally (Leasi & Todaro
2008). Some species of the Xenotrichulinae show a com-
parable muscle arrangement: The visceral component is
represented by incomplete circular muscles, whereas the
somatic component consists of dorsoventral muscle fibers
that attach to the dorsal and ventral integument. In Dra-
culiciteria tesselata and Heteroxenotrichula squamosa, the
somatic and visceral components consist of such dorso-
ventral muscles. In the lineage that leads to the predomi-
nantly freshwater inhabiting Chaetonotidae (much likely
this family does not represent a monophyletic group, see
chapter Phylogeny), only assumed basal species such as
Polymerurus nodicaudus possess comparable muscle com-
ponents: This species still has dorsoventral muscles in a
visceral position in its intestinal region, whereas any circu-
lar or dorsoventral components are absent in the somatic
position (Leasi etal. 2006, Leasi & Todaro 2008, Tab. 1.2).
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20 1Gastrotricha
is a derivate of ancestral somatic circular muscles because
not a single investigated species of the Chaetonotidae,
among them putative relatives of the Dasydytidae (see, e.g.,
Kånneby etal. 2013), possesses a somatic circular muscu-
lature. Somatic circular (or dorsoventral) musculature, still
present in Muselliferidae and Xenotrichulidae (see above),
hence must have been lost within the lineage that leads to
Chaetonotidae, Dasydytidae, and some other minor taxa
of freshwater-dwelling gastrotrichs. Oblique musculature
therefore represents a new evolutionary formation, an auta-
pomorphy of the Dasydytidae (Kieneke & Ostmann 2012).
Apart from the visceral and somatic musculature of
Gastrotricha that is present as longitudinal, circular/dorso-
ventral, and helicoidal muscles (see above), there may be
further muscle arrangements. Most prominent is a specia-
lized musculature as part of the reproductive system. Taxa
that possess a distinct caudal organ as a sperm-transfer-
ring device (see chapter Reproductive Organs) may have a
strong circularly or slightly helically arranged musculature
that surrounds this accessory reproductive organ as, for
example, in Macrodasys sp. (Ruppert 1978a), Tetranchyro-
derma papii (Hochberg & Litvaitis 2001c), or in Lepidoda-
sys ligni (Hochberg etal. 2013). Muscle contractions of the
caudal organ are used to support the release of spermatozoa
from the caudal organ lumen or, as in Macrodasys sp., to
evert the copulatory tube (Ruppert 1978a, see also chapters
Reproductive Organs and Reproductive Biology). However,
there are also species that contain a caudal organ but obvi-
ously lack a specialized musculature like Crasiella fonseci
(Hochberg 2014), although congeneric species, e.g., C.
diplura, possess such a circular muscle sheath (Guidi etal.
2011). It is hypothesized that caudal organ musculature of
C. fonseci may be formed rather late during an individual’s
development (Hochberg 2014). A sheath of circular muscles
also surrounds the distal parts of the vas deferens in species
of Thaumastodermatidae (Ruppert 1978b). A comparable
musculature on the distal section of the sperm ducts may
be present in species of Turbanella (see figure 2c of Leasi
etal. 2006). A narrow, ring-shaped muscle at the level of
the anus was reported from different species. This single
circular muscle probably represents an anal sphincter (see,
e.g., Leasi etal. 2006, Kieneke etal. 2008b). A sphincter oris
surrounding the mouth opening is reported for different
species of the Paucitubulatina (Remane 1936). A strong,
sphincter-like circular muscle is also present around
the mouth opening of the macrodasyid Crasiella fonseci
(Hochberg 2014) and in species of Turbanella (Fig. 1.12 A–B).
The ultrastructure of musculature and muscle cells
was intensively studied in the marine gastrotrich Turba-
nella cornuta (Teuchert 1974). These findings were later
complemented by ultrastructural data of several other
species from all of the three major gastrotrich subtaxa
Macrodasyida, Neodasys (Multitubulatina), and Pau-
citubulatina (Ruppert 1991, see Tab. 1.3). Longitudinal
muscle cells of T. cornuta are to 40 µm long, spindle-
shaped, and with an axially situated cytoplasmic com-
partment at one end that houses the nucleus (see Fig.
1.13 A for longitudinal muscles in Polymerurus). In cross
section, such longitudinal muscle cells are somehow
leaf-shaped with a coelomyarian to ribbon-like arran-
gement of contractile elements. The ventrolateral longi-
tudinal muscle bands of T. cornuta (musculi principales,
but see Teuchert 1974 for concerns about this termino-
logy) consist each, in cross section, of nine fibers; each
fiber is composed of 8–12 consecutive mononuclear cells
(Teuchert 1974). Circular muscle cells of T. cornuta are
as well spindle-shaped (approximately 10 µm long) but
with an abaxially positioned nucleus (Teuchert 1974). An
abaxial position of the nucleus, however, was also found
in longitudinal muscle cells of Neodasys sp. (Ruppert 1991;
Fig. 1.13 B–C). Variation among the ultrastructure and
cytomorphology of gastrotrich muscle cells can be found,
for instance, in the striation pattern, type of z-material,
and the absence/presence of a t-system for the excitation-
contraction-coupling (Ruppert 1991, Tab. 1.3). A periphe-
ral coupling of the muscle cell membrane (sarcolemma)
with the sarcoplasmic reticulum was confirmed for almost
all species investigated so far. Interestingly, taxa that are
generally regarded to occupy rather basal positions within
the phylogenetic tree of the Gastrotricha such as Neoda-
sys, Dactylopodola, Xenodasys, Chordodasiopsis, Dracu-
liciteria, and Musellifer (see chapter Phylogeny) possess
a cross-striated musculature, whereas most remaining
taxa show an oblique striation pattern (Ruppert 1991,
Tab. 1.3). Because Neodasys, Musellifer, and Draculicite-
ria have rods instead of dense bodies as z-material, their
striation type is regarded as “atypical cross-striation”. If
basal positions of the aforementioned taxa with cross-
striated musculature will be supported (but see chapter
Phylogeny for differing phylogenetic scenarios), this
striation pattern would be part of the character pattern
of the stem species of Gastrotricha as the most parsimo-
nious reconstruction (Ruppert 1991). So far, Lepidodasys
is the only known gastrotrich taxon with a smooth muscle
organization (Ruppert 1991). Except Lepidodasys all gast-
rotrichs have radially arranged, cross-striated myofibrils
in the myoepithelial pharynx (Fig. 1.13 D). Regarding the
sarcomeres per contractile element of the pharynx, the
number varies from one in Lepidodermella squamata up
to 12 sarcomeres in Turbanella cornuta (Ruppert 1982).
The mechanic coupling between neighboring muscle cells
or a muscle cell and a non-muscle cell is by adhaerens
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1.2Morphology 21
Tab. 1.3: Characters related with the ultrastructure and cytomorphology of longitudinal muscle cells of various species of the Gastrotricha.
Diameter of
single
muscle fiber
Arrangement of sarcomeres
within fiber (as seen when
cross-sectioned)
Cross-striated
myofibrils
Oblique-
striated
myofibrils
Smooth
myofibrils
Length of
sarcomere
Diameter
of myosin
Dense
bodies as
Z-material
Rods as
Z-material
Peripheral coup-
lings of sarcolemma
and sarcoplasmic
reticulum
T-system
Chordodasiopsis anten-
natus (former Xenodasys
antennatus)
× µm Circomyarian to polygonal . µm ? ? (?)
Xenodasys riedli . µm Circomyarian to polygonal . µm nm
Dactylopodola sp. . µm Circomyarian to polygonal . µm ?
Cephalodasys sp. ? ? ? ?
Cephalodasys littoralis × µm Coelomyarian/ribbon-like ? nm
Crasiella diplura . ×. µm Coelomyarian/ribbon-like ? nm
Macrodasys sp. . × µm Coelomyarian/ribbon-like ? nm
Mesodasys sp. . × . µm Coelomyarian/ribbon-like ? nm
Paraturbanella sp. × . µm Coelomyarian/ribbon-like ? nm
Turbanella cornuta × µm Coelomyarian/ribbon-like . µm nm (?)
Dolichodasys carolinensis × . µm Polygonal ? ?
Acanthodasys sp. × . µm Polygonal to coelomyarian ? nm
Thaumastoderma sp. . × . µm Polygonal to coelomyarian ? ?
Oregodasys sp. (former
Platydasys)
? ? ? ?
Lepidodasys sp. × . µm Circomyarian to polygonal ? – nm
Neodasys sp. . µm Circomyarian to polygonal . µm nm
Diuronotus sp.a. µm Circomyarian to polygonal ? nm
Draculiciteria tesselata × µm Circomyarian to polygonal ? nm ? ?
Musellifer sublittoralis . µm Circomyarian to polygonal ? ? ? ?
Chaetonotus sp. . µm Polygonal to coelomyarian ? ?
Lepidodermella squamata . × . µm Coelomyarian/ribbon-like ? ?
Xenotrichula carolinensis × . µm Circomyarian to coelomyarian ? nm
Aspidiophorus sp. . × . µm Coelomyarian/ribbon-like ? nm
Modified from Ruppert (). A question mark (?) refers to unknown data; , absence; , presence.
a Ruppert (1991) presented muscular characters of an undescribed species of an undescribed genus referring to a drawing of his gastrotrich chapter in Ruppert (1988). Todaro etal. (2005)
identied this animal as belonging to the taxon Diuronotus.
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22 1Gastrotricha
1 µm 1 µm
0.5 µm 1 µm
AB
CD
pl
sr
ml
F
cc
mg
nu
ecm
lm
lnb
mf
mi
mi
phl
lm ac
cm
Fig. 1.13: Muscle ultrastructure (TEM-cross
sections) of Gastrotricha. (A) Polymerurus
nodicaudus (Paucitubulatina). Somatic
longitudinal musculature in close proximity
to the protonephridium. (TEM micrograph
from Kieneke & Hochberg 2012, with
permission by Wiley.) (B–D) Neodasys
chaetonotoideus (Multitubulatina). (B) Cell
body of a longitudinal muscle cell with
nucleus. (C) Longitudinal muscle cells and
nervous system in close proximity.
(D) Detail of the pharynx showing
myoepithelial cells and subpharyngeal
visceral musculature. Abbreviations:
ac, apical cell; cc, canal cell of the
protonephridium; cm, circular muscles;
ecm, extracellular matrix;
lm, longitudinal muscles; lnb,
longitudinal neurite bundle; mf, cross-
striated myofilaments; mg, midgut;
mi, mitochondria; ml, musculus lateralis;
nu, nucleus; phl, pharyngeal lumen;
pl, protonephridial lumen; sr, sarcoplasmic
reticulum.
junctions, most probably desmosomes. If a muscle inserts
on the body wall, muscle cells do not attach directly to the
cuticle, but always to an epidermal cell. Tension between
muscle and cuticle is provided by microfilaments that
span through the epidermis cell from adhaerens junctions
between muscle and epidermal cell to hemidesmosomes
between epidermal cell and cuticle (Ruppert 1991). A com-
parable situation is assumed for the mechanic coupling
between the sections of partitioned musculi laterales/
oblique muscles and the movable spines in Dasydytidae
(Kieneke etal. 2008b). This, however, has to be supported
by ultrastructural studies in the future.
Mechanic coupling of contractile elements (myofibrils)
and the cuticle is slightly different in the pharynx (see also
chapter Intestinal System for this issue). Here, the myofi-
brils of the myoepithelial cells are directly attached to the
apical pharyngeal cuticle via specialized, plaque-like hemi-
desmosomes. Hemidesmosomes also attach the myofibrils
basally to the basal lamina. There is quite a high ultrastruc-
tural diversity among hemidesmosomes of the pharynges
of different species and groups of the Gastrotricha (see
Ruppert 1982 for details). Some of the basal attachments
of the pharyngeal myofibrils are furthermore mechanically
coupled to the body cuticle via intracellular fibers that
may span through different layers of cells before reaching
the cuticle (Ruppert 1991). The ultrastructure of nerve-to-
muscle connections for signal transduction was investiga-
ted in Turbanella cornuta by Teuchert (1977a). A peculiarity
of these myoneural synapses is that the muscle cell itself
forms one or few short processes that project into the neigh-
boring nerve cell (Teuchert 1977a). Whether this represents
a general pattern of the Gastrotricha, however, needs to
be confirmed by further investigations (see Fig. 1.13 C for a
close proximity between nervous and muscular cells).
Somatic circular and longitudinal muscles in Gast-
rotricha are generally regarded as reciprocal antagonists
(Ruppert 1991). Contractions of the longitudinal muscles
cause a shortening of the body, whereas its diameter has to
increase because of the unchanged volume of the animal
and incompressibility of liquid (Fig. 1.14 A–E). Owing to the
increasing diameter, the circular muscles will relax. If circu-
lar muscles contract, the diameter will decrease again that
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1.2Morphology 23
Fig. 1.14: Muscle-mediated movements of
Gastrotricha. (A–D) Turbanella subterranea
(Macrodasyida), dorsal views. The animal
was consciously disturbed and showed
a quick retraction of the trunk as a kind
of escape response. (E) Fully retracted
Turbanella subterranea with compressed
organs such as the pharynx, midgut, and
Y-cells. Due to incompressibility of liquids,
the animal is much broader than usual.
(F) A slipping Paradasys subterraneus
(Macrodasyida) that takes a sharp right
curve by contracting longitudinal muscles
of its right side (asterisk). (G) Rear
trunk of Dactylopodola deminuitubulata
(Macrodasyida) with caudal pedicles. With
the strong and cross-striated longitudinal
musculature, species of Dactylopodola can
perform rapidly repeated ventral flexions
of the caudal pedicles and thereby escape
with a “hopping” movement. Abbreviations:
an, anus; mg, midgut; ph, pharynx; vlm,
ventrolateral longitudinal muscle blocks;
yc, Y-cells.
100 µm 100 µm
100 µm
25 µm
100 µm100 µm
200 µm
ABC D
EF
yc
ph
mg
*
G
yc
mg
an
vlm
TbP
The waving of the head and anterior trunk is interpreted as a
kind of “searching behavior”. Thus, the animal tries to opti-
mize sensory perception (Remane 1936). A peculiar way of
locomotion in many species of the Macrodasyida is shown
during an escape behavior: Taxa such as Macrodasys, Turba-
nella, Paradasys, or Tetranchyroderma papii, just to mention
some, may perform a leech-like or inchworm-like cree-
ping, at which animals successively attach their posterior
(or anterior) adhesive tubes to the substratum, then
strongly flex or shorten their body, attach the adhesive
tubes of the opposite body end (anterior or posterior
tubes, respectively), and stretch the trunk again. Several
quick repetitions of such actions allow a fast escape from
a potential harmful stimulus, e.g., a collision with a pre-
dator or just with a scientist’s micropipette (Remane
1936, Hochberg & Litvaitis 2001c). There are interspe-
cific differences in this special behavior. Macrodasys,
for instance, escapes in a frontal direction, whereas
taxa like Turbanella or Paradasys escape backward.
Tetranchyroderma papii may engage in both, backward or
forward directed inchworm-like creeping (Hochberg & Litvai-
tis 2001c). A similar escape behavior can be observed in Neo-
dasys sp. However, these animals stay attached to a sand grain
by means of their posterior adhesive organs and quickly con-
tract the whole trunk accordion-like (Ruppert & Travis 1983).
leads to an elongation of the trunk and simultaneously to a
relaxation of longitudinal muscles. Body movements of Gast-
rotricha that are brought about by muscle action include,
for example, longitudinal elongation and shortening of the
trunk (see above, Fig. 1.14 A–D), ventral and lateral flexion
(Fig. 1.14 F), nodding and slightly turning the head,
flexion of appendages (Fig. 1.14 G), or spreading of cuticu-
lar spines (e.g., Remane 1936, Ruppert 1991, Hochberg &
Litvaitis 2001c, Kieneke et al. 2008b). The main mode of
locomotion in Gastrotricha is of course the cilia-mediated
gliding or, in some taxa, swimming. Muscle action, however,
severely aids ciliary gliding and swimming when, for
instance, a lateral flexion of the whole trunk or lateral plus
ventral/dorsal flexion of the head is used for controlling the
direction of locomotion. Furthermore, appendages such as
the caudal lobes or toes of many species of the Paucitubu-
latina or the already mentioned motile spines of Dasydyti-
dae (see above) can actively be moved by muscle action and
hence may be used as a “rudders” (Remane 1936, Kieneke
& Ostmann 2012). Waving movements with the anterior
trunk end are known from different species, e.g., Turba-
nella cornuta or Tetranchyroderma papii. These movements
probably involve alternating contractions and relaxations
of the ventrolateral muscle bands and the visceral longitu-
dinal muscles (Remane 1936, Hochberg & Litvaitis 2001c).
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24 1Gastrotricha
The escape response in Dactylopodola and Chordodasiopsis
is different to the aforementioned mode. In these taxa,
rapidly repeated ventral flexions of the caudal lobes (Fig.
1.14 G) cause a rearward “hopping”. A correlation between
such fast movements and the occurrence of cross-striated
body musculature in Dactylopodola and Chordodasiopsis is
obvious and can be functionally explained because cross-
striated muscles are better suited for short but quickly repea-
ting contractions than is obliquely striated musculature. The
latter, meanwhile, is hypothesized to be the optimal muscle
type for soft-bodied, vermiform animals where hyperexten-
sions are followed by strong contractions of the whole body
(Ruppert 1991). A predominant occurrence of obliquely
striated longitudinal musculature among Gastrotricha
supports this hypothesis (see Tab. 1.3). In addition to the
already mentioned defensive behavior of Dasydytidae (see
above), taxa like Thaumastoderma, Lepidodasys martini,
or Kijanebalola are able to partially retract their anterior
body end as a defensive response (Remane 1936). We have
observed a comparable behavior in some specimens of Tur-
banella cf. subterranea that where consciously disturbed.
First, the animals partially retracted the head and/or the
caudal lobes bearing the posterior adhesive tubes. Shortly
after, an extreme contraction of the whole body may follow
(see Fig. 1.14 A–E). The main role of the visceral circular and
helicoidal muscles is regarded to antagonize dilations of the
pharynx and the midgut (Ruppert 1982, 1991, Hochberg &
Litvaitis 2001c). Further roles of these muscles in the intesti-
nal region could be the allocation of propulsive force to shift
big food items (e.g., diatoms) through the midgut and to
stiffen the whole gut tube (Hochberg & Litvaitis 2001c). Egg
deposition in Macrodasyida often involves strong contrac-
tions of the trunk of spawning animals (Teuchert 1968, see
chapter Reproductive Biology). These contractions are obvi-
ously brought about by longitudinal muscles. In freshwater
Chaetonotidae, ripe eggs leave the trunk on the ventral side,
possibly through a still unknown pore, pushed by muscu-
lar contractions (Hummon & Hummon 1983a). One or two
branches of musculi dorsales, the dorsodermal muscles,
form an arch above the developing egg in paucitubulatinan
gastrotrichs. These muscles are hypothesized to stabilize
the position of the egg and during egg deposition they may
lead it ventrally and out of the body (Hochberg & Litvaitis
2003a). The functional role of yet other muscle components
like, e.g., the crossover muscle(s) in the posterior trunk of
many species of the Macrodasyida is still not satisfactorily
understood (Hochberg & Litvaitis 2001c).
1.2.4Nervous system
The nervous system of the stem species of Gastrotricha
includes a dorsal to dorsolateral, bilateral symmetric brain
in the anterior part of the body (head region) and a pair of
lateroventral longitudinal cords (neurite bundles) as main
components (Rothe et al. 2011a, Figs. 1.15 and 1.16 A–D).
The brain has been reconstructed in different ways. Its
basic structure has in principle already been described by
Ludwig (1875) and Bütschli (1876), in more detail by Zelinka
(1889) and Remane (1936). According to these authors, the
brain consists of a bridge of neurons (the dorsal commis-
sure) dorsal of the pharynx and cells (=somata) on both
sides of this “bridge”. Ultrastructural investigations by
Teuchert (1977a) and Wiedermann (1995) reconstructed
the brain as circumpharyngeal, but with a stronger dorsal
part. Both investigations found a different distribution of
somata, which cover a broader area, either more or less
homogeneous over the brain (Wiedermann 1995) or sepa-
rated in an anterior and a posterior part (Teuchert 1977a).
Immunohistochemical investigations on Dactylopodola
baltica, Macrodasys caudatus and Dolichodasys elongatus
(Hochberg & Litvaitis 2003b), on Neodasys cirritus, Xeno-
dasys riedli, and Turbanella cf. hyalina (Hochberg 2007),
on three Turbanella species (Rothe & Schmidt-Rhaesa
2008), two Dactylopodola species (Rothe & Schmidt-
Rhaesa 2009), Oregodasys cirratus (Rothe & Schmidt-
Rhaesa 2010), two Xenotrichula species (Rothe etal. 2011b),
Lepidodasys worsaae (Hochberg & Atherton 2011), and Neo-
dasys chaetonotoideus (Rothe et al. 2011a) confirmed the
description by Zelinka and Remane. There is a broad com-
missure composed only of neurites dorsal of the pharynx
(Figs. 1.16 A–C and 1.17 A). This commissure is well shown
with immunoreactivity (IR) against tubulin. IR against other
neuronal components may show only subsets, as is shown
exemplary in the IR against serotonin, histamine, and
FMRFamides in Dactylopodola species, which all stain only
some fibers within the dorsal commissure (Rothe & Schmidt-
Rhaesa 2009). This observation also accounts for the immu-
nohistochemical investigations in the other species. Nuclear
staining shows a number of cells in the region lateral of the
dorsal commissure (approximately 20 per side in Dactylopo-
dola; Rothe & Schmidt-Rhaesa 2008), but the neural markers
used (anti-serotonin, anti-FMRFamides, anti-histamine) all
stain only subsets of the nerve cells of the brain (compare
Fig. 1.16 C with 1.16 D, see also Fig. 1.17 B). Although there
are at maximum few pairs of anti-serotonin IR cells (one to
five pairs) in the studied species (e.g. Fig. 1.16 A–C), a count
of anti-FMRF amide IR cells in the brain of Nesodasys chae-
tonotoideus and Xenodasys riedli yielded a mean number of
24 cells per hemisphere of the brain (Hochberg 2007, Rothe
etal. 2011a). Therefore, it cannot be said with certainty how
many neurons in total constitute the brain of Gastrotricha.
All somata stained with any neuronal marker are positioned
lateral of the dorsal commissure, a result that gets support
by ultrastructural data (e.g., Rothe etal. 2011a).
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1.2Morphology 25
is reported (e.g. Ruppert 1991). However, in putative basal taxa
such as Neodasys, the nervous system is most likely subepi-
dermal (Fig. 1.17 B–C). Immunohistochemical investigations
show some additional aspects. The distance between the two
longitudinal nerve cords is quite wide in most species, but in
Xenotrichula species, the cords are closer together (Rothe etal.
2011b). In the broad species Oregodasys cirratus, the distance
between the longitudinal cords is wide, but not as wide as
possible. The cords run in a distance of about 50 µm from the
lateral margin and fine neurites run from the cords into the
lateral regions of the animal (Rothe & Schmidt-Rhaesa 2009).
In this species, anti-serotonin IR reveals a second pair of lon-
gitudinal neurites or neurite bundles median of the longitu-
dinal cords (Rothe & Schmidt-Rhaesa 2009), this structure is
unknown from other species so far. Sometimes it appears that
two longitudinal neurite bundles per body side are present in
close proximity (see, e.g., for Dactylopodola; Rothe & Schmidt-
Rhaesa 2009); in this case, it is likely that two fibers within the
entire broader nerve cord were stained. In Turbanella species,
the longitudinal cord first runs close to the pharynx and then
turns laterally to proceed in a more lateral position. In the pos-
terior end, both longitudinal cords merge in a loop. In Xenoda-
sys riedli, there is a strong posterior commissure, from which
a pair of additional neurites runs further posterior (Hochberg
2007). In the two Xenotrichula species and in Neodasys cha-
etonotoideus, a pair of anti-serotonin IR somata is present
in the posterior part of the longitudinal nerve cords (Rothe
etal. 2011a, b; Fig. 1.16 A, B). The presence of such an “anal
ganglion” (sensu Remane 1936) is possibly also a character
of the last common ancestor of all extant Gastrotricha (see
Rothe etal. 2011a, Fig. 1.15). In some species, putative nerve
cell somata where observed along the ventrolateral neurite
bundles (Hochberg 2007, Rothe etal. 2011a).
Very fine ventral commissures between the longitudi-
nal nerve cords are present, but these are detected only by a
particular IR. In Turbanella species, one serotonin-IR ventral
commissure is present close to the level of the dorsal com-
missure (Rothe & Schmidt-Rhaesa 2008). In Dactylopodola
species, four commissures are present in different positions
along the body, all four are stained by anti-tubulin, two of
them by anti-RF amide, and none by anti-serotonin or anti-
histamine (Rothe & Schmidt-Rhaesa 2009). Two ventral
commissures are present in Neodasys chaetonotoideus, one
is stained by anti-RF amide, and the other by anti-serotonin
(Rothe etal. 2011b; Fig. 1.16 A).
Several neurons are observed to run from the brain
region into the anterior end, these neurons likely innervate
the sensory structures in the head region. The anterior and
posterior sensory organs can usually be seen in immuno-
histochemical investigations quite well. Some neurites
also innervate the pharynx and its ciliated sensory cells
(see chapters Intestinal System and Sensory Structures).
The lateral ends of the dorsal commissure are the origin
of the longitudinal nerve cords or neurite bundles (Fig. 1.16
A–D). Ultrastructural cross sections show one pair of longi-
tudinal nerve cords in a lateroventral position in the animals
(Teuchert 1977a, Ruppert 1991, Rothe et al. 2011a; Figs.
1.13 C, 1.17 C–D). In species such as Turbanella cornuta, a
basiepithelial and intraepidermal position of the nerve cords
ph
br
sci
cg
in
vln
sci
an dc
vc
avc
scb
pc
vln
Fig. 1.15: Nervous system (schematic) of the last common ancestor
of Gastrotricha. Green color indicates general nervous patterns,
blue color indicates serotonin expressing components. The orange
ovals are serially arranged FMRF-immunoreactive cells alongside
the ventrolateral neurite bundles that were possibly also present
in the stem species of Gastrotricha. Abbreviations: an, anterior
longitudinal neurite bundles; avc, anterior ventral commissure of
the brain; br, brain; cg, caudal ganglion/anal ganglion; dc, dorsal
commissure of the brain; in, intestine; pc, posterior commissure;
ph, pharynx; scb serotonin-expressing nerve cells of the brain;
sci, sensory cilia; vc, ventral commissure of the brain;
vln, ventrolateral longitudinal neurite bundles. Drawing
according to the reconstructed character pattern of
Rothe etal. (2011a).
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26 1Gastrotricha
1.2.5Sensory structures
Long before the highly resolving electron microscopy was
available for the study of microscopic animals, numerous
different types of presumptive sensory organs were already
known for the Gastrotricha. Among these are external
sensory cilia (“tactile hairs” or “tactile bristles”), either
positioned individually or associated with adhesive tubes
(Fig. 1.18 A, G). Especially at the anterior end, those sensory
cilia are mostly arranged in groups or tufts (Remane 1936).
Further sensory structures are paired, tentacle-like palps
on the anterior head region in several species (Fig. 1.18 A,
B, D, F), sometimes combined with further structures like
clusters of composed cilia (“cirri”) such as in species of the
Xenotrichulidae. Palps in Gastrotricha may be rather short
and cone-shaped protrusions on both sides of the head like
in Turbanella cornuta (and other species of that genus) but
may also feature long and thin formations as in Dinodasys
mirabilis (Remane 1936). Species of the taxon Thaumasto-
derma always have a combination of one pair of rod-shaped
lateral tentacles plus one pair of spittle-like tentacles, a
possible autapomorphy of that group (Kieneke 2010; Fig.
1.18 F). A further presumptive sensory device that is regu-
larly described for different taxa of the Macrodasyida is the
so-called “piston pit” or “pestle organ”. Such a structure is
known from, e.g., species of Macrodasys, Urodasys, Paratur-
banella, and certain members of the Thaumastodermatidae
(Remane 1936). Each piston pit is a lateral, roundish depres-
sion in the head region that is provided with numerous
sensory (?) cilia surrounding a central, knob-like elevation
(see Remane 1936). Up to now, a full reconstruction of such
an organ based on ultrastructural data has not been carried
out. However, some scattered data and a presumptive
chemoreceptive function for the pestle organs of Macrodasys
100 µm 25 µm 50 µm 50 µm
AB
CD
dc
ag
lnb
sbr
vc
pc
ag
lnb
dc
pc
lnb
pc
sbr
dc br
lnb
pc
anb
pnb
d
v
d
v
d
v
Fig. 1.16: Nervous system of Gastrotricha. Maximum projections of confocal image stacks. Serotonin expressing cells (A–C) or neurons
with immunoreactivity against anti-FMRF-amides (D) were stained with fluorescence-labeled antibodies. (A) Neodasys chaetonotoideus
(Multitubulatina). Note that the specimen is slightly twisted in the rear trunk. (B) Chaetonotus maximus (Paucitubulatina). Note that both
N. chaetonotoideus and C. maximus have a pair of neurons close to the posterior end (“anal ganglion”). (C and D) Dactylopodola typhle
(Macrodasyida). Note that more neurons of the brain and an unpaired ventral neurite bundle of the pharynx are stained with anti-FMRF-
amide (D). Confocal datasets of A, C, and D: Birgen H. Rothe, Halle (Westf.). Abbreviations: ag, anal ganglion; anb, anterior neurite bundles;
br, brain; d, dorsal; dc, dorsal commissure of the brain; lnb, longitudinal neurite bundle; pc, posterior commissure; pnb, pharyngeal neurite
bundle; sbr, serotonin-expressing cells of the brain; v, ventral; vc, ventral commissure of the brain.
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1.2Morphology 27
(and the corresponding lateral organs of Neodasys) are
reported by Gagné (1980a). According to Teuchert (1976a),
the piston pit/pestle organ could be homologue to the
posterior head sensory organ (described below) that is
now known from different species. In addition to the afo-
rementioned sensory structures, some species across
diverse taxa possess pigment-bearing photoreceptors, for
example, Dactylopodola baltica (Fig. 1.18 C) or Thaumas-
toderma heideri (Fig. 1.18 F) with their beautiful reddish
eye spots. In several species, the species name hints to the
wealth of pigmented photoreceptors such as in Oregoda-
sys ocellatus (Clausen 1965), Turbanella ocellata (Hummon
1974), or Macrodasys ommatus (Todaro & Leasi 2013;
Fig. 1.18 E), just to mention some. Among the predomi-
nantly freshwater-inhabiting family Chaetonotidae (Pau-
citubulatina), there are few species that bear so-called
“pseudocelli” such as Heterolepidoderma ocellatum. It
is still questionable if these globular, light-refracting
10 µm 5 µm
4 µm 1 µm
AB
CD
br ph
mg
lm
lnb
dc *
cu
ed
br
*
*
br
ph
ed
lnb
lm
Fig. 1.17: Ultrastructure of the nervous system of Gastrotricha (TEM cross sections). (A–C) Neodasys chaetonotoideus (Multitubulatina).
(A) Cross section of the brain (cerebral ganglion) at the level of the dorsal commissure. (B) Left hemisphere of an anterior portion of the
brain with 3 anterior neurite bundles (asterisks). (C) Ventrolateral longitudinal neurite bundle in a subepithelial position. (D) Xenotrichula
carolinensis (Paucitubulatina). Close-up of the longitudinal neurite bundle possibly close to a synapse with a ciliated epidermis cell. Note
the high number of neurovesicles. Abbreviations: br, brain (cerebral ganglion); cu, cuticle; dc, dorsal commissure; ed, epidermis;
lm, longitudinal musculature; lnb, longitudinal neurite bundle; mg, midgut; ph, pharynx.
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28 1Gastrotricha
a light-perception sense and that both structures therefore
represent pigmented photoreceptors. Only by means of ult-
rastructural investigations it will be possible to clarify the
functional role of Neogossea’s “Rückendrüsen”.
Investigations with the TEM have yielded great
insights into microanatomy and putative function of,
and possible homology between different sensory organs
of the Gastrotricha. Until recently, full morphological
structures really represent sensory organs or are parts
of them (Schwank 1990). Species of the derived plankto-
nic taxon Neogossea exhibit a pair of pigmented, kidney-
shaped structures on the dorsal side of the anterior portion
of the pharynx (e.g., Kieneke & Riemann 2007). These struc-
tures (originally called “Rückendrüsen”) are believed to be
secretory structures (e.g., Schwank 1990). However, it is
possible that these highly specialized animals benefit from
50 µm
50 µm 50 µm
50 µm
50 µm
40 µm
50 µm
1 µm
2 µm
AB
C
D
E
F
cu
cp
hy
G
rc
ed
anb
TbA
HI
cp
cu
Fig. 1.18: Sensory structures of Gastrotricha. (A) Aspidiophorus tentaculatus (Paucitubulatina) with club-shaped tentacles and tactile cilia
on the anterior end, ventral view. (B) Dactylopodola cornuta (Macrodasyida) with cone-shaped tentacles, ventral view. (C) Dactylopodola
baltica with red-pigmented eyes. (D) Xenodasys riedli (Macrodasyida) with long cephalic tentacles, ventral view. (E) Macrodasys cf. ommatus
(Macrodasyida) with eyes that obviously comprise pigmented cup cells. (F) Thaumastoderma heideri (Macrodasyida) with several paired
sensory structures at its anterior end (pigmented eyes, spatulate tentacles, rod-shaped tentacles and sensory cilia). (G) Macrodasys caudatus
with numerous sensory cilia at the anterior end, ventral view. (A, D–G) DIC micrographs. (B and C) BF micrographs. (H and I) Ultrastructure
(TEM cross sections) of the anterior head sensory organ of Gastrotricha: (H) Dactylopodola baltica and (I) Neodasys chaetonotoideus
(Multitubulatina). Abbreviations: anb, anterior neurite bundle; cp, microvilli-like ciliary processes; cu, cuticle; ed, epidermis; hy, hypostomion;
rc, receptor cell; TbA, anterior adhesive tubes.
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1.2Morphology 29
reconstructions based on TEM investigations have been
carried out for the cephalic tentacles and regular sensory
processes of Chordodasiopsis antennatus (Rieger et al.
1974), the anterior and posterior head sensory organs of
Turbanella cornuta (Teuchert 1976a) and Dactylopodola
baltica (Hochberg & Litvaitis 2003b, Liesenjohann etal.
2006), diverse types of sensory cilia (“tactile hairs”) of T.
cornuta (Teuchert 1976a), the sensory palps of Tetranchyro-
derma papii (Gagné 1980b), and the unique gravireceptor
organs of Pleurodasys helgolandicus (Marotta etal. 2008).
Additional ultrastructural data related with certain sensory
organs exist for Cephalodasys maximus (Wiedermann
1995), Cephalodasys sp., Crasiella cf. diplura, and Xenotri-
chula carolinensis (Ruppert 1991), and for Lepidodermella
squamata (Hochberg 2001). Predominantly based on mor-
phological (ultrastructural) evidence, three functional
types of receptor organs have been identified in Gastrotri-
cha: mechanoreceptors (including the gravireceptors of P.
helgolandicus), photoreceptors, and chemoreceptors (Teu-
chert 1976a, Ruppert 1991, Marotta etal. 2008). Although
it is not possible to deduce the function of a sensory organ
just by morphological and ultrastructural evidence (Laver-
ack 1974, reviewed in Gagné 1980b), comparative mor-
phology of organs of various taxa with a known function
(e.g., proven by physiological experiments) facilitates the
development of functional hypotheses for organs of taxa
where, for example, physiological evidence is difficult to
obtain as in Gastrotricha (see Gagné 1980b and references
therein). An argument for a mechanoreceptive function
is the common construction of the receptor cell among
diverse taxa, which includes an external cilium that is sur-
rounded by a collar of circumciliary microvilli (Teuchert
1976a, see Fig. 1.19 A, B). Photoreceptors frequently possess
pigments that shield parts of the sensory cells or filter a
certain spectrum of light. Different species of the Gastro-
tricha possess such “colored eyes” (see above). Another
characteristic of photoreceptors is the presence of a signifi-
cant membrane proliferation to house the visual pigments
(Gagné 1980b), which frequently consists of stacked and
highly ordered cell processes (Eakin 1972, see Fig. 1.20).
Such structures are indicative for “non-pigmented eyes”.
Additionally, light-refracting structures may be situated
in close proximity to putative photoreceptors (Teuchert
1976a). A changing light sensitivity (negative phototaxis)
during the reproductive cycle of Turbanella cornuta (Teu-
chert 1975a) is regarded as indirect evidence for a photore-
ceptive function for the anterior of both head sensory organ
pairs in that species (Teuchert 1976a). To perceive chemical
signals, the corresponding sensory devices must be able to
communicate with the environment. Hence, one suspects
certain openings/pores in such organs that enable dissol-
ved substances to reach the actual sensory cells (Gagné
1980b). In different studied gastrotrich species such pores
are lacking in the putative chemoreceptors (e.g., Teuchert
1976a, Gagné 1980b). However, a thinned body cuticle in
the area of the chemoreceptor is assumed to be permeable
to different substances (Gagné 1980b, see Fig. 1.21).
All sensory organs of the Gastrotricha known so far
consist of one single, few, or several ciliated receptor cells.
The only hint of non-ciliated receptor cells in Gastrotricha
is the unpublished observation of rhabdomeric photore-
ceptors in some gastrotrichs (see Gagné 1980b). Especially
the anterior and posterior head sensory organs of many
gastrotrich species (see below) additionally comprise a
varying number and different types of supportive cells
(see Tab. 1.4). Generally, the sensory cells are monociliar,
bipolar, primary receptor cells with a nucleus-containing
2 µm
1 µm
A
B
cil
ec
cp
sj
rc
nu
de
ax hd
mv
ime
mi
gly
cut
ec
er
sj
ec
cp
mv
cil
Fig. 1.19: Mechanoreceptive ciliated cell (schematic) of the epidermis
of Turbanella cornuta. (A) Sagittal section. Note the single cross-
striated ciliary rootlet and the numerous vesicles at the apical side of
the cell. (B) Cross section at the level of the ciliary pit where the basal
body of the cilium passes into the axoneme (level indicated by 2 black
triangles in A). Note the 10 ridges of the ciliary pit (mv) that transform
into the 10 circumciliary microvilli more distally. Abbreviations:
ax, axon; cil, cilium; cp, ciliary pit; cut, cuticle; de, belt desmosome;
ec, epidermis cell; er, endoplasmic reticulum; gly, glycogen; hd,
hemi-desmosome; ime, inter-microvillar ECM; mi, mitochondrion; mv,
microvilli; nu, nucleus. (A, Modified from figure 2A of Teuchert 1976a;
B, according to TEM micrograph in figure 3A of Teuchert 1976a.)
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30 1Gastrotricha
2 µm
cil
er
sj
rc
nu
ax
ol
mv
mi
dy
cil (b)
sc
sc
sec nu
nu
mp
Fig. 1.20: Anterior head sensory organ (schematic) of Turbanella
cornuta, sagittal section. Note the single cross-striated ciliary
rootlet accompanied by numerous microtubules. Abbreviations:
ax, axon; cil, modified cilium (dendritic section of receptor cell);
cil, (b) modified cilium of a second receptor cell; dy, dyctiosome;
er, endoplasmic reticulum; mi, mitochondria; mp, microvilli-like
processes of the modified cilium (containing a central microtubule
each); mv, microvilli; nu, nucleus; ol, organ lumen; rc, receptor
cell; sc, sheath cell; sec, secretory cell with large secretory
occlusions; sj, septate junction. (Modified from figure 7 of
Teuchert 1976a.)
15 µm
cil
sj
rc
nu
ax
ol
mv
mi
sc
sg
nu
mt
sc
sc
sg
sc
rc
mv cu
ed
Fig. 1.21: Posterior head sensory organ (schematic) of Turbanella cornuta, horizontal section (anterior to the left). Note the single cross-
striated ciliary rootlet per sensory cell and the secretion granules of the sheath cells with differing content. Endoplasmic reticulum and
Golgi cisterns omitted for clarity. Abbreviations: ax, axon; cil, modified and irregularly branched cilium (dendritic section of receptor cell);
cu, cuticle; ed, epidermis; mi, mitochondria; mt, microtubules; mv, microvilli; nu, nucleus; ol, organ lumen; rc, receptor cell; sc, sheath cell;
sg, secretion granules; sj, septate junctions. (Modified from figure 4 of Teuchert 1976a.)
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1.2Morphology 31
Tab. 1.4: Ultrastructural characters related with the anterior and posterior head sensory organs in different species of the Macrodasyida.
Anterior head sensory organ
Number of
receptor
cell(s)
Number of
receptor
cilia
Number
of sheath
cell(s)
Additional cells Basal inflation of
receptor cell(s)
Cilium branches into
numerous microvillus-
like processes
Arrangement of
ciliar processes
Central microtubule
inside the processes
Ciliary rootlet Presumed
function
Turbanella cornuta – ≥ (secretory cell) Present Yes Regular Present Present Photoreceptor
Cephalodasys maximus ≥ (?) ≥ ≥ (?) ≥ (pigment cells) Present N.A. N.A. Present Present Photoreceptor
Cephalodasys sp. ≥ ≥ ≥ N.A. Present Yes Regular/parallel Present N.A. Photoreceptor
Crasiella cf. diplura N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A.
Tetranchyroderma papii N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A.
Dactylopodola baltica
(US Atlantic Coast)
(pigment cell) Present Yes Regular/parallel PresentaN.A. Photoreceptor
Dactylopodola baltica
(North Sea)
Absent Present Yes Regular/parallel Present Absent General light
sensivity
Stem species of
Gastrotricha
N.A. Present Yes Regular Present N.A. Photoreceptor
Posterior head sensory organ
Number of
receptor
cell(s)
Number of
receptor
cilia
Number
of sheath
cell(s)
Organ has
diract contact
with body
cuticle
Microvilli of receptor
cells and/or sheath
cells penetrate
endocuticle
Cilium branches
into numerous
microvillus-like
processes
Arrangement
of (ciliar)
processes
Micro-
tubules
inside the
processes
Ciliary
rootlet
present
Presumed
function
Reference
Turbanella cornuta – – ≥ (secretory) Yes Yes Yes Irregular Present Present Chemore-
ceptor
Teuchert ()
Cephalodasys
maximus
N.A. N.A. N.A. Yes N.A. N.A. Irregular (?) N.A. N.A. Chemore-
ceptor
Wiedermann ()
Cephalodasys sp. N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A. Ruppert ()
Crasiella cf. diplura ≥ ≥ ≥ Yes Yes N.A. Irregular N.A. N.A. Chemore-
ceptor
Ruppert ()
Tetranchyroderma
papii
–b–b– (as support
cells)b
YesbYesbNob – – PresentbChemore-
ceptor
Gangé ()
Dactylopodola baltica
(US Atlantic Coast)
N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A. N.A. Hochberg & litvaitis
(b)
Dactylopodola baltica
(North Sea)
≥ ≥ (cup-shaped,
with pigments)
Yes No N.A. Irregular N.A. N.A. Photore-
ceptor
Liesenjohann etal. ()
Stem species of
Gastrotricha
Several Several ≥ Yes N.A. Yes Irregular N.A. N.A. Chemore-
ceptor
Liesenjohann etal. ();
for presumed function:
Ruppert ()
Modified and amended from Liesenjohann et al. (2006). A questionmark (?) indicates an uncertain character state, a dash (-) indicates an inapplicable character state, n.a. no data available.
a) There is a single microfilament inside each microvillus-like process of the anterior head sensory organ of D. baltica according to Hochberg & Litvaitis (2003b).
b) Gagné (1980) considers the sensory palps of T. papii to be homolog to the posterior hso of Turbanella cornuta
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32 1Gastrotricha
frequently originate from specialized cuticular scales that
have a certain diagnostic value. Embedded in the myoepi-
thelial wall of the pharynx of many species of Gastrotricha,
there are three columns of individually positioned ciliated
receptor cells that strongly resemble the mechanoreceptive
sensory cells of the body surface (Ruppert 1982). The cilium
penetrates the enducuticle but is enclosed by the epicuticle
of the pharynx. It is surrounded by a collar of microvilli (10?)
that arise from longitudinal ridges of the ciliary pit. A dif-
ference between external mechanoreceptors and the pha-
ryngeal receptor cells is the presence of at least two ciliary
rootlets in the latter (Ruppert 1982, Rothe etal. 2011a). At the
anterior end of the pharynx in species such as Neodasys sp.
and Halichaetonotus sp., there are three receptors consis-
ting of two such ciliated sensory cells each (Ruppert 1982).
Especially in the head region, there may be mechanore-
ceptors that consist of clusters of numerous mechanorecep-
tive sensory cells as, for example, close to the mouth opening
of Turbanella cornuta. In this species, the receptors form small
bulges that emerge above the level of the epidermis (Teuchert
1976a). Receptor cells are connected to each other via cellular
junctions (apical belt desmosomes plus septate junctions, see
figures 2C and 3B of Teuchert 1976a). A comparable cluster of
three to four ciliated receptor cells is present anterior to the
sensory palps of Tetranchyroderma papii (Gagné 1980b). At
the posterior trunk end of species of the limnic-planktonic
taxon Stylochaeta there is a pair of short, blunt processes, the
so-called styli. Each stylus bears two to three cilia suppo-
sed to have sensory function (Schwank 1990). Comparable
bulges with a single cilium, however, also occur along the
body of species such as Dinodasys mirabilis (Remane 1936) or
Oregodasys cirratus (Rothe & Schmidt-Rhaesa 2010). Further
multicellular mechanoreceptors, the so-called sensory
cirri, are present in the head region of species of the taxon
Xenotrichulidae (e.g., Ruppert 1979, 1991, Rothe etal. 2011b).
They are composed of several receptor cells, the externally
projecting cilia of which are enclosed by a common lining
of the epicuticle (see Ruppert 1991). Generally, an at least
partly sensory function (besides the still locomotive duty)
is assumed for most cilia on the head of Gastrotricha, fre-
quently arranged as tufts or batches (Remane 1936). Hoch-
berg (2001) discovered a special form of such sensory cilia on
the head region of the freshwater paucitubulatinan species
Lepidodermella squamata that display a wart-like surface on
the lower ciliary shaft.
Multicellular sensory organs with a presumed mecha-
noreceptive function but a considerably different const-
ruction are described for Chordodasiopsis antennatus. This
species possesses peculiar, antenna-like, and ostensibly
articulated processes on the head region, the cephalic ten-
tacles, and along the whole trunk including the anterior
end, viz. the regular sensory processes (Rieger etal. 1974).
cell body (perikaryon), a proximal axon, and a distal
ciliary (dendritic) segment (Teuchert 1976a, Ruppert 1991).
Mechanoreceptors of Gastrotricha are sensory cells
with mostly elongated and rather stiff external cilia (the
cilium is, as all external cilia in Gastrotricha, enwrapped
by the lamellar epicuticle). The central cilium arises from
a ciliary pit and is surrounded by a collar of 10 circumcili-
ary microvilli (“stereocilia”) arranged in a regular manner
(Fig. 1.19 A, B). Microvilli arise from 10 longitudinal ridges
that line the ciliary pit. The sensory cilium possesses a basal
body and a well-developed, straight ciliary rootlet (Teu-
chert 1976a, Fig. 1.19 A). In contrast to this set of characters,
ciliated locomotory epidermis cells of Gastrotricha almost
always have a rostral plus a caudal ciliary rootlet, obliquely
aligned within the cell and a number of eight circumciliary
microvilli (Rieger 1976, Hochberg 2001, see also chapter
Integument). The number of 10 circumciliary microvilli in
mechanoreceptive sensory cells (Fig. 1.19 B) is so far only
known from Gastrotricha and could therefore represent an
autapomorphy of this phylum (Hochberg 2001). The micro-
villi are interconnected by a specialized ECM that displays
a high degree of order (see figure 3A of Teuchert 1976a, Fig.
1.19 B). This “intermicrovillar” ECM resembles the one that
can be observed between the eight circumciliary micro-
villi of the terminal cells of protonephridia of species like
Turbanella cornuta (Teuchert 1973), Chaetonotus maximus
(Kieneke etal. 2008b), or Polymerurus nodicaudus (Kieneke
& Hochberg 2012). Possibly, this similarity hints to a
common ectodermal origin of protonephridia and mechan-
oreceptors. Basally, mechanoreceptive sensory cells form an
axon like all sensory cell types in Gastrotricha (Fig. 1.19 A).
In T. cornuta, direct connections of these axons to the neuro-
pil of the brain or with the ventrolateral longitudinal neurite
bundles are reported (Teuchert 1976a). Numerous mechan-
oreceptive sensory cells (“sensory hairs”) are individually
positioned along the body and are embedded between
regular epidermal cells (Teuchert 1976a, Fig. 1.19 A, B).
In species such as T. cornuta or Neodasys sp., a single
mechanoreceptive sensory cell is furthermore associated
with each adhesive tube/adhesive organ (Teuchert 1976a,
Tyler etal. 1980). In this case, the sensory cell body may
be deeply submerged below the level of the epidermis as in
T. cornuta (see Teuchert 1976a). The number of individual
mechanoreceptive sensory cells on the trunk was drama-
tically reduced in the stem lineage of the Paucitubulatina:
species of the basal marine taxon Xenotrichulidae possess
only few pairs of elongated sensory cilia (up to seven) along
their body and at the base of the caudal furca (see, e.g.,
Ruppert 1979). Members of Chaetonotidae, a probably not
monophyletic group (see chapter Phylogeny) at maximum
possess two pairs of stiff sensory cilia on their back (see, e.g.,
Schwank 1990). These so-called setolae (“sensory bristles”)
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1.2Morphology 33
information about the animal’s position within the Earth’s
gravitational field, a sense that might be quite important
for an organism that lives in the three-dimensional space
between sand grains. However, it is so far not understood
why P. helgolandicus is the only known gastrotrich species
with such sensory devices (Marotta etal. 2008).
Based on detailed ultrastructural investigations of
two different pairs of head sensory organs (or one of
both, respectively) in the species Turbanella cornuta
(Teuchert 1976a), Dactylopodola baltica (Hochberg & Lit-
vaitis 2003b, Liesenjohann etal. 2006), Tetranchyroderma
papii (Gagné 1980b), and some more fragmentary data of
further species (Wiedermann 1995, Ruppert 1991), Liesenjo-
hann etal. (2006) postulate the presence of two such pairs
of sensory structures in the stem species of Gastrotricha,
i.e., the anterior head sensory organ and the posterior head
sensory organ (see Tab. 1.4, Figs. 1.20 and 1.21). As a result
of their phylogenetic evaluation, the last common ancestor
of Gastrotricha possessed one pair of anterior head sensory
organs in the anterolateral region of the head (Liesenjo-
hann etal. 2006). The anterior head sensory organ has no
direct contact to the body cuticle. It is positioned below
the epidermis that might, however, be thinned in the area
of the receptor (e.g., Teuchert 1976a, Liesenjohann et al.
2006). Each organ of the stem species is composed of one
receptor cell with a single distal cilium that branches into
numerous, regularly arranged, microvilli-like processes
(Fig. 1.18 H, I). There is a single microtubule inside each
ciliary process. Basally (proximal to the modified cilium),
the receptor cell is inflated and is further proximally con-
nected to the brain by a common nerve strand of anterior
and posterior head sensory organs. In addition to the recep-
tor cell, there is one sheath cell in the anterior head sensory
organ of the stem species of Gastrotricha. This supportive
cell enwraps the receptor cell with thin cytoplasmic lobes,
hence forming an organ lumen inside which the ciliary
processes of the receptor cell are densely piled. Based on
the morphological arguments presented earlier, the ante-
rior head sensory organ had a photoreceptive function.
Because of ambiguous data, it is not clear if a ciliary rootlet,
present in some but absent in other species, belongs to the
ancestral construction of the anterior head sensory organ
(see Tab. 1.4). The anterior head sensory organs have so far
been reported and investigated in Turbanella cornuta (Teu-
chert 1976a, Fig. 1.20), Dactylopodola baltica from the North
Sea (Liesenjohann etal. 2006), Dactylopodola baltica from
the western Atlantic coast (Hochberg & Litvaitis 2003b),
Cephalodasys maximus (Wiedermann 1995), and Cepha-
lodasys sp. (Ruppert 1991). In addition to the aforementi-
oned character pattern of the last common ancestor, extant
species of Gastrotricha may show further supportive cells
in their anterior head sensory organs. For instance, there
Both types of sensory processes consist of numerous stron-
gly elongated ciliated receptor cells that distally end with a
rather short cilium surrounded by short microvilli. In the
cephalic tentacles, at least two such external sensory cilia
are positioned at each “annulus”, whereas there is a single
cilium at the distal end of each “segment” of the regular
sensory processes. At the distal tip of the latter, there are
usually two cilia and three at the tip of each cephalic tentacle
(Rieger etal. 1974). Proximal to the basal body, extremely
elongated ciliary rootlets, accompanied by microtubules,
extend deeply into each sensory cell. Owing to the succes-
sive ending of the receptor cells at the annuli of the sensory
processes, each cell (and its ciliary rootlet) has a different
total length. The main cell bodies with the nuclei are
aligned within the epidermis below each process, in the
case of the cephalic tentacles these cells are in close pro-
ximity to the brain of C. antennatus. In the regular sensory
processes, the sensory cells proximally form long and thin
appendages, probably axons that lead to the longitudinal
neurite bundles. A conspicuous difference between both
types of receptors in C. antennatus is the presence of several
nerve fibers in the cephalic tentacles that originate in the
brain (Rieger etal. 1974). Owing to the exclusive occurrence
of unmodified ciliated receptor cells in the sensory proces-
ses and cephalic tentacles of C. antennatus, Gagné (1980b)
rejects homology of these organs with the sensory palps
of Tetranchyroderma papii and the posterior head sensory
organs of Turbanella cornuta (see below).
A quite unusual and among Gastrotricha unique
sensory organ is the pair of supposed gravireceptor organs
of Pleurodasys helgolandicus that are positioned on the
dorsal surface in the anterior part of the animal (Marotta
etal. 2008). Each organ consists of a single ciliated receptor
cell with a similar cytomorphology as the common mecha-
noreceptive cells of Gastrotricha, i.e., they possess a long
cilium that is basally surrounded by a collar of 10 short
microvilli (see above). Hence, Marotta etal. (2008) suggest
an evolutionary origin of the gravireceptor organs from
simple mechanoreceptor cells. The peculiarity of the gra-
vireceptor organs is the presence of a drumstick-shaped,
external protuberance of the epicuticle into which the
cilium of the receptor cell projects. The stalk and bulbous
tip of the organ are formed by up to 100 densely piled layers
of the epicuticle. Inside the globular part, there is a sphere
that consists of numerous, electron-dense vesicles that
obviously originate from the apical membrane of the recep-
tor cilium. Because the drumstick-shaped external part of
the organ has a jointed connection to the body cuticle and
is freely movable and because the sphere is reminiscent to
the otoliths of statocysts in other taxa, Marotta etal. (2008)
conclude that the organs in P. helgolandicus must display
gravireceptors. These organs provide P. helgolandicus with
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34 1Gastrotricha
is at least one pigment cell in the anterior head sensory
organ of Cephalodasys maximus (Wiedermann 1995) and
one in Dactylopodola baltica from the western Atlantic
coast (Hochberg & Litvaitis 2003b). Interestingly, not any
of those additional supportive cells has been found in
D. baltica from the North Sea (Liesenjohann etal. 2006). In
Turbanella cornuta a secretory cell, quite comparable to the
epidermal glands, is closely associated with the anterior
head sensory organ (Teuchert 1976a, Fig. 1.20).
Posterior to the anterior head sensory organ, the stem
species of Gastrotricha possessed one pair of posterior
head sensory organs (Liesenjohann et al. 2006). Each
organ is composed of several ciliated receptor cells proba-
bly with a single branching cilium (Fig. 1.21). As opposed
to the anterior head sensory organ, the ciliary processes of
the posterior organ are irregularly arranged and likely lack
a central microtubule (microtubules inside the branching
cilium were so far only discovered in Turbanella cornuta,
see Teuchert 1976a, Tab. 1.4, and Fig. 1.21). The organ lumen
is formed by at least one but probably more sheath cells and
the whole organ has a direct contact to the body cuticle (Lie-
senjohann etal. 2006). The posterior head sensory organ
of the last common ancestor of Gastrotricha much likely
had a chemoreceptive function (Ruppert 1991). Due to the
paucity of data, it is not clear if ciliary rootlets inside the
receptor cells belong to the ancestral construction of the
posterior head sensory organ (see Tab. 1.4). Posterior head
sensory organs have so far been reported and investigated
in Turbanella cornuta (Teuchert 1976a, Fig. 1.21), Dactylopo-
dola baltica from the North Sea (Liesenjohann etal. 2006),
Cephalodasys maximus (Wiedermann 1995), and Crasiella
cf. diplura (Ruppert 1991). The sensory palps of Tetranchyro-
derma papii differ considerably in their microanatomy from
the posterior head sensory organs of, e.g., T. cornuta and
D. baltica. However, they are considered to be homologous
organs with a comparable chemoreceptive function (Gagné
1980b). The palps of T. papii consist of numerous (22–23)
strongly elongated bipolar receptor cells with a modified,
non-branching distal cilium. The cilium possesses an ext-
remely short axoneme but is distally elongated into a den-
dritic process with an expanded diameter. Proximal to the
basal body there is a long ciliary rootlet, and each receptor
cell is drawn out into a thin axon that posteriorly leads to
the brain of T. papii. Inside each palp, the receptor cells are
accompanied by two to three elongated support cells that
contain a bundle of densely packed and longitudinally
arranged microtubules, bringing about mechanic support
to the whole organ (Gagné 1980b). In the posterior head
sensory organs of Turbanella cornuta, Tetranchyroderma
papii, and Crasiella cf. diplura, the sheath cells/support cells
form several short microvilli that penetrate the endocuticle
(see Fig. 1.21), a character that is possibly related to the
assumed chemoreceptive function (Teuchert 1976a, Gagné
1980b, Ruppert 1991). Interestingly, such short microvilli
have not been detected in the posterior head sensory organ
of Dactylopodola baltica from the North Sea. It is supposed
that the lack of those microvilli is related with a functional
change of this organ in North Sea populations of D. baltica.
As there is also a cup-shaped, pigment-bearing sheath cell,
Liesenjohann etal. (2006) conclude that the posterior head
sensory organ of their D. baltica rather sense directed light
shielded by the pigment cell than being a chemoreceptor.
The anterior head sensory organ of D. baltica from the North
Sea seems to lack any pigment-bearing cell and could there-
fore represent a more general light sensitive organ.
1.2.6Intestinal system
The intestinal system of gastrotrichs starts with a termi-
nal or slightly subterminal anterior mouth, followed by
a buccal cavity, a large myoepithelial pharynx, a midgut,
and it ends in a ventral anus in the posterior end (Fig.
1.22 A). The pharynx is constructed as a sucking pharynx
and all gastrotrichs appear to suck in small food partic-
les together with some water. Bacteria, diatoms, and pro-
bably detritus are the most common food particles (e.g.,
Todaro & Hummon 2008; Fig. 1.22 D, E, G, H).
The mouth opening is in many cases (Paucitubula-
tina, several macrodasyids) a narrow, round opening
(Figs. 1.22 B and 1.23 A, B). In other species, e.g., in Neo-
dasys, it widens a bit to form a slight funnel, and in some
species, especially those belonging to Thaumastoderma-
tidae, the mouth opens with a wide funnel that occup-
ies almost the entire frontal end of the animal (Figs. 1.22
C, D and 1.23 E). A narrow mouth opening appears well
suited for a targeted picking up of food particles such as
bacteria, whereas broad mouth openings appear better
suited for an untargeted sweeping of the surrounding.
In some species, e.g., in the genera Paraturbanella and
Macrodasys, the mouth opening is a longitudinal slit
rather than a round opening (Ruppert 1991). Especially
among paucitubulatinans, the mouth opening is often
surrounded by a strengthened cuticle, the mouth ring,
from which further cuticular structures, e.g., spines,
can originate and form more or less complex buccal
structures often called “buccal cage” or “mouth basket”
(see, e.g., Balsamo et al. 2010a on Diuronotus aspetos
as one example; Fig. 1.23 A). In Musellifer species, the
anterior end of the head forms a snout-like part, the so-
called muzzle, which is densely covered by cilia (e.g.,
Leasi & Todaro 2010). Some macrodasyids, for example,
Prostobuccantia have similar elaborations of the mouth
opening (Evans & Hummon 1991). Brought about by
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1.2Morphology 35
50 µm
100 µm
100 µm
20 µm
20 µm
50 µm
50 µm
50 µm
AB CD
E
F
pp
ph
mg
*
G
an
mg
ph
H
mo
*
oo
*
mo
*
pp
Fig. 1.22: Intestinal system of Gastrotricha. (A) Turbanella hyalina (Macrodasyida), horizontal view. Note the typical partition of the gut tube
into mouth, buccal cavity, pharynx, midgut, and anus. (B) A marine Chaetonotus sp. (Paucitubulatina) with a subterminal mouth opening,
ventral view. (C) Diplodasys cf. meloriae (Macrodasyida) with the characteristic funnel-shaped mouth opening of the Thaumastodermatidae,
ventral view. (D) Tetranchyroderma sp. (Macrodasyida) with a rather big diatome inside the midgut (asterisk), horizontal view. (E) Midtrunk
section (lateral view) of a Neodasys chaetonotoideus (Multitubulatina) that have had a menu of different diatomes. (F) Midtrunk section of
Xenodasys riedli (Macrodasyida). Note the high density of motile cilia inside the posterior portion of the pharynx and in the anterior part of
the midgut (asterisks). (G) Middle portion of the midgut of N. chaetonotoideus with 2 euglenoids inside. The algae were still moving when
the micrograph has been taken. (H) Posterior part of the midgut of Xenotrichula carolinensis with a tiny diatome inside (asterisk).
(A–C, E and F, H) DIC images. (D and G) BF images. Abbreviations: an, anus; mg, midgut; mo, mouth opening; oo, mature oocyte; ph, pharynx;
pp, pharyngeal pore.
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36 1Gastrotricha
5 µm
4 µm
20 µm
10 µm 15 µm
AB
CD E
an
sci
TbA
ce
TbA
sci
sci
contractions of certain pharyngeal muscles, the cuticu-
lar elements of the buccal cage can be moved forward
and the mouth opening may be extended in this way
(e.g., Remane 1936, Schwank 1990).
The mouth opening leads into a short buccal tube or
buccal cavity. In some macrodasyid species, the pharynx
appears to attach directly at the mouth opening, but in
some macrodasyid species and in pauctitubulatinan chae-
tonotids, the buccal cavity forms a short cylindric compart-
ment. Tooth-like structures are present in species of the
macrodasyid genus Lepidodasys (Remane 1936, Ruppert
1991) and in several paucitubulatinans (Chaetonotus
pawlowskii, some species of Aspidiophorus, Heterolepido-
derma, and Arenotus (Schwank 1990). These are movable
by musculature and are supposed to serve as scrapers
(Schwank 1990, see also figures 82 and 83 in Ruppert 1991).
The pharynx is a long cylinder with a triradiate
lumen (Fig. 1.24 A–C). The musculature is oriented radi-
ally between the lumen and the surrounding ECM. Con-
tracting radial myoepithelial cells rapidly extend the
pharyngeal lumen and suck in food particles. Anteropos-
terior contraction waves over the pharynx lead food into
the midgut (Remane 1936, Ruppert 1991). Most compara-
tive information on the gastrotrich pharynx goes back to
Ruppert (1982; updated in Ruppert 1991).
The triradiate pharyngeal lumen has two dif-
ferent orientations. In species of Chaetonotida
(Paucitubulatina+Neodasys), it has the shape of a Y
when cross-sectioned (Fig. 1.23 A, B), with paired dor-
solateral branches and an unpaired ventral branch;
in Macrodasyida, the orientation is an inverted Y (Fig.
1.24 C). The pharynx is ectodermal and therefore lined
by cuticle. The pharyngeal cuticle is similar to the body
cuticle and composed of endocuticle and epicuticle. The
number of epicuticular layers is often larger than in the
body cuticle (Ruppert 1991). The pharyngeal endocu-
ticle often lacks the apical fibrillar layer that is present
in the body cuticle and basally a number of spherical
structures are observed (Ruppert 1991). The cells com-
posing the pharynx are myoepithelial, nervous, sensory,
and gland cells. The apical cells, i.e., those at the end
of the luminal branches differ from the remaining (Figs.
1.13 D and 1.24 E), interapical cells in the abundant pre-
sence of tonofilaments, which connect the cuticle to the
surrounding ECM and are therefore probably respon-
sible for maintaining the triradiate shape of the lumen
(Ruppert 1991). Most macrodasyid and larger chaetono-
tid species have multisarcomeral cells; some macroda-
syids and most chaetonotids have monosarcomeric cells
(Ruppert 1982, 1991).
In general, three pharyngeal neurite bundles are
present in Chaetonotida (Fig. 1.24 A) and four in Macro-
dasyida (Ruppert 1982). Each neurite bundle may be com-
posed of about 15 neurites as in Dactylopodola baltica
Fig. 1.23: Intestinal system of Gastrotricha.
SEM micrographs of external openings of the
gut tube. (A) Ventral view of head region of
Chaetonotus sp. (Paucitubulatina) with the
subterminal mouth opening surrounded by
cuticular hook-like structures (mouth basket).
(B) Anterior end of Macrodasys caudatus
(Macrodasyida) with the terminal mouth
opening surrounded by velum-like cuticular
structures. (C) Pharyngeal pore of Mesodasys
sp. (Macrodasyida). (D) Ventral anus of
Tetranchyroderma sp. (Macrodasyida) close
to the posterior adhesive tubes. (E) Funnel-
like mouth opening of Tetranchyroderma sp.
Abbreviations: an, anus; ce, cephalion; sci,
sensory cilia; TbA, anterior adhesive tubes.
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1.2Morphology 37
1 µm1 µm
10 µm 3 µm
3 µm2 µm
ac
AB
CD
EF
pl
cm
lm
gl
*
*
*
*
tm
Fig. 1.24: Ultrastructure (TEM cross sections)
of the intestinal system of Gastrotricha.
(A) Pharynx of Neodasys chaetonotoideus
(Multitubulatina). Note the 3 pharyngeal
neurite bundles (asterisks). (B) Pharynx of
Xenotrichula carolinensis (Paucitubulatina).
(C) Pharynx of Dactylopodola typhle
(Macrodasyida). Note the ventral pharyngeal
neurite bundle (asterisk). (D) Midgut of
N. chaetonotoideus. (E) Detail of the midgut
epithelium of N. chaetonotoideus. Note
the dense fringe of microvilli. (F) Detail of
the pharynx of N. chaetonotoideus with
the multisarcomeric myofilaments and the
subpharyngeal musculature. Abbreviations:
ac, apical cell; cm, circular muscles;
gl, gut lumen; lm, longitudinal muscles;
pl, pharyngeal lumen; tm, transverse muscle.
(Rothe & Schmidt-Rhaesa 2009). However, there are at
maximum five neurites per pharyngeal neurite bundle in
Neodasys chaetonotoideus (Rothe etal. 2011a). The posi-
tion is basiepidermally, i.e., close to the outer ECM of the
pharynx. The pharyngeal neurite bundles are associated
with sensory cells, which are aligned in longitudinal rows
(Ruppert 1982, Rothe & Schmidt-Rhaesa 2009, Rothe etal.
2011a). The sensory cells have a short cilium surrounded
by microvilli. The cilium projects into the pharyngeal
lumen, but remains covered by cuticle (Ruppert 1982,
Rothe etal. 2011a, see also chapter Sensory Structures).
With the exception of Lepidodasys, the pharynx in
species of Macrodasyida opens to the external by a pair
of pharyngeal pores (Fig. 1.23 C). In many species, these
pores are in the posterior part, close to the transition to the
midgut, but in some species, the pores are further anterior
(e.g., in Macrodasys species). The pharyngeal pores have
a sphincter that is derived from circumpharyngeal circu-
lar muscles. Although their actual function is not fully
understood, it is assumed that excess water from food
uptake is released through the pores (Ruppert 1991).
Cilia and microvilli (apart from those of the pharyn-
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38 1Gastrotricha
geal sensory cells) in the pharynx are usually absent,
but in few species, their occurrence is observed. Most
conspicuous is the presence of long cilia in the region
of the pharyngeal pores in species of Chordodasiopsis
and Xenodasys (e.g., Schöpfer-Sterrer 1969, Rieger etal.
1974; Fig. 1.22 F) and Dendrodasys (Wilke 1954). Micro-
villi are less obvious, only in Lepidodasys and Neodasys
do they occur in some abundance, but remain below the
cuticle (Ruppet 1991). In Xenodasys, Dactylopodola, and
Dolichodasys, however, microvilli penetrate the cuticle
(Ruppert 1991).
In several chaetonotids the pharynx forms one or more
bulbous extensions. Schwank (1990) reports regions free of
musculature in chaetonotids, which creates a characteristic
banding pattern of the pharynx. The transition to the midgut
is simple in macrodasyids, but more complex in chaetono-
tids. In Neodasys, the posterior part of the pharynx forms
some folds before the lumen joins the midgut (Ruppert
1991). In species of Paucitubulatina, the posterior end of the
pharynx extends into the anterior region of the midgut in
the form of a plug (Ruppert 1991), which may function as a
kind of weir or valve (Swank 1990).
The midgut is straight, without any diverticles or
attaching structures, and does not show any obvious
compartmentalization. It is composed of a simple absorp-
tive epithelium (Ruppert 1991). Microvilli are present
(Fig. 1.24 D, E), cilia are rarely present (in Xenodasys and
probably in Dendrodasys, see Ruppert 1991). Teuchert
(1977a) reported putative sensory cells in the midgut of
Turbanella cornuta. In some paucitubulatinans, a regio-
nalization of the midgut is present and evident by a dif-
ferent coloration (Schwank 1990). Here the anterior part
is called stomach. A comparable regionalization may also
be found in some macrodasyidans such as Anandrodasys
agadasys (Kieneke etal. 2013a).
In Macrodasyida, no hindgut is present; only species
of Paucitubulatina possess a short cuticularized hindgut
(Ruppert 1991). The anus is a simple pore (Fig. 1.23 D), it is
often inconspicuous, and in species of Urodasys, it appears
to be lacking (e.g., Wilke 1954, Schöpfer-Sterrer 1974).
1.2.7Body cavities and connective tissue
Gastrotrichs are compact animals with comparably few
connective tissue, but this condition has been interpre-
ted in different ways. All tissues and cells attach closely
to each other. Between epidermis and intestine, muscle
and nerve cells, gonads, excretory cells, and few meso-
dermal cells called Y-cells are present. ECM surrounds
the muscle cells, the Y-cells, the protonephridial and
gonadal tissue (Ruppert 1991). This ECM is often very
thin and uniform, different layers cannot be distin-
guished (Ruppert 1991). Ruppert (1991) indicates tiny
lacunar spaces in some places, but it is not clear whether
such spaces constitute true lacunes of a primary body
cavity or regions within the ECM. In figure 56 in Ruppert
(1991), such “intercellular lacunae” have a gray stai-
ning, similar to the staining of ECM material and may
therefore also be intercellular regions filled with ECM.
Comparable widenings of the intercellular space filled
with ECM are known from the region of the protonephri-
dial terminal cells in different gastrotrich species (e.g.,
Kieneke etal. 2007, 2008c, Kieneke & Hochberg 2012).
Therefore, we interpret the body organization of gastro-
trichs as acoelomate, i.e., with a primary body cavity in
compact organization.
Despite the compact organization of the gastrotrich
body, they were occasionally interpreted as coelomate
animals. This goes back to Remane (1936), who inter-
preted a muscular layer surrounding internal tissue as
an equivalent of a mesodermal epithelium. In a case
like gastrotrichs, this means consequently that the body
cavity is filled with tissue, e.g., the gonads. This view was
extended by Teuchert & Lappe (1980; see also Teuchert
1977b and Reisinger 1978). However, this interpretation
has two flaws. First, body cavities are, as the name says,
cavities and when a cavity becomes occupied by tissue,
it is not a cavity any more. Then, as the muscle cells are
completely surrounded by ECM, a cavity, if it was present,
would be bordered by ECM and not by an epithelium.
According to this, a cavity would be a primary body cavity
(“pseudocoelom”) and not a coelom (see, e.g., Schmidt-
Rhaesa 2007).
A conspicuous cell type in a mesodermal position
are the Y-cells, which have been best investigated in
Turbanella (Teuchert 1977a, Travis 1983, Ruppert 1991).
The Y-cells are arranged in a longitudinal row lateral of
the pharynx and the intestine (Figs. 1.14 E; 1.25). Espe-
cially in the posterior part, they are in close relation to
the longitudinal musculature. Each Y-cell has a central
nucleus, little cytoplasm, and a large vacuole. It has been
speculated that the row of Y-cells forms an antagonist to
the musculature (Reisinger 1978), this would make sense
in the flexing movements observed in Turbanella during
aggregation and copulation (Teuchert 1968, 1978). Proba-
bly homologous cells occur in some other macrodasyids,
such as species of Paraturbanella, Macrodasys, Lepidoda-
sys, Acanthodasys, Oregodasys, Tetranchyroderma, and
Chordodasiopsis (Travis 1983). Sometimes they occur in
rows, sometimes as single cells. Most of these cells contain
myofilaments and are therefore likely derived from muscle
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1.2Morphology 39
cells (Travis 1983, Ruppert 1991). Apart from the assumed
antagonistic/skeletal role, their function is unknown.
Neodasys sp. has large hemoglobin-containing cells in a
comparable position (Kraus etal. 1981, Ruppert & Travis
1983), these are probably also homologous to the Y-cells,
but their storage function for hemoglobin appears to be
restricted to Neodasys (see chapter Physiology). However,
reddish-colored Y-cells may also occur in further species
such as in the recently described Oregodasys caymanensis
(Hochberg etal. 2014). Another strange organ that pro-
bably derived from muscle cells is the chordoid organ in
species of Xenodasys and in Chordodasiopsis antennatus.
It consists of anteroposteriorly piled disc-shaped cells pos-
terior to the anus. Each cell contains myofibrils that trans-
versally span through the cytoplasm (Rieger etal. 1974).
Although this organ in the mentioned gastrotrich species
has a comparable ultrastructure like the notochord of the
cephalochordate (Branchiostoma), it is not known if it
likewise has a skeletal function.
1.2.8Excretory system
Protonephridia have been known for a long time to be
present in freshwater gastrotrichs (e.g., Zelinka 1889).
Initially, the whole group of Macrodasyida was suppo-
sed to lack protonephridia throughout (Remane 1936).
Later on, serially arranged protonephridia were detected
in several Macrodasyida species (Fig. 1.26) when using
phase contrast optics (Wilke 1954, Teuchert 1967).
The first electron microscopic survey was done on the
protonephridial terminal organ of Chaetonotus sp.
(Brandenburg 1962). This study supported the general
20 µm
yc
mg
lm
gl
lnb cm
lc
TbDL
cu
ed
yc
lc
TbD
tes
Fig. 1.25: Position of the Y-cells of Turbanella cornuta, schematic
cross section at the body region of the paired testes. There is no
body cavity apart from the gut lumen and the lumina of the testes.
Abbreviations: cm, circular muscles; cu, cuticle; ed, epidermis
gl gut lumen; lc, locomotory cilia; lm, longitudinal muscles; lnb,
longitudinal neurite bundles; mg, midgut; TbD, dorsal adhesive
tubes; TbDL, dorsolateral adhesive tubes; tes, testis; yc, Y-cells.
(Modified from figure 2E of Teuchert 1977.)
ultrastructural composition of protonephridial termi-
nal structures in bilaterian animals: they consist of a
cytoplasmic hollow cylinder that is broken by pores
or clefts, which are spanned by a filtering diaphragm,
a system of motile cilia beating inside a protonepridial
lumen (hence generating a negative pressure inside the
proximal lumen), and microvilli surrounding the cilia.
Subsequent studies on the protonephridial system of Tur-
banella cornuta (Teuchert 1973) showed an aberrant mor-
phology of the protonephridia in that species consisting
of up to five monociliary terminal cells, one large canal
cell, and an adjacent putative nephridiopore cell. The
composition of protonephridia in Dactylopodola baltica
and Mesodasys laticaudatus is less complex as their pro-
tonephridia are composed of three cells: one terminal,
one canal, and one nephridiopore cell (Neuhaus 1987,
see also Bartolomaeus & Ax 1992). However, although
quite similar in morphology and ultrastructure, slight
differences were also detected: although most gastro-
trich species, as far as we know now, lack a cilium in the
nephridiopore cell, such an organelle was found in the
lumen of the nephridiopore cell of Dactylopodola baltica
(Neuhaus 1987). Recently, a series of studies on the excre-
tory system of other gastrotrich species has been carried
out (Kieneke etal. 2007, 2008c). The aim of these studies
was to get a broader database of more species to infer the
evolution of these organs as well as the character pattern
of the stem species of Gastrotricha. Besides the systema-
tically important species Neodasys chaetonotoideus (see
chapter Phylogeny), two members of the derived taxon
Paucitubulatina were studied. Data on Xenotrichula caro-
linensis and Chaetonotus maximus proved that the proto-
nephridial system of the stem species of Paucitubulatina,
whose monophyly is supported in almost all phylogene-
tic analyses (see chapter Phylogeny), consists of a single
pair of protonephridia, each composed of a bicellular
terminal organ with a so-called composite filter, a volu-
minous and aciliar canal cell with a convoluted lumen,
and a nephridiopore cell (Kieneke etal. 2008c). Such a
basic protonephridial anatomy is also much likely in the
freshwater paucitubulatinan species Polymerurus nodi-
caudus (Kieneke & Hochberg 2012). The excretory system
in Neodasys chaetonotoideus consists, as well as in mac-
rodasyids, of serial pairs (three) of tricellular protoneph-
ridia. Although the terminal and canal cell each have one
cilium, it is lacking in the nephridiopore cell (Kieneke
et al. 2007). Unique character states, possibly apomor-
phic for the genus Neodasys, are the number of seven
instead of the usually found eight circumciliary microvilli
in the terminal cell and a bundle of numerous long ciliary
rootlets in the canal cell.
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40 1Gastrotricha
Taking data from the published ultrastructure-based
reconstructions of gastrotrich protonephridia (plus scat-
tered results provided in Ruppert 1991) and using two
phylogenetic hypotheses for character optimization (i.e.,
Hochberg & Litvaitis 2000, Todaro et al. 2006a; see Fig.
1.53 A and F), a stable hypothesis for the protonephridial
system of the last common ancestor, the stem species of
Gastrotricha, was reconstructed (Kieneke et al. 2007).
Owing to several highly conserved characters shared by
Neodasys chaetonotoideus, Dactylopodola baltica, and
Mesodasys laticaudatus and to a probably derived posi-
tion of Turbanella cornuta as well as the whole Pauci-
tubulatina, a reconstruction of the gastrotrich ground
pattern on the basis of both used phylogenetic scenarios
yielded almost equal results. This is also true for most
other tree topologies because Paucitubulatina mostly
occupy a derived position (see chapter Phylogeny). In the
following, the protonephridial system as it probably existed
in the common ancestor of Gastrotricha is described.
Structural novelties in recent taxa with regard to the
ground pattern will be presented later. The stem species
of Gastrotricha has serial pairs of three-cellular protone-
phridia that are not connected to each other by a common
duct (Fig. 1.27). The exact number of pairs remains unclear
because this pattern varies considerably between the diffe-
rent species (see, e.g., Fig. 1.26). Dactylopodola baltica, for
instance, has 2 pairs of protonephridia, and in Mesodasys
laticaudatus, 11 pairs have been counted (Neuhaus 1987).
Each protonephridium is situated in a lateral compart-
ment of the trunk where it is adjacent to other tissues
as, for example, the epidermis, musculature, and gut
epithelium (Fig. 1.30 F). The nephridiopore cell, or at least a
distal bulge of it, is embedded within the ventral epidermis
via cellular junctions. A thin layer of ECM (perinephridial
50 µm
50 µm
50 µm
50 µm
50 µm
50 µm
A
BC
D
pn
E
FFig. 1.26: Different representatives of
Gastrotricha (schematic) showing position
and numbers of protonephridia (in black).
(A) Neodasys chaetonotoideus, dorsal view.
(B) Redudasys fornerise, ventral view.
(C) Turbanella cornuta, ventral view.
(D) Mesodasys laticaudatus, dorsal view.
(E) Xenotrichula carolinensis, ventral view.
(F) Dactylopodola baltica, dorsal view.
Abbreviation: pn, protonephridium.
(A and E, modified from Kieneke etal. 2007;
C, modified from Teuchert 1967; B, modified
from Kisielewski 1987; D and F, modified
from Neuhaus 1987.)
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1.2Morphology 41
(1973) seem to support such filter architecture at least in
the protonephridium of T. cornuta because cross sections
of the distal part of the terminal cell indicate an enfolded
lumen because of the presence of a septate junction in
this region of the cell (see Fig. 1.28 C). Such a construction
of the terminal cell lumen in T. cornuta was already sup-
posed by Rieger etal. (1974) and supported by their own
unpublished results on Turbanella ocellata. The terminal
cell of the stem species of Gastrotricha possesses a single
cilium projecting into the lumen and is encircled by a
column of eight long microvilli. Each of them is linked to
the adjacent one by a flocculent ECM (Fig. 1.27 B–C). In
some species, however, this inter-microvillar ECM shows
a remarkable ultrastructure: in Turbanella cornuta and
Chaetonotus maximus, it consists of numerous alternating
pores when sectioned tangentially and of alternating elec-
tron-lucent and electron-dense bands in cross sections
(Teuchert 1973, Kieneke etal. 2008c; Fig. 1.30 E). Interes-
tingly, the fine structure of this inter-microvillar ECM is
quite similar to material present between the 10 circumci-
liary microvilli of external mechanoreceptive sensory cells
(“tactile hairs”) of Turbanella cornuta (Teuchert 1976a, see
chapter Sensory Structures, Fig. 1.19 B). Such a similarity
between terminal cells and epidermal sensory cells could
hint to the assumed ectodermal origin of protonephridia.
The cilium of the terminal cell of the stem species of Gast-
rotricha has a basal body but an accessory centriole and
rootlet structures are lacking. Of course, there are species
ECM) surrounds the whole organ. This matrix can slightly
be thickened in the filter region of the terminal cell (see,
e.g., Kieneke etal. 2007 for Neodasys chaetonotoideus, Fig.
1.30 B–C). The three protonephridial cells are the proximal
terminal cell, the canal cell, and the distal nephridiopore
cell (Fig. 1.27). All cells are connected to the adjacent one
by cellular junctions, a combination of belt desmoso-
mes (probably for the histomechanic connection), and
septate junctions that seal the intercellular gap against
diffusion processes. Each of the cells forms a lumen by
curling around itself and sealing the resulting cleft with an
autodesmosome (term sensu Kristensen & Hay-Schmidt
1989). This condition was termed enfolded lumen (Kieneke
et al. 2008c). Linked to each other, the protonephridial
lumen forms a continuous duct from the proximal filter
region to the distal nephridiopore (Fig. 1.27).
In Turbanella cornuta, Dactylopodola baltica, and
Mesodasys laticaudatus, the terminal cell is described as
a cytoplasmic hollow cylinder broken by pores and short
slits (Teuchert 1973, Neuhaus 1987), hence representing a
simple filter according to the terminology of Kieneke etal.
(2008c). However, Kieneke etal. (2007) suggest an enfolded
lumen filter in the ground pattern of Gastrotricha is quite
likely (Fig. 1.27 B, C, E). In Neodasys chaetonotoideus, such
an enfolded lumen filter is formed by a meandering cleft of
the single terminal cell sealed by a diaphragm (Fig. 1.30 C).
The same cleft is further distally sealed off by an auto-
desmosome. Ultrastructural data presented by Teuchert
2 µm
AB
C
D
elf
E
ci
ci
ci
ci
ci
mv
mv
mv
mv
pl
ime
elf cj
cj
cj
cut
mi
cr
bb
mi
pl
np
tc
cc
nc
bb
ac
cj
ep
ep
ime
cj di
Fig. 1.27: Protonephridium (scheme) of
the last common ancestor of Gastrotricha.
(A) Longitudinal section through the
whole organ showing all 3 cells. Levels
of sectional plane for B, C, and D are
indicated by bold lines. (B) Cross section
of the terminal cell (region of the nucleus).
(C) Cross section of the terminal cell (filter
region). (D) Cross section of the canal cell.
(E) Exterior view of the terminal cell with the
enfolded lumen filter. Abbreviations:
ac, accessory centriole; bb, basal body;
cc, canal cell; ci, cilium; cj, cellular junction
(septate junction plus belt desmosome);
cr, ciliary rootlet; cut, body cuticle;
di, filter diaphragm spanning the cleft;
elf, enfolded lumen filter; ep, epidermis;
ime, inter-microvillar ECM; mi,
mitochondria; mv, microvilli;
nc, nephridiopore cell; np, nephridiopore;
pl, protonephridial lumen; tc, terminal cell.
Black triangles indicate the seam
of the enfolded lumen, the broken black
line represents the ECM surrounding the
whole organ.
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42 1Gastrotricha
5 µm
A
BC
sf
ci
mv
mv
mv
ime
cj
cj
cj
bb
mi
np
tc cc
nc
bb
cj
ime
cj
tc
tc
tc
tl
tl
cl
cl
cl
nl
sf sf
di
cj
Fig. 1.28: Scheme of the derived protonephridium of Turbanella cornuta (Turbanellidae). (A) Schematic longitudinal section, partially
exterior view (modified from Teuchert 1973). (B) Cross section of a terminal cell at the filter region. (C) Cross section of a terminal cell at
slightly more proximal region than in B. Levels of sectional plane for B and C are indicated by bold lines, cross sections slightly enlarged.
Abbreviations: bb, basal body; cc, canal cell; ci, cilium; cj, cellular junction (septate junction plus belt desmosome); cl, canal cell lumen;
di, filter diaphragm spanning the pores; ime, inter-microvillar ECM; mi, mitochondria; mv, microvilli; nc, nephridiopore cell; nl, nephridiopore
cell lumen; np, nephridiopore; sf, simple filter; tc, terminal cell; tl, terminal cell lumen. The black triangle indicates the seam of the enfolded
lumen of the terminal cell, the broken black line in B and C represents the ECM surrounding the whole organ. (Modified from Teuchert 1973.)
that do possess an accessory centriole and ciliary rootlet
structures in its protonephridia terminal cells as, for
example, Dactylopodola baltica (Neuhaus 1987).
The canal cell is interlinked between the proxi-
mally adjacent terminal cell and the distally adjacent
nephridiopore cell. It constitutes the major part of the
protonephridial lumen. The single cilium and a bundle of
numerous microvilli (a “brush border”) project into this
lumen (enfolded lumen, see above; Figs. 1.27 D, 1.30 G).
The large number of microvilli in this cell probably cons-
titutes an extended surface of the luminal cell membrane
and hence increases the rate of exchange processes
through this membrane. The canal cell cilium of the
common ancestor of Gastrotricha has a basal body and a
ciliary rootlet, an accessory centriole is lacking (Fig. 1.27 A).
The nephridiopore cell constitutes the permanent
and cuticle-lined, ventral nephridiopore (Fig. 1.30 H–J).
Owing to its ability to secrete a cuticle, the nephridiopore
cell, if not the whole protonephridium, is regarded to be
of ectodermal origin (see Neuhaus 1987 and above). Due
to to equivocal data – some species possess nephridio-
pore cells with an enclosed lumen, others with an enfol-
ded lumen – is yet not sure which type was present in
the common ancestor of Gastrotricha. Although there are
species that have a monociliated nephridiopore cell (i.e.,
Dactylopodola baltica, Neuhaus 1987), such an organelle
is missing in the stem species (Fig. 1.27). However, there
is a basal body and possibly an accessory centriole as
well (the latter character stayed equivocal, see table 2 in
Kieneke etal. 2007).
A characteristic set of organelles can be found in
each of the protonephridial cells of the studied species
(i.e., an active nucleus, mitochondria, rough endoplas-
mic reticulum, dictyosomes). Mitochondria are relatively
abundant in the protonephridial cells to provide energy
(or ATP, respectively) for the beating actions of the pro-
tonephridial cilia and other energy-dependant transport
processes. Especially in the canal cell one can find a high
abundance of small (50–100 nm in diameter) vesicles
close to the luminal membrane, sometimes coalesced
with it. In addition, there are coated pits and coated
vesicles (Ruppert 1991). This can hint to transport proces-
ses in both directions: excretion as well as re-adsorption
via vesicular transport to or from the protonephridial
lumen is possible. Species like Xenotrichula carolinensis
have large vacuoles in the canal cell that could be used
for storing certain degradation products (Kieneke etal.
2008c).
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1.2Morphology 43
2 µm
A
BC
mv
cf
mi
np
to
cc
nc
cj
ime
cj
tl
dcl
ci
nl
di
cj
to
cc
nc
pcl
al
ep
cu
pcl
Fig. 1.29: Scheme of the derived protonephridium of Paucitubulatina as exemplified by Chaetonotus maximus. (A) Schematic longitudinal
section, composite filter of the terminal organ as exterior view. (B) Cross section of the terminal organ at the filter region. (C) Cross section
of the canal and the nephridiopore cell at the level of the canal cell nucleus. Levels of sectional plane for B and C are indicated as bold
lines. B and C slightly enlarged. Abbreviations: al, anterior loop of the canal cell lumen, cc canal cell; cf, composite filter; ci, cilium; cj,
cellular junction (septate junction plus belt desmosome); cu, body cuticle; dcl, distal canal cell lumen; di, filter diaphragm spanning the
clefts; ep, epidermis; ime, inter-microvillar ECM; mi, mitochondria; mv, microvilli; nc, nephridiopore cell; nl, nephridiopore cell lumen; np,
nephridiopore; pcl, proximal canal cell lumen; tl, terminal organ lumen; to, terminal organ (consists of 2 adjacent terminal cells). The black
triangles indicate the seam of the enfolded lumen of the canal cell and the nephridiopore cell, the broken black line in B represents the ECM
surrounding the whole organ. (Modified from Kieneke etal. 2008c.)
Many evolutionary changes from the above developed
character states of the common ancestor of Gastrotricha have
at least (as we know today) occurred within the stem lineages
of the genus Turbanella and within that of the taxon Paucitu-
bulatina, some of which have already been mentioned earlier.
The protonephridial system of Turbanella cornuta, T. ambro-
nensis, and T. subterranea consists of four pairs of protone-
phridia situated in the middle pharynx region as well as in
the anterior, middle, and posterior intestine region (Teuchert
1967, see also Fig. 1.26 C). Each protonephridium of Turbanella
cornuta consists of two to four monociliary terminal cells, one
voluminous, monociliary canal cell and one smaller, non-cili-
ated nephridiopore cell that is embedded within the ventral
epidermis (Teuchert 1973). The multiple terminal cells neither
form a common terminal organ nor an aggregation of cells
but are singular cells attached to the canal cell at different
sites (Fig. 1.28). According to Teuchert (1973), there is no con-
tinuous lumen in the protonephridia of Turbanella cornuta
(i.e., a connection from the terminal cell lumina via the canal
cell lumen to the nephridiopore cell lumen). Within the stem
lineage of Paucitubulatina, different evolutionary transfor-
mations have happened. The number of protonephridia was
reduced to a single pair (see Figs. 1.26 E and 1.30 A). Each pro-
tonephridium consists of a bicellular terminal organ formed
by two monociliary terminal cells that lie close to each other
(Fig. 1.30 B), one huge canal cell and one small nephridiopore
cell (Fig. 1.29). Both terminal cells form a so-called composite
filter by providing reciprocally indented, finger-like processes
thus enclosing cilia and microvilli. The cleft between those
podocyte-like processes is spanned by a filter diaphragm
(Kieneke etal. 2008c, Kieneke & Hochberg 2012). The huge
canal cell constitutes the major part of the protonephridial
lumen in species of the Paucitubulatina. As in Neodasys and
macrodasyidan species, it is formed by an invagination of the
cell membrane (enfolded lumen) of the canal and the neph-
ridiopore cell. However, the canal and nephridiopore cell of
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44 1Gastrotricha
20 µm 400 nm
2 µm
1 µm5 µm0.5 µm
1 µm
2 µm
1 µm
1 µm
AB
CD
mg
mv
tc
*
te
mg
ecm *
*
mv
ed
cc
EF
G
HI J
to
cc
va
*
*
*
*
cir
npc
*
npc
*
bb
mv
Fig. 1.30: Ultrastructure of the protonephridia of Gastrotricha. (A) Chaetonotus sp. (Paucitubulatina) with 1 pair of protonephridia (triangles)
already visible under the light microscope (DIC image). (B) Cross section of the terminal organ of Chaetonotus maximus (Paucitubulatina)
consisting of 2 monociliary terminal cells. (C) Cross section of the protonephridial terminal cell of Neodasys chaetonotoideus
(Multitubulatina). Note the widened extracellular space around the cell. (D) Terminal organ and canal cell of Xenotrichula carolinensis
(Paucitubulatina). Note the convoluted protonephridial lumen (asterisks). (E) Oblique longitudinal section of the terminal organ of
C. maximus. Note the reticulate material between the circumciliary microvilli (triangle). (F) Position of the protonephridium of X. carolinensis
(asterisk) between midgut, muscles and testes. (G) Longitudinal section of the canal cell and nephridiopore cell of N. chaetonotoideus.
The protonephridial lumen is densely filled with microvilli (asterisks). (H) Lumen of the nephridiopore cell of C. maximus. Note the auto-
desmosome of the enfolded lumen (triangle). (I) Nephridiopore cell of N. chaetonotoideus with the distal lumen close to the nephridiopore
(triangle). (J) Cuticular tube (asterisk) that continues the nephridiopore of C. maximus. (A) DIC image. (B–J) TEM micrographs. Abbreviations:
bb, basal body; cc, canal cell; cir, cirri; ecm, extracellular matrix; ed, epidermis; fi, filter; mg, midgut; mv, circumciliary microvilli of the
terminal cell; npc, nephridiopore cell; tc, terminal cell; te, testis; to, terminal organ; va, vacuole.
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1.2Morphology 45
paucitubulatinan species lack cilia and microvilli altogether.
A remarkable evolutionary novelty is the strong elongation
of the canal cell lumen: in all species studied so far, Xenotri-
chula carolinensis, Chaetonotus maximus, and Polymerurus
nodicaudus, the narrow lumen runs strongly convoluted
through the canal cell (Kieneke et al. 2008c, Kieneke &
Hochberg 2012; Figs. 1.29, 1.30 D). Although not studied in
detail, such a meandering course of an elongated canal cell
lumen is also present in Aspidiophorus sp. (figure 16 of Ruppert
1991) and other (all?) members of the Paucitubulatina (see,
e.g., light microscopic image 3 of Chaetonotus bisacer and
image 38 of Heterolepidoderma sp. in Weiss 2001 and figure
3 on page 235 of Chaetonotus robustus in Kreuz & Foissner
2006). In freshwater species such as C. maximus and P. nodi-
caudus, the canal cell lumen even forms a prominent anterior
loop (see Fig. 1.29), possibly used to utilize the counter current
flow effect for concentrating salts, which shall be saved for
the organism via re-adsorption (Kieneke & Hochberg 2012). A
comparable construction with highly elongated and convolu-
ted protonephridial lumen that forms distinct loops is proba-
bly also present in other freshwater-dwelling taxa such as the
Neogosseidae (see figure 2S in Todaro etal. 2013).
Open questions addressing the protonephridial
system of Gastrotricha concern of course the morphology
of the filter in macrodasyidan gastrotrichs (i.e., simple
filter or enfolded lumen filter), which is yet not satisfyingly
known (see Kieneke etal. 2007). Furthermore, protoneph-
ridia morphology and ultrastructure is not known for the
majority of genera of the Macrodasyida. Among them are
taxa like Tetranchyroderma, Thaumastoderma, Pseudosto-
mella, Oregodasys, Acanthodasys, and Diplodasys, all of
the family Thaumastodermatidae. As Thaumastoderma-
tidae could be the sister group of Paucitubulatina accor-
ding to one of the DNA sequence-based cladistic analyses
(Todaro etal. 2006a), it would be really interesting to find
out whether there are similarities (putative synapomor-
phies) between the protonephridia of Thaumastodermati-
dae and Paucitubulatina. To our knowledge, there is just a
single published TEM micrograph of a cross section of the
protonephridium of a species of Thaumastodermatidae
(Diplodasys sp.: see figure 9f of Rieger et al. 1974). Apart
from this special focus on the Thaumastodermatidae, pro-
tonephridia ultrastructure has proven its general value for
phylogenetic questions, not only in Gastrotricha. Hence, it
is of valid interest to increase our knowledge about pro-
tonephridia morphology and ultrastructure among the
diverse lineages within this phylum. Probably, this will
provide new input to the still unresolved internal phylo-
geny of Gastrotricha (see chapter Phylogeny). Some cross
sections through a protonephridium of Chordodasiopsis
antennatus, for instance, indicate an aberrant morphology
with numerous microvilli inside the terminal cell lumen
that surround the circle of eight circumciliary microvilli of
the terminal cell (see figure 9c of Rieger etal. 1974).
1.2.9Reproductive organs
Almost all marine gastrotrich species (the entire Macro-
dasyida and the basal chaetonotidan groups Neodasys,
Xenotrichulidae and Muselliferidae) are hermaphroditic
animals with male and female gonads and a set of two
accessory structures (at least in Neodasys and Macrodasy-
ida), one of which, the frontal organ, serves as a “female”
bursa and sperm-storing device, and the other, the caudal
organ, serves as a “male” penis structure (Figs. 1.31 and 1.36
E). This fundamental function of both these structures, at
least for the genera Urodasys and Macrodasys, was for the
first time correctly interpreted by Schoepfer-Sterrer (1974).
Many species additionally possess further structures like
certain ducts (e.g., vasa deferentia), glandular tissues like
the so-called rosette organ, or the caudal gland cells that
can be found in different species of the marine taxon Thau-
mastodermatidae. Within the Paucitubulatina exclusive
of Xenotrichulidae and Muselliferidae, the reproductive
system is arranged differently, certainly correlated with a
different reproductive biology. Until the first half of the 20st
century, only few fresh or brackish water Paucitubulatina
were known to develop spermatozoa beside the eggs (e.g.,
Chaetonotus hermaphroditus), so that it was a common
thought that the freshwater inhabiting Paucitubulatina was
a group of almost exclusively parthenogenetic organisms
(e.g., Remane 1936). However, in the second half of that
century more and more reports of freshwater species pro-
ducing hermaphroditic specimens accumulated and deve-
lopment of spermatozoa in Lepidodermella squamata was
studied intensely at the cytological level (Hummon 1984a).
Weiss (2001) demonstrated in a comprehensive study the
occurrence of such sperm-bearing individuals in selected
species of the majority of freshwater-inhabiting genera of
the Gastrotricha-Paucitubulatina. Hence, it was concluded
that an assumed life cycle of parthenogenetic reproduction
followed by the development of hermaphroditic individu-
als that possibly engage in cross fertilization is widespread
among the freshwater taxa (Weiss 2001).
The morphology of the reproductive organs (male and
female gonads, accessory structures such as the frontal and
caudal organs, outlet ducts, gland tissues) were studied
in quite a lot species of Gastrotricha at the ultrastructural
level (e.g., Ruppert & Shaw 1977, Ruppert 1978a, b, 1991,
Hummon 1984a–c, Kieneke etal. 2008d, 2009, Guidi etal.
2011, Todaro etal. 2012a, Guidi et al. 2014). The study of
reproductive anatomy based on conventional light micro-
scopy can also provide detailed results (e.g., Ferraguti &
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46 1Gastrotricha
The study of Dactylopodola typhle revealed a reproduc-
tive system generally comparable to that of other species
of the Macrodasyida (Kieneke et al. 2008d). However,
there are considerable differences as well. Beside the
paired male and female gonads (ovaries mature frontally
and fuse to form a common uterus region), there is only
one voluminous accessory sex organ, the caudal organ,
that is a secretory structure with a complicated branched
lumen. Furthermore, there is a cellular duct, the cervix,
which communicates with the uterus lumen and possibly
has a dual function for (1) the uptake of the foreign sper-
matophore and (2) for oviposition. The cervix opens dor-
solaterally in a single pore that is lined by a rosette of sec-
retory epithelial cells (Fig. 1.32 B). Early oocytes are lined
by ECM only but there is an epithelial wall at the uterus
region continued by the epithelium of the cervix. The wall
of the paired testes is made up of parts of the early germ
cells (spermatogonia or spermatocytes) and therefore
Balsamo 1994, Fregni etal. 1999, Balsamo etal. 2002),
but in many cases, especially when regarding the acces-
sory organs, findings are ambiguous. Furthermore, light
optic observations do rarely provide information on, for
instance, lining epithelia, extracellular material, or incon-
spicuous genital pores. Comprehensive ultrastructural
data of the reproductive organs in putative basal species
were missing for a long time. We here briefly review the
reproductive morphology of two putative basal taxa, Dac-
tylopodola typhle and Neodasys chaetonotoideus (Kieneke
etal. 2008d, Kieneke etal. 2009) because they have been
very important for the purpose of reconstructing the cha-
racter pattern of the common ancestor of Gastrotricha (see
Kieneke etal. 2009). These ground pattern features of the
reproductive system of Gastrotricha are later presented
followed by descriptions of the reproductive organs in
further taxa that will highlight some major evolutionary
changes.
Fig. 1.31: Reproductive system (schematic)
of the last common ancestor of
Gastrotricha. (A) Reproductive anatomy,
dorsal view. (B–E) Trunk cross sections at
different levels (indicated by bold lines in
A). Abbreviations: ao, adhesive organ; co,
caudal organ; cop, caudal organ pore; cu,
cuticle; ep, epidermis; fo, frontal organ; fop,
frontal organ pore; hm, helicoidal muscle;
ip, internal pore of the frontal organ; lc,
locomotor cilia; lm, longitudinal muscle
block; lnb, longitudinal neurite bundle;
mg, midgut; mo, mature egg; mp, male
genital pore; ms, muscular sheath; mt,
mesodermal tissue; ov, ovary; ph, pharynx;
pn, protonephridium; sp, spermatozoa; te,
testis; ut, uterus.
50 µm
100 µm
A
B
C
D
te
ph
in
ov
ut
pn
co
fo
sp
pn
mo
mg
mg
te
mp
co
te
ov
mg
ut
fop
cop
ip
E
cop
ms
fop
fo
ao
lm
sp
pn
ep
cu
lnb lnb
lc
ao
ao
lm
mt
hm
ms
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1.2Morphology 47
represents a germinal epithelium. On the basis of the mor-
phological reconstruction, a hypothesis for mating and
spermatophore transfer in D. typhle has been proposed
that suggests a reciprocally transfer of the spermatophore
from the central lumen of the glandular caudal organ into
the uterus lumen of the mating partner via the cervix.
According to that hypothesis, the trunk musculature pro-
vides the pressure for draining the caudal organ because
it lacks in an own muscular sheath (Kieneke etal. 2008d).
For Neodasys chaetonotoideus, the gross anatomy of
the reproductive system already given by Remane (1936)
and for Neodasys sp. by Ruppert (1991) could generally be
confirmed by Kieneke etal. (2009). However, many histolo-
gical and ultrastructural data now complement our know-
ledge of the reproductive system of this crucial and proba-
bly most basal gastrotrich taxon (Hochberg 2005, Kieneke
etal. 2008a, see also chapter Phylogeny). In general, the
reproductive system of N. chaetonotoideus consists, like
in many macrodasyidan species, of paired lateral testes,
an unpaired dorsal and caudally maturing ovary and a
set of two accessory reproductive organs, the frontal and
caudal organ (Figs. 1.32 A, 1.36 E, and 1.37 A). However,
both accessory reproductive structures of N. chaetono-
toideus form a common organ (the frontocaudal organ;
Fig. 1.37 B) in immature, not inseminated specimens (but
with clearly separated lumina), whereas both compo-
nents seem to be more separated but still in close con-
junction in mature and inseminated animals (Fig. 1.37 D).
Such a close association or even cellular continuity of
the frontal and caudal organs was already highlighted
by Ruppert & Shaw (1977) and Ruppert (1978b) for the
taxa Dolichodasys and parts of the Thaumastodermatidae
(see Figs. 1.34 B and 1.35 C). The testicular wall is, as in
D. typhle and other gastrotrich species, a germinal epithe-
lium, whereas distinct sperm ducts are lacking in N. chae-
tonotoideus. The testes are probably discharged via simple
ventral pores. The ovary region is not provided with a wall
epithelium. Instead, mesodermal cushion cells, possibly
Y-cells, adjoin the early oocytes. More distally, there is a
special oviduct epithelium that is obviously engaged in
yolk production: The passing egg inside this vitellogenic
oviduct endocytes yolk material that is provided by exocy-
tosis of the oviduct cells (Kieneke etal. 2009). Distally, the
vitellogenic oviduct is continued by the uterus wall (Fig.
1.32 A). The mature egg inside the uterus undergoes further
vitellogenesis by auto synthesis. The uterus lumen directly
passes to the lumen of the frontal organ (dorsofrontal
lumen of the frontocaudal organ) by a narrow internal
pore. In inseminated individuals, a foreign spermatophore
is stored in that part of the frontocaudal organ (Fig. 1.37 D).
Hence, fertilization via the internal pore is warranted. The
frontal organ possesses a laterally directed external pore
for which a dual function is suggested, (1) the uptake of
foreign spermatophores and (2) the release of the fully
matured and fertilized eggs. The caudal organ of N. chaeto-
notoideus is hypothesized to engage in external formation
of the spermatophore by providing secretions that are pro-
bably released through an external pore. There is some evi-
dence that mature specimens of N. chaetonotoideus carry
their own spermatophores attached to the caudal adhesive
organs (the caudal “feet”) for a while before sticking it to a
mating partner (Kieneke etal. 2009).
Morphological data of the most satisfyingly inves-
tigated gastrotrich species, most of which studied using
a multitude of techniques (in vivo light microscopy, his-
tology, TEM, SEM), have been used to reconstruct the
character pattern of the reproductive system of the stem
species of Gastrotricha (see Kieneke etal. 2009: Table 1).
To make this inference, three phylogenetic hypotheses on
the internal relationships of Gastrotricha (Hochberg & Lit-
vaitis 2000, Todaro etal. 2006a, Kieneke etal. 2008a; see
also chapter Phylogeny) served as the basis for a parsimo-
nious character optimization. Hence, the three resulting
ground pattern hypotheses varied in some character states
due to topological differences between the three phyloge-
netic hypotheses. To obtain consistent information of the
reproductive system of the stem species of Gastrotricha,
a consensus of all three ground pattern hypotheses has
been formed (Kieneke etal. 2009). Based on this proce-
dure, the reproductive system of the common ancestor of
Gastrotricha was probably composed of the components
listed in the following. It has to be stressed that the most
recent studies on the anatomy and ultrastructure of the
reproductive tract of Crasiella diplura (Guidi etal. 2011),
Dinodasys mirabilis (Todaro etal. 2012a), and Megadasys
sterreri (Guidi etal. 2014) were not considered at that time.
The stem species was a hermaphroditic organism
with a female gonad that is separated into a proximal
ovary region and a distal uterus region that carries one
or few mature oocytes and is situated dorsally above the
intestine (Fig. 1.31 A, C). Based on the outgroup compari-
son, the oocytes much likely matured frontocaudally (see
discussion on this issue in Kieneke etal. 2009). The early
oocytes at the ovary region were not covered with a cellu-
lar wall (Fig. 1.31 A, D). Instead, they were surrounded by
a thin layer of extracellular material separating them from
other adjacent tissues. However, the mature oocyte(s) at
the uterus region was/were completely surrounded by a
flattened uterus wall epithelium (Fig. 1.31 A, C). It is equi-
vocal if the stem species of Gastrotricha had a paired or
an unpaired female gonad; the situation in putative sister
taxa of gastrotrichs such as the Cycloneuralia, Gnathi-
fera, or the Plathelminthes is ambiguous (see discussion
in Kieneke et al. 2009). Furthermore, the stem species
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48 1Gastrotricha
A cellular (epithelial) frontal organ with a simple lumen
opened to the exterior via a lateral to ventral pore (Fig.
1.31 A, D). The frontal organ was situated caudal to the
uterus region with the mature oocyte(s). There was a
subepithelial ECM surrounding the frontal organ but no
specialized musculature. Secretion vesicles were present
inside the frontal organ wall epithelium that was pro-
bably continuous with the uterus wall epithelium. The
frontal organ contained an internal pore that is directed
frontally toward the mature oocyte. Foreign sperma-
tozoa or allosperms were kept inside the frontal organ
lumen, and fertilization was enabled through the internal
pore (Fig. 1.31 A). The stem species of Gastrotricha also
possessed a cellular caudal organ provided with a simple,
not compartmentalized lumen that opened to the exte-
rior via a ventral pore (Fig. 1.31 A, E). Luminal microvilli
and secretory vesicles inside the caudal organ wall cells
had one pair of long and tube-shaped testes in a lateral
body position alongside the intestine (Figs. 1.31 A–C
and 1.36 B). The testicular wall consisted of early germ cell
stages thus forming a germinal epithelium (Fig. 1.31 B, C).
There were no distinct seminal ducts but the testicular
lumen probably opened directly to the exterior via a pair
of simple ventral pores. The general mode of spermatoge-
nesis was not considered in the reconstruction of the ance-
stral character pattern. However, in most species of the
Macrodasyida studied so far, development of spermatozoa
via spermatogonia, spermatocytes, and spermatids pro-
ceeds from the periphery of the testes toward the central
lumen (centripetal), and from posterior to anterior (see
Guidi etal. 2011 and studies referenced therein, see also
chapter Spermatogenesis and Spermiogenesis). We there-
fore assume that the last common ancestor of Gastrotricha
also showed this general modality of spermatogenesis.
50 µm
50 µm
100 µm
100 µm
A
B
C
D
te
ph
in
ov
ut
vo
xo
co
fo
spp
ce
fp (ro)
sd
ph
te
xo
mo
in
ph
in
ov
te
mp
co
te
ov
ov
mp
in
ut
spp
ph
fop
cop
ip
Fig. 1.32: Reproductive system (schematic)
of different taxa of Gastrotricha.
(A) Neodasys chaetonotoideus
(Multitubulatina). (B) Dactylopodola typhle
(Macrodasyida, Dactylopodolidae).
(C) Lepidodermella squamata
(Paucitubulatina, Chaetonotidae).
(D) Xenotrichula intermedia
(Paucitubulatina, Xenotrichulidae).
Abbreviations: ce, cervix; co, caudal organ;
cop, caudal organ pore; fo, frontal organ;
fop, frontal organ pore; fp, female genital
pore; in, intestine; ip, internal pore of
the frontal organ; mo, mature egg; mp,
male genital pore; ov, ovary; ph, pharynx;
ro, rosette organ; sd, sperm duct; spp,
spermatophore; te, testis; ut, uterus; vo,
vitellogenic oviduct; xo, x-organ.
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1.2Morphology 49
were present. The caudal organ was provided with a thick
subepithelial ECM and a sheath of subepithelial circular
and longitudinal muscles (Fig. 1.31 E). This organ served
for processing the own spermatozoa (autosperms) and
for transferring them to the mating partner by means of
muscle action. A connection of the frontal and caudal
organ was present. The exact structure and shape of this
connection, however, could not be reconstructed. There
was possibly just a compact column of cubic cells like
in Dolichodasys carolinensis (Ruppert & Shaw 1977, see
Fig. 1.34 B) that may represent a remnant of a common
ontogenetic anlage of both accessory reproductive organs.
A direct connection of both accessory organs with com-
municating lumina as it is present in different species of
the derived taxon Thaumastodermatidae (Ruppert 1978b,
see Fig. 1.35 C) obviously reflects the derived condition.
Comparing the aforementioned ground pattern features
with the reproductive system of Macrodasys sp., a species
of which the reproductive morphology (see Fig. 1.33 C) as
well as the whole mating process and mode of spermatozoa
transfer is well-known (Ruppert 1978a, see chapter Repro-
ductive Biology), one can assume that the stem species of
Gastrotricha might have engaged in a comparable mode of
mating: the own spermatozoa are released through the testi-
cular pores and then transported externally into the caudal
organ lumen where they are provided with certain substan-
ces such as mucus or nutrients. Two reproductive partners
meet and curl around each other, thus bringing the caudal
organ pore of one specimen in contact with the frontal
organ pore of the second specimen and vice versa. Owing
to muscular contraction of the caudal organ, spermatozoa
are pressed into the frontal organ lumen of the other spe-
cimen, respectively. Given the anatomic conditions recon-
structed for the stem species of Gastrotricha, a release of
the fertilized eggs through the frontal organ pores (first:
passage from the uterus to the frontal organ via the internal
pore; second, release of the egg via the external pore of the
frontal organ) rather than body wall rupture for oviposition
is possible (see discussion in Kieneke etal. 2009). Such a
multirole functioning of the accessory reproductive organs
was already suggested by Remane (1936). However, there
are indeed observations of a body wall rupture during egg
deposition in some species, too (Teuchert 1968, see chapter
Reproductive Biology; Fig. 1.50 A).
Several variations from the character pattern of the
stem species can be observed in present-day species and
will be reviewed in the following. Most of these can be
interpreted as evolutionary transformations of certain
internal lineages of the Gastrotricha. However, there still
is little knowledge of the anatomy and ultrastructure
of these tiny animals, which results in an incomplete
understanding of the structure, the function and
evolution of their reproductive system.
1.2.9.1Female gonad
Oocytes in the reconstructed ancestral ovary mature in
an anteroposterior direction, a mode that can be found
in genera such as Dolichodasys and Neodasys (Ruppert &
Shaw 1977, Kieneke etal. 2009, see Figs. 1.32 A and 1.34 B)
or in the species Urodasys viviparus, the only viviparous
species known so far (see Wilke 1954, Schoepfer-Sterrer
1974; Fig. 1.50 B). In contrast, most other extant gastro-
trichs show the opposite pattern. In taxa like, just to give
some examples, Macrodasyidae exclusive of Urodasys
viviparus (Fig. 1.33 C), Turbanellidae, Dactylopodolidae,
Thaumastodermatidae, and Gastrotricha-Paucitubula-
tina, the eggs mature from posterior to anterior (see Figs.
1.32 C, D, 1.33 A–C, 1.34 A, C, and 1.35 A–C). Flattened epi-
thelial linings of the entire female gonad (early oocytes
plus uterus region) are described in different species
that have been studied by means of TEM, e.g., Macroda-
sys sp. 1 and 2 (Ruppert 1978a, see Fig. 1.33 C), Oregoda-
sys (=former Platydasys) cf. ocellatus, Thaumastoderma
heideri, Acanthodasys sp., and Diplodasys ankeli (Ruppert
1978b, see Fig. 1.35 A, B). In other species studied by TEM,
such thin wall epithelia have been detected in the uterus
region lining the mature egg(s). Meanwhile, they could
not be found in the ovary region (e.g., Tetranchyroderma
bunti: Ruppert 1978b, see Fig. 1.35 C, Dactylopodola typhle:
Kieneke etal. 2008d, see Fig. 1.32 B, Neodasys chaetonoto-
ideus: Kieneke etal. 2009, see Figs. 1.32 A and 1.37 A, C) or
were proved to be absent at all (e.g., Paraturbanella teissi-
eri: Balsamo etal. 2002, see Fig. 1.34 A, Crasiella diplura:
Guidi et al. 2011, see Fig. 1.33 A, Dinodasys mirabilis:
Todaro etal. 2012a). In the latter two cases, the germ cells
themselves constitute the gonad wall of the ovaries, i.e.,
they represent a germinal epithelium (see Todaro et al.
in 2012a), as it is the case in the testes of most Gastrotri-
cha (see below). In Turbanella cornuta, however, there is
an incomplete cellular wall of the ovary region (Teuchert
1977a). It was reconstructed unambiguously that a uterus
wall epithelium was present in the stem species of Gast-
rotricha (Kieneke etal. 2009). Although present in many
investigated gastrotrich species (see above), an epithe-
lium enclosing the entire female gonad (ovary plus uterus
region) is unlikely for the common ancestor of Gastrotri-
cha since putative basal taxa such as Neodasys and Dac-
tylopodola lack a cellular envelope of the ovaries. It is a
scenario worth considering that a uterine wall was initi-
ally developed as an extension from the wall epithelium
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50 1Gastrotricha
Fig. 1.33: Reproductive system (schematic)
of different taxa of Gastrotricha.
(A) Crasiella diplura (Macrodasyida,
Planodasyidae). (B) Mesodasys
laticaudatus (Macrodasyida,
Cephalodasyidae). (C) Macrodasys
sp. (Macrodasyida, Macrodasyidae).
Abbreviations: an, antrum feminimum;
co, caudal organ; cop, caudal organ pore;
fo, frontal organ; fop, frontal organ pore
(external); in, intestine; ip, internal pore
of the frontal organ; mo, mature egg; mp,
male genital pore; ms, muscular sheath;
ov, ovary; ph, pharynx; sd, sperm duct; sp,
spermatozoa; te, testis; ut, uterus.
50 µm
100 µm
300 µm
A
B
C
te
ph
ov
mo
co
fo
sp
sd
ph
mp
in
ph
in
ov
te
mp
co
ov
in
ut
cop
sd
te
cop
mo
mo
fop co
cop
an
ms
sd
sp
fop
fo
ip
ip
ms
1.33 A, also probable in Megadasys: Schmidt 1974, Guidi et
al. 2014). However, they project caudally and then sharply
bend frontally in species of the taxon Turbanellidae (e.g.,
Turbanella cornuta: Teuchert 1976b, Paraturbanella teissi-
eri: Balsamo etal. 2002, see Fig. 1.34 A, Dinodasys mira-
bilis: Todaro etal. 2012a). This character is hypothesized
to be an important autapomorphy of that family (Todaro
et al. 2012a). Also, the paucitubulatinan group Xenotri-
chulidae has sperm ducts that run frontally (e.g., Ruppert
1979, see Fig. 1.32 D). In both taxa, the paired sperm
ducts fuse and open into a common unpaired midventral
gonopore. As Xenotrichulidae and Turbanellidae are
not close relatives, the anteriorly projecting and fusing
sperm ducts must have been developed twice inde-
pendently in both groups. In Thaumastodermatinae
(a subfamily of Thaumastodermatidae, e.g., Tetranchy-
roderma bunti, Thaumastoderma heideri, Oregodasys cf.
of the frontal organ. Later in evolution, this wall may have
extended to line the whole female gonad.
1.2.9.2Male gonad
Although reconstructed to be absent in the last common
ancestor (this again depends on the condition in the basal
taxa Neodasys and Dactylopodola), most contemporary her-
maphroditic gastrotrich species possess distinct seminal
ducts (vasa deferentia). These are directed caudally where
they open into two ventral male gonopores (e.g., in Macro-
dasys sp.: Ruppert 1978a, see Fig. 1.33 C, Dolichodasys caro-
linensis: Ruppert & Shaw 1977, see Fig. 1.24 B, also probable
in Chordodasiopsis antennatus: Rieger etal. 1974) or in a
common unpaired midventral gonopore (e.g., in Crasiella:
Schmidt 1974, Guidi etal. 2011, Lee & Chang 2012, see Fig.
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1.2Morphology 51
the proximal end of the cervix, respectively (Figs. 1.32 B
and 1.35 A, B). The latter structure is an epithelial duct
putatively serving for egg deposition and picking up the
allosperms via a dorsolateral pore (called the “rosette
organ” in Acanthodasys thrinax and Diplodasys ankeli,
see Ruppert 1978b). The duo-functional cervix, possibly a
continuation of the uterus wall epithelium, is so far only
described for Dactylopodola typhle (Kieneke etal. 2008d)
but is interpreted to be present in even more species (see
Kieneke etal. 2009).
Like the common ancestor of Gastrotricha, most
species of Macrodasyida and Neodasys possess a caudal
organ as a copulatory structure (or as a device included in
spermatophore formation) that has to be charged with the
own sperms prior to copulation. As the male gonopores in
many species lie apart from the pore of the caudal organ,
spermatozoa have to be transported to the lumen of the
caudal organ externally. This procedure has been studied
in detail in two species of Macrodasys (Ruppert 1978a, see
chapter Reproductive Biology). In taxa such as Mesoda-
sys, Diplodasys, or Acanthodasys, which possess a direct
connection of the sperm ducts to the caudal organ (see
above), a complicated external transport of spermatozoa
is avoided. In Turbanellidae, a real caudal organ is pro-
bably lacking (see, e.g., Fig. 1.34 A). Observations of the
mating behavior of Turbanella cornuta suggest that these
organisms transfer their spermatozoa to a putative frontal
organ of the mating partner directly from the unpaired
ventral pore of the fused sperm ducts (Teuchert 1968),
which makes a caudal organ for sperm transfer redundant
(but see for further interpretations of sperm transfer in
T. cornuta in the chapter Reproductive Biology). Such kind
of sperm transfer modalities presumably represent the
general mode in Turbanellidae, whereas structures pre-
viously mistaken for caudal organs in different species
of that family apparently have a different function, not
necessarily related to the reproductive system (Balsamo
etal. 2002). However, the recently investigated turbanel-
lid Dinodasys mirabilis possesses a huge glandular and
hollow structure, the posterior gland organ, at a compara-
ble position like the caudal organ in many other Macroda-
syida. However, the authors suggest that this gland organ
of D. mirabilis is not homologous to the “true” copulatory
caudal organ of many other taxa (Todaro etal. 2012a).
Until now, we have just reported about the presence
or absence and the general role of the accessory repro-
ductive organs in Gastrotricha. It has to be stressed that
the accessory reproductive organs, especially the caudal
organ, belong to the most complex structures in gastro-
trichs and show a high morphological diversity among
the different taxa (Hummon & Hummon 1988, Balsamo
etal. 1999). Although the frontal organ in many cases is
ocellatus: Ruppert 1978b), the seminal duct of the single
testis distally forms a glandular section and opens into a
ventral pore close to the opening of the caudal organ (Fig.
1.35 C). External ventral male gonopores are hence wide-
spread among Gastrotricha and represent the ancestral
condition. They are not always permanent and well-diffe-
rentiated openings but rather preformed areas in the body
wall that become pores when the testes are fully matured and
sperm release is immediately imminent. Such conditions
have been reported, e.g., for Dolichodasys carolinensis
(Ruppert & Shaw 1977) or Dinodasys mirabilis (Todaro etal.
in 2012a), and are also probable in species such as Neo-
dasys chaetonotoideus and Dactylopodola typhle (Kieneke
etal. 2008d, 2009). Within species of the taxon Diploda-
syinae (the other subfamily of Thaumastodermatidae,
e.g., Acanthodasys thrinax and Diplodasys ankeli: Ruppert
1978b) and in Mesodasys (e.g., Mesodasys laticaudatus:
Ferraguti & Balsamo 1994, M. adenotubulatus: Fregni etal.
1999), the seminal ducts directly discharge into the caudal
organ (Figs. 1.33 B and 1.35 A, B). Hence, the male “gonopo-
res” in these taxa are situated within the wall epithelium of
this accessory structure. The functional male gonopore in
these species, however, is the unpaired external opening of
the caudal organ. As already mentioned, one can observe a
further evolutionary transformation related with the male
gonads in species of the subfamily Thaumastodermati-
nae: they possess a well-developed right testis, whereas
the left one is completely absent (Ruppert 1978b, see Figs.
1.35 C and 1.36 C). A convergent situation was evolved in
another group: in different species of the genus Urodasys
(Macrodasyidae), the right testis is reduced or even fully
lost, whereas the left one is well developed (see Schoepfer-
Sterrer 1974). Although a bounding testicular germinal
epithelium is reported from most species studied at the
ultrastructural level, there may also be species were the
male germ cells are only partly enclosed, e.g., by lateral
somatic circular muscles such as in Chordodasiopsis
antennatus (Rieger etal. 1974).
1.2.9.3Frontal and caudal organ
Whereas a sac-shaped, hollow frontal organ serving as a
seminal receptacle for storing spermatozoa received from
the mating partner unambiguously is a component of the
reproductive system of the common ancestor, this struc-
ture is not present in some gastrotrich species such as
Acanthodasys thrinax, Diplodasys ankeli (Ruppert 1978b,
see Fig. 1.35 A, B) or Dactylopodola typhle (Kieneke etal.
2008d, see Fig. 1.32 B). In those species, another structure
takes the role of storing the foreign sperms: the frontal
sac that is a pouch-like differentiation of the uterus or of
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52 1Gastrotricha
a rounded to pear-shaped hollow epithelial pouch (e.g.,
in species of Urodasys: Schoepfer-Sterrer 1974, Dolichoda-
sys carolinensis: Ruppert & Shaw 1977, see Fig. 1.34 B,
species of Thaumastodermatinae: Ruppert 1978b, see
Fig. 1.35 C, species of Turbanellidae: Todaro etal. 2012a
and references therein, see Fig. 1.34 A), it can also be a
rather tube-shaped structure like in Chordodasiopsis anten-
natus (Rieger etal. 1974). Species of the genus Macrodasys
show a high degree of interspecific structural variability of
their frontal organs as well as a complex compartmentali-
zation of this accessory sex organ into a seminal receptacle
and a spermatheca (see, e.g., Ruppert 1978a, Evans 1994,
Fig. 1.33 C). Further variation of this organ can be found in
the position of the external pore: while the pore is situated
on the ventral body surface in many taxa (e.g., Dolichoda-
sys carolinensis: Ruppert & Shaw 1977, species of Macroda-
sys: e.g., Ruppert 1978a, Evans 1994, species of Urodasys:
Schoepfer-Sterrer 1974), it opens dorsally to dorsolaterally
in some species of Urodasys (Schoepfer-Sterrer 1974) and
in Turbanellidae (e.g., Balsamo etal. 2002, Todaro etal.
2012a) or even laterally as in species of Neodasys (Ruppert
1991, Kieneke etal. 2 009, see Fig. 1.32 A). In some species of
Macrodasys and Urodasys, the internal pore of the frontal
organ is provided with cuticularized hard parts, structures
that are interpreted to have a valve-like function to release
the sperms from the frontal organ lumen to the matured
eggs one by one (Schoepfer-Sterrer 1974).
The caudal organ lumen can be differentiated as a
narrow, branched or non-branched duct (e.g., in Macro-
dasys sp. 1 and 2: Ruppert 1978a, see Fig. 1.33 C), a highly
branched lumen (e.g., Dactylopodola typhle: Kieneke etal.
2008d, see Fig. 1.32 B), or a simple spheric chamber (e.g.,
species of Thaumastodermatidae, Crasiella, and Mesoda-
sys: Ruppert 1978b, Ferraguti & Balsamo 1994, Fregni etal.
Fig. 1.34: Reproductive system
(schematic) of different taxa of
Gastrotricha. (A) Paraturbanella teissieri
(Macrodasyida, Turbanellidae). (B)
Dolichodasys carolinensis (Macrodasyida,
Cephalodasyidae), posterior part of
the trunk. (C) Redudasys fornerise
(Macrodasyida, Redudasyidae).
Abbreviations: co, caudal organ; cop, caudal
organ pore; fo, frontal organ; fop, frontal
organ pore (external); gt, glandular tissue;
hg, hermaphroditic gonad; in, intestine;
ip, internal pore of the frontal organ; mo,
mature egg; mp, male genital pore; ms,
muscular sheath; ov, ovary; ph, pharynx;
sd, sperm duct; sp, spermatozoa; tc, tissue
connection; te, testis; ut, uterus.
50 µm
100 µm
100 µm
A
B
C
te
ph
ov
mo
gt
fo sp
sd mp
in
ph
in
ov
mp
co
ov
in
cop
te
mo
mo
fop
ms
fop
fo
ip
hg
sp
tc
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1.2Morphology 53
Fig. 1.35: Reproductive system
(schematic) of different taxa of
Gastrotricha. (A) Diplodasys ankeli
(Macrodasyida, Thaumastodermatidae,
Diplodasyinae). (B) Acanthodasys sp.
(Macrodasyida, Thaumastodermatidae,
Diplodasyinae). Posterior part of the
trunk. (C) Tetranchyroderma bunti
(Macrodasyida, Thaumastodermatidae,
Thaumastodermatinae). Abbreviations: ce,
cervix; co, caudal organ; cop, caudal organ
pore; fo, frontal organ; fop, frontal organ
pore (external), female genital pore; fs,
frontal sac; gt, glandular tissue; in, intestine;
ip, internal pore of the frontal organ/frontal
sac; mo, mature egg; mp, male genital pore;
ms, muscular sheath; ov, ovary; ph, pharynx;
ro, rosette organ; sd, sperm duct;
sp, spermatozoa; te, testis; ut, uterus.
100 µm
100 µm
100 µm
A
B
C
te
ph
ov
mo
gt
fs
sp
sd
in
ph
in
ov
mp
co
ov
in
cop
te
mo
mo
ms
ip
sp
fs
ce
ce
sd
ro
fp
co
co
cop
cop
fo
fp?
ms
ms
gt
te
sd
ip
ip
ro
fp
ce
1999, Guidi etal. 2011, see Figs. 1.33 A, B and 1.35 A–C).
In species of Macrodasys, the caudal organ is further
compartmentalized into a glandulomuscular portion and
an antrum feminimum (Ruppert 1978a, Evans 1994, see
Fig. 1.33 C). There are species whose caudal organ contains
protrudable copulatory tubes with cuticularized teeth-like
structures (e.g., Macrodasys sp. 1 and 2: Ruppert 1978a),
contractible filaments (e.g., Dolichodasys carolinensis and
D. delicatus: Ruppert & Shaw 1977, see Fig. 1.34 B), or even
cuticularized stylets or canals (several species of Uroda-
sys: Schoepfer-Sterrer 1974, Oregodasys styliferus: Boaden
1965, Tetranchyroderma bronchostylus: Atherton & Hoch-
berg 2012) (Fig. 1.36 G, H). From an evolutionary point of
view, such structures and modifications surely improved
the exchange of spermatozoa by means of internal inse-
mination whereas the exact function is hardly known
in most cases. In Urodasys spirostylis for instance, the
striking resemblance of the corkscrew-shaped stylet with
the vagina mouthpiece, the strongly cuticularized exter-
nal opening of the frontal organ, suggests that the frontal
and caudal organs represent a key-lock system (Schoepfer-
Sterrer 1974). Another strategy for efficient sperm transfer
is the formation and exchange of spermatophores. This
is reported at least for some species of the genus Dacty-
lopodola (Teuchert 1968, Kieneke etal. 2008d) and for
Neodasys sp./N. chaetonotoideus (Ruppert 1991, Kieneke
etal. 2009). It is hypothesized that the frontal organ or the
caudal organ of those species are involved in the produc-
tion of the spermatophore (Ruppert 1991, Kieneke etal.
2008d, 2009, see also chapter Reproductive Biology).
As already mentioned there are different possible
types of connectivity of both accessory reproductive
organs (frontal and caudal organ completely apart, simple
tissue connection, directly communicating lumina). The
situation in Thaumastodermatinae is of special interest
because the directly connected and communicating acces-
sory organs represent a challenging anatomic condition.
Ruppert’s (1978b) explanation is a duo-role function (male
and female) of the caudal organ in Thaumastodermatinae.
His hypothesis is that the part of the caudal organ con-
nected with the vas deferens is still male in function but
the portion that communicates with the frontal organ has
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54 1Gastrotricha
50 µm
50 µm
100 µm
50 µm
50 µm
50 µm
50 µm
25 µm
A
BC
DF
mo
sph
*
G
mo
H
mg
*
E
*
mg
nu
spf
*
*
mg
mo
fo
co co
fo
sp
ip
mg
co
fo
sp
co
Fig. 1.36: Reproductive system of Gastrotricha. (A) Xenotrichula intermedia (Paucitubulatina) with a mature egg. Note the size ratio
between gamete and organism. (B) Xenodasys riedli (Macrodasyida) with paired testes. Note the spiraled sperm heads (asterisks).
(C) Tetranchyroderma sp. (Macrodasyida) in ventral view with a single right testis (asterisk). (D) Middle portion of Oregodasys
cf. phacellatus (Macrodasyida) with mature egg and single testis. (E) Posterior trunk portion (horizontal view) of Macrodasys sp.
(Macrodasyida) with testes (asterisks), ovary and accessory reproductive organs. (F) Close-up of the accessory reproductive organs of
Macrodasys sp. Note the cuticularized internal pore of the frontal organ and the foreign spermatozoa within its lumen. (G) Frontal and
caudal organ of Urodasys spirostylis (Macrodasyida). (H) Close-up of the spiraled stylet inside the caudal organ of U. spirostylis. (A) BF
image and (B–H) DIC images. Abbreviations: co, caudal organ; fo, frontal organ; ip, internal pore of the frontal organ; mg, midgut;
mo, mature egg; nu, nucleus; sp, spermatozoa; spf, flagella of spermatozoa; sph, spiraled heads of spermatozoa.
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1.2Morphology 55
10 µm
3 µm
2 µm
10 µm
10 µm
10 µm
1 µm
A B
C
D
*
*
E
G
*
tes
F
mg
tes
ov mg
fo
co
mo
nu
fo
fo
mo
tes
co
lm
*
*
ed
sp
Fig. 1.37: Ultrastructure (TEM micrographs) of the reproductive system of Gastrotricha. (A–D) Neodasys chaetonotoideus (Multitubulatina).
(A) Cross section showing paired lateral testes and unpaired dorsal ovary. (B) Cross section through the frontocaudal organ. Note the lumen
of the frontal organ (asterisk). (C) Median section showing a mature oocyte within the uterus region. (D) More sagittal section showing a
testis with developing spermatozoa, the frontal organ, and the caudal organ. Note the spermatophore inside the frontal organ (asterisk).
(E and F) Cross sections of Dactylopodola typhle (Macrodasyida). (E) Right testis with spermatogonia or spermatids in the dorsal part
(asterisks) and maturing sperm cells below. (F) Synaptonemal complexes within the testicular germ cells of D. typhle are indicative for
meiosis. (G) Cross section through 1 testis of Xenotrichula carolinensis (Paucitubulatina). Spermatozoa inside the lumen are sectioned
at different regions (nuclear, mitochondrial, flagellar). Abbreviations: co, caudal organ; ed, epidermis; fo, frontal organ; lm, longitudinal
muscles; mg, midgut; mo, mature egg; nu, nucleus of the mature egg; ov, ovary; sp, sperm cells; tes, testis.
been modified to a female accessory structure (see also
discussion of Atherton & Hochberg 2012). In this regard,
another functional scenario is quite interesting: the distal
part of the vas deferens (glandular and/or provided with
a muscular sheath) in Thaumastodermatinae evolved as a
new structure. The caudal organ is still male in function
(uptake and transfer of spermatozoa), the frontal organ still
female (receive and storage of spermatozoa). According
to this scenario, the direct connection of both accessory
organs would imply that species of Thaumastodermatinae
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56 1Gastrotricha
parthenogenetic populations with later occurring herma-
phroditic animals is proposed for all Paucitubulatina exclu-
sive of the ancestrally marine taxa Xenotrichulidae and
Muselliferidae (see chapter Reproductive Biology). It has to
be mentioned that sperm-bearing freshwater gastrotrichs
as well as fully mature individuals of the Xenotrichulidae
exhibit an accessory structure referred to as the x-body or
x-organ (Fig. 1.32 C, D). This secretory structure derives
from undifferentiated female germ cells (as demonstrated
in Lepidodermella squamata: Hummon 1984c) and appears
in the region of the hind gut. It is regarded to play a role
in sexual reproduction and was interpreted as a copulatory
organ, a bursal organ, an oviduct, or a vitellarium repea-
tedly. However, all these hypotheses have never been confir-
med (see discussion in Weiss 2001 and references therein).
According to Hummon (1986), the cells of the developing
x-body in L. squamata also contribute to the vitellogenesis
of the postparthenogenic egg.
1.2.9.5Additional accessory structures
Glandular tissues comparable to the above mentioned pau-
citubulatinan x-organ are known from several species of the
Macrodasyida, too. Here, they are associated with the distal
parts of the seminal ducts (Figs. 1.34 A and 1.35 A, C) and/or
with the pore of the caudal organ (Fig. 1.35 C) and lie in close
proximity to the hindgut and anus (e.g., species of Uroda-
sys: Schoepfer-Sterrer 1974, Tetranchyroderma bunti, Thau-
mastoderma heideri, Diplodasys ankeli: Ruppert 1978b).
Comparable structures may be present in species that lack
a caudal organ altogether such as in Paraturbanella teissi-
eri and other species of the Turbanellidae (Balsamo etal.
2002). In these cases, the glandular organ is also associated
with the hindgut (Fig. 1.34 A). However, homology of the
described structures with the x-organ of Paucitubulatina
is improbable. Furthermore, there is no convincing hypo-
thesis on the functional role of those “glands”, neither for
the paucitubulatinan x-organ (see above) nor for glandular
structures in different Macrodasyida. It is imaginable that
these organs produce and release water-soluble substances
used for chemical communication, for instance, to aid those
small organisms attracting a proper reproductive partner.
Such a function was already suggested for the x-organ of
Lepidodermella squamata (Hummon 1986). Because these
glands in Macrodasyida may be associated with the sperm
ducts and/or the caudal organ, it seems also likely that
they produce substances (e.g., mucus) that support sperm
transfer. The recently described posterior gland organ of
Dinodasys mirabilis is hypothesized to be used for gluing
the fertilized eggs to sand grains. However, it is unlikely
are able to engage in self-fertilization (see Ruppert 1977).
However, even if anatomically possible it does not seem
that self-fertilization occurs (Balsamo 1992).
1.2.9.4Reproductive system of the Paucitubulatina
The whole reproductive system, together with the whole
life history, has strongly been modified in the gastrotrich
subtaxon Paucitubulatina. Putative basal paucitubulati-
nan groups such as the marine Xenotrichulidae (Figs. 1.32
D and 1.37 G) and Muselliferidae are still hermaphrodites
that develop full male and female gonads during their
life history (e.g., Ferraguti etal. 1995, Guidi etal. 2003a,
Balsamo etal. 2010a). Species of the genus Musellifer might
be the only members of Paucitubulatina that possibly
possess an accessory reproductive organ in addition to
the gonads (Hummon 1969). However, the presence of any
accessory organ could not be supported for at least Musel-
lifer profundus (Leasi & Todaro 2010). The more derived
and predominantly freshwater taxa (traditional families
Proichthydidae, Chaetonotidae, Dasydytidae, Neogos-
seidae) show a different morphological and temporal
arrangement of reproductive structures. As a model orga-
nism, Lepidodermella squamata was studied intensely to
reveal gametogenesis and reproductive biology in a fresh-
water gastrotrich (Hummon 1984a–c, 1986). In this species,
populations consist of individuals that possess a paired
female gonad producing subitanuous eggs (tachyblastic
eggs) by parthenogenesis. These animals can also produce
parthenogenetic resting eggs (opsiblastic eggs) with a
resistant eggshell. Specimens, possibly each individual of
a population (see discussion in Weiss 2001) enter a post-
parthenogenetic stage and cysts with simple rod-shaped,
filiform, spindle-shaped, or oval male germ cells (simpli-
fied spermatozoa) are formed (Figs. 1.32 C and 1.41 B–F).
There are no proper testes with wall epithelia or outlet
ducts; however, a vesiculated region in the ventral epider-
mis of Lepidodermella squammata was observed close to
each sperm packet and interpreted as male genital pores
(Hummon & Hummon 1983b, but see also discussion in
Weiss 2001). The cysts with 9–16 simplified non-flagellated
sperm cells in various Paucitubulatina generally occur in
one or two ventral pairs, while up to 12 sperm packets in
one individual are possible (Weiss 2001). Within the ovary,
a further resting egg is matured in these “sperm bearers”.
Although not proven, a sexual reproduction with recombi-
nation, possibly with cross-fertilization in Lepidodermella
squamata is assumed (Hummon 1986). Because sperm
bearers were discovered in dozens of freshwater-dwel-
ling species (Weiss 2001), a life history of initially pure
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1.2Morphology 57
that the posterior gland organ of D. mirabilis and the real
caudal organ, present in most macrodasyidan species, are
homologue features (Todaro etal. 2012a).
1.2.10Gametes
1.2.10.1Spermatozoa
In early monographs (e.g., Zelinka 1889), the existence
of male gonads as well as spermatozoa in Gastrotricha
was keenly doubted. It should be noted that at that time
almost only freshwater species of the taxon Paucitubu-
latina were known who develop highly simplified sperm
cells in a rather short period of their lifespan. Those her-
maphroditic specimens attracted little attention for a long
time. The discovery of many new taxa of the gastrotrich
subgroup Macrodasyida in the early 20th century (e.g.,
Remane 1924, 1927a) revealed that at least the new marine
species were hermaphrodites with testes and the ability to
develop proper spermatozoa. First descriptions of sperms
based on light microscopy can be found in Remane’s
monographs (Remane 1927c, 1929, 1936). In the later work
(Remane 1936), he depicts drawings of the long and partly
spiraled sperm cells of Oregodasys maximus and Ptychos-
tomella ommatophora as well as of the short-tailed and
compact sperm of Neodasys chaetonotoideus. Remane
(1927c) already introduced the two general sperm types of
the Gastrotricha, the nowadays termed (a) filiform sperma-
tozoon (“fadenförmig”) of most Macrodasyida and many
Paucitubulatina and the (b) commaform spermatozoon
(“eiförmig mit kurzem Schwanz”=ovoid with short tail) of
Neodasys. Later, microscopic observations of further mac-
rodasyidan species confirmed the filiform sperm type with
spiraled sperm head and/or middle region, for instance,
in Mesodasys laticaudatus (synonym: Cephalodasys lobo-
cercus), Cephalodasys cambriensis (synonym: Paradasys
cambriensis), and Oregodasys styliferus (see Boaden 1960,
1963, 1965). However, those pure light microscopic obser-
vations already demonstrated a certain morphological
complexity and diversity among gastrotrich spermato-
zoa. Microscopic observations of spermatozoa of different
species of the marine paucitubulatinan taxon Xenotri-
chulidae (Wilke 1954) demonstrated a filiform sperm type
without any spiraled parts in that group. Furthermore, the
sperms of Heteroxenotrichula squamosa displayed some
peculiar unknown differentiations, the two “thin acces-
sory flagella”, today known as the para-acrosomal bodies
(see below). A misinterpretation that unites almost all of
the early light-optical investigations of sperm morphology
in Gastrotricha is the assumption that the anterior tip of
the filiform cell represents the nucleus (see, e.g., Remane
1936, Wilke 1954).
Resolving power of the TEM opened a window to an
unexpected ultrastructural complexity of sperm cells. The
first comprehensive ultrastructural study of spermatozoa
(and sperm development, see below) in Gastrotricha was
carried out by Teuchert (1975b, 1976b) who investigated
formation and submicroscopic morphology of sperms of
Turbanella cornuta. This pioneering study was shortly
followed by an investigation of sperm transfer modali-
ties in an undetermined species of Macrodasys that also
contains many data on sperm ultrastructure (Ruppert
1978a). The mass of sperm cell reconstructions based
on TEM studies was carried out during the past 20years
beginning in the mid-1990s. Since the first investigation of
Teuchert (1976b), spermatozoa of at least 33 species from
all major subtaxa of the Gastrotricha have been studied
ultrastructurally (see Tab. 1.5): Neodasys/Multitubulatina,
1 species (Guidi etal. 2003a), Paucitubulatina, 7 species
(Balsamo 1992, Balsamo et al. 2010a, Ferraguti et al.
1995, Guidi etal. 2003a, Hummon 1984b), and Macroda-
syida, 25 species (Balsamo etal. 2002, 2007, Ferraguti &
Balsamo 1994, 1995, Fischer 1994, 1996, Fregni etal. 1999,
Guidi etal. 2004, 2009, 2011, Pierboni etal. 2003, 2004,
Marotta etal. 2005, Pierboni & Kristensen 2007, Ruppert
1978a, Teuchert 1976b, Todaro etal. 2000a, 2012a). Most
recently, Guidi etal. (2014) published the reconstruction
of the spermatozoon of yet another taxon of the Macro-
dasyida, Megadasys sterreri (not yet included in Tab. 1.5).
The general gastrotrich sperm types already described by
Remane (1927c, 1929, 1936) and Wilke (1954) were suppor-
ted by the ultrastructural studies: filiform sperms with spi-
raled head in most Macrodasyida (Fig. 1.38 A–F), filiform
sperms without spiraled regions in (basal) Paucitubula-
tina (Fig. 1.38 G–M), the latter sometimes with elongated
para-acrosomal bodies (Fig. 1.40 A–D), and commaform
sperms in Neodasys (Fig. 1.39 A–F).
Because of a certain degree of similarity between
spermatozoa of different species of the Macrodasyida,
a “basic sperm plan” for that group could be compiled.
According to this, the macrodasyidan sperm is composed
of an acrosomal anterior region, a nuclear central region,
and a flagellar distal region. The long and corkscrew-
shaped acrosome is often composed of two different por-
tions (anterior and basal) and contains an internal stri-
ated tube. The spring-shaped nucleus surrounds several
small or one giant, tube-shaped mitochondrion. The fla-
gellum (cilium) is composed of a normal axoneme (9×2+2
pattern of microtubules) that is surrounded by a striated
cylinder (Balsamo etal. 1999, Ferrraguti & Balsamo 1995,
Marotta etal. 2005; Fig. 1.44 C–G). The spermatozoon of
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58 1Gastrotricha
Tab. 1.5: Morphological and ultrastructural characters of spermatozoa of 33 species of Gastrotricha.
General morphology Flagellum/cilium
Character-number (–) according to Marotta etal. ()
Sperm shape Vestigial
spermatozoa
Flagellum (cilium) of
mature sperm
Accessory fibers or
globules
Striated
cylinder
Striated cylinder
thickness
Cephalodasys maximus Filiform Monolayered
Lepidodasys sp. Filiform N.A.
Lepidodasys unicarenatus Filiform N.A.
Lepidodasys sp. (different species than in Guidi etal. ) Filiform N.A.
Mesodasys laticaudatus Filiform Multilayered
Mesodasys adenotubulatus Filiform Multilayered
Acanthodasys aculeatus (see Fig. . A–F) Filiform Monolayered
Diplodasys ankeli Filiform Monolayered
Pseudostomella etrusca Filiform Monolayered
Tetranchyroderma sp. Filiform Monolayered
Tetranchyroderma sp. Filiform Monolayered
Tetranchyroderma papii Filiform ?
Urodasys anorektoxys Filiform N.A.
Urodasys acanthostylis Filiform Monolayered
Macrodasys sp. Filiform Monolayered
Macrodasys caudatus Filiform Monolayered
Crasiella diplura Filiform N.A.
Turbanella cornuta (see Fig. . E–H) Filiform N.A.
Turbanella ambronensis Filiform N.A.
Paraturbanella teissieri Filiform N.A.
Dinodasys mirabilis Filiform N.A.
Dactylopodola baltica (see Fig. . A) Filiform-aciliar aN.A. N.A. N.A.
Dactylopodola typhle Filiform-aciliar aN.A. N.A. N.A.
Xenodasys sp. Filiform N.A.
Xenodasys eknomios Filiform N.A.
Neodasys ciritus (see Fig. . A–F) Commaform N.A.
Chaetonotus maximus Rod-like N.A. N.A. N.A.
Lepidodermella squamata (see Fig. . B) Rod-like N.A. N.A. N.A.
Musellifer delamarei (see Fig. . G–M) Filiform N.A.
Diurunotus aspetos Filiform N.A.
Heteroxenotrichula squamosa Filiform N.A.
Xenotrichula intermedia Filiform N.A.
Xenotrichula punctata (see Fig. . A–D) Filiform N.A.
(Continued)
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1.2Morphology 59
Flagellum/cilium
Character-number (–) according to Marotta etal. ()
Axonemal microtubule arrangement Endpiece Axonemal plasma membrane Number of centriolesb
Cephalodasys maximus Parallel Bubble of cytoplasm Swollen One
Lepidodasys sp. Helical ? Not swollen One
Lepidodasys unicarenatus Parallel ? Not swollen One
Lepidodasys sp. (different species than in Guidi etal. ) Parallel ? Not swollen One
Mesodasys laticaudatus Parallel ? Not swollen One
Mesodasys adenotubulatus Helical Thin Not swollen One
Acanthodasys aculeatus (see Fig. . A–F) Parallel Hollow+thin Not swollen One
Diplodasys ankeli Parallel ? Not swollen One
Pseudostomella etrusca Parallel ? Swollen One
Tetranchyroderma sp. Helical Hollow+thin Swollen One
Tetranchyroderma sp. ? ? Swollen One
Tetranchyroderma papii ? ? ? One
Urodasys anorektoxys Helical Thin Not swollen One
Urodasys acanthostylis Parallel Thin Not swollen One
Macrodasys sp. Parallel ? Swollen One
Macrodasys caudatus Parallel Twisted Swollen One
Crasiella diplura Parallel ? Swollen One
Turbanella cornuta (see Fig. . E–H) Helical ? Swollen One
Turbanella ambronensis Helical ? Swollen One
Paraturbanella teissieri Helical ? Swollen One
Dinodasys mirabilis Helical Rounded Slightly swollen One
Dactylopodola baltica (see Fig. . A) N.A. N.A. N.A. N.A.
Dactylopodola typhle N.A. N.A. N.A. N.A.
Xenodasys sp. Parallel ? Not swollen One
Xenodasys eknomios Parallel ? Not swollen One
Neodasys ciritus (see Fig. . A–F) Parallel ? Not swollen Two
Chaetonotus maximus N.A. N.A. N.A. N.A.
Lepidodermella squamata (see Fig. . B) N.A. N.A. N.A. N.A.
Musellifer delamarei (see Fig. . G–M) Parallel Thin Not swollen One
Diurunotus aspetos Parallel Thin Not swollen
Heteroxenotrichula squamosa Parallel Thin Not swollen One
Xenotrichula intermedia Parallel Thin Not swollen One
Xenotrichula punctata (see Fig. . A–D) Parallel Thin Not swollen One
Tab. 1.5: (Continued)
(Continued)
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60 1Gastrotricha
Flagellum/cilium
Character-number (–) according to Marotta etal. ()
Cap-like,or conical structure Cap-like fibers Sheath around central
microtubules
Curled plasma membrane at
flagellum
Cephalodasys maximus
Lepidodasys sp.
Lepidodasys unicarenatus
Lepidodasys sp. (different species than in Guidi etal. )
Mesodasys laticaudatus
Mesodasys adenotubulatus
Acanthodasys aculeatus (see Fig. . A–F)
Diplodasys ankeli
Pseudostomella etrusca
Tetranchyroderma sp. ? ?
Tetranchyroderma sp. ? ?
Tetranchyroderma papii ? ?
Urodasys anorektoxys
Urodasys acanthostylis
Macrodasys sp. ? ?
Macrodasys caudatus ?
Crasiella diplura
Turbanella cornuta (see Fig. . E–H)
Turbanella ambronensis
Paraturbanella teissieri N.A.
Dinodasys mirabilis
Dactylopodola baltica (see Fig. . A) N.A. N.A. N.A. N.A.
Dactylopodola typhle N.A. N.A. N.A. N.A.
Xenodasys sp.
Xenodasys eknomios ?
Neodasys ciritus (see Fig. . A–F)
Chaetonotus maximus N.A. N.A. N.A. N.A.
Lepidodermella squamata (see Fig. . B) N.A. N.A. N.A. N.A.
Musellifer delamarei (see Fig. . G–M) N.A.
Diurunotus aspetos N.A.
Heteroxenotrichula squamosa
Xenotrichula intermedia
Xenotrichula punctata (see Fig. . A–D) N.A.
Tab. 1.5: (Continued)
(Continued)
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1.2Morphology 61
Nucleus/sperm head
Character-number (–) according to Marotta etal. ()
Shape of sperm head Shape of nucleus Reduction of nuclear diameter Chromatin condensation
Cephalodasys maximus Spiral/helical Spiral/slightly spiral Complete
Lepidodasys sp. Spiral/helical Ribbon-like Complete
Lepidodasys unicarenatus Spiral/helical Ribbon-like Complete
Lepidodasys sp. (different species than in Guidi etal. ) Spiral/helical Ribbon-like Complete
Mesodasys laticaudatus Spiral/helical Ribbon-like Complete
Mesodasys adenotubulatus Spiral/helical Ribbon-like Complete
Acanthodasys aculeatus (see Fig. . A–F) Spiral/helical Ribbon-like Complete
Diplodasys ankeli Spiral/helical Ribbon-like Complete
Pseudostomella etrusca Spiral/helical Spiral/slightly spiral Complete
Tetranchyroderma sp. Spiral/helical Ribbon-like Complete
Tetranchyroderma sp. Spiral/helical Ribbon-like Complete
Tetranchyroderma papii Spiral/helical Ribbon-like Complete
Urodasys anorektoxys Spiral/helical Spiral+straight (at base) Fingerprint-like
Urodasys acanthostylis Spiral/helical Complex spiral Fingerprint-like
Macrodasys sp. Spiral/helical Spiral/slightly spiral ? Complete
Macrodasys caudatus Spiral/helical Spiral/slightly spiral Complete
Crasiella diplura Spiral/helical Spiral/slightly spiral Complete
Turbanella cornuta (see Fig. . E–H) Spiral/helical Ribbon-like Complete
Turbanella ambronensis Spiral/helical Ribbon-like ? Complete
Paraturbanella teissieri Spiral/helical Ribbon-like Complete
Dinodasys mirabilis Spiral/helical Ribbon-like Complete
Dactylopodola baltica (see Fig. . A) StraightcAlternate layers Complete
Dactylopodola typhle Spiral/helical Alternate layers Complete
Xenodasys sp. Spiral/helical Ribbon-like Complete
Xenodasys eknomios Spiral/helical Ribbon-like Complete
Neodasys ciritus (see Fig. . A–F) Straight Straight Complete
Chaetonotus maximus Straight Straight ?
Lepidodermella squamata (see Fig. . B) Straight Straight ?
Musellifer delamarei (see Fig. . G–M) Straight Straight Partial
Diurunotus aspetos Straight Straight Complete
Heteroxenotrichula squamosa Straight Straight Partial
Xenotrichula intermedia Straight Straight Partial
Xenotrichula punctata (see Fig. . A–D) Straight Straight Partial
Tab. 1.5: (Continued)
(Continued)
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62 1Gastrotricha
Nucleus/sperm head Mitochondrium/mitochondria
Character-number (–) according to Marotta etal. ()
Shape of nuclear apex Shape of nuclear base Mitochondria Number/size of
mitochondria
Position/arrangement of
mitochondria
Cephalodasys maximus Convex Slightly concave One giant Inside nucleus
Lepidodasys sp. Flat/slightly concave Slightly concave One giant Inside nucleus
Lepidodasys unicarenatus Flat/slightly concave Slightly concave One giant Inside nucleus
Lepidodasys sp. (different species than in Guidi etal. ) Flat/slightly concave With fossa One giant Inside nucleus
Mesodasys laticaudatus Flat/slightly concave Slightly concave More than (small) Inside nucleus
Mesodasys adenotubulatus ? ? One giant Inside nucleus
Acanthodasys aculeatus (see Fig. . A–F) Convex Slightly concave One giant Inside nucleus
Diplodasys ankeli Flat/slightly concave Slightly concave One giant Inside nucleus
Pseudostomella etrusca Flat/slightly concave Flat More than (small) Inside nucleus
Tetranchyroderma sp. Flat/slightly concave Flat One giant Inside nucleus
Tetranchyroderma sp. Flat/slightly concave ? ? Inside nucleus
Tetranchyroderma papii Flat/slightly concave ? ? Inside nucleus
Urodasys anorektoxys Convex+spiraled With fossa N.A. N.A.
Urodasys acanthostylis Convex+spiraled With fossa N.A. N.A.
Macrodasys sp. Convex ? One giant Spirally around head
Macrodasys caudatus Flat/slightly concave With fossa One giant Spirally around head
Crasiella diplura Flat/slightly concave With fossa One giant Inside nucleus
Turbanella cornuta (see Fig. . E–H) Flat/slightly concave With fossa One giant Inside nucleus
Turbanella ambronensis Flat/slightly concave With fossa One giant Inside nucleus
Paraturbanella teissieri Flat/slightly concave Flat One giant Inside nucleus
Dinodasys mirabilis Concave With fossa One giant Inside nucleus
Dactylopodola baltica (see Fig. . A) Convex Convex More than (small) Along nucleusd
Dactylopodola typhle Convex Convex More than (small) Inside nucleus
Xenodasys sp. N.A. N.A. More than (small) Around connecting piece
Xenodasys eknomios N.A. N.A. More than (small) Around connecting piece
Neodasys ciritus (see Fig. . A–F) Flat/slightly concave With fossa More than (small) Randomly around head
Chaetonotus maximus Convex Convex N.A. N.A.
Lepidodermella squamata (see Fig. . B) Convex Convex N.A. N.A.
Musellifer delamarei (see Fig. . G–M) Flat/slightly concave ? More than (small) At nuclear base
Diurunotus aspetos Convex With deep fossa One giant Around nuclear base
Heteroxenotrichula squamosa Flat/slightly concave Flat One small At nuclear base
Xenotrichula intermedia Flat/slightly concave With fossa One small At nuclear base
Xenotrichula punctata (see Fig. . A–D) Flat/slightly concave Flat One small At nuclear base
Tab. 1.5: (Continued)
(Continued)
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1.2Morphology 63
Acrosome
Character-number (–) according to Marotta etal. ()
Acrosome Shape of acrosome Composition of acrosome Acrosomal thick
disks
Acrosomal tubular
structure
Cephalodasys maximus Corkscrew With different regions
Lepidodasys sp. Cylindrical+corkscrew With different regions
Lepidodasys unicarenatus Cylindrical+corkscrew With different regions
Lepidodasys sp. (different species than in Guidi etal. ) Cylindrical+corkscrew With different regions
Mesodasys laticaudatus Cylindrical+corkscrew With different regions
Mesodasys adenotubulatus ? ?
Acanthodasys aculeatus (see Fig. . A–F) Corkscrew With different regions
Diplodasys ankeli Corkscrew With different regions
Pseudostomella etrusca Corkscrew With different regions
Tetranchyroderma sp. Corkscrew With different regions
Tetranchyroderma sp. Corkscrew With different regions
Tetranchyroderma papii Corkscrew With different regions
Urodasys anorektoxys Cylindrical With different regions
Urodasys acanthostylis Helical Homogeneous
Macrodasys sp. Cylindrical+corkscrew With different regions
Macrodasys caudatus Cylindrical+corkscrew With different regions
Crasiella diplura Cylindrical+corkscrew With different regions
Turbanella cornuta (see Fig. . E–H) Cylindrical+corkscrew With different regions
Turbanella ambronensis Cylindrical+corkscrew With different regions
Paraturbanella teissieri Cylindrical With different regions
Dinodasys mirabilis Cylindrical+corkscrew With different regions
Dactylopodola baltica (see Fig. . A) Cylindrical ?
Dactylopodola typhle Cylindrical ?
Xenodasys sp. Cylindrical With different regions
Xenodasys eknomios Cylindrical With different regions
Neodasys ciritus (see Fig. . A–F) Pear-shaped With different regions
Chaetonotus maximus N.A. N.A. N.A. N.A.
Lepidodermella squamata (see Fig. . B) N.A. N.A. N.A. N.A.
Musellifer delamarei (see Fig. . G–M) Cylindrical With different regions
Diurunotus aspetos Cylindrical Two cones
Heteroxenotrichula squamosa Cylindrical Homogeneous
Xenotrichula intermedia N.A. N.A. N.A. N.A.
Xenotrichula punctata (see Fig. . A–D) Cylindrical Homogeneous
Tab. 1.5: (Continued)
(Continued)
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64 1Gastrotricha
Acrosome
Character-number (–) according to Marotta etal. ()
Acrosomal material Tubular structure
organization
Shape of tubular structure Tubular structure
withdrawal
Ribbon helix around
acrosome
Cephalodasys maximus Uncondensed Ring-like Rectilinear+twisted
Lepidodasys sp. Condensed at base N.A. N.A. N.A.
Lepidodasys unicarenatus Condensed at apex N.A. N.A. N.A.
Lepidodasys sp. (different species than in Guidi etal. ) Condensed at apex N.A. N.A. N.A.
Mesodasys laticaudatus Condensed at apex N.A. N.A. N.A.
Mesodasys adenotubulatus ? N.A. N.A. N.A.
Acanthodasys aculeatus (see Fig. . A–F) Uncondensed Ring-like Rectilinear+twisted
Diplodasys ankeli Uncondensed Ring-like Twisted
Pseudostomella etrusca Uncondensed Ring-like Rectilinear
Tetranchyroderma sp. Uncondensed Ring-like Rectilinear
Tetranchyroderma sp. Uncondensed ? Twisted ?
Tetranchyroderma papii Uncondensed Ring-like ? ?
Urodasys anorektoxys Uncondensed Ring-like Twisted
Urodasys acanthostylis Uncondensed N.A. N.A. N.A.
Macrodasys sp. Uncondensed Continuous ?
Macrodasys caudatus Uncondensed Continuous ?
Crasiella diplura Condensed at apex Helical+radial ? ?
Turbanella cornuta (see Fig. . E–H) Condensed at base N.A. N.A. N.A.
Turbanella ambronensis Condensed at base N.A. N.A. N.A.
Paraturbanella teissieri Condensed at base N.A. N.A. N.A.
Dinodasys mirabilis Condensed at apex Continuous Obliquely striated ?
Dactylopodola baltica (see Fig. . A) Uncondensed N.A. N.A. N.A.
Dactylopodola typhle Uncondensed N.A. N.A. N.A.
Xenodasys sp. Condensed at base N.A. N.A. N.A. ?
Xenodasys eknomios Condensed N.A. N.A. N.A.
Neodasys ciritus (see Fig. . A–F) Uncondensed Tubular structure-like Rectilinear
Chaetonotus maximus N.A. N.A. N.A. N.A. N.A.
Lepidodermella squamata (see Fig. . B) N.A. N.A. N.A. N.A. N.A.
Musellifer delamarei (see Fig. . G–M) Uncondensed N.A. N.A. N.A.
Diurunotus aspetos Condensed+filamentous N.A. N.A. N.A.
Heteroxenotrichula squamosa Uncondensed N.A. N.A. N.A.
Xenotrichula intermedia N.A. N.A. N.A. N.A. N.A.
Xenotrichula punctata (see Fig. . A–D) Uncondensed N.A. N.A. N.A.
Tab. 1.5: (Continued)
(Continued)
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1.2Morphology 65
Further structures Reference
Character-number (–) according to Marotta etal. ()
Perinuclear helix Para-acrosomal bodies Basal crystal
Cephalodasys maximus Fischer
Lepidodasys sp. Guidi et al.
Lepidodasys unicarenatus Guidi et al.
Lepidodasys sp. (different species than in Guidi etal. ) Pierboni & Kristensen
Mesodasys laticaudatus Ferraguti & Balsamo
Mesodasys adenotubulatus Fregni et al.
Acanthodasys aculeatus (see Fig. . A–F) Guidi et al. b
Diplodasys ankeli Ferraguti & Balsamo
Pseudostomella etrusca Ferraguti & Balsamo
Tetranchyroderma sp. Ferraguti & Balsamo
Tetranchyroderma sp. Ferraguti & Balsamo
Tetranchyroderma papii ? Ferraguti & Balsamo
Urodasys anorektoxys Todaro et al. a, Pierboni et al. , unpublished/Marotta et al.
, Balsamo et al.
Urodasys acanthostylis Pierboni et al. , unpublished/Marotta et al. , Balsamo et al.
Macrodasys sp. Ruppert a
Macrodasys caudatus Marotta et al.
Crasiella diplura Guidi et al.
Turbanella cornuta (see Fig. . E–H) Teuchert b
Turbanella ambronensis Ferraguti & Balsamo
Paraturbanella teissieri Balsamo et al.
Dinodasys mirabilis Todaro et al. a
Dactylopodola baltica (see Fig. . A) Fischer
Dactylopodola typhle unpublished/Marotta et al.
Xenodasys sp. Pierboni et al. , unpublished/Marotta et al.
Xenodasys eknomios Guidi et al.
Neodasys ciritus (see Fig. . A–F) Guidi et al. a
Chaetonotus maximus Balsamo
Lepidodermella squamata (see Fig. . B) Hummon b
Musellifer delamarei (see Fig. . G–M) Guidi et al. a
Diurunotus aspetos Balsamo et al. a
Heteroxenotrichula squamosa Ferraguti & Balsamo
Xenotrichula intermedia Ferraguti et al.
Xenotrichula punctata (see Fig. . A–D) Ferraguti et al.
Modified from Marotta etal. () and amended. A question mark (?) indicates an unknown character state; N.A., not applicable; , absence; , presence.
a Fischer () describes the penetrated spermatozoon of D. baltica. It is possible that mature free” sperms do have a flagellum.
b In several species, the centriole or basal body is strongly modified (see, e.g., Balsamo et al. ).
c According to Marotta et al. (), D. baltica possesses a helical sperm head though it is straight according to Fischer ().
d According to Marotta et al. (), D. baltica possesses mitochondria inside the nucleus though they lie along the nucleus according to Fischer ().
Tab. 1.5: (Continued)
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66 1Gastrotricha
Acanthodasys aculeatus (Figs. 1.38 A–F and 1.44 C–E)
is a good representative of this “basic sperm plan”. It
has to be stressed that this character pattern rather is a
“generalized Bauplan” than a strictly phylogenetic recon-
struction of the character pattern of the stem species of
Macrodasyida. However, modifications from the afo-
rementioned pattern are manifold. Microstructure and
special differentiations of the acrosome, for example,
are quite diverse. Acrosomal content may be condensed,
uncondensed, or just condensed in the anterior or in the
basal portion. Acrosomal tubular structures are absent
in Lepidodasys, Mesodasys, Urodasys acanthostylis
(present in U. anorektoxys), Turbanella, Paraturbanella,
Dactylopodola, and Xenodasys (see Tab. 1.5 and referen-
ces therein). Species of the Turbanellidae and Xenodasys
eknomios (not Xenodasys sp.) possess piles of thick and
electron-dense discs in their acrosomes. The chromatin
is condensed in all species of the Macrodasyida investi-
gated so far, unlike in species of Urodasys where sperm
nuclei show a conspicuous fingerprint-like microstruc-
ture (Marotta etal. 2005, Balsamo etal. 2007). Many but
not all of the studied species of Thaumastodermatidae
(the only known exception is Pseudostomella etrusca)
have a spring-shaped nucleus surrounded by a heli-
cally arranged cistern, the perinuclear helix (Ferraguti
& Balsamo 1995, Guidi et al. 2003b). Another unusual
character of the nuclear central region was observed in
species of Macrodasys: here, the giant mitochondrion
winds spirally around the central and only slightly spi-
raled nucleus (Ruppert 1978a, Marotta etal. 2005) and
not vice versa like in most remaining macrodasyids.
As already mentioned, there can be a single elongated
mitochondrion associated with the nucleus or several
small and ovoid ones (see Tab. 1.5 and the references
0.5 µm
0.5 µm
A
B
C
D
aar
ac
E
F
G
H
I
J
KL
M
ncrfpr
aarncrfpr
nu
ph
dc
sc
mi
at
aa
ab
sm
nu
mi
af
se
Fig. 1.38: Sperm ultrastructure (schematic)
of Gastrotricha. (A–F) Spermatozoon of
Acanthodasys aculeatus (Macrodasyida).
(A) Whole sperm (131 µm total length).
(B) Longitudinal sections of different
regions. (C–F) Cross sections at different
levels. (G–M) Spermatozoon of Musellifer
delamarei (Paucitubulatina). (G) Whole
sperm (28 µm total length). (H) Longitudinal
sections of different regions. (I–M) Cross
sections at different levels. Abbreviations:
aa, anterior portion of acrosome; aar,
anterior acrosomal region; ab, basal
portion of acrosome; ac, acrosome; af,
accessory fiber; at, axial tubular structure;
dc, distal centriole; fpr, flagellar posterior
region; mi, mitochondrion; ncr, nuclear
central region; nu, nucleus; ph, perinuclear
helix; sc, striated cylinder; se, septa; sm,
supernumerary membrane. (A–F, According
to Guidi etal. 2003a; G–M, according to
Guidi etal. 2003b.)
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1.2Morphology 67
in Tab. 1.5 are lost). In mature spermatozoa, mitochon-
dria can also be absent at all as in species of Urodasys
(Marotta et al. 2005, Balsamo et al. 2007). The stria-
ted cylinder surrounding the flagellar axoneme in the
“basic sperm plan” of Macrodasyida is absent in several
species, including all members of the Turbanellidae
studied so far. A distal centriole (basal body) is repor-
ted from all studied species of Macrodasyida. However,
shape and arrangement of basal structures vary a lot
between species. There might be, for instance, acces-
sory parts like conical or cap-like structures and thin
fibers that support the connection between nucleus and
axoneme (Tab. 1.5). Completely different sperm mor-
phology can be observed in species of Dactylopodola
(Fig. 1.41 A). Those sperms are filiform, too, but they
consist of a long, thin, and rod-shaped nuclear region
and an adjacent rod-like compartment where small disc-
shaped and piled mitochondria alternate with dense
bodies of unknown function (Fischer 1996). Neither an
acrosome nor a flagellum were observed, but it has to be
mentioned that only penetrated spermatozoa of D. baltica
were studied with TEM and no mature, testicular sperms.
It is also possible that both structures disappear when the
sperm cell enters the egg cell during fertilization (Fischer
1996). Further unusual sperm morphology was descri-
bed for Dolichodasys carolinensis. Mature spermatozoa of
that taxon appear like a “swollen semicolon” without a
1 µm
A
B
C
D
aar
wf
E
F
ncr
fpr
dc
aa
ab
nu
mi
pc
tu
cs
Fig. 1.39: Sperm ultrastructure (schematic) of Gastrotricha. (A–F)
Spermatozoon of Neodasys cirritus (Multitubulatina). (A) Whole
sperm (approximately 13 µm total length). (B) Longitudinal sections
of different regions. (C–F) Cross sections at different levels.
Abbreviations: aa, anterior portion of acrosome; aar, anterior
acrosomal region; ab, basal portion of acrosome; cs, crystalline
structure; dc, distal centriole; fpr, flagellar posterior region;
mi, mitochondrion; ncr, nuclear central region; nu, nucleus;
pc, proximal centriole; tu, tubule of the acrosome; wf, “wig” of
filaments. (A–F, According to Guidi etal. 2003b.)
1 µm
AB
C
D
aar
ncrfpr
ac
nu
mi
pb
pb
af
Fig. 1.40: Sperm ultrastructure (schematic) of Gastrotricha. (A–D)
Spermatozoon of Xenotrichula punctata (Paucitubulatina). (A) Whole
sperm (approximately 10 µm total length without para-acrosomal
bodies, length of para-acrosomal body is 20 µm). (B) Longitudinal
sections of different regions. (C, D) Cross sections at different
levels. Abbreviations: aar, anterior acrosomal region; ac, acrosome;
af, accessory fiber; fpr, flagellar posterior region; mi,
mitochondrion; ncr, nuclear central region; nu, nucleus; pb, para-
acrosomal body. (A–D, According to Ferraguti etal. 1995.)
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68 1Gastrotricha
(Fig. 1.44 A, B) and basal members of the Paucitubulatina
such as Musellifer delamarei, Diuronotus aspetos (Guidi
et al. 2003b, Balsamo et al. 2010a) and species of the
Xenotrichulidae (Ferraguti et al. 1995). However, because
neither the acrosomal nor the nuclear regions are spiraled
or helically arranged, the external distinction between the
three parts is less obvious. Neodasys is the only gastrotrich
taxon that possesses the commaform (or dart-shaped, see
Ruppert 1977) sperm type (Figs. 1.39 and 1.44 A, B). A some-
what conical to pear-shaped sperm head contains the ante-
rior acrosome and the rod-shaped nucleus (Ruppert 1977,
1991, Guidi etal. 2 003b, see also Kieneke etal. 2009). A short
flagellum is attached perpendicular to the nuclear base,
giving the whole cell the typical commaform shape (Fig.
1.39). Internally, the cone-shaped acrosome of Neodasys
cirritus has a tubule (apical region) and a crystalline struc-
ture (basal region). Externally, it is enwrapped by a “wig”
of short filaments in its apical region (Fig. 1.44 A), whereas
few small mitochondria are situated near the transition
from acrosome to nucleus (Guidi etal. 2003b). Until now,
N. cirritus is the only known gastrotrich that has, in addi-
tion to the distal centriole (basal body), a remnant of the
apical (accessory) centriole (Tab. 1.5). The not spiraled,
filiform spermatozoa of basal marine and fully hermaph-
roditic members of the Paucitubulatina such as Musellifer
delamarei (Fig. 1.38 G–M), Diuronotus aspetos, and species
of the Xenotrichulidae (e.g., Fig. 1.40 A–D) are composed
in sequence of an anterior acrosome, sometimes regiona-
lized by different content or even separated into two parts
(e.g., in Diuronotus aspetos), a rod-shaped and mostly
incompletely condensed nucleus, a single or few mito-
chondria (e.g., in Musellifer delamarei, see Fig. 1.38 H, J)
basal to the nucleus, and a long flagellum (Balsamo etal.
2010a, Ferraguti & Balsamo 1995, Ferraguti et al. 1995,
Guidi etal. 2003b). The flagellum consists of a standard
axoneme but with nine peculiar accessory fibers attached
to the outer doublets of axonemal microtubules (see Figs.
1.38 K and 1.40 D). The three-dimensional microstructure
of those accessory fibers is a complex system of undeter-
mined filaments and rib-like structures (Ferraguti etal.
1995). In cross section, each accessory fiber has a roughly
triangular shape with a content of different electron trans-
missibility (see, e.g., Fig. 1.40 D). Analogue differentia-
tions in the same position can be found in the flagellum
of the spermatozoa of some macrodasyidan species, e.g.,
in Cephalodasys maximus (Fischer 1994) and in species of
Urodasys (Balsamo etal. 2007). It has to be considered that
these structures evolved convergently. Another instance of
convergent evolution is the loss of mitochondria in sperms
of Urodasys and derived members of Paucitubulatina
(Marotta etal. 2005). Other differences between the sperm
1 µm
5 µm
AB
nu
mi
db
C
D
E
F
Fig. 1.41: Sperm ultrastructure (schematic) of Gastrotricha. (A)
Longitudinal section of penetrated spermatozoon of Dactylopodola
baltica (Macrodasyida). (B) Longitudinal section of sperm rod of
Lepidodermella squammata (Paucitubulatina). (C–F) Different
shapes of sperm cells in freshwater Paucitubulatina (all at same
scale). (C) Filiform shape of Chaetonotus bisacer. (D) Rod-like
shape of Chaetonotus sp. (E) Spindle-like shape of Polymerurus
rhomboides. (F) Oval shape of Stylochaeta scirtetica. Abbreviations:
db, dense bodies; mi, mitochondrion; nu, nucleus. (A, According
to Fischer 1996; B, according to Hummon 1984b; C–F, according to
Weiss 2001.)
flagellum (Ruppert & Shaw 1977). Unfortunately, sperma-
tozoa of D. carolinensis were only studied with histologi-
cal techniques and light microscopy.
Subtle interspecific ultrastructural differences in
spermatozoa are also quite diverse within the Chaeto-
notida (=Neodasys/Multitubulatina+Paucitubulatina).
In addition, the gross sperm morphology, the “sperm
types”, is more diverse among the major sub groups (Tab.
1.5). Accordingly, it was not possible to outline a “basic
sperm model” for the Chaetonotida (Marotta etal. 2005).
It has to be considered that Chaetonotida might not repre-
sent a monophylum (see chapter Phylogeny). In that case,
a ground pattern reconstruction for such a group would
be inappropriate. The tripartition into anterior acroso-
mal region, nuclear central region, and flagellar posterior
region is also present in the sperm of Neodasys cirritus
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1.2Morphology 69
gastrotrichs (subitaneous and resting eggs, both produ-
ced through apomictic parthenogenesis, and third mor-
phologically different egg type, which maybe a product of
amphimixis) is considered as possible evidence for sexual
reproduction (Hummon & Hummon 1983a, Balsamo 1992
and references therein). Another sign for functionality
of simplified sperm in freshwater Gastrotricha could be
the observation that isolated postparthenogenetic indi-
viduals generally do not lay eggs, or if yet in rare cases,
these eggs do not develop properly. This suggests that
fertilization (amphimixis) is required for proper cleavage
and embryonic development (Hummon 1984c, Balsamo &
Todaro 1988, Balsamo 1992).
Spermatozoa of the filiform and spiraled type can
reach a considerable length, several dozen times longer
than its diameter, that is mostly less than 1 µm. For
instance, sperms of Acanthodasys aculeatus are appro-
ximately 131 µm long (Guidi etal. 2003b), of Macrodasys
caudatus 75 µm (Marotta etal. 2005), and of Megadasys
sterreri 125–130 µm (Guidi et al. 2014). However, there
are also more compact filiform and spiraled sperm cells
in species such as Urodasys acanthostylis (Balsamo etal.
2007, approximately 18 µm) or Turbanella ambronensis
(Ferraguti & Balsamo 1995, no total length data provided).
It seems that the filiform but not spiraled sperm cells of
basal hermaphroditic species of the Paucitubulatina are
generally less elongate. For instance, the mature sper-
matozoon of Musellifer delamarei has a length of 28 µm
and a maximum width of almost 1 µm (Guidi etal. 2003a).
Sperms of Xenotrichulidae, para-acrosomal bodies not
considered, may be rather short with a length of 10 µm
(X. punctata, Ferraguti etal. 1995) or 14 µm (Heteroxe-
notrichula squamosa, Ferraguti & Balsamo 1995) but can
be much longer as in X. intermedia (Ferraguti et al., no
total length data provided). The commaform sperms of
Neodasys cirritus (ca. 13 µm length, Guidi etal. 2003a),
the aberrant sperms of Dactylopodola baltica (ca. 14 µm
length, Fischer 1996), and the vestigial sperm cells of Lepi-
dodermella squamata (7–8 µm length, Hummon 1984b),
and other freshwater paucitubulatinans (Weiss 2001) are
generally much shorter than those of most Macrodasyida
(see Figs. 1.39 A–F and 1.41 A–F).
Although motility of the flagellated sperm types of
marine Gastrotricha is broadly assumed, there are, to
our knowledge, only few documented observations of
actively moving spermatozoa inside the testes, e.g., in
an undescribed species of Neodasys (probably N. cirri-
tus) when the specimen was slightly compressed (perso-
nal communication of Ruppert in Hummon & Hummon
1983b) and in different species of Xenotrichulidae (Fer-
raguti etal. 1995). If spermatozoa are artificially released
cells of basal species of the Paucitubulatina exist in the
shape and arrangement of the mitochondria. They might
be quite big and barrel-shaped organelles like in Xenotri-
chula intermedia or X. punctata (Ferraguti etal. 1995, see
Fig. 1.40 B), a large, cuff-like mitochondrion enwrapping
the basal portion of the nucleus as in Diuronotus aspetos
(Balsamo etal. 2010a), or, as already mentioned, a cluster
of four small mitochondria like in Musellifer delamarei
(Guidi et al. 2003b, see Fig. 1.38 H). Peculiar differenti-
ations of spermatozoa of some species of the Xenotri-
chulidae (e.g., Xenotrichula punctata, Fig. 1.40 A–D) are
the para-acrosomal bodies, the function of which is still
unknown (Ferraguti & Balsamo 1995, Ferraguti etal. 1995).
Originating close to the transition between the real acro-
some and nucleus, these long and thin structures (approxi-
mately 20×0.2 µm) are composed of piles of electron-dense
discs (Fig. 1.40 A, B). Each disc is linked with its neighbo-
ring discs by thin filaments. The para-acrosomal bodies
are extracellular formations and not surrounded by a cell
membrane (Ferraguti etal. 1995). It still remains unclear
whether these presumably energy-costing para-acrosomal
bodies are in any connection with the fertilization process
(Ferraguti etal. 1995).
More derived and mostly freshwater-dwelling species
of the Paucitubulatina like Lepidodermella squamata or
Chaetonotus maximus develop extremely modified sper-
matozoa after a phase of parthenogenetic reproduction
(Hummon 1984b). These cells are nothing more but a
rod-shaped nucleus with fully condensed chromatin sur-
rounded by a cellular membrane (Hummon & Hummon
1983b, Hummon 1984b, Balsamo 1992). As nuclear enve-
lope and cellular membrane lie close to each other, there
is almost no cytoplasm present (Fig. 1.41 B). Comparably
simplified spermatozoa as in L. squamata and C. maximus
were first reported by a handful of researchers in cultured
or environmentally sampled freshwater gastrotrichs (e.g.,
Weiss & Levi 1980, Kisielewska 1981, Balsamo & Todaro
1987, 1988). However, it was Weiss (2001) who demonstrated
a widespread occurrence of simple, aflagellar sperm among
22 freshwater dwelling species of the Paucitubulatina.
There is a certain degree of morphological diversity among
these germ cells as they display filiform, rod-like, spindle-
like, or oval shapes (Weiss 2001, Fig. 1.41 C–F). Because of
their simplicity, these cells are frequently called vestigial
spermatozoa (e.g., Marotta etal. 2005). However, though
still not fully proven, an amphimictic function of these
simplified sperms in a sexual phase of the life cycle after
parthenogenesis is much likely (Balsamo 1992, Hummon
1984b, 1986, Weiss 2001, see also chapter Reproductive
Biology). The occurrence of three morphologically dif-
ferent egg types in cultured and free-living freshwater
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70 1Gastrotricha
from the testes, they are usually inactive (Hummon &
Hummon 1983b), but activity in freed spermatozoa was
also observed, for instance, in Turbanella cornuta (Teu-
chert 1976b) or in Urodasys acanthostylis (Balsamo etal.
2007). There are, however, several reports of actively
moving sperms inside the frontal organ of various taxa,
for instance, in two species of Macrodasys (Ruppert
1978a), in two species of Crasiella (Guidi et al. 2011),
in Dinodasys mirabilis (Todaro et al. 2012a), or in Neo-
dasys chaetonotoideus (own unpublished observation).
The configuration with one giant or several small mito-
chondria plus a well-developed axoneme also suggests
activity in flagellated spermatozoa of the Gastrotricha.
Whether sperm movement is already used during inse-
mination or just to reach the mature egg via the internal
pore of the frontal organ remains unclear. However, the
rich muscular assembly of the caudal organ or parts of
the sperm ducts, its absence in the frontal organ in many
species and the numerous observations of sperm activity
inside the frontal organ lumen (see Balsamo etal. 1999)
might account for the latter possibility. However, the
factor that activates sperm movement is still unknown
(Balsamo etal. 1999). Ruppert (1991) hypothesizes that
the spiral shape of most spermatozoa of the Macrodasy-
ida translates the beating action of the flagellum into a
rotation of the whole sperm. This could facilitate move-
ments of the sperm cell through the tissue or narrow
ducts. As opposed to the flagellated sperm, the aberrant
sperm cells without any flagellum in freshwater Pauci-
tubulatina are definitely unable to perform active move-
ments. The process how these immobile germ cells could
be transferred from one specimen to the reproductive
partner during cross fertilization, if happening at all, is
still obscure (e.g., Balsamo etal. 1999, Hummon 1986,
Weiss 2001). As already mentioned, some Macrodasy-
ida, e.g., species of Dolichodasys, and perhaps species
of Dactylopodola, possess non-flagellated sperm, too
(Fischer 1996, Ruppert & Shaw 1977). However, those
animals exhibit, like Dolichodasys carolinensis (Ruppert
& Shaw 1977), a muscularized caudal organ that is pro-
bably used for transferring the immobile sperm cells
to the mating partner. In Dactylopodola baltica and D.
typhle, male gametes are exchanged via spermatophores
(Kieneke etal. 2008d, Teuchert 1968).
1.2.10.2Spermatogenesis and spermiogenesis
The formation and differentiation of male germ cells
generally involve two consecutive developmental pro-
cesses, i.e., (1) spermatogenesis and (2) spermiogenesis
(=spermatohistogenesis) (see Gilbert & Singer 2006).
During spermatogenesis, a spermatogonion (diploid)
matures into a primary spermatocyte I (still diploid). This
cell undergoes the first meiotic division and becomes two
secondary spermatocytes II (haploid but sister chromatids
still united) and the second meiotic division leads to four
spermatids (haploid and sister chromatids separated).
Spermiogenesis is the cytomorphological process that
matures spermatids into ripe spermatozoa through severe
cellular transformations.
Early reports of sperm cell formation within Gast-
rotricha based on light microscopic observations
were made by Remane (1936) for Oregodasys (former
Platydasys), Ruppert & Shaw (1977) for Dolichodasys
carolinensis, or Ruppert (1978b) for several species of
the Thaumastodermatidae. In detail and based on TEM
studies, spermatogenesis has only been studied in the
marine macrodasyidan species Turbanella cornuta
(Teuchert 1976b, 1977a) and in the freshwater-dwelling
paucitubulatinan Lepidodermella squamata (Hummon
1984b). Some more general data concerning spermato-
genesis is meantime available for additional species,
e.g., for Acanthodasys aculeatus, Lepidodasys sp.,
Dinodasys mirabilis, Crasiella diplura, or Urodasys ano-
rektoxys (Balsamo etal. 2007, Guidi etal. 2003b, 2004,
2011, Todaro etal. 2012a). Furthermore, there is some
fragmentary data of spermatogenesis in Dactylopodola
typhle and in Neodasys chaetonotoideus (Kieneke etal.
2008d, 2009). In T. cornuta, presumably most species
of the Macrodasyida, spermatogenesis proceeds in
the germinal epithelium caudofrontally, i.e., from the
distal to the proximal pole of the testis (Fig. 1.42 A).
Such a caudocephalic maturation of male germ cells
has impressively been demonstrated for Lepidodasys
sp. (see image 3B in Guidi etal. 2004) and is assumed
to represent the ancestral mode of spermatogenesis
(see chapter Reproductive Organs). However, sperma-
togenesis may also proceed in the opposite direction
as in Urodasys anorektoxys (Balsamo etal. 2007). Since
spermatogonia and primary spermatocytes are difficult
to distinguish even at the ultrastructural level, Teu-
chert (1976b) simply described spermatogonial stages
A–D of Turbanella cornuta, whereas stage A probably
represents spermatogonia and stage D the early sper-
matids before spermiogenesis starts. In T. cornuta and
other species of the Macrodasyida (see, e.g., Kieneke
etal. 2008d for Dactylopodola typhle; Fig. 1.37 E), the
germinal epithelium consists of two or more layers of
spermatogonial cells. Stage A cells in T. cornuta are
characterized by big and active nuclei (regularly distri-
buted euchromatin) and numerous free ribosomes. In
stage B cells, electron-dense vesicles of 0.3 µm diameter
and unknown origin and function appear. Stage C cells
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1.2Morphology 71
A
B
vd
cc
ge
spermatogenesis spermio-
genesis
gp
tl
tl
frontal
caudal
Fig. 1.42: Spermatogenesis and spermiogenesis of Gastrotricha.
(A) Schematic horizontal section of testes in Turbanella cornuta
(Macrodasyida) indicating direction of spermatogenesis (gray
arrow) and spermiogenesis (black arrows) (B) Diagrammatic
spatial arrangement of the 16 spermatids (gray ovals)
within a spermatogenic cyst of Lepidodermella squammata
(Paucitubulatina). Observed (black lines) and assumed (broken
lines) cytoplasmatic bridges between spermatids are indicated.
Abbreviations: cc, cap cells of unknown function; ge, germinal
epithelium; gp, male genital pore; tl, testicular lumen; vd, vas
deferens. (A, Original according to data in Teuchert 1976b; B,
according to Hummon 1984b.)
are characterized by patterns of maturing divisi-
ons (condensed chromosomes, absence of nuclear
envelop) and cytoplasmic bridges between adjacent
cells. Stage D cells, spermatids, are characterized by
rounded nuclei with central condensed and reticulate
chromatin, peripherally electron-lucent nucleoplasm,
voluminous and active Golgi apparatus, numerous
mitochondria, and beginning formation of the flagel-
lum (Teuchert 1976b). Investigations of further species
support this scenario (see Balsamo et al. 2007, Guidi
etal. 2003b, 2004, Todaro etal. 2012a). Although only
fragmentary data are available, spermatogenesis in
Dactylopodola typhle seems to be different than in other
macrodasyidan species. Dozens of spermatids are com-
bined in a common cyst (Kieneke etal. 2008d). This is
far more than a number of four spermatids that would
result from meiosis of one primary spermatocyte.
As opposed to spermatogenesis, spermiogenesis
has been studied thoroughly in several species of the Mac-
rodasyida: Turbanella cornuta (Teuchert 1975b, 1976b, Fig.
1.43 A–H), Cephalodasys maximus (Fischer 1994), Acan-
thodasys aculeatus (Guidi etal. 2003b), Lepidodasys sp.
(Guidi etal. 2004), Urodasys anorektoxys (Balsamo etal.
2007), Crasiella diplura (Guidi et al. 2011), and Dinoda-
sys mirabilis (Todaro et al. 2012a). Spermiogenesis is a
complex cytomorphological process and can involve
up to five steps as in the species Cephalodasys maximus
(Fischer 1994). Spermiogenesis usually proceeds from
the periphery of the testis toward the lumen (centripetal
direction, Guidi etal. 2011), where mature spermatozoa
are densely stocked (Fig. 1.42 A). Generalized and sim-
plified, spermiogenesis in macrodasyidan gastrotrichs
takes place as simultaneous acrosome (pro-acrosome)
formation and growth of the flagellum. Both structu-
res protrude parallel into the testicular lumen, hence
giving the developing spermatid a characteristic U-shape
(Figs. 1.42 A and 1.43 C). This was hypothesized as a
common feature, an autapomorphy of the Macrodasyida
(Balsamo et al. 2007). During early (pro-)acrosome and
flagellum formation, the nucleus also starts to grow out
and follow the elongating and more and more twisting
acrosome (Fig. 1.43 A, C). Several small mitochondria may
follow the elongating nucleus and later fuse to form a
single giant mitochondrion enclosed by the nuclear helix
as in Turbanella cornuta (Teuchert 1975b, 1976b, Fig. 1.43
A, C, E) or Acanthodasys aculeatus (Guidi etal. 2003b).
However, it is also possible that a single mitochondrion at
the base of the elongating nucleus starts to project into it
like in Cephalodasys maximus, further mitochondria from
the spermatid may later fuse with the initial one (Fischer
1994). Spiralization of the acrosome-nuclear complex
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72 1Gastrotricha
generally seems to begin at the apex of the spermatid
appendage that contains pro-acrosome and elongating
nucleus. During the profound cytomorphological trans-
formations of spermiogenesis such as elongation, shifting
of organelles and spiralization of the acrosome-nuclear
complex, microtubules seem to play an important role. In
stage C of spermiogenesis of Cephalodasys maximus, for
instance, the acrosome-nuclear complex is enclosed by a
cuff of circular (helically?) arranged microtubules (Fischer
1994). Helically arranged microtubules encircle nucleus
and mitochondrion during spermiogenesis of Turbanella
cornuta but are absent in mature spermatozoa (Teuchert
1975b, 1976b, Fig. 1.43 B, D, G). Microtubules also occur
during formation of the nucleus-mitochondrion complex
in Crasiella diplura (Guidi etal. 2011). Comparably, micro-
tubules surround the rod-shaped nucleus in spermatids
of Lepidodermella squamata at the beginning of spermio-
genesis but disappear later (Hummon 1984b, see below).
The last step of spermiogenesis in macrodasyidan Gastro-
tricha is characterized by severe reduction of cytoplasm of
the late spermatid. Because lysosomes and peroxisomes
are frequently observed during that stage, it is hypothe-
sized that reduction of cytoplasm happens by autolysis
and reabsorption (Guidi et al. 2003b). In species such
as Urodasys anorektoxys or Dinodasys mirabilis, it is also
possible that residual bodies are formed from the debris
of the late spermatid (Balsamo etal. 2007, Todaro etal.
2012a). An interesting mode of metabolic recycling of
those residual bodies is reported from U. anorektoxys. In
that species, several macrophages per testis remove the
residual bodies (Balsamo etal. 2007).
Sperm cell formation, i.e., spermatogenesis and
spermiogenesis, was intensely studied by Hummon
(1984b) in the freshwater paucitubulatinan species Lepi-
dodermella squamata. She distinguished four stages of
sperm rod formation, spermatogenesis (until early sper-
matids) happens during stages 1 and 2 and spermioge-
nesis (until mature sperm rods) is covered by stages 2, 3,
and 4. Four spermatogonia are connected by cytoplasmic
bridges and characterized by fibrillar nuclear content;
two developing cyst cells may already be present at that
stage. Using the resolving power of the TEM, Hummon
(1984b) was able to identify possible precursor cells of
the four spermatogonia in specimens with temporally
uneven development at both sides of the body. In later
specimens, primary spermatocytes could unequivo-
cally be identified through the presence of synaptone-
mal complexes that are diagnostic for pachytene of first
maturing division of meiosis (Fig. 1.37 F). Afterward, a
cluster of 16 intertwined cells connected by cytoplasmic
bridges (Fig. 1.42 B) and enclosed within a cyst made
1 µm
0.5 µm
1 µm
A
B
C
D
er
E
F
G
mt
pa
go
np
fv
cs
dc
ci
mi
cl
H
nu
np
er
mi mt
mi
nu
ci
mi
nu
w
nu
ad
sb
ad
aarncrfpr
cl
nu
Fig. 1.43: Ultrastructure (schematic) of spermiogenesis in
Turbanella cornuta (Macrodasyida). Gray arrows indicate
direction of development. (A and B) Spermatid in an early stage
of spermiogenesis. Nucleus and acrosome start to elongate
and numerous small mitochondria are scattered along nucleus.
(C and D) Spermatid in a late stage of spermiogenesis. Cilium
(flagellum) has grown into testicular lumen and nucleus and
giant mitocjondrion are already spiraled. Note the microtubules
surrounding the mitochondrion-nuclear complex in B and D. (E–H)
Mature spermatozoon. (A, C, and E) Longitudinal sections. (B, D, and
F–H) Cross sections. Abbreviations: aar, anterior acrosomal region;
ad, acrosomal discs (alternating light and dense discs); ci, cilium
(flagellum); cl, clasp-like structure; cs, connecting structure between
basal body and flagellum; dc, distal centriole (basal body); er,
endoplasmic reticulum; fpr, flagellar distal region; fv, flagellar vacuole;
go, Golgi cisterns; mi, mitochondrion; mt, microtubules; ncr, nuclear
central region; np, nuclear plasm; nu, nucleus; pa, pro-acrosome; sb,
spiraled band; w, “wall” of acrosome. (Modified from Teuchert 1976.)
of three cells represent the spermatids of L. squamata.
Each spermatid already possesses an electron-dense,
rod-shaped nucleus, and the cytoplasm and organelles
begin to reduce (inactive Golgi complexes, only a thin
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1.2Morphology 73
spermatids follow a regular pattern (see Fig. 1.42 B). In
slightly older individuals, spermiogenesis has finished
and 16 rod-shaped, 7- to 8-µm-long sperm cells, just
consisting of rod-shaped condensed nucleus with sur-
rounding cell membrane and one large residual body
layer of cytoplasm around one pole of nuclear rods),
while mitochondria and multivesicular bodies are still
numerous in some regions (Hummon 1984b). The rod
shaped nucleus of late spermatids is surrounded by up
to 10 microtubules, the cytoplasmic bridges between
2 µm
1 µm 2 µm1 µm1 µm
1 µm
2 µm
AB
C D
*
*
EGF
ac
nu
sc
wi
nu
pc
nu
ac
wi
nu
mi
ph cs ac
nu
mi
Fig. 1.44: Ultrastructure (TEM micrographs) of the spermatozoa of Gastrotricha. (A) Neodasys ciritus (Multitubulatina). Longitudinal and
cross sections of some spermatozoa within the testis. (B) Longitudinal and cross sections of developing sperm cells within the testis of
N. chaetonotoideus. Note the different ultrastructure of the acrosome compared to N. ciritus. (C–E) Longitudinal sections of spermatozoa
of Acanthodasys aculeatus (Macrodasyida). (C) Acrosomal region. (D) Nuclear region. (E) Flagellar region (cilium). (F and G) Longitudinal
sections through 1 testis of Paraturbanella teissieri (Macrodasyida). (F) Overview with several longitudinally sectioned spermatozoa.
(G) Close-up of some sperm cells showing the helically arranged nuclear-mitochondrial complex, the acrosome, and the twisted flagellum.
Note the electron-dense structure that connects the flagellum with the nucleus (asterisk). Abbreviations: ac, acrosome; cs, clasp-like
structure; fl, flagellum (cilium); mi, mitochondrion; nu, nucleus; pc, proximal centriole; ph, perinuclear helix; sc, striated cylinder; wi, wig
of filaments. (Micrographs in A and C–G were kindly provided by Maria Balsamo and Loretta Guidi, Urbino.)
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74 1Gastrotricha
outer layer consists of fibrous material, too, but without
apparent orientation and with flocculent material dis-
persed among fibers (Rieger & Rieger 1980). Comparably,
in Dactylopodola baltica, the inner layer of the mature
egg envelope is fibrous and the outer layer consists of
electron-dark filaments. However, these are covered by a
membrane-like structure (Fischer 1996). Microscopically,
the eggshell surface of species of Macrodasyida appears
smooth and is uniformly sticky (Rieger & Rieger 1980,
Ruppert 1991). It may additionally be provided with a
thick covering of glutinous secretion, which may be pro-
duced by secretory cells of the epidermis or the uterus
wall (Teuchert 1968) or by the recently described posterior
gland organ in Dinodasys mirabilis (Todaro etal. 2012a).
This adhesive covering enables the animals to stick the
spawned eggs to the substratum such as sand grains
(Hummon & Hummon 1983a). In species of the Paucitubu-
latina, the ultrastructural composition of the inner layer
of the eggshell is fibrous, too. The outer eggshell layer
displays a more homogenous and electron-dense texture
(Rieger & Rieger 1980). The inner eggshell stratum of eggs
of Lepidodermella squamata is described as a continuous
layer of poorly stained material with a narrow dense outer
layer that forms numerous dense caps (Hummon 1984a).
It is the outer layer of the eggs of paucitubulatinans that
may exhibit eggshell sculpturing of various shapes (e.g.,
Figs. 1.45 A–C and 1.46 C–F) such as tiny spinelets, humps,
spines, or pillars, but eggshells may also be smooth
(Remane 1936, Hummon & Hummon 1983a, Ruppert
1991). Furthermore, taxa like Aspidiophorus, maybe most
paucitubulatinans possess a sticky attachment stalk at
their eggs (Rieger & Rieger 1980). As those eggs are not
uniformly sticky as the eggs of Macrodasyida, the attach-
ment stalk is used to adhere the spawned egg to the
are placed within a cyst made of three cells. The residual
body, up to 5 µm in diameter, contains presumptive cell
debris (e.g., multivesicular bodies, various membranes,
lysosomes) and disappears later. The whole process of
sperm formation (spermatogenesis plus spermiogenesis)
starts after deposition of the last parthenogenetic egg
and lasts only 1 day (Hummon 1984b). Almost nothing
is known about spermatogenesis and spermiogenesis
in more basal, hermaphroditic taxa of the Paucitubula-
tina such as the Xenotrichulidae. In juvenile specimens,
there are no traces of developing sperm cells but they
are suddenly present in mature animals (Hummon &
Hummon 1983b). This may point to a rather rapid sperm
development in those groups.
A process that might precede spermatogenesis is
mitotic proliferation of spermatogonia by ongoing cell
divisions within the germinal epithelium. Such a process
within Gastrotricha has only been reported for Oregodasys
cf. ocellatus (Ruppert 1978b, Balsamo etal. 1999). However,
in Turbanella cornuta and Dactylopodola baltica a repeated
alteration of male and female phases during a life span is
described (Teuchert 1968). It is possible that mitotic proli-
feration at least of the male germ cells is involved in such
an alternating and “phase-delayed” hermaphroditic repro-
duction mode (Hummon & Hummon 1983b, Balsamo etal.
1999). If mitotic proliferation within the testes of hermaph-
roditic gastrotrichs is a common process, long time assumed
cell constancy and eutely of Gastrotricha must be restricted
to the somatic cell line only (Balsamo etal. 1999). However,
as regeneration capacity was demonstrated in Turbanella
sp., which must involve mitotic activity of somatic cells
(Manylov 1995), the idea of eutely in Gastrotricha, at least in
Macrodasyida, has to be questioned in general.
1.2.10.3Eggs
Mature eggs of Gastrotricha may be small spheres with
a diameter of 35–45 µm but are predominantly ovals of
up to 60×120 µm (Teuchert 1968, Rieger & Rieger 1980)
(Fig. 1.36 A, D, E). Mean dimension for most taxa, however,
is an oval of 40×60 µm (Hummon & Hummon 1983a). Both
Macrodasyida and Chaetonotida have eggs with a well-
differentiated eggshell being stratified into two different
layers (Rieger & Rieger 1980, Hummon 1984a, Ruppert
1991). In species of the Macrodasyida, both layers consist
of fibrous material, whereas the innermost maybe orga-
nized into crossed fibers such as in Turbanella ocellata
(Rieger & Rieger 1980) or in T. cornuta (Ruppert 1991). The
A
BC
Fig. 1.45: Different egg shapes of freshwater Paucitubulatina.
Drawings not in scale, diameter of eggs vary between 50 and 75 µm.
(A) Egg of Chaetonotus maximus. (B, C) Eggs of 2 other species of
Chaetonotus. (A–C, According to Remane 1936.)
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1.2Morphology 75
40 µm
10 µm
5 µm 80 µm
35 µm
5 µm
AB
C
DE
ph
F
ph
Fig. 1.46: Egg types of Paucitubulatina.
(A and B) Aspidiophorus polystictos.
(A) Subitaneous egg (tachyblastic egg)
with an embryo inside that has finished
embryogenesis. (B) Surface of the egg shell
with a fine granulation. (C–F) Chaetonotus
sp. (C) Subitaneous egg with an embryo
inside. (D) Surface differentiation of a
subitaneous egg with pillar-like structures.
(E) Close-up of the egg shell. (F) Pillar-like
structures of a resting egg (opsiblastic
egg). (A, C) DIC images. (B and D–F) SEM
micrographs. Abbreviation: ph, pharynx
of the embryo. (All images were kindly
provided by Maria Balsamo & Loretta Guidi,
Urbino.)
substratum (Ruppert 1991). The eggs of the Paucitubula-
tina show even more structural diversity: during their par-
thenogenetic phase, paucitubulatinan gastrotrichs like
Lepidodermella squamata (Hummon 1984a) produce sub-
itaneous eggs (so-called tachyblastic or quick developing
eggs according to Brunson 1949; Fig. 1.46 A–C) and resting
eggs (so-called opsiblastic or late developing eggs accor-
ding to Brunson 1949). Both egg types may be structurally
different within the same species, resting eggs being gene-
rally more heavily sculptured and with a darker egg shell
(Hummon & Hummon 1983a). It is worth mentioning that
resting eggs are of high ecological and biogeographical
value because they facilitate the species to outlast periods
of unfavorable environmental conditions like dry or cold
seasons (Strayer & Hummon 1991). Furthermore, resting
eggs may represent important indirect dispersal propagu-
les (Strayer & Hummon 1991, Artois et al. 2011). A third
morphological egg type, the “plaque-bearing egg” (see
Fig. 1.49), is reported in Lepidodermella squamata that
possibly represents a fertilized egg (Levy & Weiss 1980,
see also Hummon & Hummon 1983a, Strayer & Hummon
1991, Balsamo 1992). Apart from some information on
oogenesis and vitellogenesis of Neodasys chaetonotoi-
deus (Kieneke etal. 2009), there does exist no more data
on the ultrastructure of mature eggs and the eggshell in
Neodasys/Multitubulatina.
1.2.10.4Oogenesis
It has been discussed controversially if the ovaries of Gast-
rotricha are real ovaries because according to Hummon &
Hummon (1983a) real ovaries are organs were primordial
germ cells (oogonia) produce oocytes by mitotic prolifera-
tion (see also Ruppert 1991 for this issue). There are diffe-
rent reports of cell division patterns within the proximal
part of the female gonads in several macrodasyidan gast-
rotrich species (e.g., Rieger etal. 1974: Chordodasiopsis
antennatus, Ruppert & Shaw 1977: Dolichodasys carolinen-
sis, Ruppert 1978a: Macrodasys sp., Ruppert 1978b: Ore-
godasys cf. ocellatus and Acanthodasys thrinax). However,
it is not clear whether these patterns represent mitotic
or meiotic activities (see Hummon & Hummon 1983a,
Ruppert 1991). The only certain instance of mitotic activity
is known in the ovary of post-parthenogenic specimens of
the freshwater paucitubulatinan species Lepidodermella
squamata (Hummon 1984c).
Apart from the aforementioned issue, oogenesis
was ultrastructurally studied in different species of the
Gastrotricha, most comprehensively in the marine her-
maphrodites Turbanella cornuta (Teuchert 1977a) and
Dactylopodola baltica (Fischer 1996) and in the parthe-
nogenetic freshwater species Lepidodermella squamata
(Hummon 1984a). Further data concerning oogenesis are
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76 1Gastrotricha
available for the macrodasyidan species Dactylopodola
typhle (Kieneke et al. 2008d), Crasiella diplura (Guidi
etal. 2011), Dinodasys mirabilis (Todaro etal. 2012a), and
for Neodasys chaetonotoideus (Kieneke etal. 2009). Early
female germ cell development in hermaphroditic gast-
rotrich species definitely proceeds by meiosis because
the occurrence of condensed chromosomes and synap-
tonemal complexes, diagnostic for synapsis during lep-
totene or zygotene of meiosis I, is frequently observed
(e.g., Teuchert 1977a: Turbanella cornuta, Fischer 1996:
Dactylopodola baltica). In the freshwater-dwelling gast-
rotrich Lepidodermella squamata, oogenesis leads to par-
thenogenetic eggs. Because patterns of meiosis (neither
condensed chromosomes nor synaptonemal complexes)
were never discovered in parthenogenetic individuals
during intensive ultrastructural studies using TEM, it
is hypothesized that diploid parthonegenetic eggs are
produced by apomixis in L. squamata (Hummon 1984a,
Ruppert 1991, Balsamo 1992).
Generalized, egg development in Gastrotricha invol-
ves three major successive stages prior to spawning:
growth, vitellogenesis, and egg shell formation. Young
oocytes have a rather big and active nucleus with regu-
larly scattered heterochromatin, almost no condensed
chromatin and a distinct nucleolus (Fig. 1.47 A). Within
the cytoplasm, mitochondria, free ribosomes, and
rough endoplasmic reticulum are present as in Lepido-
dermella squamata, Turbanella cornuta, or Dactylopo-
dola baltica (Teuchert 1977a, Hummon 1984a, Fischer
1996). Besides mitochondria and electron-lucent vesic-
les, Kieneke et al. (2008d) report a high quantity of
small electron-dense granules in early oocytes of Dac-
tylopodola typhle, supposedly glycogen. In early stages
of oogenesis, the centriole pair may be present like
in the young egg cells of Lepidodermella squamata or
Dactylopodola baltica (Hummon 1984a, Fischer 1996).
Next, developing oocytes continuously migrate toward
the distal uterus region. The direction of this migration
may be directed frontally or caudally, depending on the
anatomy of the female gonads (see chapter Reproduc-
tive Organs). In species with paired ovaries, maturing
eggs alternately originate from the left and the right
gonad such as in Lepidodermella squamata and Dacty-
lopodola baltica (Hummon 1984a, Fischer 1996). During
5 µm
5 µm2 µm
A
BC
*
mo
tes
ov
mg
nu
tes
tes
tes
mo
cu
lm
er
*
mg
mo
ed
ed
cu
mo
Fig. 1.47: Ultrastructure (TEM micrographs)
of the oocytes of Gastrotricha. (A) Cross
section through the trunk of Xenotrichula
carolinensis (Paucitubulatina). Paired
testes and ovaries in a lateral position.
Maturing eggs lie in close proximity to the
midgut. The large egg on the right side is
still growing while that on the left already
has different types of granules and vesicles.
Note the rather big nucleus and nucleolus
(asterisk) of the growing egg. (B) Cross
section through the trunk of Diuronotus
aspetos with a mature egg and spermatozoa
within the testis. Note the different types of
granules within the egg. (C) Cross section
of the uterus of Neodasys chaetonotoideus
(Multitubulatina). The maturing egg lies in
close contact to gut cells. Vitellogenesis
has initiated as can be seen by the
numerous electron-dark granules. Note the
active nucleus with prominent nucleolus
(asterisk). Abbreviations: cu, cuticle;
ed, epidermis; er, endoplasmic reticulum;
lm, longitudinal muscle; mg, midgut;
mo, mature/maturing oocyte; nu, nucleus;
ov, ovary; tes, testes. (Micrograph B was
kindly provided by Maria Balsamo and
Loretta Guidi; Urbino; micrograph C, from
Kieneke etal. 2009, with kind permission
by Wiley.)
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1.2Morphology 77
this phase, the eggs grow considerably, for instance,
six to eight times their original size like in T. cornuta
(Teuchert 1977a). In Lepidodermella squamata, the egg
cytoplasm grows several thousands of times, whereas
its nuclear volume still enlarges by a factor of several
hundreds (Hummon 1984a). Gastrotricha have a remar-
kably high ratio of egg and whole animal biomass,
which means that they invest considerably high energy
and matter into offspring. In gravid specimens of many
species of the Paucitubulatina, for instance, length of
the mature egg may encounter more than half of the
whole animal. With such a size ratio, eggs of Paucitu-
bulatina display the comparatively biggest eggs among
Metazoa (Remane 1936).
During the growing phase of the premature eggs,
vitellogenesis begins. Mitochondria, Golgi complexes,
and free ribosomes are very abundant within the cyto-
plasm during vitellogenesis, and the nuclear envelope
may display distinct nuclear pores (Teuchert 1977a,
Hummon 1984a). Furthermore, different inclusions of
varying sizes (ranging around 0.5 µm), textures, and
electron-transmissibility become visible within the cyto-
plasm (Fig. 1.47 B, C). Those structures are interpreted
as lipid droplets and yolk granules (e.g., Teuchert 1977a,
Ruppert 1978b, Rieger & Rieger 1980, Hummon 1984a,
Fischer 1996, Kieneke et al. 2008d, 2009, Guidi et al.
2011). Fully mature eggs are densely packed with those
rest substances. In most gastrotrich species, vitelloge-
nesis is brought about by autosynthesis of the egg cell
itself, as no nurse cells, follicle cells, or yolk contributing
cells have been observed (Hummon & Hummon 1983a).
However, a possible exception to this is reported later.
Molecular components for yolk and other rest substance
production must be transported from the gut cells to the
oocytes via the intercellular space like in Lepidodermella
squamata (Hummon & Hummon 1983a) or via direct cel-
lular connections of gut cells with the oocyte like in Tur-
banella ocellata (Rieger & Rieger 1980). The latter mode
of nutrient supply for the developing eggs was already
assumed by Wilke (1954). In L. squamata, where no ovary
wall epithelium is present, the egg plasma membrane
facing the gut epithelium forms deep invaginations into
the egg cytoplasm. These so-called vitellogenic channels
facilitate a rapid transcytotic transport of substances
from the gut cells via the intercellular space deep into the
maturing oocytes (Hummon & Hummon 1983a). Another
evidence of direct nutrient supply of the developing eggs
by gut cells comes from TEM investigations of Neodasys
chaetonotoideus. Early, pre-vitellogenic eggs lie in direct
contact with the gut cells, only separated by a narrow
intercellular cleft filled with ECM. The egg itself forms
lateral extensions that enwrap the gut thereby enlarging
the contact surface (Kieneke etal. 2009). This obviously
facilitates a better exchange of substances. However,
this peculiar species also offers a second mode of vitel-
logenesis. More distally in the ovary, a wall epithelium
completely surrounds the developing egg. In this region
of the so-called vitellogenic oviduct, the epithelial cells
form protuberances that deeply invaginate into the
oocyte and also constrict small spheres that may later
become the yolk granules of the mature egg (Kieneke
etal. 2009). A comparable situation may be present in
further species of the Gastrotricha. For instance, cross
sections of Thaumastoderma sp. demonstrated a com-
plete epithelial lining around the developing oocyte,
which forms an invagination into the ventral side of the
egg (Ruppert 1978b, Hummon & Hummon 1983a). Also,
Teuchert (1977a) reports “thin processes of the ovarian
wall epithelium that stretch in between single oocytes”
in Turbanella cornuta. Furthermore, Remane (1934, 1936)
describes nutritive cells in close adjacency to the ovaries
of Paradasys subterraneus. If all the aforementioned
structures and formations are actually involved in vitel-
logenesis and nutrient supply of the growing eggs needs
further exploration.
The final stage of oogenesis in Gastrotricha is the
formation of the egg shell. Eggshell formation still
takes place inside the gravid animal and was intensely
investigated in two marine species (Turbanella ocellata,
Macrodasyida, and Aspidiophorus sp., Paucitubulatina)
by Rieger & Rieger (1980) and in the freshwater-dwel-
ling paucitubulatinan species Lepidodermella squa-
mata (Hummon 1984a). The formation of the eggshell
in Gastrotricha occurs in late-vitellogenic eggs and is
possibly initiated by sperm penetration in hermaphro-
ditic species (Rieger & Rieger 1980). Eggshell precursor
vesicles occur inside the vitellogenic oocyte (Rieger &
Rieger 1980, Hummon & Hummon 1983a), in later stages
in close proximity to the cellular membrane (Hummon
1984b). There is evidence that eggshell vesicles are pro-
duced and processed by the rough endoplasmic reti-
culum and the Golgi complexes of the oocyte. As the
content of vesicles is quite comparable with the fini-
shed eggshell regarding its texture or even shape (small
spinelets inside the vesicles that resemble the spinelets
of the eggshell), it is assumed that they are transpor-
ted to the surface and fuse with the cellular membrane
of the egg. Thereby, content of the eggshell precur-
sor vesicles is deposited to the exterior (Hummon &
Hummon 1983a). During spawning, eggs of Gastrotricha
from both major subtaxa (Macrodasyida and Paucitubu-
latina) are reported to be highly flexible and virtually
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78 1Gastrotricha
“flow out” when passing the female gonopore or rup-
tured body wall (Teuchert 1968, Hummon & Hummon
1983a). This implies that also the eggshell must be quite
flexible because it is already formed within the gravid
animal (see above). A hardening of the eggshell begins
immediately after spawning when the egg is deposited
to the substratum. Hardening continues throughout
embryonic development (Hummon & Hummon 1989).
The hardening process might possibly be induced once
the eggshell gets into contact with the surrounding
medium, i.e., seawater, brackish water, or freshwater.
Although each of the paired female gonads of the
freshwater inhabiting Lepidodermella squamata (Paucitu-
bulatina) contains eight oocytes, only four, rarely five or
six parthenogenetic eggs are matured and spawned (Levy
& Weiss 1980, Hummon & Hummon 1983a, 1993). Most fre-
quently, the last parthenogenetic egg is a resting (opsiblas-
tic) egg (Hummon & Hummon 1983a, Hummon 1984a, see
also chapter Reproductive Biology). In a marine species of
Chaetonotidae, Aspidiophorus polystictos, usually three
to six parthenogentic eggs are produced (up to 10) before
the animals become hermaphrodites (Balsamo & Todaro
1987, Hummon & Hummon 1993). Parthenogenetic resting
eggs generally start to develop after a certain period of
dormancy. However, it is not known which factor exactly
triggers the production of and hatching from resting eggs
in Gastrotricha (Hummon & Hummon 1983a, Balsamo
1992). In post-parthenogenic specimens of L. squamata,
the remaining cells of the female gonad undergo limited
mitotic proliferation. Although some of the resulting
secondary oocytes develop into secretory cells that later
fuse to a secondary syncytium and build up the so-called
X-body of unknown function, others may develop into
eggs that are finally spawned. However, those secondary
eggs do not undergo proper cleavage in laboratory cultures
(Hummon 1984c). Regarding the Macrodasyida, there is no
knowledge how many eggs are produced and laid during
a lifetime of any species (Hummon & Hummon 1983a).
An indirect estimate for this could be the observed total
number of oocytes present inside the ovary. For instance,
Fischer (1996) depicts 12 oocytes per lateral gonad of Dac-
tylopodola baltica, in D. typhle, approximately 15 germ
cells per female gonad are reported (Kieneke etal. 2008d),
and in Crasiella diplura only four to five cells (Guidi etal.
2011). However, it is still under debate whether mitotic pro-
liferation of oocytes occurs in the gonads of hermaphrodi-
tic gastrotrichs (see beginning of this section). If true, this
could possibly mean that numeric egg production is much
higher than the aforementioned numbers. Such a scenario
may also match the expected lifetime of macrodasyidan
gastrotrichs, assumed to last between 6 and 12months
(Artois etal. 2011). However, exact life expectancy of spe-
cimens in wild populations has never been determined so
far (Hummon & Hummon 1992). What is definitely known
in some species is the number of laid eggs at a time. This
ranges between a single egg as in Lepidodermella squa-
mata and species of Cephalodasys and Mesodasys, occasi-
onally two as in Turbanella, Dactylopodola, and Urodasys,
and up to eight eggs laid at a time like in species of Macro-
dasys (Teuchert 1968, Hummon & Hummon 1983a).
1.3Reproduction and development
1.3.1Reproductive biology
We are at an initial stage of understanding the repro-
ductive biology of the predominantly hermaphroditic
gastrotrich taxa Macrodasyida and Neodasys. One phe-
nomenon related with hermaphroditism in both taxa is
the chronology of maturation of both sexes in the same
individual. Generally, macrodasyidan gastrotrichs may
be protandrous or simultaneous hermaphrodites or may
display an alteration of sexual phases (Balsamo 1992).
Teuchert (1968) already identified different chronologies
of sexual maturation: species such as Macrodasys cau-
datus, Urodasys mirabilis, Mesodasys laticaudatus, Acan-
thodasys aculeatus, and Cephalodasys maximus are true
simultaneous hermaphrodites with only a slightly earlier
development of the male gonads. The mode of simulta-
neous hermaphroditism is also present in Neodasys cha-
etonotoideus (Kieneke etal. 2009). Urodasys cornustylis
and U. spirostylis are clearly protandrous hermaphrodites
that show a much earlier maturation of the testes and the
male caudal organ before maturing oocytes are visible
and before the animals have been grown up to their full
length (Schoepfer-Sterrer 1974, Hummon & Hummon
1992). Meanwhile, species such as Dactylopodola baltica
and different species of Turbanella are reported to be
protandrous species with a following multiple alteration
of each sex (Remane 1936, Teuchert 1968, Hummon &
Hummon 1992). In Turbanella, both sexes may tem-
porally overlap in a single individual while D. baltica
either is in a male or in a female stage. Both examples
of protandry with following alteration of sexes, termed
“sequential hermaphroditism”, according to Hummon
& Hummon (1992), furthermore indicate a certain tem-
poral synchrony in reproductive activity within the
same population (Teuchert 1968). The possible presence
of an environmental factor for the control of such a
synchrony in wild populations is discussed by Hummon
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1.3Reproduction and development 79
behavior. This has in fact been investigated and documen-
ted in two species of the Macrodasyida. Teuchert (1968)
describes the copulation of Turbanella cornuta (see also
Hummon & Hummon 1992 for a review), a macrodasyidan
gastrotrich that has a frontal organ but obviously lacks a
caudal organ (but see the interpretation of Ruppert 1991
that is presented later). In this species, an individual in
the male stage lifts its caudum and performs pendulous
movements in order to touch a specimen in its female
stage ready to mate. Within a few seconds, the two indi-
viduals first form a loose, later a tight knot with their rear
trunks (see figure 2 of Teuchert 1968). Tightening the knot
is achieved by gluing to the substratum with the aid of
the batteries of anterior adhesive tubes and stretching the
trunks in opposite directions. At maximum 70 seconds
later, both animals release again. Based on the insuffici-
ent knowledge of the reproductive anatomy of T. cornuta
during that time, Teuchert (1968) was not able to clarify
satisfactorily how sperm transfer really happens. As
already mentioned, T. cornuta lacks a caudal organ as a
sperm-transferring device. Just the unpaired ventral male
gonopore of the fused sperm ducts can be used for insemi-
nation. The female gonopore of T. cornuta was assumed to
be situated on the ventral side close to the anus. However,
these anatomical conditions did not fit to the observed
copula because in neither stage did male and prospec-
tive female pores of the mating animals get into contact
(Teuchert 1968). Based on the well-known mating mecha-
nism of Macrodasys sp. (see below) and on the unpublis-
hed morphological data of Turbanella ocellata, Ruppert
(1991) reinterprets the mating and copulation in T. cornuta.
He suggests that there are in fact two accessory repro-
ductive organs in Turbanella, a frontal organ described
by Teuchert (1977a) as the “gland organ of the intestinal
region” with unknown function and a caudal organ close
to the anus. Hence, Turbanella would first have to charge
its own caudal organ like in Macrodasys before sperma-
tozoa are transferred from this organ to the frontal organ
of the mating partner (Ruppert 1991). The “gland organ of
the intestinal region” is a paired structure situated close
to the uterus region with the mature egg (Teuchert 1977a).
Kieneke et al. (2009) interpret this structure to be a so-
called cervix, an outlet duct for the mature and fertilized
egg (see also below). Such an interpretation still compli-
cates the issue of mating and sperm transfer in T. cornuta.
Further input to the mating and copulation in Turbanelli-
dae comes from a con-familiar species of T. cornuta, Para-
turbanella teissieri. This species has a frontal organ that
definitely has a dorsolateral opening. The presence of a
caudal organ, however, was rejected and therefore a copu-
lation by contact of the slightly protrudable ventral male
& Hummon (1992). However, other species of the same
genus may display a different chronology of sexual
maturity. For instance, Dactylopodola typhle might be a
simultaneous hermaphrodite (Kieneke etal. 2008d) like
the aforementioned species of Macrodasyida in contrast
to its congeneric D. baltica. Simultaneous hermaphrodi-
tism in D. typhle was already suspected by Wilke (1954),
who observed testes with spermatids in specimens of the
assumed female stage. It has to be stressed that the alte-
ration of sexes was purely deduced from the occurrence
of different size classes in Turbanella during the season
that have been either specimens in a more male or more
female stage (Teuchert 1968). Based on the observations
on a number of species from both Turbanella and Para-
turbanella, Balsamo etal. (2002) reject the occurrence of
sequential hermaphroditism at least for these two genera.
The definite presence of sequential hermaphroditism in
macrodasyidan Gastrotricha has to be confirmed urgently
by tracing specific individuals with a known life history
and individual age from laboratory cultures (Hummon &
Hummon 1992).
During her studies of the reproductive biology of
marine gastrotrichs from the North Sea, and the Baltic
Sea, Teuchert (1968) also noticed that species such as
Mesodasys laticaudatus, Macrodasys caudatus, Dactylo-
podola baltica, or Acanthodasys aculeatus were charac-
terized by a continuous reproductive activity during the
warm season with a peak from late summer to autumn.
However, a second group of species consisting of Cepha-
lodasys maximus and two species of Turbanella (T. hyalina
and T. cornuta) displayed two reproductive peaks, one
in spring and, isochronic to that of the aforementioned
species, a second during late summer to autumn (Teu-
chert 1968). Interestingly, a recent study focusing the
molecular diversity of Turbanella cornuta and T. hyalina
from the North Sea and Baltic Sea area gave evidence for
at least two sympatric cryptic species within original T.
hyalina (Kieneke etal. 2012). It is discussed whether the
two reproductive peaks of T. hyalina reported by Teuchert
(1968) could represent the reproductive maxima of in fact
two separate cryptic species.
Although explicitly studied and proofed in two instan-
ces only, all hermaphroditic species of the Macrodasyida
and Neodasys (Multitubulatina) that possess a set of two
accessory reproductive organs, i.e., the caudal organ plus
frontal organ or at least one of both structures, should
engage in mating and cross-insemination, during which
spermatozoa are transferred from one mating partner to
the other and vice versa. The mode of reciprocal sperm
transfer/cross-insemination with the aid of accessory
reproductive organs requires a certain kind of copulation
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80 1Gastrotricha
situated on the ventral surface of the animal. Once this
copula is established, own spermatozoa (autosperm) are
released from the testes and enter a posterior compartment
of the own caudal organ called the antrum feminimum (see
chapter Reproductive Organs). Owing to a severe bending
of the rear trunk within a knot of two animals, both sperm
duct openings are in close proximity to the ventral pore of
the caudal organ. Hence, spermatozoa may easily reach
the caudal organ after leaving the sperm ducts. From the
antrum feminimum, spermatozoa enter the own copula-
tory tube that already sticks inside the frontal organ of the
mating partner. Once the copulatory tube of each mating
animal is charged with autosperm, it breaks off from the
remaining tissue of the caudal organ (Fig. 1.48). Shortly
after, the mating animals release and glide away with their
frontal organs filled with foreign spermatozoa (allosperm)
and the copulatory tube from the partner (Ruppert 1978a).
The whole process of mating and copulation in Macrodasys
gonopore (common opening of fused sperm ducts like in
Turbanella and other Turbanellidae) and the dorsal pore
of the frontal organ (see, e.g., Fig. 1.34 A) of two animals
during mating is hypothesized to be the mode of copula-
tion in P. teissieri and other Turbanellidae (Balsamo etal.
2002).
Much better known in terms of reproductive biology
and anatomy is Macrodasys. Based on intensive histologi-
cal, SEM, TEM, and live observations of two undescribed
species, Ruppert (1978a) was able to fully reconstruct the
mating and copulation behavior and the structures and
morphofunctional processes involved in reciprocal sperm
transfer (see also Ruppert 1991, Hummon & Hummon 1992
and Balsamo 1992 for reviews on this issue). In this taxon,
two mating animals pair and copulate by reciprocally pro-
truding their tubular parts of the caudal organ (“copula-
tory tube”) into the frontal organ of the partner (Fig. 1.48).
Openings of both accessory reproductive organs are
A
B
C
D
E
F
testes
frontal organ
caudal organ & copulatory tube
antrum feminimum
spermatozoa
II
I
I
I
II
I
I
I
II
II
Fig. 1.48: Mating and reciprocal sperm
transfer in Macrodasys. For simplicity,
transfer is only displayed from one (I) to
the other specimen (II). Second animal (II)
drawn as a cross section at the level of its
frontal organ. (A) Simplified diagrammatic
reproductive anatomy of Macrodasys,
ovary omitted. For more details, see
Fig. 1.33 C. (B) Precopulatory behavior. The
copulatory tube is still invaginated.
(C) Attachment. Mating animals evert their
copulatory tubes into the frontal organ
of the partner. (D) Uptake of autosperm
into the caudal organ via the antrum
feminimum. (E) Reciprocal sperm transfer.
Spermatozoa move, probably by beating
action of their flagella, into the copulatory
tube. (F) Separation of mating partners.
(Modified from Ruppert 1978a, 1991 and
Hummon & Hummon 1992.)
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1.3Reproduction and development 81
occurs in just a few seconds (see figure 2 in Ruppert 1978a).
A quite differentiated behavior before and during the actual
copulation is allied with these morphofunctional processes
for reciprocal insemination in Macrodasys (Ruppert 1978a,
reviewed in Ruppert 1991 and Hummon & Hummon 1992).
Pre-copulatory actions may involve gregarious behavior of
animals as a kind of prelude to mating. However, gregari-
ousness in Gastrotricha could also have reasons different
from reproduction and mating (Hummon & Hummon 1992,
1993). During copulation, two specimens of Macrodasys
sp. form a complicated knot with their posterior trunk por-
tions (Ruppert 1978a). Within the knot, the copulatory tube
of one animal gets into contact with the frontal organ pore
of the other and vice versa. Furthermore, each specimen
within the knot brings its male gonopores in close proxi-
mity to its own antrum thereby enabling the transition of
the autosperms from the testes to the caudal organ. The
general scheme of reciprocal sperm transfer in Macroda-
sys – pairing, copulation, charging the caudal organ with
autosperm, transferring sperm from the caudal organ into
the frontal organ of the mating partner, and detachment – is
assumed to occur in many species of hermaphroditic gastro-
trichs (Ruppert 1991). Since anatomic conditions vary a lot
among the different taxa (see chapter Reproductive Organs),
different deviations from this general scheme will certainly
exist. For instance, sperm ducts directly discharge into the
caudal organ lumen in the taxa Mesodasys and Thaumas-
todermatidae. This means that the caudal organ may have
already been charged with autosperm internally before the
actual mating and copulation with a reproductive partner
happens. In Thaumastodermatinae, a subtaxon of Thau-
mastodermatidae, the continuity of sperm duct, caudal
organ, and frontal organ may also indicate the possibility
of self-fertilization (Ruppert 1991, see also chapter Repro-
ductive Organs). This hypothesis, however, has never been
tested. Another deviation from the “Macrodasys scheme”
of mating and copulation may be present in some species
of Urodasys that possess a cuticularized stylet within their
caudal organ (Schoepfer-Sterrer 1974). Those hard parts
could in principle be used for hypodermal impregnation.
Such a function of the stylet in different members of Uroda-
sys, however, has never been demonstrated (Balsamo 1992)
and was already rejected by Schoepfer-Sterrer (1974).
Another mode of reciprocal sperm transfer in marine
Gastrotricha is the formation and exchange of spermato-
phores (see also chapter Reproductive Organs). Sperma-
tophores, i.e., oval to spherical packages of spermatozoa
embedded inside a common sheath or matrix, definitely
occur in species of Dactylopodola (Teuchert 1968, Ruppert
1991, Kieneke etal. 2008d) and Neodasys (Guidi etal. 2003,
Kieneke etal. 2009) and have recently also been reported
from the newly described species Urodasys poculostylis
(Atherton 2014). However, the exact mode of spermato-
phore exchange and the involved organs are still poorly
understood. In Dactylopodola baltica, spermatozoa are
internally packed into spermatophores but it is not known
which organ facilitates spermatophore formation. The
spermatophore is then extruded to the outside and glued
to another animal where spermatozoa leave the later dege-
nerating spermatophore by an undetermined mechanism
(Teuchert 1968). For another species of Dactylopodola from
the US Atlantic coast, it is hypothesized that the complete
frontal organ is first charged with spermatozoa internally
via a narrow channel that connects sperm ducts with the
frontal organ lumen. Later, the whole frontal organ shall
be extruded in toto as the actual spermatophore (Ruppert
1991). The function of the also present caudal organ in this
species, however, is not clearly visible according to that
hypothesis. Solely based on their morphological recons-
tructions, Kieneke etal. (2008d) hypothesize that in Dac-
tylopodola typhle that spermatozoa must be transported
externally from the testes into the lumen of the glandular
caudal organ prior to mating. Here, mucous secretions are
released and build up the spermatophore, which is then
pressed from one animal, mediated by contractions of the
rear trunk musculature, into the dorsolateral female gono-
pore of a mating partner. The spermatophore reaches a posi-
tion beneath the mature oocyte inside the uterus via a short
duct called the cervix. Again mainly based on ultrastruc-
tural morphological data, another mode of spermatophore
formation was hypothesized for Neodasys chaetonotoideus
(Kieneke etal. 2009). The formation of spermatophores in
N. chaetonotoideus is assumed to occur completely exter-
nal by the aid of secretion products that originate from the
caudal organ. This assumption is supported by the obser-
vation that mature specimens may carry a spermatophore
adhered to the posterior adhesive appendages (Kieneke
etal. 2009). Inseminated specimens of N. chaetonotoideus
display one, sometimes more (own unpublished obser-
vation, but see also figure 113 in Ruppert 1991) spermato-
phores inside their frontal organ. The mechanism how the
spermatophore enters the frontal organ is obscure (Kieneke
etal. 2009). All these examples highlight the urgent need of
detailed behavioral studies of gastrotrichs in combination
with morphological reconstructions to fully understand the
reproductive biology of Macrodasyida and Neodasys.
Apart from hermaphroditism, there are also few
instances of parthenogenetic species among Macrodasy-
ida that only possess female gonads and lack any acces-
sory reproductive organs. Candidates for a solely uni-
sexual reproduction are Urodasys viviparus, Paradasys
subterraneus (and probably further species of Paradasys),
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82 1Gastrotricha
Redudasys fornerise (one of only two species of Macroda-
syida inhabiting freshwater), and Anandrodasys agadasys
(Wilke 1954, Kisielewski 1987a, Todaro etal. 2012b, Kieneke
etal. 2013a). However, Valbonesi & Luporini (1984) descri-
bed specimens of U. viviparus from the Somalian coast
that obviously possessed a testis and a caudal organ that
indeed indicates that hermaphroditic reproduction in that
species occurs (see also Hummon & Hummon 1993). Apart
from the questionable parthenogenesis in this species,
U. viviparus is still of interest in terms of reproductive
biology because it is the only known gastrotrich species
that is ovoviviparous (Hummon & Hummon 1983a).
Knowledge about reproductive biology of the gastro-
trich subgroup Paucitubulatina is much more fragmentary
than in Macrodasyida and Neodasys. Marine species of the
taxa Xenotrichulidae and Muselliferidae are, with only
few exceptions (the xenotrichulids Draculiciteria tesselata
and Heteroxenotrichula pygmaea are much likely obligate
parthenogenetic species, see Wilke 1954 and Ruppert 1979,
reviewed in Balsamo 1992 and Hummon & Hummon 1993),
hermaphroditic animals like most Macrodasyida and Neo-
dasys. However, apart from species of Musellifer, which may
possess putative accessory reproductive organs (Hummon
1969, but see Leasi & Todaro 2010), there are no compa-
rable organs in the con-familiar taxon Diuronotus (Todaro
etal. 2005, Balsamo etal. 2010a). Although Ruppert (1979)
frequently reports an unpaired ventral copulatory organ in
Xenotrichulidae at the site where both vasa defferentia fuse,
such a structure has not been confirmed so far. There might
be a glandular structure of unknown function in this region
as in Xenotrichula punctata (Ferraguti etal. 1995). Owing to
this predominant absence of accessory reproductive organs
in simultaneous hermaphroditic Paucitubulatina (Muselli-
feridae and Xenotrichulidae), it is incomprehensible how
sperm transfer might be achieved. To our knowledge, there
is no assured report of reproductive behavior in any taxon
of the Gastrotricha-Paucitubulatina. In their culture dishes,
Balsamo & Todaro (1987) encountered some pairs of indivi-
duals of Aspidiophorus polystictos that were close to each
other with their caudal ends. However, it was not possi-
ble to determine if this behavior enabled effective mating.
By chance, we have uniquely observed two individuals of
Xenotrichula intermedia in a Petri dish of freshly extracted
meiofauna, which slowly orbited each other with slightly
decreasing radius. The moment they were touching, the
animals crawled around each other quite quickly but
already released and departed after 1–2 seconds (unpu-
blished observation). This was possibly the moment of
mating and exchange of spermatozoa. However, due to the
obvious absence of any copulatory or sperm storing device
in Xenotrichulidae (see above), it is absolutely dubious
how cross-insemination will be facilitated by members of
this taxon. The frequent occurrence of coiled spermatozoa
on the surface of X. intermedia from an Arabian population
is possibly related with sperm transfer modalities in this
species (Leasi & Todaro 2009). However, this observation is
raising more questions than providing answers in terms of
reproductive biology in Xenotrichulidae.
The predominantly freshwater inhabiting paucitubu-
latinan taxa Chaetonotidae and Dasydytidae were for long
regarded to reproduce solely by parthenogenesis (e.g.,
Remane 1936, Hyman 1951). However, as already presented
in the chapters about reproductive organs and gametes,
reproductive development, and fine structure of the fresh-
water paucitubulatinan species Lepidodermella squamata
(Chaetonotidae) was studied and described in detail in a
series of papers (Hummon 1984a–c, 1986) and has finally
demonstrated the frequent development of hermaphroditic
specimens in this species. L. squamata first reproduces by
parthenogenetic formation of tachyblastic (subitaneous)
and opsiblastic (resting) eggs. After the parthenogenetic
phase, packets of simple, rod-shaped sperms are produced
and few oocytes develop into opsiblastic eggs. Spermatocy-
tes and oocytes undergo meiosis during this hermaphroditic
phase. A comparable mode of parthenogenesis followed by
the production of simplified spermatoza was also demons-
trated in a marine species of Chaetonotidae, Aspidiophorus
polystictos (Balsamo & Todaro 1987, 1988). Hence, L. squa-
mata, A. polystictos, and probably many other Chaetonoti-
dae actually represent protogynous hermaphrodites rather
than obligate parthenogens (Hummon & Hummon 1992).
With the development of eggs and sperm in A. polystictos,
L. squamata, and many more freshwater-dwelling species
of the Chaetonotidae and Dasydytidae (e.g., Weiss & Levy
1979, Kisielewska 1981, Weiss 2001), essential features for
a bisexual reproduction with recombination by cross-ferti-
lization during a hermaphroditic phase are present in these
taxa of the Paucitubulatina. However, it was until now not
possible to demonstrate cross-fertilization in Chaetonoti-
dae or Dasydytidae (e.g., Hummon & Hummon 1992, 1993,
Weiss 2001), or even in the well-studied Lepidodermella
squamata (Hummon 1986). Although this important proof
was and is still missing a partly hypothetical biphasic life
cycle for the Chaetonotidae (probably also applicable to
the remaining parthenogenetic-hermaphroditic paucitu-
bulatinan taxa Dasydytidae, Neogosseidae, Proichthydidae,
and Dichaeturidae) has been developed (Levy 1984, see
also Strayer & Hummon 1991 and Balsamo 1992 for sum-
maries). According to this scenario, that is fully congruent
with the results on reproductive development in L. squa-
mata (Hummon 1984a–c, 1986), species of Chaetonotidae
reproduce by two different reproductive phases (biphasic
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1.3Reproduction and development 83
HERMAPHRODITIC PHASE
PARTHENOGENETIC PHASE
(APOMIXIS)
AMPHIMIXIS
T
O
T
T
juvenile
hermaphrodites
parthenogenetic
female
PB F
F
2n
1n
D
sp
oo
sp
oo
MEIOSIS
Fig. 1.49: Hypothetical biphasic life cycle
of Chaetonotidae (Paucitubulatina).
Pharthenogenetic females generally
produce 4 apomictic eggs; the last one
is almost always a resting (opsiblastic)
egg, whereas the others are subitaneous
(tachyblastic) eggs. After depositing the last
parthenogenetically produced egg, animals
become hermaphrodites and develop
simple sperm and further eggs that undergo
meiosis. If fertilization really occurs has
yet to be proved. A third egg type (PB)
discovered in cultures of Lepidodermella
squamata could represent fertilized eggs.
The broken lines indicate still unproven
pathways. Abbreviations: D, dormancy;
F, fertilization; O, opsiblastic egg; oo, oocyte;
PB, plaque-bearing egg; sp, sperm rod;
T, tachyblastic egg. (Modified from Strayer &
Hummon 1991 and Balsamo 1992.)
life cycle). The first is the parthenogenetic phase (Fig. 1.49)
where animals mostly produce four or five apomictic (2n)
eggs, the last of which is almost always a resting (opsiblas-
tic) egg while the others are subitaneous (tachyblastic) eggs.
The parthenogenetic phase enables a rapid population
growth and exploitation of resources under favorable condi-
tions. Production of resting eggs serves as a “buffer” against
periods of unfavorable ecological conditions (Strayer &
Hummon 1991). When the parthenogenetic resting egg is
spawned, animals enter the second, post-parthenogenetic
(hermaphroditic) phase (Fig. 1.49) where bilateral packets
of simplified sperm (1n) are produced by meiosis, generally
32–64 per animal (see also chapters about reproductive
organs and gametes). The ovary produces meiotic eggs (1n)
during the post-parthenogenetic phase. It is assumed that
two of such hermaphroditic individuals exchange gametes
by a yet undetermined mechanism by which fertiliza-
tion is achieved and a zygote (2n) is formed. Owing to the
complete absence of accessory reproductive structures as
well as sperm ducts in L. squamata and other chaetonotids
that may serve for sperm transfer (the enigmatic secretory
x-organ is regarded to play another role in reproduction,
see chapter Reproductive Organs), one possibility for sperm
transfer, although quite bizarre, might be the ingestion of
spermatozoa by cannibalism between hermaphrodites
(Hummon 1986). The relative length of the hermaphroditic
phase compared with the parthenogenetic phase (40%–
70% versus 20%–40%, a short postembryonic phase not
considered for these values, see Balsamo 1992) may under-
line the importance of presumed sexual reproduction with
recombination in these predominantly freshwater taxa.
Ovipository behavior was studied in several species
of Macrodasyida by Teuchert (1968). Species such as
Cephalodasys maximus and Mesodasys laticaudatus
spawn only one egg at a time, whereas species of Turba-
nella, Dactylopodola baltica, or Urodasys mirabilis may
deposit one to two mature eggs, Macrodasys caudatus is
able to spawn seven to eight eggs at once. Because eggs
of macrodasyidan gastrotrichs are provided with a sticky
secretory covering (up to 20 µm thick like in Turbanella
cornuta, see figure 7C of Teuchert 1968), the animals are
able to glue the laid eggs immediately to sand grains.
In Macrodasys caudatus, a short chain or clutch of eggs
may be produced due to this glutinousness. A putative
origin of the cohesive covering of readily laid eggs has
recently been discovered in Dinodasys mirabilis. The
so-called posterior gland organ of this species is hypo-
thesized to synthesize the appropriate secretion (Todaro
etal. 2012a). Egg deposition involves a special behavior
where animals slow down their creeping locomotion
and seem to sense the substratum for suitability (e.g.,
chemical factors, surface conformation, texture of sedi-
ment grains). It is possible that gravid animals engage
in site selection to choose a spot with a certain protec-
tion for the laid egg (Hummon & Hummon 1983a). Such
a behavior might be the only contribution to parental
care in Gastrotricha. Immediately prior to egg deposi-
tion, species like Turbanella cornuta turn their body and
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84 1Gastrotricha
Fig. 1.50: Spawning of Macrodasyida.
(A) Turbanella hyalina that has currently
deposited an egg. Note the area in the
integument where the egg has left the
body (asterisk). It is still dubious whether
the egg leaves the mother by rupture of
the body wall or through an inconspicuous
pore (see main text for details). (B) An
embryo of Urodasys viviparus inside the
egg envelope and still inside the mother
animal. U. viviparus is so far the only known
ovoviviparous gastrotrich species. (A–B):
DIC images. Abbreviations: em, embryo; gc,
glutinous covering of the egg; mg, midgut;
mo, mature (spawned) egg; ov, ovary; ph,
pharynx; tes, testis.
100 µm
25 µm
AB
*
mo
mg
ov
tes
ph
em
mg
gc
press their back to the substratum to cause a rupture
of the integument (Teuchert 1968; Fig. 1.50 A). This
behavior is supported by muscular activity and adhe-
rence with the anterior tubes. Macrodasys caudatus and
Urodasys mirabilis engage in repeated contraction and
stretching of the body to press the eggs to the outside
via a lateral rupture of the body wall. Again, the animal
uses its anterior adhesive tubes to attach to the sedi-
ment during egg deposition. Dactylopodola baltica sud-
denly stops its jerky movements and executes a frontally
directed pressure, probably caused by muscle contrac-
tions. This pressure causes again a rupture of the body
wall close to the uterus (Teuchert 1968). Contraction of
the longitudinal muscles also precedes egg deposition
in freshwater chaetonotids. Here, mature eggs leave the
animal ventrally, possibly through a yet undiscovered
ovipore (Hummon & Hummon 1983a). The rupture of
the integument to release mature and fertilized eggs
in Macrodasyida was repeatedly reported in different
macrodasyidan gastrotrichs (Teuchert 1968, see above).
Also, in the ovoviviparous species Urodasys viviparus,
a rupture of the body wall of the mother animal was
assumed to give birth to the juvenile because no female
gonopore could be observed in this species (Wilke 1954).
The rather bizarre process of body wall rupture gets
support by the observation of presumptive wounds in
the integument that may persist as small bulges for two
or even more days in the area where the egg has left the
trunk (Teuchert 1968; Fig. 1.50 A). However, in different
species of the Thaumastodermatidae (Ruppert 1978b) and
in Dactylopodola typhle a short outlet duct with an at
least preformed dorsolateral pore is present. This organ
was later termed the “cervix” (Kieneke etal. 2009). Pre-
sence of a cervix is also supposed in Turbanella cornuta
(Kieneke etal. 2009 regard the “gland organ of the intes-
tinal region” as a potential cervix, see above), a species
in which egg deposition shall actually happen via
rupture of the body wall. As the cervix and female gono-
pore in D. typhle was only detectable by TEM or serial
histological sections, not even by differential interfe-
rence contrast (DIC) microscopy, it is possible that such
an outlet duct for egg deposition is in fact present (but
has not been detected yet) in species that are believed to
spawn by rupture of the body wall (Kieneke etal. 2009).
The observed wounds in different species of Macrodasy-
ida (Teuchert 1968) could in fact be swollen epidermal
cells that surround the female gonopore after spawning.
Such a situation was observed in a specimen of D. typhle
that was sectioned for histological investigation (see
figure 10E–F in Kieneke etal. 2008c).
1.3.2Cleavage and development
There are still quite few investigations on the cleavage
of the fertilized egg. First observations were made by
Ludwig (1875), who observed the first cleavage steps
in Chaetonotus larus eggs. De Beauchamp (1929) and
Brunson (1949) added further observations from a total
of three chaetonotid species, and Sacks (1955) provi-
ded the most detailed descriptrion of the embryology
of Lepidodermella squamata. Mock (1979) stated that
the first cleavage steps in two Xenotrichula species cor-
respond to Sacks’ reports. Macrodasyids were inves-
tigated even more rarely, initial observations come
from Swedmark (1955) on Macrodasys affinis, whereas
Teuchert (1968) provided a detailed description of the
cleavage and development of Turbanella cornuta, with
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1.3Reproduction and development 85
15 µm
15 µm
15 µm
15 µm
A
B
D
*
ph fu
C
nu
nu
Fig. 1.51: Development of the freshwater gastro trich
Lepidodermella squamata (Paucitubulatina). (A) Two-cell stage.
Note the sculptured egg shell. (B) Two cells migrated between
the two central ventral cells (to the bottom in the image) into the
blastocoel (asterisk). The blastopore is now closed. (C) Multicel lular
embryo during organogenesis. (D) Almost fully shaped embryo.
(A–D): DIC images. Abbreviations: fu, furca with adhesive tubes;
nu, nucleus; ph, pha rynx. All images kindly by Andreas Hejnol,
Bergen.
additional data from Cephalodasys maximus and Mac-
rodasys caudatus.
Cleavage starts within a few hours after oviposi-
tion, after already 25–35 minutes in L. squamata (Sacks
1955), after about 2 hours in T. cornuta, after 2–3 hours in
M. caudatus, and after 3–4 hours in C. maximus (Teuchert
1968). The first cleavage is total and results in two blas-
tomeres of equal size (named AB and CD; Fig. 1.51 A).
The second cleavage plane is perpendicular to the first
plane and results in a shift of two blastomeres in a 90°
angle compared with the other two blastomeres. This
stage is called rhomboid (Teuchert 1968) or tetrahedral
(Malakhov 1994). To reach this stage, some differences
exist between the observed chaetonotids and macroda-
syids. In L. squamata, there is a slight asynchrony in the
cleavage of the two blastomeres from the first cleavage
and also a slight difference in size (Sacks 1955). Blas-
tomere AB divides slightly earlier than blastomere CD.
The resulting blastomeres C and D appear to be smaller
than blastomeres A and B. In the observed macroda-
syids, there are no size differences between the blas-
tomeres A to D, but the asynchrony in division is more
pronounced, which leads to an intermediate three-cell
stage (Teuchert 1968).
In L. squamata, the asynchrony in cleavage persists
throughout the entire cleavage, the anterior blastomeres
divide before the posterior ones. Additionally, size diffe-
rences become pronounced and dorsal blastomeres are
smaller than ventral ones (Sacks 1955). After the fifth clea-
vage, the 32-cell stage constitutes the blastula with a small
blastocoel in the center.
In the four-cell stage of macrodasyids, one of the
posterior blastomeres (called C in Teuchert 1968) moves
anteriorly to a central position where it touches all three
other blastomeres, or in some cases even further, to the
level of the blastomeres A and B. The position of this
blastomere C marks the dorsal side of the developing
embryo. The following cleavages are asynchronous.
After the third cleavage, another shift of one cell occurs
in T. cornuta. Blastomere D divides into a dorsal and a
ventral cell, the ventral one is called E. This blastomere
moves into a central, ventral position and becomes the
“urmesoderm cell”. In this eight-cell stage, the blasto-
meres detach from each other in the central part and
form a small blastocoel. Consequently, Teuchert (1968)
calls this eight-cell stage already a coeloblastula. In
M. caudatus, no “urmesoderm cell” or blastocoel exists.
A blastocoel occurs during the fourth cleavage in this
species.
In T. cornuta, the subsequent cleavages are asyn-
chronous, with the “urmesoderm cell” dividing as the
last cell. The two resulting “urmesoderm cells” remain
undivided during the sixth and the seventh cleavage
(Teuchert 1968). The two “urmesoderm cells” have
extensions into the blastocoel, which can be interpreted
as an early indication of gastrulation. Embryos of both
T. cornuta and M. caudatus are bilaterally symmetrical.
For gastrulation in T. cornuta, both “urmesoderm cells”
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86 1Gastrotricha
sink into the blastocoel. Owing to the small size, the
resulting archenteron is more or less a ventral pit. By
stretching and bending of the embryo, a ventral furrow
is created, which is closed by growth of the lateral ecto-
dermal cells. Mesodermal cells originate from cells bor-
dering the two “urmesoderm cells”, they migrate into the
embryo during gastrulation.
In L. squamata, gastrulation follows the fifth clea-
vage (Sacks 1955). It consists of an inward migration of
two ventral cells, called A5.3 and A5.4, into the blastocoel
(Fig. 1.51 B). This progress is similar to T. cornuta, but the
two ventral cells have originated in a different way. The
further development of the entoderm is also described
in a different way. According to Sacks (1955), the blasto-
pore is closed for a brief moment, then cells in this region
proliferate and form a ring around the more and more
pronounced anterior invagination. Another invagination
forms at the posterior end of the embryo, these two inva-
ginations extend and approach each other. At this time,
the anterior invagination can already be recognized as the
pharynx, whereas the posterior invagination appears to
be the developing midgut.
Teuchert (1968) has produced a cell lineage for
T. cornuta. As described above, the entoderm derives
exclusively from the cell E, the “urmesoderm cell”. Meso-
derm and ectoderm derive from different cells from all
remaining lineages.
Embryos develop gradually into juveniles, which
resemble miniature adults when they hatch from the egg
capsule (e.g., Remane 1936, Teuchert 1968; Fig. 1.51 C, D).
In chaetonotids, cuticular structures are recognizable in
late embryos inside the eggs (Mock 1979). No larval stages
are present, and no molting takes place. Hatched juveni-
les grow and develop gradually into mature specimens.
There are, besides size differences and the absence of
the reproductive organs, two main differences between
juveniles and adults. They have (in macrodasyids) fewer
adhesive tubes and fewer pairs of protonephridia than
adults (Teuchert 1968), and the size relations between
pharynx and midgut are different than in adults (Fig. 1.52
A–C). Usually, in juveniles, the pharynx is comparably
longer than the midgut, whereas in adults, it is vice versa
(e.g., Remane 1924 for Macrodasys buddenbrocki, Hoch-
berg 1998 for Turbanella mustela).
Some sources, especially from popular science,
state that gastrotrichs are an example for eutely, which
means that the cell number, including the germ line, is
fixed. Hence, all cell divisions must be finished during
embryogenesis with no further mitoses after this period
200 µm 50 µm
100 µm
AB
C
Fig. 1.52: Juvenile specimens of Gastrotricha. During postembryonic
development organ sys tems such as adhesive tubes, epidermal
glands and protonephridia are increased and the go nads occur.
(A) Macrodasys caudatus (Mac rodasyida), dorsal view. (B) Turbanella
hyalina (Macrodasyida), ventral view. (C) Neodasys cha etonotoideus
(Multitubulatina), dorsal view. (A–C): BF images.
(see Balsamo etal. 1999). This requires a strictly determi-
nate cleavage with an invariant cell line, two facts that
are not known with certainty for gastrotrichs. At least in
macrodasyids, eutely is certainly not the case. Manylov
(1995) documented a complete regeneration after transsec-
tion in Turbanella sp. and also the egg release by rupture of
the body wall in those species without a female gonopore
can only be explained by regeneration capacity, which
involves the generation of new cells. Also, the assumed
mitotic proliferation of spermatogonia within the testes of
at least some species of the Macrodasyida contradicts a
strict definition of eutely (Balsamo etal. 1999).
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1.4Physiology 87
biting the spaces between sand grains. By then, a variety
of freshwater species, one of the earliest descriptions
was provided by Ehrenberg (1838), and two marine ones,
Hemidasys agaso (Claparède 1867) and Turbanella hyalina
(Schultze 1853) were known to science. The freshwater
species were considered to represent a separately evolved
group of microscopic animals, the Gastrotricha (e.g.,
Mečnikow 1865, Zelinka 1889), which initially included
the marine Turbanella (see Mečnikow 1865). Later, an affi-
liation of the two only known marine species (T. hyalina,
H. agaso) to this taxon was dismissed (e.g., Wagner 1893).
But in view of the large quantity of new marine forms,
which were first called the “aberrante Gastrotrichen”
(Remane 1924, 1925a, b), a revision of this group of exclu-
sive meiobenthic organisms was required. At the latest
with Remane’s monograph (Remane 1936) the traditional
system of Gastrotricha has been shaped. He separated two
orders among the Gastrotricha, which, at that time, repre-
sented a class of the Aschelminthes (see Schmidt-Rhaesa
2013): (1) the exclusive marine to brackish Macrodasyida
(originally termed Macrodasyoidea) and (2) the marine as
well as fresh and brackish water inhabiting Chaetonotida
(originally termed Chaetonotoidea).
Decades later, it was d’Hondt (1971) who erected two
chaetonotidan suborders to highlight the isolated position
of the marine taxon Neodasys. From then on, Gastrotricha
comprised the two sister taxa Macrodasyida and Chaeto-
notida with Multitubulatina (=Neodasys) and Paucitubu-
latina (=all remaining chaetonotids) being sister taxa of
highest rank within the Chaetonotida. When originally
described, Remane (1927a, 1929) provisionally assigned
Neodasys to the Macrodasyida but later he relocated it to
the Chaetonotida based on histological findings (Remane
1936). Much later, a cladistic analysis of a variety of mor-
phological characters (Hochberg & Litvaitis 2000; Fig. 1.53 A;
see also Hochberg & Litvaitis 2001e) confirmed this tradi-
tional system and further provided ideas of phylogenetic
relationships among the different genera of Gastrotricha.
Monophyly of several of the traditional families was sup-
ported, while for others, it was declined (Hochberg &
Litvaitis 2000, 2001e). Phylogenetic discussions that were
focused on ultrastructural features of, e.g., the pharynx
or the body wall of different gastrotrich species (Ruppert
1982, Travis 1983) confirmed the traditional thoughts of
the basal internal relationships and provided some hypo-
theses on evolutionary traits. According to these studies,
species of the subtaxon Macrodasyida would be characte-
rized by the possession of pharyngeal pores and a pattern
of an inverted Y of the cross-sectioned pharyngeal lumen,
whereas members of the taxon Chaetonotida lack pharyn-
1.4Physiology
Not much data are known about physiological proper-
ties of gastrotrichs. Most gastrotrichs are aerobic and live
in the upper layers of sediments or above the sediment.
Because some species occur deeper in the sediment, anae-
robiosis is assumed to be possible (Boaden 1985), although
it is not known whether this is just a tolerance of low
oxygen levels or whether anaerobic metabolic pathways
are present. Boaden (1974) described three species [Tur-
banella reducta, T. thiophila (=T. bocqueti) and Thiodasys
sterreri (=Megadasys sterreri)] from gray and black sands
rich in sulfide. The three species form a series occurring in
more and more anoxic and sulfidic sediments. Megadasys
sterreri is the species that appears most adopted to anoxic
conditions. It was kept in sealed jars with anoxic sand
for more than 2months (Boaden 1974). An ultrastructu-
ral investigation showed that mitochondria seem to have
fewer cristae than in other species, and it is possible that
CO2 can be fixed (Boaden 1974). The complete absence
of mitochondria has been observed in the spermatozoa
of two Urodasys species (Balsamo etal. 2007). One pos-
sible explanation is that this is an adaptation to anoxic
sediments.
Neodasys sp. has a blood-red appearance, which is
caused by red cells that are assumed to be homologous
to Y-cells (Kraus etal. 1981, Ruppert & Travis 1983). This is
in contrast to other species with colorless Y-cells and was
investigated in further detail. The red cells are arranged
in two longitudinal rows dorsolateral of the gut and make
up about 14% of the body volume (Ruppert & Travis 1983).
Branches of these cells surround perikarya of muscle and
nerve cells, whose mitochondria are close to this con-
nection site (Ruppert & Travis 1983). The cells contain
intracellular hemoglobin (Colacino & Kraus 1984), as had
been suspected by Kraus etal. (1981). Colacino & Kraus
(1984), and Kraus & Colacino (1984) compared the oxygen
consumption rate of Neodasys sp. with that of Turba-
nella ocellata and Dolichodasys carolinensis, but the rate
of Neodasys sp. is between that of the two other species.
Therefore, it is assumed that the possession of hemo-
globin does not affect oxygen consumption, but may be
important for oxygen storage, probably for sporadic move-
ments to anoxic sediments.
1.5Phylogeny
In the 1920s, the German zoologist Adolph Remane dis-
covered dozens of new taxa of marine gastrotrichs inha-
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88 1Gastrotricha
more closely associated with taxa such as Plathelmin-
thes, Gnathostomulida or Rotifera rather than with Mac-
rodasyida (Manylov etal. 2004; Fig. 1.53 E). However, all
these pioneer studies lack important taxa such as Neo-
dasys, which are of highest systematic relevance. More
recent cladistic analyses based on partial 18S rRNA gene
sequences comprise a more satisfying taxon sampling
among the gastrotrich genera (Todaro etal. 2003, 2006a,
Petrov etal. 2007, Paps & Riutort 2012). The mentioned
analyses reveal Paucitubulatina as a monophyletic group
but Macrodasyida being paraphyletic with Neodasys
nesting within a sub clade comprising different macroda-
syid genera (Todaro etal. 2003: ML analysis; Fig. 1.53 C,
Todaro etal. 2006a; Fig. 1.53 F). Alternatively, Macroda-
syida form a monophyletic group but include again Neo-
geal pores and show a Y-shaped pharyngeal lumen when
cross-sectioned (see, e.g., Ruppert 1991). However, these
characteristics of the within-groups of highest rank leave
unresolved the character pattern of the common ancestor
because we have conflicting character states in the basal
node of Gastrotricha (absence versus presence of pharyn-
geal pores; Y-shaped versus inverted Y-shaped pharyngeal
lumen).
Initial DNA sequence-based cladistic analyses or
combined morphological and molecular studies revealed
successively the paraphyly of Paucitubulatina (Wirz etal.
1999; Fig. 1.53 B), the paraphyly of Macrodasyida (Zrzavý
2003; Fig. 1.53 D) or even polyphyly of whole Gastrotri-
cha with both major subgroups (Chaetonotida, Macroda-
syida) being monophyletic each but with Chaetonotida
A
EF
B
HG
CD
Fig. 1.53: Basal internal relationships
of Gastrotricha according to different
analyses using different character systems
and methods of inference. In some cases,
the positions of putative basal genera (in
italics) are indicated. Note that the tree
topologies are strongly simplified. (A)
Relationships according to consensus tree
(50% majority rule, maximum parsimony) of
Hochberg & Litvaitis (2000). This scenario
is also congruent with late systematization
of the Gastrotricha (Remane 1936, d’Hondt
1971). (B) Relationships according to
neighbor joining tree of Wirz etal. (1999).
(C) Relationships according to maximum
likelihood tree of Todaro etal. (2003).
(D) Relationships according to summary
tree of Zrzavý (2003). (E) Relationships
according to Bayesian tree of Manylov
etal. (2004). (F) Relationships according to
Bayesian tree of Todaro etal. (2006).
(G) Relationships according to Bayesian
tree of Petrov etal. (2007)/maximum
likelihood tree of Paps & Riutort (2012)/
single most parsimonious tree of Todaro
etal. (2003). This scenario is also
congruent with early systematization
of the Gastrotricha (Remane 1929).
(H) Relationships according to consensus
tree (50% majority rule, maximum
parsimony) of Kieneke etal. (2008).
Abbreviations: Cephal., Cephalodasys;
Dact., Dactylopodola; PAUCIT.,
Paucitubulatina; Xeno., Xenodasys.
*The lineage comprises Redudasys
and Marinellina.
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1.5Phylogeny 89
of Redudasys and Anandrodasys (together forming the
new family Redudasyidae) with a well-supported posi-
tion within the Macrodasyida and no obvious affiliations
to the Paucitubulatina (Todaro etal. 2012b). A compre-
hensive overview of the major hypotheses regarding the
internal relationships but also the phylogenetic position
of Gastrotricha among the Bilateria can be found in the
review paper of Balsamo etal. (2010b).
A common phenomenon in cladistic analyses using
phenotypic (morphological) characters as data are the
low recovery values of especially basal (early) nodes when
using permutation tests such as the bootstrap to infer
the robustness of phylogenetic trees (see node support
values of, e.g., Hochberg & Litvaitis 2000, Marotta et al.
2005, Kieneke etal. 2008a). Owing to the much higher
characters to taxa ratio in studies using DNA sequences
as data (several hundreds to thousands of characters),
the resolved nodes generally get much higher support
values in those analyses (Wägele 2005). However, it has
to be stressed that there are also internal nodes with low
or just moderate bootstrap support in different 18S-based
cladistic analyses of the Gastrotricha (see, e.g., Manylow
etal. 2004, Paps & Riutort 2012, Todaro etal. 2012b). The
amount of noise in the data set is possibly much more
important than bare characters to taxa ratio. Especially
in morphological data matrices, there can be many homo-
plastic character states. Homoplasy may result from, e.g.,
convergent transformations or parallel character losses.
The latter is regarded as one major reason for incongru-
ence between trees generated on the basis of molecular
versus morphological data sets (see Bleidorn 2007).
The latest chapter in gastrotrich phylogeny reconst-
ruction has recently been started with cladistic analyses
that use multiple gene loci for phylogenetic inference.
Although very promising, these studies so far comprise
only a fraction of gastrotrich taxa and focus on certain
groups such as the Thaumastodermatidae (Todaro et al.
2011a), the Chaetonotidae, or the Dasydytidae (Kånneby
etal. 2012, 2013). Such analyses provide interesting new
insights into the relationships of, for instance, the species-
rich but probably polyphyletic Chaetonotidae. However,
support values for the important basal (early) nodes appa-
rently decrease the more taxa and positions an alignment
includes (e.g., compare Kånneby etal. 2012 with Kånneby
etal. 2013).
Instead of providing detailed descriptions of the dif-
ferent alternative in-group relationships of Gastrotricha,
which are far from being settled, we here focus on taxa
that show a certain probability to occupy a basal position
within their respective superordinate taxon. Pragmati-
cally, “probability” is here equalized with the frequency
dasys (Todaro etal. 2003: MP analysis, Petrov etal. 2007,
Paps & Riutort 2012; Fig. 1.53 G). The latter scenario ironi-
cally represents Remane’s earlier system of Gastrotricha
(e.g., Remane 1927a, 1929) before he assigned Neodasys to
the Chaetonotida.
The use of characters related with sperm morphology
and sperm ultrastructure of 28 species of Gastrotricha
grouped most of the included species of Macrodasyida as
a monophyletic clade but did not reveal the Paucitubula-
tina as a monophylum (Marotta etal. 2005). Furthermore,
the maximum parsimony analysis placed two included
macrodasyidan species of the taxon Dactylopodola as
the sister group of two paucitubulatinan species of the
taxa Chaetonotus and Lepidodermella, possibly due to a
similar aberrant but probably not synapomorphic sperm
morphology of Dactylopodola and many freshwater dwel-
ling Paucitubulatina (see chapter Gametes). Although
Neodasys ciritus was included in that analysis, it is not
possible to infer its phylogenetic position because it was
used to root the tree. Unfortunately, a non-gastrotrich
outgroup taxon was not used. In general, sperm charac-
ters are considered to bear a high content of phylogenetic
information, but also to be highly homoplastic (Marotta
etal. 2005). Another cladistic analysis of 135 phenotypic
characters often used for taxonomy of Gastrotricha (e.g.,
number and arrangement of adhesive tubes, length/
width ratios, cuticular differentiations, shape of “head”,
trunk, and “tail”, sensory appendages) provides a
slightly different phylogeny for the internal relationships
than the hitherto proposed scenarios. According to that
analysis, Gastrotricha splits into the sister taxa Neodasys
and so called Eutubulata, which comprise all remaining
gastrotrich species (Kieneke et al. 2008a, Fig. 1.53 H).
The Eutubulata are characterized by the possession of
real adhesive tubes, consisting of a duo-gland complex
of two secretory cell types and a tube-shaped cuticular
protrusion through which the cells discharge. Sometimes
an associated ciliary sensory cell may be present as well
(see chapter integument). Within Eutubulata, two mono-
phyla, Macrodasyida sensu stricto (all traditional macro-
dasyids exclusive of Redudasys fornerise and Marinellina
flagellata; characterized by the possession of epidermal
glands and pharyngeal pores) and the so-called Abursata
(characterized by the absence of the unpaired accessory
reproductive frontal and caudal organs) are sister taxa of
highest rank. Abursata comprise as sister taxa the mono-
phyletic traditional Paucitubulatina and a monophylum
consisting of the only two freshwater macrodasyidan taxa
Redudasys and Marinellina. However, a recent analysis of
a fragment of the 18S rRNA gene from numerous gast-
rotrich species has revealed a sister group relationship
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90 1Gastrotricha
of a taxon being resolved as a basal lineage among the
various phylogenetic analyses. To simplify matters, we in
the following refer to genera or even families although in
most analyses, molecular as well as morphological, dis-
tinct species have been used as terminal taxa. However,
we use traditional family names only if their monophyly is
not in doubt. Within the Paucitubulatina, the initial split
leads to the genus Musellifer (Hochberg & Litvaitis 2000,
Todaro etal. 2006a) or, if Musellifer forms the sister group
of the arctic marine taxon Diuronotus (Todaro etal. 2005,
Leasi & Todaro 2008), to Muselliferidae (Fig. 1.54). Such
a basal position of Musellifer/Muselliferidae is supported
by the pattern of body musculature of several investiga-
ted paucitubulatinan species (Leasi & Todaro 2008) and
recently also by a molecular phylogeny using partial DNA
sequences of the nuclear 18S rRNA gene (Kånneby etal.
2014). Besides Musellifer (Muselliferidae), the monophyle-
tic family Xenotrichulidae (genera Draculiciteria, Xenotri-
chula, and Heteroxenotrichula) is also resolved to occupy a
basal position within Paucitubulatina (Todaro etal. 2003,
Petrov etal. 2007), sometimes as the result of the second
speciation event after the first split that leads to Musel-
lifer/Muselliferidae (Hochberg & Litvaits 2000, Todaro
etal. 2006a). It is also possible that both Muselliferidae
and Xenotrichulidae are sister taxa and occupy a basal
position within Paucitubulatina (Kieneke et al. 2008a,
1
2
3
4
Muselliferidae
Xenotrichulidae
Polymerurus
“Chaetonotidae”
Dasydytidae
Neogosseidae
Dichaetura
Proichthydidae
Dactylopodolidae
Xenodasys/Xenodasyidae
Neodasys (MULTITUBULATINA)
Cephalodasys
“Planodasyidae”
or
or
“Macrodasyidae”
“Cephalodasyidae”
Redudasyidae
Turbanellidae
Diplodasyinae
Thaumastodermatinae
Thaumastodermatidae
Lepidodasys
MACRODASYIDA
PAUCITUBULATINA
PLATHELMINTHES
or
GNATHOSTOMULIDA / GNAT HIFERA
or
CYCLONEURALIA
or
ECDYSOZOA
Fig. 1.54: Summary tree of the Gastrotricha
that shows the known and unresolved
internal phylogenetic relationships.
The tree was manually constructed and
depicts the congruent results between
phylogenetic analyses of the past 2
decades (see text for more details). The
indicated family names follow the recent
systematization of Gastrotricha according
to Balsamo etal. (2009), Hummon & Todaro
(2010), and Todao etal. (2012) (erection
of family Redudasyidae). Lineages that
end with a black circle are monophyletic
clades; groups marked with gray boxes
and quotation marks are polyphyletic or
paraphyletic. Dashed lines indicate the
uncertain position of the Xenotrichulidae
and the putative basal lineages within
Macrodasyida (i.e., Dactylopodolidae,
Xenodasyidae, or Cephalodasys).
Unambiguous autapomorphies of the
Gastrotricha and the 3 major internal
lineages as follows (according to several
authors): (1) external cilia covered with
epicuticle, visceral muscular double
helix, mechanoreceptive cells with 10
circumciliary microvilli, (2) tenpin-shaped
habitus, loss of lateral tubes, incomplete
visceral dorsoventral muscles, visceral
muscle helix spans to one third of the
intestine, bicellular terminal organ with
composite filter, aciliar canal cell with
convoluted distal lumen, (3) adhesive tubes
as non-duo-gland organs, club-shaped
mouth tube, loss of vasa deferentia,
(4) existence of epidermal glands, existence
of pharyngeal pores.
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1.5Phylogeny 91
Kieneke & Ostmann 2012). Congruence among results of
those analyses indicates that monophyly of the menti-
oned taxa is highly probable. In contrast, families such as
Lepidodasyidae (Macrodasyida) or Chaetonotidae (Pauci-
tubulatina) in most cases turned out to be paraphyletic or
polyphyletic assemblages (e.g., Hochberg & Litvaitis 2000,
2001a, Todaro etal. 2006a, Kieneke etal. 2008a, Paps &
Riutort 2012, Kånneby etal. 2013). Monophyly of Gastrotri-
cha as a whole has also been questioned (Manylow etal.
2004, see above). However, there are at least two unique
characters most likely shared by all members of Gast-
rotricha, i.e., the cuticular covering of all external cilia
(Rieger & Rieger 1977; maybe also the multilayer condition
of the epicuticle) and the presence of a visceral muscular
double helix encircling the gut tube (Hochberg & Litvaitis
2001a, b). These two characters have recently been con-
firmed as substantial autapomorphies characterizing the
Gastrotricha and supporting its monophyly (Kieneke etal.
2008a). Other potential apomorphies of the Gastrotricha
that are mentioned from time to time, for instance, the
hermaphroditism (Ax 2003, Balsamo etal. 2010b), or the
direct transfer of filiform spermatozoa (Ax 2003), are less
robust. First, members of main platyzoan lineages (Plat-
helminthes, Gnathostomulida) and of the earliest bilate-
rian branch Acoelomorpha (Acoela+Nemertodermatida)
follow a hermaphroditic reproduction, too (see Schmidt-
Rhaesa 2007). Second, occurrence of filiform spermatozoa
could also represent a plesiomorphic character within the
Bilateria: basal groups such as Nemertodermatida (Boone
etal. 2011) and Acoela (Raikova etal. 1998) possess such
a sperm type and so do further lineages (but see Schmidt-
Rhaesa 2007 for the proposed ancestral sperm type of the
Bilateria and the use of a phylogenetic character “filiform
spermatozoon” in general).
Inferring the internal relationships of Gastrotricha will
make it possible to detect natural groups corresponding to
“genera” or “families”. However, the system has not been
settled yet (see above), and there are quite a lot of unresol-
ved regions in the phylogenetic tree of Gastrotricha (Fig.
1.54). More extensive searches analyzing different gene loci
in combination with testing the resulting topologies with
morphological and ecological characters will probably
bring us closer to the phylogenetic system of Gastrotricha.
Furthermore, the analysis of extensive data sets of mor-
phological characters will be an important source of infor-
mation for understanding the phylogeny and evolution of
this group of animals. In this context, the investigation of
morphology and ultrastructure of different organ systems
is still a valuable and necessary challenge.
As already mentioned in the introduction to this
volume (Schmidt-Rhaesa 2013), the phylogenetic position
Fig. 1.54). Data of sperm ultrastructure give strong support
for such a sister group relationship of Muselliferidae and
Xenotrichulidae (Balsamo et al. 2010b). Patterns of the
anatomy of body musculature and of the protonephrida
ultrastructure indicate that the next branch within Pau-
citubulatina leads to the freshwater taxon Polymerurus
(Leasi & Todaro 2008, Kieneke & Hochberg 2012).
Within the Macrodasyida, species of the genus Dacty-
lopodola, or the family Dactylopodolidae as a whole (Dac-
tylopodola, Dendrodasys, Dendropodola), have frequently
been resolved as the earliest branch (Ruppert 1982, Travis
1983, Ruppert 1991, Hochberg & Litvaitis 2000, Todaro
et al. 2003: MP analysis, Zrzavý 2003: Dactylopodola as
most basal lineage within whole Gastrotricha, see Zrzavý ’s
figure 5). However, according to some analyses, they share
this putative basal position with others such as Xenoda-
sys and Acanthodasys (Todaro etal. 2003: ML analysis) or
with Paradasys, Cephalodasys, Urodasys, and Neodasys
in a common clade (e.g., Todaro etal. 2006a). Exceptions
from a basal position of Dactylopodolidae provide the
studies of Petrov etal. (2007) and Kieneke etal. (2008a).
According to nucleotide sequence data of the 18S rRNA
gene, Cephalodasys is the most basal lineage within Mac-
rodasyida; however, no sequence of a dactylopodolid
species was included (Petrov etal. 2007). According to
phenotypic data (Kieneke etal. 2008a), Xenodasys could
also represent the sister group of all remaining lineages
of Macrodasyida (Fig. 1.54). Interestingly, such a result
is supported by the analysis based on sperm morpho-
logy even though the position of Dactylopodola remains
unclear (Marotta et al. 2005). It has to be stressed that
so far, the DNA sequence-based studies comprise a frac-
tion of gastrotrich genera only. Hence, we have to keep in
mind that assuming the position of a certain taxon, close
to the base or highly derived, can be strongly biased by the
incomplete taxon sampling.
The monophyletic status of most of the gastrotrich
genera is not challenged and for many taxa, very specific
generic diagnoses with unique characters (putative auta-
pomorphies) have been published, which indicates that
genera indeed represent natural units. However, definite
tests on monophyly have not been carried out very often
(see, e.g., Kieneke 2010 for the genus Thaumastoderma).
When we think about monophyly of the traditional fami-
lies of Gastrotricha, the situation is getting much more
difficult. For instance, Turbanellidae and Thaumastoder-
matidae (Macrodasyida) or Xenotrichulidae, Dasydytidae,
and Proichthydidae (Paucitubulatina) turned out to form
monophyletic clades according to different analyses (e.g.,
Hochberg & Litvaitis 2000, 2001a, Todaro et al. 2006a,
2011a, 2012b, Kieneke etal. 2008a, Leasi & Todaro 2008,
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92 1Gastrotricha
1.6Systematics
In the following, we give a short overview on the diver-
sity of gastrotrichs. There are some excellent sources to
approach gastrotrich systematics. For marine taxa, mac-
rodasyids, and chaetonotids, Todaro & Hummon (2008)
provide a useful key to the genera and Hummon & Todaro
(2010) give an exhaustive species list with synonyms and
some taxonomic remarks. See also Ruppert (1988) for an
overview. The most extensive guide to freshwater chae-
tonotids, though in German language, is from Schwank
(1990) for Central European species. Balsamo & Todaro
(2002) provide a recent key to the freshwater genera.
There are attempts to build a video database (Hummon
etal. 2005). Very helpful in terms of taxonomy and syste-
matics of Gastrotricha is the regularly updated webpage
“Gastrotricha World Portal” of Antonio Todaro (http://
www.gastrotricha.unimore.it/). We list here 801 species of
currently known gastrotrichs.
When describing or determining gastrotrichs, it is
important to have some sense for potential intraspecific
variability. For example, in those chaetonotids with cuticu-
lar scales, it is important to know whether the scale patterns
are fixed or variable and, if so, in which range. It is assumed
that some variability exists (Forneris 1966), but very little is
known about the extent of this phenomenon. Amato & Weiss
(1982) approached this problem in clones of Lepidodermella
squammata and found some differences in the scale pattern
as well as some asymmetries. In macrodasyids, some vari-
ation, especially in the position and probably also in the
number of adhesive tubes, appears to be possible.
Recently, molecular approaches, especially the “bar-
coding” of species by investigation of genes, preferenti-
ally the cytochrome oxidase 1, are applied in many animal
taxa and often reveal cryptic species among morphologi-
cally indistinguishable populations. In gastrotrichs, such
approaches are still at the beginning, but will be of great
help to distinguish species in the future (see below under
Biogeography for an example).
In the following, we briefly characterize both orders
(Macrodasyida and Chaetonotida), the suborder Pau-
citubulatina, as well as all families and genera of gast-
rotrichs. We do not provide full taxonomic diagnoses;
however, several characteristic features of each taxon
are given. Species are listed, but not further described.
Below the order/suborder level, categories other than
genus and family are not included here (there are, for
instance, some subfamilies and subgenera). Redun-
dant categories are given in parenthesis, e.g., when a
family includes only one genus. The systematics follo-
wed below is mainly based on Hummon & Todaro (2010)
of the phylum Gastrotricha is not yet clearly resolved.
Different shared morphological characters of the Gast-
rotricha and the Cycloneuralia (e.g., a stratified cuticle,
a terminal mouth opening, a cuticle-lined myoepithelial
sucking pharynx) have been regarded as synapomor-
phies that support a clade Nemathelminthes (Ahlrichs
1995, Ehlers etal. 1996, Ax 2003). However, none of the
expanding number of DNA sequence-based cladistic
analyses has ever revealed a sister group relationship
between gastrotrichs and cycloneuralians. Instead,
studies that using sequences of one to several gene
loci and more recently even data of whole transcripto-
mes (“expressed sequence tags”), repeatedly placed the
Gastrotricha into a protostomian “superphylum” known
as the Platyzoa (see Giribet 2002, Giribet et al. 2007).
Depending on the particular analysis, within Platyzoa,
Gastrotricha may either be allocated as sister group of
the Plathelminthes (e.g., Giribet etal. 2000, Dunn etal.
2008) or of the Gnathostomulida (e.g., Hejnol et al.
2009, Paps etal. 2009). The last mentioned analysis,
however, did not resolve the Platyzoa as a monophyletic
group (Paps etal. 2009). A clade Platyzoa was already
suggested by Cavalier-Smith (1998) with Gastrotricha
and Gnathostomulida as sister taxa united as the so-
called Monokonta. As diagnostic characters for Mono-
konta, Cavalier-Smith (1998) mentions the monocilia-
ted epidermis, the simple protonephridia, the compact
body organization, and the shared hermaphroditism.
However, all these characters more likely represent
plesiomorphies among the Bilateria (see, e.g., Schmidt-
Rhaesa 2007) rather than apomorphic features of a clade
Monokonta. Also, Zrzavý etal. (1998) revealed a sister
group relationship between Gastrotricha and Gnathos-
tomulida, called the Neotrichozoa, with their combined
analysis of molecular and morphological data. Further-
more, Schmidt-Rhaesa etal. (1998) discuss the possibi-
lity that Gastrotricha could be placed as the sister group
of a large clade comprising all molting animals – the
Ecdysozoa (=Cycloneuralia+Panarthropoda). Character
states that could support such a grouping are almost the
same ones as those used to support the Nemathelmin-
thes (see above): a stratified cuticle, a muscular sucking
pharynx, and a terminal mouth opening. However, such
a sister group relationship has not been revealed by
DNA sequence-based phylogenetic analyses, so far. In
summary, there are four potential sister groups for the
phylum Gastrotricha: Cycloneuralia, Plathelminthes,
Gnathostomulida (or Gnathifera as a whole), or Ecdyso-
zoa (Fig. 1.54). Hence, resolving the phylogenetic posi-
tion of the Gastrotricha still remains a major task for
evolutionary-systematic research.
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1.6Systematics 93
flat cross section; the body is strap-shaped, sometimes
very long and in some species with a delimited head;
no cuticular structures are present (“naked” cuticle);
the ventral cilia form paired longitudinal bands, which
may join anteriorly and posteriorly; the TbP are along
the blunt end of trunk; the pharyngeal pores are close
to pharynx-intestine transition; the radial pharyngeal
musculature is striated; circular muscles are present in
lateral body wall; and Y-cells are absent.
Genus Cephalodasys Remane, 1926 (Fig. 1.55)
This genus includes Psammodasys (see d’Hondt 1974,
Hummon & Todaro 2010). The body is elongate, and a
head region is slightly delimited. The TbA are on fleshy
“hands” (Fig. 1.7 I). The ventral ciliation is on the entire
for marine taxa and Balsamo et al. (2009, 2014) for
freshwater taxa. These two publications are also the
source for the species lists, whereas new descriptions
since 2009/2010 have been added. See these publications
for synonyms, species inquirendae and nomina nuda.
1.6.1Order Macrodasyida Brunson, 1950
Remane (1924) introduced the name “Macrodasyoidea“
for the increasing number of marine gastrotrichs that were
morphologically different from the gastrotrichs known up
to that date. This name replaced the term “aberrant gast-
rotrichs” (in German original “aberrante Gastrotrichen”,
see also chapter Phylogeny), which was used for these
species (e.g., Remane 1924, 1925a, b, 1926a). Brunson
(1950) used the writing “Macrodasyida”, which was sug-
gested to be the preferable name by Chandrasekahara Rao
& Clausen (1970) (although these authors still used “Mac-
rodasyoidea”).
Macrodasyids are characterized by the presence of
adhesive tubes in different positions on the body, usually
on the ventral or lateral side of the head region (anterior
adhesive tubes, TbA), along the trunk in a lateral, dorsal,
or ventral position (lateral, dorsal, or ventral adhesive
tubes, TbL, TbD, TbV), and in the posterior end (poste-
rior adhesive tubes, TbP). The pharyngeal lumen has an
unpaired dorsal branch and paired ventrolateral bran-
ches (inverted Y-shaped). Pharyngeal pores are present in
most species. Almost all other characters, the body shape,
further appendages, cuticular structures, etc., are quite
variable.
Nine families are currently recognized: Cephalodasy-
idae, Dactylopodolidae, Lepidodasyidae, Macrodasyidae,
Planodasyidae, Thaumastodermatidae, Turbanellidae,
Xenodasyidae, and Redudasyidae.
1.6.1.1Family Cephalodasyidae Hummon & Todaro, 2010
The six genera Cephalodasys, Dolichodasys, Megadasys,
Mesodasys, Paradasys, and Pleurodasys were united
as Cephalodasyidae by Hummon & Todaro (2010); for-
merly, they belonged to the family Lepidodasyidae. Most
recently, Guidi etal. (2014) discovered different charac-
ters of the reproductive system and the spermatozoa
shared between Megadasys and Crasiella and therefore
assigned Megadasys to the family Planodasyidae (see
below). Some characters of species in Cephalodasyidae,
especially in comparison to Lepidodasys, are the fol-
lowing (from Hummon & Todaro 2010): a more or less
100 µm
Fig. 1.55: Horizontal view of Cephalodasys sp. (Macrodasyida,
Cephalodasyidae) from sublittoral calcareous sand around Lee
Stocking Island, Bahamas. Note the characteristic neck constriction
at the level of the anterior adhesive tubes (triangle). DIC image.
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94 1Gastrotricha
ventral surface; it is dense in the anterior region and
fades toward the posterior.
Twelve species are known from the eastern North
Atlantic coast, the Baltic Sea, the Mediterranean Sea, the
Red Sea, the Caribbean, and the Indian Ocean around
India: C. cambriensis (Boaden, 1963), C. caudatus Chand-
rasekhara Rao, 1981, C. dolichosomus Hummon, 2011,
C. hadrosomus Hummon, Todaro & Tongiorgi, 1993,
C. littoralis Renaud-Debyser, 1964, C. maximus Remane,
1926, C. miniceraus Hummon, 1974, C. pacificus Schmidt,
1974, C. palavensis Fize, 1963, C. saegailus Hummon,
2011, C. swedmarki Hummon, 2008, and C. turbanelloides
(Boaden, 1960).
Genus Dolichodasys Gagné, 1977
Dolichodasys is characterized by the following characters
(after Ruppert & Shaw 1977). It has a large body size (up to
2.7 mm). One or two fused TbA are on each body side, TbL
are absent or only present as indistinct adhesive papil-
lae. TbP patterns vary from one single to several adhesive
tubes, with distinct changes during development (Gagné
1977). The ventral ciliation is in four bands in the anterior
end and two bands along the trunk. The small pharyngeal
pores are close to the pharynx-intestine junction. Sperma-
tozoa are aberrant, commaform, and probably aflagellate.
Three species are known from the eastern and western
coasts of the Atlantic: D. carolinensis Ruppert & Shaw,
1977, D. delicatus Ruppert & Shaw, 1977, and D. elongatus
Gagné, 1977.
Genus Mesodasys Remane, 1951 (Fig. 1.56)
No head region is delimited. TbA are several to many; in
most species, they are in a traverse row or arc. Many short
TbL are present, and sometimes, additional ventral or even
dorsal (M. ischiensis, see Hummon et al. 1993) adhesive
tubes are present. TbP are along the posterior margin of the
slender terminal end or on a broad caudal plate. The pha-
ryngeal pores are close to the pharynx-intestine junction.
A further peculiarity of Mesodasys are the posteriorly direc-
ted sperm ducts, which directly discharge into the caudal
organ (e.g., Ferraguti & Balsamo 1994, Fregni etal. 1999).
Eight species were described from the North Sea and
western Atlantic, the eastern Atlantic (Carolina), the Medi-
terranean Sea, the Caribbean and India: M. adenotubu-
latus Hummon, Todaro & Tongiorgi, 1993, M. britanicus
Hummon, 2008, M. hexapodus Chandrasekhara Rao &
Ganapati, 1968, M. ischiensis Hummon, Todaro & Tongiorgi,
1993, M. laticaudatus Remane, 1951, M. littoralis Remane,
1951, M. rupperti Hummon, 2008, and M. saddlebackensis
Hummon, 2010.
0.5 mm
co
tes
vd
Fig. 1.56: Ventral view of Mesodasys cf. laticaudatus (Macrodasyida,
Cephalodasyidae) from sublittoral sand of the Ria de Ferrol, Spain.
Abbreviations: co, caudal organ; tes, testis; vd, conspicuous
swelling of the vas deferens. BF image.
Genus Paradasys Remane, 1934 (Fig. 1.57)
In most species, a strong ciliation is present around the
head region, and the ventral ciliation extends in two
ventral bands along the trunk. There are one or two
closely located TbA; TbL are absent. Several TbP are
either along the posterior margin or on paired caudal
feet. A ciliated muzzle is around the small mouth
opening, the pharyngeal pores are close to the pharynx-
intestine junction. Apart from two species (Paradasys
lineatus and P. littoralis), no traces of male gonads have
been found in the remaining ones so far. This could
indicate a parthenogenetic reproduction (see Wilke
1954).
Seven species with wide, but scattered distribution
(Baltic Sea, western North Atlantic, India, Japan, Galapa-
gos) are known: P. bilobocaudus Hummon, 2008, P. hexa-
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1.6Systematics 95
lateral row. At about the middle level of the trunk, an
appendage composed of three long adhesive tubes is
present. TbP are along the rounded posterior edge.
1.6.1.2Family Dactylopodolidae Strand, 1929
This family contains three genera, which all have in
common a more or less tenpin-shaped body form, a
well-delimited head, and the presence of cross-striated
muscles. The pharyngeal pores are close to pharynx-
intestine junction. Three genera, Dactylopodola, Dend-
rodasys, and Dendropodola are included in this family.
Genus Dactylopodola Strand, 1929 (Fig. 1.59)
Originally named Dactylopodella (Remane 1926a), the
genus had to be renamed because the name was preoc-
cupied. Strand’s (1929) proposition of Dactylopodola was
2months earlier than Remane’s (1929) Dactylopodalia and
therefore is the valid genus name (Blake 1933).
Apart from the family characters, Dactylopodola species
have bilateral posterior feet carrying the TbP. Most species
have few TbL. Some species have eyes, and in some species,
the TbA are on fleshy hands. See Hummon & Todaro (2010)
for synonyms and Von und zu Gilsa etal. (2014) for an over-
view and an updated determination key to species.
Nine species are known from scattered locations
in the entire world, ranging from Australia to India, the
Caribbean, and the western Atlantic: D. australiensis
Hochberg, 2003, D. axi Von und zu Gilsa, Kieneke, Hoch-
berg & Schmidt-Rhaesa, 2014, D. baltica (Remane, 1926b),
D. cornuta (Swedmark, 1956), D. deminuitubulata Von und
zu Gilsa, Kieneke, Hochberg & Schmidt-Rhaesa, 2014, D.
indica (Chandrasekhara Rao & Ganapati, 1968), D. meso-
typhle Hummon, Todaro, Tongiorgi & Balsamo, 1998, D.
roscovita (Swedmark, 1967), and D. typhle (Remane, 1927).
Genus Dendrodasys Wilke, 1954 (Fig. 1.60)
The species have a well-delimited head; in some species,
with lateral extensions. There is only one pair of solid TbA.
TbL are lacking. The caudal end is elongated and terminally
bifurcated. One large adhesive tube is on the basis of each
caudal branch, and two smaller adhesive tubes are on the
caudal end of each branch. Very conspicuous is the pre-
sence of cilia in the pharynx and in the hindgut. These are
present at least in D. affinis and D. gracilis (Wilke 1954); they
were not observed in D. pacificus (Schmidt 1974). The pha-
ryngeal cilia seem to function as a kind of weir to filter par-
ticles when water is extruded through the pharyngeal pores.
A pair of testes or a single testis are present.
100 µm
vc?
ov
mg
Fig. 1.57: Horizontal view of Paradasys subterraneus (Macrodasyida,
Cephalodasyidae) from the beach slope of Schillig, Germany.
Abbreviations: mg, midgut; ov, ovary; vc?, presumptive vitellocytes.
DIC image.
dactylus Karling, 1954, P. lineatus Chandrasekhara Rao,
1980, P. littoralis Chandrasekhara Rao & Ganapati, 1968,
P. nipponensis Sudzuki, 1976, P. pacificus Schmidt, 1974,
and P. subterraneus Remane, 1934.
Genus Pleurodasys Remane, 1927 (Fig. 1.58 A–C)
There is probably only one species in this genus,
P. helgolandicus Remane, 1927 (see Hummon & Todaro
2010), which was found in the western Atlantic. Most
conspicuous are the unique “drumstick-like” organs on
the ventral side behind the head. These were investiga-
ted by Marotta etal. (2008) and may be gravity recep-
tors (see also chapter Sensory Structures). The head
is distinctly separated from trunk. TbA originate from
short fleshy hands; TbL are in a lateral and a dorso-
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96 1Gastrotricha
100 µm
mo
pp
Fig. 1.59: Ventral view of Dactylopodola typhle (Macrodasyida,
Dactylopodolidae) from the intertidal beach of Saint-Lunaire,
France. Abbreviations: mo, mature egg; pp, pharyngeal pores at the
level of the neck constriction. BF image.
100 µm
50 µm
50 µm
mo
gr
AB
CFig. 1.58: Pleurodasys helgolandicus
(Macrodasyida, Cephalodasyidae) from the
intertidal beach of Saint-Lunaire, France.
(A) Habitus of a subadult specimen in
dorsal view. (B) Dorsal view of the anterior
end with the conspicuous gravireceptor
organs. (C) Ventral view of the anterior
end. Note the hand-like arranged anterior
adhesive tubes (triangles). Abbreviations:
gr, external portion of gravireceptor organs,
mo, mouth opening. (A) DIC image. (B and
C) BF images.
Lee, Chang & Kim, 2014, D. gracilis Wilke, 1954, D. pacifi-
cus Schmidt, 1974, D. ponticus Valkanov, 1957, and D. rubo-
marinus Hummon, 2011.
Genus Dendropodola Hummon, Todaro & Tongiorgi, 1993
One species, D. transitionalis Hummon (Todaro & Tongi-
orgi, 1993) was described in this genus. It resembles Dac-
tylopodola with a tenpin shape and a well-delimited head.
The caudal end is elongated, a pair of TbP is present at the
base of the extension, and another pair at its tip. There
are three pairs of TbL along the trunk and one pair
of TbA. The pharynx is relatively long, the pharyngeal pores
are close to the pharynx-intestine junction and behind the
head constriction (see Hummon etal. 1993 for more data).
1.6.1.3[Family Lepidodasyidae Remane, 1927]
Genus Lepidodasys Remane, 1926 (Fig. 1.61)
After removal of six genera to Cephalodasyidae (see
above), Lepidodasyidae contains only one genus, Lepi-
dodasys, with the following characteristics (especially
in comparison to Cephalodasyidae) (from Hummon
& Todaro 2010): The specimens are circular in cross
section, the body is strap-shaped, without a delimi-
ted head. The body is covered with conspicuous scales
(Fig. 1.4 F). Pharyngeal pores absent, a very unique feature
Six species are known from the Mediterranean Sea,
the Black Sea, the Red Sea, the East China Sea, the Sea
of Japan, and Galapagos: D. affinis Wilke, 1954, D. duplus
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1.6Systematics 97
50 µm
50 µm
TbA
A
B
TbP
Fig. 1.60: Dendrodasys cf. gracilis (Macrodasyida,
Dactylopodolidae) from the sublittoral of Ria de Ferrol, Spain.
Note that the specimen is slightly twisted. (A) More ventral view.
(B) More dorsal view. Abbreviations: TbA, anterior adhesive tubes;
TbP, posterior adhesive tubes. (A and B) BF images.
1.6.1.4Family Macrodasyidae Remane, 1926
This family unites the two genera Macrodasys and Uro-
dasys. Both are strap-shaped gastrotrichs with anterior,
lateral, and posterior adhesive tubes, a medium-sized
mouth opening, pharyngeal pores significantly anterior
of the pharynx-intestine junction and usually a ventral
ciliation covering the entire ventral side. The posterior
end terminates in many species in an unpaired tail. Alt-
hough this tail is moderately long in Macrodasys, it is
very long in Urodasys species.
Genus Macrodasys Remane, 1924 (Fig. 1.62)
The TbA are usually in bilateral rows, TbL occur along
the entire trunk and TbP are present in various distribu-
tion and density on the posterior region of the animals. A
clear-cut delimitation between TbL and TbP is often not
possible. Species of Macrodasys generally possess well-
developed frontal and caudal organs.
This is a species-rich genus with 36 species described to
date; they occur in many places in the world oceans: M. ach-
radocytalis Evans, 1994, M. acrosorus Hummon & Todaro,
2009, M. affinis Remane, 1936, M. africanus Remane, 1950,
among macrodasyids. The radial pharyngeal muscula-
ture is not striated. TbP are present along the blunt end
of trunk. Y-cells are present; they contain myofibrils. Cir-
cular muscles in the body wall were claimed to be absent
(Hummon & Todaro 2010), but were recently shown with
phalloidin staining (Hochberg etal. 2013). Lepidodasys
species are slowly gliding, their scale pattern is the most
important taxonomic feature (Hochberg & Atherton 2011,
Lee & Chang 2011, Hochberg etal. 2013).
Nine species are known from the North Atlantic,
the Caribbean, the Mediterranean Sea, and the western
Pacific around Korea (see Hochberg etal. 2013). A key to
species is provided by Lee & Chang (2011). Species are:
L. arcolepis Clausen, 2004, L. castoroides Clausen, 2004,
L. laeviacus Lee & Chang, 2011, L. ligni Hochberg, Ather-
ton & Gross, 2013, L. martini Remane, 1926, L. platyurus
Remane, 1927, L. tsushimaenensis Lee & Chang, 2011,
L. unicarenatus Balsamo, Fregni & Tongiorgi, 1994, and
L. worsaae Hochberg & Atherton, 2011.
200 µm
Fig. 1.61: Lepidodasys sp. (Macrodasyida, Lepidodasyidae) from
coral sand of Lee Stocking Island, Bahamas. Note the characteristic
keeled scales on the surface. DIC image.
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98 1Gastrotricha
M. nobskaensis Hummon, 2008, M. ommatus Todaro & Leasi,
2013, M. pacificus Schmidt, 1974, M. plurosorus Hummon,
2008, M. remanei Boaden, 1963, M. scleracrus Hummon,
2011, M. stenocytalis Evans, 1994, M. syringodes Hummon,
2010, M. thuscus Luporini, Magagnini & Tongiorgi, 1973,
and M. waltairensis Chandrasekhara Rao & Ganapati, 1968.
Genus Urodasys Remane, 1926 (Fig. 1.63)
Species in this genus resemble Macrodasys in many res-
pects, but are clearly recognizable by the extremely long
M. ancocytalis Evans, 1994, M. andamanensis Chandrasek-
hara Rao, 1993, M. balticus Roszczak, 1939, M. blysocytalis
Evans, 1994, M. buddenbrocki Remane, 1924, M. caudatus
Remane, 1927, M. celticus Hummon, 2008, M. cephalatus
Remane, 1927, M. cunctatus Wieser, 1957, M. deltocyta-
lis Evans, 1994, M. digronus Hummon & Todaro, 2009, M.
dolichocytalis Evans, 1994, M. fornerisae Todaro & Rocha,
2004, M. gerlachi Papi, 1957, M. gylius Hummon, 2010, M.
hexadactylis Chandrasekhara Rao, 1970, M. imbricatus
Hummon, 2011, M. lakshadweepensis Hummon, 2008,
M. macrurus Hummon, 2011, M. meristocytalis Evans, 1994,
M. neapolitanus Papi, 1957, M. nigrocellus Hummon, 2011,
100 µm
100 µm
AB
co
mo
TbP
Fig. 1.62: Two undetermined specimens of Macrodasys
(Macrodasyida, Macrodasyidae) from the Caribbean Sea.
(A) Specimen from the sublittoral around Little Caiman Island,
horizontal view. (B) Individual from coral sand of Lee Stocking
Island, Bahamas. The tail with the posterior adhesive tubes
is in focus. Abbreviations: co, caudal organ; mo, mature eggs;
TbP, posterior adhesive tubes. (A and B) DIC images.
100 µm
ta
Fig. 1.63: Urodasys sp. (Macrodasyida, Macrodasyidae) from San
Salvador Island, Bahamas. The tail with the posterior adhesive
tubes is strongly contracted. Abbreviations: ta, tail. DIC image.
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1.6Systematics 99
be of unequal size. In several species, the posterior part
of the intestine has an S-shaped course.
Eight species have been described from the western
North Atlantic, the Caribbean Sea, the Indian Sea, the East
China Sea, and the Pacific around Galapagos: C. azorensis
Hummon, 2008, C. clauseni Lee & Chang, 2012, C. diplura
Clausen, 1968, C. fonseci Hochberg, 2014, C. indica Chand-
rasekhara Rao, 1981, C. oceanica d’Hondt, 1974, C. pacifica
Schmidt, 1974, and C. skaia Hummon, 2010. A determina-
tion key to species is provided in Lee & Chang (2012).
Genus Megadasys Schmidt, 1974 (Fig. 1.65)
Two species were described in the same year under diffe-
rent genus names, and because of a slightly earlier pub-
lication, the name Megadasys (Schmidt 1974) is valid and
Thiodasys (Boaden 1974) is not (see Kisielewski 1987b).
Specimens are very long and slender (up to >3 mm). They
lack TbA; short TbL are numerous along the trunk and
several TbP are on a caudal lobe along the posterior
edge. The pharyngeal pores are close to pharynx-intes-
tine junction, with a probable more anterior position in
M. pacificus (see Schmidt 1974) (see Kisielewski 1987b for
more information on the genus).
and contractile tail. Some species show peculiarities in
their reproductive anatomy or biology, such as the presence
of stylets (Fig. 1.36 G, H) or vivipary (Fig. 1.50 B).
Fifteen species are known from the western and eastern
North Atlantic, the Baltic Sea, the Mediterranean Sea, the
Caribbean, the Maledives, and French Polynesia: U. acan-
thostylis Fregni, Tongiorgi & Faienza, 1998, U. anorektoxys
Todaro, Bernhard & Hummon, 2000, U. apuliensis Fregni,
Faienza, Grimaldi, Tongiorgi & Balsamo, 1999, U. bucinasty-
lis Fregni, Faienza, Grimaldi, Tongiorgi & Balsamo, 1999, U.
calicostylis Schoepfer-Sterrer, 1974, U. cornustylis Schoepfer-
Sterrer, 1974, U. elongatus Renaud-Mornant, 1969, U. mira-
bilis Remane, 1926, U. nodostylis Schoepfer-Sterrer, 1974,
U. poculostylis Atherton, 2014, U. remostylis Schoepfer-
Sterrer, 1974, U. spirostylis Schoepfer-Sterrer, 1974,
U. toxistylis Hummon, 2011, U. uncinostylis Fregni,
Tongiorgi & Faienza, 1998, and U. viviparus Wilke, 1954.
1.6.1.5 Family Planodasyidae Chandrasekhara Rao &
Clausen, 1970
When Clausen (1968) introduced the genus Crasiella, he
was not sure about its placement among known gastro-
trichs. After the description of Planodasys marginalis
(Chandrasekhara Rao & Clausen 1970), the family Pla-
nodasyidae was introduced to unite these two genera.
Species of both genera possess caudal feet with the TbP.
They also have a “corona”, i.e., a ring of cuticular struc-
tures around the mouth opening and a buccal cavity in
common. Recently, Guidi et al. (2014) assigned a third
genus, Megadasys (formerly included within Cephaloda-
syidae, see above) to Planodasyidae. An amended diag-
nosis of Planodasyidae, now comprising the three genera
Crasiella, Megadasys, and Planodasys, is presented, but
shared characters between Megadasys and Crasiella are
mainly ultrastructural features of their spermatozoa (see
Guidi etal. 2014).
Genus Crasiella Clausen, 1968 (Fig. 1.64)
Species have small, sometimes hardly distinguishable
caudal feet carrying the TbP. A head is delimited in some
species, but not in others. The ventral side is covered
either entirely by cilia or cilia are in paired longitudi-
nal rows. The mouth opening is surrounded by a ring
of hook-like structures, and a buccal cavity is present.
The pharyngeal pores are in the posterior part of the
pharynx, close to the pharynx-intestine junction. The
TbA are in some species in continuity of the ventrolate-
ral TbL (e.g., C. azorensis), but in others clearly separa-
ted and form paired diagonal rows (e.g., C. oceanica, see
Hummon 2008a). The TbL are scarce or dense, they may
100 µm
Fig. 1.64: Crasiella cf. diplura (Macrodasyida, Planodasyidae) from
sublittoral sand of the island Elba, Italy. BF image.
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100 1Gastrotricha
Three species are known from the western Atlantic
coasts and Galapagos: M. minor Kisielewski, 1987, M. paci-
ficus Schmidt, 1974, and M. sterreri (Boaden, 1974).
Genus Planodasys Chandrasekhara Rao & Clausen, 1970
Specimens are quite large, up to 0.8mm in P. littoralis and
up to 1.5mm in P. marginalis. The caudal feet are clearly
demarcated and appear as lobe-like structures covered
with TbP. The TbA are arranged in a medially interrup-
ted crescent. A head region is not delimited. TbL are
numerous in P. marginalis (120–140), whereas P. littoralis
has fewer (about 30) (see Chandrasekhara Rao & Clausen
1970 and Chandrasekhara Rao 1993).
There are two species, both from the Bay of Bengal in
the Indian Ocean: P. littoralis Chandrasekhara Rao, 1993,
and P. marginalis Chandrasekhara Rao & Clausen, 1970.
1.6.1.6Family Thaumastodermatidae Remane, 1927
Species in this large family are very diverse. Ruppert (1978b)
has given an amended diagnosis including the following
characters: usually caudal feet are present, the body is often
covered with cuticular structures, TbL are often in a vent-
rolateral position, epidermal cells are multiciliary, radial
parynx musculature is reduced, pharyngeal pores are small,
and at the end of the pharynx, Y-cells contain myofibrils,
the caudal organ is well developed and close to the anus,
oviduct is present. Ruppert (1978b) proposed two subfami-
lies, Thaumastodermatinae (including genera Thaumas-
toderma, Tetranchyroderma, Oregodasys, Pseudostomella,
and Ptychostomella) and Diplodasyinae (including genera
Acanthodasys and Diplodasys), with Hemidasys being of
uncertain assignment. The most conspicuous difference is
that the left side of the gonad is reduced in Thaumastoder-
matinae. This is most obvious in the testis, which is only
present on the right side of animals (Fig. 1.36 C), whereas the
unpaired (right) ovary is often more or less central in posi-
tion. Diplodasyinae retain the paired nature of the gonad.
Eight genera (Acanthodasys, Diplodasys, Hemidasys, Orego-
dasys, Pseudostomella, Ptychostomella, Tetranchyroderma,
and Thaumastoderma) belong to this family.
Genus Acanthodasys Remane, 1927 (Fig. 1.66 A–C)
Species are slender and covered with cuticular spines,
which are often called uniancres. These are spined
scales. Unspined scales are additionally present in some
species. Adhesive tubes are very variable. TbA are in
diverse arrangements on the anterior end; TbL can be in
dorsolateral or ventrolateral distribution or completely
lacking. The TbP are along the posterior margin or on
small caudal feet. Several new species names were men-
tioned by Ruppert (1978b), but full species descriptions
were not provided. Hence, each of these names is con-
sidered as nomen nudum (see Hummon & Todaro 2010).
Clausen (2004a) gives a key to the five species known at
that time.
Twelve species are known from both sides of the
North Atlantic, the Caribbean, the Mediterranean Sea, the
Maledives, the seas around Korea and India: A. aculeatus
Remane, 1927, A. algarvensis Hummon, 2008, A. arcasso-
nensis Kisielewski, 1987, A. caribbeanensis Hochberg &
Atherton, 2010, A. carolinensis Hummon, 2008, A. comtus
Lee, 2012, A. ericinus Lee, 2012, A. fibrosus Clausen, 2004,
A. flabellicaudus Hummon & Todaro, 2009, A. lineatus
Clausen, 2000, A. paurocactus Atherton & Hochberg, 2012,
and A. silvulus Evans, 1992.
Genus Diplodasys Remane, 1927 (Fig. 1.67 A, B)
This genus includes flattened specimens with a dorsal
covering of flat scales (Figs. 1.4 A and 1.67 B). Scales are
also present on the ventral side; the ventral distribution of
cilia is often interrupted and appears in isolated patches.
0.5 mm
eg
co
Fig. 1.65: Megadasys minor (Macrodasyida, Planodasyidae) from
sublittoral sand of the island Elba, Italy. Abbreviations: co, caudal
organ; eg, epidermal glands. BF image.
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1.6Systematics 101
100 µm
50 µm
50 µm
ph
AB
C
tes
ov
Especially the dorsal scales may exhibit different patterns
of ornamentation such as depressions, pores, or ridges. A
head region is usually visible, but this may depend on the
state of contraction of the animals (Kieneke etal. 2013b).
Very characteristic is the presence of a row of strong
spines along the lateral margin of the trunk (Fig. 1.4 I).
The TbA are in varying number and arrangement on the
ventral side of the head region. TbL are present in paired
ventrolateral rows, and TbP are present on either caudal
feet or on the posterior margin.
Ten species have been described from diverse loca-
tions in the world oceans (eastern North Atlantic, Medi-
terranean Sea, Caribbean, Galapagos, Indian Ocean):
D. ankeli Wilke, 1954, D. caudatus Kisielewski, 1987,
D. meloriae Todaro, Balsamo & Tongiorgi, 1992, D. minor
Remane, 1936, D. pacificus Schmidt, 1974, D. platydasy-
oides Remane, 1927, D. remanei Chandrasekhara Rao &
Ganapati, 1968, D. rothei Kieneke, Narkus, Hochberg &
Schmidt-Rhaesa, 2013, D. sanctimariae Hummon & Todaro,
2009, and D. swedmarki Kisielewski, 1987.
Genus Hemidasys Claparéde, 1867
Hemidasys agaso was the second species of Macrodasyida
to be described (Claparéde 1867). It was found in muddy
sediments of the port of Naples (Mediterranean Sea), both
free living and epizoic on the polychaete Neanthes cau-
datus (Claparéde 1867). Since then, it has not been found
again, despite repeated attempts (see Hummon & Todaro
2010).
Hemidasys agaso, the single species in the genus, has
a narrow mouth opening, and a large buccal cavity being
covered by something like an oral hood. Ventral cilia are
present only in the anterior body region and few cuticu-
lar plates are found in the region of the male genital pore.
TbA are in one row, TbL are few.
Genus Oregodasys Hummon, 2008 (Fig. 1.68 A, B)
Remane (1927a) introduced the genus Platydasys, but
because this name was preoccupied, Hummon (2008a)
renamed it as Oregodasys. Specimens are very flat and
broad, and some can be quite large (up to 800 µm in
Fig. 1.66: Acanthodasys aculeatus
(Macrodasyida, Thaumastodermatidae)
from the shallow sublittoral of Elba, Italy.
(A) Habitus in horizontal view. (B) Dorsal
view of the anterior end covered with
cuticular uniancres and small scales.
(C) Ventral view of the posterior end with
the caudal pedicles and posterior adhesive
tubes. Abbreviations: ov, ovary; ph,
pharynx; tes, testes. (A–C) BF images.
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102 1Gastrotricha
50 µm
100 µm
AB
lsp
TbVL
P. ruber and P. tentaculatus, Swedmark 1956). The broad
mouth opening is directed anteroventrally. Eyes are
present in some species (O. ocellatus, O. norenburgi).
The body is covered by papillae. TbA are present
along the posterior margin of the mouth opening
and in irregular arrangement posterior of it. TbL are
50 µm100 µm
AB
pp
TbP
mg
Fig. 1.68: (A) Oregodasys cirratus
(Macrodasyida, Thaumastodermatidae) from
sand out of a submarine cave on Tenerife,
Canary Islands. Dorsal view showing the
numerous secretory papillae. (B) Subadult
specimen of Oregodasys caymanensis
from Little Cayman Island. Abbreviations:
mg, midgut; pp, pharyngeal pores; TbP,
posterior adhesive tubes. (A and B) DIC
images. (Micrograph in A was from
Rothe & Schmidt-Rhaesa 2010, with kind
permission by Verlag Dr. Friedrich Pfeil.)
Fig. 1.67: (A) Diplodasys cf. meloriae
(Macrodasyida, Thaumastodermatidae)
from calcareous sand of Lee Stocking
Island, Bahamas. Ventral view with focus on
adhesive tubes. (B) Close-up of the dorsal
scales of D. rothei from Norman’s Pond Cay,
Bahamas. Abbreviations: lsp, lateral spines,
TbVL ventrolateral adhesive tubes. (A and
B) DIC images. (Micrograph in B was from
Kieneke etal. 2013b, with kind permission
by Verlag Dr. Friedrich Pfeil.)
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1.6Systematics 103
present in a lateral and a ventral row, and TbP are
either along the posterior margin or on small
caudal feet. In six species, cirri (=compound cilia) are
present. These cirri are present in the posterior part or, in
O. cirratus, in a row along the entire trunk. See Hochberg
(2010a) and Rothe & Schmidt-Rhaesa (2010) for more
information.
Fifteeen species have been described to date with
distribution in the eastern North Atlantic including the
Canary Islands, the Mediterranean, the Caribbean, Gala-
pagos, and Japan: O. caymanensis Hochberg, Atherton &
Kieneke, 2014, O. cirratus Rothe & Schmidt-Rhaesa, 2010,
O. itoi (Chang, Kubota & Shirayama, 2002), O. kathari-
nae Hochberg, 2010, O. kurnowensis Hummon, 2008, O.
mastigurus (Clausen, 1965), O. maximus (Remane, 1927),
O. norenburgi Hochberg, 2010, O. ocellatus (Clausen,
1965), O. pacificus (Schmidt, 1974), O. phacellatus
(Clausen, 1965), O. rarus (Forneris, 1961), O. ruber (Swed-
mark, 1956), O. styliferus (Boaden, 1965), O. tentaculatus
(Swedmark, 1956).
Genus Pseudostomella Swedmark, 1956 (Fig. 1.69 A, B)
Species in the genus Pseudostomella are very distinctive
because they have very conspicuous anterior extensions,
the pre-buccal palps. These serve as grasping structures.
Papillae of different size can be present on these palps and
dorsal and ventral of the mouth rim. The mouth opening
is very broad. TbA are present along the ventral side of
the mouth opening. TbL are along the lateral sides of the
animals; additionally, a group of ventral adhesive tubes
is present in some species. The TbP are on small caudal
feet. Cuticular structures in the form of triancres, tetran-
cres, and pentancres, i.e., with three, four, or five tips are
present, the triancres can be in the form of scaled trian-
cres (or feathered triancres) (see Ruppert 1970, Hochberg
2002). Keys to species were provided by Ruppert (1970),
Lee & Chang (2002), Hochberg (2002), Clausen (2004b),
and Todaro (2012).
Sixteen species are currently known from diverse loca-
tions of the North Atlantic, the Mediterranean, the Indian
Ocean, Australia, Malaysia, and the western Pacific around
Korea: P. andamanica Chandrasekhara Rao, 1993, P. cata-
phracta Ruppert, 1970, P. cheraensis Pryialakshmi, Menon
& Todaro, 2007, P. dolichopoda Todaro, 2012, P. etrusca
Hummon, Todaro & Tongiorgi, 1993, P. faroensis Clausen,
2004, P. indica Chandrasekhara Rao, 1970, P. klauserae
Hochberg, 2002, P. koreana Lee & Chang, 2002, P. longifurca
Lee & Chang, 2002, P. malayica Renaud-Mornant, 1967,
P. megapalpator Hochberg, 2002, P. plumosa Ruppert, 1970,
P. roscovita Swedmark, 1956, P. squamalongispina Araujo,
Balsamo & Garraffoni, 2013, and P. triancra Hummon, 2008.
50 µm50 µm
AB
pa
Fig. 1.69: Pseudostomella roscovita (Macrodasyida,
Thaumastodermatidae) from the intertidal beach in Saint-Lunaire,
France. (A) Horizontal view. (B) Dorsal view. Abbreviation: pa,
prebuccal apparatus. (A and B) BF images.
Genus Ptychostomella Remane, 1926
Species in this genus are short and straight. The mouth
opening is large, and the anterior rim is folded. Eyes are
present in one species (P. ommatophora). Some species
have tentacles. The TbA are in an arc, TbL are concentra-
ted in groups and may be lateroventral or ventral. The pos-
terior end forms lateroterminal tips of caudal feet, both
covered with TbP. Cuticular structures are either absent
(most species) or present on the dorsal side. However,
the characteristic hook-shaped ancres that occur in three
other genera of the subfamily Thaumastodermatinae
(Pseudostomella, Tetranchyroderma, Thaumastoderma)
are always absent in Ptychostomella. See Lee & Chang
(2003) for a comparison of species. Todaro (2013) provides
a key to species.
Thirteen species are currently known from the
eastern North Atlantic, the Baltic Sea, the Mediterranean,
and the Northwest Pacific (Korea): P. bergensis Clausen,
1996, P. brachycephala (Levi, 1954), P. helana Roszczak,
1939, P. higginsi Clausen, 2004, P. jejuensis Lee, Hwang &
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104 1Gastrotricha
most abundant structures (Fig. 1.4 D, E). Some species
do not have a complete covering by cuticular structures.
Usually, only one type of cuticular structures is present, but
some species have a mixture of different types. Cephalic
tentacles are present in few species. The mouth opening is
very broad, and the anterior mouth rim forms a characte-
ristic oral hood. Adhesive tubes occur in the usual groups,
TbA, TbL, and TbP; ventral and dorsal adhesive tubes on
the trunk are present in some species. Most, but not all
species have caudal feet, the TbP are present on these feet,
and in some species, additionally between the feet. Todaro
(2002) provides a helpful key to species of the genus.
Currently, 82 species have been described from many
locations in the world oceans: T. aapton Dal Zotto, Ghivi-
riga & Todaro, 2010, T. adeleae Hochberg, 2009, T. aethes-
bregmum Lee & Chang, 2012, T. anisoankyrum Lee 2012,
T. anomalopsum Hummon, Todaro, Balsamo & Tongiorgi,
1996, T. antenniphorum Hummon & Todaro, 2010, T. aphe-
nothigmum Hummon, Todaro, Tongiorgi & Balsamo, 1998,
T. apum Remane, 1927, T. arcticum Clausen, 1999, T. aus-
traliense Nicholas & Todaro, 2006, T. boadeni Schrom,
in Riedl 1970, T. boreale Clausen, 2000, T. bronchostylus
Atherton & Hochberg, 2012, T. bulbosum Clausen, 2000,
T. bunti (Thane-Fenchel, 1970), T. canariense Todaro,
Ancona, Marzano, D’Addabbo & De Zio Grimaldi, 2003,
T. cirrophorum Lévi, 1950, T. coeliopodium Boaden, 1963,
T. copicirratum Hummon, 2010, T. corallium Hummon,
2011, T. coreensis Lee, 2012, T. dendricum Saito, 1937,
T. dragescoi Swedmark, 1967, T. enallosum Hummon,
1977, T. esarabdophorum Tongiorgi & Balsamo, 1984,
T. faroense Clausen, 2004, T. gausancrum Hummon, 2008,
T. gracilium Chang, Lee & Clausen, 1998, T. heterotenta-
culatum Chang & Lee, 2001, T. heterotubulatum Hummon,
Todaro & Tongiorgi, 1993, T. hirtum Luporini, Magagnini
& Tongiorgi, 1973, T. hoonsooi Chang & Lee, 2001, T. hyp-
oniglarum Hummon & Todaro, 2009, T. hypopsilancrum
Hummon, Todaro & Tongiorgi, 1993, T. hystrix Remane,
1926, T. inaequitubulatum Todaro, Balsamo & Tongiorgi,
2002, T. indicum Chandrasekhara Rao & Ganapati, 1968,
T. insolitum Lee & Chang, 2012, T. insulare Balsamo,
Fregni & Tongiorgi, 1994, T. interstitiale Hummon, 2008,
T. kontosomum Hummon, Todaro, Balsamo & Tongiorgi,
1996, T. korynetum Hummon & Todaro, 2009, T. lameshu-
rense Hummon, 2008, T. littorale Chandrasekhara
Rao, 1981, T. longipedum Hummon, 2008, T. mainensis
Hummon & Guadiz, 2009, T. massilense Swedmark, 1956,
T. megabilubulatum Lee & Chang, 2012, T. megastomum
(Remane, 1927), T. monokerosum Lee & Chang, 2007,
T. multicirratum Lee & Chang, 2007, T. norvegicum Clausen,
1996, T. oblongum Lee, 2012, T. oligopentacrum Hummon
& Todaro, 2009, T. pachysomum Hummon, Todaro & Ton-
giorgi, 1993, T. pacificum Schmidt, 1974, T. papii Gerlach,
Chang, 2009, P. lamelliphora Todaro, 2013, P. lepidota
Clausen, 2000, P. mediterranea Remane, 1927, P. omm-
atophora Remane, 1927, P. orientalis Lee & Chang, 2003,
P. papillata Lee & Chang, 2003, P. pectinata Remane, 1926,
and P. tyrrhenica Hummon, Todaro & Tongiorgi, 1993.
Genus Tetranchyroderma Remane, 1926 (Fig. 1.70)
This species-rich genus includes stout to strap-shaped spe-
cimens with a covering of cuticular structures in the form
of triancres, tetrancres, or pentancres; pentancres are the
100 µm
Fig. 1.70: Tetranchyroderma sp. (Macrodasyida,
Thaumastodermatidae) from an intertidal beach close to Ribadeo,
Spain. BF image.
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1.6Systematics 105
spatulate tentacles and one pair of lateral tentacles
(Fig. 1.18 F and 1.71 A–C). Apart from T. renaudae, all remai-
ning species have another pair of anterior, rod-shaped
tentacles (Kieneke 2010). Very conspicuous are paired
dorsal appendages, the dorsal cirrata, which are present
in 4, 5, or 6 pairs. Kieneke (2010) provides an overview on
the characters and a phylogenetic analysis of the genus.
Seventeen species are currently known, most from
the eastern North Atlantic and the waters around Korea
and Japan; fewer species from the Baltic Sea, the Medi-
terranean, the western Atlantic (South Carolina), and
the Antarctic Deep Sea: T. antarctica Kieneke, 2010, T.
appendiculatum Chang, Lee & Clausen, 1998, T. arcas-
sonense d’Hondt, 1965, T. bifurcatum Clausen, 1991,
T. cantacuzeni Lévi, 1958, T. clandestinum Chang, Kubota
& Shirayama, 2002, T. copiophorum Chang, Lee & Clausen,
1998, T. coronarium Chang, Lee & Clausen, 1998, T. heideri
Remane, 1926, T. mediterraneum Remane, 1927, T. minan-
crum Hummon, 2008, T. moebjergi Clausen, 2005, T. nat-
lanticum Hummon, 2008, T. ramuliferum Clausen, 1965,
T. renaudae Kisielewski, 1987, T. swedmarki Lévi, 1950, and
T. truncatum Clausen, 1991.
1.6.1.7Family Turbanellidae Remane, 1927
Species are strap-shaped, and the head may be delimited
or not. Head appendages are present in some species. At
1953, T. paradoxum Thane-Fenchel, 1970, T. paralittorale
Chandrasekhara Rao, 1991, T. parapapii Hummon, 2009,
T. pentasperum Nicholas & Todaro, 2006, T. pinnatum
Lee, 2012, T. polyacanthum (Remane, 1927), T. polypodium
Luporini, Magagnini & Tongiorgi, 1971, T. polyprobolo-
stomum Hummon, Todaro, Balsamo & Tongiorgi, 1996,
T. psilotopum Hummon, Todaro, Tongiorgi & Balsamo,
1998, T. pugetense Wieser, 1957, T. quadritentacula-
tum Todaro, Balsamo & Tongiorgi, 1992, T. rhopalotum
Hummon, 2011, T. sanctaecaterinae Todaro, Balsamo &
Tongiorgi, 1992, T. sardum Todaro, Balsamo & Tongiorgi,
1988, T. schizocirratum Chang, Kubota & Shirayama, 2002,
T. sinaiensis Hummon, 2011, T. suecicum Boaden, 1960,
T. swedmarki Chandrasekhara Rao & Ganapati, 1968,
T. symphorochetum Hummon, Todaro, Tongiorgi & Balsamo,
1998, T. tanymesatherum Hummon, Todaro, Balsamo &
Tongiorgi, 1996, T. tentaculatum Chandrasekhara Rao,
1993, T. thysanogaster Boaden, 1965, T. thysanophorum
Hummon, Todaro & Tongiorgi, 1993, T. tribolosum Clausen,
1965, T. verum Wilke, 1954, T. weissi Todaro, 2002, and
T. xenodactylum Hummon, 2011.
Genus Thaumastoderma Remane, 1926 (Fig. 1.71 A–C)
The species in this genus resemble those of Tetranchyro-
derma in the general body shape. Their body is covered
exclusively with tetrancres. Additionally, specimens have
at least two pairs of cephalic appendages: one pair of
50 µm 50 µm
50 µm
AB
st
C
rt
Fig. 1.71: Thaumastoderma mediterraneum (Macrodasyida, Thaumastodermatidae) from the shallow sublittoral around Elba, Italy.
(A) Ventral view. (B) Horizontal view. (C) Dorsal view. Abbreviations: rt, rod-shaped tentacles; st, spatulate tentacles. (A–C) BF images.
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106 1Gastrotricha
the posterior end there is a pair of caudal feet with adhe-
sive tubes (TbP) on the posterior margin of the entire
foot. The arrangement of adhesive tubes is variable.
TbA are often concentrated on fleshy hands; TbL can be
numerous, strongly reduced in number, or completely
absent. In some species/genera, characteristically large
adhesive tubes are present. The ventral ciliation is usually
on the entire anterior region and in paired rows along the
trunk. The pharyngeal pores are in the posterior region
of the pharynx, with the exception of the genus Prosto-
buccantia, where they are significantly more anterior.
The family includes six genera: Desmodasys, Dinodasys,
Paraturbanella, Prostobuccantia, Pseudoturbanella, and
Turbanella.
Genus Desmodasys Clausen, 1965 (Fig. 1.72 A, B)
The genus includes two species from the coast of Norway
(eastern North Atlantic) and one species from the deep sea
at the East Pacific Rise. A head is more or less delimited;
ventral ciliation is in two bands (D. borealis and D. phoco-
ides) or on the entire ventral side (D. abyssalis). Eyes can
be present. A small buccal cavity is present, and the pha-
ryngeal pores are close to the pharynx-intestine junction.
The cuticle is smooth. TbL are absent, only sensory cilia
are arranged along the trunk. The TbA are arranged in
paired anteroventral tufts. TbP are on caudal feet.
The three species described to date are: D. abyssalis
Kieneke & Zekely, 2007, D. borealis Clausen, 2000, and
D. phocoides Clausen, 1965.
Genus Dinodasys Remane, 1927 (Fig. 1.73)
The two species of Dinodasys have a more or less well-
defined head, which is bordered by a pair of large
tentacles. Additional smaller “cephalic protrusions”
are present in different number on the dorsal and the
ventral side of the head. The TbA are on ventral fleshy
40 µm50 µm
AB
TbA
TbP
Fig. 1.72: Desmodasys abyssalis
(Macrodasyida, Turbanellidae), fixed
animals. (A) Specimen from the Antarctic
deep sea floor at depth of 5191 m, ventral
view. (B) Specimen from artificial tubeworm
aggregations deposited close to a
hydrothermal vent of the East Pacific Rise
at depth of 2500 m. Abbreviations: TbA,
anterior adhesive tubes; TbP, posterior
adhesive tubes. (A) DIC image. (B) SEM
micrograph.
100 µm
TbA
Fig. 1.73: Dinodasys mirabilis (Macrodasyida, Turbanellidae) from
sublittoral sand of the outer Jade Bay, Germany. Note the cylindric
buccal cavity. Abbreviation: TbA, anterior adhesive tubes. BF image.
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1.6Systematics 107
hands, the TbP on caudal feet. TbL are numerous. The
two species described were found on both sides of the
North Atlantic, in the North Sea, and on the coast of
Delaware: D. delawarensis Hummon, 2008, and D. mirabilis
Remane, 1927.
Genus Paraturbanella Remane, 1927 (Fig. 1.74 A–D)
Very conspicuous is a paired accessory adhesive organ
made up of a long and a shorter adhesive tube; this is
present at the level of the anterior region of the pharynx
(Fig. 1.74 D). TbA are on fleshy hands (Fig. 1.74 B); TbL are
few and quite small or may be absent at all; TbP are on the
caudal feet. A key to species was provided by Wieser (1957).
Twenty-two species are currently known from the
North Atlantic, the Mediterranean, the Caribbean, the
Pacific, India, and Australia: P. aggregotubulata Evans,
1992, P. armoricana (Swedmark, 1954), P. boadeni Chand-
rasekahara Rao & Ganapati, 1968, P. brevicaudata Chand-
rasekahara Rao, 1991, P. cuanensis Maguire, 1976, P. dohrni
Remane, 1927, P. dolichodema Hummon, 2010, P. eire-
anna Maguire, 1976, P. intermedia Wieser, 1957, P. levan-
tia Hummon, 2011, P. manxensis Hummon, 2008, P.
microptera Wilke, 1954, P. mesoptera Chandrasekahara
Rao, 1970, P. pacifica Schmidt, 1974, P. pallida Luporini,
Magagnini & Tongiorgi, 1971, P. palpibara Chandraseka-
hara Rao & Ganapati, 1968, P. pediballetor Hummon, 2008,
P. sanjuanensis Hummon, 2010, P. scanica Clausen, 1996,
P. solitaria Todaro, 1995, P. stradbroki Hochberg, 2002, and
P. teissieri Swedmark, 1954.
Genus Prostobuccantia Evans & Hummon, 1991
A single species, P. brocha Evans & Hummon, 1991, has
been described from Florida (Evans & Hummon 1991).
The most characteristic feature is a “corona”, an anterior
projection of the buccal cavity. The pharyngeal pores
are, unusual for a member of Turbanellidae, not close to
the pharyngointestinal border, but further anterior. The
TbA are on hands, TbL are present posterior of about
the level of the pharyngeal pores. Quite conspicuous is
a pair of a very long and a shorter adhesive tube shortly
behind the pharyngointestinal junction. The TbP are on
caudal feet.
Genus Pseudoturbanella d’Hondt, 1968
One species, P. stylifera d’Hondt, 1968, is known in this
genus, and it was found on the French Atlantic coast
(d’Hondt 1968). The TbA are on paired hands, one pair of
very large tubes attaches on the posterior margin of the
well delimited head. TbL are reduced to one single pair at
the level of the pharyngointestinal junction. The caudal
feet carry few adhesive tubes on their inner side and their
terminal end.
Fig. 1.74: Paraturbanella pacifica
(Macrodasyida, Turbanellidae) from
sublittoral sand of Little Cayman Island.
(A) Habitus in horizontal view. (B) Anterior
end in ventral view showing the hand-
like arranged anterior adhesive tubes.
(C) Ventral view of the posterior end. (D)
Anterior end focused on the peculiar lateral
accessory adhesive organs. Abbreviations:
an, anus; TbA, anterior adhesive tubes; lao,
lateral adhesive organ. (A–D) DIC images.
200 µm
50 µm 50 µm
100 µm
TbA
AB
D
C
lao
an
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108 1Gastrotricha
Genus Turbanella Schultze, 1853 (Fig. 1.75 A–C)
A head region is more or less clearly delimited; in some
species, there are lateral lobes (Fig. 1.75 A). TbA are on
fleshy hands (Fig. 1.75 B); TbL are abundant along the
entire trunk in almost all species, frequently arranged
in ventral, ventrolateral, lateral, dorsolateral and/or
dorsal series. TbP are on caudal feet (Fig. 1.75 C). An
unpaired, median cone is present between the two
caudal feet in many species. A key was provided by
Wieser (1957).
Twenty-nine species are currently known with a dis-
tribution in the Atlantic (both coasts of the North Atlantic
plus western South Atlantic and Caribbean), the Baltic Sea
(brackish), the Mediterranean and Black Sea, the Red Sea,
the Pacific (western coast of North and Central America,
Galapagos), India, and Australia: T. ambronensis Remane,
1943, T. aminensis Chandrasekahara Rao, 1991, T. amphiat-
lantica Hummon & Kelly, 2011, T. bengalensis Chandrase-
kahara Rao & Ganapati, 1968, T. bocqueti Kaplan, 1958,
T. brusci Hochberg, 2002, T. caledoniensis Hummon, 2008,
T. corderoi Dioni, 1960, T. cornuta Remane, 1925, T. ery-
throthalassia Hummon, 2011, T. hyalina Schultze, 1853,
T. indica Chandrasekahara Rao, 1981, T. lutheri Remane,
1952, T. mikrogada Hummon, 2008, T. multidigitata Kisie-
lewski, 1987, T. mustela Wieser, 1957, T. ocellata Hummon,
1974, T. otti Schrom, 1972, T. pacifica Schmidt, 1974,
T. palaciosi Remane, 1953, T. petiti Remane, 1952, T. pontica
Valkanov, 1957, T. reducta Boaden, 1974, T. remanei Forne-
ris, 1961, T. scilloniensis Hummon, 2008, T. subterranea
Remane, 1934, T. varians Maguire, 1976, T. veneziana
Schrom, 1972, and T. wieseri Hummon, 2010.
1.6.1.8 Family Xenodasyidae Todaro, Guidi, Leasi &
Tongiorgi, 2006
This family, including four species in two genera, inclu-
des conspicuous specimens with a clearly delimited
head, from which a strong pair of segmented appendages,
usually called tentacles, originates (Fig. 1.18 D). Additi-
onal pairs of dorsal unsegmented appendages may be
present on the head. The dorsal surface is either covered
by cuticular structures (Xenodasys) or smooth (Chordoda-
siopsis). TbL are few and difficult to observe, but at least
one pair of large ventral adhesive structures, often called
pedicles, is present. Each pedicle is composed of a pair of
closely attached adhesive tubes. The caudal feet are elon-
gate and directed posteriorly. Posterior of the intestine is a
chordoid organ, a median longitudinal structure made up
of modified muscle cells. Muscles are cross-striated, and
the pharynx and intestine are, at least partially, ciliated
(see Todaro etal. 2006 for a more detailed description).
The first species was described by Swedmark (1967) as
Xenodasys sanctigoulveni, the second by Schöpfer-Sterrer
(1969) as Chordodasys riedli. A third species was described
as Chordodasys antennatus (Rieger etal. 1974). Kisielewski
(1987a) regarded Chordodasys as synonymous to Xenoda-
sys (see also Hummon 1982), but Todaro etal. (2006b),
200 µm
100 µm
50 µm
TbA
AB
C
pp
mgp Fig. 1.75: (A) Turbanella ambronensis
(Macrodasyida, Turbanellidae) from
an intertidal sand bar close to
Saint-Jacut-de-la-Mer, France. Habitus
in ventral view. (B and C) Turbanella
hyalina from the intertidal at Schillig,
Germany. (B) Anterior end in ventral
view. (C) Posterior end in ventral view.
Abbreviations: mgp, male genital pore;
pp, pharyngeal pores; TbA, anterior
adhesive tubes. (A) BF image. (B and C)
DIC images.
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1.6Systematics 109
when describing a fourth species, Xenodasys eknomios,
regarded Xenodasys antennatus as significantly different
from the three other species and erected a new genus,
Chordodasiopsis, for it.
Genus Chordodasiopsis Todaro, Guidi, Leasi &
Tongiorgi, 2006
One pair of segmented tentacles and two pairs of unseg-
mented dorsal appendages are present on the head. The
dorsal cuticle is smooth, only structured by sensory pro-
cesses. Numerous of those so-called regular sensory pro-
cesses ar arranged along the trunk in a lateral and dorsola-
teral position. The TbA originate directly from the surface
of the body, not on hands. Adhesive tubes are not visible
on the caudal feet, instead there is an adhesive pad. One
pair of ventral pedicles is present. The single species,
C. antennatus (Rieger, Ruppert, Rieger & Schoepfer-
Sterrer, 1974), was found on the western North Atlantic
(North Carolina, Florida, Virgin Islands, Bermuda), the
100 µm
Fig. 1.76: Xenodasys riedli (Macrodasyida, Xenodasyidae) from
calcareous sand of San Salvador Island, Bahamas. Dorsal view. Note
the seemingly segmented tentacles on the head region. DIC image.
Shetland Islands in the eastern Atlantic and probably in
South Africa (see Todaro etal. 2006b).
Genus Xenodasys Swedmark, 1967 (Fig. 1.76)
One pair of segmented tentacles is present; dorsal appen-
dages may be present on the head. The dorsal cuticle is
roughly structured into plates and spines. The TbA origi-
nate from fleshy hands. TbL are few, one, or two pairs of
pedicles are present. TbP are present on the caudal feet.
See Todaro etal. (2006b) for more information.
Three species have been described from the eastern
North Atlantic (X. sanctigoulveni Swedmark, 1967), the
western North Atlantic and the Caribbean (X. riedli
Schöpfer-Sterrer, 1969), and the Mediterranean Sea
(X. eknomios Todaro, Guidi, Leasi & Tongiorgi, 2006).
1.6.1.9 Family Redudasyidae Todaro, Dal Zotto,
Jondelius, Hochberg, Hummon, Kånneby &
Rocha, 2012
This family includes two species, Redudasys fornerise
and Anandrodasys agadasys. Both species cluster close
together in an analysis of their 18S rDNA sequences
(Todaro etal. 2012b). Most of the characters, in which the
two species resemble each other (see Todaro etal. 2012b)
are plesiomorphies, which are also present in several other
gastrotrich species (Kieneke etal. 2013a), but a potential
synapomorphy is that both species appear to be partheno-
genetic (Todaro etal. 2012b, Kieneke etal. 2013a).
Genus Redudasys Kisielewski, 1987 (see Fig. 1.26 B)
Redudasys fornerise Kisielewski, 1987, is one of two species
of Macrodasyida found in freshwater. It was originally
described by Kisielewski (1987a) from Brazil and then
rediscovered by Todaro etal. (2012b). The body is slender
(Kisielewski 1987a) to tenpin-shaped (Todaro etal. 2012b),
probably due to the presence of mature eggs. Two TbA are
present on each side; they originate from a common base.
At the posterior end of the animals, two TbP are present
on each side. The ventral ciliation is in separate fields of
unequal size. The pharyngeal pores are in the posterior
region of the pharynx. Recently, Garraffoni et al. (2010)
reported the discovery of several specimens of Redudasys
that possibly belong to another species.
Genus Anandrodasys Todaro, Dal Zotto, Jondelius,
Hochberg, Hummon, Kånneby & Rocha, 2012 (Fig. 1.77)
Originally described as Dactylopodola agadasys from Aus-
tralia (Hochberg 2003), Todaro etal. (2012b) found this
species to cluster close to Redudasys fornerise and created
a new genus for it, Anandrodasys. Specimens have been
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110 1Gastrotricha
etal. 2013a). Five TbP fan from what might be considered
as a very short caudal lobe on both sides of the body. The
ventral ciliation is in paired columns.
1.6.2Order Chaetonotida Brunson, 1950
Remane (1924) used the name “Chaetonotoidea” for the long-
known freshwater gastrotrichs in comparison to the newly
discovered, marine macrodasyids. Brunson (1950) used the
writing “Chaetonotida”, which was suggested to be the pre-
ferable name by Chandrasekahara Rao & Clausen (1970).
Chaetonotids live in freshwater as well as in the marine
environment. They include one genus, Neodasys, speci-
mens of which closely resemble the general macrodasyid
shape of the body. All remaining chaetonotids, summa-
rized as Paucitubulatina, have a more or less tenpin-shaped
body and have adhesive tubes exclusively on the posterior
end. In many, but not all species, the body is covered with
cuticular scales or spines, which are important taxonomic
markers. Characteristic for all chaetonotids is the absence
of pharyngeal pores (this is, among macrodasyids, only
known from Lepidodasys species) and a Y-shaped pha-
ryngeal lumen, meaning that the triradiate lumen has an
unpaired ventral branch and paired dorsolateral branches.
1.6.2.1[Suborder Multitubulatina d’Hondt, 1971]
1.6.2.1.1 [Family Neodasyidae Remane, 1929]
Genus Neodasys Remane, 1927 (Fig. 1.78)
The three species of this genus resemble in their external
morphology macrodasyidan gastrotrichs because they
have an elongate body with a number of TbL. The orien-
tation of the pharyngeal lumen (Y) and the absence of
pharyngeal pores correspond to (other) chaetonotids and
Neodasys is therefore traditionally regarded as member
of the Chaetonotida. However, this systematic position of
Neodasys within Chaetonotida is recently challenged by
several phylogenetic analyses of either molecular data or
coded morphological characters (see chapter Phylogeny).
According to these, Neodasys could also be part of the
Macrodasyida or may represent the earliest lineage within
Gastrotricha. The genus is the only component of the sub-
order Multitubulatina and of the family Neodasyidae.
A head region is evident in N. chaetonotoides and
N. uchidai, but not in N. cirritus. TbA are not present; the
TbL are inconspicuous and short. However, small papillae
on the ventral side of the head of N. uchidai were regar-
ded as remnants of TbA (Remane 1961). In the posterior
found, apart from the first record in Australia, in the Red
Sea (Hummon 2011) and in several localities in the Carib-
bean (see Kieneke etal. 2013a). The animals are slender;
the head is not clearly delimited. The buccal cavity is
large, and the pharyngeal pores are in the posterior region
of the pharynx. Three TbA are present per side; they form
a short row and decrease in size from lateral to medial.
Few ventrolateral adhesive tubes are present in about the
middle region of the trunk; they have been found to be
asymmetric in number and arrangement among several
specimens from the Red Sea and the Caribbean (Kieneke
100 µm
100 µm
AB
**
Fig. 1.77: Anandrodasys agadasys (Macrodasyida, Redudasyidae)
from calcareous sand of Lee Stocking Island, Bahamas. (A) Dorsal
view. (B) Ventral view. Note the ventrolateral adhesive tubes, which
are restricted to the midtrunk region (asterisks). (A and B) DIC
images. (from Kieneke etal. 2013a, with kind permission of Verlag
Dr. Friedrich Pfeil.)
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1.6Systematics 111
end, a pair of caudal feet is present; in N. uchidai, the feet
originate from a common unpaired stem. TbP are present
on the caudal feet. The mouth opening is surrounded by a
cup-shaped structure. The cuticle is smooth.
Three species were described from the North Sea, the
Western Mediterranean Sea, and from the Atlantic coast
of Florida: N. chaetonotoideus Remane, 1927, N. cirritus
Evans, 1992 (see Hummon & Todaro 2010 for a nomencla-
tural change), and N. uchidai Remane, 1961.
1.6.2.2Suborder Paucitubulatina d’Hondt, 1971
All species of Paucitubulatina are characterized by the
absence of adhesive tubes in places other than on the paired
caudal extensions, which are usually named furca. With two
exceptions (see Diuronotus and Dichaetura), only one single
adhesive tube is present per side. TbA and TbL are always
lacking. The caudal feet are lacking in some swimming
species; in this case, no adhesive tubes are present at all.
Most species have a more or less tenpin-shaped body form,
with a head region, a thinner neck, and a wider trunk. Very
important for the determination of species are the cuticu-
lar structures. These may be lacking, but many species are
covered with scales or spines. There is a wide diversity of such
cuticular structures (see, e.g., Schwank 1990). Scales are flat
structures, these may carry a keel or a spine. Spines appear
to be derived from spined scales; many spines have a small
scale as basis and only few spines appear to originate directly
from the cuticle. Scales may also be stalked. The pharynx has
in some species one or even more bulbs. A buccal cavity is
usually present, the mouth can be surrounded by a cuticular
ring and/or spine-like rods. Further cuticular structures are
present in the buccal cavity or pharynx of few species. Pauci-
tubulatina are abundant in freshwater, but several species do
occur in the marine environment or in brackish waters.
1.6.2.2.1 Family Muselliferidae Leasi & Todaro, 2008
On the basis of a cladistic analysis of muscle characters,
Leasi & Todaro (2008) erected the family Muselliferidae
for the genera Musellifer and Diuronotus. The head region
is weakly separated from the remaining body and it lacks
appendages or extensions. In some species, the head
characteristically tapers toward the anterior end and is
densely covered with cilia thus forming a conspicuous
“muzzle”. The mouth opening is surrounded by a ring of
teeth-like cuticular ridges. One (Musellifer) or two (Diuro-
notus) pairs of adhesive tubes is present on the furca. The
body is completely covered with uniform scales, which
are either spined (Musellifer) or keeled (Diuronotus). The
ventral ciliation is on the entire anterior ventral region
and in two longitudinal bands on the posterior region (see
200 µm
mo
fo
co
Fig. 1.78: Neodasys chaetonotoideus (Multitubulatina) from an intertidal
beach of river Ems estuary, Germany. Dorsal view. Abbreviations:
co, caudal organ; fo, frontal organ; mo, mature egg. BF image.
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112 1Gastrotricha
100 µm
TbP
st
Fig. 1.79: Diuronotus aspetos (Paucitubulatina, Muselliferidae) from
the sublittoral off island Wangerooge, Germany. The secondary
adhesive tube is out of focus. Abbreviations: st, secondary
adhesive tube; TbP, posterior adhesive tube. DIC image.
50 µm
mz
Fig. 1.80: Musellifer cf. profundus (Paucitubulatina, Muselliferidae)
from the Antarctic deep sea floor at depth of 5191 m. Fixed and
stained specimen in horizontal view. Abbreviation: mz, ciliated
muzzle. DIC image.
Leasi & Todaro 2008 for more characters). The species are
hermaphrodites and occur only marine.
Genus Diuronotus Todaro, Balsamo & Kristensen, 2005
(Fig. 1.79)
The two species of Diuronotus resemble species of Muselli-
fer in many respects, but differ from these in the following
characters (Todaro etal. 2005, Balsamo etal. 2010a): a
second pair of smaller adhesive tubes is present additi-
onal to the longer one in Diuronotus. The scales have a
keel in Diuronotus, in Musellifer a keel is, when present,
very weak and scales are spined. Finally, Diuronotus has
a smaller furca to total body length ratio compared with
Musellifer. Two species are known from sediment samples
from the shore or near the shore in Denmark and Green-
land: D. aspetos Todaro, Balsamo & Kristensen, 2005, and
D. rupperti Todaro, Balsamo & Kristensen, 2005.
Genus Musellifer Hummon, 1969 (Fig. 1.80)
The characters to distinguish Musellifer from Diuronotus
are described above. Five species were described from
the eastern North Atlantic, the Mediterranean Sea, the
eastern Pacific, and recently from the western Atlantic and
Caribbean Sea: M. delamarei (Renaud-Mornant, 1968),
M. profundus Vivier, 1974, M. reichardti Kånneby, Ather-
ton & Hochberg, 2014, M. sublitoralis Hummon, 1969, and
M. tridentatus Kånneby, Atherton & Hochberg, 2014.
1.6.2.2.2 Family Xenotrichulidae Remane, 1936
This family includes small and very fast species, which
typically occur in high-energy beaches (Ruppert 1979).
See Ruppert (1979) for a review of the family. The most
important character is that the ventral cilia are clustered
into bundles called cirri. The caudal furca is very long, its
base is covered by overlapping scales. In the head region,
three pairs of sensory structures (often called sensoria) are
present, there are at least five pairs of elongated sensory
cilia along the body.
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1.6Systematics 113
The three genera are usually split into two subfami-
lies (Ruppert 1979): Draculiciterinae (genus Draculiciteria)
and Xenotrichulinae (genera Xenotrichula and Heteroxe-
notrichula).
Genus Draculiciteria Hummon, 1974 (Fig. 1.81 A, B)
The head is well separated from the trunk; the two pos-
terior sensoria of each side are fused into one bundle of
sensory cilia (all characters from Ruppert 1979). The furca
is not well delimited from the trunk, the furcal bran-
ches are slightly curved. Most of the length of the furca
branches (about 5/6) is covered with scales. The body is
covered by scales and, on the lateral sides, with stalked
scales. The dorsal side of the head is covered by a charac-
teristic pattern of polygonal cuticular plates (Fig. 1.4 G).
The pharynx has an anterior bulb, eyes are absent.
One species is known from the eastern North Atlan-
tic (Gulf of Mexico and Caribbean) and the Mediterranean
Sea: D. tesselata (Renaud Mornant, 1968).
Genus Xenotrichula Remane, 1927 (Fig. 1.82 A–C)
The two genera, Xenotrichula and Heteroxenotrichula,
have a poorly defined head, but furcal branches are
well delimited from the trunk (Ruppert 1979). Scales are
present up to two thirds of the furcal length. In Xenotri-
chula, all locomotory ventral cirri are of equal length
(Fig. 1.82 A), the pharynx has no bulb, and the mouth
opening is surrounded by folds and spines.
Fifteen species are known from both sides of the North
Atlantic Ocean, the Caribbean, the Baltic Sea, the Mediterra-
nean Sea, the Pacific (Galapagos), and India: X. bispina Ros-
zczak, 1939, X. carolinensis Ruppert, 1979, X. cornuta Wilke,
1954, X. floridana Thane-Fenchel, 1970, X. guadelupensis
Kisielewski, 1984, X. intermedia Remane, 1934, X. laccadi-
vensis Rao, 1991, X. lineata Schrom, 1972, X. micracantha
(Remane, 1926a), X. paralineata Hummon & Todaro, 2007,
X. punctata Wilke, 1954, X. quadritubulata Kisielewski, 1988,
X. soikai Schrom, 1966, X. tentaculata Rao & Ganapati, 1968,
and X. velox Remane, 1927.
50 µm
100 µm
A
B
cir
Fig. 1.81: Draculiciteria tesselata (Paucitubulatina, Xenotrichulidae) from calcareous sand of Lee Stocking Island, Bahamas. (A) Habitus in
horizontal view. (B) Slightly smaller specimen in ventral view. Abbreviation: cir, locomotory cirri. (A and B) DIC images.
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114 1Gastrotricha
Genus Heteroxenotrichula Wilke, 1954 (Fig. 1.83)
Apart from the characters named under Xenotrichula,
the most obvious character of Heteroxenotrichula species
is the presence of ventral locomotory cirri in two size
classes. The mouth is slightly subventral and surroun-
ded by a collar, but not by folds or spines. The pharynx
has an anterior bulb.
Nine species have been described from both sides
of the North Atlantic Ocean, the Caribbean, the Baltic
Sea, the Mediterranean Sea, the Pacific (Galapagos), and
India: H. affinis (Remane, 1934), H. arcassonensis Ruppert,
1979, H. pygmaea (Remane, 1934), H. simplex (Mock, 1979),
H. squamosa Wilke, 1954, H. subterranea (Remane, 1934),
H. texana Todaro, 1994, H. transatlantica Ruppert, 1979,
and H. wilkeae Ruppert, 1979.
1.6.2.2.3 Family Chaetonotidae Gosse, 1864
A head region is more or less clearly separated, often the
head is composed of three or five lobes. Bundles of cilia
are present in the head region, often cephalic shields are
present (Fig. 1.4 J, K). A furca with one pair of adhesive
tubes is present. The cuticle may be naked, but in most
species, it is covered with cuticular scales of diverse
shapes. Ventral cilia are usually in two longitudinal
bands, rarely in other patterns. The pharynx is without
bulbs, only slight thickenings of the pharynx can be
present. A weir is usually present at the transition to the
intestine. Several species have rudimentary testes (e.g.,
Weiss & Levy 1979, Weiss 2001, see chapters Reproductive
Organs and Reproductive Biology). This is a very large
50 µm
50 µm
50 µm
AB
cir
C
cir
hf
hf
Fig. 1.82: (A) Xenotrichula intermedia
(Paucitubulatina, Xenotrichulidae) from
Geniusstrand (no more existant) in the
north of Wilhelmshaven, Germany. Ventral
view. (B and C) X. velox. (B) Specimen from
the beach of Tylosand, Sweden. Horizontal
view with focus on internal organs. (C)
Specimen from the intertidal sand flat at
Les Hemmes Plage, France. Focus on the
ventral side showing the hydrofoil scales.
Abbreviations: cir, locomotory cirri; hf,
hydrofoil scales. (A and B) DIC images. (C)
BF image.
family with 12 genera (Arenotus, Aspidiophorus, Caudich-
thydium, Chaetonotus, Fluxiderma, Halichaetonotus, Hete-
rolepidoderma, Ichthydium, Lepidodermella, Polymerurus,
Rhomballichthys, and Undula); almost all genera belong
to the subfamily Chaetonotinae, and only Undula belongs
to the Undulinae (Kisielewski 1991). Schwank (1990, page
61) includes in a key one further genus, Hemichaetonotus,
with H. clipeatus as type species and eight further marine
species that are not listed. He obviously intended to move,
Heterolepidoderma clipeatum Schrom, 1972, into a new
genus, but as a diagnosis was not given, the name Hemi-
chaetonotus has to be regarded a nomen nudum.
Genus Arenotus Kisielewski, 1987
The body is covered with a thick cuticular layer, but there
are no further cuticular structures like scales or spines (all
data from Kisielewski 1987a). The mouth is surrounded by
a complex collar, a pair of strong teeth originates dorsola-
terally in the pharynx. In the head region, cuticular plates
are present in the form of the unpaired cephalion (dorsal)
and hypostomium (ventral) and two pairs of pleuria.
One species, A. strixinoi Kisielewski, 1987, is described
from freshwater in Brazil.
Genus Aspidiophorus Voigt, 1903 (Fig. 1.84)
Species of this genus have the more or less “usual” appea-
rance of Chaetonotidae. Characteristic is that the body is
densely covered by stalked scales. The scales are often
rhombic, sometimes more oval, and usually have two to
three keels (Fig. 1.4 C). The scale covering usually ends
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1.6Systematics 115
50 µm
Fig. 1.83: Heteroxenotrichula cf. affinis (Paucitubulatina,
Xenotrichulidae) from sediment at the base of the dike in
Wilhelmshaven, Germany. Ventral view. DIC image.
50 µm
hy
Fig. 1.84: Aspidiophorus paramediterraneus (Paucitubulatina,
Chaetonotidae) from the shallow sublittoral of the Bay of Fetovaia,
Elba, Italy. Ventral view. Abbreviation: hy, hypostomion. BF image.
anterior of the furcal base. See Schwank (1990) for cha-
racters and a key and Todaro etal. (2009) for additional
comments and a key to the marine species.
Thirty-two species (22 from freshwater and 10
marine) have been described from freshwater envi-
ronments in Europe, North America, Argentina, and
Japan and from marine sediments from the North Atlan-
tic, Baltic Sea, Mediterranean Sea, the Caribbean,
and the Sea of Japan: A. aster Martin, 1981, A. bibul-
bosus Kisielewski, 1979, A. bisquamosus Mock, 1979,
A. bramhsi Grosso, 1973, A. heterodermus Saito, 1937,
A. heterodermus Saito, 1937, A. lilloensis Grosso & Drahg,
1983, A. lamellophorus Balsamo, Hummon, Todaro
& Tongiorgi, 1997, A. longichaetus Kisielewski, 1986,
A. marinus Remane, 1926, A. mediterraneus Remane,
1927, A. multitubulatus Hummon, 1974, A. microlepi-
dotus d’Hondt, 1978, A. microsquamatus Saito, 1937,
A. nipponensis Schwank, 1990, A. oculifer Kisielew-
ski, 1981, A. oculatus Todaro, Dal Zotto, Maiorova &
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116 1Gastrotricha
including the new descriptions since 2010. Usually, the
genus is subdivided into several subgenera, some of
these subgenera are more or less provisional constructs
and the list of subgenera has changed through time (see
Schwank 1990, Kisielewski 1997, Balsamo et al. 2009,
with addition of Tristatachaetus by Kolicka etal. 2013).
Taking records of all species into account, the genus has
a worldwide distribution.
C. acanthodes Stokes, 1887, C. acanthophorus Stokes,
1887, C. aculeatus Robbins, 1965, C. aegilonensis Balsamo,
Todaro & Tongiorgi, 1992, C. aemilianus Balsamo, 1978, C.
aequispinosus (Schrom, 1972), C. africanus Schwank, 1990,
C. alatus Schwank, 1990, C. alni Nesteruk, 1991, C. angustus
Schrom, 1972, C. annectens Grosso & Drahg, 1991, C. anoma-
lus Brunson, 1950, C. antipai (Rodewald, 1938), C. apecho-
chaetus Hummon, Balsamo & Todaro, 1992, C. apolemmus
(Hummon, Balsamo & Todaro, 1992 ), C. arethusae Balsamo &
Todaro, 1995, C. armatus Kisielewski, 1981, C. arquatus Voigt,
1903, C. atrox (Wilke, 1954), C. australiensis Schwank, 1990,
C. chuni Voigt, 1901, C. cordiformis Greuter, 1917, C. balsa-
moae Kisielewski, 1998, C. beauchampi d’Hondt, 1967, C. ben-
acensis Balsamo & Fregni, 1995, C. bifidispinosus Tretjakova,
1991, C. bisacer Greuter, 1917, C. bogdanovii (Schimkewitsch,
1886), C. brachyurus Balsamo, 1981, C. brasilianus (Kisielew-
ski, 1991), C. brasiliensis Schwank, 1990, C. breviacanthus
Kisielewski, 1991, C. brevispinosus Zelinka, 1889, C. carici-
cola Schwank, 1990, C. carpaticus Rudescu, 1967, C. caudal-
spinosus Visvesvara, 1964, C. cestacanthus Balsamo, 1990,
C. chicous (Hummon, 1974), C. christianus Schwank, 1990,
C. condensus Mock, 1979, C. corderoi Schwank, 1990, C. crassus
Preobrajenskaja, 1926, C. dadayi Schwank, 1990, C. daphnes
Balsamo & Todaro, 1995, C. decemsetosus Marcolongo,
Adrianov, 2009, A. ophiodermus Balsamo, 1983, A.
ornatus Mock, 1979, A. paradoxus (Voigt, 1902), A. para-
mediterraneus Hummon, 1974, A. pleustonicus Kisie-
lewski, 1991, A. polonicus Kisielewski, 1981, A. polystic-
tos Balsamo & Todaro, 1987, A. pori Kisielewski, 1999,
A. schlitzensis Schwank, 1990, A. semirotundus Saito, 1937,
A. slovinensis Kisielewski, 1986, A. squamulosus Rosz-
czak, 1936, A. tatraënsis Kisielewski, 1986, A. tentaculatus
Wilke, 1954, and A. tetrachaetus Kisielewski, 1986.
Genus Caudichthydium Schwank, 1990
Schwank (1990) introduces this genus in a key with a
very brief characterization of characters. Mock (1979) has
already speculated that the three species united in this
genus may have to be separated from the genus Ichthy-
dium, in which they were originally described. The main
character is that the furcal branches are fused more or less
significantly at their base. The cuticle is naked and has no
scales or spines. The ventral cilia occur in bundles.
Three species have been described from the North
Atlantic (North Carolina, Arcachon, Sylt): C. hummoni
(Ruppert, 1977), C. rupperti (Mock, 1979), and C. suprali-
torale (Mock, 1979).
Genus Chaetonotus Ehrenberg, 1830 (Fig. 1.85 A, B)
Chaetonotus is a large genus with species carrying
spined scales (Fig. 1.4 B). In some species, the spines
on the scales are quite long and strong. Balsamo etal.
(2009) name 163 freshwater and 40 marine species
in this genus, here we list 202 species compiled from
Balsamo etal. (2009) and Hummon & Todaro (2010) and
100 µm
100 µm
AB
fu
Fig. 1.85: Chaetonotus luporinii
(Paucitubulatina, Chaetonotidae) from
calcareous sand around the island of
Pianosa, Italy. (A) Dorsal view showing
the spined scales. Note the crest-shaped
basal part of the scales. (B) Ventral view.
Abbreviation: fu, furca with both posterior
adhesive tubes. (A and B) BF images.
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1.6Systematics 117
C. polyspinosus Greuter, 1917, C. poznaniensis Kisielewski,
1981, C. pratensis Schwank, 1990, C. pravus Kolicka,
Kisielewski, Nesteruk & Zawierucha, 2013, C. pseudo-
polyspinosus Kisielewski, 1991, C. pungens Balsamo,
1990, C. puniceus Martin, 1990, C. pusillus Daday, 1905,
C. quadratus Martin, 1981, C. quintospinosus Greuter,
1917, C. rafalskii Kisielewski, 1979, C. rarispinosus Rosz-
czak, 1936, C. rectaculeatus Kisielewska, 1981, C. remanei
Schwank, 1990, C. retiformis Suzuki & Furuya, 2011,
C. rhombosquamatus Kolicka, Kisielewski, Nesteruk &
Zawierucha, 2013, C. robustus Davison, 1938, C. rotundus
Greuter, 1917, C. sagittarius (Evans, 1992), C. sanctipauli
Kisielewski, 1991, C. schlitzensis Schwank, 1990, C. schoep-
ferae Thane-Fenchel, 1970, C. schromi Hummon, 1974,
C. schultzei (Metschnikoff, 1865), C. scoticus Schwank,
1990, C. scutatus Saito, 1937, C. scutulatus Martin, 1981,
C. segnis Martin, 1981, C. semihamus Hummon, 2010,
C. serenus (Schrom, 1972), C. sextospinosus Visvesvara,
1964, C. siciliensis Hummon, Balsamo & Todaro, 1992,
C. silvaticus (Varga, 1963), C. similis Zelinka, 1889,
C. simrothi Voigt, 1909, C. soberanus Grosso & Drahg,
1983, C. sphagnophilus Kisielewski, 1981, C. spinifer Stokes,
1887, C. spinulosus Stokes, 1887, C. splendidus Preobrajens-
kaja, 1926, C. stagnalis d’Hondt, 1967, C. striatus Preobrajens-
kaja, 1926, C. succinctus Voigt, 1902, C. sudeticus Kisielew-
ski, 1984, C. tachyneusticus Brunson, 1948, C. tempestivus
Mock, 1979, C. tenuis Grünspan, 1908, C. tenuisquamatus
Grosso, 1982, C. triacanthus Todaro, 1994, C. triangulifor-
mis Visvesvara, 1964, C. trichodrymodes Brunson, 1950, C.
trichostichodes Brunson, 1950, C. tricuspidatus Schwank,
1990, C. trilineatus Valkanov, 1937, C. triradiatus Rao, 1991, C.
trispinosus Balsamo, 1990, C. uncinus Voigt, 1902, C. vargai
Rudescu, 1967, C. variosquamatus (Mock, 1979), C. vellosus
Martin, 1990, C. ventrochaetus Kisielewski, 1991, C. venustus
d’Hondt, 1967, C. veronicae Kånneby, 2013, C. voigti Greuter,
1917, C. vorax Remane, 1936, C. vulgaris Brunson, 1950, C.
woodi (Thane-Fenchel, 1970), and C. zelinkai Grünspan, 1908.
Genus Fluxiderma d’Hondt, 1974
Characteristic for the species in this genus is the presence of
round scales. Usually the scales are in some distance from
each other, but in one species, they attach each other. Three
species are known from few freshwater localities in Europe
and North America: F. concinnum (Stokes, 1887), F. monta-
num Rudescu, 1967, and F. verrucosum (Roszczak, 1936).
Genus Halichaetonotus Remane, 1936 (Fig. 1.86)
Originally a subgenus of Chaetonotus (Remane 1936), this
taxon received genus level by Schrom (1972). The body is
covered with large keeled scales, the keels can extend into
short spines. Ventrolaterally, there are paired rows with
lamellate spines.
1910, C. disjunctus Greuter, 1917, C. dispar (Wilke, 1954),
C. dracunculus Balsamo, 1990, C. dubius Daday, 1905,
C. dybowskii Jakubski, 1919, C. elachysomus Hummon,
2010, C. elegans Konsuloff, 1921, C. enormis Stokes,
1887, C. eratus Hummon, 2010, C. erinaceus Daday, 1905,
C. euhystrix Schwank, 1990, C. eximius Kolicka, Kisielew-
ski, Nesteruk & Zawierucha, 2013, C. fenchelae d’Hondt,
1974, C. ferrarius Schwank, 1990, C. fluviatilis Balsamo
& Kisielewski, 1986, C. formosus Stokes, 1887, C. fuji-
sanensis (Sudzuki, 1971), C. furcatus Kisielewski, 1991,
C. gastrocyaneus Brunson, 1950, C. greuteri Remane, 1927,
C. heideri Brehm, 1917, C. heteracanthus Remane, 1927,
C. heterochaetus Daday, 1905, C. heterospinosus Balsamo,
1978, C. hilarus (Schrom, 1972), C. hirsutus Marcolongo,
1910, C. hoanicus Schwank, 1990, C. hystrix (Metschni-
koff, 1865), C. ichthydioides Tongiorgi, Fregni & Balsamo,
1999, C. illiesi Schwank, 1990, C. inaequidentatus Kisie-
lewski, 1988, C. insigniformis Greuter, 1917, C. interme-
dius Kisielewski, 1991, C. italicus Balsamo & Todaro, 1995,
C. jakubskii Roszczak, 1936, C. lacunosus (Mock, 1979),
C. laroides Marcolongo, 1910, C. larus (Müller, 1773), C.
laterospinosus Visvesvara, 1965, C. linguaeformis Voigt,
1902, C. lobo Kisielewski, 1991, C. longisetosus Preob-
rajenskaja, 1926, C. longispinosus Stokes, 1887, C. lucksi
Voigt, 1958, C. lunatospinosus Balsamo, 1981, C. lupori-
nii Balsamo, Fregni & Tongiorgi, 1996, C. machikanensis
Suzuki & Furuya, 2011, C. macrochaetus Zelinka, 1889,
C. macrolepidotus Greuter, 1917, C. magnificus Balsamo,
Hummon, Todaro & Tongiorgi, 1997, C. majestuosus Grosso
& Drahg, 1984, C. mariae (Todaro, 1992), C. maximus Ehren-
berg, 1831, C. mediterraneus Balsamo, Hummon, Todaro
& Tongiorgi, 1997, C. microchaetus Preobrajenskaja, 1926,
C. minimus Marcolongo, 1910, C. mitraformis Greuter, 1917,
C. modestus (Schrom, 1972), C. monobarbatus Visves-
vara, 1965, C. montevideensis Cordero, 1918, C. multise-
tosus Preobrajenskaja, 1926, C. multispinosus Grünspan,
1908, C. murrayi Remane, 1929, C. mutinensis Balsamo,
1978, C. naiadis Balsamo & Todaro, 1995, C. napoleo-
nicus Balsamo, Todaro & Tongiorgi, 1992, C. neptuni
(Wilke, 1954), C. novenarius Greuter, 1917, C. oceanides
(d’Hondt, 1971), C. octonarius Stokes, 1887, C. oculatus
Schwank, 1990, C. oculifer Kisielewski, 1981, C. odonto-
pharynx Grosso & Drahg, 1986, C. oligohalinus (Hummon,
1974), C. oplites Balsamo, Fregni & Tongiorgi, 1994,
C. ornatus Daday, 1897, C. paluster d’Hondt, 1967, C. palus-
tris Anderson & Robbins, 1980, C. parafurcatus Nesteruk,
1991, C. paraguayensis Schwank, 1990, C. paucisetosus
Marcolongo, 1910, C. paucisquamatus Kisielewski, 1991,
C. pawlowskii Kisielewski, 1984, C. pentacanthus
Balsamo, 1981, C. persetosus (Zelinka, 1889), C. pilaga
Grosso, 1982, C. ploenensis Voigt, 1909, C. poly-
chaetus Daday, 1905, C. polyhybus Hummon, 2010,
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118 1Gastrotricha
Thirty-one marine species have been described from
the North Atlantic, Baltic Sea, Mediterranean Sea, Black
Sea, Northwestern Pacific, and Australia: H. aculifer
(Gerlach, 1953), H. arenarius (d’Hondt, 1971), H. atlanticus
Kisielewski, 1988, H. australis Nicholas & Todaro, 2005, H.
balticus Kisielewski, 1975, H. bataceus Evans, 1992, H. batil-
lifer (Luporini & Tongiorgi, 1972), H. clavicornis Balsamo,
Fregni & Tongiorgi, 1995, H. decipiens (Remane, 1929), H.
etrolomus Hummon, Balsamo & Todaro, 1992, H. euroma-
rinus Hummon & Todaro, 2010, H. genatus Balsamo, Fregni
50 µm
lsp
Fig. 1.86: Halichaetonotus sp. (Paucitubulatina, Chaetonotidae)
from sublittoral sand of the North Sea off the Danish coast at depth
of 25 m. Ventral view. Abbreviation: lsp, lamellar spine. BF image.
40 µm
20 µm
A
B
po
Fig. 1.87: (A) Heterolepidoderma joermungandri (Paucitubulatina,
Chaetonotidae) from peat bog (Sphagnum spp.) in a rock pool at
Skarvesäter, Sweden. Dorsal view with focus on the keeled scales.
(B) H. ocellatum from peat bog in a rock pool at Kristineberg,
Sweden. Dorsal view. Abbreviation: po, pseudocellus. (A and B,
DIC images were kindly provided by Tobias Kånneby, Stockholm.)
& Tongiorgi, 1995, H. italicus Balsamo, Hummon, Todaro &
Tongiorgi, 1997, H. jucundus (d’Hondt, 1971), H. lamellatus
Kisielewski, 1975, H. littoralis (d’Hondt, 1971), H. margaretae
Hummon, Balsamo & Todaro, 1992, H. marivagus Balsamo,
Todaro & Tongiorgi, 1992, H. paradoxus (Remane, 1927), H.
parvus (Wilke, 1954), H. pleuracanthus (Remane, 1926), H.
polonensis Hummon, 2008, H. riedli Schrom, 1972, H. sanc-
taeluciae Todaro, Dal Zotto, Perissinotto & Bownes, 2011, H.
schromi Kisielewski, 1975, H. somniculosus (Mock, 1979), H.
susi Hummon, 2010, H. swedmarki Schrom, 1972, H. tenta-
culatus (d’Hondt, 1971), H. testiculophorus (Hummon, 1966),
and H. thalassopais Hummon, Balsamo & Todaro, 1992.
Genus Heterolepidoderma Remane, 1927 (Fig. 1.87 A, B)
Species in this genus are densely covered with keeled
scales, the keels often create a longitudinally striated
appearance. There is some nomenclatorial discussion
(d’Hondt etal. 2010, Hummon & Todaro 2010).
Thirty-four species have been described, 14 from
marine or brackish environments (Hummon & Todaro
2010 and newer descriptions) and 21 from freshwater envi-
ronments (Balsamo etal. 2009 and newer descriptions);
some species, especially H. ocellatum, seem to have some
tolerance for salinity and occur in brackish and freshwater
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1.6Systematics 119
and I. tergestinum) and the majority from freshwater envi-
ronments worldwide. The species I. podura may be found
in marine and freshwater (see Hummon & Todaro 2010).
For a key and further information, see Schwank (1990) and
Kånneby etal. (2009). Species are I. auritum Brunson, 1950,
I. balatonicum Varga, 1950, I. bifasciale Schwank, 1990, I.
bifurcatum Preobrajenskaja, 1926, I. brachykolon Brunson,
1949, I. cephalobares Brunson, 1949, I. chaetiferum Kisie-
lewski, 1991, I. crassum Daday, 1905, I. cyclocephalum
(Grünspan, 1908), I. diacanthum Balsamo & Todaro, 1995,
I. dubium Preobrajenskaja, 1926, I. forcipatum Voigt, 1902, I.
forficula Remane, 1927, I. fossae d’Hondt, 1972, I. galeatum
Konsuloff, 1921, I. leptum Brunson, 1949, I. macrocapita-
tum Sudzuki, 1971, I. macropharyngistum Brunson, 1949, I.
maximum Greuter, 1917, I. minimum Brunson, 1950, I. palus-
tre Kisielewski, 1981, I. pellucidum Preobrajenskaja, 1926, I.
plicatum Balsamo & Fregni, 1995, I. podura (Müller, 1773), I.
rostrum Roszczak, 1969, I. squamigerum Balsamo & Fregni,
1995, I. sulcatum (Stokes, 1887), I. tanytrichum Balsamo,
1983, and I. tergestinum (Grünspan, 1908).
Genus Lepidodermella Blake, 1933 (Fig. 1.89 A, B)
The genus was originally introduced as Lepidoderma by
Zelinka (1889), but as this name was preoccupied by slime
molds (Myxogastria), Blake (1933) renamed it Lepidodermella.
habitats (see Hummon & Todaro 2010). Species are
H. acidophilum Kånneby, Todaro & Jondelius, 2011, H. are-
nosum Kisielewski, 1988, H. armatum Schrom, 1966, H. axi
Mock, 1979, H. brevitubulatum Kisielewski, 1981, H. baium
Hummon, 2010, H. caudosquamatum Grilli, Kristensen &
Balsamo, 2009, H. clipeatum Schrom, 1972, H. contectum
Schrom, 1972, H. dimentmani Kisielewski, 1999, H. famail-
lense Grosso & Drahg, 1991, H. foliatum Renaud-Mornant,
1967, H. gracile Remane, 1927, H. grandiculum Mock, 1979, H.
hermaphroditum Wilke, 1954, H. illinoisense Robbins, 1965,
H. istrianum Schrom, 1972, H. joermungandri Kånneby,
2011, H. jureiense Kisielewski, 1991, H. kossinense (Preob-
rajenskaja, 1926), H. lamellatum Balsamo & Fregni, 1995,
H. longicaudatum Kisielewski, 1979, H. loricatum Schrom,
1972, H. macrops Kisielewski, 1981, H. majus Remane, 1927,
H. marinum Remane, 1926, H. multiseriatum Balsamo,
1978, H. obesum d’Hondt, 1967, H. obliquum Saito, 1937, H.
ocellatum (Metschnikoff, 1865), H. patella Schwank, 1990,
H. pineisquamatum Balsamo, 1981, H. tenuisquamatum
Kisielewski, 1981, and H. trapezoidum Kånneby, 2011.
Genus Ichthydium Ehrenberg, 1830 (Fig. 1.88 A, B)
In species of this genus, cuticular structures are either
completely absent or strongly reduced and the cuticle
appears “naked” (Fig. 1.88 A, B).
Twenty-nine species have been described, two from the
marine environment (Mediterranean Sea: I. cyclocephalum
40 µm
50 µm
A
B
Fig. 1.88: (A) Ichthydium squamigerum (Paucitubulatina,
Chaetonotidae) from peat bog (Sphagnum spp.) in a rock pool at
Skarvesäter, Sweden. Horizontal view. (B) I. skandicum from an
artificial pond on Skaftö, Sweden. Horizontal view. Note the naked
cuticle in both species. (A and B, DIC images were kindly provided
by Tobias Kånneby, Stockholm.)
50 µm
50 µm
A
B
mo
Fig. 1.89: Lepidodermella squamata (Paucitubulatina,
Chaetonotidae) from a drainage ditch in Oldenburg, Germany.
(A) Ventral view. (B) Dorsal view showing the tile-like scales.
Abbreviation: mo, mature egg. (A and B) DIC images.
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120 1Gastrotricha
not clearly separated from the body. The cuticular plates in
the head region are more or less well developed, usually a
cephalion, a slender hypostomium, and one pair of pleuria
are present. Two bundles of cilia are present in the head.
The toes are extremely long, and the terminal adhesive
tubes are strongly reduced (Fig. 1.90). In some species, the
toes are covered with spined scales; in others, the scales
are fused to form rings that give the toes a segmented
appearance. The body is covered with simple scales of
different shapes or with spines. Minute stalked spines are
present in the species P. rhomboides. The pharynx is short
and without a bulbus. A key to species is given in Schwank
(1990).
Eighteen species have been described from all con-
tinents except Antarctica, some species (P. nodicaudus,
P. rhomboides) appear to be cosmopolites: P. andreae
Hochberg, 2005, P. biroi (Daday, 1897), P. callosus
Brunson, 1950, P. corumbensis Kisielewski, 1991, P. elonga-
tus (Daday, 1905), P. entzii (Daday, 1882), P. hystrix (Daday,
1910), P. longicaudatus (Tatem, 1867), P. macracanthus
(Lauterborn, 1894), P. macrurus (Collin, 1897), P. magnus
Visvesvara, 1963, P. nodicaudus (Voigt, 1901), P. nodifurca
(Marcolongo, 1910), P. paraelongatus Grosso & Drahg,
1986, P. rhomboides (Stokes, 1887), P. ringueleti Grosso,
1975, P. serraticaudus (Voigt, 1901), and P. squammofurca-
tus (Preobrajenskaja, 1926).
Genus Rhomballichthys Schwank, 1990
The characteristic feature of species in this genus is that
the body is densely covered with rhomboidal scales that
closely attach each other. On the surface, further struc-
tures such as short spines or secondary scales can be
present (see Schwank 1990). Schwank (1990) includes
three species in this genus, but Balsamo et al. (2009)
regard two of these species as species inquirenda (R. cari-
natus Schwank, 1990, and R. murrayi Schwank, 1990). The
only remaining species is R. punctatus (Greuter, 1917). The
species has a scattered distribution in Europe.
Genus Undula Kisielewski, 1991
The genus was created by Kisielewski (1991) for one cons-
picuous species, Undula paraënsis Kisielewski, 1991, from
Brazil. It has a furca, but instead of adhesive tubes, the
furcal branches end with a spine. The name-giving feature
is an undulating band of cilia in the head region that ends
in paired ventral tufts of cilia. Some spines are present in
the posterior region of the trunk. The body is covered with
very small and inconspicuous scales (see Kisielewski 1991
for more details).
The body is covered densely with attaching or overlapping
simple scales without spines.
Thirteen species have been described, one of them
from the marine environment (Mediterranean Sea:
L. limogena), the other species from freshwater. Lepido-
dermella squamata is one of the most well-known gast-
rotrich species. A key to species is given in Schwank
(1990). The known distribution of the genus is in Europe,
North and South America, India, and Japan: L. acan-
tholepida Suzuki, Maeda & Furuya, 2013, L. amazonica
Kisielewski, 1991, L. aspidioformis Sudzuki, 1971, L. broa
Kisielewski, 1991, L. limogena Schrom, 1972, L. macroce-
phala d’Hondt, 1972, L. minor (Remane, 1936), L. serrata
Sudzuki, 1971, L. spinifera Tretjakova, 1991, L. squamata
(Dujardin, 1841), L. tabulata (Preobrajenskaja, 1926),
L. triloba (Brunson, 1950), and L. zelinkai (Konsuloff, 1913).
Genus Polymerurus Remane, 1926 (Fig. 1.90)
This genus includes large specimens, the maximal size is
up to 650 µm (all data from Schwank 1990). The head is
50 µm
ce
fu
Fig. 1.90: Polymerurus nodicaudus (Paucitubulatina, Chaetonotidae)
from a ditch in northern Germany. Horizontal view. Note the
annulated furca. Abbreviations: ce, cephalion; fu, furca. DIC image.
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1.6Systematics 121
At present, Chitonodytes is regarded as a genus and Das-
ydytes comprises the two subgenera Dasydytes and Pro-
dasydytes (Balsamo etal. 2009). For the characterization
of subgenera, see Kisielewski (1991).
Nine species are currently included in this genus;
they have been found in Europe, the USA, and Brazil:
D. asymmetricus Schwank, 1990, D. carvalhoae Kisielewski,
1991, D. elongatus Kisielewski, 1991, D. goniathrix Gosse,
1851, D. lamellatus Kisielewski, 1991, D. monile Horlick,
1975, D. nhumirimensis Kisielewski, 1991, D. ornatus Voigt,
1909, and D. papaveroi Kisielewski, 1991.
1.6.2.2.4 Family Dasydytidae Daday, 1905
In most species, the head is clearly delimited and often
has lobes. Dasydytids are pelagic and during swimming
the head is held downward (Schwank 1990). A furca is
absent, the cuticle is usually naked (but see especially dif-
ferent species from the tropical South America described
by Kisielewski 1991), with the exception of several more
or less long spines that either originate directly from the
cuticle or from scale rudiments. Spines often occur in
bundles and may sometimes be very long and movable;
they are used for locomotion and defense (see Kieneke
et al. 2008b, Kieneke & Ostmann 2012). With exception
of Halidytes, the ventral ciliation is in bundles. A putative
marine dasydytid species, Metadasydytes quadrimacula-
tus (Roszczak 1971), is not a gastrotrich, but a polychaete
larva (Hummon 2008b). All species live in freshwater.
Eight genera are included in this family: Anacanthoderma,
Chitonodytes, Dasydytes, Dichaetura, Ornamentula, Halti-
dytes, Setopus, and Stylochaeta.
Genus Anacanthoderma Marcolongo, 1910
The head is not delimited as in the other taxa of Dasyd-
ytidae. In the posterior region of the trunk are few (2–16)
spines that are not movable. The pharynx has two bulbi;
the anus is ventral.
Two not well-known species were described from Italy
and Romania: A. paucisetosum (Marcolongo, 1910) and
A. punctatum Marcolongo, 1910.
Genus Chitonodytes Remane, 1936
On the lateral sides of the animals, bundles of long spines
originate, and these extend behind the posterior end. The
spines are either “simple”, meaning without lateral exten-
sions, or they have one or two such extensions called den-
ticles. The denticles are directed toward the animal.
Three species are known from Europe: C. collini
(Remane, 1927), C. longisetosus (Metschnikoff, 1865), and
C. longispinosus (Greuter, 1917).
Genus Dasydytes Gosse, 1851 (Fig. 1.91)
The head is well delimited, and the trunk carries a large
number of spines, which are grouped in bundles or as
single spines. Spines have one lateral denticle and a ter-
minal bifurcation. There are no appendages at the poste-
rior end. The pharynx has no bulbs. When present, scales
covering the body are keeled. Schwank (1990) divided the
genus Dasydytes into three subgenera: Setopus, Setody-
tes, and Dasydytes. A year later, Kisielewski (1991) regar-
ded Setopus to be at genus level, including the former
Setodytes species. Within Dasydytes, he recognized three
subgenera: Dasydytes, Prodasydytes, and Chitonodytes.
50 µm
*
ms
Fig. 1.91: Dasydytes goniathrix (Paucitubulatina, Dasydytidae) from
a ditch close to Oldenburg, Germany. Horizontal view. Note the
rings of locomotor cilia on the head (asterisk). Abbreviation:
ms, motile spines. DIC image.
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122 1Gastrotricha
One species is known from Brazil: O. paraënsis
Kisielewski, 1991.
Genus Setopus Grünspan, 1908 (Fig. 1.93 A, B)
There is a pair of spines on the bilobed caudal trunk
end. These terminal spines may be equal or unequal
(Fig. 1.93 B) in length. The lateral spines occur in three
to six paired groups or pairs of single spines. Spines are
simple or may have one small lateral denticle. Some
species have scales, and these are dorsally larger than
ventral; the dorsal scales are incompletely keeled,
whereas the ventral scales are keeled or spined (see
Kisielewski 1991).
Eight species are described from Europe, Brazil,
India, Central Russia, and probably the USA: S. abarbi-
tus (Visvesvara, 1964), S. aequatorialis Kisielewski, 1991,
S. bisetosus (Thompson, 1891), S. chatticus (Schwank,
1990), S. dubius (Voigt, 1909), S. iunctus Greuter, 1917,
S. primus Grünspan, 1908, and S. tongiorgii (Balsamo,
1983).
Genus Stylochaeta Hlava, 1904 (Fig. 1.94)
Paired club-like extensions (protuberances) with few fine
bristles (cilia) are present in the caudal end. The lateral
spines are long, and they have a sharp tip and two to three
lateral denticles. The pharynx has one bulb.
Genus Haltidytes Remane, 1936 (Fig. 1.92)
Species have one to three pairs of ventrolateral origina-
ting long jumping spines, in relaxed state they cross over
the trunk (Fig. 1.92). There are further spines originating
from the transition of the neck to the trunk. All spines
are simple. The ventral cilia are in paired rows, which is
unusual for this family. The pharynx has no bulbus.
Five species have been described from Europe, North
America, Central Russia, Argentina, and Brazil: H. crassus
(Greuter, 1917), H. festinans (Voigt, 1909), H. ooëides
Brunson, 1950, H. saltitans (Stokes, 1887), and H. squamo-
sus Kisielewski, 1991.
Genus Ornamentula Kisielewski 1991
The body is covered with well-developed and finely orna-
mented scales, and these are very large in the dorsal and
lateral sides; ventrally, there are very small spined scales
in the posterior half of the animal. Smaller scales are also
present on the head. Long spines with a lateral denticle
originate from the lateral scales (Kisielewski 1991).
50 µm
*
ms
ms
Fig. 1.92: Haltidytes crassus (Paucitubulatina, Dasydytidae) from a
drainage ditch in Oldenburg, Germany. Ventral view. Note the rings
of locomotor cilia on the head (asterisk). The most posterior pair of
motile spines shows a characteristic crossing. Abbreviation:
ms, motile spines. BF image.
50 µm
50 µm
*
ms
*
ts
Fig. 1.93: (A and B) Setopus tongiorgii (Paucitubulatina, Dasydytidae)
from a drainage ditch in Oldenburg, Germany. A and B at slightly
different focus. Note the rings of locomotor cilia on the head
(asterisks) and the unequal length of the terminal spines. Abbreviation:
ms, motile spines; ts, terminal spines. (A and B) DIC images.
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1.6Systematics 123
Four species are known from Europe, Central
Russia, and North America: S. fusiformis (Spencer, 1890),
S. longispinosa Greuter, 1917, S. scirtetica Brunson, 1950,
and S. stylifera (Voigt, 1901).
1.6.2.2.5 Family Neogosseidae Remane 1927
The most conspicuous character for members of this
family is the presence of club-shaped tentacles on the
head. A caudal furca and therefore adhesive tubes are
absent. Locomotory cilia are present as short bands and
bundles (tufts) around the head and along the ventral
surface of the trunk. Most, but not, all species have
spined scales, toward the posterior end the spines are
usually longer. The mouth is surrounded by a mouth ring.
The male reproductive system is unknown. The pharynx
has between one and four bulbs. All species live plank-
tonic or semipelagic in freshwater. For more information
see Schwank (1990), Kisielewski (1991), and Todaro etal.
(2013). Two genera are included in this family, Kijaneba-
lola and Neogossea.
Genus Kijanebalola Beauchamp, 1932
In the posterior end, a median group of spines is present.
The body is covered by keeled scales with rudimentary
50 µm
*
ms
ms
sty
Fig. 1.94: Stylochaeta scirtetica (Paucitubulatina, Dasydytidae)
from a ditch close to Leer, Germany. Ventral view. Note the rings of
locomotor cilia on the head (asterisk). The first group of spines is
spread. Abbreviations: ms, motile spines; sty, styli. DIC image.
spines, naked regions may occur. The pharynx has up to
two bulbs, the mouth opening is surrounded by a cuticu-
lar ring. For more characters, see Todaro etal. (2013).
Three species have been described from Lake Kija-
nebalola in Uganda and freshwater habitats in South
Africa and Brazil: K. canina Kisielewski, 1991, K. deves-
tiva Todaro, Perissinotto & Bownes, 2013, and K. dubia de
Beauchamp, 1932.
Genus Neogossea Remane, 1927 (Fig. 1.95)
In the posterior end are small posterolateral projections
carrying tufts of long spines. The body is covered by spined
scales. The mouth opening is terminal, surrounded by a
large, protruding cuticular ring with longitudinal ridges and
spine-like structures. The pharynx has four bulbs, the pos-
terior one is the largest (characters from Todaro etal. 2013).
Six species are known from freshwaters in Brazil,
Paraguay, South Africa, India, North America, and
Central Europe, extending eastward to Central Russia and
the Caspian Region: N. acanthocolla Kisielewski, 1991,
N. antennigera (Gosse, 1851), N. fasciculata (Daday, 1905),
50 µm
ph
ts
ct
Fig. 1.95: Neogossea voigti (Paucitubulatina, Neogosseidae) from a
ditch close to Leer, Germany. Horizontal view. Note that the animal
was nodding with its head. Abbreviations: ct, club-shaped tentacle;
ph, pharynx (with distinct bulbs); ts, terminal spines. DIC image.
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124 1Gastrotricha
20 µm
Fig. 1.96: Dichaetura filispina
(Paucitubulatina, Dichaeturidae) from a rice
paddy close to Mano, Japan. Ventral view.
(DIC image was kindly provided by Takahito
Suzuki, Osaka.)
N. pauciseta (Daday, 1905), N. sexiseta Krivanek & Kriva-
nek, 1959, and N. voigti (Daday, 1905).
1.6.2.2.6 [Family Dichaeturidae Remane, 1927]
Genus Dichaetura Lauterborn, 1913 (Fig. 1.96)
The head region is without appendages or head plates.
Some bristles or cilia and few spines appear to be
present. Most characteristic is the presence of two pairs
of adhesive tubes on the furca, a condition otherwise
only reported for Diuronotus. However, Todaro et al.
(2005) point out that the second adhesive tube may
also be a lateral extension instead of a tube, which was
confirmed in the description of the fourth species, D.
filispina, by Suzuki et al. (2013). A reinvestigation of
the other species would be very helpful. Only very few
scales are present.
Four species were found in few places in Europe and
in Japan: D. capricornia (Metschnikoff, 1865), D. filispina
Suzuki, Maeda & Furuya, 2013, D. piscator (Murray, 1913),
and D. surreyi Martin, 1990.
1.6.2.2.7 Family Proichthydidae Remane 1927
Only two species in two genera have been described from
this family. The head is well separated from the trunk.
Tentacles, plates, or scales are absent. A terminal furca
with slightly curved brances is present.
Genus Proichthydium Cordero, 1918
Cilia have only been described as a ring around the head,
and no further cilia or cuticular structures have been repor-
ted (Cordero 1918). One species, P. coronatum Cordero, 1918
is known from freshwater near Montevideo, Uruguay.
Genus Proichthydioides Sudzuki, 1971
In the head region, several cilia, some of considerable
length, are present. Two longitudinal bands of cilia extend
to the base of the furca. One species, P. remanei Sudzuki,
1971, has been described from Japan.
1.6.2.3Gastrotricha incertae sedis
Genus Marinellina Ruttner-Kolisko, 1955
Ruttner-Kolisko (1955) described one species, Marinellina
flagellata, from an Austrian river, Ybbs. It has a slight con-
striction behind a head region and caudal feet with two
adhesive tubes per foot. One further pair of adhesive tubes
is present in the head region. There are several single long
cilia all over the body, but a ventral ciliation appears to be
lacking. The pharynx is large, and the intestine is divided
into a smaller anterior and a larger posterior part. The spe-
cimens described may be juvenile. Because of the number
and distribution of adhesive tubes, Marinellina is usually
treated as a freshwater macrodasyid gastrotrich.
1.7Biogeography
Gastrotrichs have a worldwide distribution (see Artois
et al. 2011), they have been found on all continents
exclusive Antarctica and in marine environments from
the shore to the deep sea. Knowledge on gastrotrich
diversity and biogeography has, however, still to be
regarded as fragmentary. Europe and North and South
America have been sampled more intensively than,
for example, Africa, Southeast Asia, or Australia (see
Balsamo etal. 2008 for more information). Some examp-
les for local summaries of the gastrotrich fauna are Kisie-
lewski (1991) for Brazilian freshwater, Vanamala Naidu
& Chandrasekahara Rao (2004) for Indian freshwater
and marine regions, and Schmidt (1974) for the marine
region around Galapagos. Currently, freshwater species
are described from Japan (e.g., Suzuki et al. 2013) and
marine species from South Korean waters (see Lee etal.
2013 and references therein); some investigations deal
with the Caribbean fauna (e.g., Hummon 2010, Hoch-
berg etal. 2014) or discover the Eastern Mediterranean
and the Red Sea (Hummon 2011) or South Africa (Todaro
etal. 2011b, 2013).
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1.8Ecology 125
In freshwater species as well as in marine species,
some species appear to have a wide distribution, being
found in disjunct regions. Other species have been found
with a very limited distribution. The standard question
behind a wide distribution range is whether the observed
populations really belong to one single species or whether
they represent several cryptic species. In some cases, a
closer look or advanced observation technology reveal
differences. Leasi & Todaro (2009) investigated specimens
of Xenotrichula intermedia from populations in the Medi-
terranean (Adriatic Sea) and in the Arabian Gulf (Kuwait).
Externally, the specimens could not be separated, but a
phalloidin staining of actin revealed clearly different pat-
terns of the musculature.
The standard tool to aid the recognition of species
boundaries is the “barcoding”, a comparison of gene
sequences, preferably the cytochrome oxidase I (COI)
gene. Such investigations were to date conducted only
rarely with gastrotrichs. Todaro et al. (1996) made some
pioneer work with the above mentioned Xenotrichula
intermedia and compared three populations, from the
Mediterranean (Italy), Southwestern Atlantic (Virginia),
and the Gulf of Mexico (Florida). Morphologically, only
the pharynx length differed slightly between populations,
but genetically (RFLPs, restriction fragment length poly-
morphism and partial COI gene sequence), four popula-
tions were strongly separated from each other. Therefore,
four cryptic species seem to be present in these three sites.
Recently, Kieneke etal. (2012) discovered evidence for two
cryptic genetic species within the morphospecies Turba-
nella hyalina when studying mitochondrial COI sequen-
ces of specimens from different European coastal sites. In
general, geographically separated populations even at a
rather regional spatial scale showed a deep genetic sub-
structure as in the species T. cornuta (Kieneke etal. 2012).
1.8Ecology
Gastrotrichs are important components of aquatic habitats
and can reach considerable number. Densities are usually
extrapolated from small samples to larger volumes and
have to be taken with some care. For example, Nesteruk
(1996) gives values between 495,000 and 2,600,000 spe-
cimens per m2 for freshwater standing waters. Muschiol &
Traunspurger (2009) found densities of 0.67 × 106 spe-
cimens of Chaetonotus sp. per m2 in a lake on the Gala-
pagos Islands. In the marine environment, gastrotrichs
form an important part of the meiofaunal community,
but their density depends on the grain size. On sandy
beaches, Schmidt & Teuchert (1969) counted almost 1000
specimens/50 cm-3. In muddy sediments in the Adriatic
Sea (Mediterranean), Leasi & Todaro (2010) found a low
diversity and density of gastrotrichs, ranging between 0
and 97.7 specimens per 10 cm2. Unusual high densities
are known, for example, in the marine species Turbanella
hyalina (Hummon 1976). Such high population densities
may be correlated with a high bacterial abundance due to
discharge of untreated sewage water close to the habitat
(Hummon & Hummon 1993).
In the food web, gastrotrichs have a low trophic level,
feeding on bacteria, small algae, or detritus (e.g., Bennett
1979, Balsamo & Todaro 2002, Todaro & Hummon 2008).
Gastrotrichs themselves are probably food of predators
of about the same size class or may serve, together with
other meiobenthic organisms, as nutrition resource for
large, sediment-consuming animals of the infaunal mac-
robenthos (e.g., Giere 2009). Because of the latter con-
nection, gastrotrichs and other meiobenthic animals are
considered to be an important link between the microbial
loop and higher trophic levels (Balsamo & Todaro 2002).
Measured in abundance (individuals per area), Gastrotri-
cha may rank second to fourth in numerical dominance
among all micrometazoans (e.g., Hummon 1976). Based
on his studies of gastrotrich communities of two Scot-
tish beaches, Hummon (1976) was able to estimate the
mean dry weight biomass of Gastrotricha in those bioto-
pes. Values ranged between 48 and 274 mg/m2 while the
highest station values ranged between 0.6 and 3.1 g/m2.
All marine and many freshwater gastrotrichs are asso-
ciated with the sediment and live either in the epibenthic
layer or in the sediment in the pore system (interstitial
system). A number of freshwater species is associated
with aquatic vegetation and moves among plants. Some
species are capable of short swimming periods, such as
Heterolepidoderma sp. (Bancetti & Ricci 1998), but only
species of Dasydytidae and Neogosseidae are swimming
permanently and can hence be regarded as belonging to
the planktonic community.
Among freshwater, most chaetonotoid gastrotrichs
prefer slow or no water motion. After Ricci & Balsamo
(2000), from 250 freshwater species only 35 are found in
running (lotic) waters. A number of species appears to be
quite tolerant to low oxygen content (Schwank 1990) and
a number of species is found in moors and tolerates pH
values down to 4 (Kisielewski 1981, Schwank 1990). Kisie-
lewski (1981) found the species diversity and abundance
of specimens highest in eutropicated peat bogs. Hummon
& Hummon (1979) were able to cultivate Lepidodermella
squammata in acid mine water with different contents of
carbonate. Survival and reproduction were positively cor-
related with the carbonate content.
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126 1Gastrotricha
species with also a large number of adhesive tubes, inhabi-
ted medium-exposed sediments, and Paraturbanella dohrni,
a species with much fewer adhesive tubes, inhabited tidal
ponds with fine sediment. Also, Hummon (1975) concluded
that hydrodynamic cycles, seasonal, lunar-phasic tidal,
semidiurnal tidal, or localized, can affect dramatic changes
in the distribution of Gastrotricha in a marine beach.
Acknowledgments
We are very thankful to the Gastrotricha community, espe-
cially to our colleagues Rick Hochberg and Birgen Holger
Rothe, for their collaboration in several projects. Maria
Balsamo, Loretta Guidi, Tobias Kanneby, Takahito Suzuki,
and Andreas Hejnol were so kind to send us pictures of
representatives we were lacking. Many thanks also to
Corinna Schulze for her help and to Pedro Martínez Arbizu
for giving AK the opportunity to work on this book chapter.
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between the number of adhesive tubes and wave action and
sediment type. In coarse sediment and wave action, Mac-
rodasys caudatus, a large species with numerous adhesive
tubes, was most abundant. Turbanella cornuta, a smaller
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