Download The structure and development of the jaw adductor musculature in

zoological Journal of the Linnean Society (19901, 98: 27-62. With I 1 figures
The structure and development of the jaw
adductor musculature in the turtle Chelydra
serpen tina
0. RIEPPEL, F.L.S.
Palaontologisches Institut und Museum der Universitat, Kunstlergasse 16,
CH-8006 Zurich, Switzerland
Received October 1988, accepted for publication March 1989
The investigation of the development of the trigeminal jaw adductor musculature in the turtle
Chelydra serpenha documents the early aggregation of muscle rudiments around the innervating
nerve branches, probably a consequence of inductive interaction. This may rxplain the early
continuity of the intramandibularis with the intermandibularis muscle. Several aspects of muscle
development differ in the turtle as compared to lizards. These differences highlight the fact that
conjectures of homology, based on a static topographical correspondence of adult structures, cannot
capture the dynamics of the developmental process. T h e intramandibularis muscle of turtles.
comparable to that of crocodiles, represents a plesiomorphous structure which is not homologous to
the intramandibularis muscle of lacertoid lizards, a derived feature of the Lacertoidea. A derived
feature of the chelonian jaw adductor musculature is the posterodorsal expansion of the external
adductor along a supraoccipital crest, developing according to a pattern of Haeckelian
recapitulation. Muscle development serves to corroborate the concept of a monophyletir Eureptilia.
including diapsids and synapsids, as opposed to the (paraphyletic) Anapsida. T h e impact of the
differentiation of the external adductor into a pulley system on cranial kinesis is analysed in
biomechanical terms.
KEY WORDS:
Chelonia
~
ontogeny
~
phylogeny
CONTENTS
Introduction .
.
.
.
.
.
.
.
.
Material and methods .
. . . . . .
.
Description of the fully differentiated stage .
Description of developmental stages
.
.
.
. . . .
Patterns of early development .
Subsequent development of the external adductor
Subsequent development of the internal adductor
.
Drvelopmcnt of the m. intramandibularis .
Status of the Chelonia within the Sauropsida .
Secondary cartilagc and cranial kinesis .
.
.
Conclusions .
.
.
.
.
.
.
.
.
Acknowledgements
. . . . . . .
.
.
.
.
.
.
.
.
.
References
.
.
.
Abbreviations used in the figures .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
27
. 28
. 29
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
. 51
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
. 53
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
. 34
. 55
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
32
52
_-
Ji
58
. 60
.
.
.
.
.
.
.
.
.
.
.
60
.
.
.
.
.
.
.
.
.
.
. 62
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
INTRODUCTION
The first illustration of a superficial view of the jaw adductor musculature in
Chelydra serpentina was given by Adams (1919) in his comprehensive memoir on
+
002&4082/90/010027 36 $03.00/0
27
0 1990 The Linnean Society of London
28
0. RIEPPEL
the phylogeny of the jaw muscles in fossil and recent vertebrates. However, the
illustration is schematic to an extent that it provides no useful information of
fibre arrangements or detailed muscle architecture. Ogushi (1913) was the first
author to describe the jaw adductors of a turtle, Trionyxjaponicus, in any detail,
although his terminology is by now outdated and his figures still remain
diagrammatic. Lakjer (1926), in his pioneering work on the trigeminal jaw
adductors of the Sauropsida, based his description of the chelonian structure on
a variety of taxa which did not include Chelydra. His description was to set the
stage for all subsequent work in the field such as that by Lubosch (1933);
Poglayen-Neuwall (1953) and Schumacher (summarized in 1973). None of these
papers addresses details of jaw adductor muscle architecture in Chelydra serpentina,
although the species was included in the sample investigated by PoglayenNeuwall (1953). It was left to Dr E. S. Gaffney to improve the situation with a
detailed investigation of Chelydra, laid down in a manuscript which was never
published, but which he has allowed me to see.
Knowledge of the ontogenetic development of the jaw adductor muscles of
turtles is even more deficient, the only descriptions being those of Edgeworth
( 1935), based mainly on Chrysemys and Chelydra. Edgeworth's account remains
restricted to the description of early developmental stages, and presents little or
no information on the continuing differentiation of the trigeminal jaw adductor
musculature into the adult condition. It was therefore felt desirable to provide a
detailed analysis of the development of those muscles in Chelydra serpentina,
preceded by an account of the adult structure in order to render the description
of embryonic stages more intelligible. This work will bear on a number of
problems of turtle myology discussed throughout the earlier literature quoted
above such as the nature of the internal adductor, its relation to the posterior
adductor, and the origin of the intramandibularis muscle. It will also provide a
basis for comparison with the structure and development of the jaw adductors in
lepidosaurian reptiles as described on earlier occasions (Rieppel, 1987a, 1988).
Beyond these immediate issues there is more to learn from a developmental
approach to the differentiation of the jaw adductors in a turtle. Lakjer (1926)
raised the old and controversial question whether the configuration of the
chelonian dermatocranium, corresponding to the primitive anapsid condition,
must not rather be viewed as a secondary development (see also Kilias, 1957).
While cladistic analysis strongly supports the anapsid status of turtles (Gaffney &
Meeker, 1983), the question as to why the reduction of the dermatocranium
proceeded along different pathways in turtles as opposed to diapsid reptiles still
remains unanswered.
MATERIAL AND METHODS
The present study is based on the dissection of the head of a juvenile specimen
of Chelydra serpentina (MBS 15266). The results of this dissection were checked
against macroscopically sectioned heads of four adult specimens
(AMNH DVP ESG 001-004) which formed part of the material on which
Dr E. S. Gaffney based his earlier study of the jaw adductors in Chelydra. The
investigation of the development of the jaw adductor musculature was based on
a series of specimens representing the developmental stages 12 to 25 as defined by
Yntema (1968). The heads were serially sectioned at a plane transverse to the
JAW MUSCLES OF T U R T L E
29
tectum opticum at a thickness of 15 pm, and stained after BODIAN (see
Rieppel, 1976). The slides are now housed at the Natural History Museum,
Basle (MBS).
DESCRIPTION OF T H E FULLY DIFFERENTIATED STAGE
The skull of Chelydra serpentina is characterized by a moderate embayment of
the ventral margin of the cheek region and by a rather deep embayment of the
posterior margin of the skull roof (Gaffney, 1972). This pattern of reduction of
the dermatocranium results in the formation of a ‘temporal arcade’, composed of
the postorbital, jugal and squamosal bones, bracing the otic region against the
facial region of the skull (Fig. 1A). The posterior embayment of the
dermatocranium gives way to the bulging muscle mass of deep layers of the
external adductor ( profundus- and medialis-layers) which expand in a posterior
direction (Fig. lB), taking their origin from the posteriorly projecting crista
supraoccipitalis of the supraoccipital bone (Gaffney, 1972).
Upon removal of the skin the posterior part of the deep layer of the external
adductor can be seen to be covered superficially by superficial epaxial neck
musculature (m. spinalis capitis) (Fig. 1A). This is a remarkable observation
since in those squamate reptiles (burrowing lizards and snakes) which also show
a posterior expansion of deep layers of the external jaw adductors, the latter
come to lie superficially to the epaxial neck musculature (Rieppel, 1981a, 1984a;
see also further discussion below). The large depressor mandibulae takes it5
origin from the posterior part of the lateral surface of the squamosal and
descends to the posterior tip of the lower jaw (Fig. 1A).
The ventral embayment of the cheek region is almost completely covered by
the rictal plate (Fig. 1A). Deep to it, superficial fibres of the external adductor
insert into the dorsolateral aspect of the lower jaw. Indeed the insertion of
superficialis-layer of the external adductor into the lateral aspect of the lower jaw
is quite substantive, and may have been made possible by the ventral
embayment of the cheek region: the latter would thus represent a functional
analogue to the loss of the lower temporal arch in diapsid reptiles (Rieppel &
Gronowski, 1981 ) .
Removal of the ‘temporal arcade’ (postorbital, most of the squamosal and
most of the quadratojugal bones) exposes the rictal plate to its full extent. Serial
sections of a hatchling Chelydra show that no muscle fibres insert directly into its
dorsal edge. Instead, the rictal plate merges into a temporal fascia colered
superficially by the temporal bones, and itself covering the external adductor as
it extends into the dorsal embayment of the dermatocranium. T h e temporal
fascia is attached to the medial surface of the ‘temporal arcade’ along the suture
between the postorbital and jugal. The superficialis-layer of the external
adductor originates from the medial (inner) surface of the temporal fascia at the
level of the dorsal marginal zone of the postorbital as well as of the anterior part
of the squamosal bone (Fig. 1B). Anterior fibres pass anteroventrally to insert
into the lateral surface of the base of the bodenaponeurosis and of the corner of
the oesophagus (lined by thick connective tissue) deep to the rictal plate; more
posterior fibres descend more or less vertically to the lower jaw.
No muscle fibres take their origin from more ventral marginal portions of the
medial surface of the temporal fascia below the ‘temporal arcade’. This can be
0. RIEPPEL
30
ameD
amep
'PC
ames
amep
ta
Figure 1. The fully differentiated jaw adductor musculature in a juvenile specimen of Chelydra
serpentina (MBS 15266). (Explanations of abbreviations in Appendix.)
explained on functional grounds, since fibres originating from that area would be
so short that their limited excursion range would severely restrict gape, in
particular if these short fibres were vertically orientated. The ventral embayment
of the cheek region does therefore not reduce the potential area of origin of jaw
adductor muscle fibres.
As can be seen in superficial view (Fig. 1A-D) already, there is an
individualized slip of muscle fibres taking its origin from the dorsomedial aspect
of the squamosal bone, dorsal to the widely exposed paroccipital process. This
JAW MUSCLES OF TURTLE
31
more lateral (superficial) slip of muscle, lying lateral to the posterodorsal
expansion of the bodenaponeurosis, passes anteriorly, turns ventrally in front of
the paroccipital process and merges into the medialis-layer of the external
adductor (Fig. lC, D). It inserts into the lateral surface of the posterior part of
the central tendon (bodenaponeurosis) deep to the superficial fibres which take
their origin from the posteromedial part of the ‘temporal arcade’ (squamosal) .
The subdivision of the external adductor into a superficialis-, a medialis- and a
profundus-layer goes back to Lakjer (1926) who believed it to be characteristic
of all Sauropsida. The superficialis-layer is defined by its insertion into the lateral
surface of the lower jaw; the medialis-layer inserts by definition into the lateral
surface of the central tendon (bodenaponeurosis) of the external jaw adductor;
the profundus-layer finally relates to the medial surface of the bodenaponeurosis.
As was noted by Gaffney (unpublished), the distinction of separate layers of the
external adductor in Chelydru is not very clearcut. The fibres which take their
origin from the medial surface of the ‘temporal arcade’ and which insert into the
lateral surface of the lower jaw (superficialis-layer), gradually merge into deeper
muscle layers which take their origin from the lateral part of the anterior slope of
the quadrate and which insert into the lateral surface of the bodenaponeurosis
(medialis-layer) . The main distinction between superficial and medial layers is a
reorientation of the fibre direction: the insertion into the lateral surface of the
lower jaw is more or less vertical, that into the lateral surface of the
bodenaponeurosis is anteroventrally inclined. The transition, however, is again
fairly gradual.
The bodenaponeurosis shows a broad base attached to the dorsomedial rim of
the lower jaw. Anteriorly it is connected to the corner of the mouth by thick
connective tissue. It combines with the latter structure to form a thick tendinous
raphe lying lateral to the processus pterygoideus externus (Gaffney, 1972), and
receiving into its anterior surface deep anterior fibres of the external adductor
which originate from the posterodorsal area of the orbit (lower surface of deep
parts of the postorbital bone; Fig. 1D). The bodenaponeurosis (central tendon) is
drawn out in a posterodorsal direction across the paroccipital process, separating
the medialis- and profundus-layers of the external adductor dorsal to the otic
region and providing a pinnate structure for the posterior extension of the
external adductor (Fig. lC, D).
The main part of the external jaw adductor is represented by the profunduslayer (Schumacher, 1973). The muscle is a well individualized unit of
complex pinnate structure (Fig. lC, D ) , relating to the central tendon
(bodenaponeurosis) which extends far posteriorly within the muscle mass: The
muscle itself expands in a posterodorsal direction across the paroccipital process,
taking its origin from the posterodorsal part of the descending flange of the
parietal, and from the entire lateral surface of the crista supraoccipitalis.
Removal of the profundus-layer of the external adductor along with the
bodenaponeurosis exposes the posterior and internal adductor (Fig. 1E). Lakjer
(1926) defined the posterior adductor by its position behind (and deep to) the
mandibular branch of the trigeminal nerve, while the interior adductor is
defined by its position deep to the maxillary branch of the trigeminal nerve. This
distinction is not very clearcut in Chelydru. Those muscle fibres which take their
origin from the medial part of the anterior slope of the paroccipital process (deep
part of quadrate and prootic) and which insert into the dorsomedial aspect of the
32
0. RIEPPEL
lower jaw behind the passage of the mandibular nerve into the Meckelian fossa
must, on topological grounds, represent the posterior adductor. It was identified
as the posterior head of the posterior adductor (‘amp’ in Fig. 1E) by Lakjer
( 1926), Poglayen-Neuwall ( 1953) and Schumacher ( 1973).
In front of the mandibular branch of the trigeminal nerve there is a thin
muscular layer taking its origin along the descending flange of the parietal,
extending anteriorly up into the posterodorsal corner of the orbit. The origin of
that muscle is lined dorsally by the temporal artery (stapedial artery of Albrecht,
1976). This muscular layer is pierced in its posterior dorsal part by the maxillary
branch of the trigeminal nerve which continues its course anteriorly into the
orbit in a superficial position. There is no doubt that this part of the muscle layer
lying deep to the trigeminal nerve branch must represent, on topological
grounds, the pseudotemporalis muscle, that is part of the internal adductor.
There remains some equivocation, however, in the homologization of those fibres
which take their origin from the dorsal margin of the trigeminal foramen i.e.
dorsal to the mandibular branch but behind the passage of the maxillary branch
of the trigeminal nerve (‘ampa’ in Fig. 1E). These fibres were identified as the
anterior head of the posterior adductor by Lakjer ( 1926), Poglayen-Neuwall
(1953) and Schumacher (1973), while on topological grounds they could just as
well represent a posterior extension of the pseudotemporalis muscle. The latter
interpretation would imply a slight anterior shift of the passage of the maxillary
nerve relative to the pseudotemporalis muscle as compared to other reptiles, or
conversely, a posterior extension of the pseudotemporalis muscle across the
maxillary nerve. The problem can only be solved by developmental studies.
The main (dorsal) part of the pterygoideus muscle lies in the posteroventral
part of the orbit, taking its origin from the ventrolateral aspect of the braincase
and from the internal (dorsal) surface of the pterygoid. The ventral portion of
the pterygoideus muscle invades the ventral surface of the pterygoid. More
posterior fibres of the pterygoideus muscle take their origin from a tendinous
aponeurosis which is attached to the processus pterygoideus externus (Gaffney,
1972). The fibres of the pterygoideus muscle converge into a central insertional
tendon which is attached to the inner edge of the lower jaw, close to the jaw
articulation. In its anterior part, this insertional tendinous sheet lies essentially
dorsal to the mass of the pterygoideus muscle, and receives into its dorsal surface
fibres from the deeper part of the pseudotemporalis muscle.
The levator or protractor pterygoidei muscles are absent in postembryonic
turtles (Schumacher, 1973: 104); their absence must be correlated with the
akinetic turtle skull. The pterygoid becomes immovably fused to the crista
basipterygoidea of the basicranium (basal plate, ossifying as basisphenoid)
during embryonic development (Rieppel, 1977). However, embryonic rudiments
of the constrictor internus dorsalis musculature have been described by Fuchs
(1915) and Edgeworth (1935) as will be further discussed.
DESCRIPTION OF DEVELOPMENTAL STAGES
Stage 13
In the material at hand this represents the first stage at which the aggregation
of muscular rudiments becomes discrete. The neurocranium is not yet laid down
in cartilage. The first cranial element which has made its appearance is the
JAW MUSCLES OF TURTLE
33
C
Figure 2. Section5 through the head of Chelydru serpentinu at stage 13 (scries No. 586). Scalp
bar= 1 rnm. (Explanations of abbreviations in Appendix.)
palatoquadrate, which is still in a procartilaginous stage of development,
however.
The muscle rudiment consists as yet of little more than a cell aggregation
(Fig. 2A-C), wrapping around the mandibular branch of the trigeminal nerve
and restricted to a position behind the corner of the mouth and ventrolateral to
the anlage of the palatoquadrate. This cell aggregation is absolutely
homogeneous: there is no possibility to distinguish an externus- from an internusrudiment. Similarly it is impossible to identify a rudiment of the constrictor
internus dorsalis group of muscles. Edgeworth (1935: 56) described such a
rudiment lying at the tip of the ascending process of the palatoquadrate in the
embryonic head of Chelydra, but the latter is not yet differentiated at the
developmental stage under consideration.
Of particular interest is a ventral extension of the anlage of the trigeminal jaw
adductors just posteroventral to the passage of the mandibular nerve branch.
This extension curves downwards in a medioventral direction, meeting a
medioventral cell aggregation which represents the first anlage of the
intermandibularis muscle (Fig. 2C). At a later stage of development, the ventral
extension of the early rudiment of the trigeminal jaw adductors will give rise to
the intramandibularis muscle. Stage 13, therefore, documents an early
continuity of the anlagen of the intermandibularis and intramandibularis
muscles which was also figured by Edgeworth (1935: 423, fig. 555).
This piece of information is noteworthy in the light of the fact that at this early
stage of development, the cell aggregation representing the earliest rudiments of
the trigeminal jaw musculature tend to centre around the mandibular branch of
the trigeminal nerve and its derivatives. Should this correlation prove to be a
causal and not merely a descriptive one, it might also explain the early
continuity of the intermandibularis and intramandibularis muscles. These are
innervated by branches taking their origin, with a common root, from the
posterior aspect of the alveolar nerve, that is from the anterior continuation of
the mandibular nerve (Poglayen-Neuwall, 1953; Schumacher, 1973).
Stage 14
This stage differs from the preceding one mainly by an increase in volume of
the muscle rudiment(s). The neurocranium has still not differentiated in the
34
0. RIEPPEL
orbitotemporal region. The palatoquadrate bar still remains in a
procartilaginous stage of differentiation, but has developed more clearly
demarcated boundaries. An ascending process is not yet distinct. Meckel’s
cartilage has now made its appearance.
The trigeminal jaw adductor rudiment is still concentrated around the
mandibular branch of the trigeminal nerve. At this stage of development, the cell
aggregation lying medial to the mandibular nerve reaches further anteriorly
than that lying on the lateral side of the nerve. The medial cell aggregation,
representing the prospective internus-rudiment, reaches to a level distinctly in
front of the corner of the mouth; it had already done so to a very limited degree
in the preceding stage, but the difference has now become much more
pronounced. The cell aggregation lying lateral to the mandibular nerve and
representing the prospective externus-rudiment remains restricted to a position
behind the corner of the mouth. It is this part of the muscle rudiment which
shows the greatest increase in volume, bulging laterally and raising up to a level
laterodorsal to the palatoquadrate bar behind the Gasserian ganglion.
Behind the passage of the trigeminal (mandibular) nerve down to Meckel’s
cartilage, the cell aggregation of the prospective internus- and externusrudiments remains fully homogeneous. At this level, the cell aggregation extends
downward lateral and ventral to Meckel’s cartilage. The early anlage of the
intramandibularis muscle retains only faint vestiges of its earlier continuity with
the intermandibularis muscle rudiment, however, Posteriorly, the homogeneous
anlage of the trigeminal jaw adductors reaches up to the quadrate cartilage, in
front of which it comes to an end.
Stage 15
This stage differs from the preceding one not only by an increase in volume of
the muscle rudiments, but also by some advance in the differentiation of their
shape. The neurocranial wall is still not laid down in the orbitotemporal region,
but the palatoquadrate bar and Meckel’s cartilage are now differentiated.
The palatoquadrate forms a rudimentary ascending process in front of the
Gasserian ganglion (Fig. 3A). The cell aggregation lying medial to the
mandibular branch of the trigeminal nerve extends anteriorly to a level
distinctly in front of the corner of the mouth. This aggregation, relating to the
lateral aspect of the ascending process of the palatoquadrate, represents the
prospective pterygoideus muscle ventrally and the prospective pseudotemporalis
muscle dorsally. The homogeneity of the cell aggregation prevents the
identification of separate compartments at this stage of development, however.
A separate rudiment of the constrictor internus dorsalis group of muscles, lying
at the dorsal tip of the ascending process of the palatoquadrate according to
Edgeworth (1935)’ is not identifiable.
At the level of the passage of the mandibular branch down to Meckel’s
cartilage, just behind the corner of the mouth, the cell aggregation of the
trigeminal jaw adductor musculature is still absolutely homogeneous and
continuous (Fig. 3B). Yet, continued growth and in particular the differentiation
of shape allows the demarcation of prospective muscle compartments. The
anlage of the jaw adductors extends medioventrally below the palatoquadrate
bar, there forming a distinct medioventrally projecting ‘rim’ running in a
JAW MUSCLES OF TURTLE
35
A
Figure 3. Sections through the head of Chelydru serpentinu a t stage 15 (series No. 588). Scalr
bar= 1 mm. (Explanations of abbreviations in Appendix.)
longitudinal direction and representing the future pterygoideus muscle
(Fig. 3B, C).
The cell aggregation lateral to the mandibular nerve has further increased in
volume and expanded dorsally to a level well above the palatoquadrate bar
(Fig. 3B): it represents the prospective external adductor, with the
posterodorsally expanding portion corresponding to the future profundus-layer
of the external adductor. Still further posteriorly, posteromedial and
posteroventral to the mandibular nerve, the anlage of the trigeminal jaw
adductors extends ventrally to a position lateral and ventral to Meckel’s
cartilage (Fig. 3C). This part represents the prospective intramandibularis
muscle which is now narrowly separated from the developing intermandibularis
muscle. Still further posteriorly, the muscle rudiment extends up to the quadrate
cartilage in front of which it comes to an end.
Stage 16
The palatoquadrate and Meckel’s cartilage are well-delineated, being
composed of mature chondrocytes. The basicranium, in particular the sella
turcica underlying the hypophysis, is well mapped out, but there are only vague
indications of the lateral braincase wall in the orbitotemporal region,
The muscle (internus-) rudiment lying medial to the mandibular branch of
the trigeminal nerve has expanded a little further in a n anterior direction, now
reaching to a level slightly in front of the ascending process of the
palatoquadrate. This anterior extension corresponds to an anterior growth of the
prospective pterygoideus muscle. A differentiation of the pterygoideus from the
pseudotemporalis muscle is still impossible at a level lateral to the ascending
process. Likewise, there is no indication of a separate constrictor internus dorsalis
rudiment.
I n contrast to the preceding stage, the cell aggregation lying lateral to the
mandibular nerve has also expanded slightly beyond the latter in a n anterior
direction, so that just behind the corner of the mouth the internus- (medial) and
externus- (lateral) rudiments appear as separate units (Fig. 4A). T h e distinction
becomes blurred at the ventral extremity of the muscle rudiments.
Slightly further back, a t the level where the mandibular nerve passes ventrally
towards Meckel’s cartilage, the development of the muscle rudiments shows little
36
0. RIEPPEL
h
Figure 4. Sections through the head of Chelydru serpentznu at stage 16 (series No. 589). Scale
bar= 1 mm. (Explanations of abbreviations in Appendix.)
advance over the preceding stage except for some growth and concomitant
increase in volume. The prospective pterygoideus muscle now forms a distinct,
medially bulging condensation ventral to the palatoquadrate bar which remains
continuous with the remainder of the anlage of the other trigeminal muscles. The
externus-rudiment rises along the lateral aspect of the mandibular nerve to a
level well above the palatoquadrate bar, but is does not yet reach the level of the
exit of the maxillary and mandibular branches from the Gasserian ganglion.
Behind the passage of the mandibular nerve through the muscle rudiment,
continuity and homogeneity still prevail within the cell aggregation. The ventral
extension, representing the prospective intramandibularis muscle, now reaches
to the ventrolateral edge of Meckel’s cartilage, but no longer covers the latter’s
ventral aspect. As the developing intermandibularis muscle relates to the
medioventral edge of Meckel’s cartilage, the two muscle rudiments are now
completely separated. Still further posteriorly differential growth has added to
the differentiation of the muscles (Fig. 4B). The medioventrally bulging anlage
of the pterygoideus muscle continues caudally along the medioventral aspect of
the quadrate cartilage. I t thus becomes fully separated from the externusrudiment which has further expanded in a posterodorsal direction, now reaching
to a level above the quadrate cartilage but not yet stretching beyond it. This is
the first indication of the extension of the external jaw adductor in a
posterodorsal direction, reaching across the quadrate and the otic region in later
stages of development.
Stage 27
This stage of development is characterized by a distinct advance in cell
differentiation. In particular, there is a beginning indication of fibre direction in
JAN’ MUSCLES OF T U R T L E
Figure 5. Sections through the head of Chelydra rerpentino at stagr 1 7
b a r = 1 mm. ‘Explanationsof abbreviations in Appendix.;
37
~ s r r i r sN o .
590: Scalr
the various compartments of the muscle rudiments, and the first indication of the
central tendon (bodenaponeurosis) becomes apparent. The basicranium as well
as the lateral sidewall of the braincase are now distinct in the orbitotemporal
region. The dorsum sellae, as well as the palatoquadrate bar and Meckel’s
cartilage, are fully chondrified. However, there remains a wide open prootic
incisure, within which lies the Gasserian ganglion. Behind the eyeball a n
aggregation of dark staining cells marks the beginning of the development of
(dermal) postorbital bone, the first element of the dermatocranium to make its
appearance. The first ossification centre remains small, however, and widely
separated from the developing musculature (Fig. 5A).
The internus-rudiment, lying medial to the maxillary and mandibular
38
0. RIEPPEL
branches of the trigeminal nerve, has further expanded in an anterior direction.
The anlage of the pterygoideus muscle now reaches distinctly beyond the
ascending process of the palatoquadrate and beyond the anlage of the externusrudiment, but differential growth has brought about proportional changes in the
head to the effect that the anterior tip of the internus-rudiment lies a t level with
the corner of the mouth. Lateral to the ascending process the differentiation of
fibre direction permits the identification of the medioventrally positioned
pterygoideus muscle and of the more dorsally and laterally positioned
pseudotemporalis muscle (Fig. 5A). The latter muscle does not expand dorsally
beyond the tip of the ascending process, and, more posteriorly, the anlage of the
pseudotemporalis muscle remains restricted to a level below the exit of the
maxillary and mandibular branches from the Gasserian ganglion (Fig. 5B).
In contrast to earlier stages, the anlage of the external adductor has also
expanded to a level well in front of the passage of the mandibular nerve down to
Meckel’s cartilage (or rather, differential growth of the embryonic head has
displaced the passage of the mandibular nerve posteriorly, relative to the corner
of the mouth). The externus-rudiment remains restricted to a level behind the
corner of the mouth, distinct from the internus-rudiment (Fig. 5A).
Where the mandibular nerve passes between the internus- and externusrudiment, the first indication of a central tendon (bodenaponeurosis) becomes
distinct through cell differentation within the medioventral portion of the
externus-rudiment (Fig. 5B). This anlage of the central tendon fades away in
front of the mandibular nerve as it becomes indistinguishable from a voluminous
cell aggregation surrounding the corner of the mouth and of the oesophagus.
The anlage of the bodenaponeurosis has no connection with Meckel’s cartilage.
Posteriorly, the cell differentiation of the central tendon continues within the
externus-rudiment to a level shortly in front of the quadrate cartilage (Fig. 5C),
tapering off before the muscle expands in a posterodorsal direction. The
externus-rudiment now reaches posterodorsally beyond the quadrate cartilage,
extending dorsal to the latter and laterodorsal to the prominentia canalis
semicircularis horizontalis of the otic capsule to a level well above the stapes.
The prospective intramandibularis muscle is continuous with the ventral part
of the pseudotemporalis muscle medial and posterior to the downward passage of
the mandibular nerve (Fig. 5B). The muscle rudiment has grown anteriorly
along the lateral aspect of Meckel’s cartilage behind the corner of the mouth
(Fig. 5A).
As noted before, the internus-rudiment remains restricted to below the exit of
the maxillary and mandibular branches of the trigeminal nerve from the
Gasserian ganglion (Fig. 5B). Behind the passage of the mandibular branch
down towards Meckel’s cartilage, the internus-rudiment continues along the
lateral (m. pseudotemporalis, in continuity with the intramandibularis muscle)
and ventral (m. pterygoideus) aspect of the palatoquadrate bar. Where the latter
expands into the quadrate cartilage, which in turns forms the mandibular joint
with Meckel’s cartilage, the internus-rudiment becomes subdivided (Fig. 5C).
The prospective pterygoideus muscle continues along the medioventral aspect on
the quadrate cartilage for some considerable distance, whereas the lateral
portion of the internus-rudiment covers the anterolateral surface of the quadrate
cartilage: this portion represents the posterior part of the prospective posterior
adductor (Fig. 5C).
JAW MUSCLES OF TURTLE
39
vc I
CI
,
cr b
ci
\
-
VII
A
B
exm
vc 1
cr b
VII
CI
C I
/
rnc
D I
Figure 6. Srctions through thc hcad of Chelydra serpentina at stage 18 8serit.a No. 591 ' . Scalc
b a r = 1 mm. Explanation, of abhrrviations in Appendix.)
Stage 18
At this stage the neurocranium approaches the peak of its development in the
antotic region (Rieppel, 1976). The development of the dermatocranium has
likewise progressed over the preceding stage. The postorbital ossification, lying
posterior to the eyeball, has increased in size, but still remains separated from the
developing musculature. It is still represented by a single ossification centre
(Fig. 6A). At the back end of the skull, the squamosal has made its appearance
as an ossification capping the posterior part of the dorsolateral aspect of the
quadrate cartilage. Dorsal to the Gasserian ganglion, the parietal bone makes its
first appearance in the form of an ossification centre marking its descending
flange (secondary lateral braincase wall, Fig. 6C).
40
0. RIEPPEL
All along the medioventral aspect of the palatoquadrate bar the pterygoid
bone has begun to ossify. It forms a rather narrow strip of bone, flat anteriorly
but of a more or less triangular cross-section posteriorly. Shortly behind the
eyeball, the anterior tip of the palatoquadrate cartilage is deflected laterally.
This is the area where the external process of the pterygoid (the processus
pterygoideus externus of Gaffney, 1972, corresponding to the transverse
pterygoid flange of more generalized reptiles) will develop during later stages.
The prearticular bone has begun to make its appearance medial to the posterior
part of Meckel’s cartilage (Fig. 6C).
The internus-rudiment extends anteriorly well beyond the ascending process
of the palatoquadrate. The separation of the dorsal pseudotemporalis portion
from the medioventral pterygoideus muscle is now possible a t this anterior level
on the basis of fibre direction (Fig. 6A). As in the preceding stage, the internusrudiment extends anteriorly beyond the externus-rudiment, but proportional
changes in the head have the effect that the anlage of the pterygoideus muscle no
longer reaches to the corner of the mouth.
The externus-rudiment has itself also further extended anteriorly, tapering off
along the corner of the oesophagus but remaining restricted to a position behind
the corner of the mouth (Fig. 6A). The difference of the anterior extension of the
internus- and externus-rudiments has thus become reduced, although it must be
admitted that the precise anterior delineation of the externus-rudiment is
difficult to establish due to a dense cell aggregation surrounding the corner of the
oesophagus.
At the level lateral to the ascending process of the palatoquadrate, the
internus- and externus-rudiments form well individualized units (Fig. 6B). The
pterygoideus muscle develops from the medioventral part of the internusrudiment. The anlage of the pseudotemporalis muscle has become applied to the
lateral aspect of the ascending process (in the preceding stage it remained
separated from the palatoquadrate by a narrow strand of connective tissue).
The externus-rudiment is well defined and embodies the anlage of the
bodenaponeurosis. Its medioventral demarcation still remains blurred by a dense
cell condensation surrounding the corner of the oesophagus. Medial to the
mandibular branch, between the nerve and the lateral aspect of Meckel’s
cartilage, and below the externus-rudiment, lies the anterior portion of the
intramandibular muscle (Fig. 6B).
At the dorsal tip of the ascending process of the palatoquadrate, just lateral to
the lateral head vein, lies an ill-defined cell agglomeration (Fig. 6B). It remains
doubtful, however, whether this loose aggregation does indeed represent the
constrictor internus dorsalis rudiment described by Edgeworth (1935). If it does,
it is a transient structure which will soon disappear again.
More posteriorly, there is little advance over the differentiation reported for
the preceding stage of development. The internus- and externus-rudiments have
both further expanded in a posterodorsal direction. The internus-rudiment now
rises to a level above the dorsal tip of the ascending process of the
palatoquadrate. More posteriorly, but still in front of the mandibular branch of
the trigeminal nerve, the rudiment extends dorsally to a level slightly above that
of the exit of the nerve from the Gasserian ganglion (Fig. 6C). As the muscle
rudiment approaches the nerve, however, it becomes lower again, with the
mandibular branch curving around its dorsal edge on its way down to Meckel’s
JAW AMMUSCLESOF 1 U R T L E
41
cartilage. Fibres with a vertical orientation, lying immediately deep to the
mandibular nerve, are still continuous with the ventrally situated
intramandibularis muscle. More posteriorly, these lateral fibres of the internusrudiment extend onto the anterolateral aspect of the quadrate cartilage, thus
providing the posterior head of the presumptive posterior adductor. At the
mandibular articulation this muscle anlage becomes separated from the
pterygoideus muscle which extends posteriorly along the medioventral aspect of
the quadrate cartilage and below the developing pterygoid bone. T h e latter
becomes applied against the medial surface of the quadrate for a short distance.
The externus-rudiment incorporates the anlage of the central tendon
(Fig. 6B, C). The latter merges anteroventrally into a dense cell aggregation
surrounding the corner of the mouth and of the oesophagus, but it does not yet
approach Meckel’s cartilage (Fig. 6B). Neither does the developing external
adductor relate to the medial surface of the postorbital ossification, but it has
expanded further in a posterodorsal direction. The anlage of the external
adductor can now be followed across the quadrate cartilage along the lateral
aspect of the otic capsule behind the stapes and the posterior rim of the fenestra
ovalis (Fig. 6D), where it becomes progressively less well defined, however. The
muscle rudiment does not establish any connection with the developing
squamosal bone which caps the dorsolateral aspect of the posterior part of the
quadrate cartilage. T h e anlage of the bodenaponeurosis still remains restricted to
a level in front of the quadrate.
Stage 19
At this stage the neurocranium reaches the peak of its development in the
antotic region, preceding a subsequent reduction which will become apparent in
later stages (Rieppel, 1976). Behind the eyeball, the anterior tip of the
palatoquadrate is deflected in a lateral direction. T h e pterygoid bone is a flat
ossification which lies medioventral to the palatine ramus of the palatoquadrate
bar, the processus pterygoideus externus is not yet developed, and while the
anlage of the pterygoideus muscle reaches anteriorly well beyond the ascending
process of the palatoquadrate, and even beyond the anlage of the
pseudotemporalis muscle, it fails to reach the anterior tip of the palatoquadrate
by a substantial distance. Of the elements of the lower jaw, the anterior part of
the dentary has started to ossify lateral to Meckel’s cartilage. T h e ossification
remains restricted to a level in front of the corner of the mouth, however. The
prearticular continues to ossify along the medial aspect of Meckel’s cartilage.
At their anterior extremities, the rudiments of the (ventral) pterygoideus and
(dorsal) pseudotemporalis muscle are separated by a narrow gap. They soon
merge into a continuous rudiment, within which the compartments remain
identifiable on the basis of fibre direction. Lateral to the level of the ascending
process of the palatoquadrate, the internus-rudiment becomes continuous with
the externus-rudiment, the different parts again remaining distinct because of a
different fibre direction. The externus-rudiment incorporates the anlage of the
bodenaponeurosis, which still does not approach Meckel’s cartilage (or the
prearticular bone ossifying along the latter’s medial aspect). Although the
differentiation of the central tendon is far from complete, this stage of
development shows the first but still rather vague indications of a separatii n of
the medialis- from the profundus-layer of the external adductor.
42
0. RIEPPEL
Neither the internus-, nor the externus-rudiment have increased in height in
front of the exit of the trigeminal nerves from the Gasserian ganglion. The
mandibular branch still curves around the dorsal margin of the internusrudiment. The cell aggregation marking the descensus parietalis lateral to the
neurocranial side-wall of the orbitotemporal region has increased in extent, but
the internus-rudiment remains separated from it by a large gap, even in front of
the trigeminal complex. Similarly, the developing external adductor does not
contact the medial surface of the postorbital ossification anywhere throughout
the orbitotemporal region.
The developing intramandibularis muscle has extended further along the
lateral aspect of Meckel’s cartilage, up to the anterior part of the anlage of the
pseudotemporalis muscle (the pterygoideus muscle as well as the rudiment of the
external adductor reach even further anteriorly). Posteriorly, the
intramandibularis muscle is still fully continuous with the superficial fibres of the
pseudotemporalis muscle. There is no indication of a tendinous sheet between
the two compartments as yet.
Behind the mandibular branch of the trigeminal nerve, the internus-rudiment
gives rise to the posterior adductor which has somewhat increased its volume,
covering the anterior and anteromedial surface of the quadrate cartilage. The
pterygoideus muscle extends along the medioventral edge of the quadrate
cartilage, below the pterygoid bone which is applied against the medial surface
of the quadrate.
The posterodorsal expansion of the developing external adductor can now be
followed across the quadrate cartilage to well behind the fenestra ovalis,
approaching the exit of the glossopharyngeal nerve from the recessus scalae
tympani. An extension of the anlage of the central tendon to a level dorsal to the
quadrate is not distinct.
Stage 20
This stage marks a distinct step forward in the development of the trigeminal
jaw adductor musculature and the correlated dermatocranial elements. I n fact,
most of the muscle compartments are now clearly delineated, and to the
exception of the internus-rudiment, most subsequent development will involve
little more than growth of the muscles and differentiation of their internal
tendinous skeleton.
The postorbital ossification has increased to form a broad bony plate covering
most of the dorsolateral surface of the temporal region of the skull. Below the
anterior part of the postorbital, the jugal bone has started to ossify (Fig. 7A).
The descending flange of the parietal is likewise represented by an ossified sheet
of bone, but is remains decomposed into an irregular mosaic of bony pieces along
its dorsal margin (Fig. 7A-C). The parietal ossification extends anteriorly well
beyond the ascending process of the palatoquadrate; it meets the latter at its
dorsal tip, and forms the dorsal margin of the trigeminal foramen behind it
(Fig. 7C). The parietal ossification even extends for some distance dorsal to the
anteriormost part of the otic capsule. The skull table is as yet completely
unossified, however.
The pterygoid continues to grow ventral and ventromedial to the
palatoquadrate bar. Below the laterally deflected anterior tip of the
palatoquadrate, the pterygoid ossification has expanded to form the processus
JAW MUSCLES OF TURTLE
I
43
I
D
Figure 7. Sections through the head of Chelydra serpentina at stagr 20 series No. 593:. Scalc
bar= 1 mm. Explanations of abbreviations in Appendix.)
externus, but the latter has not yet reached its full extent (Fig. 7A). In the
developing lower jaw, the dentary ossification has become more clearly
demarcated and it has expanded posteriorly. Dorsomedial to the dentary
ossification, and dorsal to Meckel’s cartilage, the coronoid bone has made its, as
yet, rudimentary appearance (Fig. 7B). The prearticular has further increased in
size, and the surangular has appeared just lateral to the mandibular articulation.
In relation to the other muscular compartments, the pterygoideus muscle has
expanded considerably in an anteior direction. I t now reaches the laterally
44
0. RIEPPEL
deflected anterior tip of the palatoquadrate bar, but does not yet cover its entire
dorsal surface. More posteriorly, both the internus- and the externus-rudiment
have considerably increased in height. Whereas they remained restricted to a
level below the maxillary branch of the trigeminal nerve during earlier
developmental stages, the nerve has now become trapped between the two
growing muscle compartments (Fig. 7B).
However, the prospective pseudotemporalis muscle still rises only little above
the nerve in front of the trigeminal ganglion, and before the maxillary branch
merges into the Gasserian ganglion, the muscle rudiment is lowered in height so
that the nerve passes across its dorsal margin (Fig. 7C). There is no extension as
yet of the internus-rudiment across the trigeminal nerve branches and their
ganglion in a posterodorsal direction. O n the other hand, the pseudotemporalis
anlage has grown in an anterior direction, expanding along the ventrolateral
edge of the descending parietal flange. I n its anteriormost portion it remains
separated from the pterygoideus muscle by a wide gap (Fig. 7A), but already in
front of the ascending process of the palatoquadrate the muscle rudiments merge
into each other on their medial side, with a continuous fascia wrapping around
the two muscle compartments (Fig. 7B). O n the lateral side of the internusrudiment persists a deep cleft, indicating the area where the insertional
tendinous aponeurosis will eventually develop. At the present stage, the common
aponeurosis of the pterygoideus and pseudotemporalis muscles makes its first
appearance a little further back, a t the level lateral to the ascending process of
the palatoquadrate (Fig. 7C), and it attaches to the dorsomedial area of the
developing lower jaw behind the ventral passage of the mandibular branch of
the trigeminal nerve.
Just medial to the mandibular nerve, lateral (superficial) fibres of the
internus-rudiment have become individualized by the fact that they bypass the
common aponeurosis of the pterygoideus and pseudotemporalis muscles
(Fig. 7C). These fibres are continuous with the intramandibularis muscle which
extends anteriorly along the lateral aspect of Meckel’s cartilage. Behind the
passage of the mandibular nerve, the internus-rudiment gains a little height,
rising above the level of the palatoquadrate bar again and expanding into what
Schumacher (1973) identified as posterior head of the posterior adductor,
related to the anterior aspect of the quadrate cartilage.
In comparison to the internus-rudiment, the externus has expanded dorsally
to a significant higher degree. Shortly behind the corner of the mouth, the
external adductor rises above the pseudotemporalis muscle, reaching up to the
level of the temporal (stapedial) artery (Fig. 7B, C). Dorsal to the trigeminal
complex it reaches even further up across the temporal artery, approaching the
dorsal area of the ossified parietal flange by a medial expansion (Fig. 7C). The
central tendon enclosed by the external adductor is now much more clearly
differentiated, its base relating to the developing lower jaw or, more precisely, to
the developing coronoid ossification (Fig. 7B, C). The coronoid bone ossifies in a
dense cell condensation into which merges the base of the bodenaponeurosis.
On the basis of fibre direction, the compartmentalization of the external
adductor is now fairly clearcut. The profundus-layer relates to the medial surface
and to the most dorsal portion of the lateral surface of the bodenaponeurosis.
The medialis- and superficialis-layers are represented by a common and
continuous compartment: medialis fibres insert into more basal parts of the
JAW MUSCLES OF TURTLE
A
45
I f
Figure 8. Sections through the head of Chelydra serpentzna a t stage 21 (series No. 594). Scalc
b a r = 1 mm. (Explanations of abbreviations in Appendix.)
lateral surface of the central tendon, while the superficialis-layer relates to the
dorsolateral aspect of the developing dentary bone.
At stage 20 the bodenaponeurosis can be observed to extend in a posterodorsal
direction to a level dorsal to the quadrate cartilage, where it gradually tapers off
(Fig. 7D). This permits the separation of the deep profundus-layer from the
superficially located medialis-layer at least above the anterior portion of the
broad paroccipital process. The external adductor as a whole has further
expanded in a posterior direction across the otic region, now reaching to the
level of the posterior surface of the otic capsule.
Stage 21
This stage is characterized by a distinct progress of ossification in the
dermatocranial elements, but perichondral ossification has not yet set in. A point
of interest emerges from the pattern of ossification, as it seems to progress along
an antero-posterior gradient. The parietal, postorbital and jugal are represented
by ossified areas of trabecular bone in the postorbital region (Fig. 8A), but the
spatial extent and thickness of these ossifications are progressively reduced as one
follows the sections in a posterior direction (Fig. 8B).
The pterygoid ossification has likewise increased in size. The laterally
deflected anterior tip of the palatoquadrate bar is now underlain by a welldeveloped external pterygoid process. A remarkable observation is that the tip of
the palatoquadrate bar caps the lateral edge of the external pterygoid process.
This demonstrates that the cartilage covering on the dermal pterygoid of adult
cryptodire turtles, acting as a guide for the lower jaw, is of splanchnocranial
origin. The dermal elements of the lower jaw are by now all well under way in
their process of ossification.
At this stage of development, the pterygoideus muscle has invaded the entire
dorsal surface of the laterally deflected anterior end of the palatoquadrate bar. A
0. RIEPPEL
46
strong tendon is observed to become differentiated along the ventrolateral edge
of the muscle. It is attached to the lateral edge of the external pterygoid process
behind the cartilage capping, and serves as a site of origin for pterygoideus
muscle fibres. From this developing aponeurosis ventromedial fibres of the
pterygoideus muscle start to invade the ventral surface of the external process of
the pterygoid bone. The differentiation of the ventral portion of the pterygoideus
muscle thus distinctly lags behind the development of the dorsal portion.
The pseudotemporalis muscle has expanded its origin along the laterally
descending flange of the parietal in an anterior direction up to a level shortly
behind the anterior tip of the palatoquadrate bar. In its anterior part, the muscle
remains widely separated from the pterygoideus muscle, but already well in front
of the ascending process of the palatoquadrate the two muscles converge to insert
into a common aponeurosis which has now differentiated into a horizontal
tendinous sheet (Fig. 8A). The latter receives the pterygoideus fibres into its
ventral surface, while the pseudotemporalis fibres insert into the dorsal surface.
The aponeurosis is attached to the dorsomedial aspect of the developing lower
jaw behind the passage of the mandibular branch of the trigeminal nerve.
Medial to the mandibular nerve branch, a superficial layer of the
pseudotemporalis muscle is continuous with the intramandibularis muscle
(Fig. 8A). This is the stage of development at which a tendon is beginning to
differentiate between the two muscle compartments; it makes its first appearance
just lateral to the tendinous aponeurosis which separates the pterygoideus muscle
from deeper layers of the pseudotemporalis muscle.
The most interesting development to be reported for stage 21 is the
differentiation of the dorsal part of the internal adductor. Its anlage has
increased in height, expanding in a posterodorsal direction across the maxillary
branch of the trigeminal nerve on to the ventrolateral aspect of the descending
parietal flange, forming the dorsal margin of the trigeminal foramen (Fig. 8B).
The maxillary nerve branch now pierces the internal adductor close to its
posterodorsal edge. The first rudiment of what Schumacher (1973) identified as
the anterior head of the posterior adductor develops from a posterior expansion
of the anlage of the internal adductor.
The mandibular branch pierces the internal adductor at a more ventral and
deeper level, separating the pseudotemporalis muscle from the posterior head of
the posterior adductor (sensu Schumacher, 1973). The development of the
external adductor has progressed by a further increase in size and volume. The
central tendon is well differentiated, relating to the dorsal edge of the coronoid
ossification which now rises above the dorsal margin of the dentary bone. As in
the previous stage, the profundus-layer is separated from the compartment
including the medialis- and superficialis-fibres. As the central tendon extends
across the anterodorsal aspect of the paroccipital process, it develops a distinctly
thickened lower edge. Posterodorsally, the bodenaponeurosis extends almost all
across the parocciptal process. The external adductor as a whole has grown all
across the otic and occipital region and into the neck area.
Stage
22
Apart from a further progress in dermal ossification, this developmental stage
shows little advance over the preceding stage. Of particular interest is the further
development of what Schumacher (1973) identified as the posterior adductor.
JAW MUSCLES OF TURTLE
47
The maxillary branch still pierces the internal adductor close to the
posterodorsal margin, the anterior head of the posterior adductor still remaining
small and in a rudimentary stage of differentiation.
The superficial layer of the pseudotemporalis muscle, which merges into the
intramandibularis muscle in front of the mandibular branch of the trigeminal
nerve, is clearly differentiated; the tendinous sheet developing between the two
muscle compartments has become quite distinct. An interesting point to note is
that in front of its connection to the intramandibularis muscle, the superficial
layer of the pseudotemporalis muscle inserts into the medial surface of the base of
the bodenaponeurosis.
Stage 23
This can in many ways be stated to represent the final stage of differentiation
of the jaw adductor musculature. Subsequent development involves little more
than an increase in size and volume, and adds almost nothing of significance to
further structural complexity of the jaw adductor musculature. The
palatoquadrate bar has not yet (partially) degenerated. T h e anterior tip is
deflected laterally and caps the lateral edge of the external pterygoid process.
The pterygoideus muscle has grown across the anterior tip of the palatoquadrate
bar, extending its origin for a short distance on to the dorsal surface of the
pterygoid bone in front of the palatoquadrate. The pterygoideus muscle has
pushed its origin to a far anterior position, to a level closely posteroventral to the
eyeball. The origin of the pseudotemporalis muscle likewise extends anteriorly
along the ventrolateral edge of the descending parietal flange up to a level
closely behind the eyeball.
In the anterior portion, these latter two muscles remain widely separated
(Fig. 9A). More posteriorly, but again well in front of the ascending process of
the palatoquadrate, they insert into the common aponeurosis which has
developed a triradiate cross-section (Fig. 9B) : a horizontal basal sheet receives
the fibres of the pterygoideus muscle into its lower surface. From its dorsal
surface emerges a parasagittal tendinous sheet which intersects the base of the
pseudotemporalis muscle. This insertional aponeurosis attaches to the
dorsomedial edge of the prearticular bone behind the passage of the mandibular
branch of the trigeminal nerve down into Meckel’s groove (Fig. 9F).
The dorsal portion of the pterygoideus muscle originates from the surface of
the pterygoid bone and from the palatoquadrate bar medially, as well as from a
strong aponeurosis laterally, which in turn is attached to the lateral edge of the
external pterygoid process (Fig. 9A, B). T h e ventral portion of the pterygoideus
muscle also relates to this aponeurosis and has extensively invaded the ventral
surface of the pterygoid bone. T h e main bulk of this ventral portion has yet to
develop during subsequent stages up to the hatchling condition.
The pseudotemporalis muscle originates from the lateral and ventrolateral
aspect of the by now well consolidated descending parietal flange (Fig. 9A). The
muscle has become futher differentiated at the level lateral to, and behind, the
ascending process of the palatoquadrate (Fig. 9C). I n particular, the tendon
relating the superficial layer of the pseudotemporalis to the intramandibularis
muscle has increased in size, enhancing the individualization of a
pseudotemporalis superficialis proper. Furthermore the internal adductor has
markedly extended its area of origin along the descending flange of the parietal
JAW MUSCLES OF TURTLE
49
in a posterodorsal direction. The dorsal portion is pierced by the maxillary
branch of the trigeminal nerve (Fig. 9C, D), while the mandibular branch
subdivides the muscle in a more ventral position (Fig. 9E). The trigeminal
complex thus separates the anterior pseudotemporalis muscle from the posterior
adductor (sensu Schumacher, 1973). T h e latter muscle is further subdivided into
an anterior dorsal head, lying behind the maxillary nerve and originating from
the parietal (Fig. 9D, E), and into a posterior head, lying behind the mandibular
nerve branch (Fig.9E) and relating to the anterior aspect of the quadrate
cartilage and to the ventrolateral aspect of the cupula anterior of the otic
capsule. It should be emphasized, however, that an unequivocal demarcation of
the anterior pseudotemporalis muscle from the posterior adductor is not really
possible (Fig. 9C). The two muscle compartments continuously merge into each
other, the branches of the trigeminal nerve serving as only landmarks for any
separation. Such is indeed to be expected from the developmental dynamics,
since the posterior adductor (sensu Schumacher, 1973) originates from nothing
but a continuous posterior expansion of the internus-rudiment. T h e same point is
borne out by the insertional relations of the posterior adductor. Its anterior fibres
still reach into the insertional aponeurosis which the anterior pseudotemporalis
muscle shares with the pterygoideus muscle (Fig. 9E). Only the posterior fibres of
the posterior adductor insert directly into the dorsal surface of Meckel’s
cartilage.
The external adductor has also completed its differentiation. The
bodenaponeurotic tendon is now fully developed; its anterior base is connected
to the corner of the mouth by a thick layer of dense connective tissue (Fig. 9A).
Anteriormost fibres of the superficial layer of the external adductor insert into
the lateral surface of this thick tendinous raphe lining the corner of the mouth
deep to the rictal plate (Fig. 1OC). This anteroventral head of the external
adductor corresponds to the lb-portion of the external adductor in lizards
(Lakjer, 1926; Haas, 1973). McDowell (1986: 355) characterized the rictal plate
of Sphenodon and lizards as “. . . essentially an invagination of the skin at the side
of the jaw”, which “. . . forms a lengthwise fold from the corner of the mouth
back nearly or quite to the level of the jaw articulation”. It receives into its
dorsal margin the fibres of the levator anguli oris muscle (Fig. 10A, B ) . A
comparable rictal plate of somewhat more restricted extent is also differentiated
in cryptodire turtles (Gaffney, 1979: 106), but no well differentiated levator
anguli oris was observed in sections through the head of a hatchling Chelydra
(Fig. lOC, D).
Behind the corner of the mouth, the bodenaponeurosis is attached to the
dorsomedial edge of the lower jaw, in particular to the coronoid bone (Fig. 9B).
From there it extends in a posterodorsal direction as described for earlier stages.
The profundus-layer of the external adductor inserts into the entire medial
surface and into the dorsal marginal zone of the lateral surface of the
bodenaponeurosis. The medialis- and superficialis-layers cannot be
unequivocally delineated from one another; deep fibres of the common muscular
compartment insert into the lateral surface of the central tendon, while more
superficial fibres insert into the dorsolateral aspect of the dentary bone
(Fig. 9B, C ) . An advance over the preceding stage is the development of a small
tendinous sheet attached to the dorsal rim of the dentary and intersecting the
deepest part of the medialis plus superficialis compartment in a parasagittal
50
0. RIEPPEL
I
/p
,Pf
A
D
Figure 10. Sections through the corner of the mouth of the lizard Podarcis sicula (A-B; Series
No. RG 800212); and of the hatchling Chelydra ser-pentina ( C D ; series No. 599). Scale bar= 1 mm.
(Explanations of abbreviations in Appendix.)
plane lateral to the bodenaponeurosis (Fig. 9C, D). As the bodenaponeurosis
approaches the anterodorsal aspect of the paroccipital process and passes over its
dorsal surface it develops a distinctly thickened ventral edge (Fig. 9F). This
provides a gliding cushion for the external adductor. The thickened ventral edge
of the bodenaponeurosis is described as incorporating a transilient cartilage in
adult cryptodire turtles (Schumacher, 1973: fig. 2), articulating with a processus
trochlearis of the prootic. It must be stressed, however, that up to the hatching
stage (the last one available for study), no chondrocytes were observed anywhere
JAW MUSCLES OF TURTLE
51
within the bodenaponeurosis in the critical region. A parasagittal sheet emerges
from the basal tendinous cushion; it separates the profundus- from the medialislayer as the external adductor passes across the paroccipital process back into the
neck region (Fig. 9F).
PATTERNS OF EARLY DEVELOPMENT
The most conspicuous feature to be observed during early stages of
development is the formation of the initially fully homogeneous jaw adductor
rudiment by a cell aggregation surrounding the mandibular branch of the
trigeminal nerve. There is at this stage no possibility of identifying prospective
muscle compartments, although that part of the rudiment which lies deep to the
mandibular branch will give rise to the internal adductor, while those cells lying
lateral to the trigeminal nerve will develop into the external adductor.
Along the posteroventral aspect of the mandibular branch the cell aggregation
extends ventrally across the lateral surface of Meckel’s cartilage (the prospective
intramandibularis muscle) and beyond the latter, establishing continuity with a
cell aggregation extending between the two primordial lower jaws and
representing the prospective intermandibularis muscle. ’This early continuity of
the intermandibularis and intramandibularis muscles appears to be another
consequence of the early formation of muscle rudiments by cell aggregation
around the innervating nerve branches: in chelonians, both the
m. intramandibularis and the m. intermandibularis are innervated by posterior
and posteromedial branches of the alveolar nerve (ventral segment of the
mandibular branch, running through Meckel’s canal of the lower jaw)
(Poglayen-Neuwall, 1953; Schumacher, 1973).
The early continuity of the intramandibularis and intermandibularis muscles
was already figured by Edgeworth (1935: 423, fig. 555), who also indicated it for
early developmental stages of Lacerta (p. 41 1, fig. 489), not represented in my
material (Rieppel, 1987a), and also for crocodiles (Edgeworth, 1935: 429,
fig. 578). This is a general feature, probably indicating a functional (inductive)
correlation between nerve growth and muscle formation. Indeed, the relation of
the m. intermandibularis to the trigeminal jaw adductor musculature would
seem to deserve further study, including an experimental approach. In
‘primitive’ selachians, the intermandibularis is innervated by the facial nerve
alone (Luther, 1909; Lubosch, 1933: 613). I n ‘primitive’ osteichthyans, in
dipnoans and in amphibians, the m. intermandibularis shows an innervation by
the trigeminal nerve in its anterior part and by the facial nerve in the posterior
part (Luther, 1913, 1914; Lubosch, 1933). For the Sauropsida, Lubosch
(1933: 615) described an innervation of the m. intermandibularis by the
trigeminal nerve alone, but Edgeworth (1935: 61) mentions the innervation of
the intermandibularis posterior by the facial nerve in at least some lizards, an
observation already reported by Willard (1915: 69) and confirmed by Smith
(1986: 268). A double innervation of the intermandibularis muscle is also
observed in Sphenodon (Rieppel, 1978a). There seems to exist, within
gnathostomes, a certain plasticity of the differentiation of the
m. intermandibularis into an anterior and posterior portion along with
variations in innervation, which might reflect dynamic developmental
interactions between nerve growth and muscle formation.
52
0. RIEPPEL
During early stages of cell aggregation the antero-posterior extent of the
anlage of the jaw adductors remains much restricted: the medial part of the
rudiment, lying deep to the mandibular branch, extends anteriorly to the
ascending process of the palatoquadrate (the prospective pseudotemporalis and
pterygoideus muscles), while it reaches up to the quadrate cartilage posteriorly
(the prospective posterior adductor). Dorsally, the cell aggregation remains
restricted to a level below the Gasserian ganglion and the exit of the maxillary
and mandibular branches from it.
The external part of the early muscle rudiment, lying lateral to the
mandibular branch, remains for some time even more restricted in an anteroposterior direction, but soon begins to rise to greater height lateral to the
Gasserian ganglion. The dorsal and posterodorsal extension of the prospective
internal and posterior adductor thus lags behind the posterodorsal extension of
the external adductor during development. This is just the opposite from the
condition observed in the lizard Podarcis, where the posterodorsal extension of
the internal adductor precedes that of the external adductor (Rieppel, 1987a).
SUBSEQUENT DEVELOPMENT OF THE EXTERNAL ADDUCTOR
The external adductor develops from that part of the adductor mandibulae
rudiment which lies lateral to the mandibular branch of the trigeminal nerve. It
becomes subdivided (compartmentalized) by the differentiation of the central
tendon (bodenaponeurosis) within the muscle anlage. During the initial stages of
its differentiation, the bodenaponeurosis of Chelydra is quite independent from
the developing lower jaw. O n the whole, the differentation of the central tendon
of the jaw adductors in Chelydra differs in its topological relations from the
bodenaponeurosis in the lizard Podarcis, where the tendon develops initially
between the internal (pseudotemporalis muscle) and external adductor
rudiments (Rieppel, 1987a). The developing bodenaponeurotic tendon is
furthermore attached to the articular bone in the lizard, and it incorporates the
ossification centre of the coronoid bone (Rieppel, 1987a). Although the relations
of the bodenaponeurotic tendon appear quite comparable in the adult turtle and
lizard (Lakjer, 1926), the developmental patterns are different. This provides
another example for the well known phenomenon (Alberch, 1985; de Queiroz,
1985) that structures judged to be homologous by their topological relations in
the adult may develop along different pathways. The problem then is to decide
whether the relation of homology should be based on the static adult topography
or rather on the dynamic developmental patterns (Oster et al., 1988). As will be
shown below, the same problem will have to be addressed in the discussion of the
differentiation of the internal adductor.
One of the most salient features of the development of the external adductor is
its successive extension in a posterodorsal direction across the paroccipital
process. The extension of the muscle is followed by the progressive differentiation
of the central tendon in the same direction. The posterodorsal extension of the
external adductor (mainly the profundus-layer) through the emarginated posttemporal fossa along a supraoccipital crest is a derived feature of turtles which,
by its development, provides an example for Haeckelian recapitulation
(Lovtrup, 1978). The jaw adductor musculature of the Triassic turtle
Proganochelys must have corresponded to the more generalized reptilian pattern,
JAW MUSCLES OF TURTLE
53
as the skull roof is not emarginated posteriorly and therefore the post-temporal
fenestrae are of standard size (although enlarged as compared to the size of the
post-temporal fenestrae in captorhinomorph stem reptiles) (Gaffney & Meeker,
1983).
SUBSEQUEN'I' DEVELOPMENT OF T H E INTERNAL ADDUCTOR
The internus-rudiment develops medial to the mandibular branch of the
trigeminal nerve and lateral to the ascending process of the palatoquadrate as is
typical for sauropsids in general (Lakjer, 1926; Edgeworth, 1935). T h e anlage of
the pterygoideus muscle first becomes distinct by the development of a
medioventral rim projecting from the internus-rudiment below the
palatoquadrate bar. This is quite comparable to the early stages of
differentiation of the internus-rudiment in Podarcis. In contrast to the lizard,
however, the pterygoideus muscle and the pseudotemporalis muscle never fully
separate except in their anteriormost part, after their growth in an anterior
direction. By this anterior extension, the pterygoideus muscle invades the dorsal
and ventral surfaces of the pterygoid bone, while the pseudotemporalis invades
the lateral parietal flange. The two muscles remain in an intimate contact with
each other, as a horizontal tendinous sheet develops within the internusrudiment, separating the ventral pterygoideus muscle from the dorsal
pseudotemporalis.
The most salient feature in the development of the internal adductor,
however, is the posterodorsal expansion of the anlage of the pseudotemporalis
muscle. By stage 18, the muscle rudiment has gained its attachement to the
lateral surface of the ascending process of the palatoquadrate. Behind the latter,
the maxillary and mandibular branches of the trigeminal nerve still pass across
the dorsal margin of the muscle rudiment. The latter progressively increases its
height between the ascending progress and the trigeminal nerve branches until,
in stage 21, the pseudotemporalis anlage begins to expand across the exit of the
maxillary and mandibular nerves from the Gasserian ganglion. This
posterodorsal expansion of the internus-rudiment along the parietal flange dorsal
to the trigeminal foramen continues until the internal adductor appears to be
pierced by the trigeminal nerve branches. At the same time, that part of the
muscle rudiment which lies deep to the trigeminal nerve branches expands
posteriorly, invading the anteromedial aspect of the quadrate cartilage.
This developmental pattern again creates difficulties for the establishment of
homologies in the adult musculature. The internal adductor which invades the
secondary lateral side wall of the braincase (parietal flange and epipterygoid),
lined by the temporal artery running along the dorsal margin of the muscle,
would seem to correspond to the pseudotemporalis muscle of lepidosaurs. In
turtles, however, this deep muscular sheet is pierced by the maxillary branch of
the trigeminal nerve which separates an anterior from a posterior head. h'hile
the anterior head has always been accepted as the pseudotemporalis muscle
proper, lying deep to the maxillary nerve, the posterior head was labelled as part
of the posterior adductor by Lakjer (1926), Poglayen-Neuwall (1953) and
Schumacher (1973),lying behind the maxillary and mandibular nerve branches.
While this homology is justified by reference to Lakjer's (1926) criteria of adult
54
0. RIEPPEL
topography, it implies a developmental origin of the posterior adductor from the
internus-rudiment. The same holds for the deeper and posterior part of the
posterior adductor which takes its origin from the anteromedial aspect of the
quadrate, that is in a position corresponding to that of the lacertilian posterior
adductor, but which again develops from the internus-rudiment lying medial to
the mandibular nerve.
The problem of homology of the posterior adductor results from the fact that
the latter muscle has no independent rudiment. It develops from the externusrudiment in lizards (Rieppel, 1987a), where in the adult it originates mainly
from the anteromedial slope of the quadrate. Its topological counterpart in
turtles is the posterior head of the posterior adductor sensu Schumacher (1973),
which develops from the internus-rudiment, however. The anterior head of the
posterior adductor sensu Schumacher ( 1973), originating from the parietal dorsal
to the trigeminal foramen, has no topographical equivalent in lizards. And
although it is correctly identified as a posterior adductor on Lakjer’s criteria
(1926), in fact it develops as a posterodorsal expansion of the pseudotemporalis
muscle. Once again, relations of homology established on static topographical
correspondences of adult structure cannot capture the dynamics of the
developmental process.
DEVELOPMENT OF THE M. INTRAMANDIBULARIS
The intramandibularis muscle provoked much discussion in the 1;‘terature on
the jaw adductors of gnathostomes. According to Schumacher (1973: 1 14), this
muscle was first described by Lubosch (1913) as an anterior extension of jaw
adductor muscle fibres within Meckel’s canal of the lower jaw in crocodiles. He
compared this muscle arrangement with a similar condition in lizards ( Varanus
and Chamaeleo), but he noted that “none of it is observed in Chelonians ”
(Lubosch, 1914: 701). Lubosch (1914: 702) also noted the topographicsl
correspondence in the differentiation of the intramandibularis portion of the
adductor musculature described for Polypterus (Luther, 1913: 21) and Amia
(Luther, 1913: 22, 32). This comparison was emphasized by Lubosch in 1933,
when he erroneously homologized the intramandibularis muscle of crocodiles
and other sauropsids with the pars symphysialis of the adductor mandibulae in
fishes. I n fact, Luther (1913: 15; 1914: 11 1) designated as pars symphysialis an
anterior head of the jaw adductor, originating from the palatoquadrate in a
preorbital position. The intramandibularis muscle on the other hand was
identified by him as a ventral extension of the posterior adductor within
Meckel’s canal (Luther, 1914: 112, 118-1 19; see also Luther, 1913: 45).
The intramandibularis muscle of turtles was first described by PoglayenNeuwall (1953: 263) as a separate muscular unit connected to the base of the
pseudotemporalis muscle by a tendinous sheet (see also Schumacher, 1973,
fig. 8). The present study confirms its developmental origin from the internusrudiment, which also gives rise to the posterior adductor of turtles. The
comparison with the intramandibularis muscle of Polypterus and Amia as
described by Luther (1913) cannot go beyond a statement of topographical
correspondence. Of greater interest is the comparison of the chelonian
intramandibularis muscle with that of other reptiles, viz. crocodiles and lizards.
The intramandibularis of crocodiles, for which Schumacher (1973: 138) suggests
J.;\\V
MUSCLES OF TURTLE
55
an origin from the internal adductor, does indeed seem rather closely
comparable to that of turtles (Schumacher, 1973, fig. 22). In both groups, the
internus-rudiment is continuous with the intermandibularis anlage during early
developmental stages, and in both groups the intramandibularis muscle lies deep
to the mandibular branch of the trigeminal nerve in the adult lower jaw. The
intramandibularis of turtles and crocodiles seems to represent a plesiomorphic
(generalized) character, differentiating from the early developmental continuity
of the internus-rudiment with the intermandibularis muscle anlage.
The same is not true of the intramandibularis muscle of lizards. Lubosch
(1933) mentions a differentiation similar to that observed in turtles for two
lizards, Varanus and Chamaeleo, although it is not clear why he chose these two
candidates for comparison. A well-differentiated intramandibularis muscle is
known for teiid, gymnophthalmid, xantusiid and lacertid lizards (Rieppel,
1980a, 1984b; the Lacertoidea of Camp, 1923, and Estes, de Queiroz &
Gauthier, 1988). In the adult lacertid Podurcis sicula, the intramandibularis
muscle lies lateral to the mandibular branch of the trigeminal nerve within
Meckel's canal of the lower jaw (confirmed by serially sectioned material; see
also Rieppel, 1987a, fig. 4 . 5 for comparison). Developmental data demonstrate
the development of the intramandibularis muscle as a n anterior extension of the
posterior adductor within Meckel's canal. Quite in contrast to the chclonian
condition, the posterior adductor of lizards develops from the externus-rudiment
in a position lateral (superficial) to the mandibular branch of the trigeminal
nerve (Rieppel, 1987a, fig. c). The intramandibularis muscles of turtles and of
lizards are non-homologous; the anterior expansion of the posterior adductor
into Meckel's canal of the lower jaw preserves its status as a synapomorph) of the
Lacertoidea (Estes el al., 1988).
SI';\TUS O F T H E CHELONIA WI'I'HIS 'IHE SAUROPSID.4
Cladistic analysis strongly supports the interpretation of the turtle skull as
representing the anapsid condition (Gaffney & Meeker, 1983), supporting the
classification of chelonians as sister group of the Diapsida which includes all
other sauropsids (Gauthier, Estes & de Queiroz, 1988). Although this
corresponds to the traditional classification of turtles (see Romer, 1956). there
has been a continuing argument in the field of comparative morphology as to
whether or not the temporal roofing in the dermatocranium of turtles might not
present a secondary (derived) condition. It is now possible to refute this
hypothesis not only on the basis of character congruence and parsimony as
employed in cladistic analysis, but also on comparative morphological grounds.
Lakjer (1926) placed much emphasis on the presence of a quadrato-maxillary
ligament in turtles. This ligament is lacking in reptiles which are characterized
by a fully diapsid skull such as crocodiles or Sphenodon, but it is present in those
diapsids in which the lower temporal arcade is reduced, such as lizards and
snakes. Lakjer (1926: 48:) concluded that turtles must also have lost a lower
temporal arcade, which implies that the 'temporal arcade', composed of the
postorbital, squamosal and jugal bones, constitutes a true upper temporal arch
homologous to that of diapsids.
Lakjer's ( 1926) homology of the quadrato-maxillary ligament with the lower
temporal arcade of fully diapsid reptiles has been extended by Haas 1930,
56
0. RIEPPEL
1973), who homologized a temporal tendon in the generalized snake Cylindrophis,
giving rise to superficial adductor fibres, with the upper temporal arcade of
lizards (see Rieppel, 1980b: 451, for a discussion). The literature thus reflects a
tendency to equate reduced bony structures with tendinous or ligamentous
substitutes, which might indeed appear reasonable in view of the developmental
plasticity of precursor cells (Hall, 1978). However, the arrangement of the jaw
adductor musculature clearly refutes the homologies in the turtle skull as
hypothesized by Lakjer (1926).
Traditionally the completely closed dermatocranium as seen in marine turtles
such as Chelonia or Dermochelys (Wegner, 1959) is seen as the generalized
(plesiomorphous) condition characteristic for anapsid reptiles. The reduction of
the dermatocranium is thought to have occurred along two different pathways:
temporal fenestration characterizes diapsids (as well as synapsids), while
temporal emargination is thought to characterize turtles. The ventral temporal
emargination probably served the expansion of the superficial layer of the
external adductor on to the lateral surface of the lower jaw in analogy to the loss
of the lower temporal arcade in diapsids (Rieppel & Gronowski, 1981), while the
posterior emargination of the skull roof serves the expansion of the medialis- and
profundus-layer of the external adductor in a posterodorsal direction, again in
analogy to the loss of the upper temporal arcade in diapsids. However, the case is
one of analogy only, since the pattern of the posterodorsal expansion of the
external jaw adductor is quite different in turtles as compared to squamates.
Lizards which show an expansion of the external adductor in correlation with
the loss of the upper temporal arcade are all miniaturized forms (Rieppel, 1984c)
such as the fossorial scincomorph genera Typhlosaurus (Rieppel, 1981a) and
Dibamus (Rieppel, 1984a). I n these reptiles, the neurocranium fused with the
dermatocranium to form a solid and closed cranial box, thus providing the
opportunity for a posterodorsal expansion of muscle origin across the otic and
occipital region. One effect of miniaturization is the obliteration of the posttemporal fossae, as the parietal meets the supraoccipital in a closed suture.
However, the epaxial neck muscles retain their typical sites of insertion into the
posterior margin of the parietal (i.e. into the suture between parietal and
supraoccipital in these miniaturized lizards), and into the dorsal and posterior
surface of the neurocranium. The result of such an arrangement is an expansion
of the external adductor from the surface of the parietal across the epaxial neck
musculature that is superficial to the latter in Dibamus.
If Lakjer’s (1926) homologies were correct, the dorsal emargination of the
dermatocranium in turtles would have to be interpreted as an upper temporal
fossa, bounded laterally by a true upper temporal arcade, and as in lizards the
external adductor would have to lie superficial to the epaxial neck muscles.
However, the posterodorsal expansion of the profundus-layer of the external
adductor lies deep to the spinalis capitis muscle, which testifies to the fact that it
is the post-temporal fossa which has become widened in turtles by a posterior
emargination of the skull roof. The musculature retains its topological relations
in comparison to non-miniaturized lizards, where the profundus-layer of the
external adductor (3b-head of Haas, 1973) originates from the circumference of
the post-temporal fossa, that is deep to the insertion of the spinalis capitis muscle
into the posterior margin of the parietal bone. In conclusion, two radically
different patterns of dermatocranial reduction must be recognized, supporting
JAW MUSCLES OF TURTLE
57
Gaffney’s (1980) classification of the Amniota but conflicting with the amniote
classification proposed by Gauthier et al. ( 1988). Dermatocranial emargination
characterizes the Chelonia, while ‘temporal fenestration’ emerges as a
synapomorphy of the Eureptilia. An upper temporal fenestra characterizes the
Diapsida (Rieppel, 1989), while the Synapsida are characterized by a lower
temporal fenestra. As the lower temporal fossa also occurs in diapsids, its
occurrence might be seen as a plesiomorphic feature so that different characters
such as the differentiation of the occiput (Reisz, 1980) must be used to diagnose
synapsids as a monophyletic group.
SECONDARY CARTILAGE AND CRANIAL KINESIS
An earlier investigation of developmental stages of the Italian wall lizard
(Podarcis sicula) has shown that those dermatocranial elements which participate
in the formation of synovial articulations involved in cranial kinesis are covered
by cartilage which is of splanchnic origin. The study had generated the
hypothesis that the splanchnocranium, ultimately derived from neural crest cells,
represents the primary kinetic component o f . the vertebrate skull (Rieppel,
1978b).
These findings are corroborated by the investigation of the development of the
skull in Chelydra. The turtle skull is akinetic, the only movably suspended element
(to the exception of the stapes) being the lower jaw. I n cryptodire turtles, the
processus pterygoideus externus is capped by cartilage, and serves as a guide for
the vertical movements of the lower jaw ramus. This cartilage, deposited on a
dermal cranial element, cannot be considered to represent true secondary
cartilage which has only been described for mammals and birds (Hall, 1984;
Hall & Hanken, 1985a, b; Irwin & Ferguson 1986). Rather the study of
developmental processes shows it to derive from the palatoquadrate, that is from
the splanchnocranium.
Metakinesis appears to be primitive for reptiles in general (Heaton, 1979) as
well as for turtles, since the Triassic genus Proganochelys retains a movable
palatobasal articulation (Gaffney, 1983; Gaffney & Meeker, 1983). T h e process
of fusion of the palatobasal articulation can be observed during the ontogenetic
development of the basicranium of Chelydra, as the developing pterygoid
ossification comes to embrace the crista basipterygoidea of the basal plate
(Rieppel, 1977). While early ontogenetic stages of the basicranium thus recall
the more generally distributed stage of differentiation of the palatobasal
articulation (assumed to represent the phylogenetically more primitive stage),
this is not the case for the development of the constrictor internus dorsalis
musculature. In fact, no constrictor internus dorsalis rudiment can be identified
unequivocally during any developmental stage of Chelydra. Department from the
metakinetic condition is thus more radical in the turtle than in Sphenodon or in
chameleons, taxa which both obliterated metakinetic movement but retain at
least part of the constrictor internus dorsalis musculature (Haas, 1973; Rieppel,
1981b, 1987b). The radical departure from the metakinetic condition, along
with the extended fusion of the pterygoid with the crista basipterygoidea
throughout the orbitotemporal region, is correlated with a different arrangement
and function of the jaw adductor musculature.
Gaffney (1975) has drawn attention to the particular arrangement of the
58
0. RIEPPEL
external adductor of turtles which forms a pulley system with the central
(bodenaponeurotic) tendon running across a trochlear process as it changes from
a vertical to a more horizontal orientation. The trochlear process is borne by the
pterygoid in pleurodires and by the prootic (as part of the anterodorsal surface of
the paroccipital process) in cryptodires. It seems conceivable that this pulley
system could develop only after the obliteration of metakinesis.
The Triassic turtle Progunochelys retains a movable palatobasal articulation
and post-temporal fossae of more or less standard size (Gaffney, 1983; Gaffney &
Meeker, 1983). The dermatocranial skull roof is not emarginated posteriorly,
and there is no supraoccipital crest projecting beyond the occiput. It might thus
be expected that the jaw adductor musculature was likewise arranged in a
standard pattern, an assumption which is corroborated by the absence of a
trochlear process both on the pterygoid as well as on the prootic (Gaffney &
Meeker, 1983).
Taking Chelydru as an example of a typical cryptodire, one finds a deep
posterior emargination of the skull roof and an extended supraoccipital crest
which, along with the parietal flanges, gives rise to the bulk of the external
adductor. If there were a line of flexion between supraoccipital and parietal as
there is in a metakinetic skull, this would render the posterodorsal expansion of
the external adductor an inefficient arrangement. A similar argument can be
construed for chameleons which again elaborate the occiput into a crest-shaped
structure involving the immovably fused parietal and supraoccipital (Rieppel,
1981c) .
The central tendon of the external adductor of Chelydru changes from a
horizontal to a vertical orientation as it curves around the trochlear process of
the prootic. From there it descends directly towards the lower jaw. The main
bulk of the external adductor exerts a horizontal force which is converted into a
vertical force on the lower jaw by the resistance of the paroccipital process
against the central tendon. The paroccipital process as a whole comes under
stress when the external adductor contracts, the contraction will tend to displace
the braincase in a posteroventral rotation (Fig. 11). An immediate effect would
be the disarticulation of the palatobasal articulation. Two factors may serve to
counter this force component: obliteration of any line of weakness in the
suspension of the braincase from the dermatocranium, and retention of a dermal
bracing between the quadrate area (squamosal bone) and the facial portion of
the skull by the intermediary of the postorbital and jugal bones. This ‘temporal
arcade’ is much reduced or even obliterated in a number of turtle genera
(Gaffney, 1979) which shows that the fusion of the parietal with the
supraoccipital on the one hand, and of the pterygoid with the basicranium on
the other, is adequate to permit the function of the pulley system. The pleurodire
turtles show an analogous differentiation of the external adductor into a pulley
system and therewith incur the same biomechanical problems which they solve
in a similar manner: fusion of the supraoccipital with the parietal and of the
dermal palate with the basicranium.
CONCLUSIONS
1. The internal and external jaw adductor muscles of Chelydra serpentinu
develop from an originally continuous rudiment formed by cell aggregation
JAW MUSCLES O F T U R T L E
59
Figure 1 I . A biomechanical analysis of the external adductor and its effect on the paroccipital
process in Che[>admserpentina.
around the innervating branches of the trigeminal nerve. Behind the mandibular
branch of the trigeminal nerve, the prospective internus-rudiment is continuous
with the anlage of the intermandibularis muscle during early developmental
stages as is also true of other sauropsids.
2. The intramandibularis muscle of turtles develops from the early connection
of the internus-rudiment with the intermandibularis muscle anlage and as such
represents a plesiomorphous character. It is not homologous with the
intramandibularis muscle of lizards which derives from the externus-rudiment
and which constitutes a synapomorphy of the Lacertoidea.
3. The bodenaponeurosis (central tendon) of the external adductor develops
along different pathways in turtles and lizards, highlighting the fact that
homology based on static topological correspondence of adult structure cannot
capture the dynamics of the developmental process.
4. The same point is borne out by the development of the posterior adductor
which in turtles develops from the internus-rudiment, whereas it derives from the
externus-rudiment in lizards.
5. In contrast to squamate reptiles, the pseudotemporalis muscle is pierced in
its dorsal part by the maxillary branch of the trigeminal nerve in turtles. This
permits the (rather arbitrary) distinction of a n ‘anterior head’ of the posterior
adductor (Schumacher, 1973), which originates from the dorsal margin of the
trigeminal foramen behind the maxillary branch, from the pseudotemporalis
proper, which lies deep to the trigeminal nerve.
6. The expansion of the external adductor across the paroccipital process in a
posterodorsal direction, typical of advanced turtles, provides an example of
Haeckelian recapitulation.
7. The relation of the posterodorsal expansion of the external adductor to the
epaxial neck musculature supports of the refutation of Lakjer’s (1926) argument
60
0. RIEPPEL
that turtles might be derived from diapsid reptiles. Whereas the dermatocranium
is reduced through posterodorsal and ventral emargination in turtles, temporal
fenestration can be seen as a synapomorphy of the Eureptilia (Gaffney, 1980),
including synapsids and diapsids.
8. The (secondary) loss of cranial kinesis in turtles is related to the specialized
arrangement and function of the external jaw adductor.
ACKNOWLEDGEMENTS
I thank PD Dr D. G. Senn, University of Basel, for the generous loan of the
material on which the main part of this study is based. The juvenile specimen of
Chelydru was made available by the Natural History Museum, Basel. Special
thanks are due to Dr E. A. Gaffney, American Museum of Natural History, who
not only let me have macroscopically sectioned heads of Chelydru on loan, but
who also let me see his manuscript on his earlier work on the jaw adductors of
this turtle genus.
REFERENCES
ADAMS, L. A,, 1919. A memoir on the phylogeny of the jaw muscles in recent and fossil vertebrates. Annals of
the N e w York Academy of Sciences, 28: 51-166.
ALBERCH, P., 1985. Problems with the interpretation of developmental sequences. Systematic zoology, 34:
4G58.
ALBRECHT, P. W., 1976. The cranial arteries of turtles and their evolutionary significance. Journal of
Morphology, 149: 159-182.
CAMP, C. L., 1923. Classification of the lizards. Bulletin of the American Museum ofNatura1 History, 48: 289-481.
De QUEIROZ, K., 1985. The ontogenetic method for determining character polarity and its relevance to
phylogenetic systematics. Systematic zoology, 34: 280-299.
EDGEWORTH, F. H., 1935. The Cranial Muscles of Vertebrates. Cambridge: Cambridge University Press.
ESTES, R., De QUEIROZ, K. & GAUTHIER, J., 1988. Phylogenetic relationships within the Squamata. In
R. Estes & G. Pregill (Eds), Phylogenetic Relatiomhips of the Lizard Families: 119-281. Stanford, CA: Stanford
University Press.
FLCHS, H., 1915. Uber den Bau und die Entwicklung des Schadels von Chelone imbricata. Ein Beitrag zur
Entwicklungsgeschichte und vergleichenden Anatomie des Wirbeltierschadels. Erster Teil: Das
Primordialskelett des Neurocraniums und des Kieferbogens. In A. Voeltzkow (Ed.), Reise in Ostafrika in den
Jahren 19051905, 5: 1-325. Stuttgart: E. Schweizerbart.
GAFFNEY, E. S., 1972. An illustrated glossary of turtle skull nomenclature. American Museum Nouitates, 2486:
1-33.
GAFFNEY, E. S., 1975. A phylogeny and classification of the higher categories of turtles. Bulletin ofthe American
Museum of Natural H i s t o v , 155: 387436.
GAFFNEY, E. S., 1979. Comparative cranial morphology of recent and fossil turtles. Bulletin of the American
Museum of Natural History, 164: 65-376.
GAFFNEY, E. S., 1980. Phylogenetic relationships of the major groups of amniotes. I n A. L. Panchen (Ed.),
The Terrestrial Environment and the Origin of Land Vertebrates: 593-610. London: Academic Press.
GAFFNEY, E. S., 1983. The basicranial articulation of the Triassic turtle, Proganochelys. In A. G. J. Rhodin &
K. Miyata (Eds), Advances in Herpetology and Euolulionary Biology: 196194. Cambridge, MA: Museum of
Comparative Zoology.
GAFFNEY, E. S. & MEEKER, L. J., 1983. Skull morphology of the oldest turtles: a preliminary description of
Proganochelys guenstedti. Journal of Vertebrate Paleontology, 3: 25-28.
GAUTHIER, J., ESTES, R. & De QUEIROZ, K., 1988. A phylogenetic analysis of Lepidosauromorpha. In
R. Estes & G. Pregill (Eds), Phylogenetic Relationships of the Lizard Families: 15-98. Stanford, CA. Stanford
University Press:.
HAAS, G., 1930. Uber die Kaumuskulatur und die Schadelmechanik einiger Wuhlschlangen. zoologische
Jahrbiicher (Abteilung Anatornie), 52: 95-218.
HAAS, G., 1973. Muscles of the jaws and associated structures in the Rynchocephalia and Squamata. In C.
Gans & T. S. Parsons (Eds), Biology of the Reptilia, 4: 285490. London: Academic Press.
HALL, B. K., 1978. Developmental and Cellular Skeletal Biology. London: Academic Press.
HALL, B. K., 1984. Developmental processes underlying the evolution of cartilage and bone. In M.-W. J.
Ferguson (Ed.), The Structure, Development and Evolution of Reptiles: 155-1 76. London: Academic Press.
JAW MUSCLES OF T U R T L E
61
HALL, B. K. & HANKEN, J., 1985a. Foreword. In G. R. DeBeer, The Development ofthe Vertebrate Skull: viixxvii. Chicago: The University of Chicago Press.
HALL, B. K . & HANKEN, J., 1985b. Repair of fractured lower jaws in the spotted salamander: do
amphibians form secondary cartilage? Journal of Experimental <oology, 233: 359-368.
HEATON, M. J., 1979. Cranial anatomy of primitive captorhinid reptiles from the Late Pennsylvanian and
Early Permian Oklahoma and l e x a s . Bulletin of the Oklahoma Geological Suruey, 127: 1-84.
IRWIN, C. R. & FERGUSON, M. W. J., 1986. Fracture repair of reptilian dermal bone: can reptiles form
secondary cartilage? Journal of Anatomy, 146: 53-64.
KILIAS, R., 1957. Die funktionell-anatomische und systematische Bedeutung der Schlafenreduktionen bei
Schildkroten. Mitteilungen aus dem zoologischen Museum in Berlin, 33: 307-354.
LAKJER, T., 1926. Studien uber die Trigeminus-versorgte Kaumuskulatur der Sauropsiden. Copenhagen: C . A. Reitzel.
LOVTRUP, S., 1978. O n von Baerian and Haeckelian recapitulation. Systematic ~ o o l o g y ,27: 348-352.
LUBOSCH, W., 1914. Zwei vorlaufige Mitteilungen iiber die Anatomie der Kaumuskeln der Krokodile.
Jenaische zeitschrft f u r Naturwissenschaft, 51: 697-706.
LUBOSCH, W., 1933. Untrrsuchungen uber die Visceralmuskulatur der Sauropsiden. Morphologisches
Jahrbuch, 72: 584-666.
LUTHER, A,, 1909. Untersuchungen uber die vom N. trigeminus innevierte Muskulatur dcr Selachier (Haic
und Rochen) unter Beriicksichtigung ihrer Beziehungen zu benachbarten Organen, Acta societatij scientiarum
Fennicae, 36(3): 1-176.
LUTHER, A , , 1913. c b e r die vom N. trigeminus innervierte Muskulatur der Ganoiden und Dipnrusten. Acla
societatis scientiarum Fynicae, 41(9): 1-72.
LUTHER, A,, 1914. Uber die vom N. trigeminus innervierte Muskulatur der Amphibieu, mit einem
vergleichenden Ausblick uber den Adductor mandibulae der Gnathostomen. Acta societatk srientzarum
Fennicae, 44(7): 1-151.
McDOWELL, S. B., 1986. T h e architecture of the corner of the mouth of colubroid snakes. ,journal qf
Herpetology, 20: 353-407.
OGUSHI, K., 1913. Anatomische Studien a n der japanischen drrikralligen Lippenschildkrdtc I Trionjlx
japonicus) . Morphologzsches Jahrbuch, 46: 299-562.
OSTER, G. F., SHUBIN, N., MURRAY, J . D. & ALBERCH; P., 1988. Evolution and morphogcnrtir rules:
the shape of the vertebrate limb in ontogeny and phylogeny. Evolution, 42: 8 6 2 4 8 4 .
POGLAYEN-NEUIVALL, I., 1953. Untersuchungen der Kiefermuskulatur und deren Inner\ ation bei
Schildkroten. Acta xoologica, Stockholm, 34: 241 292.
REISZ, R. R., 1980. T h e Pelycosauria: a review of phylogenetic relationships. In A. L. Panchen I Ed.,. The
Terrestrial Enuironment and the Origin of Land Vertebrates: 553-592. London: Academic Press.
RIEPPEL, O., 1976. Die orbitotemporale Region im Schadel von Chelydra serpentina Linnaeus (Chclonia) und
Lacerta sicula Rafinesque (Lacertilia). Acta anatomica, 96: 309-320.
RIEPPEL, O., 1977. Uber die Entwicklung des Basicranium bei Chelydra serpentina Linneaus (Cheloniai und
Lacerta sicula Rafinesque (Lacertilia). Verhandlungen der naturforschenden Gesellschaft Busel, 86: 153- 1 70.
RIEPPEL, O., 1978a. T h e throat musculature of Sphenodon, with comments on the primitive character states of
the throat muscles in lizards. Anatomischrr Anzeiger, 144: 429-440.
RIEPPEL, O., 1978b. T h e phylogeny of cranial kinesis in lower vertebrates, with special reference to the
Lacertilia. Neues Jahrbuch fur Geologie und Palaontologie Abhandlungen, 156: 353-370.
RIEPPEL, O., 1980a. T h e trigeminal jaw adductor musculature of Tupinambis, with comments on the
phylogenetic relationship: of the Teiidae (Reptilia, Lacertilia). zoological Journal qf the Linnean Society, 69:
1-29.
RIEPPEL, O., 1980b. T h e trigeminal jaw adductors of primitive snakes and their homologics with the
lacertilian jaw adductors. Journal of zoology, London, 190: 4 4 7 4 7 I .
RIEPPEL, O., 1981a. The skull and the jaw adductor musculature in some burrowing srinromorph lizards of
the genera Acontias, Typhlosaurus and Feylinia. Journal of ~ o o l o g y ,London, 195: 493-528.
RIEPPEL, 0.. 1981b. The skull and jaw adductor musculature in chameleons. Revue Suisse de zoologic, 88:
433-445.
RIEPPEL, O., 1 9 8 1 ~ .Die Funktion des Kragens der Ceratopsia. I n Reif, LV.-E. (Ed.): Paliiuntologische
Kursbiicher, I : 205-2 16. Munchen: Palaontologische Gesellschaft.
RIEPPEL, O., 1984a. The cranial morphology of the fossorial lizard genus Dibamus with a consideration of its
,
204: 289-327.
phylogenetic relationships. Journal of ~ o o l o g y London,
RIEPPEL, O., 1984b. T h e structure of the skull and jaw adductor musculature in the Gekkota, with comments
on the phylogenetic relationships of the Xantusiidae (Reptilia: Lacertilia). zoological Journal of the Linnean
SocieQ, 82: 291-318.
RIEPPEL, O., 1984c. Miniaturization of the lizard skull: its functional and evolutionary implicatitrns. I n
M.-W. J . Ferguson (Ed.), The Structure, Development and Evolution of Reptiles: 503-520. London: Arademic
Press.
RIEPPEL, O., 1987a. The development of the trigeminal jaw adductor musculature and associated skull
elements in the lizard Podarcis sicula. J O U Y ~of <oology, London, 212: 131-150.
RIEPPEL, O., 1987h. T h e phylogenetic relationships within the Chamaeleonidae, with comments on some
aspects of cladistic analysis. zoological Journal of the Linnean Society, 89: 41-62.
62
0. RIEPPEL
RIEPPEL, O., 1988. The development of the trigeminal jaw adductor musculature in the grass snake Natrix
natrix. Journal of <oology, London, 216: 743-770.
RIEPPEL, O . , 1989. A new pachypleurosaur (Reptilia: Sauropterygia) from the Middle Triassic of Monte San
Giorgio, Switzerland. Philosophical Transactions of the Royal Society of London, B, 323: 1-73.
RIEPPEL, 0. & GRONOWSKI, R. W., 1981. The loss of the lower temporal arcade in diapsid reptiles.
.Soological Journal of the Linnean Society, 72: 203-2 17.
ROMER, A. S., 1956. Osteology of the Reptiles. Chicago: University of Chicago Press.
SCHUMACHER, G.-H., 1973. The head muscles and hyolaryngeal skeleton of turtles and crocodiles. In C.
Gans & T. S. Parsons (Eds), Biology of the Reptilia, 4: 101-199. London: Academic Press.
SMITH, K. K., 1986. Morphology and function of the tongue and hyoid apparatus in Varanus (Varanidae,
Lacertilia). Journal of Morphology, 187: 21-287.
WEGNER, R. N., 1959. Der Schadelbau der Lederschildkrote Dermochelys coriacea Linni: (1 766). Abhandlungen
der Deutschen Akademie der Wissenschaften zu Berlin, Klasse f u r Chemie, Geologie und Biologie, 1959(4): 1-80.
WILLARD, W. A., 1915. The cranial nerves of Anolis carolinensis. Bulletin of the Museum of Comparative <oology,
59: 18-116.
YNTEMA, C. L., 1968. A series of stages in the embryonic development of Chelydra serpentina. Journal o j
Morphology, 125: 219-252.
ABBREVIATIONS USED IN THE FIGURES
ama:
ame:
amem:
amep:
ames:
amp:
ampa:
ampp:
ap.mpt:
boap:
C:
ci:
cid:
crb:
exm:
exr:
gg:
lam:
iem:
inr:
j:
lao:
mc:
mps:
mpsp:
mpss:
mpt:
mx:
adductor mandibulae anlage
external adductor
medialis-layer of the external adductor
profundus-layer of the external
adductor
superficialis-layer of the external
adductor
posterior adductor
posterior adductor, anterior head
posterior adductor, posterior head
aponeurosis of pterygoideus muscle
bodenaponeurosis (central tendon of
external adductor)
coronoid
internal carotid artery
constrictor internus dorsalis rudiment
crista basipterygoidea of basal plate
extrinsic eye muscle
externus-rudiment
Gasserian ganglion
intramandibular muscle
intermandibular muscle
internus-rudiment
jugal
levator anguli oris muscle
Meckels’s cartilage
pseudotemporalis muscle
pseudotemporalis profundus muscle
pseudotemporalis superlicialis muscle
pterygoideus muscle
maxillary bone
oc:
o.sin:
P:
pa:
par:
pf:
po:
Pq:
pt:
si
cu:
qlm:
R,:
rpl:
spc:
sq:
stp:
ta:
td,:
td,:
vcl:
IV:
V,:
V,:
V,:
VI:
VII:
otic capsule
orbital sinus
parietal
ascending process of palatoquadrate
prearticular
postfrontal
postorbital
palatoquadrate
pterygoid
quadrate
quadratojugal
quadrato-maxillary ligament
resultant force exerted by the external
adductor on the paroccipital process
rictal plate
spinalis capitis muscle
squamosal
stapes
temporal (stapedial) artery
tendon of pseudotemporalis and
pterygoideus muscles
tendon of pseudotemporalis and
intramandibularis muscles
lateral head vein
trochlearis nerve
ophthalmic branch of trigeminal nerve
maxillary branch of trigeminal nerve
mandibular branch of trigeminal nerve
abducent nerve
facial nerve (Ramus palatinus)