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*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.
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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-
(a)
(b)
F. Witzmann et al.
(c)
(d)
(e)
(f)
(g)
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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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.
F. Witzmann et al.
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.
(a)
(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
(a)
F. Witzmann et al.
(b)
(c)
(d)
(e)
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.
F. Witzmann et al.
(c)
(a)
(b)
(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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Anat. Histol. Embryol.
(e)
F. Witzmann et al.
(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
F. Witzmann et al.
(a)
(b)
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.
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.
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12
F. Witzmann et al.
K. Kusumi, 2004: Congenital scoliosis and vertebral malformations: characterization of segmental defects for
genetic analysis. J. Pediatr. Orthop. 24, 674682.
Gubin, Y. M., 1991: Permian Archegosauroid Amphibians of
the USSR. Moscow: Nauka. [In Russian].
Hellrung, H., 2003: Gerrothorax pustuloglomeratus, ein Temnospondyle (Amphibia) mit kn
ocherner Branchialkammer aus
dem Unteren Keuper von Kupferzell (S
uddeutschland). Stuttg Beitr Natkd Ser B. 330, 1130.
Janensch, W., 1934: Eine halbseitige uberzahlige Wirbelbildung bei einem Dinosaurier. Sitzungsber. Ges. Naturf.
Freunde. Berlin. 1933, 458462.
Jeffery, N. D., P. M. Smith, and P. E. Talbot, 2007: Imaging
findings and surgical treatment of hemivertebrae in three
dogs. J. Am. Vet. Med. Assoc. 230, 532536.
Johnson, G. D., 1988: An abnormal captorhinomorph vertebra
from the Lower Permian of North-Central Texas. J. Vert.
Paleontol. 8(Suppl), 19A.
Kacki, S., S. Villotte, and C. J. Kn
usel, 2011: Baastrups sign
(kissing spines): a neglected condition in paleopathology.
Int. J. Paleopathol. 1, 104110.
Kaplan, K. M., J. M. Spivak, and J. A. Bendo, 2005: Embryology of the spine and associated congenital abnormalities.
Spine J. 5, 564576.
Konishi, T., D. Brinkman, J. A. Massare, and M. W. Caldwell,
2011: New exceptional specimens of Prognathodon overtoni
(Squamata, Mosasauridae) from the upper Campanian of
Alberta, Canada, and the systematics and ecology of the
genus. J. Vert. Paleontol. 31, 10261046.
Kratschmer, K., 2006: Neue temnospondyle Amphibien aus
dem Rotliegend des s
udwestdeutschen Saar-Nahe-Beckens,
Teil 1. Geowiss. Beitr. Saarpf. Rotl. 4, 346.
F. Witzmann et al.
} A., and I. F
Osi,
ozy, 2007: A maniraptoran (Theropoda, Dinosauria) sacrum from the Upper Cretaceous of the Hateg Basin
(Romania) in search of the lost pterosaurs of Baron Franz
Nopcsa. Neues. Jahrb. Geol. Palaontol. Abh. 246, 173181.
Panchen, A. L., 1959: A new armoured amphibian from the
Upper Permian of East Africa. Philos. Trans. R. Soc. Lond.
B Biol. Sci. 242, 207281.
Panchen, A. L., 1977: The origin and early evolution of
tetrapod vertebrae. In: Problems in Vertebrate Evolution.
(S. M. Andrews, R. S. Miles and A. D. Walker, eds).
London: Linnean Society of London. pp 289318.
Pourquie, O., and K. Kusumi, 2001: When body segmentation
goes wrong. Clin. Genet. 60, 409416.
Resnick, D., 1985: Degenerative diseases of the vertebral column. Radiology 156, 314.
Rothschild, B. M., and R. S. Laub: Epidemiology of anuran
pathology in the holocene component of the Hiscock site:
rare or not survived. J. Herpetol (in press).
Rothschild, B. M., and L. R. Martin, 2006: Skeletal impact of
disease. Bull. New Mexico Mus. Natl Hist. 33, 1226.
Rothschild, B. M., H.-P. Schultze, and R. Pellegrini, 2012:
Herpetological Osteopathology. Annotated Bibliography of
Amphibians and Reptiles. Heidelberg: Springer.
Rothschild, B. M., L. D. Martin, J. Babiarz, and D. A. Berman, in
press: Hemivertebrae as pathology and as a window to Oligocene behavior. Internet J. Vert. Paleontol.
Ruta, M., and M. I. Coates, 2007: Dates, nodes and character
conflict: addressing the lissamphibian origin problem.
J. Syst. Palaeontol. 5, 69122.
Schoch, R. R., 1999: Comparative osteology of Mastodonsaurus
giganteus (Jaeger 1828) from the Middle Triassic (Lettenkeuper: Longobardian) of Germany (Baden-W
urttemberg,
Bayern, Th
uringen). Stuttg. Beitr. Natkd. Ser B 278,
1175.
Schoch, R. R., 2009: Evolution of life cycles in early amphibians. Annu. Rev. Earth Planet. Sci. 37, 135162.
Schoch, R. R., and F. Witzmann, 2009a: Osteology and relationships of the temnospondyl genus Sclerocephalus. Zool.
J. Linn. Soc. 157, 135168.
Schoch, R. R., and F. Witzmann, 2009b: The temnospondyl
Glanochthon from the Lower Permian Meisenheim Formation
of Germany. Special Papers Palaeontol. 81, 121136.
Schoch, R. R., and F. Witzmann, 2012: Cranial morphology of
the plagiosaurid Gerrothorax pulcherrimus as an extreme
example of evolutionary stasis. Lethaia 45, 371385.
Shawen, S. B., P. J. Belmont, T. R. Kuklo, B. D. Owens, K. F.
Taylor, R. Kruse, and D. W. Polly, 2002: Hemimetameric
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