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Anatomia, Histologia, Embryologia

ORIGINAL ARTICLE

Congenital Malformations of the Vertebral Column in


Ancient Amphibians
F. Witzmann1*, B. M. Rothschild2, O. Hampe1, G. Sobral1, Y. M. Gubin3 and P. Asbach4
r Naturkunde, Leibniz-Institut fu
r Evolutions- und Biodiversitatsforschung, Invalidenstrae 43, Berlin D-10115,
Addresses of authors: 1 Museum fu
Germany;
2
Biodiversity Center, University of Kansas, Lawrence, KS 66045, USA;
3
Paleontological Institute, Russian Academy of Sciences, ul. Profsoyuznaya 123, Moscow 117868, Russia;
4
Department of Radiology, Charit
e Universit
atsmedizin Berlin, Chariteplatz 1, Berlin 10117, Germany

*Correspondence:
Tel.: +49 30 2093 8820;
fax: +49 30 2093 8565;
e-mail: florian.witzmann@mfn-berlin.de
With 8 figures
Received November 2012; accepted for
publication February 2013
doi: 10.1111/ahe.12050
r
This work was carried out at the Museum fu
r Evolutions- und
Naturkunde, Leibniz-Institut fu
Biodiversit
atsforschung, Invalidenstrae 43,
D-10115 Berlin, Germany.

Summary
Temnospondyls, the largest group of Palaeozoic and Mesozoic amphibians,
primitively possess rhachitomous vertebrae with multipartite centra (consisting
of one horse-shoe-shaped inter- and paired pleurocentra). In a group of
temnospondyls, the stereospondyls, the intercentra became pronounced and
disc-like, whereas the pleurocentra were reduced. We report the presence of
congenital vertebral malformations (hemi, wedge and block vertebrae) in
Permian and Triassic temnospondyls, showing that defects of formation and
segmentation in the tetrapod vertebral column represent a fundamental failure
of somitogenesis that can be followed throughout tetrapod evolution. This is
irrespective of the type of affected vertebra, that is, rhachitomous or stereospondylous, and all components of the vertebra can be involved (intercentrum,
pleurocentrum and neural arch), either together or independently on their
own. This is the oldest known occurrence of wedge vertebra and congenital
block vertebra described in fossil tetrapods. The frequency of vertebral congenital malformations in amphibians appears unchanged from the Holocene.

Introduction
Temnospondyl amphibians and their vertebrae
Temnospondyl amphibians are the by far largest and
most diverse group of basal tetrapods, ranging from the
Early Carboniferous to the Early Cretaceous (Schoch,
2009). The group probably contains the ancestors of
some (Anderson et al., 2008) or all (Ruta and Coates,
2007; Sigurdsen and Green, 2011) extant lissamphibians,
although an alternative hypothesis exists (Marjanovic and
Laurin, 2008). Temnospondyls were adapted to a large
spectrum of habitats and are represented by aquatic,
terrestrial and semi-terrestrial forms, spanning a wide size
range from small, newt- or salamander-like forms like
dissorophoids to the several-metre-long, crocodile-like
stereospondylomorphs (Schoch, 2009; Witzmann et al.,
2010). The vertebral morphology and ontogeny of
temnospondyls differ from those of all extant vertebrates.
2013 Blackwell Verlag GmbH
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Temnospondyl vertebrae are plesiomorphically rhachitomous, that is, they are composed of the neural arch
(including the processus spinosus) and a multipartite
vertebral body, which consists of a large, unpaired intercentrum (or hypocentrum) and of paired, smaller pleurocentra (Moulton, 1974; Panchen, 1977; Shishkin, 1989;
Warren and Snell, 1991) (Fig. 1a). The intercentrum is
wedge-shaped in lateral and crescent in sagittal view,
embracing the persistent notochord from ventral and
lateral. The parapophysis for articulation with the capitulum of the ribs is located on the posterodorsal margin of
the intercentrum. Posterodorsal to the intercentrum and
posterior to the transverse processes of the neural arch
are the diamond-shaped pleurocentra, embracing the
notochord dorsolaterally. In the rhachitomous vertebra,
the neural arch, intercentrum and pleurocentra are normally separated by cartilage rather than being co-ossified.
In some stereospondyls (mainly Mesozoic temnospond-

Malformations in Ancient Amphibians

(a)

(b)

F. Witzmann et al.

(c)

(d)

(e)

(f)

(g)

yls), the intercentrum is often strongly ossified and has


attained a disc-like or spool-shaped morphology, greatly
reducing the space for the notochord (Warren and Snell,
1991). In contrast, the pleurocentra are often smaller
than in the rhachitomous vertebra or are even non-ossified or reduced (Fig. 1b). This vertebral morphology
is generally designated as stereospondylous and can
be found in large-growing stereospondyls, such as Mastodonsaurus (Schoch, 1999) and Cyclotosaurus hemprichi
(Kuhn, 1942), and in metoposaurids (Warren and Snell,
1991; Sulej, 2007). Typical for metoposaurid intercentra
of anterior trunk vertebrae is their opisthocoelous morphology, that is, the intercentrum is anteriorly convex and
posteriorly concave, thus forming a kind of ball-andsocket joint. This may represent the origin of synovial
intercentral joints. Among stereospondyls, the Triassic

Fig. 1. (a)(c) Schematic drawings of rhachitomous, stereospondylous and plagiosaurid


vertebrae. (a) Rhachitomous condition
(redrawn from Shishkin, 1989). (b) Stereospondyl condition (redrawn from Warren and
Snell, 1991). (c) Plagiosaurid condition, note
the intervertebral position of neural arches
and parapophyses (redrawn from Shishkin,
1989). (d)(g) Skeletal reconstructions of
some of the temnospondyl amphibians investigated in this study. (d) The Early Permian
Sclerocephalus haeuseri (total body length
approximately 1.5 m; redrawn after Schoch
and Witzmann, 2009a). (e) The Late Permian
Platyoposaurus stuckenbergi (total body
length approximately 1.5 m; drawing based
on a mounted skeleton at the Paleontological
Institute and Museum of the Russian Academy of Sciences, Moscow, Russia). (f) A Triassic metoposaurid (Metoposaurus diagnosticus
krasiejowensis, total body length approximately 2 m, redrawn after Sulej, 2007). (g)
The Middle Triassic Gerrothorax pulcherrimus
(total body length approximately 1 m;
redrawn after Schoch, 2009). Drawings are
not to scale. Abbreviations: c, centrum; dia,
diapophysis; ic, intercentrum; na, neural arch;
par, parapophysis; pc, pleurocentrum.

plagiosaurids have spool-shaped vertebral centra with


intervertebral neural arches (Shishkin, 1987, 1989; Warren
and Snell, 1991). Each parapophysis of plagiosaurid presacral vertebrae is formed by two successive vertebral centra,
and thus, the ribs are intervertebral as are the neural arches
(Fig. 1c). It is still a matter of debate as to which central
elements form the plagiosaurid centrum. Panchen (1959)
suggested that the centra are entirely formed by the pleurocentra, whereas the intercentra are lost. Shishkin (1987,
1989) interpreted the plagiosaurid centrum as fusion of
the intercentrum with the pleurocentrum of the preceding
vertebra, whereas Warren and Snell (1991) regarded the
plagiosaurid centrum as an intercentrum and the pleurocentrum as reduced. Hellrung (2003) followed this view,
but regarded the pleurocentrum as fused with the neural
arch.
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F. Witzmann et al.

The ontogeny of temnospondyl vertebrae is well documented compared with vertebrae of other fossil tetrapods,
as large growth series from small larvae to large adults do
exist in several taxa (e.g. Boy, 1974; Schoch and Witzmann, 2009a,b). In general, vertebral ossification proceeded very slowly, starting with the initially paired
neural arches, followed much later in ontogeny by ossification of the intercentrum (first laterally paired) and then
of the laterally paired pleurocentra.
Congenital vertebral malformations
During somitogenesis, the paraxial mesoderm that is
located lateral to the neural tube is segmented early in
vertebrate embryogenesis and the bilaterally paired somites are formed. Somites contain sclerotomal cells that
migrate from contralateral somite pairs in a medial and
ventral direction and surround the notochord and neural
tube, thus forming the mesenchymal anlagen of the vertebrae (Erol et al., 2002; Kaplan et al., 2005). Disruption of
genes regulating embryonic somite formation (e.g. by
environmental insults during early embryogenesis like
oxygen deficiency, increased temperature and carbon
monoxide) can cause abnormal segmentation and disruption of fusion of the paired mesenchymal vertebral anlagen, leading to congenital malformations like butterfly,
block, wedge and hemivertebrae (Pourquie and Kusumi,
2001; Erol et al., 2002; Shawen et al., 2002; Kaplan et al.,
2005). An interaction between genes and environment
probably exists, that is, genetic defects cause the susceptibility of the embryo to disease-associated environmental
factors (Erol et al., 2002, 2004). A hemivertebra may
develop from complete failure of formation of one lateral
vertebral anlage. Subsequent chondrification and ossification take place only on one lateral side. A special case of
hemivertebra formation is the hemimetameric segmental
shift, which is a defect of fusion of the paired vertebral
anlagen (Shawen et al., 2002; Witzmann et al., 2008).
Incarcerated and non-incarcerated types can be distinguished among hemivertebrae (McMaster, 2001). The
non-incarcerated type acts like a wedge in the vertebral
column and leads to a lateral curvature (scoliosis) of the
column at the location of the hemivertebra. In the incarcerated type, which is less common in humans, the vertebrae anterior and posterior to the hemivertebra are
shaped to compensate for the hemivertebra, such that no
or only a slight curvature of the vertebral column occurs.
Hemivertebrae were extensively studied in humans
(e.g. McMaster and Ohtsuka, 1982; McMaster, 2001), but
is also recognized among dogs, cats, horses and other
domestic animals (Wong et al., 2005; Jeffery et al., 2007;
Moura et al., 2010) as well as in snakes (Baur, 1891) and
feline ectomorphs like Hoplophoneus (Rothschild et al., in
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Malformations in Ancient Amphibians

press). A wedge vertebra has a similar shape, but in contrast to a hemivertebra, it extends to the contralateral side
of the vertebral column. A failure of segmentation results
in a block vertebra, in which the disc spaces between two
or more vertebrae have become very narrow or fused
(McMaster, 2001).
Congenital vertebral pathologies are exceptional finds
in fossil amphibians and reptiles (Rothschild et al., 2012).
They were described in an Early Permian captorhinomorph reptile (Johnson, 1988), the Late Jurassic
dinosaur Dysalotosaurus lettowvorbecki (Janensch, 1934;
Witzmann et al., 2008), and briefly mentioned by
Lydekker (1889) in the Late Jurassic cryptocleidid plesiosaur Muraenosaurus leedsi (designated as Cimoliasaurus
plicatus by Lydekker). Among temnospondyl amphibians,
congenital vertebral pathology has so far only been
described in a Triassic capitosauroid that suffered from
scoliosis caused by a hemivertebra (Witzmann, 2007).
Pathologies of an extinct organism are important to
document because they might give insights into the animals physiology and behaviour (Rothschild and Martin,
2006). Congenital vertebral malformations in temnospondyls provide additional information concerning the
formation of the most primitive tetrapod vertebral
pattern that does not have an analogue today. In this
study, we describe different types of vertebral pathologies
in different temnospondyls, including incarcerated and
non-incarcerated hemivertebrae, wedge and block
vertebrae, and discuss their aetiology and development.

Materials and Methods


Sclerocephalus haeuseri (basal stereospondylomorph)
Specimen MB.Am.1260.1, 2 from the Niederkirchen Bank
(Meisenheim Formation: Jeckenbach Subformation) of
Heimkirchen, Early Permian, Saar-Nahe Basin (Germany),
consists of plate and counterplate. It is an almost complete
postcranial skeleton of a larva. The trunk measures
approximately 70 mm in length. Sclerocephalus haeuseri
was a crocodile-like, semi-aquatic predator in the ancient
lakes of the Saar-Nahe Basin and reached a total body
length of more than 1.5 m (Fig. 1d) (Schoch and
Witzmann, 2009a).
Cheliderpeton lellbachae (basal stereospondylomorph)
Specimen SMNS 91279 is the cast of a complete skeleton,
showing two succeeding trunk vertebrae whose neural
spines are fused. The specimen is derived from the
Kappeln Bank (Meisenheim Formation: Odernheim Subformation) of Klauswald/Odernheim, Early Permian,
Saar-Nahe Basin (Germany). The taxon Cheliderpeton

Malformations in Ancient Amphibians

lellbachae was erected by Kratschmer (2006), but needs


taxonomic revision as it does not share the autapomorphies of Cheliderpeton (Schoch and Witzmann, 2009b).
Cheliderpeton lellbachae had a similar mode of life as
Sclerocephalus haeuseri and reached a total body length of
11.5 m.
Platyoposaurus stuckenbergi (Archegosauridae, basal
stereospondylomorph)
Specimen PIN 164/71 is a single rhachitomous vertebra
consisting of neural arch, inter- and paired pleurocentra.
The intercentrum is posteriorly fused with the intercentrum
of the succeeding vertebra, and the intercentrum of a hemivertebra is intercalated between the two on the right side.
The specimen is derived from the Late Permian (Urzum
stage, formerly Kazanian stage) of Belebey, Republic of
Bashkortostan (Bashkiria). Platyoposaurus was an upto-1.5-m-long, aquatic piscivorous predator whose snout
was extremely elongate and slender (Fig. 1e) (Gubin, 1991).
Metoposauridae indet. (Trematosauria, Stereospondyli)
Specimen MB.Am.1449 (formerly IPFUB Am.36) consists
of two fused stereospondylous intercentra with intercalated
hemivertebra on the left side. The neural arches and the
pleurocentra were not co-ossified with the intercentra and
are not preserved. It was found together with other remains
of stereospondyls (vertebrae, fragments of pectoral girdle
and skull of metoposaurids and mastodonsauroids) in the
Gres de Silves Formation (Triassic/Jurassic boundary) of
the Algarve Basin, south-western Portugal (Witzmann and
Gassner, 2008). Metoposaurids were up-to-3-m-long aquatic predators that superficially resembled broad-skulled
crocodiles or Giant Salamanders (Fig. 1f) (Sulej, 2007).
Gerrothorax pulcherrimus (Plagiosauridae,
Stereospondyli)
SMNS 83498 is represented by two specimens: specimen A
consists of two fused vertebral centra with a centrum of a
wedge vertebra and two neural arches preserved; specimen
B consists of two fused vertebral centra with the neural
arches missing. The specimens are derived from the lower
Keuper, Kupferzell, south-west Germany. Gerrothorax was
a gill-breathing, flattened lurking predator that lived on
the bottom of different types of water bodies (Fig. 1g)
(Hellrung, 2003; Schoch and Witzmann, 2012).
Micro-CT
The vertebrae of Gerrothorax were scanned in the
Museum f
ur Naturkunde Berlin using a Phoenix|X-ray

F. Witzmann et al.

Nanotom (GE Sensing and Inspection Technologies


GmbH, Wunstorf, Germany), which was especially
designed for small samples and allows for higher
resolution in the visualization of small structures. All
1440 slices were reconstructed with the software datos|
x-reconstruction 1.5.0.22 (GE Sensing and Inspection
Technologies GmbH, Phoenix|X-ray), and the threedimensional data were analysed in VG Studio Max 2.1
(Volume Graphics, Heidelberg, Germany). The scans were
made with a tungsten target and a 0.1-mm-thick Cu filter
in modus 0. The particular setting for Gerrothorax SMNS
83498 specimen A was 75kV, 350 lA, average 6, skip 3,
exposure time of 250 ms and voxel size of 31.24 lm; for
specimen B, the setting was 120 kV, 65 lA, average 3,
skip2, exposure time of 250 ms and voxel size of
26.87 lm. Micro-CT scanning of the metoposaurid specimen MB.Am.1449 yielded no results. The scanning of the
Platyoposaurus vertebrae PIN 164/71 could not be realized. The Cheliderpeton lellbachae specimen SMNS 91279
is a cast of a lost original, and macroscopic investigation
of the larval Sclerocephalus MB.f.1260 was sufficient
because its very delicate, thin bones are all compressed
two-dimensionally in a single layer.
Abbreviations (institutional)
MB, Museum f
ur Naturkunde, Berlin, Germany; IPFUB,
Institut f
ur Palaontologie, Freie Universitat Berlin, Germany; PIN, Paleontological Institute and Museum of the
Russian Academy of Sciences, Moscow, Russia; SMNS
Staatliches Museum f
ur Naturkunde Stuttgart, Germany.

Results
Hemivertebra in a larval rhachitomous vertebral column
(Sclerocephalus)
The vertebral column of the larval specimen of Sclerocephalus (MB.Am.1260.1, 2) is incompletely ossified, as
common in temnospondyl larvae (Fig. 2a,b). The central
elements, that is, inter- and pleurocentra, were completely
cartilaginous in that growth stage and were thus not preserved. Only the neural arches are ossified, but are poorly
differentiated with short zygapophyses and low neural
spines. The neural arches are not fused in the midline
(as in adult specimens), so each neural arch is represented by its paired, contralateral halves. However, the
fourth preserved neural arch of the left side has two
counterparts on the right side. Both of these right neural
arches are anteroposteriorly shortened (they attain
approximately 80% of the length of the left neural arch)
but have approximately the same height. Ribs are poorly
preserved in this specimen, but it appears that both of
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F. Witzmann et al.

Malformations in Ancient Amphibians

(a)

Fig. 2. Hemivertebra in a larval rhachitomous


vertebral column, exemplified by a larval specimen of Sclerocephalus haeuseri
(MB.Am.1260.1, 2) from Heimkirchen, Early
Permian, Saar-Nahe Basin (Germany). (a)
Complete specimen MB.Am.1260.1 in dorsal
view. (b) Close-up of vertebral column with
hemivertebra. Abbreviations: clei, cleithrum;
fe, femur; fi, fibula; ha, haemal arch; hu,
humerus; il, ilium; man, manus; na, neural
arch; ra, radius; ri, rib; sna, smaller neural
arches; sri, sacral rib; ti, tibia; ul, ulna.

(b)

the smaller neural arches are associated with ribs. The rib
of the left counterpart is not preserved. This asymmetry
can best be explained by the failure of formation of one
left lateral vertebral anlage (i.e. left halves of neural arch,
inter- and pleurocentrum did not develop), resulting in
formation of a hemivertebra on the right side. The fact
that the two right neural arches are anteroposteriorly
shortened compensates partially for the presence of a
hemivertebra so that the vertebral column is not curved
in the region of this asymmetry (Fig. 2a).
Hemivertebra in an adult rhachitomous vertebral
column (Platyoposaurus)
The investigated specimen (PIN 164/71) is derived from
the presacral vertebral column and consists of two intercentra, a hemivertebral intercentrum, two pleurocentra
and a neural arch, with all vertebral elements being connected by bone (Fig. 3ae). The rhachitomous vertebrae
in Platyoposaurus are interpreted as being anteropleural
sensu Shishkin (1989) [i.e. the pleurocentra of a respective
vertebra are associated with the intercentrum posterior to
it (see discussion below)] and the central elements are
designated accordingly. The anterior, crescent intercentrum (named here intercentrum 1) is ventrally co-ossified
with the posterior intercentrum (intercentrum 2) by
unfinished bone (i.e. covered by cartilage in life), and
thus, the boundary between both bones is well demarcated. The appertaining pleurocentra and neural arch of
intercentrum 1 are not preserved, probably due to the
lack of co-ossification with intercentrum 1. Both intercentra have slightly concave ventral and lateral sides. The
periosteal bone surface of the right half of intercentrum
1 bears some large nutrient foramina on its ventrolateral part (Fig. 3b). The wedge-like left pleurocentrum
2 (belonging to intercentrum 2) is situated between
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intercentra 1 and 2. It extends far ventrally, nearly reaching the ventral midline (Fig. 3a). It is co-ossified with
intercentrum 2 by unfinished bone and is separated from
intercentrum 1 by an unossified gap. On the right side,
an intercentrum of a hemivertebra (hemivertebral intercentrum) is intercalated between intercentrum 1 and 2
and has a bony connection with both (Fig. 3b). Whereas
the boundary between intercentrum 1 and the hemivertebral intercentrum is clearly traceable by a line of unfinished bone, the boundary with intercentrum 2 is evident
only in its dorsalmost part (Fig. 3c). As on the right
halves of intercentrum 1 and 2, an approximately circular
parapophysis with unfinished surface is developed in the
dorsolateral part of the hemivertebral intercentrum. Compared with the hemivertebral intercentrum, the parapophyseal facets on the left side of intercentra 1 and 2 are
larger. The pleurocentrum of the hemivertebra apparently
failed to develop completely. Posterodorsal to the hemivertebral intercentrum and anterodorsal to intercentrum
2 is the right pleurocentrum 2, developed only in its dorsalmost portion in contrast to its left counterpart. The
neural arch belonging to intercentrum 2 and pleurocentra
2 is developed normally with the exception that the right
transverse process is distinctly shorter than the left one.
The neural arch of the hemivertebral intercentrum failed
to develop. The hemivertebral intercentrum is accommodated in a niche on the right side between intercentra 1
and 2, thus representing a hemivertebra of the incarcerated type. It can be regarded a result of failure of formation, because there is no indication for hemimetameric
segmental shift (see discussion in Witzmann et al., 2008).
The complete, smooth fusion of the hemivertebral centrum with intercentrum 2 can be regarded as the result
of embryonic failure of segmentation, which often accompanies the development of hemivertebra (McMaster,
2001). The remaining co-ossifications between the other

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F. Witzmann et al.

(b)

(c)

(d)

(e)

vertebral elements are established by unfinished bone,


and the sutures are well traceable (intercentrum 1 with
intercentrum 2, left pleurocentrum 2 with intercentrum 2,
right pleurocentrum 2 with neural arch, hemivertebral
intercentrum and intercentrum 2), what can be interpreted as post-embryonic co-ossification. The fact that
the neural arch of the hemivertebra failed completely to
develop on both lateral sides of the column (whereas the
hemivertebral intercentrum was formed) indicates that
the development of the particular vertebral elements was
affected independently.
Hemivertebra in a stereospondylous vertebral column
(Metoposauridae)
Specimen MB.Am.1449 consists of two fused intercentra
(named here intercentra 1 and 2) of the thoracic vertebral column (Fig. 4ae). Neural arches and pleurocentra
are not preserved. Each intercentrum is cylindric or
spool-shaped, with slightly concave ventral and lateral
sides. The intercentra show a clearly opisthocoelous

Fig. 3. Hemivertebra in a rhachitomous vertebral column. (a)(e), Platyoposaurus stuckenbergi (PIN 164/71) from the Late Permian of
Belebey, Republic of Bashkortostan. (a)(c)
Drawings in (a) left lateral, (b) right lateral
and (c) ventral view. (d)(e) Photographs of
vertebral centra in left lateral and (e) right
lateral view. Abbreviations: dia, diapophysis;
hic, intercentrum of a hemivertebra; hpar,
parapophysis of hemivertebra; ic,
intercentrum; na, neural arch; par,
parapophysis; pc, pleurocentrum.

morphology. The dorsal side of the centra, which was


connected with the neural arches by cartilage, is unfinished and shows no anatomical details. The lateral and
ventral surfaces of the centra consist of smooth, periosteal
bone. In right lateral view, the boundary between intercentra 1 and 2 is indicated dorsolaterally and laterally by
a dorsoventral indentation of unfinished bone and
ventrolaterally by a broad, shallow ridge. This ridge ends
abruptly on the ventral side of the specimen. Additionally, the right side of the specimen shows two anteroposteriorly elongate parapophyses with an unfinished surface.
Each parapophysis is located in the dorsolateral part of
the respective intercentrum. Contrasting with the right
side, the left side of the specimen shows a third parapophysis between the anterior and the posterior parapophyses. It is located a short distance posterior to the
anterior one and directly anterodorsal to the posteriormost parapophysis. The discrepancy between the left
and the right sides of this specimen is caused by the
intercalation of a hemivertebral intercentrum between
intercentra 1 and 2 on the left side. The boundary
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(c)

(a)

(b)

Fig. 4. Hemivertebra in a stereospondylous


vertebral column. (a)(e) Metoposauridae indet. (MB.Am.1449) from the Triassic/Jurassic
boundary of the Algarve, Portugal. (a)(c)
Drawings in (a) right lateral, (b) left lateral
and (c) ventral view. (d)(e) Photographs in
(d) right lateral and (e) left lateral view.
Abbreviations: hic, intercentrum of a hemivertebra; hpar, parapophysis of hemivertebra; ic,
intercentrum; par, parapophysis.

(d)

between intercentrum 1 and the hemivertebral intercentrum is indicated laterally by a narrow dorsoventral
indentation of unfinished bone; more ventrally, no suture
is detectable. This region is marked by large nutrient
foramina. The boundary between the hemivertebral
intercentrum and intercentrum 2 is indicated by a short
lateral indentation of unfinished bone. These observations
indicate that fusion between the hemivertebral intercentrum and intercentra 1 and 2 was complete. The left
parapophysis of intercentrum 1 corresponds in size to
those on the right side. The parapophyses of the hemivertebral intercentrum and of intercentrum 2 are located
more dorsally and that of intercentrum 2 is shorter. Both
intercentra 1 and 2 differ from the normal cylindric
morphology of metoposaurid centra in that they are anteroposteriorly shortened on the left side. In this way, a
recess is formed that accommodates the hemivertebral
intercentrum. Thus, the hemivertebral intercentrum is of
the incarcerated type as in Platyoposaurus. It can similarly
be regarded a result of failure of formation; at least the
right intercentrum did not develop, but nothing can be
said about the neural arches. The metoposaurid hemivertebra is non-segmented (i.e. it is fused with the anteriorly
and posteriorly neighbouring centra). As this fusion is
complete and smooth, it can be interpreted as an embryonic defect of segmentation.
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(e)

Wedge vertebra and block vertebrae in two plagiosaurid


specimens (Gerrothorax)
Because it is still not clear whether the plagiosaurid vertebral centrum represents an intercentrum, pleurocentrum
or both, it will be designated in the following as centrum. In the isolated specimen A belonging to SMNS
83498, two spool-shaped vertebral centra (named here
centra 1 and 2) are fused and form a block vertebra. A
centrum of a wedge vertebra is fused to the posterior
endplate of centrum 2 (Fig. 5ac). The centrum of the
wedge vertebra is anteroposteriorly much longer on the
left than on the right lateral side of the column. On its
shortened right side, its posterior parapophyseal facet
forms a common, elongate parapophysis with centrum 1,
but its anterior parapophyseal facet is not developed. No
trace of a suture or boundary between centra 1 and 2 and
between centrum 2 and the centrum of the wedge vertebra can be detected, even not on the parapophyses. The
bone surface is entirely smooth. Compared with the
length of normal vertebral centra, the length of each
segment is shortened. This is common in block vertebrae
because longitudinal growth of the vertebrae is impaired
by the fused disc spaces (McMaster, 2001). Two neural
arches are preserved (referred to as neural archs 1 and 2)
and are co-ossified. Neural arch 1 is co-ossified with

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(a)

(b)

(c)

(d)

(e)

(f)

centra 1 and 2, and neural arch 2 is co-ossified with centrum 2 and the centrum of the wedge vertebra. The subsequent neural arch was connected with the posterior half
of the centrum of the wedge vertebra by an unossified
suture and is not preserved. Neural arches 1 and 2 are
poorly preserved, but appear to be normally developed. It
can be assumed that the missing subsequent neural arch
was developed similar to the centrum of the wedge vertebra with an anteroposteriorly shortened right lateral half.
The anterior endplate of centrum 1 and the posterior
endplate of the centrum of the wedge vertebra form an
angle of 18 with each other, thus causing a slight lateral
flexure (scoliosis) of the vertebral column.
In the isolated specimen B that belongs to SMNS
83498, two centra (called here centra 1 and 2) are fused
(Fig. 5df). The neural arches were connected with the
centra by unossified neurocentral sutures and are not

Fig. 5. Wedge and block vertebrae in plagiosaurid vertebrae (Gerrothorax pulcherrimus


from the lower Keuper (Middle Triassic) of
Kupferzell, south-west Germany). (a)(c)
SMNS 83498 (specimen A), block vertebra
with fused wedge vertebra in (a) left lateral,
(b) right lateral and (c) dorsal view. (d)(f)
SMNS 83498 (specimen B), block vertebra in
lateral (d, e) and dorsal (f) view. Abbreviations: c, centrum; dia, diapophysis; fnc, floor
of neural canal; na, neural arch; ncf, neurocentral facet; par1 + 2, parapophysis formed
by centrum 1 and 2; par 2 + w, parapophysis
formed by centrum 2 and centrum of wedge
vertebra; su, suture in parapophysis between
two fused centra; wc, centrum of wedge
vertebra; wpar, parapophysis of wedge
vertebra.

preserved. A suture in the middle of the parapophysis


indicates that centra 1 and 2 are equal in size viewed
from this side (Fig. 5d). The suture is still traceable on
the neurocentral sutural facet dorsomedial to the parapophysis (Fig. 5f). Further traces of sutures cannot be
detected because fusion is complete and the bone surface
is entirely smooth. The parapophysis formed by centra 1
and 2 of the other lateral side is too poorly preserved to
detect a suture on it (Fig. 5e). This parapophysis is
distinctly anteroposteriorly shortened as compared to its
counterpart (25% shorter) and is located not in the middle of the specimen. Observed from this side, centra 1
and 2 are of unequal length. In dorsal view, the floor of
the neural canal and the neurocentral sutural facets are
preserved (Fig. 5f). Because of the intervertebral
position of both the neural arches and the ribs, the
neurocentral sutural facets are exactly dorsomedial to the
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F. Witzmann et al.

parapophyses. The neurocentral sutural facet of the side


with the shortened parapophysis is also anteroposteriorly
shortened compared with its lateral counterpart. Thus,
both centra have a slightly rhombic rather than square
outline in dorsal view. Because the anterior endplate of
centrum 1 and the posterior endplate of centrum 2 are
parallel to each other, no curvature of the vertebral column took place.
Specimen A shows a defect of segmentation (fused centra) and a partial failure of formation (wedge vertebra
posterior to centrum 2), whereas specimen B shows only
a defect of segmentation, that is, fusion of two complete
centra. The fusions in both Gerrothorax specimens are
entirely smooth and thus strongly suggest incomplete separation of somites or their associated mesenchyme during
early embryogenesis. Micro-CT imaging, showing an
entirely homogeneous aspect of the spongy bone with no
evidence for distortion of the trabecular pattern and the
absence of any cortical structures within the centrum
(Fig. 6), clearly indicates a complete fusion of the centra.
The centrum of the wedge vertebra in specimen A can be
designated as a semi-segmented wedge vertebra, because
it is fused to its anteriorly located neighbouring centrum,
but not to the posteriorly following one. The wedge
vertebra and congenital block vertebra described here in
Gerrothorax (and Cheliderpeton, see below) are the oldest
described occurrences of these malformations in fossil
vertebrates.

Malformations in Ancient Amphibians

Fig. 6. Micro-CT scan of block vertebra with fused wedge vertebra in


sagittal cross-section (Gerrothorax pulcherrimus from the lower Keuper (Middle Triassic) of Kupferzell, southwest Germany, SMNS 83498,
specimen A). Abbreviations: c, centrum; na, neural arch.

(a)

(b)

Fused neural spines (Cheliderpeton lellbachae)


The neural arches of the 11th and 12th presacral vertebrae of Cheliderpeton lellbachae (SMNS 91279) are partially fused (Fig. 7a,b). This fusion affects the dorsal half
of the spine and is so complete that even no trace of a
suture or boundary is visible. This gives the dorsal half of
the spine the appearance of a single, elongate bone. The
bone surface shows no signs of ossified tendons or ligaments. Ventral to the fused portion, the two neural arches
are clearly not co-ossified or sutured, but abut against
each other and are thus much closer together than normal adjacent neural arches. Post- and pre-zygapophyses
on the 11th and 12th neural arches, respectively, are
poorly developed. The transverse processes of both neural
arches are normally developed and articulate with the
corresponding ribs. Unfortunately, it cannot be ascertained how the centra of these rhachitomous vertebrae
were affected. Apart from these partially fused neural
spines, the vertebral column of this specimen shows no
signs of pathologies and is straight.
Fused neural spines superficially similar to those evident
in Cheliderpeton lellbachae are described in human and
veterinary medicine as Baastrups phenomenon or disease
2013 Blackwell Verlag GmbH
Anat. Histol. Embryol.

Fig. 7. Cheliderpeton lellbachae SMNS 91279 from the Early Permian of Klauswald/Odernheim, Saar-Nahe Basin (Germany), with two
neural arches that are completely fused dorsally. (a) Drawing of specimen. (b) Photograph of specimen. Abbreviations: dia, diapophysis; na,
neural arch; ri, rib; tp, transverse process of neural arch.

(sometimes called kissing spines). This phenomenon is


characterized by the approach and contact of adjacent
neural spines, causing size increase, flattening and reactive
sclerosis of apposing interspinous surfaces (Bywaters and
Evans, 1982; Resnick, 1985; Kacki et al., 2011). However,
the diagnosis of Baastrups phenomenon in Cheliderpeton
lellbachae can be rejected because the fusion is entirely
smooth with no reactive bone surface and there is no size
increase of the neural spines. The smooth, complete fusion
and the poorly developed zygapophyses of the vertebrae in
question indicate that the fused spines in Cheliderpeton
lellbachae can rather be attributed to failure of segmentation during early embryogenesis. Defects of segmentation
do not only involve the complete vertebrae or the centra
producing block vertebrae (as described in Gerrothorax

Malformations in Ancient Amphibians

F. Witzmann et al.

above), but might also affect the neural arches (Erol et al.,
2004). To our knowledge, similar congenitally fused
neural spines have not been described in a fossil
vertebrate. Konishi et al. (2011), Fig. 8 reported and
illustrated the presumably pathological fusion of the
fourth to seventh presacral neural spines in the mosasaur
Prognathodon overtoni. Generalized vertebral infection
(e.g. in the mosasaur Platecarpus) is easily distinguished
from congenitally derived spinous process fusion (Martin
and Rothschild, 1989).

Discussion
Development of congenital vertebral malformations in
temnospondyls
Witzmann (2007) suggested that hemivertebrae in the
rhachitomous vertebral column might be the result of
failure of ossification of one cartilaginous lateral half of
an intercentrum, because ossification usually proceeded
(a)

(b)

(c)

(d)
(e)

Fig. 8. (a)(d) Schematic reconstruction of parts of the vertebral columns of some of the temnospondyls described in this manuscript in
ventral view. The preserved pathologies are held in light grey. Sutures
or boundaries that are not visible in the specimens due to complete
fusion are dashed. (a) Rhachitomous vertebrae of Platyoposaurus
stuckenbergi with non-segmented hemivertebra. (b) Stereospondylous
vertebrae of an undetermined metoposaurid with non-segmented
hemivertebra. Note that the hemivertebrae are incarcerated in (a) and
(b); thus, no scoliosis is produced. (c)(d) Plagiosaurid vertebrae of
Gerrothorax pulcherrimus. (c) Block vertebra fused with wedge vertebra anteriorly; the wedge vertebra is semi-segmented and not incarcerated and produces a scoliosis. (d) Block vertebra producing no
scoliosis. Note that the centra of the block vertebrae in (c) and (d) are
anteroposteriorly shortened due to impairment of longitudinal growth
by fusion of the disc spaces. (e) Anteropleural rhachitomous vertebra; the intercentrum is associated with the anteriorly neighboured
pleurocentra and neural arch (redrawn from Shishkin, 1989), compared with normal rhachitomous vertebra in Fig. 1a. Abbreviations:
hic, intercentrum of a hemivertebra; ic, intercentrum; na, neural arch;
par, parapophysis; pc, pleurocentrum; wc, centrum of wedge vertebra.

10

very slowly in centra and long after the ossification of the


neural arches in temnospondyl ontogeny (Boy, 1974;
Schoch and Witzmann, 2009a,b). This assumption was
based on a capitosauroid vertebral fragment consisting of
fused intercentra with an intercalated hemivertebral intercentrum, but the neural arches were not preserved. However, failure of the neural arch (which ossifies early in
temnospondyl ontogeny) to form in the hemivertebra of
Platyoposaurus and in the larval Sclerocephalus specimen
shows that the defect must have occurred early in
embryogenesis of early tetrapods, before chondrification
and is not a defect of ossification. The congenital vertebral pathologies described here thus show that defects of
formation and segmentation in the tetrapod vertebral
column represent a fundamental failure of somitogenesis
before chondrification and ossification of the vertebral
anlagen and can be followed throughout tetrapod evolution. This is irrespective of the type of vertebra that is
affected, that is, stereospondylous, rhachitomous or
plagiosaurid. All components of the vertebra can be
involved (intercentrum, pleurocentrum, neural arch),
either together or independently.
Consequences of the described vertebral malformations
for the living animals
According to Kaplan et al. (2005), a mixture of defects of
formation and of segmentation is often evident in
humans and may produce quite complex malformations
in one individual. This is also the case for the described
hemivertebrae of Platyoposaurus, for the Algarve metoposaurid and for the wedge vertebra in specimen A of
Gerrothorax. In contrast, the malformations in Gerrothorax specimen B and Cheliderpeton lellbachae are solely
defects of segmentation, and the malformation in the
larval Sclerocephalus is solely a defect of formation.
Congenital abnormalities of the spine are frequently
associated with defects in the urogenital, pulmonary and
cardiac systems (Kaplan et al., 2005). However, the individuals described here were probably not severely affected
by their vertebral malformations, because the sizes of
their vertebrae suggest that they were quite large-grown
adults, and only the Sclerocephalus specimen is a small
larva. However, the lake sediments of the Saar-Nahe
Basin have yielded hundreds of specimens of larval Sclerocephalus and other temnospondyl amphibians (Schoch
and Witzmann, 2009a), and the hemivertebra in this
specimen did not cause scoliosis. Thus, it can be assumed
that this malformation did not cause the death of this
individual. Similarly, the hemivertebrae in Platyoposaurus
and the Algarve metoposaurid did not cause scoliosis,
and this was also the case in Gerrothorax specimen B
showing a block vertebra, whereas the lateral curvature of
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F. Witzmann et al.

the column in Gerrothorax specimen A caused by a wedge


vertebra was only slight (Fig. 8ad). (As we do not know
the complete vertebral columns of these specimens except
for Sclerocephalus, we cannot say whether further wedge
or hemivertebrae were actually present in each of these
individuals.)
In all described specimens except for Sclerocephalus,
this apparently did not represent a severe disadvantage
for these individuals, as these temnospondyls were no
axial swimmers. Gerrothorax is interpreted as a bottomdwelling ambush predator, with a dorsoventrally flattened
trunk that was stiffened by heavy dorsal and ventral
osteoderms (Hellrung, 2003). Basal stereospondylomorphs
like Platyoposaurus or Cheliderpeton have a long, powerful swimming tail, whereas the trunk was stabilized by
heavy ribs with large flanges and processes (Fig. 1d,e).
Sulej (2007) reported a rather stiff presacral vertebral column but a flexible tail in metoposaurids. Thus, movement of the tail rather than of the trunk was responsible
for drive during swimming in these forms. Of course,
fusion of vertebrae might be disadvantageous in taxa that
rely to a large extent on lateral undulations of the body
for locomotion, the more so if several vertebrae are
involved in fusion. On the other hand, fusion of certain
parts of the vertebral column might also be of benefit
and is characteristic for many tetrapod taxa. Thus, it is
not always easy to decide whether the phenomenon of
fused vertebrae is pathological or is an adaptation, for
example, for mechanical strength. A number of extant
and fossil tetrapods show fusion of neural spines and/or
centra for stiffening of the trunk or to stabilize the pectoral and sacral regions. Among temnospondyls, this is
evident in the dissorophid Astreptorhachis. The distal portions of trunk neural spines are fused together to stiffen
the trunk, probably an adaptation for terrestrial locomotion (Vaughn, 1971). It is well known that pterosaurs
have a notarium in which the spines of the anterior dorsal vertebrae are fused to support the shoulder girdle and
to serve as attachment site of muscles of the foreleg
(Wellnofer, 1983). In both ornithischians and saurischians, the sacral region may be stabilized by fused neural
} and F
spines and centra (e.g. Osi
ozy, 2007; Sullivan et al.,
2011). A mechanical function can be ruled out for the
fused vertebrae described here, as this fusion is not
known from any other individual of these taxa or their
close relatives, and there is no obvious mechanical necessity to strengthen or stiffen the column in this region.
Indication for resegmentation of rhachitomous vertebrae
sensu Shiskin
The pathological Platyoposaurus specimen described here
also sheds light on Shishkins (1987, 1989) hypothesis of
2013 Blackwell Verlag GmbH
Anat. Histol. Embryol.

Malformations in Ancient Amphibians

resegmentation of rhachitomous vertebrae in temnospondyls. The intercentrum was topographically associated


(and sometimes co-ossified) with the preceding (anterior)
pleurocentra in the rhachitomous vertebrae of numerous
Palaeozoic temnospondyls. Shiskin referred this mechanical association between posterior inter- and anterior pleurocentra as anteropleural (Fig. 8e). Shishkin (1989),
however, did not deny the presence of the normal association of inter- and pleurocentrum in rhachitomous vertebrae of certain temnospondyls, with the pleurocentra
being associated with the anterior intercentrum, as shown
in Fig. 1a. He thus stated the presence of two alternative
conditions of central element association in adult temnospondyls: the normal and the anteropleural conditions.
According to him, the anteropleural situation is the plesiomorphic condition in temnospondyls and can also be
demonstrated in tetrapodomorph fishes. As indicated by
the intersegmental position of the ribs, the anteropleural
centra are intrasegmental, whereas the normal centra are
intersegmental and thus resegmented (Shishkin, 1987,
1989). In the pathological specimen of Platyoposaurus
described here, the left, normally developed pleurocentrum is co-ossified with the intercentrum posterior to it,
whereas it is separated from the anterior intercentrum by
a broad gap (Fig. 3a). This condition, which would have
been not preserved in a healthy rhachitomous vertebra
(because of the generally cartilaginous connections of the
vertebral components), is clearly anteropleural sensu
Shishkin (1989) and might support his hypothesis of the
occurrence of two different conditions in rhachitomous
vertebrae.
Comparison with the Holocene record of vertebral
anomalies
Examination of frog vertebrae from the Hiscock site
(Rothschild and Laub, in press), a Paleoindian archaeological excavation in western New York (United States)
dated at 9000 years before present, revealed only six congenital vertebral anomalies. This represented examined
0.2% of bones, a frequency indistinguishable from that
noted in temnospondyls.
Conclusions
1. Defects of formation (hemi- and wedge vertebra) and
segmentation (block vertebra) can be found in the vertebral column of Palaeozoic and Mesozoic amphibians. The
wedge vertebra and congenital block vertebra described
here are the oldest known occurrences of these malformations in the fossil record.
2. The vertebral malformations of ancient amphibians
occur in rhachitomous, stereospondylous and plagiosaurid

11

Malformations in Ancient Amphibians

vertebrae and can affect all components of the vertebrae,


either together or independently on their own.
3. Although vertebral ontogenies and morphologies of
ancient amphibians have no extant analogue among tetrapods, the malformations found here can be attributed to
the same underlying factors as in extant tetrapods including humans, that is, fundamental failure of somitogenesis
caused by genes or environmental factors.
4. Given the quite rare prevalence of congenital vertebral
malformations in humans (e.g. the occurrence of hemivertebrae is estimated at 510 in 10 000 births, WynneDavies, 1975), the congenital malformations of the
vertebral column in ancient amphibians could be more
frequent if one considers the small sample size of investigated specimens. One may speculate that this might be
an indication that ancient amphibians were more susceptible to the underlying genetic or environmental factors
resulting in disrupted somitogenesis. Large-sample-size
studies of fossil amphibians have to be carried out to
confirm or reject this hypothesis.
5. The close topographical association of the intercentrum
with the anteriorly neighboured pleurocentrum in Platyoposaurus, as shown by the pathological co-ossification in
specimen PIN 164/71 examined here, suggests the presence
of anteropleural rhachitomous vertebrae as outlined in
Shishkins (1987, 1989) hypothesis of resegmentation.
6. The frequency of vertebral congenital malformations
in amphibians appears unchanged from the Holocene.
Acknowledgements
We thank Rainer Schoch (Staatliches Museum f
ur
Naturkunde Stuttgart) for access to the collection under
his care and the two anonymous reviewers for their thorough work.
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