zoological Journal ofthe Linnnean Society (1982). 74: 207-232 .

With 5 figures

Tetrapod classification

BRIAN G . GARDINER

Biolog~Department. Queen Elizabeth College. London W.8

Accepted for publuatwn June 1981

The traditional palaeontological view that the mammals separated from the ‘reptiles’ before the origin
of all other living amniotes is challenged. A radical alternative hypothesis. based on a character
analysis of living tetrapods. is elaborated in which birds are considered the sister-group of mammals.
crocodiles the sister-group of those two. chelonians the sister-group of those three. and
squamates+Sphenodon the sister-group of those four . The living Amphibia are hypothesized to form a
natural group and to be the sister-group of the Amniota . Further. I conclude that the Anapsida.
Diapsida and Synapsida are paraphyletic or grade groups and no unique statements can be made
about their structure.

KEY WORDS .--C ladistics - Haemothermia - Thecodontia - Euamniota - Lissamphibia

phylogeny.

CONTENTS

Introduction . . . . . . . . . . . . . . . . . . . 208
Historical survey . . . . . . . . . . . . . . . . . . 209
Mammalian relationships . . . . . . . . . . . . . . . . 211
Heart . . . . . . . . . . . . . . . . . . . . 211
Aortic arches . . . . . . . . . . . . . . . . . . 212
Occipital condyle . . . . . . . . . . . . . . . . . 212
Mammals and birds compared . . . . . . . . . . . . . . 212
Homothermy . . . . . . . . . . . . . . . . . . 213
Brain and spinal cord . . . . . . . . . . . . . . . . 213
Crocodilian relationships . . . . . . . . . . . . . . . . 214
Dentition . . . . . . . . . . . . . . . . . . . 215
Braincase . . . . . . . . . . . . . . . . . . . 215
Heart . . . . . . . . . . . . . . . . . . . . 215
Ear . . . . . . . . . . . . . . . . . . . . 216
Chelonian relationships. . . . . . . . . . . . . . . . . 216
Braincase . . . . . . . . . . . . . . . . . . . 216
Reproductive system . . . . . . . . . . . . . . . . 217
Eye . . . . . . . . . . . . . . . . . . . . 217
Bones and cartilages . . . . . . . . . . . . . . . . 217
Rhynchocephalian relationships. . . . . . . . . . . . . . . . 217
Lepidosaurian relationships . . . . . . . . . . . . . . . . 218
Vertebral column . . . . . . . . . . . . . . . . . 218
Hooked 5th metatarsal . . . . . . . . . . . . . . . . 218
Amphibian relationships . . . . . . . . . . . . . . . . 219
Vertebral column . . . . . . . . . . . . . . . . . 220
Cutaneous respiration . . . . . . . . . . . . . . . . 220
Summary of living tetrapod relationships . . . . . . . . . . . . 220
207
+
0024-4082/82/030207 26 $02.00/0 0 1982 The Linnean Society of London
208 B. G. GARDINER
Fossil tetrapods . . . . . . . . . . . . . . . . . . 220
Mammalia . . . . . . . . . . . . . . . . . . 220
Triconodonta . . . . . . . . . . . . . . . . . 220
Pterosauria . . . . . . . . . . . . . . . . . . 221
Dinosauria . . . . . . . . . . . . . . . . . . 222
Megalosauridae. . . . . . . . . . . . . . . . . 222
Mammal-like reptiles . . . . . . . . . . . . . . . . 223
Cvnodontia. . . . . . . . . . . . . . . . . . 224
Dicynodontia . . . . . . . . . . . . . . . . . 225
Pelycosauria . . . . . . . . . . . . . . . . . 225
Amphibia . . . . . . . . . . . . . . . . . . . 226
Nectridia and histopoda. . . . . . . . . . . . . . . 226
Temnospondyli . . . . . . . . . . . . . . . . . 226
Summary of fossil tetrapod relationships. . . . . . . . . . . . . 227
Conclusions . . . . . . . . . . . . . . . . . . . 221
Tetrapod classification . . . . . . . . . . . . . . . . . 228
Acknowledgements. . . . . . . . . . . . . . . . . . 229
References. . . . . . . . . . . . . . . . . . . . 229

INTRODUCTION
That the tetrapods are a natural assemblage cannot be doubted. The
pentadactyl limb with its carpus, tarsus and dactyly convinces us of this
fact. Within the assemblage there are several clearcut groups such as mam-
mals, birds, crocodiles, turtles, lizards and snakes, each of which may be
characterized and distinguished from the others. These individual groups exhibit
patterns of characters which, by the application of cladistic methodology, can be
shown to fit into a series of nested sets (Fig. 2). These nested sets reflect the
distribution of homologies (synapomorphies), and the resulting cladogram
produced by such analysis indicates the relationship between the groups, and
appears to be the only unambiguous way of indicating relationships.
In this paper I endeavour to distinguish and characterize the various living
tetrapod groups and to indicate their relationships to one another. Having
achieved this for the Recent groups I shall attempt to fit some of the better known
fossil groups within this framework.
That there is as yet no acceptable phylogeny of the tetrapods (see Lavtrup,
1977; Gaffney, 1979a, b; Carrol & Holmes, 1980) is hardly surprising when we
consider the characters and methods previously employed. For the most part the
vertebral structure alone has been used in the classification of the fossil and Recent
Amphibia, while in the Amniota the number of temporal openings has
traditionally been used. The practice of classifying the Amphibia on the basis of
their vertebral structure goes back to last century (Zittel, 1895) and the amniotes on
their temporal foramina to somewhat later (Osborn, 1903). Taking these two key
characters as a framework palaeontologists and comparative morphologists have,
for the past 70 years, searched for fossil sequences (using ancestor-descendent
analyses) to fill the presumed gaps in the already prescribed evolutionary sequence
they knew to be there. At the same time they have adhered to the rule of Dollo and
concluded that since Amphibia have no temporal openings then the Chelonia must
be the oldest and most primitive amniote order. The persuasiveness of this method
can be witnessed in a recent paper by Gaffney & McKenna (1979), who concluded
that the absence of Jacobson’s organ in turtles supported the idea of turtles as the
sister-group of a monophyletic Diapsida and Synapsida. Moreover, despite the fact
that fenestrae might have arisen independently (as they have done within the
 TETRAPOD CLASSIFICATION 209

Chelonia, cf. Trionyx, Emydora, Emys; and Amphibia, cf. Ceratophrys, Pelobates,
Ceratohyla), today’s unquestioned doctrine is that the Synapsida include the
mammals’ closest relatives. This widely accepted view has recently been summed
up by Lravtrup (1977: 184) as follows: “palaeozoological evidence . . . shows with
all the necessary clarity that there is an early reptilian line which, dating back to
the Lower Carboniferous, leads from Pelycosauria over Therapsida to the early
Mammalia.” The synapsids are thus supposed to show a mixture of reptilian and
mammalian characters indicative of the gradual transition between the two groups
during the course of evolution. Such a continuum has been achieved by the
establishment of a series of intermediates between a typical (fossil) primitive
amniote and a mammal, without recourse to any other living form. Furthermore,
the intermediates have only been interpreted in the light of mammals. Thus, the
theory of the origin of the mammals from synapsids, like theories of tetrapod
,origins, has followed the traditional palaeontological method of the search for
ancestors and reliance on paraphyletic groups (Rosen et al., 1981). With the
realization that some generally accepted groups (Rhachitomi, Synapsida,
Diapsida, Anapsida, Therapsida, Reptilia) are uncharacterized (that is, they have
not been demonstrated to be natural groups), the way was open for the search for
synapomorphies specifying sister-group relationships and for a new classification of
the Tetrapoda.

HISTORICAL SURVEY

One of the earliest classifications of the tetrapods was that given by John Ray
(1693). Ray, in a dichotomous systematic table of the animal kingdom, first
combined the lunged fish-like aquatic and hairy quadruped viviparous animals in
a special category (vivipara). He further paired them with the ovipara, or aves, on
the grounds that both groups were warm blooded and possessed two ventricles. He
also recognized a group of lungbearing animals distinguished by a heart with a
single ventricle which included frogs, lizards, snakes, crocodiles and turtles (Fig.
1). Since Ray had used the vernacular term for the birds Linnaeus ( 1758) was left
the privilege of naming all three classes. He named the first Mammalia and the
third Amphibia, affording them equal rank with Aves and Pisces. Ten years later,
Laurenti (1768) changed Linnaeus’ class Amphibia to Reptilia and included
within it the three orders Salientia, Gradientia (salamanders, lizards and
crocodiles) and Serpentia. Finally, in 1822 Blainville separated the amphibians
from the reptiles. Thus by the early 1800s we had arrived at a classification of the
tetrapods based upon comparative anatomy and without recourse to evolutionary
doctrine.
Following the publication of The Origin of Species in 1859, attention was directed
towards process rather than pattern, and to a search for sequences of characters
which would fit the evolutionary doctrine. In 1866 Haeckel published what is
generally regarded as the first real attempt at both a classification and phylogeny
of vertebrate animals. Haeckel recognized that the Mammalia and Amphibia were
bicondylic whereas the Reptilia and Aves possessed a single occipital condyle. He
therefore derived the Mammalia directly from the Amphibia, grouping the two
orders together as Dicondylia, while the Reptilia and Aves were regarded as a
separate offshoot termed Monocondylia. Coincidentally, in the same year the
staunch anti-evolutionist Owen (1866) placed the mammals with the birds in a
210 B. G. GARDINER

ventricle
warm blooded

pulmonary L Ovipara A S
respiration

Vertebrates

branchial Pisces
respiration

.Invertebrates
Figure 1 . Dichotomous systematic table of the tetrapods. Original in Latin, taken from Ray (1693)

group termed the Haemothermia based on the common possession of a four-

chambered heart, warm blood and spongy lungs. This latter publication was too
much for Huxley, who’ had already (1864) pointed out the essential differences
between the articulations of the skull in mammals (bicondylic) and birds and
reptiles (monocondylic). Huxley ( 1869, 1870) stressed the separation already
adopted by Haeckel, putting the Reptilia and Aves together in the group
Sauropsida (which included some nine orders of Reptilia) characterized by a single
occipital condyle. Earlier, Owen (1841) had concluded that the dinosaurs were the
nearest reptiles to the mammals but in 1870 Huxley produced evidence (mainly
the ascending process of the astragalus) of an affinity between dinosaurs and birds.
Lankester (1870) threw his weight in with Huxley stating that although “the
four cavities of the bird’s heart are generally regarded as homologous with the four
cavities of the mammalian heart . . . The disposition of the aorta and the important
light thrown on the origin of the muscular right auriculo-ventricular valve of the
bird’s heart by comparison with an Ophidian or Lacertian heart harmonize
decidedly with the conclusion that the right ventricle of the bird is not
homogenetic with the right ventricle of the mammal.’’
From this point onwards the palaeontologists took over. Owen (1876) described
the gorgonopsid Cynodraco and placed it in the new order Theriodonta because of
the resemblance of its dentition to that of mammals. But it was Cope (1884) who
really established the mammal-like reptiles and founded the concept of the
Synapsida, a group representing an ancient lineage leading by stages to the
mammals. Cope, however, was only dealing with the Pelycosauria. Yet he
concluded that in the structure of the pelvis, coracoid and hind foot pelycosaurs
closely resembled monotremes. In considering the pelycosaurs to be ancestral to
the mammals he had to overcome Huxley’s and Haeckel’s character, the
 TETRAPOD CLASSIFICATION 21 1

monocondylic reptilian occiput, as well as the presence of three ear ossicles in the
Mammalia. This he did by drawing attention to the fact that the condyle of some
geckos is double (in reality triple-see below) and by suggesting that the
collumella auris of the pelycosaurs was partly divided into three portions. It only
remained for Broom (1915) to demonstrate the close relationship of the pelycosaurs
to the South African Therapsida and the synapsid-mammalian story was
complete. Embellishment was to follow shortly when in 1916 Goodrich decided
that the structure of the ventral aorta in all living reptiles and birds differed
fundamentally from that found in mammals and furthermore that all living
reptiles and many fossils had a hooked-shaped 5th metatarsal whilst mammal-like
reptiles did not. Thus, Goodrich corroborated the palaeontological evidence
amassed by Cope and Broom as well as the evidence from Recent animals put
forward by Haeckel, Huxley and Lankester and concluded that there was a two-
fold division of all amniotes into two major types, Sauropsida (Chelonia,
Squamata, Rhynchocephalia, Crocodilia and Aves) and Theropsida (Mammalia)
and that the ancestors of the mammals were to be found in the stem-reptiles
(cotylosaurs). Over the intervening years the story has changed little. Goodrich
(1930) added that he considered the similarity of the four-chambered hearts of
mammals and birds to be misleading while Watson (1954) made the case for
recognizing the two groups on the basis of ear structure and concluded that the
theropsids embraced some primitive fossil reptiles (cotylosaurs) as well as the
synapsids. Today few workers would doubt the monophyly of the Synapsida (cf.
Hopson, 1969; Gaffney & McKenna, 1979) or Diapsida.

MAMMALIAN RELATIONSHIPS

From the evidence summarized in the historical survey above it was evident that
the denial of any immediate relationship between the mammals and the other
great homotherm group, the birds, was based on no more than three characters;
the form of the heart, aortic arches and occipital condyle.

Heart
Both Lankester (1870) and Goodrich (1930) considered the ventricles of the
avian and mammal hearts to be nonhomogenetic (nonhomologous in the
evolutionary sense). However it has been demonstrated (Foxon, 1955; Holmes,
1975) that the interventricular septum develops ontogenetically in an identical
manner in both, from the endothelial cushion of the atrio-ventricular canal and the
bulbar ridges. Moreover, in both, the ventricles become very unequally developed,
the left becoming thicker and more muscular than the right which partially
surrounds it (Goodrich, 1930).
Other characters of the heart shared by the two groups include:
Three semilunar pocket-like valves at the origin of the pulmonary artery and
aorta (two in other amniotes).
The blood from the coronary, pre- and postcaval veins passes directly into the
heart, and a complete septum sinu-venosi separates the pre- and postcaval
openings.
There is no mixing of oxygenated and deoxygenated blood.
212 B. G. GARDINER
In birds and monotremes the left auriculo-ventricular valve consists of three
membranous folds (one in other non-mammalian amniotes) but in placental
mammals there are only two folds (mitral valve).
In the development of the heart the two atria communicate with one another by
means of a n aperture-the foramen ovale. This foramen is later closed by
secondary growths which are less complicated in birds and monotremes than in
placentals.
Lastly, the venous drainage of the heart walls is by the great cardiac vein which
opens directly into the right atrium in monotremes, marsupials and birds
(Griffiths, 1978).

Aortic arches
Goodrich’s (1916) contention that the ventral aorta in all living reptiles and
birds differed fundamentally from that in mammals is similarly open to question. It
can just as easily be argued that the birds and mammals differ from all other
amniotes in having lost (during ontogeny) the right aortic trunk and that the
mammals and birds merely differ from one another in that the birds lose the left
fourth aortic arch whereas mammals lose the right. Furthermore, Holmes (1975)
has concluded that the common carotids in mammals may be derived from the
condition seen in reptiles simply by the elimination of the subdivision of the ventral
aorta into right and left aortas.

Occipital condyle
In Recent amphibians, the exoccipitals form paired condyles which articulate
with a membrane-bone atlas. In all amniotes the atlas is endochondral and
comprises three ossifications-paired neural arches and a n intercentrum. In most
amniotes other than mammals and birds these three ossifications remain separate
and each articulates anteriorly with the occipital condyle. In turn the occipital
condyle, though superficially monocondylic, is often tricondylic with the paired
exoccipitals articulating with the neural arch bases and the basioccipital with the
intercentrum. In mammals the intercentral articulation with the basioccipital is
lost and the articulation is bicondylar (except in Echidna). In birds, on the other
hand, the neural arch articulations with the exoccipital are missing and the
articulation is monocondylar. Thus, the condylar articulation with the atlas in
birds and mammals differs both from one another and from all other amniotes.
Nevertheless the developmental pattern and topographic relationships of this
complex is similar in both groups and the atlas and axis are single ossifications.

Mammals and birds compared

Now that the objections (other than palaeontological) to a close relationship
between mammals and birds had been met, it followed that on the structure of the
heart and in the possession of homothermy the birds and mammals were probably
sister-groups. A brief survey of the literature revealed numerous features of soft
anatomy, development and physiology in which mammals uniquely resemble
birds. A few of these are given below.
 TETRAPOD CLASSIFICATION 213

Homothermy
Birds, mammals and some fishes are able to maintain a constant body
temperature, but only birds and mammals are endothermal.
Endothermy requires a high aerobic capacity and metabolic rate; the resting
metabolic rate of a mammal or bird is at least five times higher than that of
ectotherms of comparable size and similar body temperature (Heller, Crawshaw &
Hammel, 1978). Furthermore, mammals and non-passerine birds have similar
temperature-corrected metabolic rates (Schmidt-Nielsen, 1979). This higher
aerobic capacity of birds and mammals can support sustained activity and only in
these two groups do we find locomotor stamina (Bennet & Rubens, 1979).
Closely associated with endothermy is thermoregulation. Although in all
vertebrates information about the ambient temperature is obtained from
peripheral sense organs, in birds (pigeon) and mammals (mouse) an additional
mechanism for monitoring the core temperature may reside within the spinal cord
(Heller et al., 1978). In both birds and mammals the thyroid hormones have a
calorigenic effect and similar hormones contribute to the regulation of body
temperature (Bentley, 1976); both exhibit non-shivering thermogenesis (Dawson
& Hudson, 1970), and both have similar behavioural responses to high and low
temperatures (e.g. huddling).
In both birds and mammals an insulating layer of fur or feathers is present.
Smooth erector muscles attached to the hair and feather follicles fluff up the
plumage or raise the pelt hair in cold weather. In addition, only birds and
mammals use shivering and panting as thermoregulatory devices, although the
python is said to shiver in order to raise the temperature of its eggs.
Hair and feathers are interscale structures (cf. barn owl legs, rodents’ tails)
which develop in a similar manner, from a papilla enclosed by a follicle, and are
always arranged in groups. Their formation is dependent on specialized groups of
dermal papilla cells lying beneath the follicle which induce the changes in the
overlying epidermal cells. In ontogeny, neural crest cells make identical
contributions to both. Moreover there is a functional association-the ‘epidennal-
melanin unit’-whereby melanin is passed from the melanocytes associated with
the feather tracts or hair follicles to the developing feathers or fur (Quevedo, 1972).
Seasonal changes in the plumage of birds and in the mammalian pelt appear to be
under photoperiodic control and are similarly mediated through the action of
gonadal steroids, corticosteroids and thyroxine, which in turn are controlled by the
hypothalamus and pituitary (Ebling & Hale, 1970). Hairs, like feathers, are
arranged in definite tracts, and in both groups some of the feathers or hairs on the
face are often bristle-like and provided with striped muscle-fibres. These are the
tactile sinus feathers or hairs. Feathers and hair are continuously growing and the
only real difference between them appears to be the presence of a distinct sheath to
the feather. But in the young hedgehog, the reflectedintegument formsa sheathwhich
later gradually shortens and draws the quill nearer to the surface (Owen, 1868).
The most logical explanation for these similarities is that feathers are modified
hairs.

Brain and spinal cord

The cerebellum shows its greatest elaboration in birds and mammals where it is
transversely and deeply folded and proportionately larger than the optic lobe. Both
211 B. G . GARDINER
have an inferior olive and pontine nuclei which project from the brainstem to the
cerebellum (Donkelaar & Nieuwenhuys, 1979). Cerebellar hemispheres are also
prominent (enlargements between the corpus cerebelli and the flocculonodular
lobe), as is a pons varolii. The cerebellar cortex is thus underlain by a thick stratum
of white matter which in section shows up as the familiar ‘arbor vitae’ so
characteristic of birds and mammals.
Covering the brain and spinal cord in birds and mammals are three meningeal
membranes, the endomenix during development having split into an inner pia
mater and an outer arachnoid layer (de Beer, 1937).
Other shared, derived characters of birds and mammals include: many
similarities of soft anatomy such as the pancreas in which the islets are
vascularized, the production of the hormone prolactin, the pineal which is
modified as an endocrine gland, containing pinealocytes and has an autonomic
sympathetic innervation arising from the superior cervical ganglion (Bentley,
1976; Quay, 1979), and the production of the neurophysial hormone oxytocin
(Kobayashi & Wada, 1973); the macula densa, a thickening of the distal tubule,
which is concerned with the regulation and release of renin (Bentley, 1976); the
presence in the testes of a specific LDH known as LDHX (Baldwin & Temple-
Smith, 1973) and the presence in the kidney of a loop of Henle (Braun & Dantzler,
1972)(thus, birds like mammals produce urine hyperosmotic to the blood plasma
(Schmidt-Nielsen, 1979)); the presence of prominent, scroll-like turbinals, often
supported by bone, and a maxilloturbinal devoid of olfactory epithelium ; the
development of adventitious cartilage (Patterson, 1977); the atlas and axis both
form complete rings (except in Thylacinus) ; the development of a posteromedially
directed maxillary process, termed maxillopalatine in birds (Goodrich, 1930) and
alveolar process in mammals (de Beer, 1937); similar behavioural patterns in birds
and monotremes which both incubate their eggs; the unique pattern of the
spermatid nucleus in birds and monotremes (Carrick & Hughes, 1978); the fact
that both mammals and birds develop a fever on infection with bacteria (Schmidt-
Nielsen, 1979); and both share very similar collagens (Miller, 1976).
The myoglobin of alligator (Dene et al., 1980) does not, as predicted by
conventional classification, group unequivocally with birds. Rather, birds and
mammals group together on myoglobin sequence, as predicted by the view
proposed here. Haemoglobin Uukes, 1980) also links birds with mammals when
ranked with snakes, amphibians and osteichthyans.

CROCODILIAN RELATIONSHIPS

Crocodiles are generally classified as members of the subclass Archosauria

(Romer, 1956, 1966) while birds are either regarded as ‘glorified archosaurians’
(Colbert, 1955) or simply living archosaurs (Anon, 1979). If this classification is
correct we would expect crocodiles and birds to share derived characters. These
two groups do share one or two unique features, including the form of the
eustachian tube, which passes through the cranial base to open by a single opening
in the roof of the pharynx, and a lateral extension of the alisphenoid
i = pleurosphenoid) which reaches out beneath the squamosal. On the other hand
crocodiles share so many synapomorphies with mammals and birds that I am
forced to regard crocodiles as the sister-group of mammals plus birds.
 TETRAPOD CLASSIFICATION 215

Dentition
Crocodiles and mammals possess a thecodont dentition in which there is a true
periodontal membrane between the tooth and alveolus; individual teeth are set in
deep sockets and replacement teeth develop beneath (lingual to) the functional
teeth. In both, the teeth are attached to the jaw by a suspensory (periodontal)
ligament. In crocodiles the teeth are continually replaced, but in mammals the
dentition is diphyodont, alternation is absent and a single partial replacement
involves all the teeth in an antero-posterior sequence. In Recent birds, teeth are
absent and are replaced by a horny beak, but in Archaeopteryx and Hesperornis teeth
similar to those of crocodiles are present, with replacement teeth lying inside their
bases (Martin & Stewart, 1977).

Braincase
The cavum epiptericum is absent in mammals, crocodiles and birds and the
epipterygoid is incorporated into the braincase wall. The epipterygoid
(=metapterygoid) is visceral arch in origin and when incorporated into the
braincase is usually referred to as the alisphenoid. Although the epipterygoid in
squamates and chelonians lies between branches V, and V, of the trigeminal
nerve, and this relationship is maintained by the alisphenoid in all three groups
(crocodiles, birds & mammals), most present day embryologists and comparative
anatomists believe that the bone in crocodiles and birds (the so called
laterosphenoid or pleurosphenoid of de Beer, 1937) is not the homologue of the
‘reptilian’ epipterygoid. By denying this homology they have to believe instead
that the epipterygoid is lostin birds and crocodiles while a new bone has developed
in the braincase in the same position as the alisphenoid of mammals. This is
unparsimonious and in my estimation the bone (alisphenoid-laterosphenoid-
pleurosphenoid) is the same in all three groups. Furthermore, in the development
of the crocodile there is a membrane running from the epipterygoid vestige to the
braincase similar to that seen in mammals, and the alisphenoid is presumed to
develop within this membrane (Presley, pers. commn). In birds the cartilage
develops down from the orbitosphenoid to form the pila antotica spuria.
Interestingly, the epipterygoid has also been incorporated into the braincase wall
in some snakes where it separates V, and V, (Rieppel, 1976) much as in mammals,
birds and crocodiles.

Heart
There is a complete, muscular interventricular septum in crocodiles as in
mammals and birds. The right atrium in crocodiles is separated from the right
ventricle by a muscular valve similar to that in birds, whereas in mammals the
valve consists of three membranous lappets attached by chordae tendinae (except
in monotremes) to the papillary muscles.
Like mammals and birds, the crocodilian sinus venosus is more or less merged
into the wall of the right auricle. Furthermore it is divided internally by the septum
sinu-venosi.
216 B. G. GARDINER
Ear
A considerable external auditory meatus is developed in crocodiles, birds and
mammals and in all three there is a movable integumentary valve or pinna.
Extensions of the middle ear air-space are most numerous in birds and crocodiles,
where they enter the basioccipital, parasphenoid, quadrate and articular. In
mammals the diverticula of the tympanic cavity are confined to the mastoid
process. In all three groups the perilymphatic duct is expanded into a double loop
and the lagena forms a pronounced cochlear duct. The cavity of the membranous
cochlea is united with the sacculus by means of a narrow canalis reuniens and a
membrane of Corti (membrana tectoria) covers the auditory cells (Berg, 1926). All
three possess a fenestra rotundum (de Beer’s, 1937, fenestra pseudo-
rotundum = fenestra rotundum of Tarsitano & Hecht, 1980).
Other shared derived characters of crocodiles, birds and mammals include :
A complete diaphragm separating the pleural and peritoneal cavities; the
development of three turbinals ; a renal portal system (rudimentary in crocodiles,
birds and monotremes) ; four hypoglossal roots and four metotic myotomes behind
the vagus in the embryo and also in the embryo the presence of metotic cartilages
which fuse with the back of the otic capsule (de Beer, 1937); four or five
haemopophyses on the thoracic vertebrae; and tonsillae pharyngeae at the
entrance of the eustachian tube.

CHELONIAN RELATIONSHIPS

Ever since the publication of Williston’s Osteology of the Reptiles (1925),

chelonians have been regarded as members of the subclass Anapsida. Williston
recognized the solid-roofed skull as the primitive ‘reptilian’ condition and assumed
that since the skull of the chelonian must have been directly inherited from this
solidly roofed state, then chelonians were primitive amniotes. Most subsequent
authors (e.g. Romer, 1956, 1966; Carroll, 1969; Gaffney, 1979a) have followed
Williston and have regarded the chelonians as the most primitive living amniotes.
One dissenting voice was that of L ~ v t r u p(1977), who regarded them as the sister-
group of crocodiles plus birds. But of the seven synapomorphies cited by L ~ v t r u pas
uniting these groups, the single penis, solid ovary and horny caruncle are also seen
in monotremes, while in two other characters (blood proteins and albumins)
appropriate out-group comparisons were not made.
More recently Gaffney & McKenna (1979) have used the presumed primitive
absence of a Jacobson’s organ in turtles to support the idea that turtles are the
sister-group of all other amniotes. But the vomero-nasal Uacobson’s) organ has
long been recognized in amphibians (Wiedersheim, 1882) and recently it has also
been identified in lungfishes (Rosen et al., 1980).
From a consideration of L~vtrup’s(1977) list of synapamorphies mentioned
above it was apparent that the chelonians were the sister-group not of the
crocodiles plus birds but rather of the crocodiles plus birds plus mammals.

Braincase
The epipterygoid in chelonians connects the pterygoid to the parietal in front of
the trigeminal foramen. A descending flange of the parietal grows down to unite
 TETRAPOD CLASSIFICATION 217
with the epipterygoid dorsally. Similarly the alisphenoid sutures with a descending
lamina of the parietal in many mammals (opossum, cat, etc.) whereas in crocodiles
the alisphenoid meets both parietal and frontal.
During development the stapes is connected via the pars interhyales with
Meckel’s cartilage in turtles and crocodiles (de Beer, 1937), while in mammals
there is a continuous blastematous rudiment connecting the stapes and the
cartilage of the mandible (Goodrich, 1930).

Reproductive system
In chelonians, crocodiles, mammals and birds the penis is single and corresponds
to a thickened portion of the anterior lip and ventral wall of the cloaca. In all four
groups it consists of fibrous and cavernous (erectile) tissue and is protrude.
The penis bifurcates proximally in chelonians, crocodiles and some birds
(Struthio) and definite protractor and retractor muscles occur in chelonians and
ratites.
The penis is grooved above in chelonians, crocodiles and birds, but in
monotremes there is a canal.
The ovaries of all four groups are of the solid type, quite unlike those of
amphibians, snakes and lizards, which are saccular and hollow.

Eye
Chelonians, crocodiles, mammals and birds all possess a ciliary process
(Underwood, 1970), and in crocodiles, chelonians and birds the tendon of the
nictitans stretches from the orbital wall to the pyramidalis muscle on the surface of
the eye (Underwood, 1970).
In all four groups the levator muscle of the upper eyelid is supported by a lid
cartilage which may be ossified.

Bones and cartilages

The larynx becomes shifted forwards towards the nasal passage in chelonians,
crocodiles, mammals and birds, and thyroid and cricoid cartilages are present in
all four groups.
During the development of turtles, crocodiles and birds temporary, massive
cartilaginous cones form at each end of the shaft of the long bones. Moreover,
specific ‘primary osteones’ occur in the development of the bone of turtles,
crocodiles and young mammals (Enlow, 1969).
Other shared derived characters of chelonians, crocodiles, mammals and birds
include the cephalad displacement of the subclavian arteries during development.

RHYNCHOCEPHALIAN RELATIONSHIPS

Early authors classified the Rhynchocephalia as a distinct order (Zittel, 1890)

but today they are generally included with the Squamata in the subclass
Lepidosauria (Romer, 1956, 1966). There can be little doubt that this is a correct
association for the two orders share at least six unique features and must therefore
be considered sister-groups.
218 B. G. GARDINER
Synapomorphies of Sphenodon and the Squamata include :
The presence of an acrodont dentition; autotomy of the tail and epiphyseal
centres at the tips of the vertebral spines (Haines, 1969); both the tuatara and
lizards possess a cartilaginous disc in the lower eyelid; and in both the occipital
condyle supports a median hypocentral ossification; the skull of the tuatara and
the lizard show a specific form of kinetism (‘maxillary’) (Versluys, 1912) which is
characterized by a sliding joint between the tip of the epipterygoid and the skull
roof; in the Squamata and the tuatara the compact bone of periosteal origin is non-
vascular (Enlow, 1969); and in both the astragalus has a unique association with
the distal tarsals; finally, in its aromatic acid conjugation the tuatara may be
grouped with lizards and snakes (Jordan, Smith & Vaughan, 1980).

LEPIDOSAURIAN RELATIONSHIPS

Osborn (1903) first placed the Squamata together with the Rhynchocephalia
and Crocodilia in the subclass Diapsida. Although the Squamata were removed
from the subclass by Williston (1925), most subsequent authors have retained
Osborn’s subclass Diapsida for the three orders (e.g. Romer, 1956, 1966). Osborn,
however, used only the single character of the temporal opening for his
classification, and it is now clear that fenestrae have arisen independently and vary
greatly in the different orders. Further it follows from what has been argued above
that the Lepidosauria (Rhynchocephalia and Squamata) cannot be at all closely
related to the Crocodilia, but must be the sister-group of all other living amniotes.
The lepidosaurs share with other amniotes several unique features other than
the possession of amnion, chorion and allantois. These include features of hard
anatomy which are useful in comparisons with fossil groups.

Vertebral column
All amniotes possess a diplospondylous vertebral column in which intercentra
(intervertebral ossicles and/or menisci) alternate with centra. Ossified intercentra
are common in Sphenodon and many lizards and are present throughout the
thoracic region of the Erinaceidae, Talpidae and Chrysochlondae. Elsewhere
ossified intercentra are restricted to the atlas-axis complex.
The atlas is comprised primitively of three separate pieces, but fusion often
occurs during development and a complete ring is found in mammals and birds.
The axis, on the other hand, is made up of either four or five separate parts, with
the centrum of the first arch forming the odontoid process. In most adult amniotes
this odontoid fuses with the second centrum. The odontoid is trefoil-shaped in
lepidosaurians, chelonians and crocodiles, and has three articulatory facets for the
bases of the atlas neural arch pedicels and the atlas centrum (intercentrum 1). In
mammals and birds the odontoid rests on the floor of the atlas and only in some
birds does the base of the second intercentrum also articulate with the atlas
centrum.

Hooked 5th metatarsal

In 1916, Goodrich concluded that all living reptiles and many fossils had a hook-
shaped 5th metatarsal whilst mammal-like reptiles did not. By implication
 MarnrIia I Avls , TETRAPOD CLASSIFICATION

Crocor CI; mia Lepic sauria An >hibid

219

Haemothermia
(1-17)

Thecodontia (18-27)
I
I
Euamniota (28-37)

Amniota (38-44)
I (45 47)

Tetrapoda
I
Figure 2. Character-state tree of major groups of extant tetrapods. Numbered characters refer to the
following synapomorphies: I . Separation of oxygenated and deoxygenated blood. 2. Single aortic
trunk with three semilunar valves. 3. Pulmonary artery with three semilunar valves. 4. Endothermy. 5.
Similar thermoregulatory mechanisms. 6. Three meninges. 7. Folded cerebellum, pons varolii, inferior
olive and pontine nuclei. 8. Scroll-like turbinals. 9. Maxillary process. 10. Adventitious cartilage. 11.
Atlas, axis single ossifications. 12. Vascularized islets ofpancreas. 13. Pinealocytes: oxytocin; prolactin.
14. Macula densa. 15. Loop of Henle. 16. LDHX. 17. Epidermal-melanin unit. 18. Thecodont teeth.
19. Abolition of cavum epiptericum and incorporation of epipterygoid into braincase. 20. Completely
divided heart. 21. Loss of sinus venosus and development of septum sinu-venosi. 22. Complete
diaphragm. 23. External auditory meatus and valve. 24. Three turbinals. 25. Renal portal system. 26.
Pneumatization of middle ear. 27. Perilymphatic duct and coiled cochlea: canalis reuniens;
membrana tectoria. 28. Epipterygoid joins parietal. 29. Stapes unites with Meckel’s cartilage. 30. Penis
single and with erectile tissue. 31. Solid ovaries. 32. Ciliary process. 33. Eyelid cartilage. 34. Tendon of
nictitans to pyramidalis muscle. 35. Thyroid and cricoid cartilages. 36. Cartilaginous cones at ends of
longbones. 37. Subclavian arteries displaced cephalad. 38. Diplospondyly. 39. Atlas-axis complex. 40.
Odontoid process. 41. Hooked 5th metatarsal. 42. Prefrontal reaches palatine. 43. Manus with five
fingers. 44. Pisiform bone. 45. Vertebrae membrane-bone. 46. Single ossified element (=atlas)
supporting skull. 47. Cutaneous respiration; olfactory organ with blind pouches; forked naso-
lachrymal duct.

Goodrich used the absence of this feature in mammals to support his contention
that mammals were the sister-group of all other amniotes. However, a hooked 5th
metatarsal similar to that in Sphenodon, chelonians and crocodiles is also present in
such mammals as the marsupial anteater, the wombat, Dayurus, Ailuropa and
Mynnecophaga.
Other amniote synapomorphies seen in the lepidosaurs include the prefrontal
bone which reaches the palatine (as in chelonians and crocodilians), the presence
of five fingers and a pisiform bone in the manus.

AMPHIBIAN RELATIONSHIPS

The monophyly of the Recent Amphibia is questionable. Parsons & Williams

(1962) regarded them as monophyletic because they possess pedicellate teeth, but
220 B. G . GARDINER
similar teeth occur in osteichthyans and squamates. Nevertheless, the Apoda and
the Urodela and Anura show several synapomorphies.

I’ertebral column
The vertebrae in all three orders are lepospondylous, made chiefly of
membrane-bone and have co-ossified neural arches and centra. The neural arch
pedicels are perforated for the spinal nerves in the Apoda and many Urodela. No
other tetrapod group possesses almost exclusively membrane-bone vertebrae.
Individual amphibian vertebrae are ossified in one piece, thus a single vertebral
element supports the skull in contrast to the multipartite atlas-axis complex in all
other tetrapods (apart from microsaurs where the atlas is uniquely modified and
possesses an anteriorly projecting boss : Carroll, 1969).

Cutaneous respiration
All three amphibian orders are specialized for skin respiration (Foxon, 1955).
They all possess similar blood systems including a musculo-cutaneous vein and
embedded in the skin of all three groups there are numerous saccular, poison and
mucous glands of epidermal origin. Other shared derived characters of amphibians
include the olfactory organ which develops blind pouches or grooves; a forked
naso-lachrymal duct whose opening lies in an elongate ‘palpus’ below the eye in
apodans and anurans; a fenestrated septum atriorum in apodans and urodeles; a
columella auris composed of two elements; and reduced anterior neural spines.
The name Paratoidia which is used to include the Urodela and Anura is derived
from the paratoid.glands in the skin of the neck.

SUMM.4RY OF LIVING TETRAPOD RELATIONSHIPS

My conclusions based on the synapomorphies dealt with in the preceeding text

are depicted in Fig. 2 and summarized in the classification below.

FOSSIL TETRAPODS

In the space available it has only been possible to examine a few of the fossil
assemblages. By necessity these have to be either demonstrable monophyletic
groups or single species. I hare endeavoured to fit these various fossil groups into a
combined fossil and Recent classification according to the conventions adopted by
Patterson & Rosen (1977) whereby fossil species are treated as terminal taxa. In
the Recent classification I have relied heavily on characters of soft anatomy but
these remain unknown in most fossils. Moreover there is the difficulty of
interpreting the fossils themselves and this is dependent on selection of a Recent
model. Finally I have had to accept the monophyly of some extinct groups.

Mammal ia
Triconodonta
The best known member of this group is Morganucodon whose braincase has been
extensively studied by Kermack, Mussett & Rigney (1981). Morganucodon shares
 TETRAPOD CLASSIFICATION 221
many unique features with mammals including a double occipital condyle,
diphyodonty in which the molar teeth are in mesiodistal contact and bear both
cusps and roots, and a squamosal/dentary articulation. In both, the prefrontal is
missing and the frontals have grown down to contact the palatines. The
quadratojugal is also missing and there is a single petrosal in place of the opisthotic
and prootic. Morganucodon thus shares many derived characters with mammals, but
since it has only one ear ossicle it must be considered their sister-group (Fig. 3).

Pterosauria
It has been pointed out that locomotor stamina is a prerequisite of bird flight
and that endothermy probably evolved among the ancestors of birds before the
emergence of flight (Bennett & Rubens, 1979). That the Pterosauria were also
endotherms can be deduced from the recorded presence of a fine pelt (Goldfuss,
1831 ; Sharov, 1971), but whether this pelt was comprised of hair or down feathers
is not obvious. What is more certain, however, are the features in which pterosaurs
resemble birds.
Birds and pterosaurs possess a keeled sternum and this may be obliquely grooved
for the coracoids as in Pteranodon and Ichthyornis where the right coracoid overlies
the left. The limb bones of pterosaurs (Ornithocheirus) are light and hollow as in
birds, frequently have internal strengthening struts, and the humerus has a
pneumatic opening of similar shape and position.
The occipital condyle is single and directed downwards in both groups and
articulates with the intercentral portion of the atlas. The odontoid process fits into
a hole in the atlas intercentrum in both Nyctosuurus and Aptornis (BMNH
specimens).
The optic lobes of Scuphognathus (Institute of Geological Sciences specimen) were
separated from one another and the cerebellum had well developed lateral lobes
(flocculi) which met the forebrain as in birds and mammals.
In pterosaurs, the foot has five metatarsals (Williston, 1925), four phalanges and
the astragalus is fused with the tibia, and as in birds the fifth digit is missing from
the fore limb (Berg, 1926). In all of these respects and in digital proportions
pterosaurs resemble Archaeopteryx (Wellnhofer, 1974).
Pterosaurs also have a maxillary process (palatine bone of Arthaber, 1921;
Kuhn, 1967) similar to that in Archaeopteryx (Kleinschmidt, 1951) and many
Recent birds. A remarkable similarity also exists between the sacrum of Pteranodon
and Recent birds (Eaton, 1910) where the 8th and 9th vertebrae of the synsacrum
in particular resemble the two parapophysial vertebrae of the avian sacrum. The
cervical vertebrae are also similar in pterosaurs and birds.
The teeth in pterosaurs are thecodont, and in their replacement resemble
crocodiles and toothed birds. In some of the Triassic forms (Wild, 1978) the teeth
are cusped and are similar to those of mammals and cynodonts. Cusped teeth are
first found in primitive reptiles such as Diudectes from the Upper Carboniferous and
also occur in the Triassic procolophonids.
Finally, pterosaurs share one uniquely derived feature with monotremes and
marsupials, the presence of pre-pubic bones.
From a consideration of all these features I conclude that pterosaurs are the
sister-group of birds (Fig. 3).
222 B. G . GARDINER

Dinosauria
The name Dinosauria was proposed by Owen ( 1841) to include Megalosaurus,
Hylaeosaurus and Iguanodon. Since that time it has been demonstrated that
Hylaeosaurus and Iguanodon belong to a monophyletic group, the Ornithischia,
characterized by the form of the pelvic girdle and the presence of a predentary.
Megalosaurus on the other hand has been removed to the Saurischia and the
monophyly of Owen’s Dinosauria has thus been challenged.

Megalosauridae
The megalosaurs had a very distinctive method of tooth replacement in which
the new teeth lie in pockets lingual to the true alveolus. The replacement tooth
erupted separately through the dentary, lingually and ventral to the existing tooth.
Distinct open channels pass up through the high alveolar wall to connect these
eruption holes with the true alveolus. These channels (one per tooth) dissect the
high alveolar wall and give rise to the so called infradental plates (cf. Megalosaurus
BMNH R.8350 ; Tyrannosaurus; Allosaurus) .
A basically similar form of tooth replacement in which the new tooth erupts
through openings resorbed in the dentary somewhat lingual to the true alveoli is
seen in many ornithischians (hypsilophodonts, stegosaurs, ankylosaurs) and
cynodonts and is deduced to be the primitive thecodont replacement pattern
(interestingly, some ceratopsians have teeth with bifid roots, as in mammals).
Megalosaurs, however, do share one very unusual feature with ornithischians.
The distal end of the tibia in both groups extends outwards behind the fibula in
a peculiar and characteristic manner (Huxley, 1869). Other shared derived
characters of megalosaurs and ornithischians include the form of the pelvis with its
perforate acetabulum, the presence of a pubic process on the ilium, and the
compact bone which is distinctive in structure (Enlow, 1969).
In his original description of the dinosaurs Owen (1841) concluded that they
were the nearest reptiles to mammals, but Huxley ( 1868; 1870) did his best to show
they were closer to birds, and deduced that they were “most nearly intermediate
between birds and reptiles”. Huxley’s view (1868: 224) has recently been
championed by Bakker & Galton (1974), Thulborn (1970) and Ostrom (1976),
with the latter concluding that modern birds are surviving descendants of the
dinosaurs.
+
But the dinosaurs (Ornithischia Megalosauridae) share not a single unique
feature with the birds ; instead they share three synapomorphies with crocodiles,
birds and mammals and at least four derived features with the Crocodilia.
They share with crocodiles, birds and mammals a thecodont dentition, absence
of the cavum epiptericum with the incorporation of the epipterygoid
i= alisphenoid) in the braincase wall (cf. Hypsilophodon, BMNH R.2477) and
bifurcated cervical ribs which form a vertebrarterial canal.
They share with crocodiles and birds (including Archaeopteryx, BMNH specimen,
left side) a dorsolateral extension of the alisphenoid which reaches out to articulate
beneath the postorbital as in crocodiles, and a single median opening for the
eustachian tubes.
They share with crocodiles a similar extensive ventral development of the
basioccipital and basisphenoid, and the presence of a prominent pair of basal
tubera and a median keel on the basisphenoid in front of the dorsum sellae. In
 TETRAPOD CLASSIFICATION 223

1
22 25

16 -19 7 11

20 21

Figure 3. Character-state tree of major groups of Euamniota. Numbered characters refer to the
following synapomorphies: 1. Double occipital condyle. 2. Diphyodonty, molars with root canals. 3.
Frontal meets palatine. 4. Quadratojugal and prefrontal missing, lachrymal reaches palatine. 5.
Petrosal. 6. Squamosal/dentary articulation. 7. Keeled sternum with coracoid grooves. 8. Cross struts
in hollow limb bones; humerus with pneumatic opening. 9. Single occipital condyle: atlas with single
anterior articulation. 10. Fusion of astragalus to tibia: hinged mesotarsus; 5th digit missing from
forelimb. 11. Similar atlas-axis complex. 12. Distal end of tibia extends behind fibula. 13. Perforate
acetabulum. 14. Pubic process on ilium. 15. Distinctive compact bone. 16. Median keel on
basisphenoid. 17. Alisphenoid forms lateral wall of forebrain. 18. Basal tubera. 19. Palpebral bone
above the eye; 5th toe reduced; clavicles wanting. 20. Thecodont dentition. 21. Epipterygoid joins
prootic and basisphenoid. 22. Trefoil-shaped condyles and odontoid process. 23. Vomers fused and
with a longitudinal keel. 24. Loss ofteeth and replacement by horny beak. 25. Dorsal crest on pterygoid.

both, the alisphenoid is an extensive ossification which forms the lateral walls of the
forebrain. In Crocodilia and Ornithischia there is frequently a dorsal bone roofing
the orbit, the palpebral (Thulborn, 1970).
The Dinosauria (Ornithischia and Meglaosauridae) must therefore be the sister-
group of the Crocodilia (Fig.'3).

Mammal-like reptiles
As already mentioned in the historical survey, the synapsids are generally
believed to contain the mammalian ancestors. Thus, Jollie wrote (1962 : 76) "the
head skeletons of mammal-like reptiles range from highly unlike to quite similar to
the mammal. The cynodonts are usually referred to in contrasting these two
groups because of the similarity of their skulls . . . the intermediate nature of the
cynodont is quite apparent". But as long ago as 1926 Berg wrote that the mutual
similarities between mammals and theriodonts were probably due to convergence,
pointing out that even if we admit that mammals have been derived from one
224 B. G. GARDINER
group of Theromorpha then their resemblance to other theromorph groups must
be due to parallel development !

Cynodontia
At first sight, cynodonts do superficially resemble mammals, but a thorough
examination of Thrinaxodon (BMNH specimens) failed to reveal a single
mammalian synapamorphy .
Tooth replacement, for example, was very much like that in megalosaurs and
Scelidosaurus (BMNH R.111 l ) , with the replacement teeth erupting through the
lingual aveolar wall. As the tooth increased in size it apparently gained access to
the functional alveolus by resorption of the bar of bone separating it and the old
tooth. Thus, the replacement tooth did not immediately enter the pulp cavity of its
predecesor as it does in crocodiles and mammals, but instead developed in a
replacement crypt in the lingual wall, erupted through the aleveolar wall and only
then entered the old pulp cavity.
Some of the functional teeth are held firmly by a ring of attachment bone and in
Procynosuchus, Kemp (1979) has described teeth with no roots and empty alveoli
plugged by bone; closure of alveoli in mammals only occurs when neither tooth nor
periodontal membrane is present. Similar rootless teeth are present in Thrinaxodon
(BMNH R.5111, R.51 la, R.3731) where they apparently alternate with typical
thecodont teeth. I conclude that the cynodonts combine thecodonty with the more
primitive tetrapod condition in which the teeth are fused to the jaws. As Owen
( 1866)remarked, ‘Yn no mammiferous animal does anchylosis of the tooth with the
jaw constitute a normal mode of attachment. Each tooth has its own socket to
which i t firmly adheres by the alveolar periosteum which invests the roots of the
tooth.” The cynodont dentition is best considered primitive thecodont and there is
little doubt that the teeth did not occlude (Lumsden & Osborn, 1977).
Cynodonts are presumed to have a double occipital condyle (Jenkins, 1971 ;
Kemp 1980) as in mammals. But, as Broom (1932) pointed out, although the
exoccipitals form lateral condyles, the basioccipital also articulates with the
intercentrum of the atlas (cf. Thrinaxodon).
The composition of the side wall of the braincase of cynodonts is said to be of
special interest because of “the fundamental difference between mammals and
reptiles in this feature” (Kemp, 1979). The epipterygoid in Thrinaxodon is fused
dorsally to the parietal and frontal much as is the alisphenoid in dinosaurs,
crocodiles and mammals. Ventrally however it is still fused to a splint-like
pterygoid. The pterygoid in Thrinaxodon is largely replaced by the endoskeletal
epipterygoid, as it is in other advanced cynodonts (Broom, 1932). In Procynosuchus,
on the other hand, the pterygoid is much more extensive and continues posteriorly
as a stout ossification to contact the quadrate (Kemp, 1979). Thus, in all described
cynodonts the epipterygoid connects the pterygoid to the parietal (and frontal) in
front of the trigeminal foramen. Consequently, the cavum epiptericum is still
intact and the epipterygoid ventrally lies outside the braincase wall as in
chelonians. Nevertheless, there are several advances over the chelonian condition.
Posteriorly the epipterygoid has an extensive contact with the dorsolateral process
of the prootic and anteroventrally it sutures with the basipterygoid process.
Because the alisphenoid also sutures with the basisphenoid in dinosaurs, crocodiles,
mammals and birds, the condition of the epipterygoid in cynodonts is considered
 TETRAPOD CLASSIFICATION 225
advanced when compared with that of chelonians. This, together with the
thecodont dentition, places Thrinaxodon (cynodonts) as the sister-group of
Archosauria plus Haemothermia (Fig. 3 ) .
Interestingly, the cynodonts share one derived feature with birds and
Sphenosuchus; in all three a lateral process on the prootic (lateral lamina) articulates
with the quadrate (Kemp, 1979).

Dicynodontia
Today the dicynodonts are normally classified together with the cynodonts in
the order Therapsida (Romer, 1956, 1966; Hopson, 1969) but this has not always
been the case.
As early as 1869, Huxley pointed out their resemblance to the Chelonia, while in
1888, on the strength of the similarities seen in the palates, Seeley classified them
with the turtles in the new order Therochelonia. In all dicynodonts, the anterior
teeth (with the exception of the upper canine) are absent and presumed to have
been replaced by a horny beak as in turtles (Hopson, 1969).
Turning to the remainder of the dentition, posterior teeth, where present, are set
in a continuous groove with no partitions separating individual teeth and with
replacement teeth developing in pockets resorbed in the lingual bases of their
predecessors. Therefore, the teeth may justifiably be described as simple, conical
and protothecodont (Edmond, 1969). The absence of true thecodonty in the
dicynodonts bars them from any close relationship with the cynodonts. Conversely,
dicynodonts do share several derived features with the chelonians.
In dicynodonts (Cox, 1959), the parietals grow down to suture with the
epipterygoid as in turtles, cynodonts and mammals, but as in turtles the
epiptergoid never reaches the prootic posteriorly (similarly in gorgonopsids). In
turtles and dicynodonts the vomers are fused and usually bear a characteristic
longitudinal keel, and the occipital condyles and odontoid process are markedly
trefoil-shaped (Cox, 1959; Kemp, 1969). These features, together with the loss of
the anterior dentition in dicynodonts, strongly suggest that chelonians and
dicynodonts are sister-groups (Fig. 3). Dicynodonts share with dinosaurs,
pterosaurs and mammals a type of periosteal tissue termed fibro-lamellar (Ricqles,
1976, 1978).

Pelycosauria
The pelycosaurs are believed to be the earliest and most primitive synapsid
reptiles (Romer, 1956, 1966; Hopson, 1969). Their claim to synapsid relationship
apparently rests on Cope’s (1884) insistence on their closeness to mammals and the
possession of a lateral temporal fossa.
The pelycosaurian dentition however is protothecodont (Edmond, 1969),
similar to that of primitive amniotes and quite unlike the thecodont dentition of
the archosaurs and haemotherms. Furthermore, the epipterygoid is a slender strap
of bone stretching up from the pterygoid, but not apparently reaching the dermal
skull roof (Romer & Price, 1940). In this respect the epipterygoid is unlike that in
either dicynodonts or cynodonts. The atlas-axis complex is also simple (Olsen,
1966), there is no true odontoid process, and the atlas does not form a ring. The
stapes is massive and directed towards the quadrate and a tympanum is presumed
to have been absent. The lachrymal is large and the prefrontal does not reach the
226 B. G . GARDINER

5 -* 6 1 -' 4

7-8

9 -. 12

13 -' 15

palatine; the 5th metatarsal is not hooked. T h e pterygoid, however, has a lateral
projection or knee as in lepidosaurs and euamniotes.
Thus, the pelycosaurs share only five out of the ten synapomorphies uniting the
lepidosaurs with the euamniotes and consequently must be considered the sister-
group of lepidosaurs plus euamniotes (Fig. 4.).

AMPHIBIA

.!Vectridiaand ..listopoda
These two groups possess lepospondylous vertebrae in which the neural arch and
centra are co-ossified. I n addition the neural arches are perforated by spinal nerve
foramina. T h e vertebrae closely resemble those of Recent amphibians and are
unlike any found in other amphibian groups (Gardiner, in prep.). This together
with the fact that the atlas is a single ossification has prompted me to consider them
the sister-group of the Lissamphibia.

Temnospon&i
This is a large but probably monophyletic group (Gardiner, in prep.)
characterized by the possession of rachitomous vertebrae. The temnospondyls are
 TETRAPOD CLASSIFICATION 227

separable from the earlier loxommatids and ichthyostegids by the possession of

labyrinthodont teeth.

SUMMARY OF FOSSIL TETRAPOD RELATIONSHIPS

All the synapomorphies mentioned in the foregoing section are listed in Figs 3 , 4
& 5, which represent character-state trees or nested sets. The information is also
summarized in the classification below, in which fossils are incorporated according
to the method described by Patterson & Rosen (1977) and elaborated by Wiley
(1979).By this method, monophyletic extinct taxa are accorded the status Plesion
which substitutes for categorical ranks. When sequenced in a combined Recent-
fossil classification a plesion is the sister-group of all other terminal taxa within its
clade and below it in the classification.

CONCLUSIONS

The detailed correspondence between mammals and birds far outweighs the
evidence of a synapsid-mammalian transition. The Synapsida, as befits a
paraphyletic group, lacks synapomorphies, whereas mammals and birds share

4t5

-7
I
71
Figure 5. Character-state tree of Amphibia. Numbered characters refer to the following
synapomorphies: 1. Lepospondylous vertebrae, neural arch and centrum co-ossified. 2. Neural arch
pedicles perforated by spinal nerves. 3. Atlas a single ossification. 4.Teeth set in a broad alveolar
groove, pleurodont with large pulp cavity. 5. Stapes with enlarged base plate, stapedial foramen and
extends to quadrate; tabular reaches parietal. 6. Labyrinthodont teeth. 7. Pentadactyl limb and other
characters (Gaffney, 1979a).
228 B. G . GARDINER

derived features of endothermy, thermoregulation, form of the heart and

separation of the lung from body circulation, meninges, cerebellum, turbinals,
maxillary process, adventitious cartilage, atlas-axis, vascularized islets in the
pancreas, pinealocytes, macula densa, loop of Henle and LDHX.
Moreover, when the Synapsida were broken down into some of the constituent,
monophvletic groups none of these ( Thrinaxodon, Dicynodontia, Ophiacodontidae)
was found to possess a single derived feature in common with the Mammalia alone.
Finally, the conclusion that the Squamata and Sphenodon are the most primitive
living amniotes shows how misleading the use of the temporal arches in
classification has been, and emphasizes the need to establish consistent patterns of
derived characters when searching for relationships.

TETRAPOD CLASSIFICATION

Superclass Gnathostomata
Class Osteichthyes
Subclass Sarcopterygii
Infraclass Choanata
Superdivision Dipnoi
Superdivision Tetrapoda
t Plesion Ichthyostega
t Plesion Loxommatidae
t Plesion Temnospondyli
Division Amphibia
t Plesion Lepospondyli
Order IVectridia
Order Aistopoda
Subdivision Lissamphibia
Superorder Apoda
Superorder Paratoidia
Order Urodela
Order Anura
Division Amniota
t Plesion Anthracosauridae
t Plesion Microsauria
t Plesion Captorhinomorpha
Order Captorhinidae
Order Ophiacodontidae
Subdivision Lepidosauria
Order Rhynchocephalia
Order Squamata
Subdivision Euamniota
Infradivision Testudinata
t Plesion Gorgonopsidae
t Plesion Dicynodontia
Order Chelonia
Infradivision Thecodontia
t Plesion Thrinuxodon
 TETRAPOD CLASSIFICATION 229
Supercohort Archosauria
t Plesion Dinosauria
Order Ornithischia
Order Megalosauridae
Order Crocodilia
Supercohort Haemothermia
Cohort Mammalia
t Plesion Triconodonta
Subcohort Monotremata
Subcohort Theria
Plesion Multituberculata
Infracohort Marsupialia
Infracohort Eutheria
Cohort Aves
t Plesion Pterosauria
Plesion Archaeopteryx
Subcohort Ratitae
Subcohort Neognathae

ACKNOWLEDGMENTS

I would especially like to thank Dr Colin Patterson for all his help and advice,
and for encouraging me in my beliefs. I am also indebted to Miss Sally Young for
help with the illustrations and Dr Angela Milner for access to the collections, and
providing information.

REFERENCES

ANON, 1979. Dinosaurs and their Living Relatives. London: British Museum (Natural History).
ARTHABER, G., 1921. Studien iiber Flugsaurier auf Grund der Bearbeitung des wiener Exemplares von
Dovgnathw banthemis. Denkschrften der Akademie dei Wissemchaften, Wien, 97: 391-464.
BAKKER, R. T . & GALTON, P.M., 1974. Dinosaur monophyly and a new class ofvertebrates. Nature, London,
248 (5444):168-172.
BALDWIN, J. & TEMPLE-SMITH, P., 1973. Distribution of LDHX in mammals: presence in marsupials and
absence in the monotremes PlaQpus and Echidna. Comparative Biochemistry and Physiology, 44B: 80581 1.
BENNETT, A. F. & RUBENS, J. A,, 1979. Endothermy and activity in vertebrates. Science, N e w rork, 206:
649-654.
BENTLEY, P. J., 1976. Comparative Vertebra& Endocrinology. Cambridge: Cambridge University Press.
BERG, L. S., 1926. Nmogenesis or Evolution Determined Ly Law. Translated from the Russian by J. N. Rostovtsov,
introduction by D'Arcy Wentworth Thompson. London: Constable.
BLAINVILLE, M. H. M. D. de, 1822. De I'Organisation des Animaux. Tome Premier contenanl la Morphologie el
I'rlisteologie. Paris: Bandouin.
BRAUN, E. J. & DANTZLER, W. H., 1972. Functions of mammalian-type and reptilian-type nephrons in
kidney of Desert Quail. American Journal of Physzolou, 222: 617-629.
BROOM, R., 1915.On the origin ofmarnmals. Philosophical Transaction ofthc Royal Society o f l o d o n , (8)206: 1-48,
BROOM, R., 1932. The Mammal-like Reptilds of South Africa and the Origin of Mammals. London: H. F. & G.
Witherby.
CARRICK, F. N. & HUGHES, R. L., 1978. Reproduction in male monotremes. Australian <oologi.rt, 20:
21 1-231.
CARROLL, R. L., 1969. Origin of Reptiles. In C. Gans, A. d'A. Bellairs & T. S. Parsons (Eds), Biology of the
Reptilia, I : 1-44. London : Academic Press.
CARROLL, R. L. & HOLMES, R., 1980. The skull and jaw musculature as guides to the ancestry of
salamanders. <oological journal of the Linnean Society of London, 68: 1-40,
COLBERT, E. H.,1955. Evolution of the Vertebrahs. New York: J. Wiley.
230 B. G. GARDINER
COPE, E. D., 1884. The origin of the Mammalia. American .VafuralLf, 18: 1136-7.
COX, C. B., 1959. On the anatomy of a new dicynodont genus with evidence of the position of the tympanum.
Proceedings of the <mlogical Sock& oJLondon, 132: 321-367.
DAWSON, W. R. & HUDSON, J . W., 1970. Birds. In J. P. Harmon & E. Viererck (Eds). Comparative P/ysiology
oj Temperaturt Rrgulation. I : 223-310. London: Academic Press.
De BEER, G. R., 1937. T h e Development of fhe Verfebrafc Skull. Oxford: Clarendon Press.
DESE, H., SAZY, J., GOODMAN, M. & ROMERO-HERRERA, A. E., 1980. The amino acid sequence of
alligator (Alligator mississipiensis) myoglobin. Biochnica ef Biophysica A c h , 624: 397-408.
DONKELXAR. H. J. ten & NIEUWENHUYS, R., 1979. The brainstem. In C. Gans, R. G. Northcutt & P.
Ulinski (Eds,, Biology of the Repfilia, 10: 133-200. London: Academic Press.
EATON, G. F., 1910. Osteology of Pkranodon. Memoirs of the Connectkuf Arademy of ,4rfs and Sciences, 2: 1-38.
EBLING, J. M. P. & HALE, P. A., 1970. The control of the mammalian molt. Mmoirs of the Society of
Endocrinologv,18: 215-235.
EDMOND, A. G., 1969. Dentition. In C. Gans, A. d’A. Bellairs & T . S. Parsons (Eds), Biology ofthe Repfilia, 1:
1 17-~200.London: .4cademic Press.
ENLOW, D. H., 1969. The bone of reptiles. In C. Gans, A. d’.4. Bellairs & T. S. Parsons (Eds), BiologY o f f h e
Repfilia, I: 45- 80. London : Academic Press.
FOURIE, S.. 1963. Tooth replacement in the Gomphodont cynodont Dzadmodon. Soufh African Journal of Srience,
5.9: 21 I - 213.
FOXO?;, G. E. H., 1955. Problems of the double circulation in vertebrates. Biological Reviews o f t h e Cambridge
Philosophical Sociep, 30: 196--228.
GAFFNEY. E. S., 1979a. Tetrapod monophyly : a phylogenetir analysis. Bulletin of the Carnegie Museum of Natural
Hirfoty. 13: 92--105.
GAFFNEY, E. S., 1979b. An introduction to the logic ofphylogeny reconstruction. In J. Cracraft & N. Eldredge
iEds!, P/ylogenetic Analysis and Paleonlology: 71-1 1 I . New York: Columbia University Press.
GAFFSEY, E. S. & McKENN.4, M. C., 1979. A late Permian captorhinid from Rhodesia. American Museum
.Voritatw, 2688: 1 15.
-

GOLDFUSS, A , 1831. Beitrage zur Kenntnis verxhiedener Reptilien der Vorwelt. Nova A d a Plysuo-Medira
:lcademiae Caesarca Leopaldino-Carolinae Cermanicum .Vatwar Curiosorum. 15: 61 -128.
GOODRICH, E S., 1916. On the classification of the Reptilia. Proceedings o f t h e Royal Society ofLondon, ( B ) 89:
261-276.
GOODRICH, E. S., 1930 Sfudits on the Structure and Deuelopmrnt of Vertebrafes. London: Macmillan.
GRIFFITHS, M., 1978. The Biology of the Monofremw. London: Academic Press.
HAECKEL, E., 1866. Ginerelle Morphologie der Organismen. Berlin; G. Reimer.
HAINES, R. W.,1969. Epiphyses and Sesamoids. In C. Gans, A . d’A. Bellairs & T . S. Parsons (Eds),Biology of the
Repfilia, 1 : 81-1 15. London: Academic Press.
HELLER, C. M., CRAWSHAW, I,. I . & H.4MMEL, H. T., 1978. The thermostat of vertebrate animals.
Scirnfijic Ameriran, 239: 88-96
HOLMES, E. B.. 1975. A reconsideration of the phylogeny of the tetrapod heart. Journal of Morphology, 147:
209-228.
HOPSON, J . A,, 1969. The origin and adaptive radiation of mammal-like reptiles and nontherian mammals.
.4nnals of thr .!CLL rbrk .4cademp of Sciemts, 167: 199-216.
HUXLEY, T . H., 1864. IActurt-s on fhe Elemenfs of Cmparatiuc A n a l a ~ London:. J. Churchill & Sons.
HUXLEY, T. H., 1868. On the animals which are most nearly intermediate between birds and reptiles. Annals
and Magazine of .Vatural H i s t o v , ( 4 ) I : 22&224.
HUXLEY, T. H., 1869. An Infroduction lo fhe ClassiJFcnfion of Animals. London: J. Churchill & Sons.
HUXLEY, T. H., 1870. Further evidence of the afinity between the Dinosaurian Reptiles and Birds. Quarterly
Journal of fhe Geological Socie!v of London, 26: 12-31. On the classification of the Dinosauria. Ibid: 32-35.
JENKINS, F. X., I97 I . The postcranial skeleton of African cynodonts. Bulletin of the Peabody Museum of Natural
History, .?6:1 126.
-

JOLLIE, hl., 1962. Chordale A4orphology. Sew York: Reinhold.

JORDAN, 1’. h’., SMITH, J . N. & VAUGH.kN, L., 1980. Benzoic acid conjugation in Tuatara. Biochemical
SystPmafirs and Ecology, 8: 101-103.
JUKES, T. H., 1980. Silent nucleotide substitutions and the molecular evolutionary clock. Science, .‘VmYoork, 210:
973--978.
KEMP, T. S.. 1965. The atlas-axis complex of the mammal-like reptiles. ] o u m l of/50010gy,1.59: 223-248.
KEMP, T. S., 1979. The primitive cynodont PrEynosuchus; functional anatomy of the skull and relationships.
Philosophical Transactions o f the Reval Socie~of London, (Bi 285: 73-122.
KEMP, T. S., 1980. The primitive cynodont Pragnosuchuc: structure, function and evolution of the postcranial
skeleton. Philosophiral Transactions of the Royal Socir-p of London, ( B ) 288: 21 7-258.
KERM.\CK, K . A,, MUSSETT, F. & RIGNEY, H. W., 1981. The skullofkforganucodon. {oologicalJournal of f h
Linnean Soriety of London. 71: 1-158.
KLEISSCHMIDT. A., 1951. Cber eine Rekonstruktion des Schadels von Archaeornis sirmenri Dames 1884 im
Naturhistorischen Museum, Braunschweig. Proceedings of the Infernational Ornithological Congress, IO. Uppsala :
631-635.
 TETRAPOD CLASSIFICATION 23 1
KOBAYASHI, H. & WADA, M., 1973. Neuroendocrinology in birds. In D. S. Farner, J. R. King & K. C.
Parlas (Eds), Avian Biology, 3: 287-347. London: Academic Press.
KUHN, O., 1967. Die fossile Wirbclfierklasse Pterosauria. Munchen: Krailling.
LANKESTER, E. R., 1870. On the use of the term Homology in modern zoology, and the distinction between
Homogenetic and Homoplastic agreements. Annals and Magarine ofNafura1 History, (4) 6: 3 M 3 .
LAURENTI, J. N., 1768. Classis Rcptilium. Specimen meduum, exhibem synopsis Reptilium emendatam cum experimentis
circa venena et antihte Rcptilium Aushiacorwn. Vienna: J Thorn., Nob. et Trattnern.
LINNAEUS, C., 1758. S y s t n a Nature, 10th ed.
LBVTRUP, S., 1977. T h e Phylogeny of Vertebratn. London: Wiley.
LUMSDEN, A. G. S. & OSBORN, J. W., 1977. The evolution of chewing: a dentist’s view of palaeontology.
Journal of Dentistry, 5: 269-287.
MARTIN, L. D. & STEWART, J. D., 1977. Teeth in Ichthyornis (Class: Aves). Science, N e w Tork, 195:
1331-1332.
MILLER, E. J., 1976. Biochemical characteristics and biological significanceof the genetically distinct collagens.
Molecular and cellular Biochemistty, 13: 165-192.
OLSEN, E. C., 1966. The middle ear-morphological types in amphibians and reptiles. American <oologisf, 6:
39M19.
OSBORN, H . F., 1903. The reptilian subclasses Diapsida and Synapsida and the early history of the
Diaptosauria. Memoirs f r o m fhe American Museum of Nafural Histoty, I : 444-507.
OSTROM, J. H., 1976. Archaeopteryx and the origin of birds. Biological Journal o f f h e Linnean Society of London, 8:
9 1-182.
OWEN, R., 1841. Report on British fossil reptiles. Part 11. Report of the Brifish Association for the Advancement of
Science, Plymouth, 11: 6&204.
OWEN, R., 1866. On the A n a h y of Vertebrates, 2. London: Longmans Green & Co.
OWEN, R., 1868. Comparative Anatomy and Physiology of Vertebrates (or O n the Anatomy of Vertebrates), 3 Mammals.
London: Longmans, Green & Co.
OWEN, R., 1876. Descriptive and illustrated catalogue of the fossil Reptilia in the Brifish Museum. London: British
Museum.
PARSONS, T . S. & WILLIAMS, E. E., 1962. The teeth of Amphibia and their relation to amphibian
phylogeny. Journal of Morphology, 110: 375-89.
PATTERSON, C., 1977. Cartilage bones, dermal bones and membrane bones, or the exoskeleton versus the
endoskeleton. In S. M. Andrews, R. S. Miles & A. D. Walker (Eds), Problems in Vertebrate Evolution: 77-121.
London: Academic Press.
PATTERSON, C. & ROSEN, D. E., 1977. Review ofichthodectiform and other Mesozoic teleost fishes and the
theory and practice of classifying fossils. Bulletin of fhe American Museum of Natural Histoly, 158: 81-172.
QUAY, W. B., 1979. The parietal eye-pineal complex. In C. Gans, R. G. Northcutt & P. Ulinski (Eds),Biology of
the Reptilia, 10: 245406. London: Academic Press.
QUEVEDO, W. C., 1972. Epidermal melanin units: melanocyte-keratinocyte interactions. American <oologist,
12: 35-41.
RAT, J., 1693. Synopsis Methodica Animalium Quadrupedim et Serpentini Generis. Vulgarium .h‘otas Characteristicas,
Rariorum Dcscriptiones integras exhibenr: cum Hisforiis Observationibus A n a t m u i s perquam curiosis. Praemittuntur
nonnulla D e Animalium in genere, s e m , Generatione, Divisione etc. London: Smith & Walford.
RICQLES, A. de, 1976. On bone histology of fossil and living reptiles, with comments on its functional and
evolutionary significance. In A. d’A. Bellairs & C. B. Cox (Eds), Morphology and Biology of Repfiles: 123-150.
London: Academic Press.
RICQLES, A. de, 1978. Recherches Palkhistologiques sur les 0 s longs des Tetrapodes V I I s u r la classification,
la signification fonctionelle et I’histoire des tissues osseux des Tktrapodes. Annales de Palhontolosie, 64: 8 S l I 1 .
REIPPEL, O., 1976. The homology of the laternsphenoid bone in snakes. Herpefologica, 32: 426-429.
ROMER, A. S., 1956. Osteology of fhe Reptiles. Chicago: Chicago University Press.
ROMER, A. S., 1966. Vertebrate Paleontology. Chicago: Chicago University Press.
ROMER, A. S. & PRICE, L. N., 1940. Review of the Pelycosauria. Geologzcai Society ofAmerica, Special Papers, 28:
1-538.
ROSEN, D. E., FOREY, P. L., GARDINER, B. G. & PATTERSON, C., 1981. Lungfishes, tetrapods,
paleontology and plesiomorphy. Bulletin of B e American Museum of .Natural History, 167: 159-276.
SCHMIDT-NIELSEN, K., 1979. Animal Physiologv: Adaptation and Environment. Cambridge: Cambridge
University Press.
SCHULTZE, H. P., 1969. Die Faltenzahne der Rhipidistiiden crossopterygier, der Tetrapoden und der
actinopterygier Gattung Lepisosteus: nebst einer Beschreibung der Zahnstruktur von Onychodus (Struniiformer
crossopterygier). Palaentographua Italica, 65: 6G137.
SEELEY, M. G., 1888. Researches on the structure, organization, and classification ot the foss11Keptllla. L . UII
Pareiusaurus bombidens (Owen) and the significance of its affinities to amphibians, reptiles and mammals.
Philosophical Tramactions of the Royal Society of London, ( B ) 42: 337-342.
SHAROV, A. G., 1971. New flying reptiles from the Mesozoic of Kasachstan and Kirgisien. Tru@
Paleontologuheskogo Inrfituta Akademiya Nauk, S S S R , 130: 104-133 (in Russian).
232 B. G . GARDINER
TARSITANO. S. & HECHT, M. K., 1980. A reconsideration of the reptilian relationships of Archaeopteryx.
zoological Journal of fhe Linnean Socieb of London, 69: 144-182.
THULBORS. R. A., 1970. The skull of Fabrosaurk allttralis, a Triassic Ornithischian dinosaur. Palatontolog, 15:
29~60.
UNDERWOOD, G . , 1970. The eye. In C. Gans (Ed.j, Biology ofthe Reptilia, 2: 1--97. London: Academic Press.
VERSLUYS, J.. 1912. Das Streptost)-lie-Problem. Zoologische Jahrbiicher, Suppl. 15: 545-716.
WATSON, D. M. S., 1954. On Bolosaurus and the origin and classification of reptiles. Bulletin of the Museum of
Cmparatirr <oology, Harrard College. I l l : 297-449.
WELLNHOFER. P., 1974. Das funfte Skelettexemplar von .4rchueoptqyx. Palaconfographica, ( A ) 147: 196-216.
WIEDERSHEIM, R., 1882. Lehrbuch der i,ergltichende .Inatomir der Wirbeltiere. Jena: Gustav Fischer.
WILD, R., 1978. Die Flugsaurier (Reptilia, Pterosauria) aus der Oberen Trias von Cene bei Bergamo, Italien.
Bollrttino d d l a Soriefa Paleonlologica Italiana. 17: 17G-256.
WILEY, E. O., 1979. An annotated Linnean Hierarchy. with comments on natural taxa and competing systems.
Systematic zoology. 28: 308-337.
'WILLISTOS, S. \V., 1925. 7 h e Osteolou of the Reptiles. Cambridge, Mass.: H a n a r d University Press.
ZITTEL, K. A. yon, 1890. Handbuch d n Palaeonfofogie, 3. Munchen €2 Leipzig: Oldenbourg.
ZITTEL, K. A . yon, 1895. Grundcuge der Palaeontolopie (Palaeozoologie). Munchen & Leipzig: Oldenbourg.