zoological Journal of the Linnean Society (1983), 79: 1-59. With 16 figures
Gnathostome vertebrae and the
classification of the Amphibia
B. G . GARDINER
Biology Department, Queen Elizabeth College, London W8
Received March 1982, revised and accepted for publication March 1983
Four pairs of arcualia were primitively present in each segment of gnathostomes. The individual
vertebral ossifications of early temnospondyls are most economically interpreted as the
endochondral ossifications of these cartilaginous arcualia. Centra have formed independently on at
least two occasions within the tetrapods and arcualia play little or no part in the formation of true
centra in any living form. The so called pleuro- and intercentra of the temnospondyls can in no way
be homologized with the centra of either lissamphibians or amniotes. The Nectridea are considered to
be the sister group of the Lissamphibia and the Aistopoda the sister group of these two. The
anthracosaurs, seymourians and microsaurs are regarded as amniotes. There is no evidence for
resegmentation in the vertebral column.
KEY WORDS:-Arcualia
-
centra - intercentra - diplospondyly - Amphibia
~
phylogeny.
CONTENTS
Introduction . . . . . . . .
Historical survey . . . . . . .
Arcualia theory . . . . . . .
Development of centra . . . . . .
Resegmentation . . . . . . .
Diplospondyly . . . . . . . .
Vertebrae and phylogeny . . . . .
Chondrichthyan vertebrae
. . .
Osteichthyan fish vertebrae
. . .
Amphibian vertebrae . . . . .
Amniote vertebrae
. . . . .
Acanthodian and placoderm vertebrae .
Classification of amphibia . . . . .
Summary and conclusions . . . . .
Acknowledgements
. . . . . .
References. . . . . . . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
1
2
9
10
13
18
20
20
24
32
39
46
46
51
52
52
INTRODUCTION
This is the second of two papers dealing with the classification of the
Tetrapoda (see also Gardiner, 1982). Both papers are a direct outcome of earlier
collaborative work with Peter Forey, Colin Patterson and Donn Rosen (Rosen et
al., 1981) in which it was early realized, in trying to compare lungfishes with
amphibians, that there was no acceptable phylogeny of the Tetrapoda. Since
1
0024-4082/83/090001+ 59 $03.00/0
1
0 1983 The Linnean Society of London
2
B. G. GARDINER
amphibian classification had in the past been mainly concerned with vertebral
structure our attention was drawn to the totally different vertebral patterns of
living amphibians and amniotes (Rosen et al., 1981: 248). We also realized that
the manus in amphibians comprised four fingers, that in amniotes five. These
kind of observations suggested that other amniote synapomorphies (other than
amnion, chorion and allantois) might be worth looking for. I n searching for
synapomorphies to characterize and classify these early tetrapods it soon became
apparent that a study of vertebral structure and development throughout all
gnathostome groups was necessary for effective outgroup comparison.
Without doubt the greatest influence on our interpretation of the
development and the structure of vertebrae has been the arcualia theory of
Gadow & Abbott (1895; see also Gadow, 1896, 1933). Gadow & Abbott, using the
developmental stages of selachians as their archetype, argued that the
ontogeny of all vertebrae could be explained in terms of four pairs of embryonic
cartilages (arcualia) in each segment. The larger posterior arcualia in each
segment became known as the basidorsals (neural arch anlagen) and
basiventrals (haemal arch anlagen) and the smaller anterior arcualia as the
interdorsals and interventrah. Although much of the subsequent published
evidence on the development of the centrum has been at variance with the
Gadovian hypothesis (Howes & Swinnerton, 1901; Dawes, 1930; Mookerjee,
1936, Williams, 1959a), the terminology of Gadow & Abbott (1895) is still
applicable to many Recent and fossil fishes as well as primitive tetrapods
(ichthyostegids and temnospondyls, Rosen et al., 1981) and the development of
extant amphibians and amniotes.
HISTORICAL SURVEY
In 1837 Egerton (p. 188) noticed that between the cervical vertebrae of
ichthyosaurs there occurred small independent ossifications which he termed
subventral wedge bones. Owen (1847: 261) subsequently homologized one of
these subventral wedge bones with the odontoid process of the mammalian axis.
Later, however, Owen (1859: 85) considered the subventral wedge bone to be the
equivalent of the atlas hypapophysis rather than the centrum proper (odontoid
process). Meanwhile Goldfuas (1847) had published an account of the skeleton
of the Permian amphibian Archegosaurus and had sent casts of the original to the
Royal College of Surgeons (Owen, 1854: 117). Owen (1861: 196) later made
Archegosaurus the type of his new order Ganocephala. I n his redescription of
Archegosaurus based on these casts Owen (1861) pointed out that there were three
bony plates around the cap.sule of the notochord, one ventral and one either
side. The ventral ossification he regarded as a hypapophysis, equivalent to the
body of the atlas in mammals and the subvertebral wedge bone of
ichthyosaurs. This conclusion was probably prompted by the earlier work of
Rathke (1848: 78) in which it was demonstrated that the ventral arch of the
atlas of amniotes was possibly a modified haemal arch.
Despite some initial confusion Owen believed that the wedge bones of
ichthyosaurs were homologous with the hypapophysis of the mammalian atlas,
the hypapophysis of Spheno,don atlas (1853: 142), the small detached wedge
shaped ossifications between the lumbar vertebrae of the mole (1866) and the
ventral ossifications in the trunk region of Archegosaurus. In the tail region of
GNATHOSTOME VERTEBRAE
3
Archegosaurus (Figs 7E, 8A), where two sets of ventral ossifications per neural
arch are present, Owen (1861: 197) was of the opinion that only the more
posterior pair were their homologues.
Unfortunately Owen (1866: 53) also used the term hypapophysis for the
ventral projection or outgrowth seen on snake vertebrae. [Boulenger (1891: 113)
concluded Owen (1866) was correct in homologizing these ventral spines with
intercentra in the case of reptiles.] Moreover he (Owen, 1847: 250) considered
the haemapophyses or chevron bones in the tails of reptiles and cetaceans to be
homologous with sternal ribs. Huxley ( 187 1: 187) however, homologized these
chevron bones with the more anterior subvertebral wedge bones as did
Boulenger ( 1891).
Cope (187813: 327), in his description of the Permian amphibian Trimerorhachis,
maintained that the segments of the centrum were three in number (much as in
Archegosaurus) and that the superior, lateral pair of plates on each side
represented the centrum proper, while the so called intercentrum ( = Owen’s
1861 hypapophysis) was intercalated between these centra. Thus Cope, like
Owen, believed that there were essentially two centra to each segment
(intercentrum and centrum); furthermore Cope (1878a: 319; 1878d: 633)
believed that the intercentrum nearly replaced the centrum in Trimerorhachis
and did so completely in other fossil amphibians.
Cope apparently arrived at his view independently of Owen and from entirely
different comparisons. Cope ( 1878c: 5 10; 1880: 609) was describing Trimerorhachis
simultaneously with the embolomere Cricotus. In this latter form Cope (187813, c)
found that the vertebral column was characterized by the development of
diplospondylous centra: the centra and intercentra forming entire vertebral
bodies and in pairs supporting single neural arches. Cope, like Owen, therefore
considered that the centra of the rhachitomous amphibians (Archegosaurus,
Trimerorhachis) were composed of two segments (centrum and intercentrum as in
Sphenodon and embolomeres) together supporting one neural arch. Cope’s
evidence (1884: 37) rested on the fact that the pleurocentrum (=t ru e centrum)
was of larger bulk and supported the neural arch and costal articulations
whereas the intercentrum bore the chevron bones in both rhachitomes and
embolomeres. Cope assumed that the rhachitomous form of vertebra gave rise to
that of the embolomeres by the completion of the two rings (growth upwards of
intercentra, growth downwards of centra = pleurocentra). Cope (1882, 1884:
fig. 1, 1888: 253) further derived the Recent Amphibia and the Stegocephalia
( = stereospondyls) from the rhachitomes by the loss of the centrum
( = pleurocentrum), and the reptiles from the embolomeres (1880: 609) by the
loss of the intercentrum (the reptiles were considered to be descendants of
embolomeres because they possessed an atlas with an intercentrum). Finally in
1888 Cope, like Owen, concluded that the rhachitome intercentrum was
homologous with the intercentrum of Sphenodon, lizards and Erinaceidae as well
as pelycosaurs. By the end of the century most authors (Albrecht, 1883; Baur,
1886a,b,c; Dollo, 1889; Hay, 1895) agreed with Cope that the vertebral centrum
of the Amniota was derived from the rhachitome pleurocentrum.
An alternative interpretation of the rhachitomous condition to that of Owen
and Cope was given by Gaudry (1878: 62, 1883: 271) in which he considered all
three notochordal elements to belong to the same vertebra and argued that the
ventral element could not therefore be the homologue of the hypapophysis
4
B. G. GARDINER
( = intercentrum) of amnioites and accordingly called it the hypocentrum.
Gaudry also coined the term pleurocentrum for the paired lateral elements.
Finally in complete contrast to all other workers von Meyer (1857: 95)
concluded that the vertebr,al column of Archegosaurus was in an embryonic
condition and no centra were present.
Concurrent with these investigations into the nature of primitive tetrapod
vertebrae were similar studies on the structure and development of the vertebral
column of chondrichthyans and osteichthyan fishes. Thus Franque ( 1847) recognized that in the caudal region of Amia the centra were diplospondylous with
intercalated vertebrae similar to those of some sharks and rays. Schmidt (1892)
called these centra in the tail of Amia inter- and pleurocentra, while Hay
(1895: 6) considered them to be homologous with similar elements in the
Stegocephalia ( = embolomeres). In the meantime von Zittel (1887: 230, fig. 242)
redescribed the vertebral column of the fossil fish Eurycormus speciosus and
concluded (contrary to Wagner, 1861: 768) that though there were separate
pleuro- and hypocentra in the trunk region, caudally these elements had grown
round to form complete cylinders (alternating rings as in the tail of Amia).
Woodward (1895: 352; 1898: 108; fig. 77) agreed with Zittel’s interpretation
and concluded that Eurcor,mus was, in the form of its vertebral column,
intermediate between CuturuJ and Amia whereas Goodrich (1930: 39) noted that
fusion of the interdorsal anterior crescent with the posterior crescent or ring in
Eu?ycormus would give rise to the condition in the trunk of Amia. [Reexamination of the BMNH material of Eurycormus speciosus (and see
Patterson, 1973: fig. 15), including one acid prepared specimen, has shown that
the complete centra in the caudal region are no more than hemichordacentra:
that is half rings comprising calcifications of the notochordal sheath. Similar
hemicentra have recently been described in Caturus (Rosen et al., 1981).] Gadow
& Abbott (1895: 202) referred to the arch-bearing disc in Amia as the
precentrum and the archless disc as postcentrum and considered them to be
homologous with the pleurocentra and hypocentra in the tail of Eurycormus.
Gadow & Abbott further imagined that the postcentrum was formed by the
interdorsals and interventralri of the same sclerotome, while the precentrum was
formed by the basidorsals and basiventrals of the next previous sclerotome. This
analysis of the structure of the tail region of Amia led Gadow in the following
year (1896: 20) to embrace the conclusions of Owen, Cope, Gaudry and possibly
von Meyer concerning the homologies of the vertebral segments of the
rhachitomous amphibians (i.e. Archegosaurus and Trimerorhachis). Gadow
concluded that Gaudry (18713, 1883) had correctly considered the body of such
a vertebra to be composed of a hypocentrum and two pleurocentra and that
Cope (1878a,b,c,d; 1880; 1888) was also correct in homologizing the
hypocentrum ( = intercentrum) with the wedge bones of the amniota. Gadow
(1896: 21) reasoned that where the pleurocentra and hypocentra arcualia were
of equal size, as in the rhacliitomes, both entered into the composition of the
‘body’. In the embolomerous type of Cope (Cricotus) on the other hand, the
interventralia (one of Gadow & Abbott’s (1895) four pairs of arcualia and only
seen in the tail of Archegosaurus, and Chelysdosaurus ( = Cheliderpeton)) grew upwards
to form an archless disc while the basiventral ( = intercentrum or hypocentrum)
formed a similar disc whiclh carried the ribs and the tail haemapophyses.
Significantly, Gadow concluded that these embolomerous vertebrae bore a
GNATHOSTOME VERTEBRAE
5
perplexing resemblance to the double caudal vertebrae of Amia and yet had the
same composition as the typical vertebrae of all Recent amniotes. Other
embryological studies of this period include Froriep’s work on the chick (1883)
and the calf (1886), Gegenbaur (1862) on reptiles and amphibia, Howes &
Swinnerton (1901) on the tuatara, Goette (1875) and Goppert (1896) on
amphibians, Balfour & Parker (1882) on Lepisosteus and Budgett (1902) on
Polypterus. Schauinsland (1906) in his general survey and summary of much of
this work commented particularly on the similarity of the vertebral column of
rhachitomes, embolomeres and Amia and concluded that half vertebrae of this
sort did not occur in Recent Amphibia. He further suggested that the vertebral
column of embolomeres could be understood by a knowledge of the
development of the tail vertebrae of Amia, since both exhibit diplospondyly. In
contrast the rhachitome vertebral column could better be explained by fusions
and degenerations in the trunk centra of Amia.
Watson (1919a, 1926, 1929) seized on Schauinsland’s (1906) suggestion that
the vertebrae of rhachitomes resembled degenerate (embryonic) vertebrae of
Amia and concluded in contradistinction to Cope (1884: fig. 1) that the
embolomeres were the earliest, most primitive, most heavily ossified amphibians
and it was they that had given rise to the rhachitomes (1919a: 63; 1926: 250). He
reasoned (1926: 250) that “if the non arch part of the centrum in the
embolomeri failed to develop such a vertebra would at once become
quadripartite . . . as in tails of Archegosaurus and Chelidosaurus . . . and Amia”.
Goodrich (1930: 48) agreed with Gadow (1896) that the original four paired
arcualia seen in fishes could be identified in the Stegocephalia and like Cope
(1888) he assumed that the intercentrum ( = hypocentrum) had grown round
dorsally to form the anterior disc and the pleurocentra had fused and grown
round ventrally (or combined with the interventral) to form the posterior disc in
the embolomeres.
Romer (1933: 108) in his first edition of Vertebrate Paleontology nevertheless
agreed with Watson (1919a, 1926, 1929) in regard to the evolution of the
Amphibia and concluded that the primitive labyrinthodonts had the double
type of centrum (embolomerous) and that later both rings became incomplete
to give the rhachitomous type with the pleurocentra finally disappearing
altogether in the Triassic stereospondyls. I n later editions (cf. 1945: 130) Romer
changed his mind and considered the rhachitomous condition to be the
primitive one and like Albrecht (1883), Baur (1886a,c) Cope (1878b,c,d),
Dollo (1889), Gadow (1896), Goodrich ( 1930) and Hay (1895) imagined that
the pleurocentra corresponded to the true centra of higher classes. He further
imagined (like Watson) that the stereospondyls had lost the pleurocentra and
like Cope (1880, 1888) believed that in the embolomeres the intercentra and
pleurocentra had grown round to form complete discs, whereas in Seymouria the
intercentrum had remained as in rhachitomes, merely a wedge. Romer
(1947: 296) also noted the importance of the vertebral structure of Discosauriscus,
which he claimed was an ideal intermediate condition, showing the manner in
which the seymouriamorph and reptilian vertebral types had evolved from a
rhachitomous structure. Romer (1947, 1968: 74) embellished this later theory in
subsequent publications and believed that “numerous discoveries have tended to
prove its validity” particularly the structure of the vertebral column of the
ichthyostegids.
6
B. G . GARDINER
The persuasiveness of these arguments is summed up by the embryologist
Williams (1959a) who assumed that on palaeontological grounds the primary
centrum of amniotes is homologous with the pleurocentrum in labyrinthodont
amphibians. Williams then attempted to demonstrate the inapplicability of
Gadow’s (1896) theory to amphibian ontogeny by claiming that the centrum of
all tetrapods formed intersegmentally without recourse to arcualia. In other
words, formed by the union of the cranial half-sclerotome with the caudal halfsclerotome in front (each sclerotome being vertically and not obliquely divided
as suggested by Gadow clr Abbott (1895) in their theory of vertebral
development).
Panchen (1967) and Wake (1970) on the other hand considered the principal
centrum of amniotes to be the homologue of the whole compound centrum
( = intercentrum and pleurocentrum) of labyrinthodonts. Panchen ( 1963)
imagined that the oblique myoseptum moved posterodorsally in the
temnospondyls and anteroveintrally in the anthracosaurs. Panchen ( 1977a: 3 13)
further considered that the single trunk centrum of a reptile was homologous
with the pleurocentrum plus intercentrum of an anthracosaur ( = embolomeres),
but like Cope (1884) and Williams (1959a) concluded that the lepospondyl
(Nectridea, Aistopoda, Liissamphibia) centrum was a pleurocentrum
anatomically and ontogenetically homologous with that of amniotes. Panchen
(1977a: 291, 307) also concluded that Watson (1919a) had demonstrated
beyond doubt that the rhachitomous condition had given rise to the
stereospondylous vertebra by expansion of the crecentric intercentrum and the
loss of the pleurocentra. Nevertheless despite this confidence in Watson’s
(1919a) decision as to which of the two halves of the rhachitome vertebra had
expanded (or regressed), Panchen (1959) at first concluded that the single trunk
centrum of plagiosaurs was the pleurocentrum, but later (1967) changed his
mind and regarded it as intersegmental. Although these conclusions conflicted
with the knowledge that the. pleurocentra (interdorsals) and neural arches of
chondrichthyans, actinopterygians and dipnoans have a common ontogenetic
origin, only Andrews (1977: 285) seems to have noticed the discrepancy: “We
must therefore ask whether the ancestral crossopterygian pleurocentra were
ontogenetically derived from neural arch material along with the neural arches
(in which case the pleurocentrum must somehow have changed during
evolution to develop in the perichordal tube) or whether some other explanation
is possible”. Romer (1968: 84) meanwhile had concluded that in the plagiosaurs
“the intercentrum had triumphed”, and that plagiosaurs belonged with
Watson’s stereospondyls.
The impasse into which this kind of deliberation has led recent workers on
tetrapod vertebral structure has been neatly summed up by Panchen
(1977: 307) himself when hle emphasized what he considered to be “the
appalling (to the taxonomist) plasticity of early temnospondyl vertebrae”.
Inextricably bound up with tetrapod vertebral structure is the classification of
the Amphibia. As early as 1884 (p. 26, fig. 1) Cope used the structure of the
vertebral column to distinguish three main groups of batrachians; the
rhachitomes, the embolomeres and the stegocephalians ( = stereospondyls) . Von
Zittel (1895) gave a more expanded classification adding to the Amphibia the
Lepospondyli and Credner’s ( 1891) Phyllospondyli. Watson ( 1919a)
endeavoured to demonstrate. that the Rhachitomi and Stereospondyli were
GNATHOSTOME VERTEBRAE
7
merely grades, the former having given rise to the latter perhaps many times.
His view was endorsed by Save-Soderbergh (1935: 20) who maintained “that
there is a general evolutionary trend towards a simplification of the vertebrae, so
that in the Lower Triassic, various branches of the Labyrinthodonta
( = Rhachitomi), independently of one another became Stereospondyli”. Thus
Save-Soderbergh concluded that the division into Rhachitomi and
Stereospondyli was an arbitrary one and of no systematic value since both groups
were polyphyletic.
Watson (1919a; 1926; 1929) also regarded Cope’s (1884) Embolomeri as a
grade group, yet he concluded that it contained the most primitive amphibians
and subsequently divided it into the Loxommoideae and the
Anthracosauroideae ( 1929). Earlier Watson ( 1917) had argued (in common
with Williston, 1911, and Broili, 1904a,b) that the Permian fossil Seymouria was a
stem reptile, but in 1919b he suggested it formed a link between the
embolomeres and the more advanced Reptilia. This latter view was adopted by
Save-Soderbergh (1935: 107) who tried to show that Seymouria belonged “to the
same line of evolution as the Anthracosauria”, pointing out that the group
Anthracosauria-Seymouriamorpha had a different cranial roofing pattern to
that of the Ichthyostegalia-Labyrinthodontia.Save-Soderbergh (1935: 202)
placed the anthracosaurs ( = embolomeres) and Seyrnouria together with the
‘reptiles’, birds and mammals in the Superorder Reptiliomorpha.
Despite these confident assertions by Broili ( 1904a, b), Williston ( 191 1) ,
Watson (1917; 1919b), Goodrich (1930: 54), Romer (1933) and SaveSoderbergh (1935) as to the relationship of Seymouria, many authors continued
to regard it as an amphibian (Broom, 1922; Sushkin, 1925; Piveteau, 1926).
What was Seymouria then, an amphibian or a reptile? According to Romer
(1928, 1933: 123) and Colbert (1955: 110) the answer to this question lies in
whether Seymouria laid an amniote egg on land, or whether, like the frogs, it
returned to water. Since Seymouria could not furnish the answer (Romer,
1933: 123, 1945: 149) other fossils had to be found to produce a superficially
acceptable sequence which would fit the evolutionary doctrine (see Rosen et al.
1981; Gardiner, 1982). In 1942 Watson decided that a small branchiosaur
(Discosauriscus) originally described by Credner (1883: pl. 12, figs 1-1 1, 1890:
pl. 10, figs 8-10, pl. 11, 1891: figs 10, 27, 39, 44) and regarded as a rhachitome
(von Zittel & Woodward, 1932) was in point of fact a seymouriamorph, a
European contemporary of Seymouria. Romer (1947: 266) recognized that in
vertebral structure Discosauriscus* was more primitive than Seymouria and with its
large intercentra and pleurocentra unfused ventrally showed an ideal
*Credner (1883, 1890, 1891) noted that as in Brunchiosuurus the main elements of the vertebral column are
the stout neural arches with well developed, elongate transverse processes. He also observed that these arches
partially enclosed paired rings of bone which he termed pleurocentra (=chordacentra, see later under fossil
amphibians). In the tail region he found smaller, ventral crescents of bone supporting the haemal arches
( = basiventrals).
In the caudal region Credner considered the vertebrae to be distinctly rhachitomous. From an examination
of BMNH material of Discosuuriscus (R8554-61, presented by Spinar) I can confirm these observations,
but find it impossible to decide whether or not the fore limb possessed four or five digits (all other workers than
Spinar have figured just four). In other features (30-35 sclerotic segments, crenulated anterior edge of
interclavicle, anteroposteriorly elongated transverse processes, etc.) Discosuuriscus closely resembles
Branchiosuurus. The tabular also contacts the corner of the parietal as in some juvenile Brunchiosuurur, Micromelunerpeton and Leptorophus. Recently new discosauriscids have been described by Ivachenko (1981) and
Kusnetzov & Ivachenko (1981) but despite their insistence of a five fingered fore limb the evidence is
equivocal.
8
B. G . GARDINER
intermediate condition between the rhachitomes on one hand and Stymouria on
the other. Unfortunately this still left Stymouria (Romer, 1947: 281) on the
boundary between amphibians and reptiles. But the question was seemingly
finally settled when in 1952 Spinar described larval specimens of Discosauriscus
with gills; Romer (1966; 1968) was at last able to conclude that the
Seymouriamorpha belonged with the Amphibia. Unable however to dismiss his
long held view that Seymouria was the ideal protoreptilian, Romer (1968: 86)
suggested that “it is possible that the egg of Stymouria began its development in
amniote fashion . . . followed in the larva by a lapse into an aquatic phase”. As
Rosen et al. (1981) have pointed out, few transformations, however fantastic, are
forbidden by the Darwinian or Neo-Darwinian picture of the evolutionary
process! Romer (1968: 86) fhrther concluded that the Seymouriamorpha was a
side branch and that “the branching out of the reptile stock presumably took
place somewhat lower down the anthracosaurian line”. Panchen (1977a: 294)
though agreeing that the vertebrae of seymourians are closely comparable to
those of reptiles nevertheless followed Romer (1947 : 1968) in regarding them as
amphibians and resurrected Gadow’s ( 1896) term gastrocentrous to describe
their vertebrae. Romer (1966) grouped the Seymouriamorpha together with the
Embolomeri in the Order Anthracosauria, Panchen (197713) also grouped them
together, but within the Order Batrachosauria.
Further confusion in the classification of amphibians was introduced as a
result of Save-Soderbergh’s (1933: 118) and Holmgren’s (1933: 288) suggestion
that the tetrapods were polyphyletic, with the urodeles being related to
dipnoans. Jarvik ( 1942) advocated a diphyletic origin of tetrapods, but replaced
the dipnoans by the porolepiforms as urodele ancestors. More recently Rosen et
al. (1981) have concluded that the tetrapods are monophyletic (see also
Gaffney, 1979) and that the lungfishes might be their sister-group.
I n concluding this survey it should be noted that in recent years, in
compliance with evolutionary doctrine, there has been an increasing interest in
process rather than pattern. [n this way Parrington (1967: 272) tried to explain
the wide-spread occurrence of rhachitomous vertebrae by a functional analysis in
which he likened them to a geodetic framework of two pairs of girders wound on
to a cylindrical form. [Cope (1887: fig. 61) on the other hand likened the
rhachitomous vertebral column to the interspaces of his coat sleeve produced
when his arm was bent.] Such a column appeared to be designed to permit
twist. This sort of analysis allowed Parrington (1967: 275) to conclude that
Gephyrostegus may represent an intermediate condition between the
embolomerous forms and the seymouriamorphs. Panchen (1967, 1977a: 313) in
seeking adaptive reasons fix the presumed increasing importance of the
pleurocentrum in the amniotes believed it to be the result of the increasing
dominance of the load-bearing function over the locomotor compressionmember one. Yet contrariwise Parrington (1977: 400) concluded that large
intercentra, like those of ernbolomeres, allow a n unusual degree of lateral
flexure, thus extending the length of the stride. Panchen (1967), in contrast,
supposed that aquatic locomotion favoured the intercentrum and that an
oblique split in the (rhachitome) centrum separating intercentrum and
pleurocentrum moved posterodorsally in phylogeny until in a few stereospondyls
the pleurocentrum disappeared completely. That this kind of speculation has
failed to produce a coherent classification of the Amphibia is not surprising
GNATHOSTOME VERTEBRAE
9
(Rosen et al., 1981) though after 100 years of inquiry we could have hoped for
more progress than is implicit in Parrington’s (1967: 269) remark that “the
great variety of amphibian vertebrae has been used as a basis for their
taxonomy but it is not well understood, the embryology being unsatisfactory
and the palaeontology incomplete”.
ARCUALIA THEORY
Four pairs of arcualia are present in at least some segments in the
development of many selachians (squaloids, notidanoids, batoids, etc.,
Shute, 1972), holocephalians (Hydrolagus, Jollie, 1962; Callorhynchus, Remane,
1936), actinopterygians (Acipenser, Goodrich, 1909; Polyodon, Schauinsland,
1906; Amia, Hay, 1895; Goodrich, 1930), unborn juvenile Latimeria (Rosen et al.,
1981) and Neoceratodus (Remane, 1936). These arcualia are also retained in some
adult selachians (Chlamydoselachus, Goodey, 1910) and holocephalians
(Callorhynchus, Remane, 1936) and within the osteichthyans they are represented
by ossified or cartilaginous elements in at least part of the vertebral column.
Thus in actinopterygians they occur throughout the whole column in Acipenser
and Polyodon, in Pteronisculus (Nielsen, 1942: 216) they are restricted to the
abdominal region and in Caturus (Rosen et al., 1981) and Pholidophorus (Patterson,
1968) to the caudal region. In actinistians (Latimeria, Andrews, 1977) the full
complement is likewise confined to the caudal region, while in Neoceratodus the’
two dorsal pairs are only present in the caudal area whereas the two ventral
pairs are only found in the anterior trunk (Rosen et al., 1981). In tetrapods they
are present in the tail region of Archegosaurus and Chelydosaurus (Owen, 1861;
Fritsch, 1885; Meyer, 1957). From this evidence I conclude that Gadow &
Abbott (1895) were correct in assuming that four paired, cartilaginous elements
(arcualia) were primitively present even if they overestimated their importance
in the subsequent development of the definitive ‘centrum’.
Nevertheless separate interdorsals are missing in Polypterus, Lepisosteus,
Protopterus and from the development of teleosts and amniotes and from the
anterior trunk region of Neoceratodus and Latimeria; interdorsals are present in the
caudal region of the developing apodan Hypogeophis (Marcus & Blume, 1926)
and the urodele Ambystoma (Schauinsland, 1906) but elsewhere in the Amphibia
they are apparently wanting. Similarly separate interventrals are missing in
Polypterus, Lepisosteus, from the development of most telesosts, Lissamphibia and
amniotes and from the trunk of developing Amia and from Latimeria and all but
the anterior trunk of Neoceratodus, whereas in chondrichthyans they are often
irregularly developed or absent (particularly in the caudal region). I t is
impossible to decide in most of these cases whether the interbasalia have been
lost or have merely fused with the bases of their respective basalia, but in any
event little is to be gained by assuming one or the other. The embryological
evidence suggests that the interventrals are lost. Jarvik (1980) and Schauinsland
(1906), however, believe that in some instances the interbasalia fuse with the
basalia of the same segment, but in others such as Lepisosteus, teleosts and
tetrapods, the interbasalia have fused with the basalia of the metamere next in
front and the resulting vertebrae are therefore intrametameric! In many fossil
osteichthyans (including ichthyostegids, loxommatoids and temnospondyls)
only one ventral pair of arcualia is present ( = hypocentrum). This is the
10
B. G. GARDINER
condition in the anterior trunk region of the actinopterygians Osteorachis, Caturus
(Rosen el al., 1981) and Pholidophorus, the entire vertebral column of the
osteolepiforms Osteolepis (Andrews & Westoll, 1970b) and Eusthenopteron
(Andrews & Westoll, 19710a), the porolepiform Gl_yitolepis (Andrews &
Westoll, 1970b), the onychodontiform Onychodus, Ichthyostega and the majority of
temnospondyls (Eryops, Neldasaurus, Trimerorhachis, etc.) . In all of these forms
there is only one pair of ventral elements, the ventral vertebral arch, in each
segment. This element, normally single, has been called the hypocentrum in
fossil amphibians (Gaudry, 1878, 1883). The fact that the hypocentrum or
ventral vertebral arch arises from paired arcualia is witnessed by its double
nature in such diverse osteichthyans as Caturus, Eusthenopteron (thoracic region,
Jarvik, 1952), Glyptolepis and Osteolepis (Andrews & Westoll, 1970b), Rewana
(Howie, 1972), ‘Zatrachys (as Acanthostoma)’ (Steen, 1937), Amphibumus (Eaton,
1959), a lydekkerinid (Parrington, 1948) and the tail of Archegosaurus (Meyer,
1857). The interdorsals (pleurocentra) by contrast are nearly always paired
except in certain rhipidistians (Andrews & Westoll, 1970b: fig. 6) and Osteorachis
(this condition is the equivalent of Romer’s 1968, schizomeric stage). From this
comparison I conclude that the individual vertebral ossifications of
temnospondyls (neural arch, pleurocentrum and hypocentrum) are most
economically interpreted as endochondral ossifications in the cartilaginous
arcualia, homologous with tlhose in many fossil actinopterygians (Pteronisculus,
Osteorachis, Caturus, Pholidophorus) , osteolepiforms (Osteolepis, Eusthenopteron) and
porolepiforms (Glyptolepis).
Gadow & Abbott (1895: 190) further suggested that the arcualia were of
fundamental importance in the formation of centra. Accordingly in ganoids,
teleosts, amphibians and amniotes they believed that the centra were
“absolutely and directly dependent upon the existence of arcualia”, imagining
that the centra developed from the subsequent growth of these four pairs of
arcualia round the notochord and their eventual fusion into a single centrum,
outside the notochordal sheaths (perichordal centra) . In selachians,
holocephalians and dipnoans, in contrast, they maintained that cartilage cells
derived from the bases of the four pairs of arcualia invaded the primary
notochordal sheath to form segmentally arranged chordacentra.
DEVELOPMENT OF CENTRA
Initially the ontogenetic origins of the various types of vertebrate centra were
all seemingly succinctly explained by the arcualia theory (Gadow & Abbott,
1895; Gadow, 1896, 1933). Today this theory has been modified in various ways
(Higgins, 1923; Piiper, 1928; Goodrich, 1930; Schaeffer, 1967) and in some
instances (Williams, 1959a; Wake, 1970; Panchen, 1977a) it appears to have
been rejected altogether.
Any consideration of the formation of the centrum must begin with the origin
and structure of the notochordal sheath since it is here according to the theory
of Gadow & Abbott (1895) that the chordacentra in chondrichthyans and
dipnoans form. Moreover several authors had already tried to distinguish
between the notochordal vertebral centrum and the covering mass (cf. Hasse &
Schwark, 1873: 27; Hasse, 1882; Goette, 1897).
The notochord in most gnathostomes is surrounded by three distinct sheaths
GNATHOSTOME VERTEBRAE
11
(Kolliker, 1860): an inner epithelial sheath formed by peripheral notochordal
cells, a prominent elastic sheath which remains in apposition with it and an
outer, fibrous sheath which is sufficiently thick to maintain the turgor of the
notochord. The fibrous sheath is thick in chondrichthyans, osteichthyan fishes
(other than teleosts) and amniotes (Rathke, 1839: 3; Gegenbaur, 1862: 4), but
quite thin in teleosts and amphibians. The fibrous sheath is said to be delimited
externally by another elastic layer, the ‘elastica externa’ in chondrichthyans
(Klaatsch, 1893; Gadow & Abbott, 1895; Schauinsland, 1906; Goodrich, 1930),
osteichthyan fishes (Balfour & Parker, 1882; Goodrich, 1909, 1930; Mookerjee,
Ganguly & Brahma, 1954; Millot & Anthony, 1956; Franqois, 1966) and
amphibians (Hasse, 1892a; Schauinsland, 1906; Goodrich, 1930; Schmalhausen,
1968). Remane (1936) however doubted the presence of an inner elastic sheath
(‘elastica interna’) in chondrichthyans but believed there was an outer one
(‘elastica externa’). Shute (1972; 22) in contrast believed that there was no true
‘elastica externa’ in either chondrichthyans or osteichthyan fishes and that in
this respect they resembled amniotes. In my opinion there is some truth in
Shute’s observation, that the tenuous external limiting membrane of the fibrous
sheath in selachians bears little resemblance to the elastic sheath (‘elastica
interna’). Furthermore an ‘elastica externa’ is never found in amniotes (Rathke,
1839; Hasse, 1873; Schwark, 1873; Froriep, 1883; 1886; Howes & Swinnerton,
1901; Higgins, 1923) and in many selachians (Mustelus, Hasse, 1892b; Acanthus,
Gadow & Abbott, 1895; Callorhynchus, Scyllium, Schauinsland, 1906; Heterodontus,
de Beer, 1924) and osteichthyans (teleosts, Ramanujam, 1929; Gabriel, 1944;
Latimeria, Millott & Anthony, 1956; Protopterus, Goodrich, 1909) this sheath is
fenestrated, particularly in the region beneath the cartilaginous arcualia.
Besides these arguments as to the presence or absence of such layers as the
‘elastica externa’ there were other more fundamental arguments concerning the
origin of the notochordal sheaths themselves. Initially most authorities seemed
to agree that the sheaths were secreted by the notochordal epithelium (Kolliker,
1860; Klaatsch, 189313; Schauinsland, 1906; Goodrich, 1909) though Hasse
(1882; 1892a, b, 1893), Klaatsch (1893b) and Tretjakoff (1926a, b, 1927)
considered the ‘elastica externa’ to be genetically different from the chordal
sheath (e.g. mesoblastic) and Sensenig (1949) even thought the ‘elastica interna’
(his ‘elastica externa’) to be of sclerotomic origin. More recently Dawes
(1930: 119) observed that the mesenchymatous tissue around the notochord of
the mouse was histologically and genetically different from the sclerotogenous
tissue, while Shute (1972: 22) has argued that the centrum-forming ring of
chondrichthyans ( =fibrous layer) is the equivalent of the perichordal
skeletogenic layer of other vertebrates and by his definition, mesodermal. Most
authors (Gegenbaur, 1862; Froriep, 1883; Corning, 1891; Gadow & Abbott,
1895; Manner, 1899; Brunauer, 1910, etc.), like Shute, consider the amniote
perichordal skeletogenous layer to be derived from mesoblast tissue and
therefore of somitic origin. But since both mesoderm and notochord have a
similar embryonic origin (from chordamesodermal plate) and the notochord
behaves like a mesoderm derivative having the same type I1 collagen as
cartilage (Mathews, 1980), it seems pointless to argue whether or not the
mesenchyme of the sheath is chordal or mesodermal in origin, because it will
possess the same potentiality for skeletogenic development whichever its source.
It suffices to point out that there is an elastic membrane surrounding the
12
B G.GARD1NER
notochord in all gnathostomes and that on the outside of this membrane there is
a fibrous layer of varying thickness. This fibrous sheath at some stage during the
development of most gnathostomes and Petromyzon contains transverse fibres
which appear similar to those described in the notochordal sheath of
Branchiostoma by von Ebner (1895). It may or may not become skeletogenic.
Unfortunately the developmental origin of the notochordal sheaths greatly
influenced the early workers, who assumed that the centra could only form from
skeletogenic tissue, which by definition was strictly mesodermal in derivation
(viz. non-notochordal). Thus Hasse (1882) decided that the ‘elastica externa’ of
chondrichthyans was a product of the skeletogenous layer (viz. mesodermal)
and that it gave rise by proliferation to the inner layer of skeletogenic cells (in
the periphery of the fibrous sheath) that formed the selachian centrum.
However Hasse (1892b: pl. >!l) later proposed that cells immigrated into the
chordal sheath from the skeletogenous zone by breaking through the ‘elastica
externa’ from the outside, a view supported by Klaatsch (1893a). Using this sort
of evidence Gadow & Abbott (1895: 179) developed the chordacentra portion of
their arcualia theory. Gadow & Abbott imagined that instead of a wholesale
immigration of the sort proposed by Klaatsch (1893a), invasion was limited to
the bases of the arches (arcualia). Stating that in Acanthias, cells from the bases
of the arches “concentrate round the outside of the elastica and flatten against
it, some of them pass through the gaps, and others through the membrane itself’
they maintained that cartilage cells derived from the bases of the four pairs of
arcualia invaded the fibrous sheath to form segmentally arranged chordacentra.
Klaatsch (1895) concurred with Gadow & Abbott and later that year
demonstrated the invasion of the elastic sheath in Protopterus and Neoceratodus at
four points. In 1906 Schauirisland figured cartilage cells invading the fibrous
sheath in Callorhynchus and Sqyllium where as de Beer (1924) recorded the same
process in Heterodontus. Mookerjee & Ganguly (1951) on the other hand
considered that in selachians the skeletogenic cells not only infiltrated the
‘elastica externa’ from all directions but that they even migrated into the
‘elastica interna’. A similar invasion of the ‘elastica externa’ has been claimed
for teleosts by Ramanujam (1929) and Gabriel (1944). This unique process was
amplified by de Beer in 1937 (p. 37) as follows “while as a rule cartilage results
from a differentiation of rnesenchyme in situ, there are cases in which
chondrification follows a migration of cells; e.g. after invasion of the notochord
sheath in Selachi, Holocephali, Acipenseroidei and Dipnoi”. But the
notochordal sheath is never chondrified in holocephalians, acipenseroids or
Recent dipnoans, instead it contains calcified rings in Chimaera which are similar
in structure to the chordaceritra of teleosts (Franqois, 1966). Furthermore the
notochordal sheath of all other osteichthyan fishes (including several teleosts,
Franqois, 1966), amphibians (but see Tretjakoff, 1927) and amniotes does not
show this invasion. According to the theory of Gadow & Abbott this is because
the centrum in these groups is perichordal, that is, it forms outside the
notochordal sheaths which are then presumed to be constricted and even
obliterated in the adult (Goodrich, 1930: 13) by the expansion of the arcualia.
But a glance at any paper on amniote development (Froriep, 1883; 1886; von
Ebner, 1888; Goette, 1897; Manner, 1899; Howes & Swinnerton, 1901;
Brunauer, 1910; Higgins, 1923; Dawes, 1930) shows that early on, a perichordal
ring of fibrous tissue encloses the notochord and that skeletogenic material forms
GNATHOSTOME VERTEBRAE
13
within this perichordal tube and proceeds to constrict the notochord just as in
selachians. This perichordal tube in early development appears identical in form
and relationships in all vertebrate groups and it is difficult to see why it should
not be considered homologous. Goette (1897) had earlier suggested that the
primary centrum in amniotes formed quite independently of the arches
(autocentral) and this latter view has been accepted by most recent workers
(Remane, 1936; Devillers, 1954; Williams, 1959a; Wake, 1970, etc.). Even
Schauinsland (1906) and Piiper (1928) admitted the existence of a zone of
perichondrally arranged cells at the core of the centrum, and Mookerjee (1936)
has argued that the centrum in all vertebrates is of autocentral origin.
T h e situation was further complicated in amniotes when Remak ( 1851 : 52)
introduced the idea of resegmentation in which he maintained that the
definitive vertebra of the chick formed as a result of the recombination of
sclerotome halves. This led the majority of workers (von Ebner, 1888; Corning,
1891; Manner, 1899; Schauinsland, 1906; Brunauer, 1910; Higgins, 1923;
Piiper, 1928; Dawes, 1930; von Bochmann, 1937; Reiter, 1942; Sensenig, 1949,
etc.) to claim that the definitive centrum in amniotes, as well as its forerunner,
the perichordal tube, is formed from cells derived directly from the sclerotomes
and not from the notochordal sheath or from the arcualia. This perichordal tube
remains separate from the cartilaginous neural arches, as do the arcualia from
the centra in selachians, and a neurocentral suture may persist in the adult
(crocodiles and cervical vertebrae of some turtles).
O n the other hand in Polypterus, Lepisosteus, Amia, teleosts, Protopterus and
Recent amphibians the ossified centra form directly in membrane outside the
chordal sheaths but inside the arcualia (see below) and as such are truly
perichordal and quite different from the chordacentra found in selachians,
embryo teleosts and amniotes.
From all of these deliberations it appears that the perichordal, skeletogenic
tube in amniotes forms from cells which have migrated inwards from the
sclerotomes after resegmentation, whereas in selachians the skeletogenic layer
forms from either wholesale immigration (Klaatsch, 1893a; Mookerjee &
Ganguly, 1951) or by invasion a t four points (Gadow & Abbott, 1895) of the
notochordal sheaths by cells also derived from the sclerotomes (via the arcualia).
I n both cases it seems simpler to believe that the cartilage cells of the
perichordal sheath have arisen in situ from the mesenchyme surrounding the
‘elastica interna’. Whether this mesenchyme is notochordal or sclerotomic (or
neither!) is uncertain but again it is simpler to consider its origin to be the same
in both selachians and amniotes.
RESEGMENTATION
T h e original suggestion that the vertebra in amniotes was probably the
result of resegmentation was made by Remak (1851: 42). H e maintained that in
the chick the definitive vertebra formed by a recombination of sclerotome halves
with the arches coming from the posterior half of the sclerotome. Gegenbaur
(1862) also imagined that the vertebra in the chick was the result of
resegmentation, but in a somewhat different manner to that suggested by
Remak. Gegenbaur concluded that the transverse slit developed in the archless
portion of the chordal sheath separating a larger, anterior mass which remained
14
B. G. GARDINER
with the arch-bearing portion next in front, and a shorter, posterior mass
( =meniscus) which joined with the arch-bearing portion next behind.
Von Ebner (1888) and Corning (1891) agreed with Remak that the
sclerotomes in amniotes weire divided by a transverse split, and von Ebner
( 1888) further suggested that this split (intervertebral-Spalte) actually initiated
vertebral resegmentation and marked the position of the future intervertebral
joint. Like Remak (1851) they both thought that the halved sclerotomes
recombined with the adjoining halves of the neighbouring sclerotomes and thus
alternated with the myotomes. But in 1892, von Ebner agreed with Corning
that the intersclerotomic fissure was not the same as the future intervertebral
joint since it disappeared later in development to make room for the
intervertebral cartilage. Subsequently the presence of a sclerocoel has been
demonstrated in many amniotes (Manner, 1899, lizards and snakes; Brunauer,
1910, snakes; Schauinsland, 1900, 1903, 1906, Sphenodon; Williams, 1959b, Emys;
Higgins, 1923, alligator; Schultz, 1896, Piiper, 1928, birds; Schultz, 1896;
Reiter, 1942; Sensenig, 19438, mammals) and in apodans (Marcus & Blume,
1926; Marcus, 1937).
The sclerocoel or scleromic cleft communicates with the myocoel in apodans,
squamates and Sphenodon, but in most mammals the cavity is wanting. At first
the sclerotome halves do not differ in density, but later in apodans (Wake, 1970)
and many squamates (von Ebner, 1888; Corning, 1891; Manner, 1899;
Brunauer, 1910; Goodrich, ,I930) the caudal sclerotome half usually becomes
much denser and stains morle darkly than the cranial sclerotome half which is
invaded by the developing dorsal nerve ganglion. According to Remak’s ( 1851)
and von Ebner’s (1888) resegmentation theory each light anterior halfsclerotome then fuses with thie dark posterior half-sclerotome of the segment in
front (resegmentation of the sclerotome halves) to form the complete vertebral
segment and eventually the adult vertebra.* T h e vertebrae therefore alternate
with the myotomes. Today this is the text-book dogma (see also the reviews by
Goodrich, 1930; Remane, 1936; Devillers, 1954; Williams, 1959a; Wake &
Lawson, 1973), and Williams (1959a: 17) went as far as to claim that “no detail
in the ontogeny of vertebrae is better documented than resegmentation in
tetrapods”. But as Gadow & Abbott (1895: 186) pointed out “the necessity of
overlapping of contractile and passive segments has been met with before any
Amniota came into existence”, and that the splitting and fusion of the
sclerotomes proposed by Remak (1851) and von Ebner (1888) was a theoretical
necessity to explain the observed overlap of myomeres and sclerotomes. Gadow
& Abbott then proposed a different interpretation based on the observed
oblique orientation of the septa. They suggested that in all vertebrates the
ventral half of the sclerotome combined with the dorsal half of the sclerotome of
the segment next following. This recombination in their view also helped
explain the presence of the four pairs of arcualia in each complete segment.
Marcus & Blume (1928) have more recently interpreted the vertebrae of the
Apoda in a similar manner.
*In the alligator (Higgins, 1923: 376) this resegmentation is said to be more complex. First four pairs of cell
groups arise in each segment. The dorsal (neural) and ventral (haemal) anterior elements of each pair then
unite as do the two pairs of caudal eilements. Then the two part sclerotomes (scleromites?) of adjacent
segments fuse to form an entire segment. Four pairs of cartilages per segment have also been described in birds
iPiiper. 1928; Goodrich, 1930), these arc also said to fuse in a similar manner to the alligator.
GNATHOSTOME VERTEBRAE
15
Not surprisingly, many of the early embryologists refused to accept the whole
concept of resegmentation (His, 1868; Goette, 1875; Froriep, 1883, 1886) with
Goette (1875) and Schauinsland (1906) pointing out that the basic tetrapod
pattern comprised two centra per segment, not one (see below). I t is
interesting to record that Remak’s (1855: 41-43) original ideas on
resegmentation were based on squashes of the chick embryo, in which he
observed that early in development the connective tissue arch rudiments lay in
the same plane as the caudal portion of a pair of somites whereas in older
embryos the arches were carried on the cranial ends of the centra. Because
Remak assumed that the vertebrae in the chick arose from material derived
from the somatic series he found this anomaly difficult to understand and so
suggested a resegmentation had occured. Thus the original suggestion of
resegmentation in the amniotes was based on no more than supposed changes in
position of the neural arches which presumably had resulted from the use of
embryo squashes. Furthermore the splitting of the sclerotome so adequately
figured by von Ebner (1888), Corning (1891), Manner (1899) and Brunauer
(1910) shows that the sclerocoel may not only often form in the denser, darker
tissue (Manner, 1899), but also that it never penetrates to the chordal sheath,
there always being a t least three cell layers between its termination and the
‘elastica interna’. In the bird (Piiper, 1928: 289) where the sclerotomes are
delimited by a sclerotome membrane (sclerotheca) the sclerocoel can in no way
reach the perichordal mesenchyme. But here as in the human (Sensenig,
1949: 26) and in urodeles (Williams, 1959a) this perichordal mesenchyme ( =
fibrous layer) is said to be formed by cells which have migrated from the
ventromesial aspect of the sclerotome and through points of rupture of the
sclerotomic membrane in birds. Whether or not this perichordal mesenchyme is
sclerotomal or notochordal or merely general connective tissue of unknown
origin is of no great importance in this argument since, as Gadow & Abbott
(1895) have pointed out, nobody has ever observed a complete splitting into two
sclerotome halves and certainly nobody has ever witnessed their
recombination.* Further, as long as the vertebral column is in a membranous
(mesenchymatous) state there is no evidence of segmentation in it, and only
when cartilage makes its appearance does the true vertebral gap (intervertebral
split) come into being. The development of the axial skeleton is continuous and
early on an unsegmented strand of mesenchymatous, fibrous tissue surrounds
the notochord (the cover of the notochord, Rathke, 1839; the hautige
Wirbelsaule of Kolliker, 1860; the skeletogenous notochordal sheath of
Gegenbaur, 1862: 53).
I n selachians the perichordal tissue is uniform and unsegmented at a time
when the metamerism of the muscular and nervous system is perfect (Ridewood,
1899). I n this uniform substrate (perichordal blastema) the centra later arise as
adaptations of the connective tissue framework to the myomeres. Faced with this
sort of evidence some workers have tried to demonstrate an initial segmentation
in the perichordal tube itself. Accordingly Schauinsland ( 1900) contended that
this tube in Sphenodon showed distinct perichordal rings that coincided with the
*Shute (1972: 22) has used the bipartite nature of the ossification centres seen in whale embryo centra as
evidence of this fusion whereas the diplospondylic nature of the selachian tail has been used by Schauinsland
(1906) as evidence for the splitting of sclerotome halves.
16
B G GARDINER
sclerotomes. A similar situation was recorded in Larus and Struthio by Piiper
(1928). Both agreed, however, that the successive perichordal rings later fused
into a moniliform tube prior to cartilage formation. I t is worth reiterating that
the primordial vertebral column contains no centra, and the arches (arcualia)
are connected directly with a m unsegmented notochordal sheath ( = perichordal
or fibrous sheath). It is the arcualia which represent the fundamental organ in
Vertebral ontogeny and in time and space the centrum follows the arches.
That the vertebral arches form before the centra has been demonstrated in
selachians (Gadow & Abbott, 1895; Ridewood, 1899, 1921; van Wijhe, 1922; de
Beer, 1924; Goodrich, 1930) in Polypterus (Budgett, 1902), in Lepisosteus
(Gegenbaur, 1867; Balfour tk Parker, 1882), in Amia (Hay, 1895) in teleosts
(von Baer, 1835; Miiller, 1853; Lotz, 1864; Franqois, 1966) in Protopterus
(Mookerjee et al., 1954), in amphibia (Gegenbaur, 1862; Gadow, 1896;
Schauinsland, 1906; Goodrich, 1930), in crocodiles (Higgins, 1923), in birds
(Froriep, 1883) and in mammals (Froriep, 1886). I n mammals the picture is not
so clear cut because the first cartilage to form can occasionally be in the centrum
(calf-Froriep, 1886; Williams, 1959a: 1 1) .
Accepting that the arcualia are the primary part of the vertebral column
should we then expect thlem or their derivatives to show evidence of
resegmentation? Apparently so since most authorities believe that in amniotes
the neural and haemal arches arise from tissue supplied solely by the posterior
half-sclerotomes (Manner, 1899; Schauinsland, 1906; Goodrich, 1930; Remane,
1936; Devillers, 1954; Williams, 1959a) with Schauinsland (1906) and Piiper
(1928: 333) maintaining that in some cases both the half-sclerotomes may
contribute to the neural arch and that the principle of resegmentation holds true
not only in the centra but also in the arches. Evidence for this view includes the
development of the tail in Sphenodon and the Lacertilia (Gegenbaur, 1862;
Gadow, 1896; Goette, 1897; Schauinsland, 1906; Pratt, 1946; Etheridge, 1967;
Shute, 1972) where the plane of autotomy corresponds to the myosepta and
penetrates the vertebral column itself. This prompted Albrecht ( 1883), Manner
(1899), Schauinsland (1906) and Kerr (1919) to propose that the neural arches
like the centra had been developed from two half-sclerotomes and that the plane
of autotomy corresponded to the original division between the two halfsclerotomes which built up the vertebra. They suggested that the main neural
arch developed in the anterior half (the original caudal half of the sclerotome),
whereas the second weaker arch developed in the posterior half. But the fissure
differentiates late in development (Moffat & Bellairs, 1964) and the neural arch
part of it arises by the enlargement of a blood vessel foramina (Shute, 1972).
Furthermore where the caudal vertebrae possess two neural spines the vertical
plane of the autotomy fissure often passes in front of them both (Hoffstetter &
Gasc, 1969: fig. 52). As Goodrich (1930: 62) remarked this fissure “can hardly
be truly primitive since it certainly does not occur in early unspecialized
Reptiles and Amphibia”.
If we accept that the neural and haemal arches (basidorsals and basiventrals)
are homologous throughout the vertebrates it is difficult to see how they can be
formed as a result of resegmentation only in the amniotes, or conversely that
they form from the posterior Isclerotome-half of amniotes, urodeles and apodans,
but from some other source in all other vertebrates (but see Schauinsland, 1906;
and Goodrich, 1930: 18, who maintained that the arches in selachians were also
GNATHOSTOME VERTEBRAE
17
derived from the caudal half-sclerotome, a view supported by Shute, 1972).
How then do the arcualia form in lower vertebrates?
Van Wijhe (1922) has shown that in the axial column of Acanthias the
arcualia are represented by four continuous bands of cartilage along the
notochordal sheath, which subsequently break up into separate basalia and
interbasalia, and in the Devonian Cladoselache (Dean, 1909) a continuous band
of cartilage occupies the position of the haemal arches. Similar cartilaginous
bands have been described by de Beer (1924) in Heterodontus but de Beer
concluded that since all sclerotomic material is segmented then this continuity
must be secondary! Likewise the mesenchyme is concentrated into two dorsal
and two ventral tracts in Polyodon and Acipenser (Gadow & Abbott, 1895;
Schaeffer, 1967) that later differentiate into cartilaginous basalia and
interbasalia. Paired dorsal and ventral condensations in Protopterus (Mookerjee
et al., 1954) also give rise to the arcualia.
The arcualia themselves can be identified by the attachment of the myosepta,
their position relative to the arteries or their relationship to the ribs (ventral-see Rosen et al., 1981) and haemal arches. We find that in almost all
recorded cases the cartilaginous neural and haemal arches (basalia) arise from
mesenchyme (membrana reuniens) at the position of the myosepta. In
selachians (von Wijhe, 1922; de Beer, 1924, Goodrich, 1930) the arches form
between the dorsal root in front and the intersegmental vessels behind and the
myosepta pass in front of the basidorsals and behind the corresponding
basiventrals* (Shute, 1972). In Polypterus (Budgett, 1902; Daget, 1950),
Acipenser, Polyodon (Gadow & Abbott, 1895; Schaeffer, 1967), Amia (Hay, 1895;
Schaeffer, 1967), Lepisosteus (Balfour & Parker, 1882), teleosts (Lotz, 1864;
Klaatsch, 1893a; Ramanujam, 1929; Gabriel, 1944; Ganguly & Mitra, 1962;
Franqois, 1966) and Protopterus (paired dorsal and ventral condensations of
Mookerjee et al., 1954) mesenchymatous cell aggregations give rise to
chondrified neural and haemal arches at the myosepta. In larval Protopterus the
myosepta attach to the backs of the basiventrals and to the anterior margins of
the basidorsals (Shute, 1972) and similarly in amphibians. Thus in the larval
apodan Geotrypetes the myosepta attach to the front of the neural arch cartilages
and ribs while in Hypogeophis (Marcus & Blume, 1926; Marcus, 1937) they pass
just in front of the neural arch primordia. In urodeles (Gamble, 1922;
Schmalhausen, 1968; Shute, 1972) the myosepta are attached to the anterior
borders of the neural arches and to the backs of the haemal arches
(basiventrals). In anurans the myoseptem is also attached to the anterior border
of the neural arch (Shute, 1972), and in both Nutrix (Brunauer, 1910) and
Lacerta (Goodrich, 1930: fig. 69) the neural arch develops at the position of the
myosepta.
In the chick (Froriep, 1883; Piiper, 1928) and in the mammal (Froriep, 1886)
the primordial vertebral arches are composed of similar mesenchyme tissue to
that which covers the notochordal sheath, and the membranous forerunners of
the basidorsals pass laterally into the myosepta. These arches form in the
undifferentiated connective tissue in the axial interstices between the dorsal
nerve cord, the somitic series and the aorta. Therefore in all vertebrates the
*According to Gadow & Abbott (1885) the skeletogenous cells which go to make up the arcualia are
derived from the inner-halves of the ‘protovertebrae’ long before myotomes and sclerotomes as such have come
into existence.
L
18
B. G. GARDINER
basalia take up a position between consecutive myomeres and are connected
with the intersegmental myocommata. The interbasalia where they occur are
segmentally placed. But because of the persuasiveness of the resegmentation
theory most authorities (except Gadow & Abbott 1895, who maintained that
the basidorsal and interventral come from the dorsal half sclerotome-whereas
the interdorsal and basiveritral come from the ventral half sclerotome) still
believe that the arches and the rib rudiment are initiated in the hindermost part
of the primordial mesoderm segment (the caudal sclerotomite). Yet the evidence
points to an intersegmental origin for the arches and ribs (Hofmann, 1878;
Howes & Swinnerton, 1901) while the independence of the arches from the
centra is shown by the fact that in the tail region of many selachians (Ridewood,
1899) there are two (or more) sets of arches per segment, whereas in the tail of
Amia there are two centra per segment.
The only conclusions we can draw from this analysis is that firstly there is no
evidence of resegmentation either in the centrum or the arches and secondly
that there is no evidence that the basalia have been derived from the posterior
half sclerotome. The fact thitt the centra in amniotes lie in the same transverse
plane as the somitic boundaries and not the somites has been explained by
Froriep (1886) as being due to the obliquity of the primordial basalia with the
centra forming in the interval between two primordial vertebral arches.
Finally, if we accept the diplospondylic nature of the amniote vertebral
column then the resegmentation theory is redundant.
DIPLOSPONDYLY
Diplospondyly has long been recognized in the tail region of many selachians
and actinopterygians (Franclue, 1847; Goette, 1875, von Jhering, 1878; Hasse,
1879-1885) and as early as 1878 Jhering concluded that whereas the tails of
selachians and Amia were mostly diplospondylous the vertebral column in
higher vertebrates was always monospondylous. Jhering further believed that in
primitive selachians the whole vertebral column was diplospondylous and that
the monospondylous condition was secondary, introduced by a fusion of parts
from before backwards. Schmidt (1892) supported him in this view. Hasse
(1878-1885) recognized that in the caudal region of selachians there is a
complete reduplication of both arcualia and centra but in Amia only the centra
are duplicated and suggested that the terms diplospondyly and monospondyly
be confined to the state of the centra.
By 1891, Boulenger had concluded that the vertebrae of reptiles were
composed of a neural arch, centrum and intercentrum (hypapophyses,
subventral wedge bones, chlevrons) and this, and other evidence, convinced
Goette (1897) that not only were the centra in amniotes formed independently
of the arches (arcualia) but also that diplospondyly (Doppelwirbel) was the
basic gnathostome pattern. Schauinsland ( 1906), although recognizing that
diplospondyly was confined to the tail region in some fishes, nevertheless like
Goette attempted to prove that the tetrapod vertebra was based on the
diplospondylic condition rather than the monospondylic one proposed by
Jhering (1878). In so doing Schauinsland was attempting to reconcile the
conflicting claims of neontology (splitting of sclerotomes and resegmentation in
amniotes) and palaeontology (resemblances between embolomeres and Sphenodon
GNATHOSTOME VERTEBRAE
19
and the tails of Amia and selachians). Schauinsland used as evidence the double
centra of embolomeres and primitive tetrapods and the presumed double arches
in the tails of Ambystoma and lizards, as well as the division of the sclerocoel in
amniotes. But the double arches in the tails of embryo Ambystoma are normal
arcualia (basidorsals and interdorsals) and the double nature of the arches in
lizards is directly related to the plane of autotomy (see above) and only occurs
in the more posterior caudal vertebrae.
However, each body segment in primitive gnathostomes consists of a
myotome, sclerotome and neuromere. Consequently the relationships of the
vertebral arches (arcualia) and centra (where formed) may be defined by the
myomeres, myosepta, nerves and blood vessels. I t should therefore be an easy
matter to decide whether or not a vertebral column is diplospondylic or
monospond ylic.
I n euselachians there is normally one centrum per body segment, but in the
tail region there is frequently a doubling of the centra (Hasse, 1879-1885).
Diplospondyly always begins after the last rib-bearing centrum, in the region of
the cloaca, and there may or may not be a brief area of transition. This
doubling extends practically to the tip of the tail.
I n actinopterygians, dipnoans and amphibians there is normally only one
centrum per body segment. But diplospondyly does occur in the caudal region
of Amia (Franque, 1847; Hay, 1895), Caturus (Rosen et al., 1981) and other
holosteans, Australosomus (Nielsen, 1949) and Phol~do~horus(Patterson, 1968).
The diplospondyly in Caturus, Australosomus and Pholidophorus is confined to the
notochordal sheath (and in Caturus consists of hemicentra). In juvenile Lycoptera
(Saito, 1946) and Galkinia (Yakovlev, 1962) similar but complete
diplospondylous chordacentra are developed throughout the entire vertebral
column. I n the adult Lycoptera these paired chordacentra are fused into a single
centrum by the addition of membrane bone externally as in other teleosts (see
below). Complete diplospondyly has however been recognized in the fossil(?)
eel, Enchelion (Hay, 1913).
Diplospondyly is presumed to increase the flexibility in the tail region
(Ridewood, 1899; Schaeffer, 1967; Shute, 1972) and in vertebrates other than
amniotes its only recorded occurrence outside this area is in juvenile Lycoptera
and in Enchelion. From this we may deduce that diplospondyly is a
synapomorphy of amniotes.
As early as 1880 Cope recognized that the possession of a n atlas intercentrum
in reptiles meant that they had probably shared a common origin with the
embolomeres (regarded as diplospondylic fossil amphibians) and though both
Goette (1897) and Schauinsland (1906) realized that amniotes were essentially
diplospondylic many subsequent authors (e.g. Williams, 1959a) have disagreed
(but see Rockwell, Evans & Pheasant, 1938). Thus Cave (1980) maintained
that insectivore intercentra “are functional neomorphs developed to strengthen
the vertebral column during forceful limb activity”.
Yet in all living amniotes the atlas possesses two centra. The intercentrum,
which may fuse with the neural arch as in birds and mammals (other than
Thylacinus, Goodrich, 1930), and the centrum which may become closely
attached to, or fuse with, the centrum and intercentrum of the axis to form the
odontoid process. Moreover Sphenodon and some geckos retain wedge-shaped
bony intercentra throughout the whole column (Boulenger, 1891, 1893; Gadow,
20
B. G. GARDINER
1896). Elsewhere in the Lacertilia the intercentra are usually only recognizable
in the tail and neck where they persist as unpaired nodules or wedges (Osborn,
1900). In some lizards such as Varanus, Anguis and Heloderma the intercentra and
the chevrons gain attachment to the centrum in front, whereas in others such as
Tupinambis they connect with the centrum next behind, as in snakes (Boulenger,
1891).
In turtles, bony intercentra regularly occur in the first two or three cervicals
and in the tail where they may be paired or unpaired nodules (Gadow, 1896).
In crocodiles, bony intercentra only occur in the atlas, in the rest of the column
they are reduced to cartilaginous menisci. Similarly in birds, but in this group
the chevron bones often fuse with the centrum next behind (Remane, 1936: fig.
11 1). In mammals bony intercentra may be found not only in the atlas-axis and
tail regions but also in the thoracic and lumbar regions of Chrysochloris and the
lumbar regions of Erinaceus, Hylomys, Solenodon, Talpa, Mogura and Myogale
(Cave, 1980). Elsewhere as in birds and crocodiles the intercentra are reduced
to discs or menisci.
In mammals and birds a cartilaginous intercentrum (hypochordale Spange;
Froriep, 1883, 1886) develops in association with every centrum, but apart from
the atlas-axis complex and tail regions (Piiper, 1928) it disappears soon after
reaching the cartilaginous stage (except presumably from the thoracic and
lumbar regions of some insectivores) leaving a simple fibrocartilaginous
meniscus.
We may therefore conclude from this evidence that the veretebral column of
amniotes is fundamentally different from that in all other vertebrates in being
both dipospondylous throughout (Gardiner, 1982) and endochondrally ossified
(Rosen et al., 1981). It should also be emphasized that although most authorities
have considered the intercentra (wedge bones) to be homologous with the
chevron bones (Huxley, 187 X ; Boulenger, 1891, 1893; Gadow, 1896; Goodrich,
1930, etc.) which in turn represent arcualia (Gadow, 1896; Shute, 1972), the fact
that in Sphenodon, lizards, turtles and crocodiles the chevrons lie outside the
skeletogenous sheath and are attached proximally to cartilaginous intercentra
(see later under amniotes) rules out this homology.
VERTEBRAE AND PHYLOGENY
Chondrichthyan vertebrae
(i) Selachians
The notochord is surmounted throughout its length by paired cartilages
resting on the notochordal sheath, typically two for each segment in front of the
cloaca and four in the segments behind. A similar disposition of cartilages is
present beneath the notochord. All these cartilages rest upon the notochordal
sheath but are separated from it by the ‘elastica externa’.
The dorsal, posterior pair of cartilages or basidorsals initially lie in front of the
ventral spinal nerve roots, but eventually grow back to enclose them (van
Wijhe, 1922) except in Scyllium. The smaller, dorsal, anterior pair of cartilages
or interdorsals lie in front of the dorsal nerve roots and likewise grow back to
enclose these. Behind the cloaca where the paired cartilages are reduplicated,
21
GNATHOSTOME VERTEBRAE
only every other basidorsal and interdorsal is pierced respectively by ventral
and dorsal nerve roots.
The basidorsals are intersegmental in position and give rise to the neural
arches (Fig. 1A) whereas the smaller interdorsals lose their connection with the
notochordal sheath and may fuse above the neural canal as in Squalus. Of the
ventral cartilages the posterior pair or basiventrals are the larger and give rise to
the haemal arch or more anteriorly the rib articulation. The anterior, ventral
pair of cartilages or interventrals, like the interdorsals, soon lose their connection
with the fibrous sheath. They are the least regularly developed of all the
arcualia. An artery passes up behind each basiventral or every other basiventral
in the caudal region. The basalia are intersegmental and connected with the
myocommata, the interbasalia are segmentally placed.
Following the chondrification of the arcualia the unsegmented notochord
sheath begins to alter. The cells of the sheath first become flattened and fibrous
and then chondrification commences in the outer layers immediately beneath
the ‘elastica externa’. These cartilage cells appear to arise in situ (and are not the
result of immigration) and the initial observation of Hasse (1882) that they
arose by proliferation from the ‘elastica externa’ is concordant with the fact that
rca
bv
bv
I
D
iv
C
nt
Figure 1 . Vertebrae. A, Lamna, trunk region, partly cut longitudinally (from Goodrich, 1909); B,
Lamna, T. S. trunk vertebra (from Goodrich, 1909); C, Scylfium, T.S. anterior trunk, 35 mm embryo
(from Goodrich, 1930); D, Cetorhinus, T.S. trunk vertebra (from Ridewood, 1921). Heavy dots
indicate cartilage.
22
B. G . GARDINER
there is always an active perichondrium around the growing centrum (Kolliker,
1860; Hasse, 1892b; Ridewood, 1921).
According to most sources the ‘elastica externa’ gets buried deeper and deeper
in the calcified centrum arid eventually disappears (Kolliker, 1860; Hasse,
1892b; Gadow & Abbott, 1895; Ridewood, 1921; Goodrich, 1930). But it is surely
more parsimonious to consider as Shute (1972) has done that the ‘elastica
externa’ functions throughout development as a perichondrium, than to imagine
that first the notochordal sheath chondrifies by immigration through the
‘elastica externa’ which is then lost or abolished at the same time as a new
superficial perichondrium arises on the surface of the centrum.
At first chondrification of the sheath is continuous and uniform but soon rings
of hyaline cartilage differentiate (Klaatsch, 1893a). The rings thicken, lengthen
and develop into the centra while the intervening areas remain fibrous
(=intervertebral ligaments). The cartilage grows most rapidly at the ends of the
centrum and a series of typically biconcave centra result. Calcification of the
middle zone then ensues and the whole centrum comes to resemble a double
cone (Goette, 1875; Hasse, 1879-1885, 189213; Ridewood, 1921). I n the
meantime the outer zone of the centrum continues to grow in thickness by
proliferation of the superficial perichondrium ( = ‘elastica externa’) . Eventually
individual tesserae with a perichondral cap of bone develop peripherally at the
boundary between the cartilage and perichondrium.
In some selachians (Pristis, Mustelus, Hexanchus, Lamna) the perichondria of the
arcualia are very active, and the basidorsals and basiventrals elongate,
consequently the activity of the superficial, central perichondrium is restricted
to the four points between the expanded bases of the arches. The result is four
wedge-shaped masses of cartilage (Periostale keile of Hasse, 1892b) which
emtomb the elongated arch bases (Fig. lB, D). The arches nevertheless remain
separate from the centrum and can be pulled out of it like fingers from a glove.
The arches are always embedded to a greater or lesser extent in the centra in all
euselachians (fossil and living) but, unlike the centra, the arches are never
calcified apart from an outer cover of tesserae of calcified cartilage, and they
always remain separate from the centra.
The different types of calcification seen in selachian centra are characteristic
and Hasse (1879-1885) has used them as a basis for classification.
(ii) Holocephalians
The holocephalians closely resemble the selachians in having four pairs of
arcualia per segment and in doubling this number in the caudal region. They
differ however in having a persistent and unconstricted notochord (Hasse,
1879-1885; Klaatsch, 1893-1895) and in the irregularity of the arcualia. Thus
in Hydrolagus (Jollie, 1962) there are sometimes two ventral pairs of arcualia per
segment and sometimes only one enlarged ventral pair extending a segment
and a half. The interdorsal lies behind the ventral nerve root whereas the dorsal
root is at its apex (Fig. 2A, B).
Immediately behind the skull in Chimaera and Hydrolagus there is a rigid,
continuous chordal cartilage, surrounding the nerve cord and notochord and
supporting the dorsal fin and spine.
Calcified rings form in the fibrous sheath of Chimaera and Hydrolagus and
alternate with ringless portions. These are much more numerous than the
23
GNATHOSTOME VERTEBRAE
A
B
id
nts
D
C
bd
id
nts
bv
Hasse., 1882);
Figure 2. Vertebrae
Vertebrae. A, Chimaera, trunk region (from
(frorm Hasse,
1882), B, Chimaera,
Chemaera, T.S.
T S trunk (from
Schauinsland,
1906), D, Acipenser,
Actpenser, T.S.
T S.
Hasse, 1882);
1882), C , Polyodon, trunk-caudal transition (from Sc
:hauinsland, 1906);
1906) Heavy
cartilage
trunk, schematic (from Schauninsland, 1906).
Heabiy dots in A, B and D indicate cartilage.
segments, up to six per arch in Chimaera, fewer in Hydrolagus, but the number
varies in different parts of the trunk, mostly four or less. These rings gradually
disappear tailwards and in the whip-like end of the tail, the arcualia form a
uniform mass of cartilage.
(iii) Fossil chondrichthyans
No centra have been recorded in Palaeozoic selachians although there is some
evidence of chondrification of the notochordal sheath in xenacanths.
Notochordal calcifications similar to those in Rhinochimaera (six per segment)
and other Recent chimaeroids are found in several fossil holocephalians such as
Ischyodus (two to three per segment) and Squaloraja (four to five per segment). In
this latter genus (Hasse, 1882) the thick, ring-like calcifications extend further
into the notochord than in living chimaeroids and similarly there is no constant
relationship between these calcifications and the arcualia (Patterson, 1965).
Traces of notochordal calcifications have also been recorded in Myriacanthus,
Metopacanthus and Acanthorhina (Patterson, 1965) while in Chondrenchelys (MoyThomas, 1935) there is a single, ring-like notochordal calcification, or centrum,
in each segment. The centra in Chondrenchelys are of a fibrous nature, devoid of
bone cells and each has a neural arch and in the caudal region a haemal arch
24
B. G. GARDINER
covered in prismatic calcified cartilage (BMNH P.4085, P. 18058). These centra
are similar in structure to the calcifications of the notochord in Recent
chimaeroids (Patterson, 196ij).
From this we may deduce that chordacentra have formed on at least two
occasions within the chondrichthyans, once in chimaeroids where they are nonsegmental and once in Chondrenchelys. Cartilaginous centra have arisen only once
in euselachians.
Osteichthyan jish vertebrae
(i) Polypterus
Only a single pair of cartilaginous arcualia occur above and below the
notochord in Polypterus and Erpetoichthys. These are widely spaced, rest directly
on the notochordal sheath and give rise to the neural and haemal arches.
Interbasalia are absent (Buclgett, 1902; Daget, 1950).
Anteriorly and throughout the abdominal region there is in addition a lateral
pair of cartilages in each segment (Fig. 3A, B). Both Goodrich (1930) and
Schaeffer (1967) believed that these ‘lateral processes’ were formed by a
subdivision of the basiventrals. But they form a series in continuity with the
dorsal ribs (in the horizontal septum) similar to that formed by the ‘ventral
cartilages’ ( = basiventrals) and ventral ribs in the wall of the coelom. Dorsal ribs
are only found in polypterids and teleosts (Rosen et al., 1981), but lateral
cartilages are confined to polypterids.
A single layer of cartilage-like cells surrounds the ‘elastica interna’ and
represents the chordal sheath. Connective tissue continuous with the
intersegmental septa bounds the chordal sheath and the neural and haemal
arches. Initially a thin sheet of bone differentiates in the connective tissue to
form a thin hourglass-shaped centrum which expands widely at both ends. This
membrane-bone centrum is continuous with the thin sheet of membrane bone
surrounding the neural and haemal arches. Eventually the arch cartilages and
lateral cartilages are replaced by bone.
In summary, the vertebra of Polypterus is formed mainly of membrane bone
outside the chordal sheath and arcualia. Its centrum is correctly considered
perichordal.
(ii) Lepisosteus
Lepisosteus resembles Polypterus in possessing a single pair of cartilaginous
basalia above and below the notochord (Gegenbaur, 1867; Balfour & Parker,
1882; Schauinsland, 1906). ‘The haemal arches however are presumed to arise
from a continuous cartilaginous bar as in Acanthias and Heterodontus.
The notochord has a thick fibrous investment ( =cuticular sheath of Balfour
& Parker, 1882) which is bounded externally by an ‘elastica externa’ upon
which the arches rest (Fig. 3C). Cartilaginous rings differentiate
intersegmentally in this fibrous sheath. Gegenbaur (1867), Balfour & Parker
(1882), and Gadow & Abbott (1895) concluded that these rings originate from
the spreading of the arch bases whereas Schaeffer (1967) thought they may
represent fused interbasalia. But these rings are always eventually completely
separate from the arches and consist mainly of fibrocartilage which is
histologically very distinct from the cartilage of the arch bases (Balfour &
GNATHOSTOME VERTEBRAE
25
A
rnb
- nts
bv
C
Figure 3. Vertebrae. A, Polyptern, T.S. trunk early embryo; B, Polypterur, T.S. trunk late embryo
(A, B from Budgett, 1902); C, Lepisosteus, T.S. trunk, future vertebral region, 5.5 mm; D, Lepisosteus,
T.S. trunk, future intervertebral region 5.5 mm (C, D from Balfour & Parker, 1882); E, Lepisosteus,
trunk vertebra from in front F, Lepisosteus, trunk region; (E, F from Goodrich, 1909). Heavy dots in
A, C and D indicate cartilage.
Parker, 1882), I t is simpler to suppose that these cartilaginous rings have arisen
in situ in the notochordal sheath independently of the arches (see for example
Shute, 1972).
Ossification is said to begin partly in the perichondrium and partly in the
connective tissue investing the arches and spreads rapidly around the notochord
within the connective tissues thereby uniting neural and haemal arches in a
single ossification.
I n the meanwhile the intervertebral rings of cartilage become thickened
26
B. G. GARDINER
medially and constrict the notochord. They then become divided transversely
into two parts that form the adjacent faces of contiguous vertebrae. The
intervertebral cartilages subsequently ossify to form the opisthocoelous joint
(Fig. 3E, F).
Thus the development of the vertebrae of Lepisosteus is similar to that of
Polypterus except for the presence of intervertebral rings of cartilage which give
rise to the opisthocoelous articulation. The vertebrae are formed chiefly of
membrane bone and only the ends of the centrum and cores of the arches are
formed of cartilage bone. The centrum is therefore best considered perichordal.
(iii) Amia
The development of the vertebrae in Amia is well documented (Goette, 1875;
Hay, 1895; Gadow & Abbott, 1895; Schauinsland, 1906; Goodrich, 1930;
Shute, 1972). There are four pairs of cartilaginous arcualia per segment in the
caudal region: the basidorsals which meet above the dorsal ligament, the
basiventrals which meet below the caudal vein, and interdorsals and
interventrals which lie behind the intersegmental artery and are separated from
their respective basalia.
Separate interventrals are absent from the anterior caudal and abdominal
regions while the interdorsals in this area become wedged beneath the
basidorsals which succeed them.
The notochord develops a thick fibrous sheath ( = cuticular sheath of Hay,
1895) bounded externally by a distinct ‘elastica externa’. The arch bases rest on
this sheath which persists even in adult life.
Ossification begins in the connective tissue and first appears in the angles
between the arches and the notochord and the interbasalia and the notochord
(Fig. 4A, B). Bone spreads rapidly round the notochord and over the neural
arches, basiventrals and interbasalia. Where it is in connection with the
cartilages of the arches the bone is perichondral in origin.
In the posterior caudal region, which is diplospondylous (Fig. 4C), the
membrane bone postcentrum incorporates the neural and haemal arches
whereas the precentrum includes only the interbasalia. The myocommata insert
on the arch-bearing centra. As growth continues the centrum increases in size by
the addition of cancellous membrane bone. Elongation of the interdorsals and
interventrals accompanies this ossification in the precentrum and there is a
corresponding elongation of the arches in the postcentrum. T h e bases of these
cartilaginous elements remain embedded in the membrane bone centra (much
as the arcualia in Lamna remain embedded in the cartilaginous centrum) and
stretch outwards from the notochordal sheath (Fig. 4B).
As the centrum increases in diameter in the trunk region only the haemal
arch (basiventral) and the interdorsals elongate and the neural arches remain
on the perimeter of the centrum much as to the interdorsals and interventrals in
selachians. The basiventrals in this region grow out laterally as well as ventrally.
This lateral projection in the trunk region forms the parapophysis
[ = basapophysis of Remane, 1936) which articulates with the ventral rib.
Eventually all the parts of the cartilaginous basalia and interbasalia which lie
within the centra ossify as cartilage bone.
Amia differs from both Polypterus and Lepisosteus in possessing interbasalia but
its ossification pattern is similar. The vertebrae of Amia are formed mainly of
GNATHOSTOME VERTEBRAE
mb
27
bv
iv
Figure 4.Vertebrae. A, Amia, T.S. abdominal vertebra, 27 mm; B, Amia, T.S. abdominal vertebra,
125 mm (A, B from Hay, 1895 and Schaeffer, 1967); C, Amia, early embryo showing a
monospondylic centrum interspersed between two diplospondylic centra (from Schauinsland,
1906). Heavy dots indicate cartilage.
membrane bone which is deposited outside the chordal sheath and in the
perichondria of the arcualia. Although its centrum is rightly considered
perichordal it does include the cartilage bone bases of the arcualia.
(iv) Teleosts
The development of the teleost vertebra has been a subject for study for
almost 150 years. As long ago as 1835, von Baer concluded that in the
28
B. G. GARDINER
Cyprinidae no part of the vertebra is derived from the notochord or its sheath,
while Muller (1853) demonstrated that the centrum formed independently of
the arches. Today most authorities agree with these conclusions and consider the
teleost centrum to be made up of membrane bone.
At the outset a single pair of cartilaginous arcualia develop above and below
the notochord. These give rise to the chondrified neural and haemal arches at
the myosepta as in Lepisosteus, Polypterus and Amia. I n some forms however
interventrals also occur anteriorly as in Salmo (Fig. 5C). The notochordal sheath
thickens and becomes fibrous and shows no evidence of metamerism. Then in
certain genera such as Clupea, Esox and Salmo (FranCois, 1966) the sheath
calcifies to form thin chordacentra. These are eventually replaced by the
definitive, membrane bone, centra. Chordacentra are formed in such diverse
(Nielsen,
1949), aspidorhynchids,
actinopterygians
as Auslralosomus
pholidophorids, pachycormids, pleuropholids, galkiniids, catervariolids,
‘Tetraganolepis (Patterson, 1973), Caturus and Lycoptera (Saito, 1936) where they
often calcify from dorsal and ventral crescents.
In primitive teleosts the arches ossify as cartilage bone and remain
independent of the centra (Patterson, 1977a). Ossification usually begins in the
C
D
no or bd
Figure 5. Vertebrae. A, Griphognuthus, trunk region (from Rosen et al., 1981); B, Osteorachis, trunk
region, oblique lateral and posterior views (from Goodrich. 1909); C, Salmo, abdominal region, 25
m m (from Schauinsland, 1906); D, Scomber, trunk vertebra (from Schauinsland, 1906). Heavy dots
in C indicate cartilage.
GNATHOSTOME VERTEBRAE
29
perichondrium of the arch bases and at points of contact of the lower arches
with the notochordal sheath (Lotz, 1864). Ossification then spreads rapidly
around the notochord in the connective tissue, and arch and centrum become
continuous in more advanced teleosts. The centrum thickens rapidly outwards,
forming radiating bony laminae. The arches may be embedded in the centrum
and may persist as four tracts of cartilage running outwards through the bony
centrum (e.g. Esox) much as in chondrichthyans, or they may be restricted to
the periphery.
In many teleosts the arches themselves develop extensive outgrowths of
membrane bone, especially in the caudal region (Patterson, 1977a) and in other
more advanced forms the arches may ossify without cartilage preformation
either in part of the column or throughout the entire column (Faruqui, 1935;
Emilianov, 1939). In these latter instances the vertebra is a membrane bone.
In most teleosts the centra are amphicoelous and strongly constrict the
notochord and fibrous sheath (Fig. 5D). Intervertebrally the fibrous sheath gives
rise to the intervertebral ligament, but in the blenny Andamia it forms a ring of
cartilage (Ganguly & Matra, 1962) which is divided as in Lepisosteus by a
transverse cavity: these cartilages fuse to the adjacent centra and ossify to form
an opisthocoelous joint.
Special membrane bone intervertebral articulations are also formed in many
teleosts. Those on the centra are called ‘zygapophyses’.
In general the development of the teleost vertebra is very similar to that of
other actinopterygians. Ossification commences in the connective tissue
bounding the surface of the arcualia and spreads over the surface of the chordal
sheath. The first shreds of bone are completely cell-less and rapidly form a
homogeneous layer round the surface of the centrum. The bone gradually
increases in thickness and becomes cellular and an irregular network of bony
trabeculae spreads outwards to form the definitive centrum. At the same time
the arches usually become completely bony following vascularization and
destruction of the cartilaginous core.
Teleosts, like Polypterus and Lepisosteus, generally lack interbasalia. The vertebrae
are formed chiefly of membrane bone and only the ends of the centrum in such
forms as the blenny and the cores of the arches in primitive members are formed
of cartilage bone. The centrum is perichordal.
(v) Dipnoans
In the Dipnoi the notochord is persistent and unconstricted. It is surrounded
by a thick fibrous sheath similar to that in chondrichthyans, Lepisosteus, Amia,
Latimeria and amniotes and is delimited externally by a stiff ‘elastica externa’
(Klaatsch, 1895; Goodrich, 1909; Mookerjee et al., 1954). The fibrous sheath
may become semicartilaginous in Neocerutodus (Shute, 1972) or even partly
calcified.
There is usually a single pair of cartilaginous arcualia above and below the
notochord. In Neoceratodus (Goodrich, 1930) and Protopterus (Mookerjee et al.,
1954) these have particularily enlarged bases ( = perichordal cartilages of
Mookerjee et ul., 1954). The basalia chondrify to give rise to the neural and
haemal arches at the myosepta. In Neocerutodus there are additionally
interventrals in the anterior thoracic region and interdorsals in the tail (Rosen et
al., 1981).
30
B. G. GARDINER
The enlarged bases of the neural and haemal arches (only the neural arch
bases are enlarged in Lepidosiren) rest on the notochordal sheath and usually
remain cartilaginous, but the perichondrium around the narrow distal parts of
the arches always ossifies.
I n Protopterus Mookerjee et al. (1954) have described the formation of thin ring
centra. In the specimens they studied membrane bone developed in the
connective tissues covering the notochordal sheath and spread over the enlarged
arch bases. The arch bases subsequently ossified as cartilage bone and were
enclosed within the centra.
Thus the centrum in Protopterus as in all living actinopterygians is formed
perichordally. The membrane bone shell however encloses a higher content of
cartilage bone than in most actinopterygians.
(vi) Fossil osteichthyans
The earliest centra found in actinopterygians comprise thin calcifications of the
sheath of the notochord (chordacentra). They occur in several palaeoniscids
including Haplolepis (Baum & Lund, 1974) from the Upper Carboniferous and
Turseodus (Schaeffer, 1967) and Pygopterus (Aldinger, 1937) both from the
Triassic. In Turseodus there are only dorsal and ventral hemicentra as in Caturus
and Eurycormus speciosus Wagner (Patterson, 1973) but in Haplolepis and the tail
of Pygopterus there are complete ring centra. I n Haplolepis, as in Pholidophorus,
Pleuropholis and pachycormids, these ring centra are developed from the dorsal
and ventral hemicentra.
Also in the Triassic chordacentra appear to have been independently acquired
by the pholidopleurids. Thus Australosomus (Nielsen, 1949) has thin ring centra
throughout the column. These are overlain by endochondrally ossified neural
and haemal arches and interdorsals. I n the diplospondylic caudal region
interventrals are also present and like the interdorsals in this area are separated
from their respective neural and haemal arches. Macroaethes is similarly calcified
except that contrary to Wade (1935: fig. 39) it does not possess diplospondylous
caudal rings (Patterson, 1973; see BMNH P. 15778).
By the end of the Jurassic many actinopterygians possessed calcifications of the
notochordal sheath including hemichordacentra in Furo philpotae (Agassiz) and
Caturus (Patterson, 1973; Rosen el al., 1981) and complete ring centra in
pholidophorids,
archaeomaenids,
some
pachycormids,
pleuropholids,
catervariolids, Galkinia and Ichthyokentema (see Patterson, 1973). I n most of these
fishes the hemichordacentra are dark, coarsely fibrous and overlain by
endochondral neural and haemal arches, but in Caturus (Rosen et al., 1981) there
may also be interdorsals and interventrals. Today the notochordal sheath is still
involved in the early ontogenetic stages of the centra of primitive living teleosts
such as Salmo (FranGois, 1966). If our phylogenies are correct (Patterson, 1973,
1977b; Rosen et al., 1981) then chordacentra must have arisen on at least three
occasions within the actinopterygians: once within the palaeoniscids (Haplolepis,
Pygopterus and Turseodus); once within the pholidopleurids; and once in the
Halecostomi
(caturids, oligopleurids,
pachycormids,
aspidorhynchids,
catervariolids, Galkinia, pleuropholids, Ichthyokentema. archaeomaenids and
pholidophorids). In section the chordacentrum appears as an amorphous mass
in Pholidophorus and Belonostornus.
GNATHOSTOME VERTEBRAE
31
By the Upper Jurassic several groups of actinopterygians had acquired much
more substantial centra in the form of stout perichordal cylinders of membrane
bone. Thus annular centra are found in the Upper Jurassic caturids Furo
microlepidotus (Agassiz), Neorhombolepis and Macrepistius (Schaeffer, 1960), both
Macrepistius and Neorhombolepis valdensis (Woodward) show caudal diplospondyly
(Patterson, 1973). Interestingly the well developed and massive crescentic
hemicentra of the Lower Liassic Osteorachzs (Fig. 5B) appear to have substantial
additions of perichordal, membrane bone on their inner surfaces and are not
therefore ossifications of the sheath of the notochord as supposed by Woodward
( 1895). This perichordal membrane bone has a characteristic woven
appearance seen elsewhere in the perichordal centra of Furo, Polypterus and
Megalichthys. By the end of the Kimmeridgian several other actinopterygians had
also gained membrane bone centra including the macrosemiids,
aspidorhynchids and oligopleurids.
The macrosemiid genera possessing perichordal centra include Macrosemius,
Ophiopsus, Histonotus, Notogogus and Enchelyolepis (Bartram, 1977). In the latter
genus however these rings give way to crescentic wedges (hemicentra?) in the
tail (cf. E. andrewsi (Woodward), BMNH P.603).
That the ring centra in the aspidorhynchids are truly perichordal can be
verified in Belonostomus (see BMNH P.2 1958) where distinct chordacentra are
enclosed within stout membrane bone rings.
Finally the centra of most of the Oligopleuridae are thoroughly ossified in
membrane bone, without diplospondyly and probably preceded ontogenetically
by hemichordacentra (see Callopterus, Zittel, 1887: fig. 243). Accordingly stout
perichordal vertebrae are found in Ionoscopus (Patterson, 1973: fig. 24, see
BMNH P.449 1 1), Spathiurus and Oligopleurus. Again if our phylogenies are
correct, then like chordacentra, perichordal centra must also have developed on
several different occasions within the actinopterygians. Perichordal, membrane
bone centra have developed at least five times (Polypterus, Lepisosteus, Amia,
aspidorhynchids and teleosts) and possibly as many as seven (oligopleurids and
macrosemiids) . Certainly the vertebrae of Polypterus, Lepisosteus, Amia and teleosts
develop in quite different ways (Balfour & Parker, 1882; Hay, 1895; Budgett,
1902; Daget, 1950; Franqois, 1966).
Within the so called rhipidistians complete annular centra are found in the
Lower Carboniferous genera Rhizodopsis, Megalichthys and Strepsodus and the
presumed Permian relative of Megalichthys, Ectosteorhachis. In Rhizodopsis,
Megalichthys and Strepsodus the centra are perichordal and made up of a similar
reticular, woven bone to that seen in Furo while from the published descriptions
of Ectosteorhachis centra (Cope, 1891; Thomson & Vaughn, 1968) there is every
reason to believe that they are likewise perichordal membrane bone.
I n Megalichthys (see BMNH P.7861, P.7863, P.46585/6) and Rhizodopsis
(Hunterian Museum V.2540) neural and haemal arches are fused to the
centra and in Ectosteorhachis the neural arches are said to be attached. In
Strepsodus where the centra are more markedly hourglass-shaped and the
notochord space severely restricted the arches are not apparently fused with the
centra.
I n all of these genera the centra are simple, ring-shaped and resemble the
centra of Furo and Amia. If the published phylogenies and classifications of the
rhipidistians are to be believed then perichordal centra have evolved at least
32
B. G . GARDINER
twice within this assemblage, once in the osteolepids (Megalichthys,
Ectosteorhachis) and once in the rhizodontids (Rhizodopsis, Strepsodus).
Within the dipnoans are found the earliest completely ossified centra. These
occur in the Devonian rhynchodipterids Griphognuthus (Miles, 1977),
Rhynchodipterus (Save-Soderbergh, 1937; Jarvik, 1952; Lehman, 1959, 1966) and
Soederberghiu (Lehman, 1959, 1966) and in Chirodipterus (Miles, 1977) where they
are spool-shaped and presumed to be made up of cartilage bone (Fig. 5A). In
Griphognuthus and Chirodipterus there is also a cranial centrum (Miles, 1977) and
according to Schultze (1970) resorption of calcified cartilage and the subsequent
deposition of bony tissue in the vertebrae of Griphognuthus was identical with the
formation of bony tissue in uncalcified cartilage in Tetrapoda. Centra are also
said to occur in two other Devonian forms, Jarvikia (Lehman, 1959, 1966) and
Dipterus (Pander, 1858; Egerton, 1861; Jarvik, 1952). I n Jarvikia the centra
Uarvik, 1952; Lehman, 1959, 1966) resemble those of the rhynchodipterids and
Chirodipterus, but the minute, laterally placed holes (two dorsal and one ventral)
in the former are far too small to have contained arcualia (cf. sharks and Arniu)
as implied by Jarvik (1952, figs 17, 18, 19) and are more likely to be nutritive
foramina as in many snakes and amphisbaenids. Transverse sections of
Griphognuthus and Chirodipterus failed to reveal any such pockets or lacunae, and
in both genera the neural arches sit between adjacent centra (Rosen et al., 1981:
fig. 54A; and BMNH specimens) while the haemal arches are fused to the
centra. The centra in Dipterus on the other hand are so poorly known that some
authorities have doubted their existence (Andrews & Westoll, 1970b). Centra
are absent in all known post-Devonian dipnoans apart from the delicate
perichordal centra in Protopterus. From this we may conclude that centra have
arisen at least twice within the Dipnoi, cartilage bone ossifications of the
notochordal sheath in the rhynchodipterids, Chirodipterus and possibly Dipterus
and perichordal membrane bone ossifications in Protopterus.
Amphibian vertebrae
(i) Apodans
Development of the apodan centrum has been studied by Gegenbaur (1862),
Goppert (1896), Schauinsland ( 1906), Gamble (1922) and Marcus & Blume
( 1926) who all agree that initially a series of paired, cartilaginous arcualia
( = basidorsals) occur above the notochord resting on its outer sheaths. These
arcualia may fuse at their bases to give two continuous cartilaginous rods.
Vestigial interdorsals have also been described in Hypogeophis (Marcus & Blume,
1926, Marcus, 1937). Later as in some anurans (Bufo, Runu) a median
cartilaginous rod appears below the notochord and becomes divided into
basiventrals ( = parachordale of Marcus & Blume, 1926; paracentral of Shute,
1972). These basiventrals occupy a more dorsal position than normal, but the
parapophysis for the ventral head of the rib arises from the basiventral just as in
Necturus (Gamble, 1922: 565). Anteriorly the basiventrals form a spinal tube
(Gadow, 1933) which passes inside the divergent posterior ends of the
parachordals and articulates with the parachordals by condylar processes
(Shute, 1972). Similar condylar processes are seen in urodeles and anurans.
Ossification begins by the formation of a delicate ring of bone in the perichordal connective tissue immediately outside the notochordal sheath and in contact
GNATHOSTOME VERTEBRAE
33
with the bases of the arches (basidorsals). Ossification spreads round the
notochord and neural arches and connects the dorsal with the ventral cartilages
(basiventrals) which as in Polypterus, Lepisosteus and advanced teleosts become
included in the finished vertebra. The resultant centrum is hourglass-shaped,
wider at each open end than in the middle where it constricts the notochord
(Peter, 1894). Intervertebrally, in the expanded ends of the bony cylinders,
cartilaginous rings form within the notochordal sheath. In the adult however
the centrum retains a large cavity filled by the dilated notochord, and the
intervertebral cartilage is reduced. Intravertebrally, in contrast, the cartilage of
the chordal sheath increases by a process of inward proliferation (as in
Sphenodon) and becomes highly mineralized as in urodeles (Gegenbaur, 1862),
anurans (Goette, 1875) and lepidosaurs (Gegenbaur, 1862; Gadow, 1896;
Howes & Swinnerton, 1901). A similar ‘calcified notochordal plug’ has been
described in supposed actinopterygian vertebrae from the Lower Permian
marine beds of Utah (Vaughn, 1967) and in anthracosaurs (Panchen, 1977b).
In 1959 Williams concluded, contrary to all previous workers, that the
development of the centra in apodans was essentially similar to that of amniotes
and that neither the centra nor arches differed in terms of sclerotome
components. Furthermore he believed that as in amniotes, the apodan centra
showed evidence of resegmentation. In this view he has been supported by
Wake (1970). However the amniote vertebra is diplospondylic and mainly
composed of cartilage bone with perichondral additions whereas that of the
apodan (Fig. 6B, C) is chiefly membrane bone formed in the perichordal
connective tissue and essentially similar to that of other living amphibians,
teleosts, Lepisosteus and Polypterus.
(ii) Urodeles
There have been inumerable studies of the development of the urodele
vertebral column including those of Gegenbaur (1862), Hasse (1892a), Field
( 1895), Goppert ( 1896), Gadow ( 1896), Schauinsland ( 1906), Wiedersheim
(1909), Kerr (1919), Mookerjee (1930), Emelianov (1936), Williams (1959a),
Schmalhausen ( 1968) and Shute ( 1972).
Paired cartilaginous basiventrals and basidorsals develop in the position of the
myosepta. The latter join to give a neural arch dorsally and the former to a
haemal arch ventrally in the tail. Thus the haemal and neural arches lie in the
same vertical plane. Vestigial interdorsals (Fig. 6A) have been described in the
caudal region of Ambystoma (Schauinsland, 1906) but these have been
interpreted as interneurals by Goodrich (1930: Fig. 57) in his reconstruction of
Ambystoma.
Bone makes its appearance as a cell-less sheath in the mesenchyme round the
surface of the centrum (Fig. 9G). It rapidly increases in thickness and soon
becomes cellular as it encloses the connective tissue cells (Kerr, 1919;
Schmalhausen, 1968). The bone first appears in the angles between the arch
bases (Schmalhausen, 1968) and spreads over the surface of the notochordal
sheath in the connective tissue mesenchyme. At the same time in Ranodon a
separate ossification centra arises in the middle of each neural arch (Fig. 9H).
From this centre, bone spreads over the surface of the neural arch in the
perichondrium. In other urodeles this neural arch ossification centre is wanting
and the bone spreads from the notochordal mesenchyme into the perichondrium
3
B. G. GARDINER
34
B
A
bd
na
id
fl0
D
/
E
PO
P
C
no
Figure 6 . Vertebrae. A, A?n6ystoma, anterior caudal region, 50 mm (from Schauinsland, 1906j; B,
Hypo.pophzs, trunk region, schematic (from Marcus ti Blume, 1926); C, Epicrionops, anterior trunk
region (from Fritsch, 1885);D, Salamandra, lateral and dorsal views of trunk vertebra; E: D ~ ~ ~ U C Q U ~ U J ,
lateral and dorsal views of trunk vertebra (from Remane, 1936). Heavy dots in A indicate cartilage.
of the neural and haemal arches. As ossification continues the bone also
penetrates under the bases of the arches and in Ranodon completely cuts off the
cartilaginous arch from the notochordal sheath. In other adult urodeles the
cartilaginous core of the neural arch rests directly on the notochord (Williams,
1959a).
During the time that the centrum and arches are ossifying, cartilaginous
intervertebral rings form and become enclosed within the ends of two centra
(Gegenbaur, 1862). Thus the husk-like centrum is certainly not a perichondral
ossification as suggested by Williams (1959a) and Wake (1970) since it ossifies
prior to the formation of the intervertebral cartilage (Gegenbaur, 1862;
Schmalhausen, 1968). Furthermore, as Hasse (1892a) originally maintained,
this intervertebral cartilage lies between the two sheaths of the notochord (as in
selachians and Lepisosteus) and is chordacentral. Confirmation of the
GNATHOSTOME VERTEBRAE
35
chordacentral origin of this cartilage was provided by Field (1895: pl. 12;
figs 16, 19) in Amphiuma. As in Lepisosteus the intervertebral rings are nearly
equidistant from successive myosepta and from the arches. I n some urodeles the
ring remains short anteroposteriorly but in others it grows forward and
backward to extend from one vertebra to the next behind. At this stage there is
a series of biconcave hourglass-shaped centra alternating with a series of
cartilaginous rings (Gegenbaur, 1862). Finally, in such forms as Proteus, Ranodon
and Necturus, each cartilaginous ring remains undivided and the notochord is
continuous, but in more terrestrial salamanders such as Salamandrina and Triturus
the ring thickens and constricts the notochord intervertebrally and becomes
transversely segmented (Wiedersheim, 1909: Fig. 44) so as to form an
opisthocoelous joint between consecutive vertebrae much as in Lepisosteus.
The vertebrae in urodeles are formed chiefly of membrane bone with only the
cores of the arches ever formed of cartilage bone. Intervertebral rings of
cartilage, chordacentral in origin, give rise to the opisthocoelous articulation.
The centrum is therefore perichordai with some chordacentral additions.
(iii) Anurans
I n anurans (Gegenbaur, 1862; Goette, 1875; Gadow, 1896; Ridewood, 1897;
Schauinsland, 1906), as in urodeles, paired basidorsals develop in the position of
the myosepta. However the future development of the vertebral column varies
from the perichordal to the epichordal type.
I n the former (represented by Rana and Bufo) the basidorsals fuse basally to
form two continuous longitudinal rods, whereas the basiventrals take the form
of a median rod of cartilage or hypocord. This ventral rod may eventually
subdivide (Goodrich, 1930) but often only persists in the urostylar region
(Mookerjee, 1930).
Shortly after metamorphosis thin rings of bone, slightly constricted in their
centres, are developed in the membrane investing the notochord. Ossification
then spreads from the centra through the perichondrium of the neural arches.
I n the meantime a large transverse process grows out from the side of the neural
arch and extends into the septa between the myotomes.
In the intervertebral regions, between the successive bony rings, cartilage
forms in the notochordal sheath. This cartilage grows inwards so as to constrict
and ultimately obliterate the notochord, much as in Lepisosteus. The
intervertebral cartilage becomes divided into an anterior and a posterior portion
which fuse with the bony centra of adjacent vertebrae and ossify to form their
articular ends. I t may either chiefly fuse to the front of the centrum as in Pi#a
(procoelous condition) or to the back as in Rana and Bufo (opisthocoelous).
In the epichordal type (represented by Bombinator, Pelobates and Pipa) the
basidordals appear to be the only cartilaginous elements formed, though some
authorities (Williams, 1959a; Wake, 1970) claim that lateral and ventral
cartilages degenerate and disappear. The notochord is enclosed by a membrane
bone cylinder and this subsequently grows up over the neural arches and
transverse processes.
In summary the vertebrae of living amphibians are formed chiefly of
membrane bone and only the ends of the centrum and cores of the arches are
formed of cartilage bone. The centra are therefore perichordal with some
chordacentral additions as in Lepisosteus and some teleosts.
B. G. GARDINER
36
(iv) Fossil amphibians
The earliest amphibian centra are found in the Lower Carboniferous (Viskan)
of Scotland and belong to the adelogyrinids (Watson, 1929) and aistopods
(Fig. 7C, Dj. By the Upper Carboniferous centra belonging to the Nectridea are
also quite common (Figs 6E, 7A, B).
The centrum of Adelogyrinus consists of a flat bony surface which passes
internally into a system of crossbeams. Dorsally and ventrally there are a pair of
depressions for the neural and haemal arches which were separately ossified.
The structure of this centrum is very similar to that of Amia and primitive
teleosts in which the arches ossify as cartilage bone and remain independent of
the centra. From this comparison there is every reason to consider the centrum
of Adelogyrinus to be composed of membrane bone as in teleosts and Recent
Amphibia.
The centra of aistopods (Baird, 1964, 1965) and nectrideans are
lepospondylous and fused to the neural arch (Figs 6E, 7A, B, C, D ) . I n the
A
DB
B
no
C
C
D
C
.ho
E
Figure 7. Vertebrae. A, Urocordylus ( = Sauropleura), anterior trunk and tail region; B, Scincosaurus,
anterior caudal vertebra (from Schwartz, 1923); C, Doltchosoma ( = Phlegethontiu), trunk region; D ,
Ophiderpeton, trunk vertebra, ventral view ( C , D from Fritsch, 1885); E, Archegosaurus, thoracic,
anterior caudal and three posterior caudal vertebrae (from Jaekel 1886 and Goodrich 1930).
GNATHOSTOME VERTEBRAE
37
A
B
oiv’
Figure 8. Vertebrae. A, Archegosaurus, posterior caudal region (from Meyer, 1857); B, Chelydosaurus
(=Cheliderpefonj, caudal region (from Fritsch, 1885).
aistopods the neural arch is low and similar to apodans while the haemal arches
are reduced to a pair of longitudinal ridges. In the Nectridea the caudal
vertebrae bear fan-shaped neural and haemal arches. In both groups the neural
arch pedicels are interlocking and perforated for the spinal nerves as in apodans
and urodeles. Ribs are absent from the atlas. The centra are husklike,
sculptured with fine vermiculate lines and bear strong transverse processes (ribhangers) as in Recent Amphibia. There can be little doubt that the
lepospondylous centra in aistopods and nectrideans are similarly composed of
membrane bone.
Other than these lepospondylous forms three groups of Triassic
temnospondyls also possessed completely ossified centra; the plagiosaurs,
mastodonsaurs and metoposaurs (Fig. 9A, B, C, D, E, F) as well as one Permain
genus Peltobatrachus (Panchen, 1959). The plagiosaurs are represented by the
Rhaetic Plugiosaurus (Nilsson, 1937) and such Triassic forms as Plugiosternum and
Gerrothorax (Nilsson, 1946). Mastodonsaurus and the rnetoposaurs are confined to
the Triassic. In all three groups the majority of the neural arches lie posterior to,
and separate from, the centra.
B G.GARDINER
38
C
D
fia
E
F
+--
bd
nts
- \
mb
nt
Figure 9. Vertebrae. A, Pehbatrachus, dorsal vertebrae; B, Peltobatrachus, dorsal vertebra in front
view; C, Pe/tobntrachus, caudal vertebra in front view (all from Panchen, 1959); D, Mastodonsourus,
dorsal vertebrae (from Nilsson, 1937); E, hfastodonsaurus, atlas in front view; F, hfastodonsaurus,
dorsal centrum in front view (E, F from Fraas, 1889); G, Ranodon, T.S. second vertebra, 25 mm; H.
Ranodon, trunk vertebrae, 27 mm (from Schmalhausen, 1968). Heavy dots in G indicate cartilage.
In Peltobatrachus the centra are amphicoelous cylinders, slightly constricted
between the ends and with a small central perforation. Anteriorly, paired raised
facets for the neural arch articulations form partial side walls to the neural
canal. In the tail region there are a few separate haemal arches each fused to a
small shallow crescent. These appear to be interspersed between the regular
centra much as are the neural arches dorsally and probably represent
basiventrals. An alternative explanation is that this region is diplospondylic as in
sharks and many actinopterygians. Towards the end of the tail the centra and
neural arches are fused. I n the Triassic plagiosaurs the centra are stouter,
cylindrical, with intervertebral neural arches and all traces of the notochordal
GNATHOSTOME VERTEBRAE
39
canal obliterated. In the caudal region of Gerrothorax the fused haemal arches
described by Nilssen (1946) probably represent fused neural arches as suggested
by Panchen (1959: 256). The facets for the neural arches stand on ridges above
the cylindrical body of the centrum; similar facets are seen in Mastodonsaurus
(Frass, 1889) and Buettneria.
The caudal centra of Mastodonsaurus (Fraas, 1889; Huene, 1922) show that
ossification starts ventrally and gradually embraces the notochord (cf.
Osteorachis). A similar ontogenetic pattern is also recognizable in the
metoposaurs where the centra in the European Metoposaurus consist of little more
than a ventral hemicylindrical shell (Colbert & Imbrie, 1956; Chowdhury,
1965). This together with the opisthocoelous joints in at least the cervical
vertebrae in both groups strongly suggest that the centra in Mastodonsaurus and
metoposaurs are perichordal with cartilage bone additions as in Lepisosteus.
Similar opisthocoelous joints are also present in Plagiosternum (Huene, 1922:
fig. 24) and there is every reason to suppose that the centra in the plagiosaurs
and Peltobatrachus are similarly periochordal. The neural arches fuse to the
centra in the cervical region (atlas) of Buettneria and the bases of the
haemapophyses may also fuse with the centra caudally (Case, 1932), likewise in
Mastodonsaurus (Wepfer, 1923). The centra of stereospondyls appear to be
perichordal, nevertheless it is possible that they are made of cartilage bone as in
amnio tes.
Thus centra have arisen on at least three occasions within the Amphibia; once
in the lepospondyls (aistopods, nectrideans) and Lissamphibia, once in the
temnospondyls (plagiosaurs, metoposaurs, mastodonsaurs) and once in
Peltobatrachus. Additionally one other group of temnospondyls, the Permian
branchiosaurs, parallel actinopterygians in the possession of chordacentra. Thus
Discosauriscus (Credner, 1890: figs 10, 11; Spinar, 1952: pl. 29) has thin ring
centra of dark fibrous bone (=pleurocentra of Spinar, which are overlain by
endochondral neural and haemal arches.
Amniote vertebrae
Centra are characteristic of all amniotes and their similarity of development and
structure suggests them to be homologous throughout the various groups, and to
have arisen but once. The centra are primitively diplospondylous with ossified
centra and intercentra, but in more advanced forms (crocodiles, birds and most
mammals) intercentral ossifications are wanting except from the atlas
intercentrum (Fig. 1 lC, D, E). Elsewhere in the column the intercentra persist
as cartilaginous discs or menisci (they arise approximately midsegmentally and
earlier than the centra). Basiventrals ossify to form chevrons in the tails of most
amniotes and are often supported by cartilaginous intercentra (Fig. 10D).
(i) Sphenodon
Initially a perichordal tube forms around the notochord as in all amniotes.
This continuous skeletogenous sheath is particularly thick and similar to that in
chondrichthyans. At about the same time cartilaginous basidorsals (neural
arches) and basiventrals (chevrons) arise (Goette, 1897; Howes & Swinnerton,
1901; Schauinsland, 1903, 1906). These are closely followed by the
chondrification of the perichordal tube in which a series of segments become
40
B. G. GARDINER
C
ie
IC
Figure 10. Vertebrae. A, Cricotus ( =Archeria), caudal region (from Williston, 1925); B, Eogyrinus,
trunk region; C , Seymouria, trunk region (B, C from Panchen, 1977a); D, Crocodilus, caudal region,
intercentrum also in front view (from Gadow, 1896); E, Euryodus, anterior most vertebrae (from
Carroll & Gaskill, 1978). Heavy dots in D indicate cartilage.
recognizable, each comprising a centrum and an intercentrum (Fig. 13). Both
centra and intercentra are paired in origin and fuse in the midventral line
anteroposteriorly. The paired intercentra according to Howes & Swinnerton
(1901) not only arise prior to the centra but also are initially continuous with
the differentiating ribs. Later in development some intercentra are said to
disappear (from segments 5530) and to be replaced by secondary intercentra
which lie outside the skeletogenous sheath.
The neural arches ossify independently of each other and the centrum by a
similar perichondral process. An identical pattern is exhibited by the chevrons
and the intercentra, except that in the latter the ossification is limited to a small
ventral crescent (Fig. 12A). I n this way a bony sheath develops round the
centrum and bone formation spreads inwards into the substance of the
cartilaginous centrum while the chevrons may fuse by superficial ossification
with their intercentral crescents (Gadow, 1896). Subsequent growth and
enlargement of the centra is by the addition of layers of perichondral bone
peripherally as in all amniotes. In the adult the centra are deeply amphicoelous
and every intercentrum extends dorsalwards as a fibrocartilaginous ring which
surrounds the notochord. The chevrons are stoutly ossified and in the anterior
GNATHOSTOME VERTEBRAE
A
B
C
'C2
Figure 11 Vertebrae A, Pe~odosotzs,trunk region, B, Ostodolepzs, trunk region (from Carroll &
Gaskill, 1978), C , Sphenodon, atlas and axis, D, Chelone, atlas and axis, E, Gauzalzs, atlas and axis (all
from Remane, 1936)
B
C
IC
C
Figure 12. Vertebrae. A, Sphenodon, anterior trunk; B, Sphenodon, chevron bones in tail (from
Hoffstetter & Gasc, 1969); C, Priodon, tail vertebra, front view; D, Phocaena, tail vertebra, front
view; E, Thylacinus, atlas, front view (C-E from Remane, 1936).
41
42
B. G. GARDINER
B
A
bd
ric
nts
Figure 13. T.S. post sternal vertebra of Sphenodon, stage Q. A, intervertehral region; B, vertebral
region (from Howes & Swinnerton. 1901). Heavy dots indicate cartilage.
part of the tail the base is unpaired (Fig. 12B) but in the middle and posterior
regions the base is paired (Hoffstetter & Gasc, 1969).
(ii) Squarnata
There is little difference in the development of the centra in lizards, and
snakes to that described in Sphenodon apart from the reduction of the intercentra
in some forms (von Ebner, 1888; Boulenger, 1891; Corning, 1891; Gadow, 1896;
Manner, 1899; Schauinsland, 1906; Branauer, 1910; Goodrich, 1930).
Nevertheless prior to segmentation the perichordal tube is said to be converted
into a continous tube of cartilage in both Lacerta and Gekko (Gadow, 1896).
The intercentrum in the Gekkonidae, as in Sphenodon, appears in consecutive
sections as a complete ring, the ventral third only being ossified, the rest of the
ring remaining cartilaginous. I n the tail these intercentra form thick triangular
wedges which are incompletely separated from the paired chevrons with which
they may fuse by superficial ossification (Gadow, 1896). The chevrons in
Pseudopus on the other hand fuse with the caudal ends of the centra (Boulenger,
1891) as they do also in amphisbaenians and snakes. I n amphicoelous gekkonids
the cervical intercentra bear hypapophyses (Hoffstetter & Gasc, 1969) and in
Heloderma (Boulenger, 1891) the anterior intercentra are often paired. The
cartilaginous protion of the intercentra varies in thickness even within the same
individual. I n Phyllodactylus and Gekko the intercentra are thin but in Platydactylus
they are considerably thicker and constrict the notochord intervertebrally.
Where the intercentra are totally unossified they often form persistent discs
which are interposed between the caudal ends of the centra and the articulating
condyles (of amphicoelous forms) around which they fit like a collar (much as in
crocodiles, Fig. 10D). I n the procoelous Gekkonidae the whole ring acts as an
articular pad. In other lizards such as iguanids where in part of the column the
intercentra are wanting, they are presumed to have fused with the back end of
the centrum to form the posterior condyle (Hoffstetter & Gasc, 1969), but this
seems unlikely since the cervical vertebrae possess both posterior condyles and
intercentra.
GNATHOSTOME VERTEBRAE
43
(iii) Cheloniu
I n chelonians ossified intercentra occur regularly between the anterior
cervicals and in the tail as paired or unpaired nodules (Gadow, 1896). Despite
the fact that these intercentra form an homologous series both with one another
and with other amniotes, Williams (195913) has homologized the cervical
nodules in cryptodires with the capitular portion of vestigial ribs. Significantly
the neural arches, ribs and intercentra all lie in the sane transverse plane, that is
in front of the centra in young tortoises (Gadow, 1896).
The atlas in chelonians (Fig. 11D) shows considerable variation. Primitively it
consists of a neural arch and an intercentrum which may fuse (Shute, 1972). I n
the Pleurodira, Trionychoidea and Carettochelyoidea the atlas centrum also
fuses with its intercentrum and neural arch so that the neck joint passes between
the occipital condyle and the biconcave atlantal intercentrum (Hoffstetter &
Gasc, 1969). T h e dorsal part of the first intercentrum often forms a ligamentum
transversum (Gadow, 1896) as in some amphisbaenids (Hoffstetter & Gasc,
1969), birds and mammals (Mayer, 1834).Elsewhere in the column intercentra
are reduced to fibrocartilaginous discs as in crocodiles, birds and mammals.
(iv) Crocodilia
The development of the vertebral column in the Crocodilia (Gadow, 1896;
Higgins, 1923; Shute, 1972) shows most clearly that intercentra in the Amniota
are not homologous with chevrons and that chevrons arise from arcualia in a
similar manner to the neural arches. Thus the direction of chondrification is
towards the notochord in both neural and haemal arches (Higgins, 1923).
Furthermore, a t about the same time as the basidorsals (neural arches) and
basiventrais (haemal arches) chondrify, the skeletogenous tube surrounding the
notochord segments into cartilaginous centra and intercentra. However not only
is the neural arch not continuous with the underlying centrum, but also neither
are the bases of the haemal arches (chevrons) with the intercentra; instead they
are separated from them by loose connective tissue (Higgins, 1923).
The first intercentrum ossifies to form the crescentic atlas base (Fig. 11E) but
all remaining intercentra form cartilaginous rings or menisci. The intercentra
occur regularly throughout the vertebral column although the second
intercentrum fuses completely with the first and second centra (to form the
odontoid process) and others may be abolished by the subsequent fusion of
adjoining vertebrae (Gadow, 1896). T h e centra are procoelous (with the
exception of the first two sacrals and first caudal), bearing small condyles
posteriorly. The cartilaginous intercentra form collars ( = meniscal rings) round
these condyles much as in Heloderma. However on the first caudal the meniscal
ring sits on the anterior condyle and bears two facets ventrally for the
articulation of the posterior end of the last sacral vertebra (Fig. 10D). Ossified
haemal arches or chevrons are continuous with these meniscal rings in the
caudal region.
The anterior thoracic and cervical centra possess stout hypapophyses which
can be seen during development to be continuous with the centra and to arise as
outgrowths from them (Higgins, 1923). Similar outgrowths occur in many birds
and in Ornithorhynchus.
44
B. G . GARDIKER
(v) Mammalia
Despite the many papers written on the development of mammalian
vertebrae (Schultz, 1896; Bardeen, 1906; Schauinsland 1906; Dawes, 1930;
Reiter, 1942; Sensenig, 1943) Froriep’s 1886 paper on the development of the
cervical vertebrae of Bos remains the most illuminating.
Froriep demonstrated that initially procartilaginous neural arches form in the
intervals between successive muscle blocks and are shortly followed by the
development of a dense mesoblastic layer around the notochord. Subsequently
the skeletogenous layer differentiates into alternating perichordal rings
(intercentra) and centra. In other mammals the skeletogenous layer is said to
form a continuous cartilaginous rod prior to segmentation (Schultz, 1896;
Schauinsland, 1906). The perichordal ring or intercentrum begins to constrict
the notochord. Dorsally it consists mainly of longitudinal fibres ( = rudiment of
the intervertebral ligament) and is continuous both with the neural arches and
rib bases. This latter area eventually gives rise to the interarticular ligament of
the head of the rib. Ventrally the perichordal ring chondrifies to form the
‘hypochordale Spange’. This cartilaginous portion of the perichordal ring, often
referred to as the hypochordal clasp, is restricted to the ventral surface of the
notochord. It passes continuously into the rest of the intervertebral disc. With
the increasing obliquity of the septa this cartilaginous part of the perichordal
ring moves caudalwards. The cartilaginous hypochordal clasps have a fleeting
existence and are soon reduced and disappear, only the first and second
remaining (presumably those in the thoracic and lumbar regions of some
insectivores also remain).
During this time bilateral, cartilaginous rudiments appear in the centrum and
grow into a horseshoe shape, open dorsally. Simultaneously the neural arches
chondrify from their tips inwards and though initially separated from the
centrum by a perichondrium they fuse with it a t the same time as the
cartilaginous hypochordal clasp atrophies and disappears. The centrum forms
between the intersegmental arteries and neural arches, in the same plane with
the somitic boundaries.
Ossification starts dorsally in the neural arch and in the centrum dorsal to the
notochord. The notochord is obliterated except for a small vestige in the middle
of the intervertebral ligament. Subsequent growth of both centra and neural
arches is periosteal, by the direct formation of membrane bone in the
periosteum.
The cartilaginous first intercentrum ossifies to form the base of the atlas, but
the second intercentrum is said by Froriep (1886) to be totally suppressed.
Nevertheless it survives in man as a pair of ossicles between the rudimentary rib
and the second centrum (Gadow, 1891). I n marsupials it is worth noting that
the whole of the ventral part of the axis may be reduced to a fibrous band.
Elsewhere in the column the intercentra are reduced to fibrocartilaginous discs.
The development of the haemal arches closely follows that of the neural
arches except that instead of finally fusing with the centra they remain loosely
attached to the intercentral disc. Y-shaped chevron bones occur in the tails of
monotremes, marsupials, sirenians, cetaceans, edentates and pangolins.
Sometimes the right and left halves of these haemal arches remain separate or
they may fuse distally or occasionally they may fuse to the posterior end of the
centrum next in front (Fig. 12C, D).
GNATHOSTOME VERTEBRAE
45
(vi) Aues
The most impressive description of vertebral development in the chick like
that of the mammal was given by Froriep (1883). Other useful studies include
those of Jager ( 1859), Schwark ( 1873), Schauinsland ( 1906), Piiper ( 1928) and
Remane ( 1936).
As in the mammal the notochord soon becomes surrounded by a moniliform,
mesenchymatous, perichordal tube. This tube then segments into perichordal
rings which are split into bundles of longitudinal fibres at the dorsal and ventral
surfaces of the elastica interna. Simultaneously with this event the
bilaterally symmetrical neural arch rudiments chondrify, closely followed by the
thickening and chondrification of the ventral margin of the perichordal ring.
This latter cartilage is the hypochordal clasp and, as in the mammal, is
horseshoe-shaped and displaced somewhat caudalwards with respect to the
fibrous portion. I t is continuous dorsally with the cartilaginous neural arch.
This hypochordal portion of the intercentrum arises from bilaterally
symmetrical arch rudiments similar to those in Sphenodon (Howes & Swinnerton,
1901).
Caudal to the intercentrum the first rudiments of the cartilaginous centrum
appear as a new perichordal tissue condensation. Formed of two symmetrical
halves (again as in Sphenodon) the cartilaginous centrum surrounds the
notochord like a ring and eventually fuses with the bases of the neural arches, as
in mammals. In the meantime the ventrolateral corners of the hypochordal
clasp thicken and extend laterally into the intermuscular septa as dense fibrous
tissue, which subsequently chondrifies to form the ribs. The cartilaginous
hypochordal clasp then gradually disappears except from the first and second
cervicals and possibly some of the caudal vertebrae. The first hypochordal clasp
ossifies and fuses with its neural arch to form the atlas, as in mammals, while the
innermost fibrous disc portion of the first intercentrum remains as the
ligamentum transversum atlantis. This ligamentum transversum is perforated by
the remnant of the notochord, as are the menisci in mammals, birds and
crocodiles. The second intercentrum a t first persists as an intervertebral pad
between the odontoid (centrum 1 ) and the centrum of the epistrophus but later
following ossification it fuses with them to become an essential part of the axis.
Thus the ligamentum transversum atlantis together with the ossified portion of
intercentrum one is serially homologous with the intervertebral pad two and the
remainder of the menisci occurring between successive centra (see also Jager,
1859 and Gadow, 1896). The original cartilaginous components (hypochordale
Spange) of these menisci having atrophied and disappeared except from the
atias/axis (and in mammals from the thoracic and lumber regions of certain
insectivores).
(vii) Fossil amniotes
T h e earliest amniote centra belong to the anthracosaurs (Gardiner, 1982) and
are found in the Lower Carboniferous. They occur in the Namurian limestones
of the Lothian Coal field. Microsaurs are also recorded from the Namurian
limestones.
I n anthracosaurs such as Eogyrinus and Cricotus (Fig. 10A, B) each vertebra
consists of a neural arch and two complete, amphicoelous discs perforated for a
persistent notochord. I n Anthracosaurus the perforations are occluded by
46
B. G . GARDINER
mineralized plugs (Panchen, 1977b). The circumference of both centra is
markedly thickened by periosteal bone. I n the anterior segments the
intercentrum is a crescentic wedge and in the tail is continuous with the haemal
arch. The neural arches are sutured with the centra in the trunk but in the
caudal region of Eogyrinus they are fused with them (Panchen, 1966).
I n microsaurs (Figs 10E, 11A, B) the intercentra are frequently reduced to
hemicylinders (Euryodus, Ostodolepis, Pelodosotis) or may even be entirely lacking
(Pantylus). The neural arches are fused to the centra and the atlas is unique
amongst amniotes (Fig. 10). The atlas forms a long strap-like articulation with
the occiput, comprising paired depressions in the centrum (for the occipital
condyles) with a central projection between, much like the odontoid in Recent
urodeles. Unlike amphibians there is usually an intercentrum intercalated
between the atlas and axis centra (as in amniotes) and the body of the atlas
supports two ribs. Haemal arches lie freely in the tail and are never fused with
the centra.
Acanthodian and placoderm vertebrae
In all acanthodians the notochord is persistent and the arcualia are
represented by paired neural and haemal arches (basidorsals and basiventrals) .
The neural arches bear spines as do the haemal arches posteriorly. Both arches
are perichondrally ossified in Acanthodes, Diplacanthus and Parexus.
Placoderms like acanthodians have perichondrally ossified, paired neural and
haemal arches (Arthrodira, Phyllolepida, Ptyctodontida) . Posteriorly the
haemal arches enclose the haemal canal and the two halves are fused as are the
corresponding neural arches and spines. The anterior, paired haemal arches in
Ctenurella have been interpreted by Brvig (1960) as haemal arches with detached
haemal spines (but see BMNH P.48236, P.48245).
In the rhenanids Gemuendina and Jagorina ring-like perichondral centra link
the neural and haemal arches (Stensio, 1959; Gross, 1963). These perichondral
shells are deduced to have formed around cartilaginous centra. Anteriorly the
centra are fused to form the synacral.
Similar perichondrally ossified centra occur in the pachyosteid arthodire
Erromenosteus (Stensio, 1959). From this I conclude that centra must have arisen
at least twice in placoderms, once in rhenanids and once in Erromenosteus.
CLASSIFICATION O F AMPHIBIA
With the recognition of the diplospondylic nature of the vertebral centra in
amniotes it was clear that such groups as the anthracosaurs, seymourians and
microsaurs, often classified as amphibians, were in fact amniotes (Gardiner,
1982). Of the remaining Amphibia only four groups possess centra, the
Lissamphibia, the stereospondyls (mastodonsaurs, metoposaurs, plagiosaurs) ,
the temnospondyl Peltobatrachus and the lepospondyls (aistopods, nectrideans) . I n
the stereospondyls and Peltobatrachus, however, the centra are massive and
composed of membrane bone or possibly endochondral bone, whereas the centra
of the lepospondyls are husk-like and closely resemble the membrane bone centra
of the Lissamphibia. Further analysis showed that the stereospondyls formed a
monophyletic group within the temnospondyls while the lissamphibia and
47
GNATHOSTOME VERTEBRAE
Q."
@Q+
$
3
'
19
Figure 14. Cladogram of major groups of choanates. Numbered characters refer to the following
synapomorphies: 1, choana; 2, cavum epiptericum (ascending process sutures with skull roof and/or
side wall of orbitotemporal region); 3, pterygoids joined in midline, excluding the parasphenoid
anteriorly from roof of mouth; 4, quadrate in advance of occiput; 5, hyomandibula plays no part in
jaw suspension; 6, infraorbital sensory canal interrupted by external nostril which is close to margin
of mouth; 7, fusion of right and left pelvic girdles; 8, pentadactyl limb; 9, internasal bone; 10,
septomaxillary forms part of external surface of cranial roof; 11, occipital condyle tripartite, paired
exoccipitals predominate; 12, neural arches strongly ossified and with zygapophyses; 13, bicipital
ribs with uncinate processes; 14, fenestra ovalis with stapedial plate, stapes posteroventrally
orientated towards quadrate; 15, infraorbital canal passes onto the maxilla; 16, sensory canals
superficial on bone surface u. enclosed in bone; 17, infraorbital canal interrupted in region of
lachrymal; nasolachrymal duct bone enclosed; 18, opisthotic with paroccipital process to tabular u.
no paroccipital process; 19, Cheek without pre- and subopercular bones, u. one or more present; 20
skull without internasal bone, u. internasal present; 21, labyrinthodont teeth, u. complex
polyplocodont; 22, apical fossa small, vomers meet premaxillae anteriorly, u. large apical fossa and
vomers that meet premaxillae laterally; 23, infraorhital canal looped over the lachrymal and
continuous over both jugal and lachrymal, u. infraorbital canal in two parts; 24, teeth replaced from
beneath, new tooth in bony pedestal of predecessor, u. lateral tooth replacement; 25, skull roofing
pattern in which tabulars contact parietals, u. tabulars not contacting parietals; 26, sternum
present, u. sternum absent; 27, long postanal tail of 40+ caudal vertebrae, u. 30-35 caudals; 28,
notochord highly mineralized; 29, septomaxillary internal, u. on skull surface.
lepospondyls shared several other synapomorphies (Figs 15, 16) the distribution
of which suggest that the Nectridea and Lissamphibia are sister groups and that
the Aistopoda is the sister group of those two (Fig. 15). The position of
Peltobatrachus on the other hand is uncertain.
With the establishment of the monophyly of the Division Amphibia (see also
Gardiner, 1982) it was then possible to investigate the relationships of the early
tetrapods and to produce preliminary cladograms of the Temnospondyli and
Amphibia. Not surprisingly the Amphibia were found to be the sister group of
the amniota sharing with them a skull roofing pattern where the tabulars
contact the parietals and the. postparietals are reduced (this condition is
B. G. GARDINER
48
I
Figure 15. Cladogram of Amphibia. Numbered characters refer to the following synapomorphies: I ,
lepospondylous vertebrae composed of membrane bone; 2, elongate centra with attached neural
arches; 3, post temporal fossa absent, u. post temporal fossa present; 4,neural arches perforated for
spinal nerves; 5, otic notch closed, u. otic notch open; 6, ectopterygoid absent, u. ectopterygoid
present; 7, sickle-shaped hyoids, v . straight hyoids; 8, reduction in number of dermal bones in lower
jaw: single coronoid mesially, 3 bones laterally; 9, interlocking neural arches; 10, atlas devoid of
ribs; I I , squamosal large, contacts parietal, u. squamosal contacts temporal bone; 12, haemal arches
fused to centrum; 13, bifurcated, membrane bone ribhanders; 14, condyles medially directed with
notochordal pit; 15, roofing bones in temporal region consisting of partietals only; otic bones
exposed; 16, nasolachrymal duct terminates in palpus; 17, surangular absent, u. surangular present;
18, similar craniovertebral joint: short ribs not encircling body cavity; 19, musculocutaneous vein;
20, pterygoids abut neurocranium; 2 1, plectrum and operculum with opercularis muscle; 22,
postfrontal absent, u. post frontal present; 23, intermaxillary gland; 24, K-shaped ribs; 25,
squamosal/tabular absent, u. squamosal/tabular present; 26, very broad transverse processes.
paralleled in several branchiosaurs including Micromelerpeton, Discosauriscus and
Leptorophus) . Other shared derived features include the method of tooth
replacement in which each new tooth develops in the bony pedestal of its
predecessor and the dentition is essentially pleurodont; a notochord which is
highly mineralized in both the Amphibia and the squamates and Sphenodon; the
possession of a sternum, a long postanal tail of 40+caudal vertebrae and a
septomaxillary which is never exposed (Fig. 14).
The temnospondyls proved to be the sister group of the Amniota plus
Amphibia, sharing with them an infraorbital sensory canal which is continuous
over the jugal and lachrymal and with a distinct loop on the latter bone;
labyrinthodont teeth (Schultze, 1969); a reduced apical fossa and the absence of
the internasal.
The loxommatids are the sister group of these three, uniquely sharing with
them superficial sensory canals and an infraorbital sensory canal which
anteriorly passes onto the maxilla (the infraorbital canal however is interrupted
in the middle of the lachrymal, Beaumont, 1977: fig. 8) and a bone-enclosed
nasolachrymal duct. A similar duct has been described in anthracosaurs,
GNATHOSTOME VERTEBRAE
29-1-31
324-33
,
1
49
34
28
21--23
I
Figure 16. Cladogram of Temnospondyli. Numbered characters refer to the following
synapomorphies: 1, basipterygoid region of parasphenoid sutured to pterygoid; 2, development of
interpterygoid vacuity; 3, stapes projects dorsally, sutured to the parasphenoid; 4, cleithrum narrow
(often splint-like) u. broad; 5, interdorsals ossified, articulate with neural arches; 6 , vomers
elongate, occupying at least one third of total head length, u. vomers broad and short; 7, internal
nostrils large, oval in shape, u. small, round nostrils; 8, skull long-faced; 9, lachrymal does not reach
orbit, prefrontal and lachrymal in tandem; 10, jugals long, project below lachrymal; 11, nasals
almost twice as long as wide; 12, interfrontal sometimes present; 13, exoccipital with membrane
bone flanges which extend over labyrinth and vagal foramen; 14, sutural union between quadrate
ramus of pterygoid and prootic; 15, parafenestral crista between parasphenoid and pterygoid; 16,
pterygoids joined to parasphenoid by a broad, strongly interlocked suture; 17, interpterygoid
vacuity large; pterygoids short, do not reach vomers, separated from palatine by ectopterygoids; 18,
occipital condyles paired, widely separated, basioccipital not ossified; 19, separate interdorsals
absent, v. interdorsals present; 20, infraorbital canal with a Y-shaped fork in postorbital; 21,
parasphenoid separates the vomers posteriorly for some considerable distance; 22, parasphenoid
sutures with exoccipital posterolaterally; 23, pterygoid sutures with exoccipital posteriorly; 24,
centra, with shoulders round the neural canal (=interdorsals?); 25, neural arches fuse with centra
in cervical and tall regions; 26, a single bone occupies space of prefrontal and lachrymal; 27,
squamosal projects posteriorly and has a broad lateral face; 28, premaxilla separated dorsally by
oval fenestra; 29, parasphenoid produced into a short lateral wing immediately behind the
basipterygoid process; both wing and area over basipterygoid process sutured to pterygoid; 30,
lachrymal enlarged, extending over most of the ventral margin of the orbit; 31, otic notch absent, u.
otic notch present; 32, external nostril considerably elongated; 33, squamosal with articular process
dorsally; 34, quadrate way behind occiput; 35, nasals occupy more than one-third total head
length.
~
microsaurs, seymourians and in such temnospondyls as Brachiosaurus, Dendrerpeton
(Watson, 1956: fig. 29) and Aphaneramma (Save-Soderbergh, 1936: fig. 26).
Finally the Ichthyostegidae are the sister group of the loxommatids,
temnospondyls, amphibians and amniotes, sharing with them a pentadactyl
limb; a tripartite occipital condyle in which the paired exoccipitals
predominate; strongly ossified neural arches with zygapophyses; bicipital ribs
with uncinate processes; a fenestra ovalis and stapedial plate; a superficial
septomaxillary bone and an internasal. This information is summarized in
4
50
B. G. GARDINER
Fig. 14 where all the synapomorphies mentioned above are listed. I n addition
cladograms for the Amphibias and Temnospondyli are given in Figs 15 & 16.
In the Amphibia the Adelogyrinidae are shown to be the sister group of the
Aistopoda which together form the sister group of the Nectridea plus
Lissamphibia. This means that the plesion Lepospondyli previously used to
include the Aistopoda, Nectridea and Microsauria and which I had used for the
Aistopoda and Nectridea (Gardiner, 1982) should be abandoned.
In concluding this section it is worth emphasizing that the establishment of
the monophyly of the temnospondyis presented the greatest challenge. This was
due in part to the long held belief that the primitive amphibian palate is kinetic
and that the palate in loxommatids, temnospondyls and anthracosaurs is
movable on the braincase (e.g. Watson, 1912; Panchen, 1970; Beaumont, 1977).
However, the skull in all these forms is very solid, with dermopalatine,
ectopterygoid, vomers and pterygoids firmly keyed to one another and to the
cheek bones, and the cheek bones are keyed to the skull roofing bones (Rosen et
al., 1981). Re-examination of whole series of temnospondyl skulls (including
Trimerorhachis, Erpetosaurus, Colosteus, Saurerpeton, E?yops, Dendrerpeton,
Archegosaurus, Micropholis, Discosauriscus) revealed that in every case that portion
of the parasphenoid which covered the basipterygoid process was sutured to the
pterygoid. In many instances, due presumably to crushing, the two surfaces had
separated, nevertheless the interlocking edges of the two dermal bones could
clearly be recognized. I n the more advanced temnospondyls such as the
trematosaurs, capitosaurs and stereospondyls, the pterygoids and parasphenoid
are joined by a much broader interlocking suture and the pterygoids may also
join with the exoccipitals. Furthermore, in the loxommatids, the epipterygoids
suture with the skull roof whereas in the temnospondyls they suture (often by
cartilage fusion) with the side wall of the orbitotemporal region. Thus as in
dipnoans a cavum epiptericum must have been present in all of these primitive
tetrapods and the skull was autostylic. A kinetic palate on the other hand is a
synapomorphy of squamates plus Sphenodon.
SUPERCLASS Gnathostomata
CLASS Osteichthyes
SUBCLASS Sarcopterygii
INFRACLASS Choanata
SUPERDIVISION Dipnoi
SUPERDIVISION Tetrapoda
tplesion Ichthyostegidae
tplesion Loxommatidae
tplesion Temnospondyli
DIVISION Amphibia
tplesion Adelospondyli
ORDER Adelogyrinidae
ORDER Aistopoda
tplesion Nectridea
SUBDIVISION Lissamphibia
SUPERORDER Apoda
SUPERORDER Paratoidia
O R D E R Urodela
ORDER Anura
GNATHOSTOME VERTEBRAE
51
All of the information contained in this section is additionally summarized in
the classification above; fossils are incorporated according to the method
described by Patterson & Rosen (1977) and elaborated by Wiley (1979).
SUMMARY AND CONCLUSIONS
Four pairs of arcualia were primitively present in each segment of
gnathostomes and all tetrapods retain a t least two pairs of arcualia per segment
in the form of neural and haemal arch anlage. I n some tetrapods the bases of
the arcualia are embedded in the definitive centrum. I n selachians the neural
and haemal arch anlagen are embedded in the centrum, while the interdorsals
and interventrals remain separate, whereas in Amia all four pairs of arcualia are
embedded in the centrum, which ossifies without a cartilaginous precursor in
the mesenchyme outside the chordal sheath. Perichordal membrane bone centra
are also characteristic of Polypterus, Lepisosteus, teleosts, Protopterus and the
Amphibia and in all these the centrum encloses the bases of the arches. The
centra of stereospondyls may also have been perichordal. The centrum in
selachians and the centrum and intercentrum in amniotes by contrast forms
directly in the notochord sheath. I n amniotes, as in Polypterus, Lepisosteus, most
teleosts and Protopterus, only neural and haemal arch anlagen are present and in
the amniotes these chondrify before the centra ossify. These anlagen therefore
always lie outside the vertebral body in amniotes although the subsequent
neural arches, in most cases, fuse with the centra; the haemal arch anlagen, on
the other hand, always lie with their bases in contact with the perichordal tube
and become intimately associated with the intercentra. In Lepisosteus
cartilaginous rings form intervertebrally within the notochord sheath in the
expanded ends of the hourglass-shaped centra. These rings subsequently ossify
to form the opisthocoelous joint in the adult vertebra. This type of vertebra is
unique among fishes but parallels that seen in Recent amphibians where similar
intervertebral cartilages constrict the notochord and form the articular faces of
contiguous vertebrae.
I n many fossil dipnoans and amniotes the centra are preformed in cartilage.
I n amniotes there are primitively two centra per segment (intercentrum and
centrum). T h e neural arch is normally fused to the centrum and the haemal
arch to the intercentrum, but in Chelone the neural arches are intercentral in
position. Both the centrum and intercentrum chondrify prior to ossification
which begins perichondrally. Primitively the amniote vertebral column was
diplospondylic throughout its length but ossification of the intercentra is never
complete in living members except in the atlas vertebra. Elsewhere in squamates
and Sphenodon the intercentra ossify as half rings which caudally support the
chevrons. These half rings or crescents are continued dorsally in cartilage so as
to completely clasp the notochord. I n chelonians, crocodiles, mammals and
birds the intercentra only chondrify ventrally (the hypochordale Spange) but
this chondrification later atrophies and disappears (except from the first and
second cervicals, the caudal vertebrae and from the thoracic and lumbar region
of some insectivores). Nevertheless the fibrocartilaginous sheath portion of the
intercentrum persists to form an intervertebral pad or meniscus.
The intercentra can in no way be homologized with the chevrons which lie
52
B. G. GARDINER
outside the skeletogenous sheath and which are primitively always attached
proximally to a cartilaginous intercentrum. Chevrons are ossified basiventrals
and therefore homologous with haemal arches.
The presence of an atlas and an axis formed in ontogeny from several
elements (neural arches, centra, intercentra) is a specialization of amniotes.
There is no evidence of resegmentation either in the centrum or the arches of
any vertebrate and furthermore there is no evidence that the basalia have been
derived from the posterior half sclerotome.
Chordacentra are deduced to have formed on at least two occasions within
the chondrichthyans and perichordal membrane centra at least five times within
the actinopterygians and twice more within the rhipidistians. Centra have also
arisen at least twice within the Dipnoi, thrice within the amphibians and once in
the amniotes. Complete endochondral centra are only found in the Amniota
although they are deduced to have been present in fossil dipnoans.
It is concluded that the Temnospondyli are the sister group of the Amniota
plus Amphibia, the Loxommatidae the sister group of these three and
lchthyostega the sister group to all four.
ACKNOWLEDGEMENTS
I wish to express my gratitude to Dr Colin Patterson who has provided me
with much good advice and to colleagues Dr Donn Rosen and Dr Peter Forey
for their encouragement. I also wish to thank D r Angela Milner for supplying
information.
REFERENCES
ALBRECHT, P., 1883. Note sur une HCmivertebre gauche surnumkraire, de Python sebae, DumPril. Bulletin du
Music Royal &Histoire de Belgique, 2: 23-38.
ALDINGER, H., 1937. Permische Ganoidfische aus Ostgrenland. Meddelelser om Grmland, 102: 1-392.
ANDREWS, S. M., 1977. The axial skeleton of the coelacanth Latimeria. In S. M. Andrews, R. S. Miles & A.
D. Walker, (Eds), Problems in Vertebrate Euolution: 27 1-288. London: Academic Press.
ANDREWS, S. M. & WESTOLL, T. S., 1970a. The postcranial skeleton of Eusthenopteronfoordi Whiteaves.
Transactions of the Royal Society of Edinburgh, 68: 207-329.
ANDREWS, S. M. & WESTOLL, T. S., 1970b. The postcranial skeleton of rhipidistian fishes excluding
Eusthenopteron. Transactions of the Royal Society of Edinburgh, 68: 381489.
BAER, E. E. VON, 1835. Untersuchungen uber die Entwicklungsge~chichteder Fische nebst eiaem Anhange uber die
Schwimmbase. Leipzig: Vogel.
BAIRD, D., 1964. The aistopod amphibians surveyed. Breuiora, 206: 1-17.
BAIRD, D., 1965. Paleozoic lepospondyl amphibians. American <oologist, 5: 287-294.
BALFOUR, F. M. & PARKER, W. N., 1882. On the structure and development of Lepidosteus. Philosophical
Transactions ofthe Royal Society of London, 173: 359-442.
BARDEEN, C. F., 1906. The development of the thoracic vertebrae in man. American Journal of Anatomy, 4:
163-174.
BARTRAM, A,, 1977. The Macrosemiidae, a Mesozoic family of holostean fishes. Bulletin ofthe British Museum
(Natural History) Geology, 29: 137-234.
BAUM, K. A. & LUND, R., 1974. Vertebral centra in Haplolepis (Haplolepidae, Paleonisciformes) from the
Allegheny group, Pennsylvania. journal of Paleontology, 48: 199-200.
BAUR, G., 1886a. The Intercentrum of living Reptiles. American Naturalist, 20: 174.
BAUR, G., 188613. The ribs of Sphenodon (Hatteria). American Naturalid. 20: 979-980.
BAUR, G., 1886c. Uber die Morphologie der Wirbelsaule der Amnioten. Biologisches zentralblatt, 6: 332-342,
353-363.
BEAUMONT, E., 1977. Cranial morphology of the Loxommatidae (Amphibia: Labyrinthodontia).
Philosophical Transactions of the Royal Society of London, B, 280: 29-101.
BEER, G. R. DE, 1924. Contributions to the Study of the Development of the Head in Heterodontus. Quarterly
Journal of Microscopical Science, 68: 39-65.
GNATHOSTOME VERTEBRAE
53
BEER, G. R. DE, 1937. The Development of the Vertebrate Skull. Oxford: Clarendon Press.
BOCHMANN, G. VON, 1937. Die Entwicklung der Saugetierwirhel den hinteren Korperregionen.
Morphologisches Jahrbuch, 79: 1-53.
BOULENGER, G. A,, 1891. Notes on the osteology of Heloderma horridum and H . suspectum, with remarks on
the systematic position of the Helodermatidae and on the vertebrae of the Lacertilia. Proceedings of the
<oological Society of London, 1891: 10%118.
BOULENGER, G. A., 1893. On the nature of haemapophyses. Annals and Magazine of Natural History, 12:
6041.
BROILI, F., 1904a. Stammreptilien. Anatomischer Anzeiger, 25: 577-587.
BROILI, F., 1904b. Permische Stegocephalen und Reptilien aus Texas. Palaeontographica, 51: 1-49, 5 1-1 20.
BROOM, R., 1922. On the persistence of the mesopterygoid in certain reptilian skulls. Proceedings of the
,Zoological Society of London, 1922: 455460.
BRUNAUER, E., 1910. Die Entwicklung der Wirbelsaule hei der Ringelnatter. Arbeiten aus dem <oologischen
Instituten der Universitut Wien, 18: 133-1 56.
BUDGETT, J . S., 1902. On the structure of the larval Polypterus. Transactions of the <oological Society of London,
16: 3 15-346.
CARROLL, R. L. & GASKILL, P., 1978. The order Microsauria. Memoirs of the American Philosophical SocieQ,
126: x + 2 l l p p .
CASE, E. C., 1932. A collection of stegocephalians from Scurry County, Texas. Contributionsfrom the Museum of
Paleontology, University of Michigan, 4: 1-56.
CAVE, A. J. E., 1980. The intervertebral ossicles of the Insectivora. Journal of ,Zoology, London, 190: 109-124.
CHOWDHURY, T. R., 1965. A new metoposauroid amphibian from the Upper Triassic Maleri formation of
Central India. Philosophical Transactions of the Royal Society of London, B, 250: 1-52.
COLBERT, E. H., 1955. Evolution of the Vertebrates. A History of the Backboned Animals Through Time. New York:
Wiley.
COLBERT, E. H. & IMBRIE, J., 1956. Triassic metoposaurid amphibians. Bulletin of the American Museum of
Natural History, 111: 399452.
COPE, E. D., 1878a. The Homology of the Chevron bones. American Naturalist, 12: 319.
COPE, E. D., 1878b. A new Fauna. American Naturalist, 12: 327-328.
COPE, E. D., 1878c. Descriptions of Extinct Batrachia and Reptilia from the Permian formation of Texas.
Proceedings of the American Philosophical Society, 17: 505-530.
COPE, E. D., 1878d. Geology and Palaeontology. The Vertebrae of Rhachitomus. American Naturalist, 12: 633.
COPE, E. D., 1880. Geology and Palaeontology. Extinct Batrachia. American Naturalist, 14: 609-610.
COPE, E. D., 1882. Geology and Palaeontology. The Rhachitomous stegocephali. American Naturalist, 18:
334-335.
COPE, E. D., 1884. The Batrachia of the Permian Period of North America. American Naturalist, 18: 26-39.
COPE, E. D., 1887. The Origin of the Fittest, Essays on Evolution. New York; Appleton & Co.
COPE, E. D., 1888. On the Intercentrum of the Terrestrial Vertebrata. Transactions of the American Philosophical
Society, 16: 243-253.
COPE, E. D., 1891. On the characters of some Palaeozoic fishes. Part V. On the paired fins of Megalichthys
nitidus Cope. Proceedings of the United States National Museum, 14: 447463.
CORNING, H. K., 1891. Uber die sogenannte Neugliederung der Wirbelsaule und iiber das Schicksal der
Urwirbelhole bei Reptilien. Morphologisches Jahrbuch, 17: 61 1-622.
CREDNER, H., 1883. Die Segocephalen aus dem Rothliegenden des Plauen’schen Grundes hei Dresden. IV
Theil. <eitschnyt der Deutschen Geologischen Gesellschaft, 35: 275-300.
CREDNER, H., 1890. Die Stegocephalen und Saurier aus dem Rothliegenden des Plauen’schen Grundes bei
Dresden. I X Theil. ,Zeitschrift der Deutschen Geologischen Gesellschaft, 42: 240-277.
CREDNER, H., 1891. Die Urvierfiissler (Eotetrapoda) des sachsischen Rothliegenden. fiaturwissenschafttliche
Wochenschrift, 5: 483484, 491497, 507-509.
DAGET, J., 1950. Revision des Affinitits PhylogCnttiques des PolypttrideCs. Mkmoires de l‘hstitut Franpis
d’Afrique Noire, Centre de Cameroun, 11: 1-178.
DAWES, B., 1930. The development of the vertebral column in Mammals as illustrated by its development in
Mus musculus. Philosophical Transactions of the Royal Society of London, B, 218: 115-170.
DEAN, B., 1909. Studies on fossil fishes (sharks, chimaeroids, and arthrodires). Memoirs from the American
Museum of Natural History, 9: 2 11-287.
DEVILLERS, C., 1954. Structure et ivolution de la colonne verttbrale. In P. P. Grass6 (Ed.), Traitd de
<oologie, 12: 605472. Paris: Masson et Cie.
DOLLO, L., 1889. Sur le proatlas. <oologische Jahrbucher, Anatomie, 3: 433446.
EATON, T. H., 1959. The ancestry of modern Amphibia: a review of the evidence. University of Kansas
Publications. Museum o f Natural History, 12: 157-180.
EBNER, V. VON, 1888. Urwirbel und Neugliederung der Wirbelsaule. Sitzungsberichte der Akademie der
Wissenschaften, 97: 194-206.
EBNER, V. VON. 1892. Uber die Beziehungen der Wirbel zu den Urwirbeln. Sitzungsberichte der Akademie der
Wissenschaften, 101: 235-260.
EBNER, V. VON. 1895. Ueber den Bau der chorda dorsalis des Amphioxus lanceolatus. Sitzungsberichte der
Akademie der Wissmchaftten, 104: 199-228.
54
B. G. GARDINER
EGERTON, P. G . , 1837. O n certain peculiarities in the cervical vertebrae of the Ichthyosaurus, hitherto
unnoticed. Transactions of the Geological Society, 5(2): 187-193.
EGERTON, P. G., 1861. Tristichopterus alatus. In Figures and Descriptions Illustrative of British Organic Remains.
Memoirs of the Geological Survy of Great Britain. Decade X : 5 1-55.
EMELIANOV, S. V., 1935. Die Morphologie der Fischrippen. xoologische Jahrbiicher f u r Anatomie, 60: 133-262.
EMELIANOV, S. W., 1936. Die Morphologie der Tetrapodenrippen. zoologische Jahrbiicher f u r Anatomie, 62:
173-274.
EMELIANOV, S. V., 1939. Sequence in the ontogenetic appearance of vertebral arches in teleosts and the
omission of chondral stages in their development. Dokladj Akademii Nauk SoyuZa Souetskikh Sotsialisticheskikh
Respublik, 23: 978-981.
ETHERIDGE, R., 1967. Lizard caudal vertebrae. Copeia, 4: 699-721.
FARUQUI, A. J., 1935. The development of the vertebral column in the haddock (Gadus aegleJinus). Proceedings
of the zoological h i e & of London, 2: 3 13-332.
FIELD, H. H., 1895. Bemerkungen uber die Entwicklung der Wirbelsaule bei der Amphibien; nebst
Schilderung eines abnormen Wirbelsegementes. Morphologisches Jahrbiich, 22: 340-356.
FRAAS, E., 1889. Die Labyrinthodonten der schwabischen Trias. Palaeontographica, 36: 1-158.
FRANCOIS, Y . , 1966. Structure et dkveloppement d e la vertkbrae de Salmo et des tC1Costiens. Archives de
zoologie Expe‘rimentale et Gintrale, 107: 287-328.
FRANQUE, H., 1847. Affaruntur nonnulla ad Amiam calvam (Lin.) accuratius cognoscendum. Dissertatio inauguralis
comparto-anatomica. Berlin: Gustavi Shade.
FRITSCH, A,, 1883-1895. Fauna de Gaskohle und der Kalksteine der Pernformation Bohmens. Prag, 1885, Vol. 11,
pt. 1: 1-32.
FRORIEP, A,, 1883. Zur Entwicklungsgeschichte der Wirbelsaule, insbesondere des Atlas und Epistropheus
und der Occipitalreson. I Beobachtung an Hiihnerembryonen. Archiv f & Anatomie und Physiologie, 1883:
177-234.
FRORIEP, A,, 1886. Zur Entwicklungsgeschichte der Wirbelsaule, insbesondere des Atlas und Epistropheus
und der Occipitalregion. I1 Beobachtung an Saugethierembryonen. Archio fcr Anatomie und
Entwickelungsgeschichte, 1886: 69- 150.
GABRIEL, M . L., 1944. Factors affecting the number and form of vertebrae in Fundulus heteroclitus. Journal of
Experimental zoology, 95: 105-147.
GADOW, H., 1896. O n the evolution of the vertebral column of amphibia and amniota. Philosophical
Transactions ofthe Royal Society of London, B, 187: 1-57.
GADOW, H., 1901. Amphibia and Reptiles. I n S. F. Harmer & A. E. Shipley (Eds), The Cambrzdge Natural
History, 8: xii 668. Cambridge: Cambridge University Press.
GADOW, H. F. 1933. The Evolution of the Vertebral Column. Cambridge: Cambridge University Press.
GADOW, H. & ABBOTT, E. C., 1895. O n the evolution of the vertebral column of fishes. Philosophical
Transactions of the Royal Society of London, B, 186: 163-22 1.
GAFFNEY, E. S., 1979. Tetrapod monophyly: a phylogenetic analysis. Bdletin of the Carnegie Museum of
Natural History, 13: 92-105.
GAMBLE, D. L., 1922. The morphology of ribs and transverse processes in Necturus maculatus. Journal of
hf07phOlOU, 36: 537-566.
GANGULY, D. N. & MITA, B., 1962. O n the vertebral column of the teleostean fishes of different habits and
habitats. 1. A4ugul corsula, Pama pama, Triacanthus brevirostris and Andamia heteroptera. Anatoniischer Anzeiger,
110: 289-3 1 1.
GARDINER, B. G . , 1982. Tetrapod classification. zoological Journal of the Linnean Society, 74: 207-232.
GAUDRY, A,, 1878. Les Reptiles de l’kpoque permienne aux environs d’Autun. Bulletin de la Sociltt Gtologique
de France, 7(3:1:62-77.
GAUDRY, A., 1883. Les Enchainements du Monde Animal dans les Temps Gtologiqites. Paris: Savy.
GEGENBAUR, C., 1862. Untersuchungen zur uergleichenden Anatomie der Wirbelsaule bei Amphibien und Reptilien.
Leipzig: W. Engelmann.
GEGENBAUR, C., 1867. Ueber die Entwicklung der Wirbelsaule des Lepidosteus mit vergleichendenanatomischen Bemerkungen. Jenaische zeitschrqt f u r Medizin und Naturwissenschaften, 3: 359420.
GOETTE, A,, 1875. Die Entmickelungsgeschichte der Unke (Bombinator ingneus) als Grundlage einer uergleichenden
~Morphologieder Wirbelthiere. Leipzig: L. Voss.
GOETTE, A,, 1897. Uber den Wirbelbau bei den Reptilien und einigen anderen Wirbelthieren. <eitschriffur
Wissenschaftliche <oologie, 62: 343-394.
GOLDFUSS, G. A., 1847. Beitrage zur vormeltichen Fauna des Steinkohlengebirges. Bonn: Henry & Cohen.
GOODEY, T., 1910. A contribution to the skeletal anatomy of the frilled shark, Chlamydoselachus anguineus Gar.
Proceedings of the zoological Society of London, 19: 340-57 1.
GOODRICH, E. S., 1909. Vertebrata Craniata. First Fascicle: Cyclostomes and Fishes. In E. R . Lankester
(Ed.), A Treatise on ,5001ogy, 9: 518 pp, London: Black.
GOODRICH, E. S., 1930 Studies on the Structure and Development of Vertebrates. London: Macmillan & Co.
GOPPERT, E., 1896. Die Morphologie der Amphibienrippen. I n Festschrift zum Siebenzigsten Geburtstage aon
Carl Gegenbaur, I: 393-346. Leipzig: Engelmann.
GROSS, W., 1963. Gemuendina stuertzi Traquair. Neuuntersuchung. Notizblatt des Hessischen Landesamtes f u r
Bodenforschung zu Wiesbaden, 91: 36-73.
+
GNATHOSTOME VERTEBRAE
55
HASSE, C., 1873. Die Entwicklung des Atlas und Epistropheus des Menschen und der Saugethiere. I n C.
Hasse (Ed.), Anatomische Studien, I : 21-1 71, 542-566. Leipzig: Engelmann.
HASSE, C., 1879-1885. D a s naturliche System der Elasmobranchier auf Grundlage des Baues und der Entwicklung ihrer
Wirbelsaule. Eine morphologische und palaeontologische Studie. vi 76pp., 2pls, 1879; vi +94pp., 12pls, 1882;
pp. 95-179, 11 pls, 1882; pp. 180-284, 17pls, 1882; 27pp., Ipl, 1885. Jena: Fischer.
HASSE, C., 1892a. Die Entwicklung der Wirbelsaule der ungeschwantzen Amphibien. Zweite Abhandlung
iiber die Entwicklung der Wirbelsaule. Zeitschnft fur Wissenschaftliche Zoologie, 55: 252-263.
HASSE, C., 1892b. Die Entwicklung der Wirbelsaule der Elasmobranchier. Dritte Abhandlung iiber die
Entwicklung der Wirbelsaule. Zeitschrifi fur Wissemchaftliche Zoologie, 55: 5 19-53 1.
HASSE, C., 1893. Die Entwickling der Wirbelsaule der Dipnoi. Vierte Abhandlung iiber die Entwicklung der
Wirbelsaule. ZeitschriJ fur Wissenschaftliche <oologie, 55: 533-542.
HASSE, C. & SCHWARK, W., 1873. Studien zur vergleichenden Anatomie der Wirbelsaule insbesondere
des Menschen und der Saugethiere. In C. Hasse (Ed.), Anatomische Studien, I: 816 pp. Leipzig: Engelmann.
HAY, 0. P., 1895. On the Structure and development of the vertebral column of Amia. Publications of the Field
Museum o f Natural H i s t o y , <oological Series, 1: 5-54.
HAY, 0, P., 1913. O n the collection of Upper Cretaceous fishes from Mount Lebanon, Syria, with
descriptions of four new genera and nineteen new species. Bulletin of the American Museum of Natural H i s t o v ,
19: 3955452.
HIGGINS, G. M., 1923. Development of the primitive reptilian vertebral column as shown by a study of
Alligator mississippiensis. American Journal of Anatomy, 31: 373-407.
HIS, W., 1868. Untersuchungm uber die erste Anlage des Wirbelthierleibes. Die erste Entwickelung des Hunchens im Ei.
Leipzig: Vogel.
HOFFSTETTER, R. & GASC, J.-P., 1969. Vertebrae and ribs of modern reptiles. In C. Gans, A. d’A.
Bellairs & T . S. Parsons (Eds), Biology of the Reptilia, I : 201-310. London: Academic Press.
HOFMANN, C. K., 1878. Beitrage zur vergleichenden Anatornie der Wirbelthiere. Niederlandsches Archiu f i r
<oologie, 4: 112-248.
HOLMGREN, N., 1933. On the origin of the tetrapod limb. Acta Zoologica, Stockholm, 14: 185-295.
HOWES, G. B. & SWINNERTON, H. H., 1901. On the development of the skeleton of the Tuatara
Sphenodon punctaks with remarks on the egg, on the hatching and on the hatched young. Transactions of the
<oological Society of London, 16: 1-86.
HOWIE, A. A., 1972. On a Queensland labyrinthodont. In K. A. Joysey & T . S. Kemp (Eds), Studies in
Vertebrate Euolution: 5 1 4 4 . Edinburgh: Oliver & Boyd.
HUENE, F. VON, 1922. Beitrage zur kenntnis der Organisation einiger Stregocephalen der Schwabischen
Trias. Acta Zoologica, Stockholm, 3: 395-460.
HUXLEY, T. H., 1871. O f t h e Anatomy of Vertebrated Animals. London: Churchill.
IVACHENKO, M. F., 1981. Discosauricids from the Permian of Tadjikistan. (In Russian).Paleontologischeskit
zhurnal, 1981: 114-128.
JAGER, G., 1859. Das Wirbelkorpergelenk der Vogel. Sitzungsberichte der Akademie der Wissenschaften, 33:
527-564.
JARVIK, E., 1942. On the structure of the snout of crossopterygians and lower gnathostomes in general.
Zoologiska Bidrag fran Uppsala, 21 (3): 235475.
JARVIK, E., 1952. On the fish-like tail in the ichthyostegid stegocephalians with descriptions of a new
stegocephalian and a new crossopterygian from the Upper Devonian of East Greenland. Meddelelser om
Grenland, 114: 1-90.
JARVIK, E., 1980. Basic Structure and Evolution of the Vertebrates, 1. London: Academic Press.
JHERING, H. VON, 1878. Das peripherische Nervemystem der Wirbelthiere als Grundlage fur die Kenntmiss der
Regionenbildung der Wirbelsaule. Leipzig: Vogel.
JOLLIE, M., 1962. Chordate Morphology. London: Chapman & Hall.
KERR, J. G., 1919. Textbook OfEmbryology. I1 Vertebrates with the exception of Mammalia. London: Macmillan &
co.
KLAATSCH, H., 1893a. Beitrage zur vergleichenden Anatomie der Wirbelsaule: I. uber den Urzustand der
Fischwirbelsaule. Morphologisches Jahrbuch, 19: 649480.
KLATTSCH, H., 1893b. Beitrage zur vergleichenden Anatomie der Wirbelsaule: 11. uber die Bildung
knorpeliger Wirbelkorper bei Fischen. Morphologisches Jahrbiich, 20: 143-186.
KLAATSCH, H., 1895. Beitrage zur vergleichenden Anatomie der Wirbelsaule: 111. Zur Phylogenese der
Chordascheiden und zur Geschichte der Umwandlungen der Chordastruktur. Morphologisches Jahrbuch, 22:
5 14-560.
KOLLIKER, A., 1860. 1. Ueber die Beziehungen der Chorda dorsalis zur Bildung der Wirbel der Selachier
und einiger anderen Fische. 2. Kritische Bemerkungen zur Geschichte der Untersuchungen iiber die
Scheiden der Chorda dorsalis. Verhandlungen der Physikalisch-Medizinischen Gesellschaft zu Wurzburg, 10:
193-242.
KUSNETZOV, V. V. & IVACHENKO, M. F., 1981. Discosauriscids from the Upper Palaeozoic of the
southern part of Kazakhstan (In Russian.) Paleontologicheskii <hurnal, 1981: 102-1 10.
LEHMAN, J. P., 1959. Les Dipneustes du Dtvonien supkrieur du Groenland. Meddelelser om Grmland, 160:
1-58.
+
56
B. G. GARDINER
LEHMAN, J. P., 1966. Dopnoi et Crossopterygii. In J. P. Lehman (Ed.), Traitd de Palhtologie, 4 (3). Paris:
Masson.
LOTZ, T., 1864. Ueber den Bau der Schwanzwirbelsaule der Salmoniden Cyprinoiden, Percoiden und
Cataphracten. <eitschrift f u r Wissenschaftliche <oologie, 14: 8 1-106.
MANNER, H., 1899. Beitrage zur Entwicklungsgeschichte der Wirbelsaule bei Reptilien. Zeitschrifi f u r
Wissenschaftliche <oologie, 66: 43-68.
MARCUS, H., 1937. uber Myotome Horizontal septum und Rippen bei Hypogeophis und Urodelen. Zeztschrift
f i r Anatoniie und Entwickelungsgeschichte, 107: 53 1-552.
MARCUS, H . & BLUME, W., 1926. Wirbel und Rippen bei Hypogeophis. zeitschrft f u 7 Anatomie und
Entwickelungsgeschichte,80: 1-78.
MATHEWS, M. B., 1980. 14. Coevolution of collagen. I n A. Viidik & S. Vaust (Eds), Biology of Collagen:
193-209. London: Academic Press.
MAYER, A. F. J. C., 1834. u b e r ein neuentdecktes Band, Jochband der Rippen (Ligamentum costarum
conjugale). Archiu fur Anatomie und Physiologie und Wissenschaftliche Medicin, 1834: 273-277.
MEYER, H. VON., 1857. Beitrage zur Naturgeschichte der Vorwelt. Palaeontographica, 6: 1-252.
MILES, R. S., 1977. Dipnoan (lungfish) skulls and the relationships of the group: a study based on new
species from the Devonian of Australia. <oological Journal o f t h e Linnean Society, 61: 1-328.
MILLOTT, J. & ANTHONY, J., 1956. Considkrations prkliminaries sur le squelette axial et le systkme
nerveux central de Latimeria chalumnae Smith. Mimoirs de l'lnstitut Scientifque de Madagascar, 11: 167-188.
MOFFAT, L. A. & BELLAIRS, A. d'A., 1964. The regenerative capacity of the tail in embryonic and postnatal lizards (Lacerta uivipara Jacquin). Journal o f Embryology and Experimental Morpholou, 12: 769-786.
MOOKERJEE, H. K., 1930. O n the development of the vertebral column of Urodela. Philosophical
Transactions of the Royal Society of London, B, 218: 415-446.
MOOKERJEE, H. K., 1936. The development of the vertebral column and its bearing on the study of
organic evolution. Proceedings of the Indian Science Congress, 23: 307-343.
,MOOKERJEE, H. K. & GANGULY, D. N., 1951. The study of the development of the vertebral column in
the Elasmobranchii as shown in the life-history of Scoliodan palasorrah and Narcline timlei. Proceedings of the
Indian Science Congress, 38: 224-225.
MOOKERJEE, H. K., GANGULY, D. N. & BRAHMA, S. K., 1954. O n the development of the centrum
and its arches in the Dipnoi Protopterus annectens. Anatomischer Anzeiger, 100: 2 17-230.
MOY-THOMAS, J. A., 1935. The structure and affinities of Chondrenchelys problematica T r . Proceedings of the
<oological Sociely of London, 1935: 39 1 4 0 3 .
MCLLER, A., 1853. Beobachtungen zur vergleichenden Anatomie der Wirbelsaule. Archiv f@r Anatomie und
Physiologie und CVissenschaftliche Medicin, 1853: 206-3 16.
NIELSEN, E., 1942. Studies on Triassic fishes from East Greenland. I. Glaucolepis and Boreosomus. Meddelelser
om Grmland, 138: 1 4 0 3 .
NIELSEN, E., 1949. Studies on Triassic fishes from East Greenland. I1 Australosomus and Birgeria. Meddelelser
om Granland, 146: 1-309.
NILSSON, T., 1937. Ein Plagiosauride aus dem Rhat Schonens. Beitrage zur kenntnis der Organisation der
Stegocephalengruppe Brachyopoidei. Acta Uniuersitatis Lundensis, 34: 1-75.
NILSSON, T., 1946. A new find of Gerrothorax rhaeticus Nilsson, a plagiosaurid from the Rhaetic of Scania. Acta
Uniuersitatis Lundensis, 42: 1 4 2 .
BRVIG, T., 1960. New finds of acanthodians, arthrodires, rrossopterygians, ganoids and dipnoans in the
Middle Devonian calcareous flags (Oberer Plattenkalk) of the Bergisch Gladbach-Paffrath Trough 1,
Palaeontologische <eitschr& 34: 295-335.
OSBORN, H . F., 1900. Intercentra and hypapophyses in the cervical region of Mosasaurs, lizards and
Sphenodon. American Naturalisl, 34: 1-7.
OWEN, R., 1847. Report on the Archetype and Homologies of the Vertebrate Skeleton. Report of the British
Association for the Advancement of Science, 16: 169-340.
OWEN, R., 1850. A History of British Fossil Reptiles, I : Crocodilia, Ophidia. London: Cassell.
OWEN, R., 1853. Descriptive catalogue of the osteological series contained in the Museum of the Royal College of Surgeons,
England. 1 pt. 1. Pisces, Reptilia, Aues, Marsupialia. London: Taylor & Francis.
OWEN, R., 1854. Descriptiue catalogue of fossil organic remains of Reptilia and Pisces contained in the Museum of the
Royal College of Surgeons, England. London: Taylor & Francis.
OWEN, R., 1861. Palaeontology. A systematic summary of extinct animals and their geological relations, 2nd ed.
Edinburgh: Black.
OWEN, R., 1866--1868. Comparative anatomy andptyiology of vertebrates (or On the anatomy of zerlebrates). 1. Fishus
and reptiles, 18&. 2. Birds and mammals, 1866. 3. Mammals, 1868. London: Longmans, Green & Go.
PANCHEN, A. L., 1959. A new armoured amphibian from the Upper Permian of East Africa. Phzlosophirnl
Transactions of the Royal Society of London, B, 242: 207-28 I .
PANCHEN, A. L., 1963. The homologies of the Labyrinthodont centrum. International Congress of <oology, 16:
161.
PANCHEN, A. L., 1966. The axial skeleton of the labyrinthodont Eogyrinus attheyi. Journal of ~ o o l o g y ,150:
199-222.
PANCHEN, A. L., 1967. The homologies of the labyrinthodont centrum. Euolution, 21: 24-33.
GNATHOSTOME VERTEBRAE
57
PANCHEN, A. L., 1970. Anthracosauria. In 0. Kuhn (Ed.), Handbuch der Paliioherpetologie, 5a: 1-84.
Stuttgart: Fischer.
PANCHEN, A. L., 1977a. The origin and early evolution of tetrapod vertebrae. In S. M. Andrews, R. S.
Miles & A. D. Walker (Eds), Problem in Vertebrate Euolution: 289-318. London: Academic Press.
PANCHEN, A. L., 1977b. O n Anthracosaurus russelli Huxley (Amphibia: Labyrinthodontia) and the family
Anthracosauridae. Philosophical Transactions of the Royal Society of London, B, 279: 447-5 12.
PANDER, C. H., 1858. uber die Ctenodipterinen des Deuonischen Systems. St. Petersburg: Kaiserlichen Akademie
der Wissenschaften.
PARRINGTON, F. R., 1948. Labyrinthodonts from South Africa. Proceedings of the <oologicaI Society of London,
118: 426445.
PARRINGTON, F. R., 1967. The vertebrae of early tetrapods. Colloques internationaux du Centre National de la
Recherche Scientifique, 163: 269-279.
PARRINGTON, F. R., 1977. Intercentra: a possible functional explanation. In S. M. Andrews, R. S. Miles
& A. D. Walker (Eds), Problem in Vertebrate Euolution: 397-401. London: Academic Press.
PATTERSON, C., 1965. The phylogeny of the chimaeroids. Philosophical Transactions of the Royal Society of
London, B, 249: 101-219.
PATTERSON, C., 1968. The caudal skeleton in Lower Liassic pholidophorid fishes. Bulletin of the British
Museum (Natural History), Geology, 16: 201-239.
PATTERSON, C., 1973. Interrelationships of holosteans. In P. H. Greenwood, R. S. Miles & C. Patterson
(Eds),Interrelationships of Fishes: 233-305. London: Academic Press.
PATTERSON, C., 1977a. Cartilage bones, dermal bones and membrane bones, or the endoskeleton versus
the exoskeleton. In S. M. Andrews, R. S. Miles & A. D. Walker (Eds), Problem in Vertebrate Euolution:
77-1 21. London: Academic Press.
PATTERSON, C., 1977b. The contribution of paleontology to teleostean phylogeny. In M. K. Hecht, P. C.
Goody & B. M. Hecht (Eds), Major Patterns in Vertebrate Euolution: 579-643. New York: Plenum Press.
PATTERSON, C. & ROSEN, D. E., 1977. Review of ichthyodectiform and other Mesozoic teleost fishes and
the theory and practice of classifying fossils. Bulletin of the American Museum of Natural History, 158: 81-172.
PETER, K., 1894. Die Wirbelsaule der Gymnophionen. Bericht (iiber die Verhandlungen) der Natu7frschenden
Gesellschaft zu Freiburg i. Breisgau, 9: 35-58.
PIIPER, J., 1928. On the evolution of the vertebral column in birds, illustrated by its development in Larus
and Struthio. Philosophical Transactions of the Royal Society of London, B, 216: 285-351.
PIVETEAU, J., 1926. Paleontologie de Madagascar-XI1 Amphibiens et Reptiles permiens. Annales de
Paliontologie, 15: 55-179.
PRATT, C. W. M., 1946. The plane of fracture of the caudal vertebrae of certain lacertilians. Journal of
Anatomy, London, 80: 184-188.
RAMANUJAM, S. G . M., 1929. The study of the development of the vertebral column in teleosts, as shown
in the life-history of the herring. Proceedings of the <ooZogical Society of London, 25; 364414.
RATHKE, H., 1839. Entwickelungsgeschichte der Natter (Coluber natrix). Konigsberg: Borntrager.
RATHKE, H., 1848. Ueber die Entwickelung der Schildkroten. Braunschweig: F . Vieweg & Sohn.
REITER, A,, 1942. Die Friihentwickelung der menscheichen Wirbelsaule. I. Mitteilung. Die
Friihentwickelung der Brustwirbelsaule. Archiv f u r Analomie und Entwickelungsgeschichte,II2: 158-200.
REMAK, R., 1850-1855. Untersuchungen uber die Entwickelung der Wirbelthiere. Berlin: G. Reimer.
REMAK, R., 1851. Untersuchungen uber die Entwickelung der Wirbelthiere. (I. Ueber die Entwickelung des Huhnchens i m
Eze). Berlin: G. Reimer.
REMANE, A,, 1936. Wirbelsaule und ihre Abkommlinge. In L. Bolk (Ed.), Handbuch der uergleichenden Anatomie
der Wirbeltiere, 4: 1-206. Berlin: Urban & Schwarzenberg.
RIDEWOOD, W. G., 1897. The development of the vertebral column in Pipa and Xenopus. Anatomzscher
Anzeiger, 13: 359-375.
RIDEWOOD, W. G., 1899. Some observations on the caudal diplospondyly of sharks. Journal o f t h e Linnean
Society of London, <oology, 27: 46-59.
RIDEWOOD, W. G., 1921. Calcification of vertebral centra in sharks and rays. Philosophical Transactions of the
Royal Society, B, 210: 31 1-407.
ROCKWELL, H., EVANS, F. G. & PHEASANT, H, C., 1938. The comparative morphology of the
vertebrate spinal column. Its form as related to its function. Journal of Morphology, 63: 87-1 17.
ROMER, A. S., 1928. A skeletal model of the primitive reptile Seymouriu, and the phylogenetic position of that
type. Journal of Geology, 36: 248-260.
ROMER, A. S., 1933. Vertebrate Paleontology. Chicago: University Press.
ROMER, A. S., 1945. Vertebrate Paleontology, 2nd Ed. Chicago: University Press.
ROMER, A. S., 1947. Review of the Labyrinthodonta. Bulletin of the Museum of Comparatiue <oology, Haruard
College, 99: 1-368.
ROMER, A. S., 1966. Vertebrate Paleontology, 3rd Ed, Chicago: University Press.
ROMER, A. S., 1968. Notes and Comments on Vertebrate Paleontology. Chicago: University Press.
ROSEN, D. E., FOREY, P. L., GARDINER, B. G . & PATTERSON, C., 1981. Lungfishes, tetrapods,
paleontology and plesiomorphy. Bulletin of &heAmerican Museum of Natural History, 167: 159-276.
SAITO, K., 1936. Mesozoic leptolepid fishes from jehol and Chientao, Manchuria. Report f r o m thejrst Scientific
Expedition to Manchuckuo, 2: 1-23.
58
B. G. GARDINER
SAVE-SODERBERGH, G., 1933. The dermal bones of the head and the lateral line in Osteolepis macrolepidotus
Ag., with remarks on the terminology of the lateral line system and on the dermal bones of certain other
crossopterygians. Noua Acta Regiae Societatis Scientiarum Upsaliensis, 9: 1-1 30.
SAVE-SODERBERGH, G., 1935. O n the dermal bones of the head in labyrinthodont stegocephalians and
primitive Reptilia. Meddelelser om Grenland, 98: 1-21 1.
SAVE-SODERBERGH, G., 1936. O n the morphology of Traissic stegocephalians from Spitzbergen, and the
interpretation of the endocranium in the labyrinthodontia. Kungliga Suenska Vetenskapsakademiens Hundlingar,
16: 1-181.
SAVE-SODERBERGH, G., 1937. On Rhynchodipterus elginensis n.g., n.sp., representing a new group of
Dipnoan-like Choanata from the Upper Devonian of East Greenland and Scotland. A preliminary note.
Arkiufer zoologie, 29: 1-8.
SAWIN, H. J., 194.5. Amphibians from the Dockum Triassic of Howard County, Texas. Unicersity of Texas
Publications, 4401: 361-399.
SCHAEFFER, B., 1960. The Cretaceous holostean fish Macrepistius. American Museum Nouitates, 2011: 1-18.
SCHAEFFER, B., 1967. Osteichthyan vertebrae. In C . Patterson & P. H. Greenwood (Eds), Fossil Vertebrates,
Papers presented to Dr. E. I. White: 185-195. London: Academic Press.
SCHAUINSLAND, H., 1900. Weitere Beitrage zur Entwickelungsgeschichte der Hatteria. Archtc fur
Mikroskopische Anatomie, 56: 747-867.
SCHAUINSLAND, H., 1903. Beitrage zur Entwickelungsgeschichte und Anatomie der Wirbeltiere. I.
Sphenodon, Callorhynchus, Chamaleo. 11. Studien zur Entwickelungsgeschichte der Sauropsiden. 111. Beitrage
zur Kenntnis der Eihaute der Sauropsiden. zoologica, 16: 1-98, 99-143, 145-168.
SCHAUINSLAND, H., 1906. Die Entwickelung der Wirbelsaule nebst Rippen und Brustbein. In H. Oskar
f Ed.), Handbuch der uergleichenden und e.vperimentellen Entwickelungslehre der Wirbeltiere, 3: 339-572. Jena: Gustav
Fischer.
SCHMALHAUSEN, I. I., 1968. The Origin of Terrestrial Vertebrates. New York: Academic Press.
SCHMIDT, L., 1892. Untersuchungen zur Kenntnis der Wirbelbaues van Amia calua. zeitschrzft fur
Wissenschaftliche zoologie, 54: 748-764.
SCHULTZ, O., 1896. Uber embryonale und bleiblende Segmentierung. Verhandlungen der Anatomischen
Gesellschaft, 10: 87-93.
SCHGLTZE, H.-P., 1969. Die Faltenzahne der rhipidistiiden Crossopterygier, der Tetrapoden und der
Actinopterygien--Gattung Lepisosteus. Palaeontographia Italica, 65: 60-1 37.
SCHULTZE, H.-P., 1970. Die Histologie der Wirbelkorper der Dipnoer. Neues Jahrbuch fir Geologie und
Palaontologie, Stuttgart, 135: 3 1 1-336.
SCHWARK, W., 1873. Beitrage zur Entwickelungsgeschichte bei den Vogeln. In C. Hasse (Ed.), Anatomische
Studien, I: 569-582. Leipzig: Engelmann.
SENSENIG, E. C . , 1943. The origin of the vertebral column in the dear-mouse Peromyscus maniculatus rujnus.
Anatomical Record. 86: 123-141.
SENSENIG, E. C., 1949. The early development of the human vertebral column. Contributions to Embryology,
33: 21-41.
SHUTE, C. C. D., 1972. The composition of vertebrae and the occipital region ofthe skull. In K. A. Joysey &
T. S. Kemp (edsj, Studies in Vertebrate Evolution: 21-34. Edinburgh: Oliver & Boyd.
SIEBENROCK, F., 1894. A contribution to the osteology of Hatteria. Annals and Magazine of Natural History,
13(6):297-311.
SPINAR, 2. V., 1952. Revise ntkterych moravskych Diskosauriscidu (Labyrinthodontia). (English summary.)
Rosprav Ustiedrfiho Ustauu Geologickkho, 15: 1-160.
STEEN, M. C., 1937. O n Acanthostoma uorax Credner. Proceedings of the zoological Society of London, 107: 491-500.
STENSIO, E. A., 1959. O n the pectoral fin and shoulder girdle of the arthrodires. Kungliga Svenska
Vetenskapsakad~miensHandlingar, 8: 1-229.
SUSHKIN, P. P., 1925. O n the representatives of the Seymouriamorpha, supposed primitive reptiles from the
Upper Permian of Russia and on their phylogenetic relations. Occasional Papers of the B o s h So&& of Natural
History, 5: 179-181.
SUSHKIN, P. P., 1928. Notes on the Pre-Jurassic Tetrapoda from Russia. 111. O n Seymouriamorphae from
the Upper Permian of North Dvina. Palueontologia Hungarica, I : 323-344.
THOMSON, K. S. & VAUGHN, P. P., 1968. Vertebral structure in rhipidistia (Osteichthyes,
Crossopterygiij with description of a new Permian genus. Postilla, 127: 1-19.
TRETJAKOFF, D., 1926a. Die funktionelle Struktur der Chordascheiden und der Wirbel bei Zyklostomen
und Fische. zeitschrift f u r <ellforschung und Mikroskopische Anatomie, 4: 266-3 12.
TRETJAKOFF, D., 1926b. Die Wirbelsaule des Neunauges. Anatomischer Anzeiger, 61: 387-396, 3 figs.
TRETJAKOFF, D., 1927. Die Chordascheiden der Urodelen. zeitschrij f u r <elCforschung und Mikroskopische
Anatomie, 5: 174-207.
VAUGHN, P. P., 1967. Evidence of ossified vertebrae in actinopterygian fish of early Permian age from
southeastern Utah. Journal of Paleontology, 4Z: 151-160.
WADE, R. T., 1935. The Triassic Jishes of Brookuale, N e w South Wales. London: British Museum (Natural
History).
WAGNER, A,, 1861. Monographie der fossilen Fische aus den lithographischen Schiefern Bayerns.
Abhandlungen der Kaniglich Bayerischen Akademie der Wissenschaften, 9: 279-748.
GNATHOSTOME VERTEBRAE
59
WAKE, D. B., 1970. Aspects of vertebral evolution in the modern Amphibia. Forma Functio, 3: 33-60.
WAKE, D. B. & LAWSON, R., 1973. Developmental and adult morphology of the vertebral column in the
plethodontid salamander Eurycea bislineata, with comments on vertebral evolution in the Amphibia. Journal
of Morphology, 139: 251-300.
WATSON, D. M. S., 1912. The larger coal measure Amphibia. Memoirs and Proceedings ofthe Manchester Literary
and Philosophical Society, 57: 1-14.
WATSON, D. M. S., 1917. A sketch classification of the pre-Jurassic tetrapod vertebrates. Proceedings of the
<oological Society of London, 1917: 167-186.
WATSON, D. M. S., 1919a. The structure, evolution and origin of the Amphibia-The ‘Orders’ Rhachitomi
and Stereospondyli. Philosophical Transactions of the Royal Society of London, B, 209: 1-73.
WATSON, D. M. S., 1919b. On Seyrnouria, the most primitive known reptile. Proceedings ofthe <oological Society
of London, 1918: 267-301.
WATSON, D. M. S., 1926. Croonian Lecture-The evolution and origin of the Amphibia. Philosophical
Transactions of the Royal Society ofLondon, B, 214: 189-257.
WATSON, D. M. S., 1929. The Carboniferous Amphibia of Scotland. Palaeontologia Hungarica, I : 221-252.
WATSON, D. M. S., 1942. On Permian and Triassic tetrapods. Geological Magazine, 79: 81-116.
WATSON, D. M. S., 1956. The brachyopid labyrinthodonts. Bulletin of the British Museum (Natural Histoiy)
Geology, 2: 3 15-392.
WEPFER, E., 1923. Der Buntsandstein des badischen Schwarzwalds und seine Labyrinthodonten.
Monogruphien zur Geologie und Palaeontologie, l ( 2 ) : 1-101.
WIEDERSHEIM, R., 1909. Vergleichende Anatomie der Wirbeltiere. Fur studierende Bearbeitet. Jena: Gustav
Fischer.
WIJHE, J. VAN, 1922. Friihe Entwickelungsstadien des Kopf- und Rumpfskelettes von Acanthias vulgaris.
Bijdragen tot de Dierkunde, 22: 271-298.
WILEY, E. O., 1979. An annotated Linnaean Hierarchy, with comments on natural taxa and competing
systems. Systematic <oology, 28: 308-337.
WILLIAMS, E. E., 1959a. Gadow’s arcualia and the development of tetrapod vertebrae. Quarterly Reuzem of
Biology, 34: 1-32.
WILLIAMS, E. E., 1959b. Cervical ribs in turtles. Breviora, 101: 1-12.
WILLISTON, S. W., 1911. Restoration of Seyrnouria baylorensis Broili, an American Cotylosaur. Journal of
Geology, 19: 232-237.
WOODWARD, A. S., 1895. Catalogue ofthe fossilfishes in the British Museum (Natural History), 3. London: British
Museum (Natural History).
WOODWARD, A. S., 1898. Outlines of Vertebrate Palaeontology f o r Students of ,zbology. Cambridge: University
Press.
YAKOVLEV, V. N., 1962. Jurassic fishes of the order Pholidophoriformes from Karatau. (In Russian.)
Paleontologicheskil zhumal, 3: 9G10 1.
ZITTEL, K. VON, 1887. Handbuch der Palaeontologie, 3. Miinchen & Leipzig: Oldenbourg.
ZITTEL, K. VON, 1895. Grundziige der Pataeontolopie (Palaeozoologie).Munchen& Leipzig: Oldenbourg.
ZITTEL, K. VON & WOODWARD, A. S., 1932. Text-book of Palaeontology, 3. London: Macmillan.
ABBREVIATIONS USED IN FIGURES
bd
bv
c
calc
dip
epr
f
ha
ic
id
iv
lc
lig
m
mb
basidoral
basiventral
centrum
calcified ring
diapophysis
epineural rib
facet for articulation
haemal arch
intercentrum
interdorsal
interventral
lateral cartilages
transverse ligament
meniscal ring
membrane bone
BMNH British Museum (Natural History)
na
nc
nt
nts
obd
obv
oid
oiv
Pap
rc
rca
ric
sdli
trP
neural arch
nerve cord
notochord
notochordal sheath
ossified basidorsal or neural arch
ossified basiventral or haemal arch
ossified interdorsal
ossified interventral
parapophysis
rudiment of centrum
radial calcifications
rudiment of intercentrum
supradorsal ligament
transverse process