J . Linn. Soc. ( Z o o l . ) ,46, 310,p. 223
With 17 jigures
Printed in Great Britoin
April, 1967
Mechanisms of intracranial kinetics in fossil rhipidistian
fishes (Crossopterygii) and their relatives
BY KEITH STEWART THOMSON, F.L.S.
Department of Biology and Peabody Mupeum of Natural History,
Yale University
(Acceptedfor publiccction April 1966)
The fishes of t’he Order Crossopterygii arc characterized by a unique articulation within the
braincase, by which the anterior division of the endocranium may be moved dorso-ventrally
with respect t o the posterior division. The st.ructure of the skull in both groups of crossopterygian fishes (the fossil Rhipidistia and the fossil and Recent Coelacanthini) is such that
‘normal ’ operation of the intracranial mc.chanisni involves lateral movements of the cheek
region and palate corresponding t o the dorso-vent,ralmovements of the ethmoid portion of the
braincase. The hyomandibular has a function of prime importance in integrating the movcinents of the various skull components relative to each other. There are important differences
hetween the characteristic intracranial mechanisms of Rhipidistia and Coelacanthini which
may be interpreted in adaptive as well as morphological terms. Analysis of the intracranial
kinetics of the Rhipidistia rcveals a trend, in certain lines, for the amount of relative movement between the skull components to be tlrcrpased and this may be used to explain the loss of
t,he intracranial joint in t,he Amphibia during their evolution from the Rhipidistia. The
functional significance of the intracranial articulation has both a kinetic and a dynamic aspect
and while in the Arnphibia the kinetic ability of the skull is almost wholly restricted, the
dynamic features of the ancestral condition arc modified and developed as the basal articulation
between the palate and endocranium is retained.
INTHODUCTION
The fishes of the Subclass Sarcoptervgii (Ronier, 1955) comprise three groups-the
Dipnoi (fossil and Recent lungfishes), the Coelacanthini (including the Recent Latimeria)
and the Rhipidistia (the group of Palaeozoic fossil fishes from which the Amphibia arose).
The Rhipidistia and Coelacanthini together form the Crossopterygii.
The skull of dipnoan fishes, from Devonian to Recent times, is invariably autostylic (see
discussion of Diphorhynchus in the final section of this paper).The skull of Rhipidistia and
Coelacanthini, on the other hand, is a kinetic amphistylic structure with the palatoquadrate movably articulated on the braincase and the hyomandibular forming a principal
part of the suspensorium. This basically primitive arrangement of the skull is common
among the early vertebrates. However a unique feature of the rhipidistian and coelacanth
skull is the presence of a joint within the braincase itself. The joint, separates the
endocranium into two distinct moieties-anterior and posterior-and is situated immediately anterior of the prefacial commissure of the lateral endocranial wall. The aim of
this paper is t o examine the structural relationships of the skull in rhipidistian and
coelacanth crossopterygjans and to investigate the mode of action and functions of this
unusual intracraniai articulation. The rhipidistian skull is considered in greater detail, the
coelacanth skull being considered separately in view of the fact that in both anatomy and
function it differs somewhat from that of Rhipidistia.
* Formerly : Department of Zoology, University
College London.
224
KEITHSTEWART
THOMSON,
F.L.S.
Most workers (e.g. Watson, 1926; Versluys, 1927 ; Aldinger, 1930, 1931 ; Holmgren &
Stensio, 1936; Romer, 1937; Moy-Thomas, 1939; Hofer, 1945; Lehman & Westoll, 1952;
Schaeffer, 1953,1965) agree that operation of the intracranial articulation involved movement of the two divisions of the endocranium relative to each other, together with corresponding movements of the palate relative to the braincase. Jarvik (1937 and following
papers), however, has drawn attention to the fact that several specimens of Rhipidistia
exist in which there is evidence of fusion of the palate to the endocranium in front of and
behind the intracranial joint, or in which the pattern of the dermal bones of the skull roof
is modified in such a way as to prevent articulation. These specimens, as Jarvik demonstrates, were clearly unable to make movements of the two divisions of the endocranium
relative to each other or to the palate. However, it must be noted that, nonetheless, the
intracranial joint is present and the only indications of fusion of the separate elements of
the skull occur as modifications of what have clearly once been articular surfaces. This
strongly suggests that, the loss of articulation in these specimens is a secondary phenomenon resulting from age, trauma or some other non-adaptive cause. The importance of
Jarvik‘s observations is in demonstrating that whatever the normal function of the kinetic
ability of the skull may be, certain individuals may have been perfectly viable after loss of
this faculty.
I n this study it is taken as a first principle that a structure as clearly defined and complicated as the intracranial joint, which is known to have persisted for a t least 300 million
years (in coelacanths) must have a function of clear adaptive value. The problem of elucidating its particular significance is made all the more challenging by the evidence, noted
above, that this kinetic ability may occasionally be lost.
The most widely accepted interpretation of the function of the intracranial articulation
has been the suggestion (Watson, Romer, Moy-Thomas) that movement of the anterior
division of the skull relative to the rest of the skull during occlusion of the powerful lower
jaws acted as a shock-absorbing mechanism. Certainly the shock produced by the mandibles in such predacious fishes as the Rhipidistia may have been considerable, but the
results of this study show that the actual intracranial kinesis in Rhipidistia would have
added little to the efficiency of the skull in absorbing such a shock. Schmalhausen (1960,
quoted by Szarski, 1963) suggested that when the jaws were closed gentle flexure of the
anterior section of the skull would, by causing slight changes in the volume of the oral
cavity, produce a passage of water through the nasal cavity and that such ‘sniffing’movements would be almost imperceptible to potential prey whose presence was being thus
investigated. This theory is also implausible, especially in view of the fact that a similar
effect could be produced by simple movements of the mobile operculum or gular apparatus,
and, of course, the coelacanths have no internal naris.
The first part of this paper consists of a concise description of the various components of
the rhipidistian skull and of the articulations between them. I n the second section the
possible movements of the skull during operation of the intracranial articulation are
analysed and their functional and adaptive significance is examined. I n the third section
the coelacanths are briefly considered and finally the phylogenetic implications of the
study are discussed.
MATERIAL
The material upon which my studies have been based comes principally from three
sources-the Museum of Comparative Zoology a t Harvard University, the British Museum
(Natural History) and the Royal Scottish Museum. The extensive collection of specimens
of the Lower Permian osteolepid rhipidistian Ectosteorhachis a t the Museum of Comparative Zoology, includes the material which formed the basis of Romer’s original descriptions
of the rhipidistian endocranium (1937) and hyomandibular (1941),see also Eaton (1939).
This suite of specimens has the great advantage for detailed anatomical studies that in
Intracranzal kiiirtics in Crossopterygii
225
addition t o sectioned material, several specimens are available preserved ‘in the round’ on
which every detail of muscle scars, cranial nerve foramina, etc. is easily visible. The
dermal skull roof and nasal anatomy of Ectosteorhachis have been described previously
(Thornson, 1962. 1964a, b ) and in the folloning pages further new anatomical information is recorded.
I have also been able to use Professor Watson’s material of OsteoEepis which, together
with material from the British Museum (Natural History) and the Royal ScottishMuseum,
formed the basis of a recent description of the endoskeleton of this form (Thornson, 1965a).
Professor Jarvilr’s fine descriptions of the Upper Devonian rhizodontid rhipidistian
Eusthenopteroi~foordi and other forms (1937, 1942, 1944, 1948, 1954) have of course been
widcly consulted and referred t o during the course of this work.
THE RIIIPIDISTIAN SKULL
In this section a concise description is given of the structure of the various component
units of the rhipidistian skull-namely thc braincase, palato-quadrate complex, hyomandibular and dermal skull bones. The description is based primarily upon the structure
of Ectosteorhachis and incorporates some new details of information about this form with
original figures. Special mention is made when the structure of other Rhipidistia differs
significantly from that of Ectosteorhachis.
The a7iferior bruincase
The braincase is of significance to our studies in two main respects-as a region of
skeletal support and attachment of the structures of the sliull and as a protective enclosure
around the brain. Both of these functions directly affect the general shape and proportions
of the braincase.
In all Rhipidistia so far described the intraeranial joint is situated a t the level of the
separation of the mesencephalic and metencephalic regions of the brain (cf. Stensio, 1963 ;
Thornson, 1965a, b ). The anterior division of the braincase thus contains the olfactory
apparatus, olfactory hemispheres, the thalamic structures, and tectum and the dorsum
sellae.
Ot
v. p.
i.c.
hyfy
VII
‘ I
tf.
M
Fig. 1. Eetosteorhmhis nitidm. Left lateral view of endocranium.
bpt., Basipterygoid process; em., external naris; f.B., fossa Bridgei; f.f., facial foramen
(posterior opening of jugular canal) ; hy. f., facets for hyomandibular articulation; I.c., lateral
commissure; n.c., nasal capsule; sp.gr., groove for spiracular diverticulum; s.s.o., notch for
spiracular sense organ.
i.c., (position of) internal carotoid art,ery; v.P., pituitary vein; mni. V., pf. V, (foramina for)
maxillary-mandibular and profundus rami of fift,h cranial nerve; 0s. VII, ot. VII, pal. VII,
ophthalmicus superficialis, oticus and palatine rami of seventh cranial nerve; 11,IX, X, XII,
optic, ninth, tenth and twelfth cranial nerves.
i5
226
KEITHSTEWART
THOMSON,
F.L.S.
.pm
Fig. 2. Eetosteorhachis nitidus. Skull in (A) dorsal view and ( B )left lateral view.
e.n., Externalnaris; it., intertemporal; ju., jugal; l., lachrymal; l.e., lateral extrascapular;
m.e., median extrascapular ;mx., maxilla; op., operculum ; p., parietal ;pm., premaxilla ;PO.,
postorbital; pop., preopercular; pp., postparietal; q-j., quadrato-jugal; sop., subopercular;
sp., spiracle; sq., squamosal; st., supratemporal; t., tabular.
Intracranial Einet ics in Crossopterygii
"7
Behind the nasal capsule the side walls of the anterior endocranium (Fig. 1) enclose
foramina for the passage of cranial nerves 11,111, IV in addition to foramina for the vena
cerebralis anterior, pituitary vein, internal carotoid and possibly others.
A prominent basipterygoid process is situated on either side of the postero-ventral part
of the braincase wall. The curved articular surface of this process faces almost directly
forwards. Above the basipterygoid process there is a slight groove along which passed the
anterior continuation of the jugular vein (vena capitis lateralis). From the anterior portion
of the basipterygoid process to the orbito-nasal wall extends a slight ridge of the lateral
endocranial wall and beneath this is a pronounced excavation of the wall into which fits
the medial margin of the palato-quadrate. In most genera (including Eusthenqteron,
Megalichthys and Ectosteorhachis) the recess ends anteriorly as a deep notch between the
curved orbito-nasal wall and the median internasal wall (see Jarvik, 1942, Fig. 5 5 ) . I n
Osteolepis, and possibly other genera, this notch is lacking (Thomson, 1965a).
In Eusthenopteron , as Jarvik has described, there is evidence of an articular surface high
on the posterolateral surface of the anterior endocranium indicating an additional point
of contact between the palato-quadrate and the endocranium. This has not been described
in other rhipidistians and can be stated definitely to be lacking in the available material of
Ectosteorhachis and Rhizodopsis. (It has been pointed out above that the specimens
discussed by Jarvik may have lost, traumatically, the power of articulation of the intracranial joint and the apparent synchondrosis in this region is possibly therefore atypical.)
On to the ventral surface of the anterior endocranium are attached the median dermal
parasphenoid (usually completely fused) and the paired vomers. The dorsal surface of the
endocranium is fused to the overlying dermal bones of the skull roof, parietals, rostrals,
nasals, tectals and the supraorbital and interteniporal (Fig. 2 ) . The dorsal surface of the
endocranium is pierced by a foramen for the parietal and/or pineal organs, which open to
the surface between the parietal bones (in many genera such as Megalichthys, Ectosteorhuchis and all Porolepidae and Holoptychidae this dermal opening is not present). The
tip of the notochord fitted into a large circular facet on the postero-ventral margin of the
anterior endocranium.
V
1
-
pf.V
c
bpt.
D
Fig. 3. Intracranial joint region of four Rhipidistia in left lateral view. A, Rl~koClop8issuurodes. B, Osteolepis mawolepidotus. C , Ectosteorhuchis nitidus. D , Eusthenopteron joordi (after
Jarvik, 1954).
bpt., Basipterygoid process; d.f., dorsal flange of endocranial wall; mm. V, pf. V, foramina
for maxillary-mandibular and profundus rami of fifth cranial nerve ; 0s. VII, ophthalmicus
superficialis ramus of seventh cranial nerve ; V, combined rami of fifth cranial nerve.
-9.38
KEITHSTEWART
THOMSOK,
F.L.S.
Various markings on the outer surface of the side wall of the anterior endocranium in the
region of the opening of the optic nerve indicate the sites of insertion of the eye muscles.
The ventro-lateral surfaces of the endocranium immediately posterior t o the foramen for
the internal carotid artery show similar markings which indicate the insertion of the subcephalic muscles passing forwards from the posterior division of the braincase (Fig. 6 , see
below).
The actual articular surfaces on the rear margin of the anterior endocranium differ in the
various genera. I n Ectosteorhachis (and most probably in Osteolepis also) where the profundus V nerve leaves the endocranial cavity through the intracranial joint, the articular
region is arranged as in Fig. 3, with two separate sets of articular surfaces, the dorsal pair
resemble ball and cup joints and the ventral pair fit into facets on the inner surface of the
corresponding portion of the posterior braincase-the anterior margins of the otic shelves
(see below). I n Eustlienopteron and Rhizodopsis (where the profundus nerve foramen is
situated in the prefacial region) the articular region is arranged as in Fig. 3. Essentially
there is a single articular surface with no lateral overlapping. The shape of the two articulating surfaces, facing backwards and forwards in Eusthenopteron, however, is such that on
each side two posterior extensions of the anterior braincase fit into two excavations of the
posterior section. Obviously, the configuration of these surfaces is of importance in respect
to the nature of the movements made a t the intracranial joint.
Posterior division of the braincase
The posterior division of the braincase houses the principal parts of the brain, the metencephalon and myelencephalon, and the organs of the ear. A spiracular sense organ lay
close against the side of the braincase in the region of the spiracle and spiracular diverticulum (Figs 1 and 4). The large notochord is enclosed in a bony canal lying underneath
and distinct from the neural cavity.
The posterior division of the braincase itself is made up anteriorly of an otic shelf on each
side, partially enclosing the lateral head vein, and a prefacial commissure which may
become more or less completely unified with the anterior wall of the otic capsule. Through
and between these structures open the foramina for various branches of the fifth and
seventh cranial nerves and also the vena cerebralis medialis-this latter opening rather
more anteriorly in the osteolepids Ectosteorhachis and Osteolepis than in the rhizodontids
Eusthenopteron and Rhizidopsis (see Thomson, 1 9 6 5 ~ )Across
.
the side of the otic capsule,
enclosing the lateral head vein and the facial foramen, is situated the lateral commissure,
which is formed by the merging of the otic shelf with a dorsal parotic process. The lateral
commissure/parotic process region bears two facets for the articulation of the hyomandibular, a dorsal facet (on the parotic process) which in Ectosteorhachis and Osteolepis faces
more or less laterally and in Eusthenopteron faces posterolaterally, and a ventral facet, just
below the level of the jugular vein, which invariably faces posterolaterally. Immediately
posterior to the ventral hyomandibular facet is situated the ventral articular facet of the
first branchial arch. The parotic process buttresses the otic capsule dorsally against the
dermal skull roof in the region of the suture between the supratemporal and tabular bones.
Behind this the posterior corner of the tabular is buttressed by a second process-the
paroccipital process (which is modified in Ectosteorhachis and Rhizodopsis,but is present in
Osteolepis and Eusthenopteron, see Thomson, 1 9 6 5 ~ )The
. paroccipital process also forms
the lateral wall of a large cavity overlying the posterior half of the otic capsule and widely
open posteriorly. Into this cavity, the fossa Bridgei, are inserted the portions of the axial
musculature which are responsible for movements of the head upon the trunk. I n most
cases the fossa Bridgei is in communication with the prefacial region by means of two narrow canals, one of which is probably homologous with the canal for the vena capitis
dorsalis in tetrapods. I n Osteolepis (see Thomson, 1 9 6 5 ~there
)
is a notch separating the
parotic and paroccipital processes where a slip of muscle may have arisen. The ventral part
Intracranial kinetics i n C'rossopterygii
229
of the posterior wall of the otic capsule is marked by a groove for the lateral head vein and
a t the posterior limit of this groove are situated the foramina for the ninth and tenth
cranial nerves. I n this region also is situated the small postotic process on t o which, in all
probability, articulated the dorsal head of the first branchial arch.
Several scars for the insertion of muscles may be observed in the surface of the posterior
endocranium. Principal among these is the large set of scars on the ventral surface of the
notochordal canal which indicate the position of insertion of the subcephalic muscles
which passed forwards t o the postero-ventral portion of the anterior endocranium. The
extremely close resemblance between these muscle scars and the arrangement of the subcephalic muscles in Coelacanthini (see below) enables us to restore these muscles with
considerable confidence. On to the posterior wall of the otic capsule were inserted, in all
probability, the adductor hyoidens, the protractor muscles of the first branchial arch and
also a protractor and an adductor opercularis (cf. Thomson, 1965a).Antero-medial to the
position of the spiracular sense organ and dorsal to the fifth and seventh cranial nerve
foramina is the site of the insertion of the levator arcus palatini (Fig. 4) which passed
directly forwards to insert upon the upper margin of the palato-quadrate just anterior t o '
the intracranial articulation. Corroboration of the position of all these muscles is provided
by the anatomy of the living coelacanth Latimeria (see Millot & Anthony, 1958). A further
corroboration of the site of insertion of the levator arcus palatini is afforded, I believe, by
the unusual morphology of this region in Eusthenopteron. As shown in Jarvik's description
(1954) the dorso-lateral margin of the braincase in this region in Eusthenopteron is expanded into a fenestrated dorsal flange (see Fig. 3). I have been puzzled for some time by
this curious structure but now believe that this is a simple example of a common osteological phenomenon whereby, in many animals, the region of an important muscle insertion
is expanded and fenestrated. A protractor hyoideus was probably closely associated with
the levator arcus palatini.
The palato-quadrate complex
The palate in Rhipidistia is completely closed and the adductor mandibulae musculature inserted solely on the palate, no portion of it attaching to the braincase. The rhipidistian palato-quadrate has been most fully described in Megalichthys (Watson, 1926) and
Eusthenopteron (Jarvik, 1954). The general arrangement of the various portions of the
single palato-quadrate ossification is the same in all genera as far as I have been able t o
ascertain. One point of difference lies in the structure of the anterior tip of the complex. I n
Ewthenopteron (Jarvik, 1937, 1942), Mrgnlichthys (Thomson, 1964a ; Watson, 1926),
Ectosteorhachis (Thomson, 1964a) and doubtless other genera, there is a distinct pars autopalatina which fits into the notch between the orbito-nasal wall and the side wall of the
braincase mentioned earlier. I n Osteolepis (Thomson, 1965a)and at least one other Devonian osteolepid-Gyroptychius (cf. Thornson, 19656) this notch is lacking and obviously a
pars autopalatina is also absent. There is thus a difference in the manner of attachment of
the anterior portion of the palatal complex to the endocranium. This difference is emphasized by the fact that in certain of the genera where the pars autopalatina is present there
may actually be a tendency towards fusion of the palate and endocraniiim a t this point (see
Thomson, 1964b.1965a for discussion).
I n Ectosteorhachis (original), Negalichthys (Watson, 1926), Ewthenopteron (Jarvik,
1954) and probably all Rhipidistia, the palato-quadrate bears a deep notch in the region of
the adjacent intracranial articulation (Fig. 4) which obviously served for the passage of
branches of the fifth and seventh nerves into the orbital cavity. Immediately anterior to
this notch the palate is developed into a dorsal flange ('processus ascentlens ') on t o which
the levator arcus palatine muscles must have attached. Posterior to the notch there is also
a slight extension of the dorsal margin of the palate (' processus oticus') where it lies against
the outer surface of the otic shelf of the posterior endocranium.
230
KEITHSTEWART
THOMSON,
F.L.S.
Fig. 4. Eclosteorhachis nitidus. Left lateral view of skull with dermal bones removed and
including restorations of various nerves, vessels and muscles.
ad.hy., (facet for) Adductor hyomandibularis ; ad.op., adductor opercularis ; ax.mm., axial
musculature; l.a.p., levator arcus palatini; I.b., levatores hranchiales; a.m., (restoration of)
adductores mandibulae.
jug., Jugular vein; hy. VII, m. VII, 0s. VII, ot. V I I , hyoideus, mandibular, ophthalmicus
superficialis, and oticus rami of seventh cranial nerve; l.p., posterior lateralis nerve; mm.V,
pf. V, maxillary-mandibular and profundus rami of fifthcranialnerve ;11, X, X I I , optic, tenth,
and twelfth cranial nerves; p.q., palato-quadrate; sp.d., apiracular diverticulum.
Jarvik (1954) has reconstructed the palate of Eusthenopteron as having had an open
spiracular cleft connecting the mouth cavity to the surface of theskullviaapassage between
the postero-dorsal margin of the palato-quadrate and the anterior surface of the hyomandibular. Associated with the spiracular cleft were a spiracular sense organ and a lateral
diverticulum which (as first noted by Romer, 1937, in Ectosteorhachis) leaves a noticeable
groove on the anterior surface of the parotic process (Fig. 1).
The ventro-medial margin of the palatal complex fits into the lateral excavation of the
anterior endocranium from the level of the postnasal wall to the basipterygoid process.
The quadrate region of the palato-quadrate is greatly thickened to form the facet for the
articulation of the mandible. The postero-mesial surface of the posterior margin of the
palate bears a shallow groove where the hyomandibular fitted against it; this groove is
especially prominent on the posterior surface of the quadrate region where the hyomandibular seems t o have participated directly in the formation of the suspensorium.
The hyommlzdibular
The rhipidistian hyomandibular is a large elongate, curved or slightly angled, rodshaped structure. Descriptions of the hyomandibular have already been given for the
following genera Ectosteorhachis (Romer, 1941), Eusthenopteron (Westoll, 1943a ; Jarvik,
1954) and Osteolepis (Thomson, 1965a, q.v. for comparisons). Special mention may be
made here of the following points.
The proximal articulation of the hyomandibular is by means of two separate heads,
fitting into appropriate facets on the parotic process lateral commissure region of the
posterior endocranium. It has been noted above that in some genera the dorsal endocranial facet is directed more laterally than in others. I n these forms (Ectosteorhachis,
Osteolepis) the dorsal head of the hyomandibular is offset medially rather than occupying a
terminal position as does the dorsal head in other forms and the ventral heads of all known
forms. Despite the offsetting of the dorsal head the hyomandibular is set a t approximately
Intrucrunial kinetics in Crossopterygii
231
the same angle t o the skull in all Rhipidistia. A possible functional significance of the modification of the dorsal head is discussed in a later section.
The hyomandibular has five distinct articular surfaces-for the two proximal, the middorsal opercular, the terminal quadrate and the subterminal stylohyal articulations.
The actual nature of the distal tip of the hyomandibular is not known in any rhipidistian
since in all cases the bone seems to have been continued distally in cartilage (possibly as a
separate element) which has not been preserved. However, the presence of quadrate and
hyal articulations may be confidently predicted from such indirect evidence as the groove
on the posterior surface of the ‘quadrate’ and the relative position of the various elements.
From the structure of the hyomandibular in Ectosteorhachis we may conclude that the
m. adductor hyoideus inserted on the postero-dorsal margin of the hyomandibular,
proximal to the processus opercularis, and the m. protractor hyoideus probably inserted on
the antero-dorsal surface of the bone a t approximately the same level. According to Jarvik,
the latter muscle in Eusthenopteron inserted on the hyomandibular in the region of the
opening of t,he hyomandibular canal (1954, Pig. 26).
Dermal bones of the skull
The general features of the dermal bone pattern of the rhipidistian skull (see Figs 2 and
5 ) are widely known and detailed discussion of the subject is not required. We may note
that the dermal skull roof is divided into two sections by a suture corresponding exactly to
the intracranial joint beneath. The nature of the connexions, sutural and otherwise, of
these two dermal bone units to each other and to the cheek plate, are of greatest significance
to our study. The genus in which these subjects have been studied most closely is Eusthenopferon (Jarvik, 1937,1944).
The principal factor in the structural iiitegration of the rhipidistian skull is the hyomandibular which interconnects the lower jaw, cheek, operculum, braincase, visceral
skeleton and (indirectly) the skull roof. The cheek plate is loosely connected with the
operculum and dorsally, as far forwards as the postorbital bone, seems to have been
connected to the skull roof merely by a strip of connective tissue. Anteriorly the maxillary,
lachrymal and postorbital bones are connected to the anterior section of the skull roof in an
Fig 3 . Euathenopteron foordi. Left lateral view of head, showing overlapping connexions
(dotted lines) of dermal bones (solid lines).
cl., Cleithrum;d., dentary; it., intertemporal; ju., jugal; I., lachrymal; Le., lateral extrascapular ; mx., maxilla ; op., opercular; p., parietal ; pm., premaxilla;PO.,postorbital; pop.,
preopercular; pp., postparietal; q-j., quadrato-jugal; sop., subopercular; sp., spiracle; sq.,
squamosal; st., supratemporal; t., tabular.
232
KEITHSTEWART
THOMSON,
F.L.S.
overlapping system (Fig. 5) which seems to be arranged in such a way as to allow a small
degree of lateral flexure but no dorso-lateral movement. I n most cases the maxilla and
lachrymal overlap on to the bone lying in front of them. In addition the maxilla bears near
its anterior end a short and fairly stout dorsal projection which probably fitted up against
the postnasal wall (see Fig. 5 ) and was overlapped by the dermal bones of the snout. The
interconnexions of the postorbital, intertemporal, and supratemporal bones have been
described in great detail in Eusthenopteron (Jarvik, 1937,1944).As summarizedinPig. 5, a
flange of the intertemporal slightly overlaps a flange of the supratemporal and the postorbital overlaps both of these bones. It must be remembered that a branch of the lateral line
system passes through the intertemporal to the postorbital. As noted by Jarvik (1950) the
posterior extent of the postorbital bone seems to vary between the families Osteolepidae
and Rhizodontidae-in the latter extending as far posteriorly as the junction between the
supratemporal and tabular. However, it will be noted from Jarvik’s figures (e.g. 1944, Fig.
19) that the extent of the overlapping of the postorbital on to the supratemporal is approximately the same in the two families. Immediately behind this region of overlap the supratemporal itself overlaps fractionally on to the cheek plate-on to the squamosal in
osteolepids and on to the postorbital in the rhizodontids.
The suture between the parietal and postparietal bones is a straight line (except in
exceptional individuals as mentioned previously). The adjoining surfaces of the bones are
rounded and no doubt there was, in life, a gap between the two divisions of the skull roof
which was covered by a band of connective tissue.
The structure of the lower jaw requires little mention except for the subject ofthe retroarticular process. A well-developed retroarticular process has been described in the
Carboniferous osteolepid Megulichthys (Watson, 1926, Figs 37 and 38). I n all other
rhipidistians known to the author, including the genus Ectosteorhuchis (Thomson, 1964a,
Fig. 4) which is a close relative of Megulichthys, a retroarticular process of this type is not
developed. It is extremely difficult to believe that the rlripidistian retroarticular process is
homologous with that of tetrapods, that is, that it served for the insertion of a depressor
mandibulae muscle of the tetrapod type. In many genera of Rhipidistia in which the
process is lacking there is a groove on the posterior corner of the lower jaw which is very
similar to the groove into which the depressor mandibulae muscle inserts in those amphibians such as the Embolomeri which also lack a retroarticular process. On the other hand
there is no immediately obvious place in the cheek/operculum region where a depressor
mandibulae muscle could have been located and on the whole it seems most likely that
depression of the lower jaw was effected by hypobranchial muscles such as Jarvik has
described in Eusthenopteron and Glyptolepis (1963). The presence of the posterior groove
and the retroarticular process in Rhipidistia requires explanation and it is possible that
here was inserted the distal end of a mandibular-hyomandibular ligament. Such a ligament, though rather differently situated, is seen in coelacanths.
A small discoid bone separating the two lower jaw rami a t their anterior symphysis may
have been of importance in facilitating the slight relative movements of the two rami
during expansion of the cheek region.
Note on embryology
Romer (1937) was the first to analyse the structure of the rhipidistian endocranium in
terms of its basic embryonic components and he recognized (cf. Cope, 1883; Aldinger,
1931) that the division between anterior and posterior division of the endocranium
corresponds to a separation of elements of trabecular and parachordal origin. More
recently Jarvik (1954,1960)has elaborated this analysis and has developed an interesting
theory of the embryonic derivation of both endocranium and palate. The details of these
hypotheses need not be discussed here but i t is important to note that several authors,
including Szarski (1962),have tended to regard the assertion that the joint exists as a relic
233
Intracranial kiiletics in. Crossopterygii
of an ancestral primary metamerism as a comprehensive explanation of its persistence and
as a satisfactory alternative to a functional interpretation of its presence.
K I S E T I C S AND DYNAMICS O F THE R H I P I D I S T I A N SKULL
Mechanical considerations
From an examination of the points of attachment and articulation of the various
components of the skull, noting particularly the orientation of the various articular facets,
it is possible to deduce the general nature of t'he movements that might have been achieved.
The structure of the intracranial joint itself allows only a direct dorso-ventral rotation
of the anterior division of the braincase upon the posterior division. There is a firm connexion between the anterior portion of the palato-quadrate (pars autopalatina, where
present) and the orbito-nasal wall of the anterior endocranium, and the lateral margin of
I""
a d hy
n
\
subc
ur
/
Fig. 6. Ectosteorhachis nitidus. Head in left lateral view, with dermal bones removed, palate
shown in outline (dotted line) and the notochord and certain muscle restored.
add.hy., Adductor hyomandibularis; c.m., coraco-mandibularis ; l.a.p., levator arcus
palatini; n., notochord; st.hy., sterno-hyoideus; subc., subcephalic; ur., urohyal bone.
the palato-quadrate is firmly attached to the maxillary bone of the cheek plate. This,
together with the connexions between the dermal bones of the cheek and those of the
rostrum, which allow only a small amount of lateral bending, dictate that the anterior unit
of the skull (anterior endocranium, anterior dermal skull roof, cheek plate and palate)
moves as a unit upon the posterior unit of the skull (posterior endocranium and dermal
roof elements). (We have already noted that there is no direct connexion, except possibly
pathologically, between the palato-quadrate and the posterior endocranium.) Internally,
the shape and orientation of the articular surface of the basipterygoid articulation is such
that a t this joint the only possible movements were a lateral movement of the palate upon
the endocranium and a small movement along the arc described by the curvature of the
articular surface. While the palatal complex (with associated dermal elements) has little
scope for movement in the dorso-ventral direction relative to the anterior endocranium,
there is obviously a greater potential for such a movement relative to the posterior endocranium. Apart from ligamentous attachments of the cheek to the skull roof the whole
complex is supported from the posterior endocranium only a t the suspensorium, where the
hyomandibular and quadrate elements articulate with the mandible. The exact nature of
234
KEITHSTEWART
THOMSON,
F.L.S.
the proximal and distal articulations of the hyomandibular is thus of very great importance
in controlling the relative movements of the skull components. The hyomandibular stands
a t an angle of about 45" to the braincase. The proximal articulation, by means of the two
heads separated as far apart as possible on the lateral commissure, seems to be designed to
prevent any movement of the hyomandibular in the plane of its long axis-for downward
deflection of the distal end of the hyomandibular would disarticulate the dorsal head, and
upwards deflection would disarticulate the ventral head. I n fact the arrangement of the
proximal articulations of the hyomandibular is such as to allow only an antero-lateral to
postero-medial rotation of the bone. There can have been no direct dorso-ventral movement of the bone although in most genera the arc of lateral rotation may have been set in
such a way that the plane of movement of the tip of the bone was slightly inclined from the
horizontal.
Although the exact nature of the distal connexion between the hyomandibular and
quadrate in Rhipidistia has not been determined, a small degree of sliding of the two bones
relative to each other probably occurred in a groove on the posterior margin of the palatoquadrate.
The arrangement of the intracranial joint is such that the only possible relative niovement of the anterior and posterior divisions of the endocranium was in the vertical plane.
The shape of the articular surfaces in a fish such as Ectosteorhuchis suggests that the position of the fulcrum of this joint might differ in movements of the snout upwards and downwards from the resting position (cf. Figs 3 and 7 ) . This may also be true of other genera.
The arrangement of the two component units of the skull and the orientation of the
articular facets of the hyomandibular indicate that dorso-ventral movements a t the intracranial joint were accommodated by lateral rather than dorso-ventral movements of the
suspensorium. Thus when the tip of the snout was raised relative to the posterior endocranium, the suspensorium on each side was moved forwards and outwards by a corresponding rotation of the hyomandibular (see Fig. 7 ) .
These combined movements obviously affect the relative positions of the dermal bones
of the skull, especially in the region of the intracranial joint, and it will be seen that the
complicated series of overlapping flanges (described above) by which certain of these bones
articulate with each other forms a mechanism for accommodating these movements. The
shape of each overlapping articulation reflects quite closely the nature of the potential
movement. I n certain instances there is a second function for this system of flanges: that of
preventing excessive flexure or accidental disarticulation of the cranial joint, especially
in a lateral direction. Thus the slight overlap of the supratemporal on to the cheek plate
would act as a check against excessive deflection downwards of the anterior portion of the
skull. We may finally note that the presence of the flexible notochord attaching to the
posterior surface of the anterior endocranium will have given some structural rigidity to
the joint region and is likely t o have 'damped' the whole system.
With respect to the principal muscles concerned with the cranial kinesis it is obvious
that the large and well-developed subcephalics are the principal agents in depressing the
anterior unit of the skull, but it is not immediately apparent which muscles oppose the
subcephalics and are responsible for dorsal movement of the snout (Millot & Anthony,
1958a, have noted the same problem in Latimeria).Close consideration, however, indicates
that the subcephalics must be opposed principally by the muscles responsible for depressing the lower jaws. Thus contraction of the coraco-mandibular muscles, inserting near the
tip of the jaws, would cause a significant anterior and lateral deflection of the suspensorium.
This action would of course, require appropriate ligamentous interconnexion of the lower
jaw, hyomandibular and palate. Evidence for the presence of such ligaments in Rhipidistia
is not complete (see above) but corroboration is very clearly provided by the arrangement
of the ligaments in the suspensorial region of the coelacanth Latimeria (see below).
The total movements of the skull during operation of the intracranial articulation.
together with the muscle actions which effect these movements, may now be summarized.
Intracranial kinetics
235
i i Crossopterygii
~
................................
.......................
C
Fig. 7. Ectosteorhachis nitidus. Diagrams showing the relative movements within the skull
during operation of the skull kinesis.
Top: lateral view of movement of skull from resting position (solid black lines) t o raised
position of snout (open lines). A’ represents initial angle of upper jaw to horizontal; B’ increased angle of upper jaw.
Centre: lateral view of movement of skull from resting position (solid black lines) t o depressed position of snout (open lines). A‘ represents initial angle of upper jaw; C’ decreased
angle ofupper jaw.
Bottom: dorsal view of skull showing relative movements from the raised snout position C,
through the resting position B, t o the depressed position C.
KEITHSTEWART
THOMSON,
F.L.S.
236
Dorsal flexure of the anterior unit of the skull upon the posterior unit was accompanied
by a lateral and forward movement of the cheek region. The movements were effected by
contraction of the m. levator arcus palatini which was inserted on to the palate dorsal to
the fulcrum of the intracranial joint, and by contraction of the ni. protractor hyomandibularis which swung the suspensorium outwards and forwards, while at the same time the
lower jaw was depressed by the hypobranchial coraco-mandibular muscles (Fig. 6).
Depression of the anterior unit of the skull, accompanied by closing of the mouth and
retraction of the cheek region, was effected by contraction of the subcephalic musculature.
the m. adductor hyomandibularis, and possibly also the ventral branchial constrictors. If
the suggested presence of a hyomandibular-mandibular ligament is correct then the action
of the nim. adductores mandibularum in closing the mouth would be accompanied by a
tightening of the ligament binding the hyomandibular, quadrate and mandible more
closely together.
The sequence of events just described accounts for a simple opening of the gape. If
breathing movements were involved, the opening of the gape (dorsal flexture of the anterior unit) may have been accompanied by retraction of the operculum, and closing of the
gape (ventral flexure) by opening of the operculum with raising of the basihyal by contraction of the geniohyoideus system to expel an exhalant water current from the orobranchial chamber.
Quantitative analysis of the skull mechanism
Figure 7 shows the relative movements of the skull components during flexure of the
skull in Ectosteorhachis. The figure depicts the maximum movement possible in the skull of
this particular animal (the species E . nitidus from the Lower Permian of Texas),which has
been deduced in the following way. By making accurate drawings of a specimen such as
this we may reconstruct quite readily the potential movements of the various components
relative to each other at, for example, the basicranial articulation, which are produced b y
cranial flexure through specified angles. Since we know the actual shape of the basipterygoid articulation in the species, and may expect it t o reflect quite closely the nature of
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301
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.
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15
0
10 20 3 0 40 5 0
Length of posterior division o f ihe skull roof
FIG.8.
FIG.9.
Fig. 8. Osteolepis macrolepidotus. Scatter diagram showing relationship of the length of the
anterior division of the skull roof and the length of the posterior division of the skull roof.
Measurements of 47 specimens.
Fig. 9. Eustheiiopteron joordi. Scatter diagram showing relationship of the length of the
anterior division of the skull roof and the length of t,he posterior division of the skull roof.
Measurements of 22 specimens.
Intracranial kinetics in Crossopterygii
237
the actual movements occurring a t the articulation (since the joint is unlikely to have been
a loose one) we may check the hypothetical movements of the reconstructed skull against
the actual ones.
These and similar techniques may be used to reconstruct the potential cranial movements in other rhipiclistian fishes. Obviously the extent of the potential cranial movements in a given fish will depend to a great extent upon the proportions of the skull,
especially the relative lengths of the two sections of the braincase, the lower jaw and palate,
and the hyomandibular.
First of all we may check skull proportions in known material for allometry." Good
suites of material including an extensive size range are available for the osteolepid Osteolepis macrolepidotus and the rhizodontid Eusthenopteron f o o d . As the graphs show (Figs
8 and 9) there is no indication of allometric growth in these fishes.
A well-known and characteristic feature of the Rhipidistia, which is an extremely
valuable taxonomic guide, is a variation in the relative lengths of the anterior and posterior
divisions of the skull (see for example, Jarvik, 1948, Fig. 13).Obviously this has an important bearing on the length of the jaws ; it is interesting to note therefore that, as shown
in Fig. 10, there is a constant relationship between the length of the lower jaw and the
.
IlO]
m
0
10
30
50
70
90
110
130
Length o f lower j a w
Fig. 10. Scatter diagram showing relationship of length of the combined skull roof to the
length of the lower jaw, measured as the straight,-line distance from the tip of the dentary to
the end of the dentary. Average measurements for 18 different species of Rhipidistia. Key to
species in this and following graphs: a, Osteolepis mncrolepidotus; b, 0. pnnderi; c, Thursius
imcrolepidotus; d, T . moy-thomasi;e, T . p?!olidotus; f, Gyroptychius ugnssizi; g, Cyroptychius
ttiilleri; h, Clyptoponaus elginensis; i, G . kinnriirdi; j, Eusthenopteron dalgleisiensis; k, E.
, f o o d ; 1, Rhizodopsis sauroides; m, Ectosteorhrtchis n i t i d u s ; n, Tristicopterus alatus; 0 ,
Gyroptychius? kiaem'; p, Cyroptychius grortilandicus; q, Glyptolepis cf paucidens, r, Eusthenod o n wangsjoi. Data original and from Jarvik (1948, 1950) and Thomson (19G4a, 19G6).
length of the skull roof in the three superfamilies of Rhipidistia. Note that this relationship
also is independent of the absolute size of the fishes. Further analysis confirms what is
obvious from simple observations of the material-that in general changes in the proportions of the skull are due to relative elongation or shortening of the anterior division. This
is shown clearly by the graphs in Fig. 11.
One effect of change in the relative lengths of the two divisions of the skull roof and
braincase is a change in the relative width of the skull. It should, however, be noted that
inore than one factor is involved in determining the width of the skull (the nature of the
adductor musculature of the jaws is certainly also involved). I n connexion with our
* Note that in most cases the numbers of specimens available and the fact that in some cases there
may be slight distortion of the material means that it is not really possible to use very sophisticated
statistical analysis. Nevertheless certain reasonably accurate results may be obtained from simple
methods.
KEITHSTEWART
THOMSON,
F.L.S.
238
2-5
4 01
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1.0.
2.5.
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20
15
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0.5
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Fig. 11. A. Scatter diagram comparing the proportion l/b (length of lower jaw relative to the
length of the anterior division of the skull roof) and b/a (length of anterior division of skull roof
relative to length of posterior division) in 18 species of Rhipidistia. B, Scatt,er diagram comparing the proportion l/a (length of lower jaw relative t o the length of the posterior division
of the skull roof) and b/a, in the same species. Key to species in caption to Fig. 10.
present study of the cranial kinetics of the skull the length of the hyomandibular is more
directly important than the width of the skull and in Fig. 12 a n attempt is made to explore
the relationships between the three most important dimensions of the skull-the length of
the anterior division of the roof (b),the length of the posterior division (a), and the ‘effective length’ of the hyomandibular (hy). Note that in this connexion we consider only the
‘effectivelength’ of the hyomandibular, that is, the radius of the arc through which the tip
of the hyomandibular moves during the operation of the skull kinesis. The graphs show
that in different Rhipidistia the ‘effective length’ of the hyomandibular is maintained as
more or less constant proportion of the length of the posterior division of the skull (perhaps
increasing slightly) and is independent of any increase in proportion of the snout. The
inference from this is that the angle through which the hyomandibular is rotated is
maintained roughly constant in all Rhipidistia and that, therefore, if the anterior division
of the skull is elongated then the angle through which the tip of the snout is moved must
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Intracranial kinetics in Crossopterygii
239
be decreased. This result may be checked by making graphical reconstructions (as outlined above) of the maximum extent of cranial movement in skulls of differing proportions
corresponding to known fishes. Thus it may be shown that in a skull of given size, relative
increase in the ratio b/a, that is in the relative length of the anterior division of the skull, is
accompanied by a reduction of the angle through which the intracranial joint may be
moved (Fig. 13) and that there is a corresponding decrease in the movement relative to
....................
...’ ....*..
.........................._........,,~._
Fig. 13. Diagram of the mechanical arrangenient of the rhipidistian skull showing the effect
of change in the position of the intracranial joint ( I , 2 , 3 , 4 ) upon the angle through which the
snout may be deflected (1’,2’, 3’, 4’) for a given movement of the hyomandibular.
1, 2, 3, 4 position of intracranial joint in Rhizodopsis, Osteolepis, Eusthenopteron and the
amphibian Ichthyostega (position of intracrmiial suture), respectively.
each other of the palate and braincase manifest by a decrease in the size of the articular
surface of the basipterygoid articulation. It should be emphasized, however, that the number of species for which details of both the cranial proportions and the intracranial articular surfaces are known are still few-namely Ectosteorhuchis nitidus, Osteolepis macrolepidotus, Eusthenopteron foordi,Rhizodopsis sauroides and Glyptolepis sp. (rather less well
known). Thus we may establish a t this point only a general pattern of the action of the
rhipidistian intracranial kinesis. Therefore it is not appropriate to extrapolate from the
present study conclusions concerning particular lineages or radiations of rhipidistian
fishes, although this may develop a t a later date. One interesting observation may be
made, however, which has a general phylogenetic importance. If we continue our exercise
by concocting a fish with a typical rhipidistian kinetic skull but with the overall skull
proportions of the primitive amphibian Ichthyostega (Fig. 13) we discover that the relative
movement of palate and braincase a t the basipterygoid articulation is very small indeed.
(In fact such a rhipidistian does exist and will be described in a future work.) This observation goes some way toward accounting for the loss of the kinetic skull in Amphibia, and is
discussed further below.
Functional and adaptive aspects of the cranial mechanism
In the preceding section an attempt has been made to determine the extent of the relative movements of different components of the skull that could be achieved through
operation of the intracranial articulation in various genera of Rhipidistia. Our problem
now is to discover how this range of potential movement might actually have been utilized
and thus to elucidate the functional and adaptive significanceof this system of intracranial
articulation.
We may deal first with the theory that the intracranial articulation existed primarily as
a shock-absorbing mechanism, protecting the brain from damage by the shock delivered
by adduction of the powerful lower jaws. We have seen above that the braincase in Rhipi-
240
KEITHSTEWART
THOMSON,
F.L.S.
distia is essentially suspended from the dermal skull roof and is only attached to the palate
by the anterior and basipterygoid joints and (indirectly) through the hyomandibular. Now
when the mandibles are snapped shut shock is received upon the lateral parts of the palate
and upon the marginal bones of the dermal skull complex (maxillae and premaxillae). A
small amount of the shock will pass directly to the braincase a t the rather firm anterior
joint between the tip of the palate and the orbito-nasal wall, and possibly also where the
anterior tusks (when present) fit into the anterior palatal recesses of the snout (see Thonison, 1962). The main part of the shock, however, will be absorbed within the arch of the
skull roof and if there is any flexibility of the sutures here, will be dissipated without
dangerously affecting the braincase. Similarly transmission of any medial component of
the shock received upon the palate t o the braincase will de prevented by the flexibility of
the basipterygoid and hyomandibular articulations. It will be seen therefore that the
principal factors in absorbing shock from the lower jaws are the loose articulations of the
basipterygoid and hyomandibular and a certain amount of overall flexibility of the dermal
skull complex. The joint within the endocranium does not materially affect this mechanism. It may further be noted that the nature of the overall movements of the skull is such
that operation of the cranial articulation causes the anterior division of the skull to be
brought d o a n hard upon the mandibles as they are being adducted, thus serving to increase the shock of swift closing of the mouth. Finally since some individuals seem to have
lost the kinetic facility with little apparent disadvantage, the lovr er jaw ‘shock’ seem3
unlikely t o have been large enough t o warrant the development of this complicated system.
The potential physical effects of operation of the cranial kinesis are as follows: ( 1 ) the
angle of the gape is changed but with minimal vertical of antero-posterior movement of the
suspensorium ; ( 2 )operation of the intracranial articulation in conjunction with opening of
the mouth reduces the extent by which the lower jaws must be depressed in order to open
the gape t o a given angle (by the extent of the elevation of the upper jaws) ; (3) changes
in the volume of the orobranchial cavity are produced by the expansion and retraction of
the cheek region. It seems most likely that operation of the intracranial kinesis was normally accompanied by opening and closing of the mouth, since the mandibular retractor
muscles have an important role in operating the kinesis. It is possible, however, that effects
(1)and (3), above, might have been produced also when the mouth was closed by raising of
the snout either by the action of the palatal and hyomandibular muscles alone, or with
isometric contraction of the coraco-mandibular muscles. As we have seen above, the extent
of the mechanical displacement of the various skull components caused by operation of the
intracranial articulation varies in different fishes according to the proportions of the skull.
It is greatest in those fishes in which the anterior division of the skull is relatively short.
The adaptive significance of the intracranial articulation must obviously be connected
with the general life habit of the rhipidistian fishes and it may be remarked that it is perhaps improbable that such a fundamental modification of the skull would be associated
with merely a single functional requirement such as, for example, ‘shock absorbing’.
Available evidence indicates that the Rhipidistia lived in shallow water conditions and
that it was possible for them to make short excursions overland, or a t least through mud or
swamp. I n fishes of such elongate shape living in shallow water there is necessarily some
restriction of general mobility in a vertical direction, especially with respect to feeding or
breathing at the surface-the head may not be raised because the trunk and tail cannot be
lowered. In this case the cranial mechanism of Rhipidistia might be of significant adaptive
value. By raising the snout region the whole mouth could be directed upwards towards the
surface or, of course, downwards towards the bottom. No doubt this particular mode of
utilization of the cranial kinesis would have been of greater importance in those Rhipidistia
with a short snout and a large angle of cranial flexure, such as Rhizodopsis, rather than those
in which the snout was long, such as Eusthenopteron. Even so, this particular usage is
probably unlikely t o have been of prime importance.
A second important factor concerning life in shallow water, and particularly in very
Intracranial ki7zetics i n Crossopterygii
241
shallow water or activity on land, concerns the operation of the lower jaws. I n these conditions the process of opening the gape is likely to be hindered by the fact that the lower
surface of the head is resting on or is very near the bottom. The rhipidistian adaptation of
opening the gape in part by raising the upper jaws could have been of significant value in
such circumstance. Watson (1951) has noted that in solving this problem another group of
vertebrates (the labyrinthodont amphibians) developed an analogous adaptation whereby
the whole of the skull was raised relative to the rest of the body. Furthermore shallow
water conditions would certainly also have considerably hampered the process of closing
the mouth in these fishes. The arrangement of the adductor muscles of the lower jaw in
Rhipidistia was basically what Olson (1961) terms the ‘kinetic inertial system’. The long
lower jaws, armed with their battery of sharp tusks were used in a ‘sling’ action with the
main muscular force delivered when the jaws were wide open so that they were swiftly
accelerated from this position and then snapped shut largely through their own momentum. The adductor muscles are thus arranged so that relatively little force could be
developed when the jaws were more than, say, half closed. ‘Chewing’ was not strictly
possible. The jaws of modern crocodilians operate under approximately the same principle.
The arrangement of the rhipidistian skull with a n additional set of ‘ adductor ’ muscles in
the shape of the subcephalics would presumably have been of importance not only in
allowing the fish to develop maximum force in closing the mouth even from positions
where the ‘pterygoid’adductors could not act efficiently, but also in adding to the basic
‘kinetic inertial ’ system a means of holding firmly on to, or even ‘ chewing ’ prey when the
mouth was nearly closed. This particular mode of utilization of the intracranial articulation would have been of greatest significance to those fishes with the proportionately
longest snouts and jaws.
Most fishes possess a mechanism for ventilating the gill chamber through niovements of
the cheek region. The Crossopterygii are unusual in that they accomplish this by anteropost)erior movements of the suspensorium in a horizontal plane rather than by lateral
movements in a vertical plane. This system would not appear to confer any particular
selective advantage and is doubtless a secondary product of the particular characteristics
of the cranial mechanism. There is. however, an interesting side-effect of the peculiar
movements of the cheek. We have seen that palate and cheek move together. The movement of the two sides of the palate with their batteries of teeth during the cranial kinesis,
will have been as follows: jaws opening-palate moved fornards and outwards on each
side, jaws closing-palate moved backwards and towards the midline. This together with
the associated movements of the visceral arch skeleton (also denticulated, see Jarvik,
1954) would possibly have been of importance in gripping and swallowingthe prey.
Finally it should be noted that if, for one reason or another; the cranial kinesis failed to
operate, the operation of the lower jaws in a ’normal way’ would have continued unimpaired. While this would obviously have been inadaptive in the long term doubtless a few
individuals could have survived in this condition by seeking deeper water in which to feed
and relying upon use of the lungs or ventilation of the gills by movements of the gular
apparatus (as in Dipnoi) in respiration.
The above paragraphs have been concerned with the possible functional and adaptive
significance of the physical displacements of various portions of the skull which, together
with the muscular actions which might affect thcm, may be termed the cranial kinesis.
I n toto the various intracranial movements add a small but obviously significant dimension
to the mobility and efficiency of the basic liyostylic jaw suspension from which the rhipidistian system has been modified. It will be seen that the advantage of this kinetic system
lies in different directions in different fishes and probably also in different environments.
Thus in both structure and function the intracranial articulation is seen to be a fundamental adaptation of the crossopterygian fishes, rather than a specialized modification of
secondary importance.
One further aspect of the functional significance of the intracranial articulation remains
16
242
KEITHSTEWART
THOMSON,
F.L.S.
to be explored. Although it cannot be studied in any very precise way the possibility exists
that part of the significance of the system of intracranial articulation lies in its dynamic
rather than kinetic properties. This might apply particularly t o the arrangement of the
subcephalic muscles which, as we have seen may have been used as much to deliver
pressure downwards through the anterior division of the skull as actually to move it. Thus
an additional function of the system of articulations between the various skull components
might be to help accommodate within the skull the tensions and pressures developed by
the various muscular systems. Naturally such a function would have evolved secondarily
but it might have been of great significancein these lines of predacious Rhipidistia in which
elongation of the snout and jaws was obviously accompanied by a considerable development of the cranial muscle system.
MECHANISMS OF THE COELACANTH SKULL
We are extremely fortunate that a considerable amount of detailed information is
available concerning the anatomy of the living coelacanth Latimeria, see especially,
Millot & Anthony (1958a, b ) . This is invaluable in discussion of the structure and functions of both the fossil coelacanths and the Rhipidistia. (See Schaeffer, 1952, for principal
references to fossil Coelacanthini.) However, in view of the fact that our knowledge of the
habits and structure of the living Latimeria is likely to increase greatly in the future our
discussion of the Coelacanthini a t this stage will be brief and hopefully will be improved
upon a t some later date.
As we have already noted with respect to the Rhipidistia, the presence of the intracranial articulation in coelacanths, living and fossil, leads one to believe that this joint had
a particular adaptive significance, and that its particular function (or functions) must
involve movements of the anterior and posterior divisions of the skull relative to each
other (Watson, 1921 ; Aldinger, 1930, 1931 ; et aha).It is, however, only correct to record
that Millot & Anthony (1958a) considered that very little movement was possible. In
Pig. 14. Latimeriu chalumncce. Skull in left lateral view showing the disposition of the principal
skull elements.
antiend., Anterior division of braincase; cer.h., cerato-hyal; ep.h., epihyal; hy., hyomandibular; int.j., intracranial joint; mand., mandible; op., operculum; p-q., palato-quadrate;
post.end., posterior division of braincase; sth., stylohyal; sympl., symplectic.
Intracranial kinetics in Crossopterygii
243
the study we may examine what range of movements within the skull seem possible and
may suggest functions for the intracranial kinesis.
Figures 14 and 15 summarize the structure of Latimeria. It is remarkable t o note
(Schaeffer, 1952, 1953) how very little the coelacanth skull has been modified between
Devonian and Recent times. One constant feature is that the dorsal section of the hyoid
arch skeleton seems always to have been made up of more than one element (hyomandibular, epihyal and symplectic in Latimeria). The separate bones are bound together and to
mlap.
r-I
.
lig p m-h.
Fig. 15. Latimeria chaZumnae. Hyoid region in left, lateral view showing positions of various
muscles and ligaments. (Redrawn from Millot & Anthony, 1958b.)
ep.h., Epihyal; hy., hyomandibular ; 1ig.a.m-h., anterior mandibulo-hyoid ligrtment ;
1ig.p.m-h., posterior mandibulo-hyoid ligament; 1ig.i.q-h., inferior quadrato-hyoid ligament ;
1ig.s.q-h., superior quedrato-hyoid ligament.; lig.s.sy., superior sylnplectic ligament; m.1.e.p..
levator arcus palatini muscle; m.subc., subcephalic muscle; op., operculum ; p-q., palatoquadrate ;sth., stylohyal ;sympl., symplectic.
the palato-quadrate and mandible by a series of ligaments (Fig. 15). The hyomandibular
seems always t o have had a double proximal articulation with the braincase although the
joint seems to have been rather less precisely defined than that in Rhipidistia. The ventral
articulation is usually located somewhat anterior to the dorsal one. The palato-quadrate is
constructed essentially as in Rhipidistia, although often consisting of several separate
ossifications. Exactly as in Rhipidistia, it is bound firmly to the anterior endocranium,
with which it presumably moved as a single unit, behind the nasal capsule and has no direct
attachment to the posterior endocraniurn. The quadrate is always located a t the anteroposterior level of the intracranial joint, considerably more forward than in Rhipidistia. As
a consequence the jaws and gape are rather short. The basipterygoid process of the anterior
endocranium is lost in post-Carboniferous coelacanths, but an antotic process, unknown in
Rhipidistia, is present.
The coelacanth mandible is constructed differently from that of Rhipidistia. The quadrate-articular joint is located about two-thirds of the way along the mandible and the
symplectic has a separate insertion on t o the posterior tip of the jaw together with a pair
244
KEITHSTEWART
THOMSON,
F.L.S.
of hyomandibular-mandibular ligaments (Fig. 15). There is a well-developed coronoid
process in all genera. I n Latimeria and almost certainly the fossil genera also, retraction
of the mandible is effected by a coraco-mandibular system (Millot & dnthony, 1958 3) ;
there is no depressor mandibulae of the tetrapod type.
I n the majority of structural features the skull of coelacanths is very similar to that of
Rhipidistia, but the differences just mentioned niake it quite clear that there must be
certain differences in the mechanisms of the jaw and of the intracranial articulation. Being
made up of three separate parts the hyomandibular is unlikely to have great resistance to
distortion through compression in the direction of its long axis, although the presence of
the various ligaments almost certainly would have prevented stretching in this direction.
The relative positions of the proximal articulations of the hyomandibular suggest that if it
moved as a single unit it would have rotated outwards in an arc the plane of which was set
a t about 60" to the vertical. The position and orientation of the quadrate-mandibular
articulation shows that the rather short gape faced more directly forwards than in
Rhipidistia.
The key to understanding the coelacanth cranial mechanism seems t o lie in the nature of
the articulations between the quadrate, symplectic and mandible. Whereas in Rhipidistia
the hyornandibular was closely attached to the quadrate and there was a common articular
facet on the mandible to receive them, in coelacanths there are two separate articulations
and the articular facet for the symplectic is situated some distance behind that for the
quadrate (see Smith, 1939 ; Smith-Woodward, 1940; Schaeffer, 1952 ; Millot & Anthony,
19583). By virtue of this arrangement the movements of the hyoid arch and palatoquadrate relative both to the lower jaw and endocranium will differ, whereas in Rhipidistia
the palato-quadrate and hyomandibular move essentially as a single unit.
Depression of the lower jaw in coelacanths is effected by the coraco-mandibular muscles
whose direction of action is principally backwards and downwards. As the lower jaw is
depressed, rotation around the quadrate hinge will displace the symplectic upwards
(Fig. 15). It is obvious therefore that the operation of the skull liinesis must be such as to
accommodate this movement (cf. Trewavas, 1959).
As in Rhipidistia, the intracranial kinesis seems to have been concerned primarily with
the opening of the gape. The sequence of movements, in Latimeria, may be deduced from
the arrangements of the various skull components, as follows.
Retraction of the lower jaw (by the coraco-mandibular muscles) and branchial skeleton
(by the sternohyoideus muscles) is accompanied by expansion of the cheek and palate, by
the action of the levator arcus palatini muscles. These muscles insert proximally upon the
posterior endocranium and probably produce, in addition to the lateral movement of the
palate and cheek upon the anterior endocranium. a dorsal movement of the anterior
endocranium upon the posterior endocranium. This action is reinforced by the action of
the coraco-mandibular and sterno-hyoid muscles through the ligamentous connexions
between the palato-quadrate and hyoid arch elements. As a result the quadrate is moved
both outwards and forwards. The forward movement of the quadrate (and thus of the
whole lower jaw) compensates for the small dorsal movement of the posterior tip of the
mandible and the symplectic during depression of the jaw (Fig. 16). I n this connexion it is
perhaps significant that there are no levator hyoideus muscles in Latimeria.
Downward flexure of the anterior portion of the skull and retraction of the cheek region
are affected by the adductor arcus palatini, adductor hyomandibularis and subcephalic
muscles, the lower jaw being raised by the adductor mandibulae. The whole process is
helped by the presence of the strong hyomandibular-mandibular ligaments. When the
mandible is raised, the posterior section of the jaw, rotating around the quadrate hinge, is
actually depressed, pulling upon the ligaments. The adductor hyomandibularis also pulls
on the hyomandibular and the net effect will be to increase the forces constricting the whole
of the hyoid arch and the posterior portion of the palato-quadrate.
A most important difference between the rhipidistian fishes and Latimeria, a t least, is in
Intracranial kiizetics in Crossopterygii
245
Fig. 16. Latimeria cl~ulumnae.Head in lert lateral view showing attempted restoration of the
relative movements of the skull from the ‘reding position’ (solid lines) to the ‘snout-raised’
position (dotted lines).
the relations of the subcephalic muscles. In Rhipidistia they are inserted on to the posterior
margin of the anterior division of the braincase, but in coelacanths they extend forwards,
either side of the parasphenoid bone to ligamentous insertions under the nasal region. Thus,
while the general action of the subcephalic muscles is the same in both groups of fishes,
there is probably a significant difference in the way in which the intracranial kinesis is
utilized.
The gape in coelacanths. due to the forward position of the quadrate, is rather short, and
in general the teeth are less prominently developed than in Rhipidistia. The presence of a
coronoid process on the mandible in all known forms indicates a considerable difference in
the arrangement of the adductor mandibulae musculature from the situation in Rhipidistia where the adductors all inserted on the rim of the adductor fossa.
What we know of the fossil and recent coelacanths suggests that they are not active
predacious fishes in the way that their rhipidistian relatives were. The whole structure of
the jaws (including, in many forms such as Latimeria, loss of the maxilla and its replacement with a denticulate fold of the upper lip) suggests that the coelacanths fed on small
prey and that the mouth and jaws were adapted to making short, powerful, snapping
movements. The intracranial articulation is probably utilized in increasing the general
mobility of the mouth and gape, as in Rhipidistia, and because of the relatively anterior
position of the suspensorium may have been particularly effective in this respect. The
difference in the mandibular adductor and subcephalic muscle systems, however, indicates
that the coelacanths have considerably modified the basic rhipidistian kinesis and have
developed it into a dynamic system for increasing the power of the jaw mechanism.
In view of the fact that it is possible that we may eventually be able to study the behaviour of living coelacanths it seems undesirable to enter into detailed speculation about
the utilization of the intracranial kinesis of these fishes. Of more immediate importance are
the differences that we can observe between the relevant structures in coelacanths and
Rhipidistia (as noted above), since they give some indication of the range of possible
modifications of the basic system of kinetics involving the intracranial articulation.
246
KEITHSTEWART
THOMSON,
F.L.S.
DISUUSSION
The inception and evolution of a particular cranial mechanism in any group of vertebrates result from a whole series of interacting factors involving, for example, both general
habits and specific feeding requirements. Without direct knowledge of the ancestral
forms it is often difficult to pick out those characteristics of the resulting morphological
adaptation which are specialized modifications and those which represent the basic
structural pattern. However, from our knowledge of the structure and evolution of the
Rhipidistia and of their close relatives the.Coelacanthini we may make a tentative reconstruction of the characteristics of the ancestral stock from which the Crossopterygii, as we
know them, arose.
The Coelacanthini show several structural characteristics which may be interpreted as
modifications of the more basic system of intracranial kinetics seen in the Rhipidistia.
Among these are the presence of the coronoid process on the lower jaw and the forward
position of the suspensorium, with which the changed manner of operation of the lower
jaw, the development of retroarticular process and the complicated structure of the
hyoid arch are also directly connected. The differences in the mode of operation of the
coelacanth intracranial articulation are also accompanied by loss of the basipterygoid
process and the development of the antotic process. Considerations such as these suggest
that the Coelacanthini represent a side-shoot of the crossopterygian stock in which the
cranial structures have evolved in a particular way which has involved shortening of the
gape, specialization of the jaw musculature, and modification of the function of the intracranial articulation. Other aspects of the structure of the Coelacanthini, however, suggest
that they are phylogenet,icallymore primitive than the Rhipidistia : here we may cite as an
example the structure of the nasal apparatus (lacking a choana). Of course, except that
they are manifestly different, we have little justification for considering either of the two
crossopterygian groups as being closer to the ancestral stock than the other. Nonetheless,
from my study of the two groups, I favour the view that the system of intracranial mechanics seen in the fossil Rhipidistia more closely represents the conditions in the ancestral
stock from which the two lines of crossopterygians evolved.
I n the ancestral stock the braincase was most probably a single ossification extending
from the nasal capsule to behind the otic capsule. The cheekplate, posterior to the forwardly placed orbit, was probably only connected to the skull table by means of a sheet of
ligaments, and there was a movable articulation of the palate on the braincase a t the
basitrabecular process. The jaw suspension will have beenof the hyostylic type with a single
large hyomandibular ossification,probably with an essentially single proximal articulation
on to the parotic process/lateral commissure region of the braincase. The cranial movements will have been essentially as in, say, palaeoniscids, with a lateral movement of the
whole cheek on the braincase effected by a muscle system not greatly different from that in
Rhipidistia. The adductor musculature €or the lower jaw will probably have its origin
solely on the palate. I n the absence of definite information concerning the homology of the
subcephalic musculature of crossopterygians we may hazard the guess that it is of visceral
origin and was originally used in moving the whole skull in the vertical plane upon the
trunk (cf. Trewavas, 1959). Such a condition would convincingly foreshadow the development of the crossopterygian intracranial articulation, part of the function of which, as we
have seen, is to increase the manoeuvrability of the jaws and gape in the vertical plane.
One may suppose that such a set of muscles, in this hypothetical ancestor, would have been
opposed by the mandibular retractor muscles and those trunk muscles inserting in the
fossa Bridgei on the otic region of the skull. The mode of action of such a subcephalic
series would probably require that the anterior insertion on to the ventral surface of
the braincase should be fairly far forward, probably a t the level of the future lateral
commissure. Once the intracranial articulation had been developed this insertion
would be shifted to the anterior division of the endocranium and there would also be
a:
Intracranial kinetics in Crossopterygii
347
a considerable mechanical advantage to having the origin of the subcephalic muscles
transferred to the posterior division of the endocranium. We may note here that it is
most probable, if the above hypothesis is correct, that the notochord in the adult ancestral
form ended anteriorly a t the level of the joint between the otic region of the skull and the
trunk. Thus the persistence of a large notochord extending forwards to the level of the
dorsum cellae in Crossopterygii must be regarded as a structurally specialized character
directly related to the development of the intracranial articulation.
Once the intracranial articulation had become established there would immediately be
considerable selective pressure for the evolution of a more sophisticated proximal articulation of the hyomandibular in order to contain and direct the various intracranial movements. We have seen above that the optimum situation in Rhipidistia seems to be a double
proximal articulation with the two heads located as far apart as possible. It seems unlikely
that the ancestral form would have needed a double proximal articulation of the hyomandibular and most probably there was a single head to the bone. Although a t this time
this is a matter for conjecture only, it is an interesting point to discuss because of the bearing it has on the nature of what is ‘primitivc’ or ‘advanced’ in Crossopterygii and on the
relationship between ontogeny and phylogeny. I t is xl-ellknown that fishesotherthan crossopterygians have but a single proximal articulation between hyomandibular and braincase : in the case of the bonyfishes this is dorsal to the jugular canal, while in elasmohranchs
it is ventral. From embryological evidence de Beer (1937) put forward the theory that the
hyomandibular primitively was double-headed and that each group, as it evolved,
retained only one of the original articulations. The most up-to-date embryological analysis
of the Rhipidistian skull, that of Jarvik (1%4), indicates that the two proximal articulations of the hyomandibular represent the original articulations between the supra- and
infrapharyngohyal and epihyal elements of the hyoid arch skeleton. Romer (1937)
suggested that the discovery of a double-headed hyomandibular in Crossopterygii supported this theory and concluded that the rhipidistian hyomandibular was therefore ‘most
probably primitive’. Similar arguments might be used to indicate that the persistent and
prominent notochord in the posterior division of the skull of Crossopterygii might also be
‘primitive’. However, all available evidence seetns to indicate that the double-headed
proximal articulation of the hyomandibular and the persistent intracranial notochord
were not present in the immediate ancestors of the Crossopterygii but are innovations
directly associated with the presence of the intracranial articulation and the establishment
of a particular (novel) set of intracranial kinetics. Thus the fact that these particular
features might be postulated as characters of an hypothetical vertebrate ancestor (in the
sense that they are morphologically intertnediate between other morphological tS.pes) and
the fact that they are manifestations in the adult of ontogenetic characters of living forms
do not in any way signify that they are ‘primitive’ in those forms in which they occur.
The discovery of the primitive dipnoan Dipnorh ynchus sussmilchi Etheridge, described
by Etheridge (1906),Hills (1933,1941; cf. Westoll, 1943b) and the subsequent description
of a related form D . lehmanni by Lehman & Westoll (1952) and Westoll (1949) raised
considerable hope that this genus might represent some form of link between the Crossopterygii and the Dipnoi. Very recently Dr K. 8 . TV. Campbell has made a preliminary
description (1965) of a second specimen of Dipnorhynchus sussmilchi which shows quite
clearly that far from possessing an amphistylic type of jaw suspension close to that of the
hypothetic crossopterygian ancestor postulated above, this early dipnoan had an extremely
solid palatal apparatus firmly fused to the braincase and lacking even the separate
parasphenoid ossification seen in the later Dipnoi. The overall similarity between this
species and D. lehmanni, especially with respect to the development of dental batteries on
the pterygoids, raises the possibility that in the latter form also the skull is essentially
autostylic. Thus a t the present time we know of no fossil fish which closely resembles a
crosaopterygian ancestor or which might serve to link together the Crossopterygii and
Dipnoi.
KEITHSTEWART
THOMSON,
F.L.S.
248
Some interesting observations may be made concerning the modifications of the rhipidistian cranial mechanisms to be seen in their phylogenetic offspring the Amphibia (here,
as in other discussions, we may usefully exclude from our considerations the highly
modified Recent members of the Class). The earliest known fossil Amphibia, the Upper
Devonian Ichthyostegalia, are remarkable in that they retain an indication of the division
of the braincase into two divisions (Save-Soderbergh, 1932 ; Jarvik, 1952) in the form o f a
suture behind the level of the basipterygoid articulation. They also retain a notochordal
canal. However, the dermal skull roof of ichthyostegalians, like that of all fossil Amphibia,
is a solid table and is firmly attached to the braincase. Thus there can have been no dorsoventral flexure of the skull like that of Crossopterygii. There is no indication whatsoever of
an occipital joint between skull roof and braincase in stegocephalians (cf. Bock, 1963).
Similarly, although the basipterygoid articulation seems to have been movable, the dermal
bones of the cheek were firmly bound by sutures to the posterior skull table. Apart from the
presence of the intracranial suture and the intracranial notochord, the structure of the
ichthyostegan skull is thus not very different from that of primitive Rhachitomi and the
liq
B
Fig. 17. Pulneogyrinus. Skull in left lateral view. A. Showing arrangement of the dermal bones.
B. Dermal bones removed and the positions of certain muscles, and the upper margin of the
mandible, restored (data from Panchen, 1964).
at., Anterior tectal; f., frontal; it., intertemporal; j., jugal; l., lachrymal; lig., ligamentous
connexion between squamosal and supratemporal; mx., maxilla; n., nasal; on., otic notch;
p., parietal; pf., postfrontal; pm., premaxilla; PO., postorbital; prf., prefrontal; q-j., quadratojugal; sq., squamosal; st., supratemporal; t., tabular. 1, 2, 3 and 4, adductor mandibulae
musculature; 5, levator arcus palatini muscle ; 6, depressor mandibular muscle. The arrows
indicate the direction of the pull of the muscles and the small circle marks the position of the
basipterygoid articulation.
Intracranial kirietics in Crossopterygii
249
possible cranial movements of these amphibians will be considered together in later
paragraphs. A note may be added here about the function of the notochord in ichthyostegids. It seems most probable that the notochord acted as a means of support for the
whole skull upon the trunk since there are no well-developed occipital condyles and if the
animal came out of the water i t is unlikely that muscular action alone could have supported the head.
It is in amphibians of the Order Embolomeri that we see a cranial mechanism most
closely resembling that of crossopterygian fishes. I n these aquatic amphibians the movable
basipterygoid articulation is retained and furthermore the posterior portion of the cheek
plate has only a ligamentous attachment to the dermal skull roof. In a recent study of the
Carboniferous genera Palaeogyrinus and Eogyrinus, Panchen (1964) has described the
cranial movements of embolomeres as consisting of a slight rotation of the palate in the
dorso-ventral plane, around the basipterygoid articulation. According to Panchen the
movement is developed by the anterior adductor mandibulae muscles, arising on the
ethmoid endocraniuni and inserting on the lower jaw essentially anterior to the basipterygoid articulation, and by the levator arcus palatini and depressor mandibulae muscles
whose line of action passes behind the basipterygoid articulation (see Fig. 17). However,
close consideration of Panchen’s study shows that in fact the movements of the palate a t
the basipterygoid articulation cannot strictly be described as a rotation. The embolomere
skull consists of a large braincase (essentially in one piece) firmly attached to the dermal
skull roof, the dermal bones of the cheek are loosely connected to the skull table posteriorly
and closely sutured to the skull table in front of the orbit. The palate seems to have been
firmly attached to the cheek, a t the maxilla and syuamosal. It is probably firmly connected
to the vomers and movably articulated with the braincase a t the basipterygoid process.
The braincase plus dermal skull roof and the palate plus cheek thus form two component
units which move relative to each other. However, it must be noted that while the basipterygoid joint between the two units seems freely movable, the movement possible a t the
anterior connexion of the two units must have been very slight-from Panchen’s descriptions it would seem that only slight downward and lateral movement of the palatelcheek
complex would be allowed, and this would perhaps have been even less than a t the same
position in the Rhipidistia.
It will be seen from the directions of the forces developed by the depressor mandibulae
and levator arcus palatini muscles and by the adductor mandibulae muscles, acting on
opposite sides of the basipterygoid articulation, that the palate essentially moves as a
lever hinged a t the anterior end. The actual articular surface of the basiphenoid is cupshaped and this suggests that rather than the palate moving directly dorso-ventrally
relative to the braincase, the cheek was also slightly expanded and contracted. Note
(Fig. 17) that the portions of the adductor mandibulae arising on the braincase (the only
portions of the adductors to take part in operating the kinesis) inserted on the anterior
portion of the primordial fossa of the lower jaw and thus, like the depressor mandibulae
muscles, delivered a diagonal pull. Only the levator arcus palatini acted in the vertical
plane.
Of the other Orders of fossil Amphibia, an apparently movable basipterygoid articulation is retained in Seymouriamorpha (which may be considered as having evolved from
Embolomeri), in the Ichthyostegalia (which are a primitive and independent development
from the early tetrapod stock) and in many members of the Order Rhachitomi. According
to Romer (1947) this is a characteristic of the more primitive members of the Rhachitomi.
In all of these forms, however, there is firm sutural connexion of the palate, cheek and skull
roof. Also there is no indication of a movable connexion between braincase and skull roof.
Two problems therefore arise from these observations : (1) what is the functional significance of the retention of an apparently kinetic skull in Embolomeri; and (2) what is the
functional significance of the retention of the basipterygoid articulation in other amphibians where the skull seems generally akinetic?
250
KEITHSTEWART
THOMSON,
F.L.S.
It is important to note that in the embolomeres the presence of a movable joint between
the palate and the braincase, and the possibility of movement of the suspensorial region
relative to, say, the occiput, plus the fact that the hyomandibular (stapes)takes no part in
the suspensorium, means that there is less direct skeletal support for the suspensorium
than in either the rhipidistian fishes or the amphibians of other Orders such as the Ichthyostegalia or Rhachitomi. I n the former the jaw suspension is hyostylic and in the latter
(even where an apparently movable basipterygoid joint is maintained, see below) the cheek
plate, palate and dermal skull are bound firmly together by sutures. I n the Embolomeri,
where the posterior portion of the cheek is only loosely attached to the dermal skull roof.
the support of the suspensorium must be in part dynamic-deriving from the strongly
developed depressor mandibulae and levator arcus palatini muscles. Presumably these
two sets of muscles are used alternately-the levators contracting when the depressors
are relaxed during closing of the mouth. Apart from any general tendency towards
disarticulation of the skull during biting, there is also a downward pull of the palate
delivered by the anterior division of the adductor mandibulae muscles. Although these
muscles would in fact have been in operation during the beginning of the ‘bite’ when the
gape was largest, it is most probable that the levator arcus palatini muscles would have
been contracted in order to provide bracing for the suspensorium during the whole of the
bite. This more or less dynamic function of the embolomere cranial mechanism, as Panchen
(1964) has noted, probably serves to accommodate the stresses and strains developed by
the jaw musculature. The jaw muscles in Embolomeri seem to have been particularly
large : Panchen suggests that this is because the Embolomeri were aquatic and the force
necessary to depress and raise the relatively massive lower jaw would be greater than in
terrestrial animals where the action of the mandibular depressors is supplemented by
gravity and the resistance of the surrounding medium is less. If this is true then it is possible that a dynamic system of support for the suspensorium may have been more efficient
than a rigid structural system. Thus in the embolomere line of evolution, while loss of the
intracranial articulation and the hyostylic jaw suspension prevent the development of
intracranial movements of significant dimension, the dynamic aspects of the ancestral
rhipidistian skull mechanism have been elaborated to a novel and important degree.
No such situation exists in the Rhachitomi, Ichthyostegalia or Seymouramorpha ;
indeed it is difficult to discover any positive attribute, kinetic or dynamic, of the movable
basipterygoid articulation in these forms. It is, however, possible to suggest one explanation for the retention of this articulation which concerns the general dynamics of the skull
and a specific shock-absorbing function. I n all these amphibians in which the basal
articulation is retained, even where the dermal skull roof is clearly sutured to the dermal
cheek plate, it is likely that the skull was not a perfectly rigid structure. A small but significant amount of general flexibility was present. Since the dermal skull roof and braincase
seem normally to be firmly interconnected, any slight bowing or compression of the cheek
region will be chiefly manifest a t the point of contact between the braincase and palate
(assuming that the palate and cheek always move together, as seems to be the case). If
there were even this small degree of flexibility between the skull roofing bones and thus
this small movement between the palate and braincase we must assume also that in all
probability the whole system is under some sort of general dynamic control from the
cranial muscles, even though the mechanical interconnexion of the various skeletal
components is still the principal factor in the structural integration of the skull.
I n those amphibians in which the basal articulation is completely lost and the palate and
braincase are sutured together, often in a complicated manner, the whole skull is more
massive and solidly built and presumably in these animals all vestiges of a dynamic factor
in the integration of the skull have been lost and a system of completely rigid connexions
of the dermal skull elements developed.
Thus in a general way we may trace through various lines of fossil Amphibia a pattern of
progressive modification of the kinetic and dynamic aspects of the original rhipidistian
Zntracranial kinetics in Crossopterggii
251
cranial mechanism. Some useful information concerning this problem may be gained from
study of the modification of the cranial kinesis in various genera of Rhipidistia. Thus, as
noted above, as the skull becomes more elongate, the angle through which the intracranial articulation may be moved is decreased. One of the principal differences between
the Rhipidistia and primitive Amphibia such as the ichthyostegans is in the proportions of
the skull-in particular the anterior division of the braincase is extremely elongated in the
amphibians. No doubt the functional significance of this trend toward elongation of the
snout region is connected, a t least in part, with increasing the length of the tooth row,
increasing the size of the gape, and thus of improving the predatory capabilities of these
animals. Throughout, this trend toward elongation of the anterior unit of the skull there
must have been a corresponding reduction in the potential relative movements in the
cranial kinesis, leading to a situation where the intracranial joint became redundant but
where, as we have seen the dynamic functions of the basic amphistylic jaw suspension was
still of great importance. This dynamic function apparently was only lost when other
factors, possibly connected with the adoption of a more terrestrial habitat and with certain
aspects of an increase in absolute size, necessitated the development of an entirely rigid
skull construction.
The limited kinetic abilities of the early Amphibia may thus be considered as secondary
modifications of the original (and far more complicated) crossopterygian kinesis. I n most
lines of Amphibia even this restricted kinetic ability is eventually lost. It is most interesting that no sign is seen in these early tetrapods of the advanced kinetic mechanisms
developed in the Reptilia, Aves and Mammalia. For this reason in the preceding account I
have deliberately avoided the use of the specialized terminology customarily applied to
these more advanced mechanisms (except, of course, the general term ‘kinesis’).The literature pertaining to these systems is considerable and no attempt will be made to summarize
it here. However, although treatment of these systems does not fall within the compass of
this paper, a few brief notes of comparison may be included here. It will be seen that a
limited analogy may be made between the mesokinetic axis of the skull of Reptilia such as
lizards (Frazetta, 1962) and the axis of the intracranial joint of Crossopterygii. The
maxillary segment of the lizard skull has no direct equivalent in Crossopterygii, although
what we have termed the anterior unit of anterior endocranium plus anterior skull roof,
plus cheek and palate, closely resembles this unit. Similarly the occipital segment in lizards
resembles, but does not exactly correspond to the posterior.unit of posterior endocranium
plus posterior skull roof in Crossopterygii There is no metakinetic joint in crossopterygian
fishes. The basal articulation is apparently the only feature which is fully homologous in the
two systems. The reptiles probably had their origin from within the anthracosaur line of
Amphibia. The presence of a movable basipterygoid articulation in this ancestral stock
was probably of great significance, for it demonstrates that there was a continuity of
intracranial mobility between amphibian and reptile which kept the way open for the later
development de novo of the mesokinetic and metakinetic articulations and a second system
of intracranial kinesis.
ACKNOWLEDGEMENTS
A considerable portion of the work involved in this study was done a t University College
London and was supported by N.A.T.O. Felowship B/RF/OGl. It is a pleasure to scknowledge the generous hospitality of Professor M. Abercrombie and other colleagues a t
University College, and of Dr E. I. Whitc of the British Museum (Natural History). I am
grateful to Dr White, Professor A. S. Roiner (Harvard University), Dr C. D. Waterston
(Royal Scottish Museum) and Professor D. M. S. Watson for the loan of specimens.
252
KEITHSTEWART
THOMSON,
F.L.S.
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ADDENDUM
Subsequent t o the completion of this paper I have had the good
fortune to be ablc to study a fresh specimen of the living coelacanth
Latimeria chalumnae Smith (ser Thomson, 1966). It was gratifying
to be able to see that the nature of the possible movements of the
skull, jaws and intracranial joint in the intact fish corresponds
precisely with that predicted from the skeletal restorations.
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