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Vertebral Comparative Anatomy and Morphological Differences in Anguine

Lizards with a Special Reference to Pseudopus apodus: Vertebral column and
ribs of Pseudopus apodus

Article  in  The Anatomical Record · January 2019

DOI: 10.1002/ar.23944

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 THE ANATOMICAL RECORD (2018)

Vertebral Comparative Anatomy and

Morphological Differences in Anguine
Lizards With a Special Reference to
Pseudopus apodus
ANDREJ CER  
NANSKÝ ,1 OLEKSANDR YARYHIN ,2,3,4 JANA CICEKOVA,  1
INGMAR WERNEBURG,2,5,6 MIROSLAV HAIN,7 AND JOZEF KLEMBARA1*
1
Faculty of Natural Sciences, Department of Ecology, Comenius University in Bratislava,
Bratislava, Slovakia
2
Senckenberg Center for Human Evolution and Palaeoenvironment (HEP) an der Eberhard
Karls Universität Tübingen, Tübingen, Germany
3
I.I. Schmalhausen Institute of Zoology of National Academy of Sciences of Ukraine, Kyiv,
Ukraine
4
Faculty of Biology, Department of Zoology, Lesya Ukrainka Eastern European National
University, Lutsk, Ukraine
5
Fachbereich Geowissenschaften der Eberhard-Karls-Universität Tübingen, Tübingen,
Tübingen, Germany
6
Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung an
der Humboldt-Universität zu Berlin, Berlin, Germany
7
Institute of Measurement Science, Slovak Academy of Sciences, Bratislava, Slovakia

ABSTRACT
The article reports on the first detailed vertebral and rib morphology of
anguine taxon Pseudopus apodus using micro-computed tomography. A
comparison shows significant morphological differences of vertebrae of
Pseudopus relative to those of Anguis and Ophisaurus. Usually, there are
55 presacral vertebrae, two sacral, and 95–97 caudal vertebrae. Pseudopus
apodus can be defined by 23 diagnostic features concerning the vertebral
column. Although zygapophyseal articulation between atlas and axis is
well developed in limbed anguid gerrhonotine lizards like Abronia or Bari-
sia, it is absent in the extant representatives of the clade Anguinae, which
are limbless. Thus, our study brings further support to the hypothesis
about the complete reduction of this articulation in forms with reduced or
absent limbs. Comparison of adult and juvenile morphology of vertebrae of
P. apodus was also analyzed. Heterochrony in the evolution of this taxon
was previously confirmed by its skull morphology and it can be also docu-
mented on the basis of vertebrae. Our data suggest that a peramorphic het-
erochronic process played a role in the evolution of this largest extant
anguine species. Geometric morphometric analyses revealed a pattern of
high vertebral disparity among species. We found a clear separation of
limbless forms in morphospace. Pseudopus apodus always clusters within
Ophisaurus-species confirming molecular and some morphological phyloge-
nies. Only the first tail vertebra shows a distinct difference to those of

Grant sponsor: NSF; Grant number: EF-0334961; Grant spon-
sor: DigiMorph.org; Grant sponsor: University of Texas at Aus-
tin; Grant sponsor: SNF; Grant number: P300PA_164720.
*Correspondence to: Jozef Klembara, Faculty of Natural Sci-
ences, Department of Ecology, Comenius University in Bratislava,
Ilkovicova 6, 842 15 Bratislava, Slovakia. Tel: 02/602 96 257
Fax: (02) 654-29-064 E-mail: jozef.klembara@uniba.sk
Jana Ciceková is currently affiliated with The Bridge Lan-
guage Centre, Baštová 344/7, 811 03 Bratislava 1.
Received 21 November 2017; Revised 22 March 2018; Accepted
6 April 2018.
DOI: 10.1002/ar.23944
Published online 00 Month 2018 in Wiley Online Library
(wileyonlinelibrary.com).

© 2018 WILEY PERIODICALS, INC.

2 
CER 
NANSKÝ ET AL.
other anguids, which might be related to altered locomotion associated to
the larger body size in this species. Anat Rec, 2018. © 2018 Wiley
Periodicals, Inc.
Key words: squamata; legless lizards; postcranial skeleton; mor-
phology; ribs
This article represents a contribution to the knowledge
of the osteology of Pseudopus apodus and refers to the
previous papers of Klembara et al. (2014, 2017a) on the
lower jaw and skull morphology. Nowadays, P. apodus
(Pallas, 1775)—the glass lizard or sheltopusik—occurs in
South-East Europe to Central Asia. It composes, together
with Ophisaurus (North America, South-East Asia, and
North Africa) and Anguis (Europe and West Asia), the
Anguinae clade, which is nested inside Anguidae
(Conrad, 2008). All extant members of Anguinae are leg-
less having serpentiform morphology. The limb reduction
is not restricted to Anguinae, but is frequently observed
in other lizard clades such as Scincoidea, Gekkota, or
Amphisbaenia (see e.g., Lande, 1978; Gans and Montero,
 nanský, 2016). In addition to
2008; Lee et al., 2009; Cer
Anguinae, three other clades belong to the Anguidae: Ger-
rhonotinae, Diploglossinae, and Glyptosaurinae (Conrad,
2008). The Gerrhonotinae and Diploglossinae are
restricted to the territories of the New World. The Glypto-
saurinae consists of exclusively fossil members recorded
in North America and Eurasia in deposits dated from the
Late Cretaceous to the Late Oligocene (Sullivan, 1979;
Estes, 1983; Böhme, 2007).
In general, the fossil history of the clade Anguinae is
well documented from the Cenozoic of Europe
(e.g., Fejérváry-Lángh, 1923; Rage and Augé, 1993; Klem-
 nanský et al., 2015; Klembara and Rum-
bara, 2012; Cer
mel, 2018), however, most of the finds are represented
only by isolated elements like jaws, skull bones, verte-
brae, and osteoderms. In such cases, it is very difficult to
associate different types of skeletal elements to a single
species. Besides this, there is a lack of comparative stud-
ies of the skeletons of the extant forms. The oldest known
representative of Pseudopus (P. ahnikoviensis Klembara,
2012) comes from the early Miocene (MN 2) of Germany
 nanský et al., 2015), although its earlier appearance
(Cer
cannot be excluded (see Cer nanský et al., 2016). In addi-
tion to P. ahnikoviensis, four other species of Pseudopus
are known in the Cenozoic of Eurasia: P. confertus (early
Miocene of Europe), Pseudopus laurillardi (early-middle
Miocene of Europe), P. pannonicus (late Miocene-middle
Pleistocene of Central and Eastern Europe), and
P. apodus (late Pleistocene-Recent; Klembara et al., 2010;
Klembara, 2012, 2015; Klembara and Rummel, 2018).
Extant P. apodus inhabits open to poorly vegetated envi-
ronments of arid and sub-arid territories of the South-
East Europe and West and Central Asia (Obst, 2004).
Pseudopus apodus feeds on various invertebrates like
slugs with or without shells, insects, and small verte-
brates, mostly young rodents and lizards. Rifai
et al. (2005) reported that the stomach of this species con-
tained both arthropods (88.7%) and molluscs (5.3%), and
Çiçek et al. (2014) reported that insects are the
predominant food (86.1%), with gastropods forming 8.3%
of the prey. The locomotory behavior of this legless large
anguine lizard was described by Gans and Gasc (1990).
The only source of knowledge of the anatomy of the ver-
tebral column and ribs of Pseudopus apodus are the line
drawings of several vertebrae and ribs in the paper of
Fejérváry-Lángh (1923) used for comparative purposes
for the description of the fossil species P. pannonicus.
Hoffstetter and Gasc (1969) published line drawings of
sacral vertebrae of P. apodus and briefly described them
in the context of the vertebral column anatomy of all liz-
ards. In addition to P. apodus, in all other papers dealing
with the anatomy of the postcranial skeleton of other spe-
cies of anguines, the authors mostly provide only short
descriptions or simple figures of the given vertebral ele-
ment in terms of the comparisons with the fossil forms
(e.g., Hilgendorf, 1885; Meszoely, 1970; Bachmayer and
Młynarski, 1977; Klembara, 1981, 1985, 1986; Młynarski
et al., 1982, 1984; Rocek, 1984; Venczel and Sen, 1994;
Tempfer, 2009). Hence, our knowledge of the anatomy of
the vertebral column and ribs of the members of the
Anguinae clade is very limited.
The phylogenetic position of P. apodus is contested.
Some morphological analyses find an unresolved relation
to Anguis and Ophisaurus (Klembara et al., 2014). Molec-
ular and some morphological data suggest a position of
Anguis and P. apodus within Ophisaurus, although there
is no consistency about the exact position within this
group (Conrad et al., 2011; Pyron et al., 2013; Zheng and
Wiens, 2016).
The present study has the following aims:
1. The detailed anatomical description of the vertebral
column and ribs of P. apodus and their comparisons with
those of Ophisaurus (living in three continents—North
Africa, South-East Asia, and North America, including
very rare species, e.g., Ophisaurus sokolovi) and Anguis,
to determine the distinguished features of these three
extant anguine genera. This will serve as a reference for
other comparative anatomical studies of any other angui-
morph, extant, or extinct (such a study is crucial for the
determination of the abundant record of the fossil post-
cranial elements).
2. To test the hypothesis regarding the loss of the
zygapophyseal articulation between the atlas and axis
during the transition from limbed to serpentiform body
 nanský (2016) observed that in members of the
form. Cer
clade Scincoidea such a loss is present during this tran-
sition. Our aim is to find out whether similar morpholog-
ical changes occurred also within the members of the
clade Anguidae. For such purposes, members of Gerrho-
notinae (Abronia, Mesaspis and Barisia) and Diploglossi-
nae (Celestus) will be compared with members of
Anguinae.
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS 3
3. To study, whether the peramorphic heterochronic TABLE 2. Specimens of Pseudopus apodus observed
process, which was identified in the evolution of the
Skulls of dry specimens
P. apodus lower jaw and skull (Klembara et al., 2014, Specimen number skull length (snout-occipital condyle
2017a), can be recognized also in the vertebrae of this distance)
species. Heterochrony is a change in timing and rate of DE 10 (juvenile) 26 mm
the developmental events in descendant relative to tim- DE 58 (juvenile) 21.8 mm
ing and rate of the developmental events in the ancestor DE 4 (adult) 39.4 mm
(Alberch et al., 1979; McNamara, 1986). We evaluate the DE 6 (adult) 46 mm
ontogenetic, and/or growth stages of anguines in the con- DE 8 (adult) 36 mm
text of their phylogeny. The potential heterochronic pro- DE 52 (adult) 40 mm
cesses are identified on the basis of the comparison of DE 53 (adult) 36.5 mm
Disarticulated skulls of dry specimens
adult and juvenile morphology of the descendant with Specimen number
those of the adult and juvenile morphology of the ances- juveniles: BSPG 1982 X 2383, DE 9
tor. The aim is to detect the possible occurrence of the DE 11 (3 months old)
ancestral adult morphology in a descendant juvenile adults: DE 1, DE 3, DE 13, DE 22, DE 23, DE 29, DE 54, DE
stage of development as it was detected in the case of sev- 59
eral cranial features of P. apodus (Klembara et al., 2014, Specimens preserved in alcohol
2017a), Specimen number head length (snout-middle ear distance)
4. To compare the shape of selected vertebrae among DE 61a (juvenile) 18.8 mm
different anguid species using geometric morphometrics DE 62a (juvenile) 23.4 mm
DE 64a (subadult) 33.5 mm
in order to recognize phylogenetic or ecological patterns DE 55a (adult) 46 mm
in morphospace distribution. Specimen stained in toto for cartilage (Alcian blue) and bone
(alizarin red) and preserved in glycerine (g)
Specimen number head length
MATERIALS AND METHODS DE 104 g (adult) 34.5 mm
The terminology of the individual structures of the Specimens used for micro CT
given bones are primarily from Fejérváry-Lángh (1923), Specimen number head/skull length
DE 11 (juvenile)—disarticulated
Hoffstetter and Gasc (1969), Romer and Parsons (1977),
DE 61a (juvenile) 18.8 mm
Estes (1983), and Conrad (2006). For institutional abbre- DE 62a (juvenile) 23.4 mm
viations, see Table 1. In total, we examined nine anguine DE 64a (subadult) 33.5 mm
species, representing all described extant genera: Pseudo- DE 1 (adult)—disarticulated
pus (Table 2), Ophisaurus, and Anguis (Table 3). Addi- DE 4 (adult) 39.4 mm
tionally, several morphological characters from other DE 8 (adult) 36 mm
anguid taxa were examined, but not described in detail DE 13 (adult)—disarticulated
(Abronia, Barisia, Mesaspis, and Celestus—see Table 3). DE 27 g (adult) 32.5 mm
DE 52 (adult) 40 mm
DE 55a (adult) 46 mm
Micro-Computed Tomography Imaging Specimens photographed using SEM
Specimen number
A GE Phoenix nanotom VR 180 X-ray tomography DE 13 (adult), DE 22 (adult)—disarticulated
nano-CTVR system at the Slovak Academy of Sciences in Histological sections
Bratislava was used (Fairfield, CT) for micro-computed Specimen number head length
tomography imaging (μCT)-scanning of the specimens. DE 109 (3 months old juvenile) 16 mm
The X-ray tube was fitted with a tungsten target, microfo-
cusing mode M0 was used and no filtering was applied for
outgoing X-ray radiation. Accelerating voltage was typi-
cally set to U5120 kV and beam current to I,580 lA; these
parameters were optimized for each CT scan. In each
TABLE 3. Additional lizard taxa observed for
comparisons
TABLE 1. Institutional abbreviations Species specimen number(s)
Anguis fragilis DE 14-21, 24, 25, 45-48, 102a, 103a
Abbreviations Institution Location
Ophisaurus ventralis DE 34, 35, 38, 99a, 100a; AMNH
AMNH American Museum of Natural USA 73057; UF 52539; CM 1411; ZFMK 27411, 95,414
History New York O. attenuatus DE 32, 33, 43, 44
BSPG Bayerische Staatssammlung für Germany O. compressus DE 50; ZFMK 32194
Paläontologie Munich O. mimicus DE 49
CM Carnegie Museum of Natural USA O. koellikeri DE 30, 41; ZFMK 13118, 13,119
History Pittsburg O. harti DE 36, 37, 56, 57, 86; AMNH 34956; ZFMK 9472
DE Department of Ecology, Faculty of Slovakia O. sokolovi ZFMK 91063
Natural Sciences, O. gracilis DE 42
Comenius University in Bratislava Abronia graminea DE 67
FMNH The Field Museum Chicago USA Barisia rudicollis DE 68-70
UF University of Florida Gainesville, USA B. imbricata NHMUK 92.9.5.32
ZFMK Zoologisches Forschungsmuseum Germany Mesaspis monticola DE 71, 72
Alexander Celestus enneagrammus FMNH 108860
Koenig Bonn Eumeces schneideri DE 60
4 
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NANSKÝ ET AL.

Fig. 1. Pseudopus apodus (Pallas, 1,775): Anterior region of vertebral column of DE 55 in (A) lateral, (B) dorsal, and (C) ventral aspects. (D) Region
around sacral portion in lateral aspects.
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS 5

Fig. 2. Pseudopus apodus (Pallas, 1,775): Atlas of DE 55 in (A) dorsal, (B) ventral, (C) lateral (compared to the size of axis), (D) lateral, (E) anterior,
and (F) posterior aspects.
6 
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NANSKÝ ET AL.
Fig. 3. Pseudopus apodus (Pallas, 1,775): Axis of DE 55 in (A) dorsal, (B) ventral, (C) lateral, (D) anterior, and (E) posterior aspects.
measurement, 1,800 projections were recorded. The CT data
sets were analyzed using Avizo 8.1 and the outlines of the
vertebrae and ribs were manually selected using the magic
wand tool. Surface meshes were exported as ply format files
for the geometric morphometric analyses. Celestus ennea-
grammus was scanned using University of Texas High-
Resolution X-ray CT facility (see Digimorph.org, 2002) .
3D-Geometric Morphometrics of Vertebral
Shapes
The following 10 specimens were used in the 3D
geometric morphometric analysis (the exact position of each
vertebra is known due to scanning of complete specimens):
Pseudopus apodus DE 55, DE 64, Anguis fragilis DE
102a, Abronia graminea DE 67, Ophisaurus compressus
ZFMK 32194, O. gracilis DE 42, O. harti ZFMK 9472,
O. koellikeri ZFMK 13118, O. ludovici ZFMK 91690,
O. sokolovi ZFMK 91063, O. ventralis ZFMK 95414.
For geometric morphometric analyses, we have chosen
vertebra 2 (cervical 2, axis, CV2), vertebra 4 (second post-
axis vertebra, CV4), vertebra 23 (trunk vertebra, TV),
sacrals 1 and 2 (SV1, SV2), and caudal vertebral
1 (KV) for each specimen. For each vertebra, we defined
13 homologous landmarks, which were added to the sur-
face meshes of each vertebra using the software “land-
mark” (Wiley et al., 2005). We did not include the atlas to
the analysis, because it has great anatomical disparity
and it is difficult to define homologous landmarks. The
landmark data were transferred to PAST version 3.15
(Hammer et al., 2001) and Procrustes modified. The Pro-
crustes procedure removed translation, size and rotation
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS
Fig. 4. Pseudopus apodus (Pallas, 1,775): The fourth (second postaxis) vertebra of DE 55 in (A) dorsal, (B) ventral, (C) lateral, (D) anterior, and (E)
posterior aspects.
effects. Classical cluster analyses were performed for all
vertebrae. Afterwards, the same vertebrae of all species
were analyzed separately as covariance-matrices by prin-
cipal component analyses (PCA) to see whether there are
regional patterns specific for the respective vertebrae.
RESULTS
Adult Morphology
Here, we describe the morphology of vertebrae and ribs
of the adult specimens of P. apodus (Fig. 1) in detail. The
typical vertebra of the adult is procelous with the cen-
trum in shape of a conical frustrum. The cotyles and con-
dyles are depressed—oval to kidney shape. The cotyles
have an anteroventral orientation. The condyles are pos-
terodorsally oriented and they lack a precondylar con-
striction. The intercentra are present on the ventral face
of the centra in the first few presacral vertebrae. Their
7
position varies, most commonly they are in the middle of
the ventral surface of the centrum but they can be located
more or less anteriorly or posteriorly. The sutures
between centrum and intercentrum are absent. The inter-
centra in the caudal region are present in the form of hae-
mal arches (haemapophyses) on the ventral surface of
each vertebra. The zygosphenes and zygantra are absent.
The articular facets of both prezygapophyses and postzy-
gapophyses are oval, being more or less laterally
expanded. The prezygapophyses are laterodorsally ori-
ented and, anteriorly, they overreach the centrum of the
vertebra. The postzygapophyses have a ventrolateral ori-
entation and posteriorly they do not reach the level of the
end of the condyle. In dorsal view, the prezygapophyses
as well as postzygapophyses have approximately the
same length. The anterolaterally located synapophyses
are dorsoventrally oriented and slightly inclined posteri-
orly. They extend in slightly anteroposterior direction
8 
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NANSKÝ ET AL.
Fig. 5. Pseudopus apodus (Pallas, 1,775): Dorsal vertebra of DE 23 (26th vertebra) in (A) dorsal, (B) ventral, (C) lateral, (D) anterior, and (E)
posterior aspects.
from the anterior edge of the ventral region of the cen-
trum to the base of the prezygapophyses.
Since it is difficult to distinguish the cervical region
from the trunk region in limbless forms (Romer, 1956;
Hoffstetter and Gasc, 1969), we have divided the verte-
bral column into three regions: presacral, sacral, and cau-
dal region. The number of all vertebrae varies from
151 to 154. There are 54 (DE 23) to 55 (DE 13) vertebrae
in the presacral region. There is one sacral vertebra; how-
ever, the first caudal vertebra may be considered as the
second sacral (Hoffstetter and Gasc, 1969). The number of
caudal vertebrae in our specimens varies from 95 to 97.
As mentioned, the number of vertebrae in the presacral
region is usually 55. The atlas, axis, and the third vertebra
are ribless. The fourth vertebra is the first one bearing a
rib. Apart from the first three, the synapophyses of all the
presacral vertebrae are well-developed. The first few ante-
rior presacral vertebrae possess keeled intercentra.
Atlas
The atlas is present in a form of atlantal ring that is
attached to the anterior region of the axis (Fig. 2). Like in
other lepidosaurs, it is composed of three parts—the two
atlantal (neural) arches whose pedicles rest on each side
of the ventrally located first intercentrum. The neural
arch is formed from the lower part—above mentioned
thick pedicles, which bears anterior and posterior articu-
lar facets (articular portion) and the upper part—lami-
nae, which frame the neural canal (neural portion). They
are wedge shaped, being anteriorly inclined. There is no
dorsal contact of the laminae, but a small gap is present.
In large specimens (e.g., DE 13 or DE 52), the dorsome-
dial margins of the arches attach very closely to each
other. These ones have a dorsal contact but are not fused.
The transverse process is small, forming only a postero-
laterally expanded bulge on the base of each atlantal
arch. It represents a vestige of the synapophyses. The
posterodorsal process is short, having no articular facet
on the ventral side. It reaches further posteriorly than
the transverse process. The first intercentrum bears a
well-developed robust ventral keel that is oriented poster-
oventrally. It is ovoid in lateral view, having a rounded
margin and being thin in anterior view. In lateral view,
its maximum anteroposterior width is bigger than its dor-
soventral height. The keel reaches a deeper level
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS 9

Fig. 6. Pseudopus apodus (Pallas, 1,775): The first sacral vertebra of DE 55 in (A) dorsal, (B) ventral, (C) lateral (compared to the size of the
second sacral vertebra), (D) lateral, (E) anterior, and (F) posterior aspects.
10 
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NANSKÝ ET AL.

Fig. 7. Pseudopus apodus (Pallas, 1,775): The second sacral vertebra of DE 55 in (A) dorsal, (B) ventral, (C) lateral (compared to the size of the
first sacral vertebra), (D) lateral, (E) anterior, and (F) posterior aspects.
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS
Fig. 8. Pseudopus apodus (Pallas, 1,775): The first caudal vertebra of DE 55 in (A) dorsal, (B) ventral, (C) lateral, (D) anterior, and (E) posterior
aspects.
ventrally than the second intercentrum. The height of the
atlantal ventral crest is approximately the same as the
height of the articular portion of the atlantal arch, and
the maximum width of it is 1.5 of its height. The dorsal
surface of the intercentrum bears two articular facets, the
anterior, and posterior, respectively. Together with the
articular facets of neural arches anteriorly, these articu-
lar facets form two articular surfaces, which provide the
articulation with the occipital condyle of the skull. In
anterior view, the maximum size of the anterior one is
larger than the size of lateral articulations on the pedi-
cles. The posterior articular facets open more widely than
the anterior ones and contact the odontoid process of
the axis.
Axis
The centrum of the axis is large and robustly built,
being extended anteroposteriorly (Fig. 3). In ventral view,
its lateral margins are almost straight, rendering the ver-
tebral body rhomboidal in shape. Anteriorly, the odontoid
process is fused to the centrum. The sutures between the
centrum of the axis and the odontoid process (= the atlan-
tal pleurocentrum) are usually not visible, or only small
traces of the fusion are still present in some specimens.
The anterior projection of the odontoid process is short,
dorsally inclined, and protrudes approximately to the
11
level of the half of the atlantal ring. It ends bluntly. On
the lateral wall of the centrum, approximatelly in the
anterior third, a well developed although short synapo-
physis is present. It is expanded posterolaterally, being
slightly inclined ventrally in anterior view. Prezygapo-
physeal articulations are completely missing and the sup-
porting structures remain only as small vestiges. The
postzygapophyses have large elliptical (or roughtly
square; more elongated than in other presacral vertebrae)
articulation surfaces, oriented more or less posteriorly.
The posterior end of the axis centrum forms a dorsally
depressed condyle, which is kidney shaped in posterior
view. This condyle is not so markedly developed as it is in
other vertebrae. Ventrally, there is a long, slightly poste-
riorly curved keel, formed by the robust second intercen-
trum. The anterior region of the second intercentrum
forms a large area for a contact with the first intercen-
trum. In lateral view, there is a small notch on the ante-
rior margin of the second intercentrum. Its posteroventral
region is fused to the third intercentrum. In the upper
region, a small oval fenestra is located between them (how-
ever, this can vary—they can be completely fused into a
single crest). The third intercentrum is posteroventrally
oriented, having a straight course.
The neural canal is roughtly pentagonal in shape and
small. Its dorsal end reaches the level of postzygapo-
physes and the entire hight of canal forms only 23% of
12
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Fig. 9. Pseudopus apodus (Pallas, 1,775): The fourth left rib of DE 55 in (A) medial, (B) lateral, (C) anterior, and (D) posterior aspects.
the entire axis hight. In lateral view, the neural spine is
ax shaped, having a rounded dorsal margin. It reaches its
highest level in its posterior section, whereas the height
decreases anteriorly. The anterior region protrudes far
more anteriorly relative to that of the posterior expansion
of posterior region. Although the anterior region runs
close to the level of the end of the odontoid process, this
region never exceeds this level. The posterior region
approximately reaches the level of the condyle. In dorsal
view, the width of the neural spine is constant in the first
half of its entire anteroposterior length. Then, it widens
gradually posteriorly having a small notch at its end.
Thus, the whole neural spine forms a structure of a
reversed letter Y.
Postaxis Presacral Vertebrae
In all postaxis presacral vertebrae, there is a strong
tendency to uniform morphology, probably associated
with limb reduction and multipication of vertebral seg-
ments (Hoffstetter and Gasc, 1969). There are, however,
few characteristic features that can be attributed to verte-
brae belonging to a certain part of the vertebral column.
The relative size of vertebrae increases regularly from
anterior to posterior (especially seen in the first seven
vertebrae—including atlas and axis; these vertebrae are
smaller than the posteriorly located ones and their size
gradually increases posteriorly in all dimensions). The
first few postaxis presacral vertebrae have relatively
short centra compared with posterior presacrals—the
length of the centrum of the first postaxis vertebra is
approximatelly half of the length of the last presacral ver-
tebra. There is an abrupt presacral shortening of the cen-
trum of the last three presacral vertebrae, however, the
centra are never smaller than the centra of the first pre-
sacral vertebrae. Besides their relative smaller size, the
first presacrals have several morphological differences
from other presacral vertebrae and could be considered as

NANSKÝ ET AL.
neck vertebrae. Ventrally, the centra of these vertebrae
(including atlas and axis) are keeled (bearing hypapo-
physes). Hypapophyses of the third and forth vertebra
are well developed (Fig. 4). All consecutive ones gradually
become reduced up to a faint medial ridge on the last ver-
tebra. The neural spine of the third vertebra differs from
the posteriorly located one by its more pronounced poste-
rior inclination, exceeding the level of posterior end of the
condyle. Moreover, it has a narrower appearence in lat-
eral view than others. The dorsal region of the neural
arch of typical mid-trunk vertebra slightly rises in height
posteriorly. The neural spine is square in shape in lateral
view (Fig. 5). It starts to rise dorsally approximatelly at
the mid level of the entire length of the neural arch. Ante-
riorly, a low medial ridge runs to the end of the neural
arch, where it forms a small spike. In lateral view, the
dorsal margin of the neural spine is almost straight. It
does not exceed the condyle posteriorly. In dorsal view, it
gradually widens only slightly in posterior direction. Its
height remains constant across the entire length of presa-
cral region.
The neural canal is oval and small. Pre and postzygapo-
physes are well expanded laterally. They are dorsally
inclined in an angle of 39 degree. Articular surfaces are
large, elliptical, and oblong laterally. Posteriorly, the postzy-
gapophyses reach only the level of the base of the condyle,
but the condyle itself reaches further posteriorly. The inter-
zygapophyseal constriction is well developed and deep.
The synapophyses are well developed, especially from the
fourth vertebra, where the first ribs appear. The synapo-
physes are slightly posterolaterally oriented and their length
remains approximately the same throughout the entire ver-
tebral column. As the length of the vertebrae increases in
posterior direction, the ratio of the two lengths decreases.
Subcentral foramina of the last vertebrae are small and elon-
gated, forming an incision on each side of the medial plane.
The subcentral ridges are straight and gradually
become closer from anterior to posterior region. The
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS 13

Fig. 10. Pseudopus apodus (Pallas, 1,775): Juvenile morphology, axis of DE 62a in (A) lateral aspect with separation of its parts. (B) In lateral
aspect in normal anatomical position of its parts. Dorsal vertebra of BSPG 1982 X 2383 in (C) dorsal, (D) ventral, (E) lateral, (F) anterior, and (G)
posterior aspects.
14 
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NANSKÝ ET AL.

Fig. 12. Comparison of atlas in (A) dorsal, (B) ventral, (C) lateral, (D)
anterior, and (E) posterior aspects.

Fig. 11. Comparison of atlas in (A) dorsal, (B) ventral, (C) lateral, (D)
anterior, and (E) posterior aspects (continued in the following figure).

whole ventral region of the centrum is flat; only around

the cotyle, there is a small bulge. The pair of small sub-
central foramina is located in the anterior third of the
centrum.

Sacral Vertebrae
According to Hoffstetter and Gasc (1969) there is one
sacral vertebra, however the authors suggested that the
next posteriorly located caudal vertebra can be considered
as the second sacral. Unlike the first sacral vertebra
(Fig. 6), the second one usually bears chevron bones
which form haemal arches ventrally (DE 13). However,
the overall morphology of this vertebra is more similar to
that of the first sacral than the posteriorly located caudal
vertebrae. In addition, in DE 55, we have observed a total
absence of the haemal arch on the second sacral vertebra
(Fig. 7). Therefore, we follow the definition of Hoffstetter
and Gasc (1969) and we consider this vertebra as the sec-
ond sacral.
The first sacral vertebra lacks a haemal arch (Fig. 6).
The subcentral foramina on the ventral surface of the ver-
tebra run into the incisions, extending posteriorly along
both sides of the medial line of the centrum. The centrum
is significantly shorter than the centrum of the anteriorly
located vertebrae, and its length is approximately the
same as the length of the vertebrae in the middle part of
the presacral region. The condyle is oval rather than kid-
ney shaped. The cotyle is oval as well, although its ven-
tral margin is almost straight. This margin is V shaped Fig. 13. Comparison of axis in (A) dorsal, (B) ventral, (C) lateral, (D),
in ventral view. The height of neural spine is the same as anterior, and (E) posterior aspects (continued in the following figure).
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS 15
seem more robust than the pleurapophyses of the first
sacral. Distally, they are also forked and in the middle of
the bifurcation there is an opening of the transverse
canal. In comparison to the first sacral, they are not as
long. There is no contact of the pleurapophyses of the first
and second sacral vertebrae. The chevron bones are pre-
sent, forming a posteroventrally oriented haemapophysis.
The neural canal is thinner laterally relative to the neu-
ral canal of the first sacral.

Caudal Vertebrae
The length of the longest caudal centrum is not bigger
than the length of the centrum of any presacral vertebra.
Posteriorly, there is a strong tendency toward the elonga-
tion of the centra and a relative reduction of all processes.
In general, caudal centra are relatively slimmer than presa-
cral ones. Anteroposteriorly, the ventral face of the centrum
is slightly concave with a shallow groove on each side of the
medial plane. In posterior caudal vertebrae, the condyle is
separated from the centrum of the vertebra by a sharp inci-
sion that, however, cannot be interpreted as precondylar
constriction. From the posterolateral margins of the cen-
trum, the haemapophyses arise posteroventrally (they are
fused to the centrum). The tip overreaches the posterior
margin of the condyle. The angle between the ventral part
of the centrum and anterior margin of the haemapophyses
increases distally. The height of the haemapophysal canal
is the same as the length of the distal part of the haemapo-
physes. In anterior vertebrae, the haemapophyses have the
same length as the length of the vertebrae, however, poste-
riorly they shorten. The anterolateral corners of the cen-
trum bear dorsoventrally flattened pleurapophyses. The
Fig. 14. Comparison of axis in (A) dorsal, (B) ventral, (C) lateral, (D)
anterior, and (E) posterior aspects.

in all presacral vertebrae, but it is anteroposteriorly

short, having a rectangular appearance in lateral view.
The length of the dorsal margin of the spine is almost half
of the length of the spines of preceding vertebrae.
The typical feature of sacral vertebrae is the presence
of pleurapophyses. They are large, lateroventrally ori-
ented, and forming long processes. They are broad, espe-
cially on their bases, almost reaching the length of the
centrum without the condyle. They slightly widen ventro-
laterally, expanding from the centrum to the level where
they reach the half of their length. The anterior
section ends here, forming a small anterior spina. The
posterior section runs further and it is posteriorly
inclined in lateral view. It becomes thinner distally, being
bluntly ended. The anterior edge of the pleurapophysis
runs continuously into the ventral margin of the cotyle.
The total length of pleurapophyses does not extend the
dorsal length of the vertebra (measured from the ventral
margin of the centrum to the dorsal end of the neural
spine). On the ventral face, at the base of each pleurapo-
physis, there is an opening of the transverse canal that
connects the posterior lymphatic hearts and the median
perivascular lymphatic space (Hoffstetter and Gasc,
1969). The distal part of the pleurapophysis articulates
with the ilium, which has a ventrolateral orientation. The
connection is via a ligament. As mentioned above, the
morphology of the second sacral vertebra (Fig. 7) strongly Fig. 15. Comparison of the fourth (second postaxis) vertebra (A)
resembles that of the first sacral. The pleurapophyses dorsal, (B) ventral, (C) lateral, (D) anterior, and (E) posterior aspects
gradually slightly widen distally, and, therefore, they (continued in the following figure).
16 
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NANSKÝ ET AL.

Fig. 17. Comparison of dorsal vertebra in (A) dorsal, (B) ventral, (C)
lateral, (D) anterior, and (E) posterior aspects (continued in the following
figure).

articular facet and several outgrowths. The dorsoventrally

Fig. 16. Comparison of the fourth (second post-axis) vertebra in (A) oriented articular facet is of oval shape, and it meets the syna-
dorsal, (B) ventral, (C) lateral, (D) anterior, and (E) posterior aspects. pophysis of the corresponding vertebra. Posterodorsally from
the base of the facet, a relatively robust posterodorsal process
anterior edges of the pleurapophyses are slightly concave, arises. In biggest ribs, it is almost as long as the horizontal
and they protrude straight from the centrum behind the
cotyle. The posterior edges of the pleurapophyses arise from
the middle of the centrum and they are anterolaterally ori-
ented. The pleurapophyses of the first two caudal vertebrae
are slightly wider (Fig. 8) than the pleurapophyses of the
rest of caudals. Anteriorly, the prezygapophyses overreach
the cotyles. There is a faint ridge connecting the prezygapo-
physes and pleurapophyses. The postzygapophyses do not
overreach the condyles posteriorly. The ratio between the
size of the zygapophyses and the length of the centrum
decreases distally. From the posterior part of the neural
arch, a neural spine arises. It is posterodorsally oriented.
The caudal spines are, contrary to the presacrals, slim and
tall, and in the distal part of the vertebral column, they
overreach the posterior margin of the condyle. Distally they
gradually shorten and slope down to the postzygapophyses.
No transverse autotomic split is present in any caudal ver-
tebrae. However, almost all caudals possess an autotomy
foramen at the base of each pleurapophyses.

Ribs
Atlas, axis, and the third vertebra possess no ribs, all other
presacral vertebrae bear ribs attached to the synapophyses
(Fig. 1A–C). A typical rib is holocephalous (Fig. 9). It has two
segments—a long proximal needle-like bony segment and a
small distal cartilaginous segment of triangular shape. All
ribs extend outward from the vertebrae and downward along
the flanks of the body. Ventrally, they come very close Fig. 18. Comparison of dorsal vertebra in (A) dorsal, (B) ventral, (C)
together but never meet. On the head of the rib, there is an lateral, (D) anterior, and (E) posterior aspects.
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS 17
diameter of the facet. On the anterior edge of the rib, there is
a tiny anteroventral pinching. The rib is anteroposteriorly
flattened and a strong ridge runs dorsally from the head to
the distal end of the rib. The ridge and the border of the ante-
roventral pinching meet distally and thus create a small pro-
longed area of triangular shape. As mentioned above, the ribs
are needle like but distally, they are slightly widened at the
very end. As it is impossible to distinguish cervical vertebrae
from thoracic vertebrae, it is also impossible to do so with the
ribs. However, the most anterior ribs are shorter and their
posterodorsal processes are more subtle than the processes in
more posterior ribs. Distally, the ribs regularly prolongate.
The last two pairs of presacral ribs are significantly shorter
than the preceding ribs (Fig. 1D).

Posthatchling Morphology of Vertebrae

Atlas. The atlas of juvenile specimen DE 54 is thinner
in lateral view when compared to that of the adult. The Fig. 19. Comparison of dorsal vertebrae of (A, D) Pseudopus apodus,
(B, E) Ophisaurus ventralis, and (C, F) Anguis fragilis. (A–C) ventral and
neural canal is large and, therefore, neural arches are lon-
(D–F) anterior aspects. The red dotted line indicates different courses of
ger relative to the ventral portion of the atlas. The laminae the subcentral ridges. Note that the ratio of the cotyle and neural canal
of the neural arch widen dorsally rather than narrow in height in Ophisaurus represents a different character state (blue color)
lateral view. They have a more or less dorsal course rather relative to that in Pseudopus and Anguis (red color).
than being anteriorly inclined. Transverse processes are
short and laterally oriented rather than posteriorly.
anteroposterior length of the hypapophysis is shorter
than the maximum length of the remaining portion of the
Axis. The axis of young Pseudopus apodus consists of
atlas.
four separated elements (Fig. 10A,B): vertebral body,
odontoid process or atlantal pleurocentrum and two inter-
centra. The morphology of the corpus resembles those of
Axis. 4. The neural canal reaches dorsally the level of
the following postaxis vertebrae.
the postzygapophysis. In Anguis and Ophisaurus, the dor-
sal portion of the neural canal reaches dorsally to the
Post-Axis Presacral Vertebrae. The vertebrae are deli- level of the postzygapophyses (for comparison see Figs. 13
cately built (Fig. 10C–G). The neural canal is large, having and 14).
almost the same height as the cotyle. The neural spine is 5. The odontoid process is inclined anterodorsally in an
low with a rounded (convex) dorsal margin. The subcentral angle of about 130 degree relative to the horizontal plane.
ridges are not as straight as they are in adults, but they In Anguis and Ophisaurus, the odontoid process is always
have a slightly concave appearance. The pre and postzyga- less inclined. The exception is the axis of O. koellikeri, in
pophyses are small, oriented more or less in anteroposter-
ior direction rather than being distinctly laterally
expanded. Moreover, they are less dorsally inclined rela-
tive to those in adults.

Diagnostic Characters
Our study shows morphological differences of the verte-
brae of Pseudopus relative to those of Anguis and Ophi-
saurus. The Recent P. apodus is distinguished from the
extant species of Ophisaurus and Anguis by the following
diagnostic characters:

Atlas. 1. Anterior margin of the hypapophysis reaches

anteriorly to the level of the anterior margin of the neural
arch. In Anguis and Ophisaurus, the anterior margin of
the hypapophysis lies posteriorly to the anterior level of
the neural arch (for comparison see Figs. 11 and 12).
2. In lateral view, the laminae of the neural arch are
distinctly narrowed anterodorsally and have a pointed
termination. In Anguis, the laminae are relatively antero-
posteriorly wider and their termination is oblique. In
Ophisaurus, the dorsal portions of laminae are distinctly
anteroposteriorly wide.
3. The anteroposterior length of the hypapophysis is Fig. 20. Comparison of the first sacral vertebra in (A) dorsal, (B)
bigger than the maximum length of the remaining portion ventral, (C) lateral, (D) anterior, and (E) posterior aspects (continued in
of the atlas. In Anguis and Ophisaurus, the the following figure).
18
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Fig. 21. Comparison of the first sacral vertebra in (A) dorsal, (B)
ventral, (C) lateral, (D) anterior, and (E) posterior aspects.
which the dorsal inclination of the odontoid process is still
bigger than that of P. apodus.
6. In posterior view, the dorsal margin of the condyle is
more or less concave. In Anguis and Ophisaurus, the dor-
sal margin of the condyle is convex.
Fourth presacral vertebra. 7. In anterior view, the lateral
margins of the prezygapophyses reach dorsally to the level of
the roof of the neural canal. In Anguis and Ophisaurus, the
Fig. 22. Comparison of the second sacral vertebra in (A) dorsal, (B)
ventral, (C) lateral, (D) anterior, and (E) posterior aspects (continued in
the following figure).

NANSKÝ ET AL.
prezygapophyses reach ventrally to the level of the roof of the
neural canal (for comparison see Figs. 15 and 16).
8. In the median plane, the height of the cotyle is
markedly bigger than the height of the neural canal. In
Anguis and Ophisaurus, the height of the cotyle is smal-
ler than the height of the neural canal.
9. The triangular hypapophysis, in lateral view, is
anteroposteriorly longer than high. In Anguis and Ophi-
saurus, the hypapophysis is distinctly elongated; the
exception is O. gracilis in which the hypapophysis is only
weakly developed.
Remaining presacral vertebrae. 10. The neural spine is
of square shape. It is only slightly inclined posteriorly. In
Anguis and Ophisaurus, the neural spine is trapezoidal
and the length of its basal portion is bigger than the height
of the neural spine (for comparison see Figs. 17 and 18).
11. The lateral margins of the centrum (subcentral
ridges) are straight (see Fig. 19A) rather than concave
(Ophisaurus) or parallel with their anterior-most sections
being expanded laterally (Anguis).
12. The height of the neural canal is distinctly smaller
than the height of the cotyle (Fig. 19D). The same condi-
tion is similar to that of O. harti, however, the overall
morphology of the vertebra of this species is different to
that of P. apodus.
13. In ventral view, the centrum is wide, its mid-width
forms 62% of the maximum anteroposterior length of the
centrum. In Anguis, the centrum is narrow with its mid-
width forming only 40% of the maximum anteroposterior
length of the centrum. In Ophisaurus, the centrum is mod-
erately wide, its mid-width relative to the maximum ante-
roposterior length ranges from 42% (in O. compressus) to
51% (in O. ventralis). One exception is only O. harti, where
the ratio is 59%.
Fig. 23. Comparison of the second sacral vertebra in (A) dorsal, (B)
ventral, (C) lateral, (D) anterior, and (E) posterior aspects.
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS
Sacral vertebrae. 14. In anterior view, the pleurapo-
physes gradually narrow distally having a straight course
along their entire length. In Ophisaurus, the distal ends
of the pleurapophyses are more or less flexed ventrally.
In Anguis, the distal ends of the pleurapophyses are
widely bifurcated (for comparison see Figs. 20–23).
15. In dorsal view, there is no bifurcation of the pleura-
pophysis into the anterior and posterior branches and its
distal margin is only shallowly embayed. In Anguis and
Ophisaurus, the bifurcation of the pleurapophysis is pre-
sent. In O. ventralis, the space between the anterior and
posterior branches is filled by a thin bony lamella.
16. Small neural canal; in anterior view, its height
forms only 16% of the entire height of the vertebra (mea-
sured from the ventral margin of the cotyle to the dorsal
end of the neural spine). In Anguis, the height of the neu-
ral canal forms 26% and in Ophisaurus, the ratio ranges
from 21% (only in O. harti) to 27%.
17. The cotyle is rounded in shape and not markedly
depressed. In Anguis and Ophisaurus, the depressed
cotyle is present.
18. In lateral view, the neural spine gradually narrows
dorsally. In Anguis and Ophisaurus, a more-or-less dis-
tinct constriction is present in about the mid-length of the
neural spine.
First caudal vertebra. 19. In dorsal view, the medial
margin of the prezygapophysis lies at the level medially to
the lateral margin of the mid-length portion of the neural
arch. In Anguis and Ophisaurus, the medial margin of the
prezygapophysis lies at the level of the lateral margin of the
Fig. 24. Comparison of the first caudal vertebra in (A) dorsal, (B)
ventral, (C) lateral, (D) anterior, and (E) posterior aspects (continued in
the following figure).
19
mid-length portion of the neural arch. The exception is the
vertebra of O. koellikeri, in which the conditions are similar
to those of Pseudopus (for comparison see Figs. 24 and 25).
20. The cotyle is rounded in shape and not markedly
depressed. In Anguis and Ophisaurus, the cotyle is
depressed.
21. In lateral view, the neural spine gradually narrows
dorsally. In Anguis and Ophisaurus, a more-or-less dis-
tinct constriction is present in about the mid-length of the
neural spine.
22. The vertebra is short; the posteromedial margin of the
pleurapophysis partly overlap the anterior margin of the
postzygapophysis in ventral view. In Anguis and Ophisaurus,
the vertebra is more-or-less elongate; the pleurapophyses do
not reach the articulation facets of postzygapophyses and
there is a more-or-less gap between these structures.
The rest of caudal vertebrae. 23. The autotomic split in
caudal vertebrae is absent, only autotomic foramina are
developed. In Anguis and Ophisaurus, the autotomic split
is present, well visible (see Hoffstetter and Gasc, 1969).
Ophisaurus. The recent species of Ophisaurus are dis-
tinguished from the extant species of Pseudopus apodus
and Anguis fragilis by the following diagnostic characters
(for comparison see Figs. 11–25):
1. In the lateral aspect, the anteroposterior length of the
dorsal portion of the lamina of the atlas neural arch is
Fig. 25. Comparison of the first caudal vertebra in (A) dorsal, (B)
ventral, (C) lateral, (D) anterior, and (E) posterior aspects.
20 
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NANSKÝ ET AL.
bigger than the anteroposterior length of its ventral
portion. In Pseudopus and Anguis, the anteroposterior
length of the ventral portion of the lamina of the atlas
neural arch is always bigger than the length of its dor-
sal portion.
2. The maximum height of the intercentrum of the atlas
is smaller than the half the height of the remaining
portion of the atlas. In Pseudopus and Anguis, the
height of the intercentrum is bigger than the half of
the remaining portion of the atlas.
3. The condyle of the axis is depressed and of elliptical
shape in posterior aspect. It is kidney shaped in Pseu-
dopus and rounded in Anguis.
4. The lateral margins (subcentral ridges) of the dorsal
vertebrae are concave (Fig. 19B).
Fig. 26. Landmarks of vertebra used for morphometric analyses.
5. The height of the neural canal is slightly bigger than
the height of the cotyle (Fig. 19E).
6. The anterior branch of the pleurapophysis is more
robustly developed than the posterior branch. In Pseu-
dopus, there in only very indistinctly developed ante-
rior branch; the posterior branch is well developed. In
Anguis, the posterior branch is more robustly devel-
oped than the anterior branch.
Anguis. The recent species A. fragilis is distinguished
from the extant species of Ophisaurus and Pseudopus apo-
dus by the following diagnostic characters (for comparison
see Figs. 11–25):
1. In the axis, the second intercentrum is distinctly
shorter and thinner than the third intercentrum. In
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS
Pseudopus and Ophisaurus, the second intercentrum
is equally or almost as large as the third
intercentrum.
2. The condyle of the axis is rounded in shape, whereas it
is kidney shaped in Pseudopus and depressed in
Ophisaurus.
3. In dorsal view, the posterior section of the third
intercentrum is well visible and its length equals one
third of the entire length of the neural spine.
21
4. Except of a short anterior section, the entire dorsal
margin of the neural spine of the axis is straight and
horizontally oriented in lateral aspect. In Pseudopus
and Ophisaurus, the dorsal margin is
anteroventrally–posterodorsally inclined.
5. The lateral margins of the centrum of dorsal vertebrae
are almost parallel and their anterior-most sections
are expanded laterally (Fig. 19C). There is a slight
constriction immediately posterior to the subcentral

Fig. 27. Cluster analysis of all data illustrating similarity of vertebrae in all species (A) and of (B) the second vertebrae (CV2, axis); (C) the fourth
vertebrae (CV4); (D) the middle trunk vertebrae (TV); (E) the first sacral vertebrae; (F) the second sacral vertebrae (SV2); (G) the first caudal vertebrae
(KV1) illustrating similarity of vertebrae in all species. Abbreviations: CV, cervical vertebra; TV, trunk vertebra; KV, caudal vertebra; SV, sacral
vertebra; AF, Anguis fragilis; AG, Abronia graminea; OA, Ophisaurus attenuatus; OC, O. compressus; OG, O. gracilis; OH, O. harti; OK, O. koellikeri;
OL, O. ludovivi; OM, O. mimicus; OS, O. sololovi; OV, O. ventralis; PA, Pseudopus apodus.
22 
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NANSKÝ ET AL.

foramina (Klembara, 1981: fig 3). As for the condi-
tions in Pseudopus and Ophisaurus, see Figure 19.
6. The haemal arches of the first sacral vertebra are
long and ventrally fused one to another. In O. harti
and Ophisaurus mimicus, only the vestiges of the
proximal portions of the haemal arches are present.
7. The pleurapophyses of the first sacral vertebra are
laterally and only slightly ventrally directed. In
Pseudopus and Ophisaurus, the pleurapophyses are
distinctly ventrolaterally directed.
8. The bifurcation of the pleurapophyses of the first
sacral vertebra is visible in anterior and posterior
views, by which the posterior branch is more ven-
trally located than the anterior one. In Pseudopus
and Ophisaurus, both branches more or less overlap
one another in anterior and posterior views.

Fig. 28. Principal component analysis (PC1/PC2) of (A) the second vertebrae (CV2, axis) of all species, (B) fourth vertebrae (CV4) of all species,
(C) the middle trunk vertebrae (TV), (D) the first sacral vertebrae (SV1), (E) the second sacral vertebrae (SV2), (F) the first caudal vertebrae (KV1) of all
species. Abbreviations: CV, cervical vertebra; TV, thoracal vertebra; KV, caudal vertebra; SV, sacral vertebra; AF, Anguis fragilis; AG, Abronia
graminea; OA, Ophisaurus attenuatus; OC, Ophisaurus compressus; OG, Ophisaurus gracilis; OH, Ophisaurus harti; OK, Ophisaurus koellikeri; OL,
Ophisaurus ludovivi; OM, Ophisaurus mimicus; OS, Ophisaurus sololovi; OV, Ophisaurus ventralis; PA, Pseudopus apodus.
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS 23
9. In lateral view, the haemal arch of the first caudal
vertebra is markedly posteriorly directed, in an angle
of 40 degree (from the horizontal plane). In Pseudo-
pus and Ophisaurus, the angle is always bigger—
the haemal arch is more ventrally directed.
10. In anterior and posterior views, the dorsoventral
length of the mutual contact of the rami of the hae-
mal arch of the first caudal vertebra is short, always
shorter than that of Pseudopus and Ophisaurus.
11. The neural spine of the first caudal vertebra is short;
its height equals that of the neural canal in anterior
and posterior views. In Pseudopus and Ophisaurus,
the height of the neural spine is always bigger.

Geometric Morphometric Analyses

Cluster analyses. The cluster analysis of all vertebrae
(for landmarks see Fig. 26) shows a general separation in
neck vertebrae on the one side and in postcervical verte-
brae on the other side (Fig. 27). With few exceptions, a sep-
arate clustering of CV2 and CV4 exists, and most sacral
and caudal vertebrae cluster together. Within the postcer-
vical cluster of vertebrae, the trunk vertebrae are broadly
distributed in the similarity diagram. The most distin-
guished vertebrae are the caudal vertebra of P. apodus
and the second vertebra of Ophisaurus mimicus.
The clustering of all CV2s shows O. mimicus to be most
distinct from all other species of our sampling (Fig. 27B).
Abronia graminea and A. fragilis cluster together. All
other species form a diverse clustering with P. apodus Fig. 29. The atlas-axis complex of gerrhonotine lizard body form
inside. anguid (A–G) Abronia graminea (DE 67) and (H-N) Barisia rudicollis
The clustering of all CV4s shows O. ventralis to be (DE 69) in (A) lateral, (B) dorsal, (C) ventral, (D) anterior, and (E) posterior
most disctinct from all other species (Fig. 27C). The aspects. Axis in (F) lateral and (G) anterior aspects.
clustering of the Ab. graminea and An. fragilis resem-
bles the phylogenetic arrangement of those species
compared to the Ophisaurus/Pseudopus-group (Pyron
PC1/2 of CV4 shows Abronia graminea separated from
et al., 2013; Zheng and Wiens, 2016). In the latter,
all other species (Fig. 28B). Anguis fragilis and all other
P. apodus is clustering separately from Ophisaurus
species cluster together except for Ophisaurus ventralis,
species.
which, apparently, shows a very distinct anatomical
The clustering of all TVs shows the best representation
shape of CV4.
of molecular phylogenies (Pyron et al., 2013; Zheng and
Wiens, 2016) with Ab. graminea opposing all Anguinae.
For Anguinae, An. fragilis opposes all other anguines
(Fig. 27D). P. apodus clusters inside the Ophisaurus/
Pseudopus-group and three of the four North-American
species cluster together.
The clustering of all SV1s and all SV2s shows Ab. gra-
minea opposing all Anguinae and P. apodus deep inside
the cluster of the remaining species (Fig. 27E,F).
The clustering of all KVs shows P. apodus to be most
distinct from all other species in our sampling (Fig. 27G).
All other species form a diverse clustering with Ophi-
saurus and Abronia and Anguis cluster together inside a
larger cluster.

Principal component analyses. The PCA of all data pro-

vide a great overlap of species (now shown). The PCA of
CV2 (PC1/2) shows Abronia graminea and Anguis fragilis
distinct from all other species, possibly resembling a close
phylogenetic position of both species (Fig. 28A). All other Fig. 30. The atlas–axis complex of diploglossine anguid Celestus
species cluster together with the exception of Ophisaurus enneagrammus FMNH 108860 in (A) lateral, (B) dorsal, (C) ventral, (D)
mimicus, which apparently has a very distinct anatomy anterior, and (E) posterior aspects. Axis in (F) lateral and (G) anterior
of the axis. aspects.
24 
CER 
NANSKÝ ET AL.
PC1/2 of TV again shows Abronia graminea and Anguis
fragilis separated from all other species (Fig. 28C). Pseu-
dopus apodus is most similar to the three separate clus-
terings of the Ophisaurus-species as well as to the
outgroup representatives indicated by its central position
in the “web” of the minimal span tree.
PC1/2 of SV1 shows Abronia graminea separated from
all other species (Fig. 28D). Anguis fragilis and Pseudo-
pus apodus cluster together with all remaining species.
PC1/2 of SV2 shows Ab. graminea and An. fragilis sepa-
rated from all other species and P. apodus cluster
together with all remaining species, which, however,
show a broad disparity (Fig. 28E).
PC1/2 of KV1 shows a broad clustering of all species
except for Pseudopus apodus, which, apparently, has a
very distinct anatomy of the first caudal vertebra
(Fig. 28F).
PC1/2 of all vertebrae always show more than 50%
shape variance. Other PC-axes do not show any obvious
ecological or phylogenetic pattern.
DISCUSSION AND COMPARISON
The elongated, serpentiform body and leg reduction
have evolved convergently in numerous reptilian and
amphibian lineages for adaption to different environ-
ments, and thus such a transformation represents an
important biological phenomenon. As was previously
 nanský (2016), the transition from lizard
observed by Cer
body form to serpentiform morphology shows some evolu-
tionary patterns in the atlas–axis complex as well.
Although zygapophyseal articulation between atlas and
axis is well developed in limbed gerrhonotine anguids, for
example, Abronia (Fig. 29A–G), Mesaspis, and Barisia
(Fig. 29H–N), it is absent in the limbless Anguinae
representatives—Pseudopus, Anguis, and Ophisaurus. In
the diploglossine anguid Celestus, which shows some
degree of body elongation and limb reduction, vestiges of
zygapophyses are present, but without articular surfaces
(Fig. 30). Thus, our study brings further evidence of
 nanský (2016) about the loss of this
hypothesis of Cer
articulation in forms with reduced or absent limbs. In ser-
pentiform lizard Anniella pulchra, the connection through
zygapophyseal articulation is completely absent (although
it should be noted that Anniella is specialized, showing
the reduction of postzygapophyses of the axis as well; see
Rieppel, 1980: Fig. 26f ). In contrast, well developed zyga-
pophyseal articulation between atlas and axis is present
in for example, Shinisaurus crocodilurus, an anguimorph
which represents a lizard body form (see Conrad,
2006: Fig. 2).
The first intercentrum in Anguinae representatives is
oriented ventrally or more often inclined posteriorly. Only
in O. sokolovi is the first intercentrum slightly inclined
anteriorly. However, in Abronia, the robust atlantal inter-
centrum is markedly inclined anteriorly, reaching futher
anteriorly than all other atlas portions. The atlas–axis
complex of other lizard clades was previously studied in
 nanský et al. (2014: Chamaeleonidae) and
detail by Cer
 nanský (2016: Scincoidea).
Cer
Heterochrony in the Evolution of Vertebrae of
Pseudopus apodus
Heterochrony in the evolution of Pseudopus apodus
was previously confirmed for the lower jaw and skull
characters (Klembara et al., 2014, 2017a). It was demon-
strated that several cranial features present in the juve-
niles of P. apodus are present (1) in the adults of
phylogenetically more basal species of Pseudopus like late
Miocene and Pliocene species P. pannonicus (Fejérváry-
Lángh, 1923; Tempfer, 2004) and early Miocene species
P. laurillardi (Klembara et al., 2010) and Pseudopus
ahnikoviensis (Klembara, 2012; Klembara et al., 2014,
2017b); (2) in the adults of the other species of the sub-
family Anguinae (species of Ophisaurus and Anguis); and
(3) in the adults of the earliest potential anguines like
Ophisauriscus quadrupes from the middle Eocene of
Germany (Sullivan et al., 1999; Klembara et al., 2017b;
Klembara and Rummel, 2018), Early Cretaceous Odaxo-
saurus piger (Meszoely, 1970; Klembara et al., 2017b) and
the adults of basal outgroup taxa (Klembara et al., 2017a,
2017b). It was also shown, that several lower jaw and
skull bones of the adults of the most basal species of Pseu-
dopus (early Miocene P. ahnikoviensis and P. laurillardi)
exhibit the morphology of the adults of Recent and fossil
Ophisaurus and Anguis (Klembara, 2012). From this
results that the ancestral adult morphology is that exhib-
ited by the adults of the most basal members of Pseudo-
pus and the adults of Ophisaurus and Anguis. In this
context, it was demonstrated that the peramorphosis (the
occurrence of the ancestral adult morphology in a descen-
dant juvenile stage of development; McNamara, 1986) is
responsible for the morphology of certain cranial features
present in adults of P. apodus (Klembara et al., 2014,
2017a).
We present here two cases in which the morphology of
the juvenile vertebrae of Pseudopus apodus exhibit sev-
eral features very similar to those in the adults of Ophi-
saurus. These features are as follows:
1. In juveniles of Pseudopus apodus, the cotyle of the
dorsal vertebra is large, but its height is almost the
same as the height of the neural canal. This condition
is similar to that of adults of Recent Ophisaurus
(cf. Figs. 10F and 19), adults of the middle Miocene
Ophisaurus sp. (Cer nanský and Klembara, 2017),
adults of the late Oligocene Anguinae indet. (Augé,
2005), adults of the middle Eocene Ophisauriscus
quadrupes (Sullivan et al., 1999) and also adults of
the basal outgroup taxa like the anguimorph Xeno-
saurus grandis (Hecht and Costelli, 1969) and scincid
Eumeces schneideri.
2. In early juvenile specimens of Pseudopus apodus, the
subcentral ridges (lateral margins of the centrum) of
dorsal vertebrae are not as straight as in adults, but
they are slightly concave. Such morphology of the
dorsal vertebrae of juveniles of P. apodus resembles
that of the adults of recent Ophisaurus (cf. Figs. 10D
and 19), as well as many other finds within the Ophi-
saurus clade like Ophisaurus sp. from the late Eocene
of England (Meszoely and Ford, 1976; cf. Anguine
Morphotype B, Klembara and Green, 2010), Ophi-
saurus sp. from the middle Miocene of Slovakia
 VERTEBRAL COLUMN AND RIBS OF PSEUDOPUS APODUS
 nanský and Klembara, 2017) and Asia (Vasilyan
(Cer
et al., 2016), O. canadensis from the late Miocene of
Canada (Holman, 1970) and Ophisaurus (Dopasia)
sp. from the Pliocene of Italy (Delfino et al., 2011).
This feature is very important for the evaluation of
the fossil material in which the dorsal vertebrae of the
juvenile Pseudopus may be interpreted as represent-
ing those of the adult Ophisaurus or vice versa (see
also Klembara, 1981). The slightly concave lateral
margins of the centrum of the dorsal vertebrae exhibit
also the middle Eocene Ophisauriscus quadrupes
(Kuhn, 1940; Klembara, 1981; Sullivan et al., 1999)
and a scincid Eumeces schneideri.
Thus, the two above vertebral characters, together with
six cranial characters (Klembara et al., 2014, 2017a), sup-
port the hypothesis that a peramorphic heterochronic pro-
cess may have played role in the evolution of certain
skeletal features of Pseudopus apodus, very likely reflect-
ing an increasing body size of this taxon during its
evolution.
Geometric Morphometric Analyses
The geometric morphometric analyses revealed a gen-
eral separation of the limbed species Abronia graminea
from the remaining sampling. This could indicate that
the vertebral column largely differentiated in limbless
forms compared to limbed anguids. This is particularly
true for SV1 and SV2.
It is worth mentioning that Pseudopus apodus almost
always clusters within Ophisaurus-species, which agrees
with the phylogenetic findings of molecular studies (Pyron
et al., 2013; Zheng and Wiens, 2016), which recovered Pseu-
dopus always within that clade. The performed Procrustes
analysis reduced size parameters and made all species,
including P. apodus, comparable for the geometric morpho-
metric analysis. The analyses revealed that the vertebrae of
P. apodus do not drastically derivate in their anatomical
shape (PC-scores) when compared to all other species. Only
the first caudal vertebra shows distinctly different shape
parameters in P. apodus, which could be related to a special-
ized locomotion related to the large body size of this species.
For the axis, we found a largely distinct pattern for the
small species Ophisaurus mimicus. This anatomy could
indicate a special ecological adaptation, maybe in regard
to fossoriality, feeding, and/or combat behavior, in which
head/neck mobility is of particular importance. We can
most likely exclude miniaturization as reason for this pat-
tern as also the geometric morphometry of other verte-
brae of this species would be expected to modify based on
miniaturization processes. In O. ventralis, we found a
derived pattern of neck vertebral anatomy, that is, CV4,
which could be interpreted in a similar manner.
ACKNOWLEDGMENTS
We are indebted to Prof. W. Böhme (Zoologisches For-
schungsmuseum Alexander Koenig, Bonn, Germany) for
the borrowing of specimens of Ophisaurus for the μCT
scannings. We thank M. Augé (Museum national d’His-
toire naturelle Paris), A. Bolet (University of Bristol), and
one anonymous reviewer for their critical reading of the
25
manuscript. For CT data of Celestus enneagrammus, we
thank J. Maisano.
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