The development of the orbital region of Caretta caretta (Chelonia, Reptilia)

J. Anat. (1987), 154, pp. 187-200 187 With 6 figures Printed in Great Britain The development of the orbital region of Caretta caretta (Chelonia, Reptilia) SHIGERU KURATANI Department of Anatomy, University of the Ryukyus, 207, Uehara, Nishihara, Okinawa, 903-01, Japan (Accepted 16 December 1986) INTRODUCTION The orbitotemporal region of vertebrates is a highly modified part of the skull and has been one of the most intriguing subjects of cranial morphology. Such study has dealt primarily with the basic definition of the components of the neuro- and splanchnocranium (Gaupp, 1900, 1902; de Beer, 1937; Goodrich, 1930; Portmann, 1976; Jollie, 1962; Romer & Persons, 1977; Starck, 1979 a). In particular, the morphological concept of the cavum epiptericum (Gaupp, 1902) was an innovation which enabled later anatomists to homologise the complicated cranial base elements (Rice, 1920; Matthes, 1921; Presley & Steel, 1976). These works were mainly on the homology of the skeletal element itself (de Beer, 1926; Rieppel, 1976; Starck, 1979 a, b), but the interrelationship with the eye muscles, which has often been implied by some authors (Terry, 1917; de Beer, 1937), has never been extensively investigated. The present paper is intended to give a precise description of the developing orbital region in reptiles for the purpose of reconsidering the meaning of the orbital region of the developing skull in the light of functional and comparative morphology. The Caretta caretta embryos were used because it is a reptile from which it is easy to get staged embryos. MATERIALS AND METHODS One hundred and twenty Caretta caretta, (Loggerhead turtle) embryos were gathered in Shirahama, Wakayama, Japan in 1984. The eggs were taken from two sites and were probably laid by two different females. Each embryo was staged from the day when the maternal footprints were discovered for the first time. After incubation, they were fixed either in Bouin's solution to make paraffin sections or 10% formalin to make whole stained specimens according to the method of Dingerkus & Uhler (1974). The carapace length of each embryo was measured after fixation for determining the stage of development (see Table 1). The sections were cut serially in frontal, sagittal and horizontal planes and stained with Weigert's iron haematoxylin and eosin or with Azan.The sections were projected on to a screen and traced to make graphical reconstruction drawings for which the sagittal sections were mainly used. OBSERVATIONS General morphology of the orbital region Figure 1 shows a lateral view of the orbital region of the Caretta embryo at a stage where the developing skull is seemingly most appropriate for the general description of the initial architecture of the orbital region of this animal. 7-2

188 Table 1. SHIGERU KURATANI List of the sectioned embryos Carapace length Ser. no. No. (mm) Stage A-28e 4 898 II A-29e 3 9.43 II A-30e 2 9 67 II A-32e 1 116 II A-34e 1 139 III A-36e 1 166 III A-38e 1 16 76 III B-16e 3 675 I B-17e 2 7 05 I B- 18e 1 8 90 II B-26e 2 131 III B-27e 2 14 08 III B-32e 4 23 4 IV B-34e 1 26-3 IV B-36e 1 30-1 IV The orbit of Caretta develops inferolateral to the developing forebrain as an extracranial space. The walls of the orbit are composed of six irregularly shaped cartilages, each being a constituent of the neurocranium. The superior wall or roof of the orbit is composed of the taenia marginalis, the anterior wall of the planum supraseptale and the interorbital septum, the posterior wall of the pila metopica and the postorbital cartilage or the later pila antotica. An important feature of the orbit at this stage is that the pila metoptica protrudes prominently into the space of the orbit, and thereby distinctively delineates the posterior portion, the cavum epiptericum. At this stage, the formation of the inner wall of the orbit by these cartilages is not yet completed; at the apex of the orbit, the primitive optic foramen remains wide open, transmitting the optic nerve and the ophthalmic artery into the orbit. Near the base of the orbit, the margin of the cartilage is more or less deeply indented. From these cartilages originate the extrinsic eye muscles, i.e., the superior, posterior, inferior and internal rectus muscles, and the superior and inferior oblique muscles. The ophthalmic nerve (V1) traverses the orbit anteriorly, passing inferior to the superior rectus muscle, crossing over the ophthalmic artery and the optic nerve, and finally, after having passed between the superior oblique and the inferior rectus muscles, leaves the orbit to enter the nasal region. The major veins, the supraorbital and the infraorbital, are also observed to traverse the orbit posteriorly. The supraorbital vein runs inferior to the superior oblique and superior to the superior rectus muscle, while the infraorbital passes first across both the superior and inferior surface of the inferior oblique muscle, and then inferior to the internal and inferior rectus Fig. 1 (a-b). (a) A somewhat simplified reconstruction of the Caretta chondrocranium with neighbouring extracranial structures, viewed from the lateral side. Some parts of the visceral skeleton and the posterior part of the chondrocranium, including the otic capsule, are not shown. The proximal heads of three rectus muscles, superior, inferior, and posterior are situated in this cavum. (b) the chondrocranium of the same embryo. The extracranial space lateral to the pila metoptica and the postorbital cartilage is called the cavum epiptericum, the posterior portion of the orbit. The anterior portion of the inner wall of the cavum epiptericum, the pila metoptica forms the posterior margin of the optic nerve foramen. Abbreviations for all Figures are on p. 200.

Orbital development in Caretta caretta 189 1(a) 1(b)

190 SHIGERU KURATANI muscles. Both these veins thus enter the cavum epiptericum and unite to give rise to the anterior cardinal vein. The prominent pila metoptica (the anterior reflection of the flexured cranial wall), and pile antotica (the posterior reflection), are arranged at an acute angle to each other, resulting in the formation of a flexured wall with a deep hollow extracranial space called, as mentioned above, the cavum epiptericum (Fig. l,a,b). The flexured wall is pierced by the foramina for the cranial nerves, the ophthalmic artery, and for the hypophysial vein. The postorbital cartilage, which represents the posterior moiety of the flexured wall, is marked in its lower half by a deep indentation for the trigeminal ganglion. Contained in the cavum epiptericum are the proximal parts of the posterior, superior, and inferior rectus muscles, the ophthalmic artery, the anterior cardinal vein with its tributaries (the supraorbital, infraorbital and the hypophysial veins), the large trigeminal ganglion with the proximal part of the ophthalmic nerve, and the cranial nerves (Fig. 1 a). Development of the orbital region Stage I, 7 mm carapace length (Fig. 2 a, b) This is the earliest embryo employed in this study. The anterior portion of the orbit is not yet formed; it is merely bordered posteriorly by the pila metoptica and inferiorly by a pair of trabecular cartilages which are portions of the cranial base. The taenia marginalis, planum supraseptale, and interorbital septum are not formed yet, and neither is the primitive optic foramen. Posteriorly the postorbital cartilage is developing. At this stage, the pila metoptica is observed to be a complex which consists of the supratrabecular cartilage and its four processes, superior, middle, antero-inferior, and postero-inferior. The anteromedial process is not yet formed (see below). The supratrabecular portion located superior to the ophthalmic artery is the principal, and in fact, the most densely condensed part of the pila metoptica. The superior process unites with the postorbital cartilage superior to the foramen for the oculomotor nerve. This process extends upwards to become continuous with the primordium of the taenia marginalis and gives rise to the superior rectus muscle. The middle process extends between the oculomotor nerve and the hypophysial vein posteriorly to unite with the postorbital cartilage. The postero-inferior process lies just medial to the posterior rectus muscle uniting the supratrabecular cartilage with the polar cartilage. The antero-inferior process also unites the supratrabecular cartilage with the cranial base, and the inferior rectus muscle originates from this cartilage. The later pila antotica, or the postorbital cartilage, on the other hand, develops as a thick vertical cartilage wall traversing the cranial cavity. This cartilage is penetrated by the trochlear nerve where the superolateral portion of this cartilage makes the summit of the flexure. The abducens nerve penetrates the cranial base at the base of the postorbital cartilage, or at the junction of the latter and the parachordal cartilage. The nerve runs anteriorly for a short distance to innervate the posterior rectus muscle anlage. The proximal head of this muscle anlage is attached to the inferolateral part of the anterior surface of the postorbital cartilage. The oculomotor nerve passes down along the anterior surface of the latter cartilage making the groove on it for the proximal part of its course. Having penetrated the cranial wall, it innervates the superior rectus, grazing the ophthalmic artery from behind and ending in the belly of the inferior rectus muscle.

2(a) Orbital development in Caretta caretta 191 soy~~~~~i 2(b) Fig. 2(a-b). (a) Stage I Caretta embryo. Lateral view of the orbitotemporal region of the chondrocranium, along with other structures, seen from the lateral side. The posterior part of the chondrocranium is not shown. Note the low position of the optic nerve. (b) Chondrocranium of the same embryo. The pila metoptica is composed of the supratrabecular cartilage and neighbouring processes.

192 SHIGERU KURATANI Stage II, 9 mm carapace length (Fig. 3 a, b) In Stage II, the planum supraseptale, the interorbital septum and the taenia marginalis develop and constitute the superior and the posterior walls of the orbit; they simultaneously form the superior and the anterior boundaries of the primitive optic foramen respectively, thereby completing the formation of the foramen. The superior process of the pila metoptica expands to the front of and above the oculomotor nerve to unite with the newly formed taenia marginalis, thus forming the superior margin of the primitive optic foramen. The superior rectus is attached to the posterior end of this cartilage. The lateral edge of the postorbital cartilage now lies medial to the abducens foramen and this cartilage itself is not perforated by the latter nerve. The anterior continuation of the taenia marginalis, i.e. the planum supraseptale, which develops dorsal to the interorbital septum, serves as the roof of the orbit, and simultaneously bounds the primitive optic foramen superiorly. This planum gives origin to the superior oblique muscle. In the cavum epiptericum, the anlage of the posterior rectus and retractor bulbi muscles are observed to be separated from each other. The anlage of the former muscle is attached to the postero-inferior process and the latter to the basal part of the postorbital cartilage. The inner rectus muscle is found to develop from the anteromedial portion of the inferior rectus muscle which is not yet attached to any part of the chondrocranium (Fig. 1 a). Stage III. 15 mm carapace length (Fig. 4a, b) In Stage III, rather drastic morphological changes occur, especially in the region of the pila metoptica with its processes and in the pila antotica. The most characteristic change is that the postero-inferior process degenerates. This results in the fusion of the foramina for the hypophysial vein and for the ophthalmic artery, and simultaneously, the posterior rectus muscle loses its central portion of origin, and bridges between the posterior part of the supratrabecular cartilage and the cranial base. The antero-inferior process is also beginning to fade, causing the primitive optic foramen to fuse with the foramen of the ophthalmic artery. Some of the whole stained embryos have lost this process prior to the formation of the anteromedial process (see below), so that the inferior tip of the pila metoptica looks as if it is hanging in the middle of the orbit. The supratrabecular portion of the pila metoptica is beginning to develop an anteromedial process passing medially towards its counterpart and anteriorly to the posterior process of the interorbital septum, i.e., the cartilago hypochiasmatica. The superior process of the pila metoptica expands further anteriorly, rendering the cavum epiptericum still shallower. The middle process is also beginning to be reduced to form a large foramen, the fenestra metoptica, through which the oculomotor nerve and the hypophysial vein pass out of the cranial cavity into the cavum epiptericum. The trochlear nerve passes through the foramen in the taenia marginalis. The superior and inferior oblique muscles and the inner rectus muscle originate from the interorbital septum. The medial portion of the postorbital cartilage is beginning to be resorbed, but the superior and lateral edges of this cartilage remain. The latter is now to be called pila antotica. Simultaneously, the pila antotica has also moved a little posterolaterally toward the abducens nerve foramen, thus making the expansion of the cavum epiptericum less distinctive. By this stage, the pilae metoptica and antotica no longer make an acute angle. The separation of both pilae and the obliteration of the cavum epiptericum proceed still further in the following stage.

3(a) Orbital development in Caretta caretta 193 jos 3(b) Fig. 3 (a-b). (a) Partly reconstructed drawing of Stage II chondrocranium along with other structures. The taenia marginalis is indicated by broken lines. The inferior rectus is attached to the anteroinferior process and the posterior rectus to the postero-inferior process. The taenia marginalis and planum supraseptale are developing encircling the optic foramen. (b) Chondrocranium of the same embryo.

4(a) 194 SHIGERU KURATANI 4(b) ~~~~~~~~of VA- ~~~~~amp.:- \. 1- Fig. 4(a-b). (a) The orbitotemporal region of a Stage III chondrocranium with the extracranial structures. Note that the posterior rectus bridges the posterior corner of the supratrabecular cartilage and the cranial base. (b) Chondrocranium of the same embryo. Note that the postero-inferior process has degenerated and the anteromedial process is beginning to develop. The middle process is also beginning to disappear.

Orbital development in Caretta caretta 195 Stage IV. 35 mm carapace length (Fig. 5 a, b) The chondrocranium of the Stage IV embryo shows the more or less fully developed features of the Chelonian orbit as is described in the literature (in general: Kamal & Bellairs, 1980; Dermochelys: Nick, 1912; Chelonia: Fuchs, 1915; Emys: Kunkel, 1912; Chelydra: Rieppel, 1976). Specifically, the formation of the subiculum infundibuli and the cartilago hypochiasmatica are shown in these forms. The anteromedial process of the former stage, the subiculum infundibuli, has united with its counterpart on the opposite side, and united anteriorly with the cartilago hypochiasmatica which has developed as the projection of the posterior edge of the interorbital septum. This fusion occurs inferior to the optic chiasma in the midline, causing an elevation of the inferior margin of the secondary optic foramen. As a result, the level at which the optic nerve passes through this foramen has moved superiorly as compared to the Stage III position. The antero-inferior process has totally disappeared (Figs. 4b, 5), and the inferior rectus muscle is now attached to the subiculum infundibuli but remains orientated as much downwards as before. As a result, the former ophthalmic artery foramen has become confluent with the inferior portion of the primitive optic foramen. In this connection, it should be mentioned that the ophthalmic artery, which at earlier stages passed through the ophthalmic foramen, has disappeared by this stage. Thus, the newly formed optic foramen is now encircled posterolaterally by new cartilages and comes to be called the secondary optic foramen. The inner rectus, on the other hand, has moved still farther superocaudally up to the anterior edge of the secondary optic foramen. Thus, the proximal heads of the four rectus muscles, superior, posterior, inferior, and the inner rectus muscles are gathered around the secondary optic foramen as close to each other as before. The pila metoptica thus has no original cartilage part that connects directly with the cranial base. The middle process has completely disappeared, leaving a more enlarged foramen, the fenestra metoptica, which, as mentioned above, is confluent with the former ophthalmic artery foramen and the space just beneath the cartilago hypochiasmatica. On the other hand, the superior process has moved more obliquely and anteriorly to border the superior edge of the secondary optic foramen. This process now lies in a transverse plane so that it does not serve as the laterally reflected wall of the cavum epiptericum but appears to be a part of the lateral wall of the neurocranium. The basal portion of the pila antotica has moved still further laterocaudally to end close to the abducens nerve foramen. Its superior end, which is fused with the posterior portion of the taenia marginalis, also bends caudally. The retractor bulbi muscle continues to be attached solely to the pila metoptica as before. DISCUSSION In the above descriptions, it has become clear that the pila metoptica changes its form during development (Fig. 6). The two main factors or changes which seem to be involved in the configuration of this structure are the formation of the expanded interorbital septum and the rearrangement of the extrinsic eye muscles. These changes also result in the apparent obliteration of the cavum epiptericum. In the following discussion, the configuration and deformation of the pila metoptica will be illustrated first and then the two factors which are correlated with the cartilage development in the orbitotemporal region will be dealt with. Configuration and deformation of the pila metoptica The pila metoptica is comprised of the main part called the supratrabecular cartilage (de Beer, 1937; the cartilago suprapolaris: Goldschmidt, 1972), and the peripheral

196 5(a) SHIGERU KURATANI 5(b) los ch '.:.-., '. :'..'- :' Fig. 5 (a-b). (a) Graphically reconstructed illustration of a Stage IV Caretta embryo. Lateral view of the orbitotemporal region of the chondrocranium along with other structures. The subiculum infundibuli is fused with the cartilago hypochiasmatica, elevating the optic nerve. The antero-inferior process is lost. The ophthalmic artery has degenerated as well. The middle process has vanished, leaving the fenestra metoptica. (b) The chondrocranium of the same embryo. Note that the cavum epiptericum no longer exists as a separate space.

Orbital development in Caretta caretta 197 tm Fig. 6. Diagramatic illustration of the changing orbital region of the Caretta chondrocranium. The lines representing the contours of the developing chondrocranium are superimposed, assuming that the distance between the optic nerve and the cephalic flexure does not change during development. Note that the position of the optic nerve moves higher with the development of the interorbital septum and the pila metoptica shifts anteriorly during development. The pila antotica or postorbital cartilage also moves posteriorly. Black arrows indicate the movement of the cartilage elements and the large arrows indicate the shift of the proximal heads of the superior, inferior and the posterior rectus muscles respectively. processes around it, i.e. the superior, anteromedial (chondrifies later), antero-inferior, postero-inferior and the middle processes. These processes have had little mention in the literature and are provisionally named as shown above in the present study. The cartilages are all chondrifications of the primary cranial wall and the changing pila metoptica is to be illustrated through the chondrification and the degeneration of these subdivisions as follows. The supratrabecular cartilage is at first almost independently chondrified and is seen as the posterior portion of the subiculum infundibuli in the fully formed chondrocranium (Fig. 6). The postero-inferior process serves as the posterior edge of the ophthalmic artery foramen connecting the supratrabecular cartilage and the cranial base, and is the first to regress. The antero-inferior process is another element which connects the supratrabecular cartilage with the cranial base. This forms the anterior edge of the ophthalmic artery foramen. By the regression of this cartilage, the pila metoptica loses its original connections to the skull base. The middle process dis-

198 SHIGERU KURATANI appears next and the pilae metoptica and antotica become separated completely leaving the fenestra metoptica between them. Around the time the last two processses degenerate, the anteromedial process grows from the supratrabecular cartilage, and finally fuses with the cartilago hypochiasmatica. This fusion results in the formation of the posterior edge of the secondary optic foramen. In the course of these changes, the superior process also moves gradually forward and the pila metoptica as a whole looks as if it has shifted anteriorly, moving over the ophthalmic artery. A similar shift of the pila also seems to take place in other reptilian embryos that have some of the above cartilage elements (Kamal & Bellairs, 1980; Kunkel, 1911, 1912). All through the above stages of modification, the pila metoptica is always found between cranial nerves II and III, and it can be so-called wherever it is situated, although it consists of different elements at each stage of development. This seems never to have been mentioned in the literature but is important because this change does not appear to occur in other vertebrates such as placental mammals which also have a cartilage called the pila metoptica (de Beer, 1926, 1937; Presley & Steel, 1976; Starck, 1979 a, b; Jarvik, 1980). The homology of the pila metoptica, especially in relation to the ophthalmic artery, needs further study. Arrangement of the eye muscles As mentioned above, the proximal heads of the rectus muscles in Caretta have a tendency to gather around the optic chiasma during development (Figs. 5 a, 6), and these movements seem to be correlated with the anterior shift and the deformation of the pila metoptica as well as with the formation of the cartilago hypochiasmatica and the subiculum infundibuli. The postero-inferior process disappears with the movement of the posterior rectus muscle, and the antero-inferior process disappears with the upward movement of the inferior rectus muscle which finally attaches to the anteromedial process. The rostral movement of the superior process is related to the superior rectus muscle which also reaches to the posterior edge of the secondary optic foramen. This final condition of the eye muscle appears in many lower vertebrates and is regarded as the basic arrangement of the muscles, i.e. the rectus muscles are attached to the interorbital septum around the optic foramen and the obliquus muscles to the planum antorbitale or the reptilian planum supraseptale (Corning, 1900; Goodrich, 1930). However, in those forms which have an extensively chondrified cranium, the muscle migrations probably do not affect the apparent development of the chondrocranium, even if such migrations exist. Growth of the interorbital septum, elevation of the optic chiasma and the modification of the cavum epiptericum The reptilian skull is classified as being of the tropibasic type in which the trabecular cartilage narrows into a broad, vertical interorbital septum (de Beer, 1937; Starck, 1980). The formation of the latter cartilage results in the inward invasion of the extracranial space (the orbit) and consequently, modification of the inner wall of the cavum epiptericum. The narrowing begins from the anterior tip of the trabecular and continues posteriorly whereby the anterior half of the cranial flexure, i.e., the pila metoptica and a part of the taenia marginalis, is obliged to lie longitudinally. In doing so, the superior process of the pila metoptica moves forward with the proximal head of the superior rectus, and in the fully formed chondrocranium, the anterior half of the flexure does not surround the cavum epiptericum any longer but continues cranially to become a part of the planum supraseptale. The original cephalic flexure is now to

Orbital development in Caretta caretta 199 be observed merely as a faint midway curvature of the taenia marginalis (Fig. 5a,b). The dwindling of the cavum in reptilian chondrocranium development might be thus associated with the formation of a broad interorbital septum, which may be an adaptation to the relative growth of the large eyeball. Such a condition is repeated in the avian chondrocranium which has a similar extensive interorbital septum (de Beer, 1937; Starck, 1979a). Curiously enough, the reflection of the flexure is reserved in mammalian skulls as the meningeal membrane covering the trigeminal ganglion anteriorly as a part of the tentorium cerebelli (Presley & Steel, 1976). This may be due to the smaller size of the eyeball and the low grade of deformation in the orbital region. SUMMARY In the development of the orbital region of the Caretta chondrocranium, the rearrangement of the several eye muscles seems to be correlated with the apparent anterior shift of the neurocranial element, the pila metoptica. The pila consists of the main part, the supratrabecular cartilage, and five processes, the superior, middle, anteromedial, antero-inferior and the postero-inferior. The superior process forms the attachment of the superior rectus muscle and, together with the muscle, moves anteriorly during development. In the course of the anterosuperior shift of the inferior rectus muscle, the antero-inferior process degenerates and the anteromedial process is newly formed. The postero-inferior process gives origin to the posterior rectus muscle and regresses as a result of the upward shift of the muscle. All these changes are the result of the secondary arrangement of the eye muscles gathered around the secondary optic foramen which has been newly formed through the pila metoptica deformation. The elevation of the optic nerve which is brought about through the formation of the interorbital septum, is another factor that brings about the above changes. Because of these changes, the anterior part of the cranial flexure, the pila metoptica, lies in a longitudinal plane and consequently it, as well as the cavum epiptericum, is obliterated and a large antero-inferiorly opening extracranial space, the orbit of the reptile, is produced. I am most grateful to Mr. H. Tanase of Seto Marine Biological Laboratory, Kyoto University, for his help during the search for turtle eggs on Shirahama sea shore, to Dr. M. Tasumi of the Department of Zoology, Kyoto University for providing me with the ideal environment to carry out this study and to Professor Dr. S. Tanaka for his critical reading of the manuscript. REFERENCES DE BEER, G. R. (1926). Studies on the vertebrate head II. The orbitotemporal region of the skull. Quarterly Journal of Microscopical Science 70, 263-370. DE BEER, G. R. (1937). The Development of the Vertebrate Skull. London: Oxford University Press. BURDA, D. J. (1965). Development of intracranial arterial patterns in turtles. Journal of Morphology 116, 171-188. CORNING, H. K. (1902). Ueber die vergleichende Anatomie der Augenmuskulatur. Morphologisches Jahrbuch 29, 94-140. DINGERKUS, G. & UHLER, L. D. (1977). Enzyme clearing of alcian blue stained whole small vertebrates for demonstration of cartilage. Stain Technology 52, 229-232. FUCHS, H. (1915). Ueber den Bau und die Entwicklung des Schaedels der Chelone imbricata. Ein Beitrag zur Entwicklungsgeschichte und vergleichenden Anatomie des Wirbeltierschaedels. Erster Teil: Das Primordialskelett des Neurocraniums und des Kieferbogens. In Reise in Ostafrica in den Jahren 1903-1905. Wissenschaftliche Ergebnissee (ed. A. Voeltzkow), vol. 5., pp. 1-325. Stuttgart: E. Schweizerbart.

200 SHIGERU KURATANI GAUPP, E. (1900). Das Chondrocranium von Lacerta agilis. Ein Beitrag zum Verstaendnis des Amniotenschaedels. Anatomische Hefte 15, 433-595. GAUPP, E. (1902). Ueber die Ala temporalis des Saeugerschaedels und die Regio orbitalis einiger anderer Wirbeltierschaedel. Anatomische Hefte I. Abtheilung 19, 155-230. GOLDSCHMIDT, A. (1972). Die Entwicklung des Craniums der Mausvoegel (Colidae Coliformes Aves) I. Morphologisches Jahrbuch 118, 105-138. GOoDRICH, E. S. (1930). Studies on the Structure and Development of Vertebrates. London: Macmillan. JARVIK, E. (1980). Basic Structure and Evolution of Vertebrates. London: Academic Press. JOLLIE, M. (1962). Chordate Morphology. New York: Reinold. KAMAL, A. M. & BELLAIRS, A. D'A. (1980). The chondrocranium and the development of the skull in recent reptiles. Biology of the Reptilia 11, 1-263. KUNKEL, B. W. (1911). Zur Entwicklungsgeschichte und vergleichenden Morphologie des Schildkroeten Schaedels. Anatomischer Anzeiger 39, 354-364. KUNKEL, B. W. (1912). The development of the skull of Emys lutaria. Journal of Morphology 23, 693-780. MArrTBS, E. (1921). Zur Entwicklung des Kopfskeletes der Sirenen. II. Das Primordialkranium von Halicore Dugong. Zeitschrift fuer Anatomie und Entwicklungsgeschichte 60, 1-306. NICK, L. (1912). Das Kopfskelett von Dermochelys coriacea. Zoologisches Jahrbuch, anat. Abt. 33, 1-238. PORTMANN, A. (1976). Einfuehrung in die vergleichende Morphologie der Wirbeltiere, Ste Revidierte Auflage. Basel: Schwabe & Co. PRESLEY, R. & STEEL, F. L. D. (1976). On the homology of the alisphenoid. Journal of Anatomy 121, 441-459. RICE, E. (1920). The development of the skull in the skink Eumeces quinquelineatus L. I. The chondrocranium. Journal of Morphology 34, 119-216. RIEPPEL, 0. (1976). Die Orbitotemporale Region im Schaedel von Chelydra serpentina Linneaus (Chelonia) und Lacerta sicula Rafinesque (Lacertilia). Acta anatomica 96, 309-320. RoMER, A. S. & PERSONS, S. (1977). The Vertebrate Body, 5th ed. Philadelphia: Saunders. STARCK, D. (1979a). Vergleichende Anatomie der Wirbeltiere, II. Berlin: Springer Verlag. STARCK, D. (1979b). Cranio-cerebral relations in recent reptiles. Biology of the Reptilia 9, 1-38. TERRY, R. J. (1917). Primordial cranium of cat. Journal of Morphology 29, 281-434. VOIT, M. (1909). Primordialkranium des Kaninchens unter Beruecksichtung der Deckknochen. Anatomische Hefte 38, 425-616. aip, antero-inferior process of the pila metoptica; amp, anteromedial process of the pila metoptica; btr, basitrabecular process; ch, cartilago hypochiasmatica; fin, fenestra metoptica; gc, ganglion ciliaris; gt, ganglion trigemini; hv, hypophysial vein; ic, internal carotid artery; ios, interorbital septum; iov, infraorbital vein; mp, middle process of the pila metoptica; na, nasal capsule; oa, ophthalmic artery; of, primitive optic foramen; oi, m. obliquus inferior; os, m. obliquus superior; pa, pila antotica; pc, parachordal cartilage, Abbreviations for Figures pip, postero-inferior process of the pila metoptica; PM, pila metoptica; po, postorbital cartilage; pq, palatoquadrate cartilage; pss, planum supraseptale; ret, m. retractor bulbi; rinf, m. rectus inferior; rint, m. rectus interior; rp, m. rectus posterior; rs, m. rectus superior; si, subiculum infundibuli; sof, secondary optic foramen; sov, supraorbital vein; sp, superior process of the pila metoptica; st, supratrabecular cartilage; tr, trabecula cranii; tc, trabecula communis; tm, taenia marginalis; vca, vena cardinalis anterior; II-VII, cranial nerves.