<oological Journal of the Linnean Socicy (1989), 96: 185-21 1. With 8 figures
The evolution of the dicynodont feeding system
G. M. KING
University Museum and Department of <oolo&r, Oxford
B. W. OELOFSEN
Department of Sea Fisheries, Private Bag 13184, Windhoek, South West AfricaNamibia
AND
B. S . RUBIDGE
National Museum, P . 0. Box 266, Bloemfontein, South Africa
Received August 1988, acceptedfor publication November 1988
The skull structure of dicynodonts may be regarded as a complex adaptation towards herbivorous
feeding. The present work examines how and why this adaptation may have evolved. A cladogram
of the dicynodonts is presented and from it a sequence of hypothetical ancestral forms is inferred.
The jaw musculature of dicynodonts and other therapsids is described and in particular the early
dicynodont Eodicynodon oosthuizmi is described in detail. This information is used to draw up a
sequence of ancestral stages whose basic skull anatomy, jaw muscle organization and masticatory
properties are described. Differences in masticatory properties between these stages are pinpointed
and an explanation to account for the development of these differences is advanced. It is concluded
that the changes in skull organization seen during the evolution of dicynodonts are consistent with
the hypothesis that a propalinal jaw action was being improved by selection, and that this was
required to permit dicynodonts to be efficient herbivores.
KEY WORDS:-Dicynodontia
-
herbivory
-
mastication - Therapsida
-
Permian.
CONTENTS
Introduction . . . . . . . . . . . . . . .
Dicynodont relationships . . . . . . . . . . . .
Hypothetical ancestral stages on the dicynodont line
. . . . .
The jaw adductor musculature of dicynodonts and other therapsids .
The jaw adductor musculature of Eodicynodon oosthuizmi . . . .
Summary of musculature and osteology in the ancestral stages . .
An explanation for the development of the adaptive complex . . .
The importance of propaliny . . . . . . . . . . .
Conclusion
. . . . . . . . . . . . . . .
Acknowledgements
. . . . . . . . . . . . .
References
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01989 The Linnean Society of London
186
G . M. KING E T A L .
INTRODUCTION
The dicynodonts have traditionally been regarded as an infraorder within the
order Therapsida, taken here to represent the mammal-like reptiles of Late
Permian to Jurassic times and their descendants, the mammals (Hopson &
Barghusen, 1986). Recent work (Cluver & King, 1983; King, 1988) has
suggested that the Dicynodontia should be enlarged to include certain early
Russian forms and the Dromasauroidea.
Earlier students of mammal-like reptiles (such as Cope, Huxley and Owen)
recognized the unusual nature of the dicynodont skull, and as the fossil record,
particularly of the South African Karoo forms, became better known, it soon
became apparent that the Dicynodontia represented a highly-specialized branch
of the therapsids, sharing features associated with a herbivorous way of life that
affected almost every part of the skull and lower jaw (see for example, Cluver &
Hotton, 1981). These features include a shortened snout and anteriorly displaced
orbits, elongated temporal fenestra, anterior insertion of the adductor muscles on
the lateral surface of the lower jaw, zygoma emarginated from below and bowed
outwards, sliding quadrate-articular jaw joint, replacement of upper and lower
tooth rows by horny beaks, reduction of the coronoid eminence, a secondary
palate formed by posterior and medial extensions of the premaxilla, maxilla and
palatine, reduction of the lateral pterygoid process and enlargement of the
squamosal which resulted in a new area of origin for a lateral division of the
external jaw adductor musculature (Crompton & Hotton, 1967; Watson, 1948;
Ciuver, 1971; Cluver, 1974a, b; Cluver & Hotton, 1981; Cluver & King, 1983).
Dicynodonts, then, are very specialized animals compared to the rest of
therapsids. Their skull structure may be interpreted as a complex adaptation
(Padian, 1986) towards herbivorous feeding and when faced with such a
complex of features which carry out a joint function, such as the feeding system,
two questions become of immediate interest. How did the complex evolve and
why? In the present context, ‘how’ is taken to mean, ‘Through what previous
adaptive stages did the complex evolve?’. ‘Why?’ is taken to mean, ‘What was
the reason that adaptive stage A gave rise to adaptive stage Byrather than some
different stage, C?’.
In order to try to answer these questions for the dicynodont feeding system it is
necessary first of all to identify a number of ancestral stages along the main line
of dicynodont evolution in order to be able to view changes in the complex
adaptation through time. Dicynodonts have left a reasonable fossil record and
therefore we do have at our disposal a series of fossil forms from different time
zones. From these actual fossil forms a cladogram of relationships may be erected
(using synapomorphies to relate sister groups) and by determining which
characters occur at the nodes of cladograms it is possible to deduce, partially at
least, the nature of the hypothetical ancestral stage at each node, as opposed to
its derived descendants. Obviously, we cannot use actual, derived fossil forms
when looking at changes in the complex adaptation through time, since the way
the complex is expressed in any particular derived form might be a specialization
rather than part of a long-term trend.
In the study which follows first, a cladogram of the relationships of
dicynodonts will be presented. Next a series of ancestral stages will be suggested
and their basic skull anatomy, jaw muscle organization and masticatory
EVOLUTION OF DICYNODONT FEEDING
187
properties described. The differences between these stages, in terms of their
masticatory properties, will be pinpointed and an explanation to account for the
development of these differences will be advanced. Finally, the importance to the
animal of developing these differences will be discussed.
DICYNODONT RELATIONSHIPS
The classification of Cluver & King (1983) amplified by King (1988) will be
used here to provide the taxonomic pattern which is the basis of the analysis. A
cladogram based on the named works is given in Fig. 1. The characters used to
generate it are shown below.
King (1988) gives some of the following synapomorphies of the relevant
groups; others have been added from the present analysis.
Synapomorphies of Anomodontia ( A )
(Dinocephalia, Venjukovioidea, Dromasauroidea, Higher dicynodonts)
1. Non-terminal nostrils and long posterior spur of premaxilla (modified in
higher dicynodonts) .
2. Grooved or troughed palatal exposure of the vomers.
3 Reduction or loss in internal trochanter of the femur.
Synapomorphies of Dicynodontia ( B )
(Venjukovioidea, Dromasauroidea, Higher dicynodonts)
1. Slightly emarginated zygoma.
2. Palatal surface of premaxilla extended posteriorly, approaching the level
of the canine tooth or process.
3. Presence of intramandibular fenestra.
4. Covering of horn on upper jaw in most forms, shortened tooth row.
Higher dicynodonts
r
Sohenacodontids
Sphenacodontids
\
Dinocephalio
Vmjukoviu
Dromasauroidea
EodcynOdm
I
Advanced forms
D
Figure 1 . A cladogram showing the relationships of the forms discussed in the text. After King, 1988.
I88
G . M. KING E T AL.
5. Jaw joint permits some antero-posterior movement of lower jaw.
6. Shortening of preorbital region of skull.
7. Larger temporal fenestra with medial surfaces slightly turned down
forming area for muscle attachment.
8. Some reduction of lateral pterygoid process and redirection anteriorly.
9. Loss of coronoid eminence but dentary still expanded dorso-posteriorly.
10. Fusion of dentaries at symphysis.
Synapomorphies o f Dromasauroidea and Higher dicynodonls
1. Reduction of septomaxilla.
2. Reduction of postorbital and zygomatic branches of the jugal.
Synapomorphies of Higher dicynodonts (C: Eodicynodon
+ Advanced forms))
1. Further shortening of preorbital area of skull.
2. Dorsal spur of premaxilla between nasals short.
3. Lateral plate of squamosal and external surface of zygoma elaborated for
attachment area of adductor externus lateralis.
4. Loss of teeth on anterior part of maxilla; horn present.
5. Vomers form anterior part of interpterygoidal vacuity.
6. Temporal fenestra further elongated with posterior margin extending
posteriorly beyond level of foramen magnum; medial margins of fenestra
further down-turned, forming vertical area for muscle attachment.
7. Dentary with built up area on lateral surface for insertion of adductor
musculature.
8. Articular and quadrate with long, convex articulatory surfaces.
9. Zygoma displaced dorsally.
Synapomorphies of Advanced dicynodonts ( D )
(Endothiodontoidea, Pristerodontoidea, etc.)
1. Premaxillae fused.
2. Lateral pterygoid process reduced and fully oriented anteriorly.
3. Insertion of lateral external adductor forwardly-placed.
4. Palatal exposure of premaxilla extended posteriorly to beyond the level of
the canine tooth or caniniform process.
5. Further lengthening of temporal fenestra.
6. Lowering of height of skull roof relative to jaw hinge.
7. Medial migration of postcanine teeth.
In addition, the following character states, presumably present in the pretherapsid ancestors of anomodonts, should be borne in mind for comparative
purposes.
1. Small or no coronoid eminence.
2. Long snout and tooth row.
3. Premaxilla without extensive palatal exposure.
4. Short temporal fenestra.
5. Large lateral pterygoid flange.
EVOLUTION OF DICYNODONT FEEDING
189
HYPOTHETICAL ANCESTRAL STAGES ON THE DICYNODONT LINE
From the cladogram four stages of dicynodont development have been
selected. Each stage is represented by a hypothetical common ancestor
determined by the characters present at certain nodes on the cladogram. For
example, the last common ancestor of dinocephalians and dicynodonts is called
the Pre-dicynodont stage and is represented by the characters found at node A
on the cladogram, shared by all dinocephalians and dicynodonts. The ancestor
of all dicynodonts, called the Ve’enjukouia-stage, possesses those characters which
all dicynodonts share and is found at node B on the cladogram.
For ease of description, features relating to musculature will be discussed in
detail first, then summarized together with relevant osteological features.
The j a w adductor musculature of dicynodonts and other therapsids
I n the following discussions the jaw musculature of dicynodonts of the
advanced dicynodont stage is to be compared with that of the pre-dicynodont
stage typified by the sphenacodont pelycosaur, Dimetrodon (Barghusen, 1973) and
where possible with ‘eotheriodonts’ (e.g. Biarmosuchus Sigogneau & Tchudinov,
1972), and with Venjukouia-stage dicynodonts such as the early dicynodont
Venjukouia (Barghusen, 1976). I t is not possible to reconstruct the jaw
musculature of Otsheria, an even more primitive dicynodont from the USSR, as
the lower jaw is unknown. A reconstruction of the early South African form,
Eodicynodon will also be given so that an Eodicynodon-stage may be included.
Several authors have attempted to reconstruct the jaw muscles of dicynodonts.
Cox (1959) discussed the cranial muscles of Kingoria. Ewer (1961) of
Daptocephalus, Cluver (1971) of Lystrosaurus, Cluver ( 1975) of Chelydontops,
Crompton & Hotton (1967) of Emydops and Lystrosaurus, King (1981a) of
Dicynodon trigonocephalus and Watson (1948) of Dicynodon. In general it is accepted
that the two main groups of jaw muscles found in extant reptilian-grade
amniotes, namely the external and internal adductor groups, were also present
in dicynodonts. The external adductor group consists of lateral and medial
external adductor muscles, while the internal adductor group is composed of the
pseudotemporalis and the pterygoideus muscles. A posterior adductor may also
have been present (Barghusen, 1973).
The external adductor muscles (Fig. 2)
The lateral external adductor muscle ( A E L ) . In Dimetrodon (Barghusen, 1973) the
external adductor muscles probably formed one undifferentiated mass
originating from the underside of the temporal roof, the walls of the posterodorsal parts of the temporal fenestra, the lateral part of the quadrate, and the
quadratojugal. There was also an origin from the cheek area and the muscle
might have extended from the cheek area to the lateral part of the temporal
fenestra attaching to an aponeurosis. The skull morphology of the
‘eotheriodonts’ suggests that a similar origin would have been present there. The
external adductor in Dimetrodon is postulated as inserting into a
bodenaponeurosis attaching to the coronoid eminence of the lower jaw.
In Venjukovia (Barghusen, 1976) the external adductor was probably
differentiated into two portions, a lateral and medial. Of these, the lateral
190
G . M. KING E T AL.
A
AEM
.
B
.
.
F
Figure 2. Lateral views of the skulls of A, Dimelrodon, B, Venjukouia, C , D, Eodicynodon, E, F, Dicynodon,
showing diagrammatically the attachments of the external adductor muscles. Scale bars: A, B, E,
F = 40 mm; C, D=20 mm. Abbreviations: AE, external adductor muscle; AEL, adductor externus
lateralis; AEM, adductor externus medialis.
muscle formed a fairly small mass originating from the inferior and medial
surfaces of the zygomatic arch, and possibly from the lateral surface of the
squamosal. The latter would be an incipient condition elaborated on in later
dicynodonts. The insertion of the muscle was probably into the fossa on the
lateral surface of the surangular and dentary of the lower jaw.
EVOLUTION OF DICYNODONT FEEDING
191
In later dicynodonts a large area of origin for the AEL is provided by the
squamosal which extends ventrally of the temporal fossa to form an external
plate below the rear of the zygomatic arch. This, together with the ventral
surface of the zygomatic arch (possibly right up to the postorbital bar) provided
a large area for the original of the AEL. It is probable that the lateral dentary
shelf which was present above the mandibular fenestra of some dicynodonts
(Cluver, 1970, 1971, 1974b, 1975; Crompton & Hotton, 1967) marks the site of
insertion of this muscle (Cluver, 1971, 1975; Crompton & Hotton, 1967; King,
1981a). Where a lateral dentary shelf is not present, the muscle probably
inserted onto the anterior part of the lateral surface of the lower jaw, where a
rugosity is sometimes present (King, 1979).
The medial external adductor muscle ( A E M ) . As implied earlier there is no
separate medial division of the external adductor in Dimetrodon. In Venjukovia the
external adductor probably took origin from the undersurface of much of the
skull roof and from the outer face of that part of the postorbital forming the
lateral margin of the temporal roof, as well as from the dorsal and lateral parts of
the posterior wall of the temporal fenestra including the squamosal and
quadrate. Its insertion may have been into a bodenaponeurosis on to the apex of
the coronoid eminence, as for the external adductor in Dimetrodon. Barghusen
(1976) reviews the evidence for these attachments.
In later dicynodonts two divisions of the muscle are identified and it is
generally accepted that the medial external adductor muscle in later
dicynodonts filled the temporal fossa and originated from its medial, posterior
and lateral margins. However, as regards the area of insertion of this muscle
numerous ideas have been put forward. In Chelydontops a coronoid eminence is
present on the lower jaw and it is possible that the AEM inserted on this
elevation via a bodenaponeurosis (Cluver, 1975), as has been postulated for
Dimetrodon (Barghusen, 1973). In Emydops and Lystrosaurus (Cluver, 1970;
Crompton & Hotton, 1976) this muscle probably inserted into the longitudinal
groove on the dorsal surface of the dentary and may also have extended onto the
dorso-medial side of the anterior portion of the surangular.
On the other hand, King (1981a) considers that a more likely insertion in later
dicynodonts is on the medial side of the lower jaw into the intramandibular
cavity as she considers that there was a horny covering in the dorsal dentary
groove, prohibiting muscle insertion.
The posterior adductor muscle
Barghusen (1973) finds no direct evidence of this muscle in Dimetrodon but it
would be expected to originate from the quadrate, medial to the origin of the
external adductor. By analogy with Sphenodon the origin would have included the
lateral face of the anterior process of the quadrate. The insertion would have
been into the broadly-open posterior part of the adductor fossa on the medial
side of the lower jaw. Little can be said about the position or occurrence of this
muscle in Venjukovia.
As far as Advanced dicynodonts are concerned, in Chelydontops, Oudenodon and
Dicynodon there is evidence for a posterior adductor as a scar is present on the
antero-lateral surface of the quadrate which possibly marks the origin of such a
192
G . M. KING E T AL.
muscle (Cluver, 1975; King, 1981a). This muscle most probably inserted into the
posterior part of the intramandibular cavity (Cluver, 1975; King, 1981a).
The internal adductor muscles (Fig. 3)
The pterygoideus muscles. The terminology adopted here for the two portions of
the pterygoideus muscle follows Barghusen (1973) whose terminology is based on
comparison of modern reptilian-grade amniotes (Sphenodon, chelonians,
crocodilians, lacertilians). The terms anterior pterygoideus and posterior
pterygoideus used by Barghusen and here are not equivalent to those used by,
for example, Cox ( 1959), Cluver ( 1971) or King ( 1981a), who all follow Adams’s
(1919) terminology. Barghusen (1973) argues that Adams did not consider
topographic equivalency when naming parts of the pterygoideus muscle in
different reptiles. Barghusen’s identification of the various parts of the
pterygoideus muscle complex is consistent with those of Haas (1973) and
Schumacher (1973) in extant forms.
Following Barghusen (1973), and most authors, two portions of the
pterygoideus, the anterior and posterior, are recognized. However, evidence for
the site of origin and insertion of the anterior part of the muscle is scanty, not
only in dicynodonts, but also in Dimetrodon. Barghusen (1973) says that there is
no direct evidence of the muscle in Dimetrodon, but that it may have originated
from the dorsal surface of the palate in the suborbital region. I t might have
inserted on the medial surface of the lower jaw in and around the adductor fossa
anterior to the insertion of the posterior adductor. This muscle is not discussed
for Venjukouia by Barghusen (1976). The reconstruction of the muscle without
direct morphological evidence of its presence is usually done on the basis that a
division of the pterygoideus muscle into two parts is a primitive amniote feature,
occurring as it does in chelonians and crocodilians (the absence of the anterior
pterygoideus in modern lizards is presumed to be secondary). The reconstruction
of the muscle in later dicynodonts given here is based on the reexamination by
one of us (G.M.K.) of Dicynodon trigonocephalus (No. TSK 14) and two specimens
of Oudenodon bainii (Nos. TSK 67 and 104) housed in the Oxford University
Museum.
The origin of this muscle could not have been from the dorsal palate as in
Dimetrodon because the only area available for such an origin would be the
antero-ventral part of the floor of the orbit, so far forward that the muscle would
have obstructed the orbit. With shortening of the snout and tooth row in
dicynodonts (see below) came a reduction in the dorsal palatal area available for
muscle attachment and at some point the anterior pterygoideus muscle (if the
origin postulated by Barghusen for Dimetrodon is correct) must have shifted to a
new area on the palate. The morphology of the skull of Venjukouia would suggest
that this had already occurred in that form. I t is considered here that the origin
of the anterior pterygoid muscle in dicynodonts was on the ventro-lateral part of
the lateral pterygoid flange.
In order to clear the grinding surfaces of the lower jaw and to prevent fibres of
the muscle becoming trapped between the jaws during antero-posterior
movement, the insertion of the anterior pterygoideus must have been fairly far
back below the insertion of the medialmost fibres of the medial external adductor
muscles on the inner side of the lower jaw. A shallow fossa is present in the forms
EVOLUTION OF DICYNODONT FEEDING
193
AP
/ -
lat pt p r o ~
B
F
PF
l
.
.
ti
Figure 3. Lateral and ventral views of A, E, Dimetrodon, B, F, Venjukouia, C, G , Eodivnodon and D, H,
Dicynodon showing diagrammatically the attachments of the internal adductors. Stippling= areas of
origin; broken lines=attachments or muscles passing behind a bony surface. Scale bars: A, B, D, E,
F, H = 4 0 mm; C, G = 2 0 mm. Abbreviations: AP, anterior pterygoideus muscle; lat pt proc, lateral
pterygoid process; PP, posterior pterygoideus muscle.
examined, extending anteriorly from the medial condyle of the articular. The
prearticular is shallowly excavated posteriorly to form part of this fossa, which
also incorporates the medial side of the prearticular ventral to the mandibular
fenestra. The posterior excavation of the prearticular is covered with fine
I94
G . M. KING E 7 AL.
striations and it is proposed that this would make a suitable site for the insertion
of the anterior pterygoideus. It would therefore pull forwards, upwards and
medially .
Turning now to the posterior pterygoideus muscle, more morphological
evidence is usually available for the reconstruction of this muscle. In Dimetrodon
Barghusen postulates that it would have arisen from the surface of the pterygoid
posterior to the medial pterygoid crest, including the whole of the quadrate
ramus of the pterygoid. The muscle would have inserted on the descending
process of the articular (on the medial side of the jaw) and possibly through the
notch postero-medial to the reflected lamina of the angular to insert on the
lateral surface of the body of the angular. The attachment areas of the muscle in
the Russian ‘eotheriodonts’ was probably very similar since the relevant areas of
morphology of these forms are not very different from those in Dimetrodon.
The origin in Venjukouia would have been similar, but the insertion would have
been on the ventro-medial face of the articular and the antero-medial face of the
retroarticular process. Barghusen feels that this muscle would not run around the
lower surface of the lower jaw to insert on the lateral face because the space for
the muscle beneath the reflected lamina of the angular would be too confined.
In the later dicynodonts examined there is a discrete patch of striations on the
lateral surface of the anterior pterygoid ramus, extending onto the
ectopterygoid. If, as Barghusen (1976) argues, this area is the equivalent of the
lateral pterygoid flange in forms such as Dimetrodon, then part of this striated area
could form the origin of the posterior pterygoideus muscle which would occupy
the postero-lateral surface of the lateral pterygoid flange extending into the
ventral recesses on either side of the median pterygoid ridge and posteriorly part
way along the quadrate ramus of the pterygoid. By analogy with modern
reptilian-grade amniotes the insertion would probably have been the medial
surface of the lower jaw on the ventral surface of the median condyle, on the
ventral surface of the prearticular, and also wrapping round the jaw ramus to
find a small insertion on the lateral surface of the jaw. Although Barghusen
(1976) thinks that an insertion onto the lateral surface of the jaw is unlikely in
therapsids there does seem to be ample room for at least a small insertion of the
muscle, postero-ventral to the reflected lamina, in most dicynodonts. There are
fine striations on the jaw bones in the areas postulated for the insertion in the
specimens examined. So positioned, the muscle would pull upwards, forwards
and medially.
The pseudotemporalis muscle. In Dimetrodon the origin of this muscle is from the
parietal and epipterygoid and it inserted into or around the anterior margins of
the adductor fossa. No information about this muscle in Venjukouia is given by
Barghusen ( 1976).
A constant feature in all dicynodonts is a clearly demarcated recess beneath
the lateral edge of the intertemporal skull roof which is considered to be the
origin of the pseudotemporalis muscle (Cluver, 1975). (King ( 1981a) considered
that in Dicynodon trigonocephalus this recess served for the origin of an inner slip of
the AEM, but further investigation shows that the recess described by King is
not in the same position as that described by Cluver). I t is considered in the
present paper that the muscle has its origin not actually in the fossa described by
Cluver, but on its medial wall. The fossa is simply the byproduct of a tendency to
EVOLUTION OF DICYNODONT FEEDING
Russian
Zone ISZ
---
195
Daptocephalu!
ZOM
Flowerpot
S. Anqelo
Oiinetrwbn
Clear Fork
Oiinei-n
Wichita
Cutkr
Figure 4. Time chart showing the relative ages of the forms discussed in the text.
evolve a low angle insertion wall in its medial side. This complies with the idea of
Frazetta (1968) that a low angle insertion is important for strong muscle
attachment.
According to Cluver ( 1975) the pseudotemporalis probably inserted on the
inside of the lower jaw above the Meckelian fossa so that it occupied the space
between the pterygoideus and the AEM (Crompton & Hotton, 1967). It is here
considered that in view of the fact that the AEM inserted partly in the
Meckelian fossa, the more medial position of the pseudotemporalis fibres would
have restricted the insertion of the pseudotemporalis to the antero-ventral rim of
the Meckelian fossa. However, the origins and insertions of this muscle cannot be
defined with any certainty (Crompton & Hotton, 1967; King, 1981a).
The j a w adductor musculature of Eodicynodon oosthuizeni
Recently, several papers have been written on the cranial morphology of
Eodicynodon oosthuizeni, the earliest dicynodont known from South Africa (Barry,
1972, 1974a, b; Cluver & King, 1983; Rubidge, 1984, 1985). Figure 4 illustrates
the relative ages of the Permian forms. Although Eodicynodon displays features
advanced over the early Russian forms such as Venjukovia, and over the
dromasauroids, it still lacks several of the synapomorphies which unite other,
later dicynodonts, given on page 188. As can be seen from the character suites
and the cladogram (Fig. l ) , Eodicynodon retains some primitive characters such as
paired vomers and premaxillae, a greatly (compared with later dicynodonts)
expanded lateral pterygoid process, a deep skull and a zygoma which is not
emarginated as much as in other dicynodonts (Fig. 5). Below, it will be argued
G. M. KING E T AL.
196
-
-
Figure 5. Eodicynodon oosthuizeni. Skull in A, dorsal, B, C, F, palatal, D, lateral views and lower jaw in
E, lateral, G, dorsal views. Scale bars: A, B, C, F = 10 mm; D, E, G = 2 0 mm. Broken
lines =incomplete parts of specimen. After Cluver & King, 1983 and Rubidge, 1985. Abbreviations:
lat d s, lateral dentary shelf; lat pt proc, lateral pterygoid process; pc t, postcanine teeth.
that is is possible to trace a sequence of anatomical/functional grades in the
Dicynodontia, and the retention of the primitive features mentioned above
indicate that Eodicynodon had not reached the same anatomical/functional grade
as later dicynodonts and is therefore an important link in the investigation of
the sequence. Until now the functional anatomy of Eodicynodon has been little
investigated and so a detailed account of the jaw muscles in this form will be
presented.
It should be noted that Rubidge (1984) considered that in Eodicynodon the
squamosal did not form an external plate below the rear of the zygomatic arch as
is characteristic of all other dicynodonts. This had important implications
regarding the origin of the AEL. More recently, however, two better preserved
specimens of Eodicynodon have been found in which a lateral external plate of the
squamosal is definitely present.
The lateral external adductor muscle (Fig. 2 )
It is considered that the AEL muscle arose, as in other dicynodonts, from the
lateral external plate of the squamosal as well as from the postero-ventral part of
the zygomatic arch to about halfway along the temporal fenestra. It inserted on
the postero-dorsal portion of the lateral dentary shelf of the lower jaw. The
lateral dentary shelf is dorsally placed in Eodicynodon (Cluver & King, 1983), and
is situated just ventrally to a coronoid eminence in a position which is relatively
far back in the lower jaw when compared with other dicynodonts. From the top
EVOLUTION OF DICYNODONT FEEDING
197
of the coronoid eminence the dentary slopes ventro-laterally to the lateral
dentary shelf which then extends in a lateral direction. The area on the dorsal
side of the lateral dentary shelf is suggestive of an insertion for the AEL, as a
triangular groove is present here with its apex pointing forward and becoming
broader towards the posterior side.
The medial external adductor muscle (Fig. 2 )
The AEM muscle arose on the medial, posterior and postero-lateral borders of
the temporal fenestra which are formed by the postorbital and squamosal bones
and which provide a large area for the attachment of muscles.
In Dimetrodon and most other therapsids (as mentioned earlier) a coronoid
process is present onto which the AEM inserts. However, in all dicynodonts
except Chelydontops (Cluver, 1975) a coronoid eminence is absent. Eodicynodon
retains a structure which appears to be homologous to a coronoid eminence just
dorsal to the posterior end of the lateral dentary shelf. This has fine striations on
the medial side and seems to be an appropriate site for the insertion of the AEM
which would have extended ventrally as far as the Meckelian fossa as King
( 1981a) postulated for Dicynodon trigonocephalus. This insertion would mean that
the AEM would exert a postero-dorsal pull on the lower jaw.
I n Eodicynodon, insertion of the AEM into a longitudinal dentary groove as in
Emydops and Lystrosaurus is not possible as no groove is present.
Posterior adductor muscle
It is inferred that the posterior adductor muscle of Eodicynodon arose on the
antero-medial face of the quadrate and inserted in the adductor fossa as
described for Dimetrodon and noted by Cluver (1975) in Chelydontops. A
longitudinal ‘trough’ is formed on the medial side of the lower jaw running from
the posterior end of the lower jaw to the adductor fossa between the prearticular
and angular bones and provides a large area for insertion of this muscle.
Internal adductor muscles (Fig. 3 )
The pterygoideus muscles. The anterior muscle would probably have had an
origin and insertion similar to those of other dicynodonts as the morphology of
Eodicynodon in the relevant areas is not very different from that of other
dicynodonts. The origin of the muscle was on the dorso-lateral sides of the lateral
flange of the pterygoid, topographically equivalent to the situation in Dimetrodon,
and it would have inserted on the medial and lateral surfaces of the articular,
antero-medial to the median condyle. The anterior pterygoideus muscle of
Eodicynodon would have exerted a forward, upward and medial pull on the lower
jaw.
The attachment areas of the posterior pterygoideus would not have been
greatly different in Eodicynodon from those in later dicynodonts. There are wellmarked recesses on either side of the median pterygoid ridge in Eodicynodon,
whose surfaces grade smoothly into that of the lateral surface of the lateral
pterygoid process and probably served for the origin of the posterior
pterygoideus muscle. This muscle wrapped around the postero-ventral surface of
the angular behind the reflected lamina, ventral to the insertion of the anterior
pterygoideus muscle, to insert on the ventro-lateral side of the angular and onto
the antero-lateral side of the lateral condyle. Apart, then, from the lateral
198
G . M. KING E T AL.
pterygoid process being more extensive ventrally, and not so anteriorly directed
in Eodicynodon, there would seem to be little evidence for a very different position
of the pterygoideus from that in later dicynodonts.
The reconstruction of this muscle in Eodicynodon would imply that the muscle
would have exerted a predominantly upward, forward and medial force on the
lower jaw.
The pseudotemporalis muscle. In Eodicynodon there is a recess on the ventral side of
the parietal just lateral to the dorsal portion of the epipterygoid. As in other
forms, the medial wall of this recess, and not the roof of the fossa, in all
probability served for the origin of the pseudotemporalis muscle.
In generalized lizards the pseudotemporalis muscle inserts on the coronoid
process via a bodenaponeurosis (Lakjer, 1926). However, in Eodicynodon the area
of insertion of this muscle is not certain.
To summarize, the jaw musculature of Eodicynodon was probably not arranged
very differently from that in later dicynodonts. The main points of difference
would be the presence of a coronoid eminence to which the AEM attached, the
postero-dorsal position of the lateral dentary shelf and hence insertion of the
lateral external adductor muscle, and the large lateral pterygoid process, not so
anteriorly directed as in later forms, to which the pterygoideus muscles attached.
These differences are taken below to indicate that Eodicynodon had not reached
the same functional level as later dicynodonts.
Summary of musculature and osteology in the ancestral stages
A comparison of the structure of Eodicynodon and later dicynodont skulls and
their possible muscle attachments, with earlier forms such as sphenacodonts and
eotheriodonts suggests that the stages in skull anatomy listed below evolved
between the Ufimian and Kazanian Ages. This is estimated to be a period of
some 5.0 million years. Russian eotheriodonts (Sigogneau & Tchudinov, 1972)
date from the Ufimian Age (Fig. 4).Although detailed skull functional anatomy
has not been carried out, their osteology is so similar to that of sphenacodonts in
all pertinent features mentioned below that it seems reasonable to conclude that
they were little advanced over the sphenacodont grade in these respects. At
present no older eotheriodonts are known and until this is so the age of the
Russian forms is taken to represent the lower time boundary of the evolution of
dicynodont characters. The upper boundary is taken to be the Tapinocephalus
zone of South Africa which is the first date at which fully-developed dicynodonts
(Diictodon) are known.
The Pre-dicynodont stage ( A )
At this stage the attachment area for the pterygoideus muscles was large. The
adductor muscle insertion on the lower jaw was situated posteriorly. There was
no attachment of adductor muscle fibres on the zygoma. Perhaps the most
salient osteological features at this stage were the absence of a secondary palate,
the long preorbital part of the skull and a jaw-hinge which permitted little or no
longitudinal movement of the lower jaw.
EVOLUTION OF DICYNODONT FEEDING
199
The Venjukovia-stage (B)
At this stage of dicynodont development there was a slight reduction in the
mass of the pterygoideus muscles and a slight forward migration of the adductor
insertion on the lateral side of the lower jaw. This second feature was aided by
the zygoma being emarginated from below. There was possibly incipient
attachment of the AEL muscle to the lateral surface of the squamosal. In
addition, the temporal fenestra became elongated and establishment of muscle
origin on both its medial and posterior surfaces took place. Osteological features
at this stage included the shortened preorbital region and the shortened tooth
row. There was some covering of horn on jaws in some forms and the jaw joint
permitted some antero-posterior movement of the lower jaw. An incipient
secondary palate was present.
The Eodicynodon-stage (C)
At this stage there was further forward migration of the adductor insertion on
to the built-up area on the dorso-lateral surface of the lower jaw. An external
plate of the squamosal had developed, and there was a well-developed
attachment of the AEL to the lateral surface of the squamosal. Teeth had been
lost from the anterior part of maxilla and horn was present. Extensive anteroposterior movement of lower jaw was possible.
Advanced dicynodont stage (D)
At this stage a more antero-ventral and more extensive insertion of the AEL
on the lateral dentary shelf or side of the lower jaw is seen. The lowering of skull
roof relative to the jaw articulation and to the muscle insertions increased the
back-pull of the AEM and AEL. There was further reduction of pterygoideus
muscle. The secondary palate extended posterior to the canines and the extent of
the horn covering had increased. There were more extensive contact areas on the
upper and lower jaws for food processing and medial migration of the postcanine
teeth had taken place.
AN EXPLANATION FOR THE DEVELOPMENT OF THE ADAPTIVE COMPLEX
In order to explain the development of the sequence of changes seen above we
shall put forward the hypothesis that the particular adaptive complex described,
i.e. the masticatory system of the dicynodont, was responding to the need to
break up food in the mouth more effectively. More specifically, it will be
suggested that in the four stages that were outlined above, the masticatory
system becomes more effective at food preparation by increasing the amount and
nature of relative jaw movements, amongst other things.
The evolution of propaliny (fore and aft movement of the lower jaw with
respect to the upper) as manifested in the dicynodonts imposes three
prerequisites (Pl-3) and consequences (Cl-8) on skull function which are
outlined in the flow diagram of Fig. 6. These prerequisites are not present at the
pre-Venjukovia grade (or at least only in a very rudimentary fashion) and the
intention here will be to see whether, if such prerequisites are evolved, they result
in an organization similar to that of the dicynodont skull.
G . M. KING ET AL.
200
column 2
column I
PREREPUISITES FOR EFFECTIVE PROFALINY
PI. Robtln movomont of t k ] a m
Slldlng law hlngo
P2. Murclo orgonlaatbn
a) pmdrtlon of mbtkw monmont
b) productbn of adwuak moment arm and powor
C) probdbn of adoquah lowrr jou oncumbnP3. Guldma of the l o w law
ACCOMPLISHED IN DICYNOM)NTS BY:
Adduclor mmck lnwtion migmtlng ankktly
-Antorbr m w l r Inrrrtlm+addltlonal bulk of m ~ c l o r
+
Anterior murck lnaortbn kngthmlng of
Ptmy@dwr origin klng pbed mom modblly (ouocbtod wllh CS)
M a rxhrnur lakmllr orlgln klng p l a d moro lotrmlly
(amclatod with C5)
column 3
ANATOMICAL CONSEQUENCES
Figure 6. Flow chart outlining functional requirements for effective propaliny and their anatomical
consequences for the dicynodont skull.
Relative movement of the j a w s (PI)
In order to have relative movement of the jaws various possibilities present
themselves, such as a jaw-hinge which permits longitudinal or transverse
movement of the lower jaw, or skull kinetism which permits movement of some
part of the upper jaw against the lower (see, for example, Norman &
Weishampel, 1985 for a discussion of Iguanodon). An examination of the
dicynodont jaw-hinge shows that it would have permitted extensive anteroposterior movement of the lower jaw (Watson, 1948; Crompton & Hotton, 1967;
King, 1981a). Both the quadrate and articular have lateral and median condylar
surfaces. The lower jaw condylar surfaces are extensive. The anterior portion is
composed of surangular and articular forming a single concave facet (the lateral
condylar surface). Posteriorly this lateral surface becomes convex anteroposteriorly and concave from side-to-side. From its medial side the convex
median condyle arises. The profile of the articular condylar surfaces at this level
is a W-shape, and this is matched by the profile of the quadrate condyles. The
elongated nature of the articular condylar surfaces permits longitudinal
movement of the quadrate with two preferred resting positions. In the first, the
quadrate lateral condyle rests in the anterior, dish-like lateral articular facet and
the median condyles do not contact. In the second, the quadrate lies further
back, at the level of the W-shaped profile, with each quadrate condyle resting on
an articular condyle. However, as well as permitting antero-posterior movement,
the design of the jaw hinge also imposes some stability on the joint. The Wshaped profile forms an extremely stable jaw joint in which the articulatory
surfaces can contact one another over a large area, even with the lower jaw
EVOLUTION OF DICYNODONT FEEDING
20 1
protracted far forwards and with the jaw open, when there is a risk of
dislocation. In addition this joint rules out relative transverse movement of the
lower jaw (see also page 204). This situation contrasts with that of the retracted
position of the lower jaw when the quadrate lateral condyle rests in the dish of
the surangular-articular lateral condyle but the median condyles do not touch at
all. This position is a very stable rest position with the jaw closed.
It can be seen, then, that if relative movement of the jaws is a prerequisite for
propaliny, then the dicynodont skull is capable of meeting this requirement.
Muscle organization ( P 2 )
In order to move the lower jaw backwards and forwards and to retain the
lower jaw in close contact with the upper for mastication, adductors are
necessary which are (a) positioned to produce relative movement, (b) forceful
enough (i.e. with an adequate moment arm) to produce mastication and (c)
long enough to permit adequate excursion of the lower jaw. Can these
prerequisites be found in the dicynodont skull?
One of the striking differences between the muscle organization of dicynodonts
and other therapsids is that the insertion of the external adductor muscles is far
anterior on the outside of the lower jaw. This has several consequences related to
the requirements outlined above.
Production of relative movement. For relative movement to take place the origin
and insertion of the jaw adductor muscles must not be in a vertical line. The
positions of the adductors have been described in detail and it can be seen that
the dicynodont jaw muscle organization meets this requirement since the
insertion of the external adductors is far anterior to their origin, more so than in
any other therapsid group. Obviously, this displacement of origin and insertion
could also be accomplished by moving the origin of the adductors more
posteriorly, or indeed by doing both. That it is in fact a movement of the
insertion and not the origin (at least in earlier dicynodonts) that has taken place
may be confirmed by studying the relative proportions of the dicynodont skull
and jaw compared to those of other therapsids.
Anterior displacement of the insertion of the adductors in this way produces a
muscle which has a large backward component. I t is at least theoretically
possible that a forwardly pulling muscle could accomplish the same task of
producing relative movement of the jaw; for example, a muscle which originated
on the external surface of the maxilla or on the zygoma, and inserted on the
posterior corner of the external suface of the lower jaw (as occurs in rodents
today). There is, in fact, no evidence of any such muscle being present in
dicynodonts (see King, 1981a). On the contrary, the presumed ancestral
condition would have already had a slightly backwardly-pulling muscle (as
evidenced by sphenacodonts and eotheriodonts) and it must therefore be
considered that this is a phylogenetic constraint on the system under discussion.
A backwardly-pulling muscle is the evolutionary starting point for the muscle
organization and this will be discussed later.
However, the internal adductor muscles do present forwardly-pulling muscles
(the anterior and posterior pterygoideus muscles) which might have been useful
in producing a forward power stroke. It is possible that these muscles were not
elaborated further because their area of origin on the palate is limited, restricting
G . M. KING ET AL.
202
cor em
AE
A
0
Figure 7. Diagram illustrating the effect on the moment arm of different muscle insertions.
A, Muscle inserted posteriorly on un-elevated surface of the lower jaw. B, Muscle inserted on a
coronoid eminence. C, Muscle inserted anteriorly. Abbreviations: AE, average line of action of the
external adductor muscle; cor em, coronoid eminence; 1, line passing through jaw-hinge and anterodorsal tip of the jaw symphysis; m, moment arm of AE. Large dots indicate points of insertion.
their bulk, and also because the moment arm of these muscles is limited. The
obvious ways of increasing the moment arm of these muscles would involve
changes to the structure of the palate or deepening of the lower jaw perhaps not
possible within the adaptive complex.
Assuming then, that the insertion of the external adductors is moved
anteriorly, this also has a bearing on other requirements of propaliny as
discussed next.
Production of an adequate moment arm. Other parameters being equal in the jaw
muscle organization, an insertion of the adductors further away from the jawhinge will increase the moment arm, and thus the force, of the muscle (see
Fig. 7). In addition, adding extra bulk to the muscles would also obviously
increase their force. As pointed out earlier, dicynodonts are the only noncynodont therapsids which have a lateral, as well as a medial, division of the
external adductors. Barghusen ( 1976) considers that in Venjukouia a lateral
external adductor muscle which had its origin on the lateral. side of the
squamosal, was already present. As the medial adductors became more
important in later dicynodonts, so the lateral external muscle was elaborated
and its area of origin increased by expansion of the squamosal lateral to the
zygoma, as is the case in Eodicynodon and all subsequent dicynodonts.
It was noted that stage E dicynodonts have reduced the height of the skull, repositioning the origin of the external adductors. This increases the backward
component of the muscles, but could reduce the moment arm if there is not
sufficient antero-ventral displacement of the insertion of the muscles. Obviously
EVOLUTION OF DICYNODONT FEEDING
203
the positions of the origins and insertions of any of the muscles under discussion
will be a compromise between producing different effects such as increased
moment arm or increased backward component.
At the same time, as the area of origin of the AEL muscle, and hence the
muscle itself, became larger, the insertional area of the muscle shows evidence of
increase too. In Venjukouia there was incipient insertion of the lateral fibres on the
lateral surface of the lower jaw, and slightly more in Eodicynodon. In later
dicynodonts even more extensive insertion took place on the lateral surface of the
dentary, often on the lateral dentary shelf, with a tendency to be more ventrally
placed than in Eodicynodon.
Production of adequate excursion of the lowerjaw. The lower jaw of an average-sized
Late Permian dicynodont (Oudenodon bainii) may move approximately 13% of
the jaw length anterio-posteriorly. Obviously the muscles which produce this
movement must be long enough that their contraction will produce this change
in horizontal distance. This is not likely to be a limiting factor as far as the
external adductors are concerned. However, it may well be important when the
pterygoideus muscles are considered.
If the lower jaw moves back and fore to any great degree the problem arises
that the pterygoideus muscle fibres in a pre-dicynodont stage are too short and
therefore inhibit jaw excursion. A possible solution to this problem is to move the
origin of the muscles further forward, increasing the length of the muscle. As has
been stated before, sphenacodont pelycosaurs have an enormously expanded
lateral pterygoid process which is oriented backwards, while in Venjukouia and
Eodicynodon the process, while still quite large, is oriented forwards. In later
dicynodonts the pterygoid process is greatly reduced and does not protrude far
ventrally. The forward orientation of the process and its later reduction could
have been a result of the need for a longer fibre length of the pterygoideus
(particularly anterior) muscles in order to permit extensive propalinal movement
of the jaw. It has been postulated that one of the functions of the lateral
pterygoid process in primitive synapsids was to guide the lower jaw and help to
prevent dislocation of the jaw when struggling prey was taken into the mouth.
The fact that dicynodonts became herbivores early on would render this function
unnecessary and therefore the lateral pterygoid process was free to change its
orientation and be reduced in size.
However, one problem with reorientation and reduction of the process is that
a smaller area is left for the origin of the pterygoideus muscles which must in
consequence become smaller, and cannot subsequently take a major role in
producing the force for mastication (although they would still be adequate for
producing the non-power protractive stroke). Another problem is that with the
reduction of the process there is less guidance for the movement of the lower jaw
during propalinal movement. Accurate movement of the lower jaw, and
therefore some kind of guidance, would have been essential to make sure that the
contact surfaces of the jaws came together accurately to masticate food.
Reduction of the lateral pterygoid process and the concomitant reduction of the
pterygoideus muscles would not impair guidance of the jaw as, just as the
external adductors take over the task of longitudinal movement of the lower jaw
from the pterygoideus muscles, so also the lower and more lateral placing of the
AEL (see page 207) would put it in a more favourable position for lateral control
204
G . M.KING ET AL.
of the lower jaw during propaliny, as well as in its roles of adduction and
retraction. In turn the more medial placing of the origin of the pterygoid
muscles, once the lateral pterygoid processes are reduced, would provide an
antagonistic force to the laterally placed AEL, producing finer control of the
medio-lateral movement of the lower jaw.
Both of these changes in position of the muscles involved come about in
response to more than one selection pressure. They permit muscular guidance of
the lower jaw, and the new placement of the pterygoideus results from the need
to make its fibres longer to permit adequate antero-posterior jaw excursion. This
makes it an effective protractor of the jaw, and the new placement of the AEL
results from bowing out of the zygoma as a necessity for permitting an anteriorly
placed external adductor (see below).
There is evidence which indicates that in some forms control of the lateral
movement of the lower jaw was not entirely muscular. Cluver (1974b) notes that
in Emydops sideways movement was prohibited by the upper postcanine teeth
fitting outside the lower teeth; in Lystrosaurus the tight-fitting tusks, caniniform
process and palatal rim, as well as the W-shaped jaw-hinge prevent transverse
movement of the lower jaw. The form of the dicynodont jaw-hinge which also
helps to prevent transverse movement of the jaw has been mentioned earlier
(page 201). Such mechanisms would aid muscular control in making sure that
the dentary meets specific areas of the palate.
The lateral pterygoid process becomes further reduced in dicynodonts past the
Eodicynodon level. In Eodicynodon the dentary symphysis of the lower jaw is short
and there are no expanded areas on the dorsal side of the dentary except for a
small dentary table just behind the symphysis (Rubidge, 1984). The secondary
palate is also relatively small as the premaxilla is not as expanded posteriorly as
in later dicynodonts with the result that there is not a large anterior contact area
between the upper and lower jaws. The major areas of contact were the dorsal
surface of the lower jaw just anterior to the lateral dentary shelf, where there are
sometimes teeth present, and the small dentary table in front of them. These
would probably have occluded against the rugose palatine areas and median
palatal portion of the maxillae respectively (Rubidge, 1984).
Later forms with better developed secondary palates would have had a more
extensive palatal occlusal area and to make contact with most of this the lower
jaw would need to be retracted a considerable distance. If a well-developed
lateral pterygoid flange had been present in these forms (as is found in
Eodicynodon) then as the lower jaw was pulled back it would have eventually
either abutted against the lateral pterygoid process and been caused to stop, or it
would have been caused to ride over the process. If the anterior part of the lower
jaw was being forced dorsally at this point to make occlusal contact, then the
lateral pterygoid process would have acted as a pivot, forcing the posterior end of
the jaw away from the hinge (Fig. 8). In Eodicynodon with its shorter occlusal
palatal surface retraction is less extensive and the lateral pterygoid process
always remains separated by a gap from the jaw ramus, therefore not obstructing
retraction. However, in later forms this possibility of obstruction, as well as
reorganization of the pterygoideus muscles, might have been associated with
reduction of the process.
Considering the anatomical consequences (column three of Fig. 6) on skull
design these prerequisites for muscle organization cause, it can be seen that the
EVOLUTION O F DICYNODONT FEEDING
A
205
0
d
Figure 8. Diagram illustrating the effect of an extensive lateral pterygoid process on excursion of the
lower jaw. A, Lower jaw protracted and not abutting on the lateral pterygoid process. B, Lower jaw
retracted and abutting on the lateral pterygoid process. C, Lateral view showing the lower jaw
riding over the lateral pterygoid process causing the jaw articulation to be forced apart.
Abbreviations: lat pt proc, lateral pterygoid process; Ij, lower jaw; p, lateral pterygoid process acting
as a pivot. Arrows show the direction of movement of the tip and articular region of the lower jaw.
typical dicynodont skull could indeed be explained as being adapted to meeting
the prerequisites.
The reduction of the lateral pterygoid process, so typical of the dicynodonts,
has already been accounted for above. Other dicynodont features (C3-C7)
require further explanation, but are basically understandable as consequences of
moving the insertion of the external adductors anteriorly.
DeMar & Barghusen (1973) investigated the increase in height of the coronoid
process in the therapsid lineage leading to mammals. They argue that two
factors in the mastication system are being improved: the degree of the
backwardly-pulling component of the external adductors and the moment arm
of those adductors. The first may be in response to the need to counteract the
force of the weight and struggles of prey at thc front of the jaws, and the second
would increase the force of the muscle. DeMar & Barghusen show that the
moment arm of the adductors could be increased in two basic ways: either the
insertion could be onto a raised coronoid process (which would also position the
muscle to give more of a backward component) or the insertion of the muscle
could be more anterior on the lower jaw. Initially, the second alternative gives a
206
G . M.KING ET AL.
much greater increase in MA for a given increase in the horizontal distance of
the insertion moved, than does increasing the height of the coronoid process
(Fig. 7). However, as DeMar & Barghusen show, most therapsids have adopted
the first alternative. It is argued that this is because inserting the adductors on a
coronoid process increases the backward component which in itself is useful, but
more importantly perhaps, inserting the adductors further forward results in
“morphological absurdities” by which it is meant that the adductor musculature
would encroach into the orbital region so that the orbits and subtemporal fossa
would be displaced anteriorly, possibly leading to the relative length of the tooth
row being reduced and the relative position of the nares being modified. A study
of the dicynodonts, however, indicates that these are just the kinds of changes
seen in the dicynodont skull: the preorbital region of the skull is short compared
to that of other therapsids and the tooth row/horn-covered areas are short; the
temporal fenestra does extend into the anterior half of the skull; and, of course,
there is no coronoid process. To the extent that the dicynodonts were successful
animals, these morphological changes could not have been so absurd! However,
the question still remains of why dicynodonts improved the MA of the adductors
in a way quite different from all other therapsids, i.e. by moving the insertion of
the adductors anteriorly and not raising the coronoid process. The simplest
explanation is that if the raising of the coronoid process was initially to give a
more backwardly-pulling muscle added strength to combat the forces of weight
and struggles of prey, then presumably dicynodonts became committed to a
herbivorous diet before such changes began. The fossil evidence certainly points
to the earliest dicynodonts currently known (i.e. Venjukoviu and Otsheriu) already
being adapted to herbivory but since nothing is known about dicynodont
ancestry prior to these stages this part of the hypothesis cannot be directly tested
at present.
To return to the forward displacement of the orbit necessitated by inserting
the adductors more anteriorly, it was suggested that a consequence of this was a
reduction of the preorbital part of the skull. One obvious way to counteract this
problem would be to elongate the immediate preorbital area, carrying the orbit
forwards out of the way of the muscle. However, this would have the
disadvantage that the length of the jaw would be increased thereby reducing the
strength of the bite-force. If a kinetic inertial feeding system were being used
then length of the jaw would not affect the strength of the bite force, as Kemp
(1982) points out for dinocephalians. However, the importance of the ability to
grind food between the jaws requires a transition to a static pressure system in
dicynodonts, where the inverse relationship between the bite force and the
length of the jaw does become a consideration. I t may well be that the typical
dicynodont short preorbital region reflects both (a) an attempt to increase the
relative size of the bite force by reducing the length of the lower jaw, and
therefore the skuli, as well as (b) the consequence of inserting the adductors more
anteriorly. Reduction in the portion of the skull available to house the olfactory
organs would be a consequence of a shorter preorbital region.
A feature so far not described in detail is C5, the lateral bowing and dorsal
emargination of the lower border of the zygoma. These features are typical of the
dicynodont skull, although present to a lesser degree in Eodicynodon and only
incipiently in Venjukoviu. These features, together with the anterior extension of
the temporal fenestra, are necessary to allow the AEM to pass underneath the
EVOLUTION OF DICYNODONT FEEDING
207
zygoma and insert further anteriorly on the lower jaw. It also permits the AEL
to attach more laterally; the importance of this was mentioned above (page 203)
and will be emphasized below (P3).
Guidance of the lower j a w (P3)
Certain features of the skull which could have been consequences of other
requirements, e.g. the need to position the adductors more anteriorly and to
lengthen the pterygoideus muscles, have already been mentioned as having a
bearing on the requirement for guidance of the lower jaw. Such guidance is
necessary to enable the lower jaw to move backwards and forwards without
colliding with other skull structures.
Eodicynodon, in comparison with later dicynodonts, has a relatively high skull,
the temporal fenestra is relatively short, and the zygoma not as expanded
posteriorly. Lowering of the skull roof and elongation of the temporal fenestra (in
dicynodonts post Eodicynodon) would increase the back-pull of the AEM (as
discussed on page 202). In turn, elongation of the temporal fenestra would also
increase the length and the backward-pulling component of the AEL, while
lateral bowing of the zygoma would place the origin of the muscle more
laterally. This last feature would give the muscles greater control over possible
transverse movement of the lower jaw during propaliny. This becomes very
advantageous in the light of what is happening to the pterygoideus muscle as
described on page 203.
THE IMPORTANCE OF PROPALINY
Having adopted an explanation for the development of the adaptive complex
which we have been discussing, it is interesting to try to put this explanation into
a broader context and attempt to work out the importance of propaliny to the
rest of the animal’s organization.
Relative movement of the jaws, together with appropriate contact areas, will
enable an animal to process food more effectively: food may be cut, shredded or
ground into fine pieces enabling more nutrition to be obtained from it and/or
nutrition to be obtained more quickly. These abilities could be at a premium if
the animal in question has a high metabolic rate or if food is in short supply, or
both.
There is no convincing evidence that dicynodonts had a high metabolic rate
or elevated body temperature. Evidence of such characters cannot, obviously, be
found directly in fossil animals. Therefore, one must look for fossilizable features
(or those that may be inferred from fossil information) which could correlate
with endothermy, i.e. an elevated body temperature linked with a high
metabolic rate. Various authors have suggested the following correlates.
1. Presence of a diaphragm indicated by loss of lumbar ribs and strengthening
of thoracic ribs (Brink, 1956; Parrington, 1967; Geist, 1971).
2. Elaboration of the dentition to permit extensive preparation of food (Brink,
1956; Parrington, 1967 inter alia).
3. Presence of a secondary palate to permit simultaneous eating and breathing
(Brink, 1956; Parrington, 1967).
4. Presence of turbinal bones to permit ccmoisteningand cleaning [of] the air
208
G . M. KING ET AL.
as it was breathed”, linked with a more ‘‘developedYY
respiration (Parrington,
1967).
5. ’Pitted snout surface inferring presence of vibrissae and therefore hair
(Brink, 1965; Parrington, 1976).
6. More complex brain related to agility and increased activity (Hopson,
1980; Parrington, 1967).
7. Mammal-like locomotion, upright stance indicative of sustained locomotion
(Parrington, 1967; Ostrom, 1980).
8. Bone histology comparable to that of present-day endotherms (Ricqlks,
1974, 1976).
9. High blood pressure and rapid circulation (Ostrom, 1980).
10. Low predator-prey ratios (Bakker, 1975; Ostrom, 1980).
1 1. Group behaviour (Ostrom, 1980).
12. Geographical distribution (Ostrom, 1980).
These characters may be applied to dicynodonts. There is no evidence for
characters 1, 4, 6 and 9 in dicynodonts. Characters 2, 5 and 10 are not
applicable to dicynodonts: a dentition is not present (usually), the snout was
covered with horn, and a predator-prey ratio cannot be calculated for an
exclusively herbivorous group. Character 3 is present but can also be interpreted
as a device for strengthening the skull (Thomason & Russell, 1986). Characters
11 and 12 have not been adequately investigated in dicynodonts. (Character 11
may be present in dicynodonts (Bandyopadhyay, 1988) but loose herding
behaviour is not confined to endotherms anyway.)
This leaves characters 7 and 8 which are both applicable to dicynodonts and
are exhibited by them. As far as 7 is concerned McNab (1978) and Ricqlb
(1980) have argued that improved gait and sustained activity could be
correlated with large size and/or inertial homeothermy. Similarly McNab argues
that character 8: ‘endothermy-like bone might also reflect inertial
homeothermy. In discussing dinosaurs, Ricqlb (1980) suggests that even if they
were endothermic their metabolic rates were not as high as those of large living
endotherms, and he prefers to describe large dinosaurs as developing a thermal
physiology that was “uniquely their own”, enjoying “at the very least incipient
endothermy coupled with passive homoiothermy”. His arguments do not apply
to small dinosaurs, less than 30-40 kg, however, where he feels that evidence of
high levels of metabolic activity (viz. bone histology) “must have some other
physiological basis”. In other words a reasonable explanation for a ‘mammalian’
type bone histological pattern occurring in these smaller forms would be that
they were endothermic. Most dicynodonts would fall into this latter size
category. Dicynodont bone histology displays a laminar or plexiform pattern,
which on the above basis should be seen as indicating an endothermic regime
(Ricqlb, 1976).
It seems reasonable to conclude at present that all of the characters which
typify mammalian endothermy had not yet arisen: dicynodonts were not fully
endothermic, but might have occupied some kind of intermediate metabolic
position with a slightly higher body temperature. In this context any mechanism
which enabled the animal to obtain more nutrition per unit food eaten, or per
unit time taken preparing food, would be an advantage.
It is almost universally agreed that dicynodonts were herbivorous animals, if
only because of their vast abundance as fossils compared to other forms found in
EVOLUTION O F DICYNODONT FEEDING
209
the same localities. Even the rare exceptions to this agreement (e.g. King, 1981b;
Cox, 1959) usually postulate some kind of omnivorous diet which included plant
matter. In order to examine the suggestion that food for dicynodonts might have
been scarce, leading to a premium being put on more efficient food processing,
we should need to have detailed knowledge not only of the plant life of the
Permian palaeoenvironment, but also of possible competitors for the food which
it represented. At present we do not have such information.
CONCLUSION
It can be seen that due to the adoption of herbivory and the need to process
food more effectively, dicynodont morphology was modified in order to produce
a very efficient masticatory system. This system was already well on its way in
early dicynodonts such as Venjukovia. The slightly later form Eodicynodon showed
some refinements of the early condition and by the time the major Permian
forms such as Oudenodon and Diictodon had evolved, all the characteristic features
of the masticatory system were present. Further adaptive radiation took place in
the feeding system but compared to the modifications which occurred between
pelycosaurs and the earliest dicynodonts these were merely variations on a
theme.
ACKNOWLEDGEMENTS
We would like to thank Tom Kemp (University Museum, Oxford) for
extensive reading and improvement of this paper and Denise Blagden for her
help with illustrations. Diana Fourie, Zubi Gregorowski, John Nyaphuli, Riana
Slaughter and Burkard von Schlichting prepared specimens of Eodicynodon and
we are grateful to them. The C.S.I.R. and National Museum, Bloemfontein
provided funding which enabled fieldwork to collect Eodicynodon to take place.
Mike Cluver (South African Museum, Cape Town) supplied many ideas,
incentive and encouragement for the work and, as always, we are indebted to
him for his time and support.
REFERENCES
ADAMS, L. A,, 1919. A memoir on the phylogeny of the jaw muscles in recent and fossil vertebrates. Annals of
the New rork Academy of Sciences, 28: 51-166.
BAKKER, R. T., 1975. Experimental and fossil evidence for the evolution of tetrapod bioenergetics. In D. M.
Gates & R . B. Schmerl (Eds), Perspectives of Biophysical Ecology: 365-399. New York: Springer-Verlag.
BANDYOPADHYAY, S., 1988. A kannemeyeriid dicynodont from the Middle Triassic Yerrapalli Formation.
Philosophical Transactions of the Royal Society, Series B, 320: 185-233.
BARGHUSEN, H. R., 1973. The adductor jaw musculature of Dimetrodon (Reptilia: Pelycosauria). Journal of
Paleontology, 47: 823434.
BARGHUSEN, H. R., 1976. Notes on the adductor jaw musculature of Venjukovia, a primitive anomodont
therapsid from the Permian of the U.S.S.R. Annals of the South African Museum, 69: 249-260.
BARRY, T. H., 1972. Terrestrial vertebrate fossils from Ecca-defined beds in South Africa. In S. H. Haughton
(Ed.), Proceedings and Papers of the Second Iniernational Union of Geological Sciences Gondwana Symposium: 653-659.
Pretoria, South Africa: CSIR.
BARRY, T. H., 1974a. Affinities and systematic position of the South African Lower Middle Permian
Dicynodonts (Therapsida: Dicynodontidae). In K. S. W. Campbell (Ed.), Proceedings and Papers from the
Third Gondwana Symposium: 475-479. Canberra, Australia: Australian National University Press.
BARRY, T. H., 1974b. A new dicynodont ancestor from the Upper Ecca (Lower Middle Permian) of South
Africa. Annals of the South African Museum, 64: 117-136.
210
G. M. KING E T A L .
BRINK, A. S., 1956.Advanced mammalian characteristics in the higher mammal-like reptiles. Palueontologia
Africana, 4: 77-95.
CLUVER, M. A., 1970. The palate and mandible in some specimens of Dicynodon testudirostris Broom &
Haughton (Reptilia, Therapsida). Annals of the South African Museum, 56: 133-153.
CLUVER, M. A., 1971.The cranial morphology of the dicynodont genus Lystrosaurus. Annals of the South African
Museum, 56: 155-274.
CLUVER, M. A., 1974a.The cranial morphology of the Lower Triassic dicynodont Myosauruc gracilis. Annuls
of the South African Museum, 66: 35-54.
CLUVER, M. A., 1974b.The skull and mandible of a new cistecephalid dicynodont. Annals of the South African
Museum, 64: 137-156.
CLUVER, M. A., 1975. A new dicynodont reptile from the Tafinocephalus zone (Karoo System, Beaufort
Series) of South M i c a , with evidence of the jaw adductor musculature. Annals of the South African Muscum,
67: 7-23.
CLUVER, M. A. & HOTTON, N. III., 1981.The genera Dicynodon and Diictodon and their bearing on the
classification of the Dicynodontia (Reptilia, Therapsida). Annals of the South African Museum, 83: 9S146.
CLUVER, M. A. & KING, G. M., 1983. A reassessment of the relationships of Permian Dicynodontia
(Reptilia, Therapsida) and a new classification of dicynodonts. Annals of the South African Museum, 91: 195273.
COX, C. B., 1959.O n th2 anatomy of a new dicynodont genus with evidence of the position of the tympanum.
Proceedings of the Joological Socieg of London, 132: 321-367.
CROMPTON, A. W. & HOTTON, N. III., 1967. Functional morphology of the masticatory apparatus of
two dicynodonts (Reptilia, Therapsida). Postilla, 109: 1-51.
DEMAR, R. & BARGHUSEN, H. R., 1972.Mechanics and evolution of the synapsid jaw. Evolution, 26: 622637.
EWER, R. F., 1961. The anatomy of the anomodont Daptocephalus leoniceps (Owen). Proceedings of the Joological
Society of London, 136: 375-402.
FRAZETTA, T. H., 1968.Adaptive problems and possibilities in the temporal fenestration of tetrapod skulls.
Journal of Morphology, 125: 145-157.
GEIST, V., 1971. An ecological and behavioural explanation of mammalian characteristics, and their
implication to therapsid evolution. Jeitschriit f u r Siiugetierkunde, 37: 1-1 5.
HAAS, G., 1973. Muscles of the jaws and associated structures in the Rhynchocephalia and Squamata. In
C. Gans & T. S. Parsons (Eds), Biology of the Reptilia, 4: 285-490. New York Academic Press.
HOPSON, J. A., 1980. Relative brain size in dinosaurs: implications for dinosaurian endothermy. In R. D. K.
Thomas & E. C. Olson (Eds), A Cold Look at the Warm-Blooded Dinosaurs. Amm'can Association f o r the
Advancement of Science Selec&d Symposium, 28: 287-3 10.Boulder, Colorado: Westview Press.
HOPSON, J. A. & BARGHUSEN, H. R., 1986. An analysis of therapsid relationships. In N. Hotton, P. D.
MacLean, J. J. Roth & E. C. Roth (Eds), The Ecology and Biology of Mammal-Like Reptiles: 83-106.
Washington: Smithsonian Institution Press.
KEMP, T . S., 1982.Mammal-like Reptiles and the Origin of Mammals. London: Academic Press.
KING, G. M., 1979. Permian dicynodonts from Jambia. Unpublished D. Phil. Thesis. University of Oxford,
England.
KING, G. M., 1981a. The functional anatomy of a Permian dicynodont. Philosophical Transactions of the Royal
Society, Series B, 291: 243-322.
KING, G. M., 1981b. The postcranial skeleton of Robertia broominnu, an early dicynodont (Reptilia,
Therapsida) from the South African Karoo. Annals of the South African Museum, 84: 203-321.
KING, G. M., 1986.Distribution and diversity of dicynodonts: an introductory approach. Modern Geology, 10:
10% 120.
KING, G. M., 1988. Anomodontia. Handbuch der Paliioherpetologie, 17C: 1-174. Stuttgart: Gustav-Fischer
Verlag.
LAKJER, T., 1926.Studien uber die trigeminus-versogtekaumuskulatur der sauropsiden. Copenhagen: C. A. Ritzel.
MCNAB, B. K., 1978. The evolution of endothermy in the phylogeny of mammals. American Naturalist, 112:
1-21.
NORMAN, D. B. & WEISHAMPEL, D. B., 1985. Ornithopod feeding mechanisms: their bearing on the
evolution of herbivory. American Naturalist, 126: 151-164.
OSTROM, J. H., 1980.The evidence for endothermy in dinosaurs. In R. D. K. Thomas & E. C. Olson (Eds),
A Cold Look at the Warm-Blooded Dinosaurs. American Associationf o r the Advancement of Science Selected Symposium,
28: 15-54. Boulder, Colorado: Westview Press.
PADIAN, K., 1986.A comparative phylogenetic and functional approach to the origin of vertebrate flight. In
M. B. Fenton, P. Racey & J. M. V. Raynor (Eds), Recent Advances in the Study of Bats. Cambridge:
Cambridge University Press.
PARRINGTON, F. R., 1967.The origins of mammals. Advancemenf of Science, 1967: 165-173.
RICQLES, A. J. DE, 1974. Evolution of endothermy: histological evidence. Evolutionary Theory, I: 51-80.
RICQLES, A. J. DE, 1976.O n bone histology of fossil and living reptiles, with comments on its functional and
evolutionary significance. In A. d'A. Bellairs & C. Barry Cox (Eds), Morfihology and Biology of Reptiles.
Linnean Socieg Symposium Series, 3: 123-150. London: Academic Press.
EVOLUTION O F DICYNODONT FEEDING
21 1
RICQLES, A. J. DE, 1980. Tissue structures of dinosaur bone. Functional significance and possible relation to
dinosaur physiology. In R. D. K. Thomas & E. C. Olson (Eds), A Cold Look at the Warm-Blooded Dinosaurs.
American Association for the Advancement of Science Selected Symposium, 28: 103-140. Boulder, Colorado: Westview
Press.
RUBIDGE, B. S., 1984. The cranial morphology and palaeoenvironment of Eodicyodon oosthuizmi Barry
(Therapsida: Dicynodontia). Nauorsinge uan die Nasionale Museum Bloemfontein, 4: 327-402.
RUBIDGE, B. S., 1985. The first record of a complete snout of the primitive dicynodont Eodicynodon oosthuizmi,
Barry 1974 (Therapsida: Dicynodontia). Nauorsinge van die Nasionale Museum Bloemfontein, 4: 501-512.
SCHUMACHER, G.-H., 1973. The head muscles and hyolaryngeal skeleton of turtles and crocodylians. In
C. Gans 81 T. S. Parsons (Eds), Biology ofthe Reptilia, 4: 101-109. New York: Academic Press.
SIGOGNEAU, D. & TCHUDINOV, P. K., 1972. Reflections on some Russian eotheriodonts. Palaeouertebrata,
5: 79-109.
THOMASON, J. J. & RUSSEL, A. P., 1986. Mechanical factors in the evolution of the mammalian palate: a
theoretical analysis. Journal of Morphology, 189: 199-213.
WATSON, D. M. S.,1948. Dicyodon and its allies. Proceedings of the <oological Society of London, 118: 823477.