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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. 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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)