The development of the skull of the turtle with remarks on fossil reptile skulls.код для вставкиСкачать
THE DEVELOPMENT O F THE SKULL OF T H E TURTLE, WITH REMARKS ON FOSSIL REPTILE SKULLS RALPH F. SHANER Department of Anntonzy, Universitil of Alberta, Edmonton, Alberta, Canada SIXTEEN FIGURES This paper is the report of a study undertaken at the suggestion of a distinguished paleontologist, who lamented the lack of knowledge of the development of the reptile skull. There have been of course numerous studies on the reptile skull, as the long bibliographies of Gaupp (’06) and others show. Some of Rathke’s pioneer work in vertebrate embryology was done in this field. The renewed impetus to the study of the skull that Huxley’s Croonian lecture gave moved W. K. Parker to investigate the reptile as thoroughly as the technical means of the time allowed. More recent studies, however, have fallen into two rather narrow groups and have concerned themselves either with the story of certain parts of the skull or with detailed descriptions of single embryonic stages. From neither group can one gather a very clear idea of just how the adult reptile skull comes into existence. The study here reported is an attempt to apply modern methods to the older and broader problem, to give a straightforward account of the development of a representative reptile skull from the precartilaginous to the adult stage. The interest of most recent writers on the development of the reptile skull has lain in comparative embryology, and interpretative discussions have been chiefly comparisons of the form studied with other reptilian chondrocrania or with those of amphibia. I n the study here presented, the author 343 THE ANATOXICAL RECORD, VOL. 32, NO. 4 Iias sought for any light tlie developmental story might throw apoii the adnlt reptile skull of living a i d fossil forms. A t f l i c k clnd of this paper Ihcrc is atltlcd a short discussion of the Fossil reptile skull frwin the standpoint of embryology. 1’11(1 turtle, C,’hrysemys marginata, lias bcc.11 used for material iii this work, partly because of its availability, partly l ) ~ ( m i s cof tile writer’s previous esperieiice wit11 it, aiitl 1)ill.t ly l)ecaiis~of tlie possible value its e m b r p l o g y might liavt~ f o r s t i i d ~ ~ of t s fossil forms. Despite its spccializcd ~*i~l’>t~ tlic ) i itnrtlc ~, still rclmaiiis our hest living example of a loiig-departccl aiiimul world. It is much iieurer the gcncrali z d l’ermiaii vertebrates tliaii 2111)- living form c w i l F ;ivailable for embryological study. Tlic s t o r - of tlic turtle skull falls naturally into two partst lie tle\vlopmerit of the clioiitli.ocraiii~lmmtl the rqjlacemeiit of t l i c csartilagiiioiis skiill hy the 1)oiiy oiic. THE CII0SI)KOC’RA~IUIL In (’1irj-sem;vs the cartilaginous skull reaches its greatest ( l ~ v ~ l o j ~ min ( wRt l!)-mm. embryo (figs. 11 to 13). Tlic braiii is then c ~ c l o s e din aii iricomplcte cartilaginous shell. Thc:, pilrts of tlic hraiii hcliind tlie Iiypopliysis lie iii a Imx, tlic floor of which is foi*metl of cartilage laid domi o i l either side of the notocliorti and of remains of the hypoglossal vertehixie. tlie sides by tlie otic capsules, a i d the roof 1);- an estciision of tile last t o foi*ma tecaturn. Tlic parts of the 1)rain aiiterior l o the hypophysis lie in a sczilepaii-sliapeti structure k i m w ;is tlic plarium supraseptale. T h e plaiium is supportetl 1))m i iiiterorhital septum. “lie septum is joiiied to the posterior part of thc skull 11)- a l--shapecl bar, tlie trabecula craiiii. A n t cbriorly, the interorbital septum contililies between tlicl LN the nasal septum. ( ~ l t ’ i i ( ~ tcapsules ol*~ T l i ~remaiiiing pai.ts of tlic! clioiiclrocranium arc not coiiwiwd with the hixiii. I,atei*d to tlie otic capsules alreacl!. mentioiicd a r e foimd the quadrate cartilages. Each quadrate cartilage is hollo~vf o r the reception of the midcllc~ear. 111 ntltlitioii, it bears aii aiiterior pterygoicl process and articu- DEVELOPMENT OF THE SKULL OF THE TURTLE 345 lates belov- with lleckel’s cartilage of the lower jam-. The rostra1 end of the skull is formed by the tm-o nasal capsules. To follow the whole of such a complicated structure from stage to stage is a hopeless task. It is better to divide the skull up into convenient parts a i d to treat of each in turn. Accordingly, 1 shall discuss tlic following : 1) Prechordal region, i.e., the skull proper anterior to the hypophysis, 2 ) Parachordal aiid hypoglossal regions. 3 ) Otic capsules and columella auris. 1) Quadrate a i d Meckel’s cartilage. 5 ) Xasal capsules. P rec h ord nl ,regio n The first clement of the chondroeranium anterior to the hypophysis to appear is a pair of rod-like trabeculae craiiii (figs, 1 to 3 ) . They lie close to the miclliiic and extend from the hypophysis to the nasal sacs. I n the 6-mm. stage figured, they are the only parts of the skull that are choiidrified. The secoiid element, also present in the same stage, is an ill-defined arch of mesenchyma attached at either root to the caudal tip of a trabecula and springing across the space filled with the hypophysis. In the 6-mm. stage the arch is penetrated by the oculomotor nerve and deeply notched f o r the trochlcar nerve. The best name for this element is ‘miclbrain arch’ (arcus mescnceplialicus). It is the ‘middle tra1)ccula’ of Ratlike, the ‘alisphenoid-platten7 of Sewertzoft’, and thc ‘ splieriolateralknorpel’ of Gsupp. Ratlike’s name is confusing, the others assume unjustifiable associations witli adult bones. The third clement has appeared in a slightly older embryo of 5.75-mm. length (figs. 4 to 6). Here one finds two lateral plates, one on either side of the forebrain, anterior to the optic nerve, and at first loosely attached to the trabeculae cranii. The two lateral plates can he called the laminae proseiicephalicae. It will be noticed, in passing, that the whole prechordal part of the skull is at first quite unconnected to the notochord or to any other part of tlie skull (fig. 3 ) . I n addition, 346 RALPH F. SHANER the long axis of the prechordal part makes a riglit angle with that of the rest of the skull, in conformity to the general outline of the brain at that time (fig. 2). Each forebrain plate is at first attached to an independent trahecula cranii, of the sort found in the 6-mm. embryo (fig. 1). The loose connection of the plate to the trabecula becomes a more intimate one, and at the same time a center of chondrification appears between the trabeculae cranii. A general fusion of all structures ensues, and the scalepan-like support for the forebrain comes into being (fig. 4). ABBREVIATIONS A.m., niidbrain a i eh ~J.C., Sleekel's cartilage A?&.,angular bone A.op.. ophthalmic a i t e i y Boc., basioccipital bone Bsp., hasisphenoid bone P a , columella auris Coin., complementary bone C . ~ . H , .lateral , iiasal cartilage C.p..n., paranasal cartilage C T . ~ . ,crista parotica C.S., crista sellaris C . I , 2 , 3 , cervical vertebrae D., dienceplialon D m t . , dental bone Bnc., exoccipital bone Rpo., epiotie bone B p t . , epipterygoid P.b., forelmtin F.b.p., posterior basicrauial fe1iesti;i Pxntl., foramen f o r endo1yrnpli:itic duct Fh., fenestrz for liypopliysis F.m.-x., nietotir fissure, foramen of vogus nerve I?., frontal lione E'.ve. fenestra 1 estibuli h'.tt-m, foiamen f o r tlie cereljral nerves G o . , gonial hone TI.b., hindbrain H I / . , lryoid cartilage I€.Z,2,5,hypoglossal I ertebtae L p . , lamina prosrncephalica M.b., midblain Mx., maxillary bone N.c., nasal capsule A 7 4 nasal sac O.C., otic capsule Opn., opisthotir bone P.,palatine lmie P.u., abducens process Par., parietal bone P.et., epipterygoid process P.t., iiiterhyial process PZ.9., planurn supraseptale Pof., postfrontal bone P.pr., pila prootica P.pt., pterygoid process Prf., prefiontal bone Pr m., premaxillary bone Pro., prootic bone Pt., pterygoid bone Q., quadrate cartilage and bone Q..?., quadratojugal bone Su., surangular h i e S.L., iuterorbital septum S.n., iiasal septum Noc., supra-occipital bone Sq., squamosal bone T o . , vomer Z.C., trabecula craiiii T . m , taenia mxrginalis Z'.p., tectum posterior %., zygoma it-mt., cerebral iicrres DETELOPMENT O F THE SKULL O F THE: TURTLE 347 Rleaiiwliile the ends of the two trabeculae craiiii grow forward between the nasal sacs. Beyond t h e cerebrum they form a single vertical plate (fig. 4) wliicli becomes a part of the nasal septum. c /-\ Pigs. 1 t o (i W a s models of the clionilrocrania of embryos of Clirysemys marginata. I a n d 2 , riglit side; 3, dorsal side from a 6-mm. embryo, Alberta Ernbryo1ogic;il Collection, series 110; 4 aiiil 3 , riglit side; 6, dorsal side from a 3.75-mm. eml)rTo. A.E.C. 107. X 15. 348 R A L P H I?. SHANER The two forebrain laminae are next bent toward each other and partly fused together. The wide-open V is converted into a U with flaring limbs above. The fused ventral parts of the laminae together with one underlying fused trabecula make the interorbital septum (figs. 7, 9, Il), while the upper flaring limbs of the laminae form the planum supraseptale of the completed chondrocranium. While the above changes are taking place, the midbrain arch is also growing. I n the first stage modeled (fig. 1) it encloses only the oculomotor nerve. I n the next model (figs. 4, 5) the arch surrounds the trochlear nerve and the ophthalmic artery, and extends in two flanges, one on either side, along the midbrain and diencephalon toward the optic nerve. The nerve then lies in a notch. The optic notch is converted into an optic foramen by the fusion of the flange of the midbrain arch with the forebrain lamina (figs. 7,s). A process of the forebrain lamina pushes backward beneath the nerve at the same time, between it and the trabeculae, and forms the floor of the optic foramina. While the midbrain arch grows forward, it also extends backward and joins the tip of the notochord (fig. 4 ) , thus forming the first connection of the prechordal region with the rest of the skull. At the same time two slender mesenchymatous processes push forward from the otic capsules. Each process is penetrated by the abducens nerve, and on that account may be called the abducens process. I n the 5.75-mm. embryo modeled (fig. 6), each process is still free from the midbrain arch; shortly afterward, fusion with it takes place, and the union of the prechordal region with the rest of the skull is accomplished (compare figs. 6 and 9). The subsequent history of the midbrair, arch is one of differentiation and reduction. The sharp bend in the skull is reduced (compare figs. 4 and i), the flange-like extensions of the arch (fig. 4) tear away from it, but remain attached to the forebrain lamina and form the posterior boundary of the optic foramina (figs. 7, 9). A persisting remnant of the connection of the flange with the parent arch forms the DEVELOPMENT O F THE SKULL O F THE TURTLE 349 taenia marginalis of other reptiles. The midbrain arch itself is reduced, the oculomotor and trochlear nerves and the ophthalmic artery regain their freedom. The arch then flattens down into a bar behind the hypophysis, the crista sellaris of Figs. 7 to 10 Wax model of the chondrocranium and membrane bones of an 8-mm. embryo of Chrysemys marginata, A.E.C. 104. x 15. 7 and 8, right side; 9, dorsal side; 10, ventral side of nasal capsule. 350 RALPH F. SHANER Kunkel (figs. 11, 13), which continues to divide the fenestra basicraiiialis posterior from the foramen hypophyseos. The early midbrain arch bears two pointed processes (fig. 6, P.pr.). They persist and are molded into the pilae prooticae of the mature chondrocranium (figs. 7, 9, 11). Behind the pila prootica the trigemiiial nerve leaves the brain case. Parachordal a i d hypoglossal regions I n the youngest stage modeled (6 mm., fig. 3 ) , the notochord extends backward beneath the hindbrain without any special covering of precartilaginous tissue. This area bet~veeiithc otic capsules is gradually filled in from behind forward with unsegmented mesoderm (figs. 6, 9). The notochord lies at first above the floor plate, and tlien is embedded into it. Chondrification follows from no specially defined centers. When this part of the skull floor is finished, a small fenestra basicranialis remains, behind the crista sellaris (fig. 13). The extreme posterior part of the slrull floor, the l-lypoglossal region, has a more interesting history. Three precartilaginous hypoglossal vertebrae are formed, corresponding to the roots of the hypoglossal nerve (figs. 1 to 3 ) . The first pair of hypoglossal arches are short and stubby, the rest differ in no wise from the cervical vertebrae that follow. The neural arches of the hypoglossal vertebrae at first lag behind those of the cervical vertebrae (fig. 6 ) , and their bodies are fused into a common mass which joins the floor of the skull. The first hypoglossal foramen seems t o be obliterated. Later, the hypoglossal arches grow rapidly and form a single big process which pushes up heliind the otic capsule (figs. 7, 9 ) and fuses with it. A large cleft always remains between the common hypoglossal process and the otic capsule for the passage of the vagus nerve-the fissura metotica of the mature chondrocranium (figs. 9 , l l ) . The entire hypoglossal regioii is chondrified in an 8-mm. embryo. No distinct centers could he found in the bodies of the vertebrae. An ill-defined center can be distinguished in each neural arch. I ~ E V E I J O I ’ J I E S T O F T H E SKTJLL O F T H E TCRTLE 331 O t i c capsule and colunzella atiris The otic capsule is partly sketcl~erlin precartilage iii tlic (i-mm. stage (figs. 1, 3). Tlie basal and lateral portions between the facial aiid glossopliar!-ngeal nerves a r e definite enough to be modeled. The rest of the capsule is outliiiecl iii precartilage in the next stage modeled (figs. 4, 6 ) , and is well clionclrified a t 8 mm. (figs. 7, 9). No definite centers of cdiondrifieation could he made out. I n the turtle tlie glossopharyngeal nerve lies very close heliind the otocyst, and the facial nerve similarly skirts around its anterior margin. When the prccartilaginous otic capsule is laid down, it surrounds the first p a r t s of both nerves. The glossopliarpngeal runs into the large hole 011 the median side of tlie otic capsule together with the acousticofacial complex. The upper p a r t of the I-acnitj- is filled with the endolymphatic duct (fig. 6 ) . A bar of cartilage then separates tlie ninth from the otlier nerves, so that the former enters the otic capsule through a distinct foramen (fig. 9 ) , passes through the cavity of the capsule, and emerges from a special foramen behind (fig. 7)an arrangement that is permaiient. The intracapsular course of the facial nerve is shorter arid has been questioned lo>- Terry (’19). I n the 3.75-mm. embryo (fig. 6 ) the combined acousticofacial trunk enters the otic capsule, aiid the iiidepeiiclent course of tlie facial nerve does not begin until the acoustic nerve is spread out over the otocyst. Tlie little bar of cartilage anterior to the nerve exit, tlie prefaciai commissure, seems as much a p a r t of the otic capsule a s any otlier part. It seems correct, therefore, to speak of a n intracapsular course f o r the facial nerve in turtles. The intracapsular path of the facial nerve is eventually partitioned off from the rest of the capsular cavity. The large vacuity in the median wall of the otic capsule is gradually subdivided into several openings, one each f o r the glossopharyngeal nerve, endolymphatic duct, a i d facial nerve, and two f o r the acoustic nerve. One or more foramina for hlood vessels also remain. 352 R A L P H F. SHANER The dorsal crests of the otic capsules extend upward and form the tectum, the roof of the completed chondrocranium. The columella auris of the turtle is simpler than in some other reptiles. When fully laid down in cartilage, it is a dumb-bell-shaped structure. The long curved shaft is divided in the middle by a constriction. The inner head o r operculum fits into the foramen vestibuli, and together with its part of the shaft constitutes the columella proper. The rest of the shaft and the outer head make up what is known a s the extracolumella. The outer head or insertion piece of the extracolumella bears a tapering interhyal process (fig. 11)’which in a 19-mm. embryo is attached by a non-chondrified shred to the tip of Meckel’s cartilage. Much interest has been lavished on the stages leading up to the cartilaginous columella auris. The evidence of my material confirms the work of Miss L. S. Smith (’14) on the same species and harmonizes with the results of Shiino (’14) and Golby (’25) 011 the crocodile and alligator. I n the 6-mm. stage (fig. l ) , the turtle columella, extracolumella, and interliyal process are all laid down as one piece of precartilage. The extra-cdumella and the interhyal process show the most advanced precartilage. The precartilage of the shaft and operculum fades out into the younger sort of which the otic capsule is made. The operculum is distinct, however, from the more or less nebulous otic capsule. The precartilage of the extracolumella is in the same stage of development as is that which forms the hyoid apparatus, a sort considerably adraiiced over the precartilage of the otic capsule aiid Meekel’s cartilage. It seems very likely that, as Miss Smith states, the interhyal process at a slightly earlier stage joined the hyoid arch. The union must have been very transient; the interliyal process of the stage modeled (fig. 4) is already turning toward Meekel’s cartilage. I n two other embryos of nearly the same age (A.E.C. 108, 6 mm., A.E.C. 109, 7 mm.) the interhyal process definitely joins the tip of Meckel’s cartilage. DEVELOPMENT O F THE SKULL O F THE TURTLE 353 In a 7-mm. embryo a constriction appears in the shaft where it passes over the first pharyngeal pouch. The extracolumella is then marked off from the columella in the narrower sense. In an 8-mm. embryo centers of chondrification appear in the extra-columella and columella. From this time the columella auris is truly subdivided. A third center in the interhyal process is doubtful; it is imperfectly chondrified. In later stages the interhyal process dwindles (figs. 7, 11). In the adult the extracolumella remains cartilaginous ; the rest is replaced by bone, a trace of which can be found in a 28.5-mm. embryo. The old question whether the columella auris is derived from the hyoid or from the otic capsule, o r both, is an unreal one. I n the first place, the division of the columella is a secondary one that appears only with chondrification. The simple precartilaginous columella, like any other piece of precartilage, is laid down in situ. It is not budded off from surrounding structures. After all, the columella simply develops out of the head mesoderm as a high light does in a photographic plate, correctly fashioned and properly placed from the start. Quadrate and Meckel’s cartilage A fragment of the quadrate and a small h-leckel’s cartilage are sketched in prechondrial tissue in the first stage modeled (fig. 1). Meckel’s cartilage is temporarily joined to the growing quadrate in a slightly older embryo (5.75 mm., fig. 4 ) . It regains independence and shows traces of cartilaginous matrix in a 7-mm. embryo. At 8 mm. the right and left cartilages fuse at their anterior tips without the aid of an intercalated cartilage. The fused tips are fashioned to conform to the peculiar shape of the lower jaw and the articular facet f o r the quadrate is modeled out (figs. 11, 15). The fragment of the quadrate present in the 6-mm. stage (fig. 1) expands into a definite quadrate in the next stage modeled (fig. 4). I t then consists of a dorsal and posterior 354 RALPH F. SHAXEIL mastoid portion, a rod-like articular part temporaril;-- fused with Meckel’s cartilage, and a pterygoid process. I n a 7-mm. embryo cartilage matrix appears in the mastoid part aiid the quadratomecltelian joint is laid out. I n an 8-mm. embryo (fig. 7 ) the mastoid part is enlarged, aiid an ascending epipterygoid process, homologous with the ‘columella ’ of ltiiiocraniate lizards, is added t o the pterygoid process. Tlie whole is now in cartilage. While the chondrocranium grows to its maximum in the 19-mm. embryo (fig. ll), the mastoid part of the quadrate is hollowed out to accommodate the middle-ear outgrowth from the first pharyngeal pouch. The pterygoid process of the quadrate of embryos around 6 mm. in length (fig. 4) lies just above the ruclimciitary dental ridge of the upper jaw. The pterygoid process thus bears the same relation t o the upper jam that Rleckel’s cartilage does to the lower. The quadrate, its pterygoid process, and Meckel’s cartilage form an oral visceral skeleton w r y much like that found in salmon embryos (Gaupp, ’06). Nasal capsule The first part of the nasal skeletoii to appear is the septum, the rostra1 part of which develops on tlie fused tips of tlic trabeculae craiiii (fig. 4). Tl‘hen the nasal capsules appear (8 mm., fig. 7 ) , they extend backward along the interorbital septum for some distance. Tlie part of the interorbital septum that lies between the capsules is added to the nasal septum in the mature cartilaginous skull. Each nasal capsule arises from two distinct cartilages which appear in the 8-mm. stage (figs. 7, 10). Tlie smaller medial paranasal cartilage lies along the ventral margiii of tlie iiasal septum. The larger lateral cartilage forms tlie side arid roof of the capsule. To form the roof, the lateral cartilages fuse with the dorsal margin of tlie nasal septum--a process already begun at this stage aiid completed in the iiext older one modeled. The kioor of the nasal capsule is completed by fusion of the paranasal with the lateral cartilage, and with the ventral margiii of the septum. A persisting DEVELOPNEXT O F T H E SKULL O F THE TTJRTLE 355 slit on either side of tlie \-eiitral margin of tlie septum forms the prepalatiiie foramen. The tips of the two nasal cartilages are distinct at the posterior choaiiae long after the capsule is complete. The general contour of the nasal capsule is governed hy the nasal sacs. In the completed cartilaginous capsule (fig. 11) one caii distinguish hetweeii a ventral cylindrical respiratory part, which forms a direct passage between thc two choanae, and a dorsal dome-shaped olfactory portion. The line of separation is marked by a slight fold on tlic lateral wall of the capsule aiid by a parallel ridge on its iiirier surface. A small ~ioclule,tlie pila supraglandularis of Kuiiltel, which is attached to the nasal septum, may separate the two parts medially. In tlie mature cartilagiiious nasal capsule, tlie iipper lip of each anterior clioaiia is deeply incised to accommodate a dorsal gland, which spreads out between the capsule and the bones that form over it. The fiiiished cartilaginous skull, the several parts of wliicli have been followed in development, is found in a 19-mm. embryo (figs. 11, 12, B ) . Icunltel’s ( ’12). admirable and exhaustive descriptioii of the mature chontlrocranium of Emys is easily accessible, and 110 special discussioii of this stage iii Chrysemys need be attempted here. DEVELOPMEKT OF T I I E ADULT SKI‘LL As the choiidrocraiiium approaches its maximum, the memhraiie hones appear around it, takiiig up at oiice their permaiieiit positions and relations. The chondrocranium is no sooner finished than it degenerates. Much of it is replaced 1,y bone developed from centers located in the cartilage matrix. This second class of cartilage bones comes into correct articulatioii with the membrane bones to finish off tlie adult skull. The remaining portioiis of the chondrocraiiium, in the turtle a t least, are largely resorbed. T’he three steps, then, in the development of tlie adult skull, which caii now be followed in detail, are : 1) Ih-elopment of memhraiie bones. 356 RALPH F. SHAWER 2 ) 1)evclopmeiit of cartilage lioiies. 3 ) Ihgeiieratioii of t h e c.11OII drocraiiiii ni. *If? )>I 1) )'I2 It P 110 I ) V.S 'l'licl first memhraiie Imies are fouiicl in an 8-mm. emhrJ-o which the squamosal, prefrontal, maxillar>-, ant1 dental boiies appear. In the 19-mm. stage (figs. 11, 12, 13) all membrane bones are present but the parasphenoid and the doubtful membrane element of the hasioccipital. The last two are found in the oldest embryo modeled (figs. 14, 15, 16). The memhrane bones of the turtle skull fall into six groups : Group I. Dental, angular, suraiigular, gonial, and comj)lemeiitary h i e s . These form the greater part of thc lower ( fig. i ) ,in J?I%-. ( t roup 1I . Parasplieiioid, palatine, ptcrygoid, vomei-, ant1 maxillary ?,ones. These form the roof of the month, supplemtwt the floor of the ctioric~rocl.aniumanterior to the Iiypophysia, aiid iii tlie adult form tlie h x c of the skull over the samv area. ( i i*oup 111. Parietal arid frontal 1)oiitls. These two cornp l d c . the 1.0of of tlie brain casc. ( f r o ~ p11'. E'refroritnl, postfroiital, zygomatic, p;irts of the ~)alntiiiea i d of the maxillary 1,ones. This well-tlc.fiiied gi*oiip malccs n p the orbit. Group T.'. Premaxillary boiic. Tlic premaxil1ar~-is the s o l t a ixyJresentatire iii turt1c.s of tlic group of memhraiie 1)oneh that tlevclop around the iiasal capsule. In otlier reptiles tlic1 irasal and septomaxillary bones w ~ ~ i i lfall d here. (froup VI. Squamosd R I M I qnadratojugal hones. Both of tliese are closely related to the quadrate cartilage a i d bone. Wietlier or no thcsc g ~ o u p shave aiiy sigriificance outside reptiles the writer leaves to others more skilled in following the intricacies of skull development in other vertehrate classes. Of the value of the groups in understanding thc reptile skull more d l be said below. DEVELOPMENT O F T H E SKVLL O F T H E TURTLE 357 Figs. 11 to 13 TVax rnodel of the clioritll.ocl.:rriiurri and niciii1)r:ciir lmies of a 19-mm. eml)r>o of Cliryseniys rii:crgiiiat:i, A.E.C. 103. x 11. 11, lcft sitlc; 12, riglit side; 13, ieritral side. 338 IlALPH F. S H B S E R (’artilnge hoizes ‘I’lie bones which arise in cartilagc arc all fouiicl I)eliiiitl the hypophysis. They are s h o ~ v i i iii thc oltlcst embryo modeled (28.5 mm., figs. 14, 15, 16). The basispheiioid arises from two centers. The bone so formed fuses with tlie membraiie-bone parasplieiioitl just anterior t o it. The parasphenoid lies lieiieatli tlie li~-pophysis ; it closes off tlie hypophyseal fenestra of the clioiiclrocratiiii~~. Tlie lateral boiiiiclaries of the fencstra, i.e., the arms of the Y-shaped trahecula craiiii (fig. 13), later ossify a s cartilagc bone and fusc with tlie parasplicwoid beiic~~tli to form tliv sliallow pocket in which tlie Iiypophysis rests. ‘I’lie adult h s i sphenoid is theref ore formed of two cm+lage-hoiie clement s, the basisphenoitl proper am1 the ossified p a r t s of the trnhecnla cranii, and the memhi*aiie-hoiie pai.asplieiioic1. The basioccipital also arises from two centers. The hone extends back into the occipital coiid~-le. Aiiteriorly, the h s i occipital aiiiiexes two delicate lamellae which lie heneath thr. cartilage floor atid which are p~-obahlyof mcmbraiie hoitc. The basioccipital in Cllirysemys is a l ~ a p sdistinct from tlic exoccipitals. I n Chrysemps tlie extreme lateral p a r t of tlic1 cartilage floor, the crista substapedialis of Iiniiliel, seems t o lie i q l a c e t l by R tiny ossicle that remains iiitiepeiitleiit of tlie Iiasioccipital. The exoccipital o r pleui.occipita1 hones prohahly ossify f rorn several centers which could not be clearly distinguished. Tlic bony matrix extends d o ~ winto the side of the occipital coiitlyle and up into tlie hypoglossal or exoccipital process. In C‘hrysemys the exocacipital does not fusc with the opisthotic. The epiotic is coiitiiinous in tlie stage modeled with tlic. supra-occipital, the ossification in the tectum. Tlie two arc’ usually described as distinct lmies mcoiidarily fused. Yo trace of secondarj- fusion appears in the 28.5-mm. emhryo. The tecatum, it shoalcl he remembered, is a n exteiision of the otic capsules atid has n o coiiiiectioii with the occipital cartilage. In the 28.5-mm. embryo the supr;i-occipital likewise seems to lie a n extens;oti of the two elliotics. DEVELOPMEST O F 'L'HE SIiPLL OF THE TT-HTLlC 359 menibraiic bones, and cartiFigs. 14 t o 16 Wax model of the elioiidroera~~iuiii, lage bones of :I. 28.5-niui. embryo of ClirpemJ-s margiiint,a, 4.E.C.106. x 7. 14, left side; 1.7, riglit. side; 16, ventral side. TIIE :\XATOMICAL RXCORr). VOli. :12. NO. 4 360 RALPH F. S H A N E R The quadrate, exclusive of the pter:-goid process, ossifies as tlie quadrate bone. Before ossification sets in, the cartilage beneath the squamosal degenerates, and tlie large hole left in the quadrate remains, although covered by the squamom1 bone. The pterygoid process breaks away from the quadrate cartilage (fig. 14) and ossifies into the tiny epipterygoid hone, which completes the lateral wall of the brain case. ‘Iko more cartilage bones, not directly connected with tlie s k i i l l ai-c fourid in the 28.5-mm. embryo. The articular bone appears beneath tlie quadratomeckelian joint in Meckel’s cwtilagc (fig. 3 5 ) . The opercnlum of the columclla anris sliows a trace of ossification. The extra-columella remains cbartilaginous throughout life. ljsgeneration of the chondvoct-aniwm ‘1’11~~chondrocranium behind tlie hypophpsis is replacecl by cartilage bones. The extra-columella is the only pcrsisting cltrtilagirious structure in this region. The pilae prooticae are degeiieratiiig in the 19-mm. and the 88-mm. embryo. They disappear witliout trace in the ;Id111 t. The rest of tlie clioiidrocranium, the trabecula cranii (exwpt tlie parts incorporated into the basisphenoid) , the intcr( ~ r l ) i t dseptnm arid tlie planum mpraseptale, which together made up the basket for the forebrain, are reduced to a set of riwrnl)t*ane~.The membranes rctaiii the extent and shape of thc cartilage, but are devoid of matrix and are made up of c.oiinective tissue. No ossicles develop in the interorbital Z;Cp t 1111. ‘I’lie nasal capsule is also reduced to a connective-tissue rneml)raiie, which contains scattered groups of cartilage-like cells without matrix. The nasal septum is also largely mcmhranons ; it does contain, however, :E delicate plate of hyalinc vnrt ilagc. DEVELOPMENT OF THE SKULL OF THE TURTLE 361 NOTE Oh- FOSSIL SKULLS The turtle skull, because of its simplicity and massiveness alike in the embryo and in the adult, lends itself very well to an embryological interpretation of the reptile skull. With its help, embryological criteria for many bones can be laid down, which may help to clear up homologies in fossil forms, and some of the more bizarre features of certain extinct species can be understood and explained. Cartilage bones Of the occipital- and otic-bone groups nothing need be said, for the criteria of these are obvious and homologies in this part of the skull rarely cause difficulty. On the sphenoid group, however, the data in this paper can shed some light. ‘Basisphenoid, ’ ‘parasphenoid, ’ ‘presphenoid, y ‘orbitosphenoid, ‘alisphenoid,’ and ‘ethmoid’ are terms applied by paleontologists to various bones that replace the crista sellaris and the prechordal chondrocranium. The terms, as used by many writers, are ill-defined and overlapping. The following criteria, some old, some new, may be of use. The basisphenoid, in the narrower sense, is an ossification of the cartilage skull floor behind the hppophysis, in the crista sellaris. I n many reptiles the cartilage floor and the basisphenoid bone have a lateral basipterygoid process on either side. The process is absent in turtles generally. The parasphenoid is a membrane bone which closes off the hypophpseal fenestra and (especially in primitive reptiles) extends forvi-ard beneath the trabecula cranii and the interorbital septum. The terms presphenoid and ethmoid should be applied to ossifications in the interorbital septum, the former restricted to bone formed in the posterior part of the septum; the latter, to bone laid down in that part of the septum adjacent to the nasal septum. The orbitosphenoid is an ossificatioii of the planum supraseptale, above and behind the optic nerve and anterior to the oculomotor and trochlear nerves. The true iiIi~pIieiioi(1in wl)tilcs is ail ossification of the piln prootica, w t l lieiicch lies hetween tlie oculomotor and troclil(~ar~ierves i i i front a i d the trigeminal nerve behind. In ~)~iitzc,iitologicalliteratnix? the I)asisplimioitl ttnd pai-ahplic~iioiclare seldom icleiit Xed incorrectly. The parasplieiioit I s l ~ o its ~ ~fundamental s iiatnrc \'cry clearly in the cotylosaurs, for example. Tlie presplienoid is typically clevelopecl in I,;imhiosautw,-: (Uilmorc., '24) m t l in Ecimoiitosaums (Lambc, '20). I11 ('oi.;\-tliosauriis l'arlis ( 7237pl. ITT) givtw the iiaino ~mrasplieiioid'to il large vertical blade \I-liich projects forward from the basisplienoitl lieileath tlie optic 17en-e. W l d c t l i r 1)oncmay have R ~~araspliciic~icl edge, most of it is almost ccAi.tainly replacing tlic tlahecula c n i i i i ant1 the iiitcrorl~ital scptum, ~ i t lshoiilcl he called a presphcnoid. The term 'c~thmoicl'lias been loosely applied to an ossification of the w l i o l ~iiitomrbital septum iii Laccrta ( Parker and Haswell) a i i t l iii 1)intlcctes (('asp). In siwli cases 'prespliciioitl' is prcfci.ahle; the term 'ethmoid' slioiiltl hc restricted to the rostra1 part of the interorbital septum, n-hich may hare some re1at'ion t o t h e tltlimoicl of mammals, a s Sollas aiitl Sollas ('14) liave lJoiiitcv1 out in their monograpli 011 I)icyiotloii. X i 1 ossification of tlie part of the planum supraseptale Bchind the optic nerve-the metotic region--has been called the 6alisplienoid' b~ Parker ('79). Snch a bone lies iii the field of tlic orbitospliciioicl. 'I'lie truc alisphenoitl, in all modern forms in which its development can bc follomxl, arises as an ossification of the pila prootica. X more important source of confusion in tlie alisplienoid ~ ~ y i oisi i the qiiestion of tlie presence of mi epipterygoid iii p I a ~ eof 811 alisphenoicl boiie. il true alispheiioid ossificatioii of tlie pila prootica is fouiitl iii Tropidonotus (Parker, '78) :\11d in the crocodile (Kesteveii, '18). In Lacerta the cartilaginous pila prootica persists. In the turtle tho pila disappears ant1 tlie gap in the brain case is filled 1))- an epip t el*ygoid os sificat ion of t lie epipt erygoid and p ter 5- goid processes of the quadrate (figs. 11, 14). 111 fossil forms oiie c i i i i sometimes determine wliicli hone is preseiit t)y iiotiiig DETELOPLMENT O F T H E SKULL O F THE: TTTIITLI.: 363 the slight differences in relations to nerves and bones which follow upon the differing developmental histories of tlie two bones. The alisplienoid is an ossification of tlie pila prootica (fig. 11). The trochlear and oculomotor nerves lie anterior and the entire trigeminal nerve lies posterior to tlie pila. The alisphenoid takes over the same relations. !Phe alisphenoid develops in the plane of the otic capsule, and hence is not apt to overlap the prootic bone and will not usually cover the foramen of the facial nerve. The epipterygoid hone is an ossification of the epipterygoid and pterygoid processes of the quadrate cartilage. In the chondrocraiiium the maxillary and mandibular nerves cross the pterpgoitl process behind tlie epipterygoid process, but the ophthalmic turns forward along the inner side of the pterygoid process to reach the orbit. When the cartilage structures are replaced by the epipterygoid bone, the first part of the ophthalmic nerve is covered. Also, since the epipterygoici bone has a more lateral position, it tends to grov backward over the lateral surface of the prootic bone, and can cover the facial foramen, as it actually does in the turtle. I n Edmoiit osaurus (Lambe, '20) tlie alisphenoid clearly fits into the space in front of the prootic and the exits of the trigeminal a i d facial nerves are unohstructed. I n Lambeosaurus (Gilmore, '24) the bone marked ' alisphenoid' extends back t o the paroccipital (opisthotic). No facial foramen shows in the drawing. I n tlie text Gilmore quotes Lambe as saying, " The ophthalmic branch of the trigeminal nerve is enclosed in bone in its forward course . . . , " I n this illstance the presence of an epipterygoid" is very likely. Nembrasze hones The membrane bones of the higher vertebrate skull are descendants of ossifications found beneath tlie skin of the head and around the oral cavity of lower t-ertebrates, bones which at first had no close relation to the skull proper. In mammals this overskull has been intimately welded to the 364 RALPH F. SHAKER caartilaginous bones. I n reptiles one finds an interesting halfwag stage in evolution, mliere the membrane bones retain wnsiderahle freedom in tlie adult and betray their origin rery clearly in the embryo. From the embryonic grouping of the membrane bones some useful criteria for the adult bones can be established and some of the extraordinary developments of the reptile skull explained. The group of hones laid down on the ventral aspect of the c4iondrocranium (group 11) corresponds fairly well to the ' Zaliiiknoclien' of Hertwig and G egeiibaur (Oaupp, '06)a group thought to have arisen around the teeth. I n reptiles their secondary relation to the brain case is more important. The separate bones are usually easily identified from their standard relation to one another and to the overlying brain case. The pterygoid may have a constant relation t o the pterygoid process of the quadrate ; in reptiles it generally encloses the palatine branch of the facial nerve, as Gaupp has pointed out. Tlie parietal and Frontal bones (group 111) complete the roof over the brain case. They can be identified by their standard relation to the cranial cavity. The two bones seem to he the most conservative in the reptile skull. Almost the extreme of variation can be found in the turtle and tlie snake. Ti1 the turtle the parietal seiids a long process ventrally to lill in part of tlie vacant alisphenoid area. 111 the snake the froiital extends ventrally and does duty for absent orbitosphenoid-a defect correlated with the slight development of the orhitosphenoid (prechordal) region in snakes. Group I V includes the prefrontal, postfrontal, zygomatic, and in part the maxillary bones, to which may be added the postorbital and lac~hrymalof other reptiles. All are subtlcrmal ossifications that have at first a very loose connection with the skull. They are an early generation of sclerotic bones which are later incorporated into the skull to form ;t socket for the eye. No matter what changes take place in tlie skull, the members of this group retain their relation to each other and to the eye-a characteristic which serves to iclentify them in most diverse types of reptile skulls. DE\'ELOPI\IEXT OF THE SKULL O F THE TURTLE 365 I n the nasal group (V) the turtle skull has but one bonethe premaxillary. I n other reptiles the septomaxillary and nasal bones would be included. All three bones develop as ossifications to cover the cartilaginous nasal capsule and hax7e at first a very loose connection with the rest of the skull. The premaxillary lies on the ventrolateral (respiratory) surface, the nasal on the dorsal (olfactory) surface, and the septomaxillary lies beneath the ventromedial cartilage and tlie organ of Jacobson. In the turtle a process of the prefrontal takes the place of a nasal, and the absence of a septomaxillary is perhaps correlated with the doubtful presence of an organ of Jacobson. The close relation of the t h e e bones to tlie cartilaginous nasal capsule explains the formation by them of the extraordinary crests of tlie helmet-crested Hadrosauridae, e.g., Lambeosaurns and Hypacrosaurus (Gilmore, '20). The helmet in the crested dinosaurs contains an hypertrophied olfactory apparatus. The premaxillary and nasal bones have only developed with the organ around which they are laid clown in the first place. The nasal capsule and its related bones are semi-independent of tlie rest of the embryo skull, and can hypertrophy ivithout affecting the rest of the skull. It is unlikely that the frontal bone, for example, would follow the nasal capsule and participate in the formation of such a crest, as Parks ('22) thinks the bone does in Parasaurolophus. The last group of membrane bones (VI), the squamosal and quadratojugal, are definitely associated with the quadrate cartilage and bone. The squamosal appears on the posterior and dorsal aspects of the quadrate cartilage and the quadratojagal develops along its anterior margin. I n later stages (fig. 15) the squamosal overlaps the quadratojugal along the dorsal margin of the quadrate. These are the embryonic criteria f o r the bones tliat Thyiig ('06) has established f o r vertebrates generally. T ~ ipno ral a w h es and varwifiP-9 The grouping of the membrane bones in turtle embrpos suggests aii explaiiatioii for the origin of the temporal arches a i d vacuities. Ti1 riearly cvery case the tcmporal arclies can be thought of as an arrangement wliereb>- the quatlratc+sciuamosal-quadratojug.al group is fixed to tlie cwmium and its roof bones on one hand ant1 to the orbital group of hones oii the other. The object would seem to be tlie slioring of the quadrate-mandibular joint. Roily tissue characteristically iiicreases along lines of stress aiid strain, and disappears where these are absent. Tlie arclies seem to be placed 011 such lines of stress and strain which would appear d i e i i the mandibular joint is l'mictioriiiig; the vacuities mark elements of the stegocephalian memhraiie-bone orerskull which are not needed in tlic more compact reptile skull. It is true tlie turtle is ahcrrant iii this matter; its hoiiy arclies clo riot easily lend themselves to comparisoii with those of other reptiles. The turtle is an exception, ~ O T V C T ~ *wliicli , helps prove tlie rnle. The turtle quadrate is unusually hroaci and flat, and is wcll fixed to the otic bones. Heiicc the temporal arches are less needed and are more variable. Such is, of course, not the d o l e story of the temporal arclies. The writer is in iio seiise of the word an expert on fossil reptiles. It does seem to him, a student of the reptile embryo, tliat the paleontologist lays too much stress on the vacuities and the loss of such loosely articulated bones as the intertemporal. Both of these are secondary to the arches ilnd the reiiiforcement of the cluadrate-maiitlil)ulal. joint in a type of skull that is chaugiiig from the loosely articulated ampliibiaii sort to tlic compact unified sliull of higher vertebrates. L I T E R A T U R E CITED 1907 e b e r die Entwickeliing tlcs 01jcrculuiiis der L-rodelen und dcs Distelidiuins (Coluriielln auris) einiger Ilcptilien. Anat. Anz., ErgSnzungslieft, Bd. 30. GAUPP, E. 1906 Die Entwickeliuig tlrs Kopfskelcttcs. Hand. (1. rerg. u. e s p F h t . (1. \Virb., Bd. 3, T. 2. 1900 D:IS Clioiidrocr:iiiiiiiri roil Lacerta agilis. Annt. Hefte, Bbt. 1, H. 49. GILMORE,C. W. 1924 Contributions t o vertebrate Paleontology. Bull. 38, Geological scrirs 43, Caiindinii Geological Survey. GOLBY,F. 192.? Tlie development of tlic coluniel1:r anris in the Crocodilia. J o u r . Anat., ~ o l 59. . KUNKEL, B. 1912 Tlie developm~~iitof the skull of Emys lutnrin. Jonr. Morph., 1-01. 23. KESTEVEN, €1. I,. 1918 The liomology of tlic m:immnalian alisphenoid and the E:cliidti:i-pter?goid. J o u r . Anat., vol. 32. ILUIBE, L. 111. 1920 The IIadrosaur Edinontosaurus from t h e upper Cretaceous of A l l ~ ~ t a Memoir . 120, gcw1ogic:il serirs 102, Canadian Geological Surrey. PARKER, W. K. 1878 On the strneture and derclopment of the common biiake. Phil. Trans. R.S., 169, pt. 2. -___ 1879 On the structure a n d development of the skull in the Laecrtilia. Pliil. Trans. R.S., 170, pt. 2. ~ ’ . ~ K K sW. , A . 1922 1’ar:is:iurolopliiis wulkrri. Univ. Toronto Studies, geological series 13. 1923 Corytliosaurus intermedius, :I new species of Tracliodoiit dinosaur. Univ. Toronto Studies, geological series l.?. RICE, E. L. 1920 Tliu devplopmwt of the skull in t h e skink, Eumeces quinquclineatus. Joor. Rlorph., vol. 34. SHIISO, I(. 1914 Das Clionrirocraniuiii voii Crocodilius mit Beriicksichtigung tler Geliirnrierven und der Kopfgefiisse. Anat. Hefte, H. 30, AM. 1. SNITH,L. W. 191.2 The origin :rnd de~elopirieiit of the coluniella auris in (’hryseniys marginata. An at. Anz., Bd. 46. SOLLAS, I. €3. J., AND SOLLAS, w. J. 1914 A study of the skull of a Dicyiiodon hy means of serial sections. Trans. R.S., 204 B. TERRY,R. J. 1919 The relation of the faci:rl nerre and otic capsule. Anat. Rec., vol. 17. TIIYNG,3’. W. 1906 Hquainosal bone in tetrapodnus vertebrata. Proc. Boston Soc. Nnt. Hist., vol. 3 2 , no. 11. FUCHS, H.