Paleopathology in Amphibia Paleopathology in Amphibians

ORIGINAL ARTICLE

Congenital Malformations of the Vertebral Column inAncient AmphibiansF. Witzmann1*, B. M. Rothschild2, O. Hampe1, G. Sobral1, Y. M. Gubin3 and P. Asbach4

Addresses of authors: 1 Museum fur Naturkunde, Leibniz-Institut fur Evolutions- und Biodiversitatsforschung, Invalidenstrae 43, Berlin D-10115,

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, Charite Universitatsmedizin Berlin, Chariteplatz 1, Berlin 10117, Germany

*Correspondence:

Tel.: +49 30 2093 8820;

fax: +49 30 2093 8565;

e-mail: [email protected]

With 8 figures

Received November 2012; accepted for

publication February 2013

doi: 10.1111/ahe.12050

This work was carried out at the Museum fur

Naturkunde, Leibniz-Institut fur Evolutions- und

Biodiversitatsforschung, 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 stereo-

spondylous, 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 congeni-

tal 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.

Temnospondyl vertebrae are plesiomorphically rhachit-

omous, that is, they are composed of the neural arch

(including the processus spinosus) and a multipartite

vertebral body, which consists of a large, unpaired inter-

centrum (or hypocentrum) and of paired, smaller pleuro-

centra (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 capitu-

lum 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 nor-

mally separated by cartilage rather than being co-ossified.

In some stereospondyls (mainly Mesozoic temnospond-

2013 Blackwell Verlag GmbH

Anat. Histol. Embryol. 1

Anatomia, Histologia, Embryologia

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-ossi-

fied or reduced (Fig. 1b). This vertebral morphology

is generally designated as stereospondylous and can

be found in large-growing stereospondyls, such as Masto-

donsaurus (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 mor-

phology, that is, the intercentrum is anteriorly convex and

posteriorly concave, thus forming a kind of ball-and-

socket joint. This may represent the origin of synovial

intercentral joints. Among stereospondyls, the Triassic

plagiosaurids have spool-shaped vertebral centra with

intervertebral neural arches (Shishkin, 1987, 1989; Warren

and Snell, 1991). Each parapophysis of plagiosaurid presa-

cral 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 pleu-

rocentra, 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 pleuro-

centrum as reduced. Hellrung (2003) followed this view,

but regarded the pleurocentrum as fused with the neural

arch.

(a) (b) (c)

(d)

(e)

(f)

(g)

Fig. 1. (a)(c) Schematic drawings of rhachit-

omous, stereospondylous and plagiosaurid

vertebrae. (a) Rhachitomous condition

(redrawn from Shishkin, 1989). (b) Stereo-

spondyl 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 inves-

tigated 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 Acad-

emy of Sciences, Moscow, Russia). (f) A Trias-

sic metoposaurid (Metoposaurus diagnosticus

krasiejowensis, total body length approxi-

mately 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.


Anat. Histol. Embryol.2

Malformations in Ancient Amphibians F. Witzmann et al.

The ontogeny of temnospondyl vertebrae is well docu-

mented 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 Witz-

mann, 2009a,b). In general, vertebral ossification pro-

ceeded very slowly, starting with the initially paired

neural arches, followed much later in ontogeny by ossifi-

cation 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 som-

ites 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 verte-

brae (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 disrup-

tion of fusion of the paired mesenchymal vertebral anla-

gen, 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 suscepti-

bility 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 ossifica-

tion 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 distin-

guished 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 incar-

cerated type, which is less common in humans, the verte-

brae 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

press). A wedge vertebra has a similar shape, but in con-

trast 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 cap-

torhinomorph 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 plesio-

saur 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 ani-

mals physiology and behaviour (Rothschild and Martin,

2006). Congenital vertebral malformations in temno-

spondyls 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 Sub-

formation) of Klauswald/Odernheim, Early Permian,

Saar-Nahe Basin (Germany). The taxon Cheliderpeton



F. Witzmann et al. Malformations in Ancient Amphibians

lellbachae was erected by Kratschmer (2006), but needs

taxonomic revision as it does not share the autapomor-

phies 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 hemi-

vertebra 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 up-

to-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 aqua-

tic 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 fur Naturkunde Berlin using a Phoenix|X-ray

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 three-

dimensional 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; forspecimen 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 speci-men MB.Am.1449 yielded no results. The scanning of the

Platyoposaurus vertebrae PIN 164/71 could not be real-

ized. 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 fur Naturkunde, Berlin, Germany; IPFUB,

Institut fur Palaontologie, Freie Universitat Berlin, Ger-

many; PIN, Paleontological Institute and Museum of the

Russian Academy of Sciences, Moscow, Russia; SMNS

Staatliches Museum fur Naturkunde Stuttgart, Germany.

Results

Hemivertebra in a larval rhachitomous vertebral column

(Sclerocephalus)

The vertebral column of the larval specimen of Sclero-

cephalus (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 pre-

served. 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 repre-

sented 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




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 inter-

centra, a hemivertebral intercentrum, two pleurocentra

and a neural arch, with all vertebral elements being con-

nected by bone (Fig. 3ae). The rhachitomous vertebraein 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 intercen-

trum (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 demar-

cated. The appertaining pleurocentra and neural arch of

intercentrum 1 are not preserved, probably due to the

lack of co-ossification with intercentrum 1. Both inter-

centra 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 ventrolat-

eral part (Fig. 3b). The wedge-like left pleurocentrum

2 (belonging to intercentrum 2) is situated between

intercentra 1 and 2. It extends far ventrally, nearly reach-

ing 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 inter-

centrum) is intercalated between intercentrum 1 and 2

and has a bony connection with both (Fig. 3b). Whereas

the boundary between intercentrum 1 and the hemiverte-

bral intercentrum is clearly traceable by a line of unfin-

ished 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. Com-

pared with the hemivertebral intercentrum, the parapo-

physeal 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 hemi-

vertebral intercentrum and anterodorsal to intercentrum

2 is the right pleurocentrum 2, developed only in its dor-

salmost 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 accommo-

dated in a niche on the right side between intercentra 1

and 2, thus representing a hemivertebra of the incarcer-

ated type. It can be regarded a result of failure of forma-

tion, because there is no indication for hemimetameric

segmental shift (see discussion in Witzmann et al., 2008).

The complete, smooth fusion of the hemivertebral cen-

trum with intercentrum 2 can be regarded as the result

of embryonic failure of segmentation, which often accom-

panies the development of hemivertebra (McMaster,

2001). The remaining co-ossifications between the other

(a)

(b)

Fig. 2. Hemivertebra in a larval rhachitomous

vertebral column, exemplified by a larval spec-

imen 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.




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 inter-

preted 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 verte-

bral column (Fig. 4ae). Neural arches and pleurocentraare not preserved. Each intercentrum is cylindric or

spool-shaped, with slightly concave ventral and lateral

sides. The intercentra show a clearly opisthocoelous

morphology. The dorsal side of the centra, which was

connected with the neural arches by cartilage, is unfin-

ished 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 inter-

centra 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. Addition-

ally, the right side of the specimen shows two anteropos-

teriorly 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 parap-

ophysis between the anterior and the posterior parapoph-

yses. It is located a short distance posterior to the

anterior one and directly anterodorsal to the posterior-

most 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

(a) (b)

(c)

(d) (e) Fig. 3. Hemivertebra in a rhachitomous verte-bral column. (a)(e), Platyoposaurus stucken-

bergi (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.




between intercentrum 1 and the hemivertebral intercen-

trum 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 intercen-

trum 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 hemiver-

tebral 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 ante-

roposteriorly 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 hemiver-

tebra 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 embry-

onic defect of segmentation.

Wedge vertebra and block vertebrae in two plagiosaurid

specimens (Gerrothorax)

Because it is still not clear whether the plagiosaurid verte-

bral centrum represents an intercentrum, pleurocentrum

or both, it will be designated in the following as cen-

trum. 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 thewedge 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 verte-

bra 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

(a)

(b)

(c)

(d) (e)Fig. 4. Hemivertebra in a stereospondylousvertebral column. (a)(e) Metoposauridae in-

det. (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 hemiver-

tebra; hpar, parapophysis of hemivertebra; ic,

intercentrum; par, parapophysis.




centra 1 and 2, and neural arch 2 is co-ossified with cen-

trum 2 and the centrum of the wedge vertebra. The sub-

sequent 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 verte-

bra 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 lateralflexure (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 thecentra by unossified neurocentral sutures and are not

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 parap-

ophysis (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 mid-

dle 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

(a)

(c)

(b)

(e)

(d)

(f)

Fig. 5. Wedge and block vertebrae in plagio-

saurid 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. Abbrevia-

tions: c, centrum; dia, diapophysis; fnc, floor

of neural canal; na, neural arch; ncf, neuro-

central 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.




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 col-

umn took place.

Specimen A shows a defect of segmentation (fused cen-

tra) 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 sep-

aration 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.

Fused neural spines (Cheliderpeton lellbachae)

The neural arches of the 11th and 12th presacral verte-

brae of Cheliderpeton lellbachae (SMNS 91279) are par-

tially 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 liga-

ments. 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 nor-

mal 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 ascer-

tained 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

(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 segmenta-

tion during early embryogenesis. Defects of segmentation

do not only involve the complete vertebrae or the centra

producing block vertebrae (as described in Gerrothorax

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

sagittal cross-section (Gerrothorax pulcherrimus from the lower Keu-

per (Middle Triassic) of Kupferzell, southwest Germany, SMNS 83498,

specimen A). Abbreviations: c, centrum; na, neural arch.

(a) (b)

Fig. 7. Cheliderpeton lellbachae SMNS 91279 from the Early Perm-

ian of Klauswald/Odernheim, Saar-Nahe Basin (Germany), with two

neural arches that are completely fused dorsally. (a) Drawing of speci-

men. (b) Photograph of specimen. Abbreviations: dia, diapophysis; na,

neural arch; ri, rib; tp, transverse process of neural arch.




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

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 inter-

centrum, but the neural arches were not preserved. How-

ever, 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 verte-

bral 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 evolu-

tion. 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 metopo-

saurid and for the wedge vertebra in specimen A of

Gerrothorax. In contrast, the malformations in Gerrotho-

rax 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 indi-

viduals 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 Sclero-

cephalus 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

(a) (c) (d)

(e)

(b)

Fig. 8. (a)(d) Schematic reconstruction of parts of the vertebral col-

umns 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 verte-

bra anteriorly; the wedge vertebra is semi-segmented and not incar-

cerated 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 verte-

bra; the intercentrum is associated with the anteriorly neighboured

pleurocentra and neural arch (redrawn from Shishkin, 1989), com-

pared 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 verte-

bra.




the column in Gerrothorax specimen A caused by a wedge

vertebra was only slight (Fig. 8ad). (As we do not knowthe 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 bottom-

dwelling 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, power-

ful 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 col-

umn but a flexible tail in metoposaurids. Thus, move-

ment 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 pec-

toral and sacral regions. Among temnospondyls, this is

evident in the dissorophid Astreptorhachis. The distal por-

tions of trunk neural spines are fused together to stiffen

the trunk, probably an adaptation for terrestrial loco-

motion (Vaughn, 1971). It is well known that pterosaurs

have a notarium in which the spines of the anterior dor-

sal 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 sauris-

chians, the sacral region may be stabilized by fused neural

spines and centra (e.g. }Osi and Fozy, 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 neces-

sity 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

resegmentation of rhachitomous vertebrae in temno-

spondyls. 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 mechani-

cal association between posterior inter- and anterior pleu-

rocentra as anteropleural (Fig. 8e). Shishkin (1989),

however, did not deny the presence of the normal associ-

ation of inter- and pleurocentrum in rhachitomous verte-

brae 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 temno-

spondyls: the normal and the anteropleural conditions.

According to him, the anteropleural situation is the ple-

siomorphic 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 pleurocen-

trum 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 archaeo-

logical excavation in western New York (United States)

dated at 9000 years before present, revealed only six con-

genital 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 verte-

bral column of Palaeozoic and Mesozoic amphibians. The

wedge vertebra and congenital block vertebra described

here are the oldest known occurrences of these malforma-

tions in the fossil record.

2. The vertebral malformations of ancient amphibians

occur in rhachitomous, stereospondylous and plagiosaurid




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 tetra-

pods, the malformations found here can be attributed to

the same underlying factors as in extant tetrapods includ-

ing 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 hemi-

vertebrae is estimated at 510 in 10 000 births, Wynne-Davies, 1975), the congenital malformations of the

vertebral column in ancient amphibians could be more

frequent if one considers the small sample size of investi-

gated specimens. One may speculate that this might be

an indication that ancient amphibians were more suscep-

tible 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 Platyo-

posaurus, 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 fur

Naturkunde Stuttgart) for access to the collection under

his care and the two anonymous reviewers for their thor-

ough work.

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Paleopathology in Amphibia Paleopathology in Amphibians