Contributions to the Study of the Developmentof the Head in Heterodontus.

By

G. R. de Beer, B.A., B.Sc, F.L.S.,Fellow of Merton College, Demonstrator in Zoology and Comparative

Anatomy, University Museum, Oxford.

With 21 Text-figures.

CONTENTS.

PAGK

I N T R O D U C T I O N . . . . . . . . . . 3 9

T H E S K U L L . 4 0

R E L A T I O N S O F T H E S K U L L T O T H E A R T E R I E S . . . . 5 0

R E L A T I O N S O F T H E S K U L L T O T H E N E R V E S . . . . 5 3

T H E V E R T E B R A L C O L U M N . . . . . . . . 5 7

T H E T E R M I N A L A N D O L F A C T O R Y N E R V E S . . . . . 6 2

S U M M A R Y . . . . . . . . . . 6 4

I N T R O D U C T I O N .

THROUGH the kindness and generosity of Mr. 1\ D. F. Murray,I have been able to study some embryos of Hete rodontusphil ippi at stages varying from 11 mm. to 70 mm. in lengthI have concerned myself principally with the head, and inthis paper I propose to record my observations on the develop-ment of the skull and its relations to nerves and blood-vessels,and to add a few remarks concerning certain nerves. Thedevelopment of the prootic somites into the eye-muscles, andthe placodes in connexion with the profundus nerve, I havedealt with elsewhere.1 The work was done in the Departmentof Zoology and Comparative Anatomy at Oxford.

1 Page 17 of this volume, and a forthcoming paper.

40 G. R. DE BEER

THE SKULL.

The works of Gaupp (6), Goodrich (7), Parker (11), Sewert-zoff (14), and Van Wyhe (17 and 18) have acquainted us withthe development of the skull in Scyll ium, P r i s t i u r u s ,and Squalus , but as far as I can gather there has as yetbeen no work done on the Heterodonti except for the earlieststages of development (Haswell, 7 b).

The earliest stage at which rudiments of the skull appear isin embryos 37 mm. long. Text-fig. 1 is a reconstruction of suchan embryo seen from the left side.

TEXT-FIG. 1.

6c

Reconstruction of an embryo of H e t e r o d o n t u s p h i l i p p i ,37 mm. long, seen from the left side.

EXPLANATION OF LETTERING.

a., small artery between the two branches of the olfactory nerve ;ah., abducens nerve ; aba., afferent branchial artery ; acr., arteriacentralis retinae ; aha., afferent hyoidean artery ; ale, antero-lateral cartilage of the auditory capsule ; anteba., anterior efferentbranchial artery; apa., afferent pseudobranchial artery;bal., first branchial arch ; bd., basidorsal cartilage ; buc, ramusbuccalis facialis ; bv., basiventral cartilage ; cb., ceratobranchial;fc, cross commissure between efferent branchial arteries; eg.,ciliary ganglion; ch., ceratohyal; da., dorsal aorta; dr., dorsal

HEAD OF HETERODONTUS 41

The first structures to appear are the parachordal plateBwhich flank the notochord from about the level of the facial

root of a spinal nerve ; eb., epibranchial; ee., elastica externa ;ep., epithelium; epa., efferent pseudobranchial artery; exb.,extrabranchial cartilage; exh., extrahyal cartilage; exo.,external branch of the olfactory nerve ; exr., external rectus ;/., facial nerve ; fb., fore-brain ; fepa., foramen for efferent pseudo-branchial artery; fgl., foramen for glossopharyngeal nerve;

fhv., foramen for hypophysial vein ; fnam., foramen for nerveto adductor branehialis muscle; foe, foramen for oculomotornerve; fpa., foramen for pathetic nerve; fvr., foramen forventral root of spinal nerve; gl., glossopharyngeal nerve;h., hyoid arch ; lia., hypobranchial artery ; hb., hypobranchial;hf., ramus hyoideus facialis ; km., hyomandibular ; hmf., ramushyomandibularis facialis ; hv., hypophysial vein; ic, internalcarotid artery ; id., interdorsal cartilage (intercalary) ; ig,,isolated ganglion not connecting with a ventral root; infr.,inferior rectus; ino., internal branch of the olfactory nerve;inob., inferior oblique ; inr., internal rectus; isn., invadedsheath of the notochord ; Ic., layer of cartilage connecting twobasiventrals ; in., mandible; ma., mandibular artery; max.,ramus maxillaris trigemini; md., ramus niandibularis trigemini;mdin., inferior branch of niandibularis trigemini; mds., superiorbranch of niandibularis trigemini; mexf., ramus niandibularisexternus facialis ; minf., ramus niandibularis interims facialis;mxnid., maxillo-mandibulary branch of trigeniinal ; mxn. 1, firstmixed spinal nerve ; n, notochord ; oa., occipital arch ; oc,oculomotor nerve ; ol., olfactory sac ; on., optic nerve ; ophma.,ophthalmica magna artery ; orba.y orbital artery ; j?., parachordalcartilage; pa., pathetic nerve; pb., pharyngobranchial;pc.t posterior cartilage of the auditory capsule; pee., procartila-ginous rudiment of the ethmoid ; phgl., ramus pharyngeus glosso-pharyngei; phf., ramus palatinus facialis; ppb., palatobasalprocess; pq., pterygoquadrate; prf., ramus pretrematicusfacialis; prgl., ramus pretrematicus glossopharyngei; prv.,ramus pretrematicus vagi; planlgl., ramus post-trematicus anteriorglossopharyngei; pteba., posterior efferent branchial artery;ptptgl., ramus post-trematicus posterior glossopharyngei; r.,rostrum ; rale, rudiment of the antero-lateral cartilage of theauditory capsule ; ro., rudiment of the olfactory nerve ; rop.,ramus ophthahnicus profundus ; ros., combined rami ophthalmiciauperiores ; ros VII, ramus ophthalmicus superior facialis; rt.,rudiment of nervus terminalis ; s., muscle segment; sa., segmentalartery ; sg. 1, first spinal ganglion; sp., spheno-lateral cartilage ;apt., septum; stgl., ramus supratemporalis glossopharyngei;suob., superior oblique ; sur., superior rectus ; sv., small veinrunning between trigeminal and facial nerves ; t., nervus ter-minalis ; tc, trabecula cranii; tp., trabecular plate; tr.,trigeminal nerve ; ts., tectum synoticum ; tsp., tectum formedby spheno-laterals ; v., vagus nerve ; va., ventral aorta ; vr.,ventral root of spinal nerve ; vr. 1,2, 3 ; first, second, and thirdventral roots.

42 G. B. DE BEEB

nerve and pass back into the region where the procartilagerudiments of the vertebral column are to be found. Theseplates are quite flat and show no sign of segmentation.

Ventral to the anterior extremity of the parachordal cartilagesand almost touching them are the trabecular cartilages. Theselie fairly wide apart, on either side of the hypophysis and ventralto the floor of the fore-brain to the form of which they aremoulded. It will be seen from Text-fig. 1 that the trabeculaemake a certain angle with the parachordals, but this angle issmaller than that described for Squalus by Sewertzoff (14),

£c ' i i, balpq m en

Reconstruction of the skull of an embryo 40 mm. long.

yet larger t h a n tha t obtaining in S c y l l i u m according toGoodrich (7).

A separate ' Polknorpel', such as Van Wijhe (17) describes,I have not been able to find, probably because the requisitestage of development is not in my possession. It is possible,however, that the ' Polknorpel', though possessing a distinctcentre of chondrification of its own, may be connected withthe trabeculae by procartilage.

In Text-fig. 1 I have indicated the position of the efferentpseudobranchial artery. This is of some importance, as therelations of this artery to the trabeculae differ in Selachiansfrom the conditions obtaining in all other craniates. From

HEAD OF HETEHODONTUS 43

the earliest appearance of the trabeculae the artery runsdorsally over them to join the internal carotid, instead ofunder them as in other forms.1

The mandibular arch contains a cartilage just forming fromthe procartilage condition, and which represents the palato-

TBXT-FIG. 3.

cb

Reconstruction of the skull of an embiyo 45 mm. long(from a wax model).

pterygoquadrate bar and Meckel's cartilage, as yet unseparated.The pterygoquadrate is attached from the first to the trabeculaeby dense connective tissue. This connexion represents theprocessus palatobasalis (or possibly the processus ethmoidalis,since it is at present impossible to diagnose them with certainty),and it is of interest to observe that there is no trace or sugges-tion of an otic process. The early fossil Heterodonti wereamphistylic, and.Heterodontus in its development mighthave shown traces of an amphistylic condition. That this is

1 This matter is the subject of a shortly forthcoming paper.

44 G. R. DE BEER

not the case need not be surprising, for unless the fossilamphistylic (and presumed) ancestral Heterodonti wereamphistylic in their embryonic stages there is no reason tobelieve that He te rodontus phi l ippi would show thischaracter. In later stages the palatoquadrate of Hetero-dontus is larger than that of any other non-amphistylicSelachian, without however possessing a true otic process.A conclusion which might be drawn from this would suggestthat the otic process of amphistylic forms was not present inthe embryonic stages of such forms but developed late. Thereare reasons for believing the otic process to represent a modifiedgill-ray (Allis), and this would fit in with the suggestion thatit is a structure of secondary nature and developed late.

In the hyoid arch the hyomandibular and ceratohyal cartilagesarise in conjunction. The hyomandibular is in contact withthe parachordal ventral to the auditory sac. There is no traceof any pharyngohyal element (see Sewertzoff, 15).

Anterior to and separate from the parachordals, but extend-ing along the same axis, are the cartilages variously describedas alisphenoid (Sewertzoff, 14), pleurosphenoid (Van Wijhe,18), or sphenolateral (Gaupp, 6). They lie dorsal to the oculo-motor and behind the patheticus at this stage. Between thesphenolaterals and the parachordals runs the hypophysial vein.This vein will at later stages lie anterior to the junction betweensphenolaterals and parachordals. This junction, the pilaantotioa, has not yet appeared, and though present at laterstages I am unable to say whether it has a separate origin or not.

Behind the hyoid the remaining branchial arches have pro-cartilaginous rudiments only. These rudiments are piercedby the adductor branchialis muscle, which splits off mesiallyfrom the main muscles of the visceral arch, as described bySewertzoff (15). By piercing the visceral arches the adductorbranchialis muscles come to lie median to the visceral arches,while the main band of muscles (dorsal, medial, and ventralconstrictors and the interbranchials) lies outside them.

At the next stage (39 mm., Text-fig. 2) the most noteworthychanges are that in the mandibular and hyoid arches the

HEAD OF HETERODONTUS 45

skeletal elements have separated into dorsal and ventralportions, and that by the pila antotica the sphenolaterals areconnected with the parachordals. The trabeculae are con-nected with the parachordals. Dorsolateral to the trabeculaethe procartilage rudiments of the ethmoid cartilages appear.Anterior to the pila antotica the hypophysial vein enters thecavity of the skull, and at this stage it has already beensurrounded by cartilage forming the interorbital canal. Ventralto it is the efferent pseudobranchial artery which runs over thetrabecula to join the internal carotid, and which has likewisebecome enclosed by the developing cartilage. In the broadgap between the trabeculae and the sphenolaterals the opticand oculomotor nerves pass freely out. The pathetic liesanterior to the sphenolaterals, the trigeminal facial andabducens nerves emerge behind the pila antotica.

The parachordals, dorsal to the hyomandibular (which isseparated from the ceratohyal), show rudiments of two pro-cesses which will be the anterolateral and posterior cartilagesof the auditory capsule. They have no separate origin of theirown, but develop as processes of the parachordals.

The palatoquadrate has separated from Meckel's cartilage ;the former, in close connexion with the trabeculae, begins toshow an anteriorly directed palatine process.

The branchial arches at this stage are simple hoops of pro-cartilage, as yet undifferentiated into their component elements,though the dorsal half is marked off from the ventral half.Daniel (3) states that in Hete rodontus francisci thereare traces of a sixth branchial arch. This is not apparent inray preparations ; possibly it develops at a stage later thanany represented in my series. The adductor muscles are stillconnected with the main muscles dorsally and ventrally, andpass through foramina in the dorsal and ventral halves of thevisceral arches.

At 45 mm. (Text-fig. 3) the existing elements of the proceed-ing stages have enlarged. The sphenolaterals have extendedforwards and enclose the pathetic nerve in a foramen. Thespace between the sphenolaterals and the trabeculae is closing

46 G. R. DE BEER

up from behind forwards, and the oculomotor is enclosed ina foramen. In connexion with the trabeculae the ethmoidcartilages or lamina orbito-nasalis have arisen, stretchingforwards lateral to the trabeculae with Avhich they are fused.The trabeculae of each side are joined together anteriorlyby a trabecular plate Avhich extends back as far as the hypo-physis. This shows that the skull of He te rodontus isplatibasic, or ' platitrabic ', to use Van Wijhe's (18) term.

The antero-lateral cartilage of the auditory capsule hasgrown up and reaches as high as the sphenolaterals, towardswhich it extends anteriorly. The trigeminal, facial, andabducens nerves thus lie between the sphenolaterals andthe anterolateral otic cartilages. The posterior cartilageof the auditory capsule is developing and encloses the glosso-pharyngeal nerve in a foramen. Behind this is the rudimentof the occipital arch between which and the posterior oticcartilage the vagus passes freely out. The rest of the oticcapsule is foreshadowed by procartilage, the extent of whichis indicated by the dotted line.

In the branchial arches the subdivision into four elements,pharyngo-, epi-, cerato-, and hypo- is discernible. The epi-branchials and ceratobranchials are pierced no longer by theadductor branchialis muscle which has lost all connexion withthe other muscles, but by the nerves, branches of the ramuspost-trematicus branchialis, which supply the adductorbranchialis muscles. Other than the presence of these nervesthere is no trace of the fact that the adductor branchialismuscles have split off from the constrictors and pierced thevisceral arches. A reconstruction showing the relations of thenerves to the cartilage at this stage is given in Text-fig. 4.

At 70 mm. the skull has taken on more or less the form ofthe adult (Text-figs. 5 and 6). The sphenolaterals, ethmoids,and trabeculae have fused up on each side, so that the lateralwalls of the cranium are complete and the optic nerve isenclosed in a foramen.

The sphenolaterals have fused dorsally with the anterolateralcartilage of the auditory capsule, this enclosing the trigeminal,

HEAD OF HETEEODONTUS 47

facial, and abducens nerves in the foramen prooticum, whichis then divided into two. The auditory capsule itself is com-plete, the antero-lateral and posterior cartilages having fusedcompletely. The latter has also joined with the occipital archwith the result that the vagus is enclosed.

The trabecular plate has extended backwards and underliesthe hypophysis, whose connexion with the exterior has dis-

max & due'

Reconstruction of the skull of an embryo, 45 mm. long, showingthe relations of the cartilages to the nerves.

Posteriorly the trabecular plate stops short justanterior to the parachordals, and through this foramen theinternal carotid enters the skull.

Anteriorly the trabecular plate is prolonged into the rostrum,which passes forward between the two olfactory sacs. Laterallythese sacs are surrounded by thin cartilages which connectposteriorly with the ethmoid region of the wall of the cranium.

At this stage the roof of the skull is forming. The roofingstarts in two places : anteriorly in connexion with the spheno-laterals, and posteriorly with the auditory capsule. The latter

G. R. DB BEER

is the second to form, and at this stage the processes from eachside have not yet met in the middle line. The tectum synoticum,therefore (for this posterior roofing process represents thisstructure), arises later than the anterior roofing, as in Amia

antebaeha '

Reconstruction of the skull of an embryo, 70 mm. long, showingthe relations of the cartilages to the arteries (from a wax model).

(Pehrson, 12), but this is the opposite of what occurs inPr i s t iu rus according to Sewertzoff (14).

The notochord is persistent in the skull and extends a shortdistance in front of the parachordals. The palatine process ofthe pterygoquadrate is now well developed.

In the visceral arches the conditions do not differ muchfrom those obtaining at the previous stage, except that thegill-rays and extrabranchial cartilages have appeared (Text-

HEAD OF HETERODONTUS

fig. 7). Gill-raj's are carried by the ceratohyal and the epi-and ceratobranchials. These gill-rays lie posterior to theanterior efferent and afferent arteries and to the post-trematie

TEXT-FIG. 0.

e%r — tsP

Reconstruction of the skull of an embryo, 70 ram. long, seenfrom the dorsal surface.

branchial nerves. They lie anterior to the posterior efferentarteries and to the pretrematic branchial nerves.

The extrahyal of the hyoid arch is represented only by theventral element, the dorsal one being absent in the adultHete rodontus (Daniel, 4. Fiirbringer, 5, however, claimedto find a rudiment of it). The extrabranchials at this stage onlyhave the dorsal element. Since the adult has ventral extra-

NO. 269 E

50 G. H. DB BEER

branchials also, these must appear at a later stage. The visceralarch lies median to the cross commissural vessels between theanterior and posterior efferent arteries ; the extrabranchialarch Iie3 lateral to this vessel (see Krivetski, 8). The labial andprespiracular cartilages have not yet appeared.

Posteriorly the skull articulates with the vertebral column,the development of which will be described below.

RELATIONS OP THE SKULL TO THE ARTERIES.

The internal carotid, which is the anterior prolongation ofthe dorsal aorta, enters the skull through the foramen betweenthe parachordals and the trabecular plate. Just before doingso it gives off a small artery dorsally, which pierces the cartilageand emerges at the side of the skull by a foramen situated justbeneath that of the facial nerve. This is the orbital artery(external carotid of some authors) which runs down antero-ventrally on the outer margin of the pterygoquadrate(Text-fig. 5).

Further forward the internal carotid receives the efferentpseudobranchial artery, which passes up from the pseudobranchmedian to the orbital artery and enters the skull through aforamen dorsal to the trabecula. The relations of this arteryto the trabecula in Selachians have already been commentedupon.1 Just before entering the skull the efferent pseudo-branchial artery gives off the ophthalmica magna, which entersthe eyeball, passing dorsal to the orbital artery.

Opposite the optic foramen the internal carotid gives offan artery which accompanies the optic nerve through the opticforamen into the eyeball. This is the arteria centralis retinae.

Further forward the internal carotid gives off two smallarteries to the olfactory region and then curves upwardsand backwards along the under-surfaee of the brain. Thetwo arteries, one on each side, fuse to form the arteria basilaris,which continues backwards beneath the spinal cord.

Behind the place where the internal carotid gives off the1 See previous foot-note.

HEAD OP HETERODONTUS 51

orbital artery it passes median to the hyomandibular andreceives the efferent hyoidean artery. Prom here it becomesthe lateral dorsal aorta, and just in front of and lateral to thepharyngobranchial of the first branchial arch it receives thefirst efferent branchial artery. The lateral dorsal aorta then

f ehahm

The hyoid and first branchial arches of an embryo, 70 mm. long,showing the relations of cartilages, arteries, and nerves.

curves over the pharyngobranchial and passes backwards overits mesial face.

The branchial vessels are shown in greater detail in Text-fig. 7. The efferent hyoidean artery represents the posteriorefferent artery*of the hyoid arch (the anterior element notbeing formed), for it lies behind the hyal rays. Ventrally itconnects by a cross commissure with the pseudobranch, i.e. bythe afferent pseudobranchial artery.

52 G. R. DE BEER

This commissure passes on the inside of the ramus mandi-bularis internus facialis, and therefore cannot represent theoriginal afferent mandibular vessel. The latter vessel isprobably represented by a small artery which is given off bythe lateral hypobranchial artery running forward from theventral extremity of the efferent hyoidean artery. The hypo-branchial artery runs forward inside the afferent hyoid arteryand on the under-surface of the ceratohyal. The true mandi-

TEXT-FIG. 8.

The ophthalmic, oculomotor, pathetic, and abducens nervesand their relations to the eye-muscles. 70 mm.

bular artery which it gives off runs up the outer side of themandible between the two branches of the ramus mandibularisfacialis. At earlier stages it connects with the commissurerunning to the pseudobranch, but at 70 mm. this connexionis lost (cf. Allis, 1).

The efferent hyoidian artery is connected with the anteriorefferent branchial artery of the first arch beneath the firstgill-slit. The afferent hyoidean and branchial arteries lieexternal to the hyoid and visceral arches respectively, and alsoexternal to the cross commissural vessels between the efferentarteries. The lateral hypobranchial arteries connecting theventral ends of all the efferent arteries are still incomplete.

HEAD OF HETERODONTUS 5 3

KELATIONS OF THE SKULL TO THE NERVES.

Of the olfactory nerves little need be said ; they reach theolfactory epithelium through the wide openings in the olfactorycapsules. The optic nerve penetrates the optic foramen.The oculomotor pierces the lateral wall of the skull andemerges by a foramen slightly above and behind the opticforamen. It divides into two branches, the more dorsal ofwhich passing over the ramus ophthalrnicus prof undus innervatesthe superior and internal recti, the ventral branch passingbeneath the profundus innervates the inferior rectus andinferior oblique (Text-fig. 8).

The pathetic nerve traverses a foramen far forward anddorsal in the lateral wall of the skull, and passes below the ramiophthalmici superficiales trigemini and facialis and above theprofundus to the superior oblique.

The abducens passes forwards within the skull median tothe facial and trigeminal and emerges through the trigeminalforamen anterior to the Gasserian ganglion. It arises by fouror five roots.

The trigemino-facialis complex (Text-fig. 9) is interestingas differing considerably from that described for S q u a 1 u sby Norris and Hughes (10), and from other forms. Thetrigeminal ganglion is large compared Avith the facial, and is notover-lain by it as in S q u a 1 u s . The ophthalmic ganglion of thefacial emerges through the same foramen as the trigeminal,and the combined superficial ophthalmic nerves run forwardalong the side of the skull on the dorsal border of the orbit.The trigeminal and facial ganglia are separated by a smallvein from the vena capitis lateralis and representing part ofthe original vena capitis medialis. The hypophysial veinrepresents a branch of the latter.

The profundus leaves the root of the superficial ophthalmicganglion and runs over the external rectus, and the inferiorbranch of the oculomotor, under the superior and internalrecti, over the optic nerve, under the superior oblique, andre-enters the skull through a small foramen on the anterior

G. R. DB BEER

edge of the orbit accompanied by a small vein. It continuesits forward course on the inside of the lateral wall of th» skull.

The rnaxillo-rnandibular branch of the trigeminal passesbehind and beneath the external rectus and runs to the outeredge of the pterygoquadrate and divides (Text-fig. 10). The

, -rSVrop-

e p a -*:•••••

mxmd8cbuc-h'mf

prrThe trigemiual and facial ganglia and their relations to the

neighbouring arteries and veins.

anterior division, ramus maxillaris, runs forward along theouter edge of the palatoquadrate in conjunction with theramus buccalis of the facial. The posterior or mandibulardivision divides into two, both branches run down on the out-side of the pterygoquadrate, one supplying the adductormandibulae, the other sending branches to the skin.

The facial emerges through the foramen close behind thetrigeminal. Ventrally it gives off a branch which divides intotwo; one portion goes forward beneath the skull as the ramus

HEAD OF HETBBODONTUS

palatinus, the other passes to the anterior -wall of the spiracleand is th.e ramus pretrematicus. The ramus hyomandibularispasses back dorsal to the hyomandibular and then verticallydown along the posterior face of the latter. It divides into

HF

\^ ptpLgfptantgl

The relations of the cartilages and nerves in a 70 mm. embryo.

three. One branch, the ramus mandibularis externus facialis,runs forward in the lower jaw external to Meckel's cartilage.The ramus mandibularis internus facialis passes in to the medianside of Meckel's cartilage, between the latter and the hyo-mandibular. Before doing so, however, it lies external to thevessel connecting the pseudobrancli with the efferent hyoidean

56 G. E. DE BEER

artery. The rarnus hyoideus continues downwards in the hyoidarch behind the ceratohyal.

The ramus oticus facialis of Norris and Hughes's descriptionof Squalus I have not been able to find.

The glossopharyngeal, which emerges from the skull beneaththe auditory capsule, gives off a ramus supratemporalis,a ramus pharyngeus, and pre- and post-trematic branchialnerves. The pretrematic passes lateral to the lateral dorsal

TEXT-FIG. 11.

sSfl bd idi

The occipital region of a 70 mm. embryo.

aorta but median to the efferent hyoidean artery, and liesbehind the hyal rays.

The post-trematic branch divides into two : an anterior-which lies inside the lateral dorsal aorta and anterior to theanterior efferent branchial vessel; and a posterior which runsoutside the aorta, behind the anterior efferent vessel, medianto the afferent vessel, lateral to the cross commissural vessel,and anterior to the branchial rays. It gives off branches whichpierce the epibranchial and ceratobranchial to innervate theadductor branchialis muscle.

The pretrematic branch of the first vagus root lies behindthe branchial rays and median to the cross commissuralvessel and the posterior efferent artery.

HEAD OF HETERODONTUS 57

In the occipital region (Text-fig. 11) three ventral rootspierce the skull, and each is distributed to a myotome. Corre-sponding to the last of these roots, there is within the skulla dorsal ganglion which is isolated from the ventral root anddoes not communicate with it. From a notch in the posteriorface of the occipital arch there emerges a ventral root whichjoins with the next dorsal root to form the first mixed spinalnerve. Thereafter the ventral roots pierce the basidorsalsand the dorsal roots the interdorsals. I have not yet a sufficientseries of early stages to be able to say to which segment thefirst permanent postotic myotome belongs and how manysegments are included in the skull.

THE VERTEBRAL COLUMN.

The sheath of the notochord is invaded as in all Selachiansby cells from the sclerotome. The invasion takes place notby total disappearance of the elastica externa at four points,but the elastica is perforated at these points and the invadingcells pass singly through the perforations. The consequenceis that in sections more than 10p thick the elastica externaappears to be intact and does not show any interruptions atthe points where invasion is occurring.

The centra are formed of basidorsal and basiventrals whicharise in the septa between the segments (Text-fig. 12). Thebasidorsal and basiventral of one centrum arise in one andthe same septum.

Van Wijhe (18) states that in Squalus along the notochordthere are four continuous bands of cartilage Avhich becomeseparated up into the basidorsals and basiventrals of eachside. This is contrary to the views of Schauinsland (13), whosays : ' Es muss iibrigens noch hervorgehoben werden, dassdie Anlagen der einzelnen Bogen sowie auch der Interkalar-stiicke offenbar von "vornherein von einander ge t renntsind, obgleich sie in dem scheinbar einheitliehen Gewebe deroben beschriebenen Langsleisten ihren Ursprung nehmen.'

The ' Langsleisten ' are the bands running along the noto-chord which Van Wijhe describes as cartilaginous, and

58 G. R. DE BEER

therefore according to him the elements of the vertebrae areat first continuous.

I have observed these bands and there seems to be no doubtabout their existence; but the question is, are they truecartilage ? In order to test this point I have prepared sections

TEXT-FIG. 12.

6K sa dr45 mm. embryo. Relations of dorsal and ventral roots to seg-

mental vessels, septa, muscle segments, and vertebral elements.

TEXT-FIG. 13.

bv

70 mm. embryo. Vertical longitudinal section in trunk region,showing the layer of cartilage connecting two basiventrals.

from different stages of the trunk, stained in thionin. Thisstain is metachromic, staining cartilage red, and all other tissuesincluding procartilage blue. At the early stages (40 mm.)the longitudinal bands appear to be homogeneous, but in theregions of the basidorsals and basiventrals thionin shows thatchondrification is much more active than in the interveningregions. But there is cartilage in the intervening regions(Text-fig. 13). I therefore agree with Van Wijhe that theelements of the vertebrae are connected from a very early

HEAD OF HETERODONTUS 59

but my impression is that the vertebral elements do notarise as subdivisions of a primitive continuous band, but thatthe band arises by the intervening regions between the vertebralelements becoming ' infected ' by the process of chondrinea-tion. The cartilage in the intervening regions is closely pressedagainst the elastica externa of the notochord, and is three orfour cells thick. In the mid-ventral, mid-dorsal, and mid-lateral lines this cartilage does not exist, so that there areveritably four bands.

TEXT-FIGS. 14 AND 15.

id bd

Relations of nerves and vertebral elements in the tail and trunkregions of Pr is t iurus .

It is difficult to conceive of any other explanation for thesebands, for the sclerotomic material is segmented and thecontinuity must be secondary.

In the adult He te rodontus the basidorsal is piercedby the ventral root, and the intercalary immediately behindit is pierced by the dorsal root of any one mixed spinal nerve(see Daniel, 3, for description of the cartilage of adultH. francisci).

As Van Wijhe points out, there are two distinct types in theSelachians as regards the relations of the nerve-roots to theelements of the vertebral column. In one type the ventralroot pierces the basidorsal and the dorsal root pierces thesucceeding intercalary. In the other type the ventral root

60 G. R. DE BEER

emerges between the basidorsal and the next posterior inter-calary, and the dorsal root between that intercalary and thefollowing basidorsal. To the latter type belong the Scyl-lioidei, to the former the Notidani, Heterodonti, Squaliformes,and Batoidea. It becomes interesting to inquire as to how thisvariation is brought about.

Text-figs. 14 and 15 are reconstructions of the relations inthe tail and trunk respectively of a P r i s t iu rus embryo,a form which is of the Scyllioid type. It is plain that the nerve-roots emerge between the skeletal elements and do not piercethem.

Primitively, a ventral root running straight to its myotomeis intrasegmental, and the corresponding dorsal root is behindit and intersegmental, running in the septum between themyotome supplied by the ventral root and the next posteriormyotome. The mixed nerve runs in the septum immediatelybehind the segment which it supplies (Goodrich, 7). This isplain from Text-figs. 14 and 15.

Now in the case of the other type, to which He te rodon tusbelongs, haA'e the nerve-roots moved forwards or backwards tobecome enclosed in the cartilages? Text-fig. 16, which isa reconstruction of a 45 mm. embryo, shows that as in theprevious case the roots run out in the septum behind thesegment which they supply. Text-fig. 17, which representsa 70 mm. embryo, shows the segmental blood-vessel. (Oneonly of the two, artery and vein, for clearness.) The blood-vessel indicates the position of the septum, and if there werea migration of the roots backwards, the nerve would cross theblood-vessel. This does not occur, suggesting that the migra-tion was not backwards but must be forwards. That thisis so is proved by the fact that in early stages the ventralroot is only just enclosed by the posterior face of the basidorsalin front of it, and that it becomes more enclosed as developmentproceeds. The dorsal roots come to lie immediately overinstead of behind the intercalaries, and these being notchedpresent a heart-shaped appearance before fully enclosing thedorsal root. A complete reconstruction of the relations in a

HEAD OF HETERODONTUS 61

70 mm. embryo is given in Text-fig. 18, and it shows that theventral root pierces the basidorsal anterior to the one corre-

TEXT-FTG. 16.

H e t e r o d o n t u s , 70 ram. longitudinal vertical section. Thenerves run in the posterior septum of their segment.

TEXT-FIO. 17.

fvr

The foramina through which the nerves pass.

TEXT-FIG. 18.

Complete diagrammatic reconstruction of the trunk regionin a 70 mm. embryo.

sponding to the septum in which the mixed nerve runs. Thisconfirms Goodrich (7 a), who states on p. 136 that ' the ventral

62 G. E. DE BEER

root . . . comes out behind or through the neural arch ', thusindicating the forward nature of the displacement of the nerveswhen they pierce the skeletal elements.

THE TERMINAL AND OLFACTORY NERVES.

Locy's (9) nervus terminalis is represented in 22 mm.embryos of He te rodon tus by a string of stellate cells,close to the fore-brain on its anterior surface, and in the regionwhere the neural crest is disappearing (Text-fig. 19). Locy is

TEXT-FIG. 19.

•Fb

Transverse section through anterior region of 22 mm.stage, showing the rudiment of the terminalis.

also of opinion that the neural crest contributes to theterminalis, and the demonstration by Brookover (2) that theterminalis contains elements of a sympathetic nature derivedfrom a placode, leads to the conclusion that the terminaliscontains elements of mixed nature.

At 45 mm. (Text-fig. 20, reconstructed as seen from in front)the terminalis is connected with the brain, and the point ofconnexion is not ATentral as in Ami a and Squalus buton the anterior surface as in Raja . It runs straight to theplacode formed by the olfactory organ and which gives riseto the olfactory nerve.

At 70 mm. (Text-fig. 21) the olfactory nerve is double,consisting of a lateral and a median element. At this time the

HEAD OF HETERODONTUS

TEXT-FIG. 20.

68

0/ f

Reconstruction of the fore-brain from in front. 45 mm.

TEXT-FIG. 21.

Reconstruction of the fore-brain from in front, 70 mm., showingthe relations of the terminalis to the olfactory nerves.

64 G. K. DE BEER

second set of Schneiderian folds (Sund, 16) has appeared ; butas Norris and Hughes (10) find for S q u a 1 u s, so in H e t e r o -dontus the subdivisions of the olfactory nerve and of theolfactory sac do not correspond.

The terminalis runs outwards dorsally to the median sectionof the olfactory nerve, and between it and the lateral sectionswells out into a ganglion. It is interesting that there shouldbe much variation in connexion with these ganglia, for inSqualus Locy describes two, in Must el us none; as faras I can make out He te rodon tus has one. This ganglionlies dorsal to a small artery which, running forwards under thebrain from the internal carotid, passes between the twodivisions of the olfactory nerve. From the ganglion theterminalis fibres run in olose association with those of thelateral olfactory nerve to the olfactory epithelium, but withoutappropriate neurological methods I have not been able tofollow their distribution further.

SUMMARY.

1. The development of the skull of He te rodon tus isdescribed.

2. There is no trace of an otic process.3. The tectum synoticum forms after the more anterior

roofing.4. The efferent pseudobranchial artery is from the first

dorsal to the trabecula.5. The afferent pseudobranchial artery is not the mandibular

artery.6. Longitudinal bands of cartilage exist along the notochord

but are probably not primary.7. The dorsal and ventral roots have moved forwards so as to

be enclosed in cartilages.8. The olfactory nerve is subdivided into two, which sub-

divisions do not correspond with the subdivisions of theolfactory sac.

9. The neural crest contributes to the terminalis, which showsone ganglion.

HEAD OF HETERODONTUS 65

LIST OP LITERATURE CITED.

1. AUis, E. P.—" The so-called mandibular artery, &c", ' Journ. Morph.',27, 1916.

2. Brookover, C.—" The olfactory nerve and nervus terrainalis in Amia,calva ", ' Journ. Comp. Neur.', 20, 1910.

3. Daniel, J. F.—" The anatomy of Heterodontus francisci", ' Journ.Morph.', 26, 1915.

4. • ' The Elasmobranch fishes', Univ. California Press, 1922.5. Ftirbringer, K.—" Beitrage zur Kenntnis des Visceralskeletts der

Selachier ", ' Morph. Jahrb.', 31, 1903.6. Gaupp, E.—" Die Entwickelung des Kopfskelettes", Hertwig's

' Handbuch der Etitwickelungslehre '.7. Goodrich, E. S.—" On the development of the segments of the head

in Scyllium ", ' Quart. Journ. Micr. Sci.', 63, 1918.7 a. ' Vertebrata Oraniata. Cyclostomes and Fishes.' London,

1909.76. Haswell, W. A.—" On the development of Heterodontus philippi " ,

' Proc. Linn. Soc. New South Wales', 22, 1898.8. Krivetski, A.—" Sur la morphologie des elements de l'arc hyoide chez

les Selaciens ", ' Rev. Zool. Rus.', 2, 1917.9. Locy, W. A.—" A new cranial nerve in Selachians ", ' Mark. Anniv.

Vol.', 1903.10. Norris, H. W., and Hughes, S. R.—"Nerves of Squalus acanthias",

' Journ. Comp. Neiir.', 25, 1920.11. Parker, W. K.—" On the structure and development of the skull

in Sharks and Skates ", ' Trans. Zool. Soc.', 10, 1878.12. Pehrson, T.—" Some points in the cranial development of Teleo-

stomian fishes ", ' Acta Zoologica ', 3, 1922.13. Schauinsland, H.—" Die Entwickelung der Wirbelsiiule ", Hertwig's

' Handbuch der Entwickelungslehre '.14. Sewertzoff, A. N.—' Die Entwickelung des Selachierschadels,' Festschr.

v. K. von Kupffer.15. " Die Morphologie des Visceralapparates der Elasmobranchier " ,

' Anat. Anz.', 56, 1923.16. Sund, O.—" Die Entwickelung des Geruchsorgans bei Spinax ",

' Zool. Jahrb., Abt. Anat.', 22, 1906.17. Wijhe, J. van.—" Die Entwickelung des Kopfskelettes bei Selachiern ",

' Comptes rendus 6° Cong. Int. Zool. Berne ', 1904.18. " Friihe Entvvickelungsstadien des Kopf- und Rumpfskelettes von

Acanthias vulgaris ", ' Bijdragen tot de Dierkunde, Amsterdam ',22, 1922.

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