Studies on the Vertebrate Head. Part I. Fish. G. It. De Beer, M.A., B.Sc

Studies on the Vertebrate Head. Part I. Fish.

By G. It. de Beer, M.A., B.Sc, F.L.S., Fellow of Merton College, Demonstrator in Zoology and Comparative Anatomy, Oxford University.

With 42 Text-figures.

CONTENTS. PAGE 1. INTRODUCTION ...... 288 2. SELACHIANS ...... 289 (a) The Venae Capitis 289 (b) The Arteries 298 (i) Development 298 (ii) Relations of the Arteries ..... 301 3. TELEOSTOMES ...... 304 (a) Amiacalva...... 304 (i) The Venae Capitis 304 (ii) The Relations of the Arteries . . . .309 (iii) Development of the Arteries .... 315 (Ji)Salmo trutta 316 (i) The Venae Capitis 316 (ii) The Arteries 318 (c) Cottus bubalis 319 The Venae Capitis 319 4. DIPNOI 320 Ceratodus forsteri ...... 320 (i) The Venae Capitis 320 (ii) The Arteries 323 5. CYCLOSTOMES ...... 324 Petromyzon ...... 324 (i) The Venae Capitis 324 (ii) The Arteries 327 288 G. E. DB BEER

PAGE 6. CONSTANT RELATIONS ...... 328 7. INCONSTANT RELATIONS ...... 329 (a) The Mandibular Vessel 329 (b) The Hyomandibular 333 8. CONCLUSIONS ...... 337

9. SUMMARY 339 10. LIST OF LITERATURE CITED ...... 339

1. INTRODUCTION. THE structure of the head of the vertebrate might appear to be more suitable as a subject for a text-book than for a paper. There exist innumerable and admirable descriptions of the structure of the head of various forms in books and papers, but it appeared to the writer that detailed comparisons between related forms belonging to one group not only constituted a less threadbare subject for investigation, but also might reveal some points either unknown, unexplained, or not well under- stood. Accordingly the present work aims at a description of few new structures, but at the comparison of the relations which these structures bear to one another in related forms. The present communication deals with the most lowly groups, the Fish and Cyclostomes. The forms investigated were: Scyllium canicula, Squalus acanthias, Pristiurus melanostomus, Heterodontus philippi, Torpedo ocellata, Amia calva, Salmo trutta, Cottus bubalis, Ceratodus forsteri, Petrornyzon planeri, P. fluviatilis. The relations of the eye-muscles and the oculomotor nerve have been dealt with elsewhere (14). Here the structures calling for consideration are the arteries and veins, and the relations which they bear to various nerves and cartilages. The work was done in the Department of Zoology and Comparative Anatomy, University Museum, Oxford. I desire to acknowledge my indebtedness to Professor Goodrich, P.B.S., for his encouragement during the work. VERTEBRATE HEAD 2S9

2. SELACHIANS. (a) The Venae Capitis. The external jugular veins of the adult dog-fish are, as is well known, not the primitive veins of the head region (see Hochstetter, 19 and 20 ; Babl, 26). The primitive vein, or vena capitis medialis as it is termed from its position, is the only cranial vein in ScyIlium, Stage I (Text-fig. 1). In

TEXT-FIG,

Selected transverse sections through Scylliuni oanicula, Stage I, in the regions of (a) trigeminal, (6) facial, (c) auditor nerve, (d) auditory vesicle, (e) glossopharyngeal, (/) vagus, (g) first postotic myotome. EXPLANATION OF LETTERING OF PIGS. 1-42.

a, auricle; ah, abducens; aba, afferent branchial artery; abalt first branchial artery; ac, anterior cardinal; am, anterior cerebral artery ; acr, arteria centralis retinae ; aha, afferent hyoid artery; anteba, anterior efferent branchial artery; apa, afferent pseudobranchial artery; as, av, auditory sac ; on, auditory nerve ; auc, auditory capsule ; ba, branchial arch ; bas, third branchial arch ; baa, basilar artery ; hue, ramus buccalis facialis; ca, cerebral artery; cc, cross commissure between efferent branchial arteries; ch, ceratohyal; cv, connecting vessel between 290 G. R. DB BEER transverse sections of embryos it is seen to lie median to the' trunks of all the dorsal cranial nerves, i. e. trigeminal, facial, glossopharyngeal, and vagus ; and in the region of the auditory hypobranchial artery and ductus cuvieri; eim, connecting vessel between facial vein and vena capitis medialis ; da, dorsal aorta ; do, ductus cuvieri; e, eye; eb, epibranchial cartilage; ebai_h, first to fifth efferent branchial artery; ec, external carotid ; eha, efferent hyoid artery; ehv, hyoid vein; en, endostyle; epa, efferent pseudobranchial artery ; exr, external rectus ; exv, extra vein ; ,/', facial nerve ; fb, forebrain ; fgl, foramen for glossopharyngeal; fhmf, foramen for hyomandibular branch of facial; foe, foramen for oculomotor ; forba, foramen for orbital artery ; fv, facial vein ; cjl, glossopharyngeal nerve; ?«]_<, gill-slits 1 to 4; h, hypophysis ; ha, hypobranchial artery ; Kb, hind-brain ; hm, hyomandibular ; hmc, cut dorsal portion of hyomandibular ; hmf, ramus hyomandibularis facialis ; hmnis, hyomandibular muscle ; hv, hypophysial vein; i, inf undibulum; ic, internal carotid; infr, inferior rectus; indb, inferior oblique; inos, inferior orbital sinus ; inr, internal rectus ; lev, lateral cutaneous vein ; ma, mandibular artery ; max, ramus maxillaris trigeinini; me, Meckel's cartilage ; md, ramus mandibularis trigemini; mdmx, maxillomandibular branch of the trigeminal; mexf, ramus mandibularis externus facialis ; minf, ramus mandibularis internus facialis ; ms, mandibular sinus ; my, myotome; inyd, dorsal part of myotome ; vvyv, ventral part of myotome ; n, notochord ; nic, notch for internal carotid ; nrpf, notch for ramus palatinus facialis ; oc, oculomotor nerve ; ocs, occipital sinus ; ol, lateral occipital cartilage ; on, optic nerve ; op, operculum ; ophma, ophthalmica magna artery ; orba, orbital artery ; os, orbital sinus ; pa, pathetic nerve ; pant, pila antotica ; papa, primary afferent pseudobranchial artery ; pasc, processus ascendens ; pb, pharyngobranchial cartilage ; pc, parachordal; pun,, posterior cerebral artery ; pev, posterior cardinal vein ; peba, posterior efferent branchial artery ; po, processus oticus of the pterygoquadrate ; poc, polar cartilage ; pohm, processus oticus hyomandibularis ; ppb, processus palatobasalis ; ppq, palato- pterygoquadrate; pr, profundus nerve; ps, pseudobranch; r, rostrum ; re, ramus communicans between the facial and vagus ; rop, ramus ophthalmicus profundus; ros, rami ophthalmioi superiores ; ros VII, ramus ophthalmicus superficial facialis ; rpf, ramus palatinus facialis ; rvel, rudiment of the vena capitis lateralis; «,, 2> s» first, second, third somites; sh, stylohyal; si, sphenolateral cartilage ; sn, sinus venosus ; sp, spiracle ; sip, styloid process ; snob, superior oblique ; siios, superior orbital sinus ; sur, superior rectus ; sv, secondary vein ; te, trabecula cranii; tcom, trabecula communis ; th, thymus ; tp, trabecular plate ; Ir, trigeminal nerve ; v, vagus nerve ; va, ventral aorta ; vahm, vein accompanying the hyomandibular nerve ; zap, vein accompanying the profundus nerve; vea, velar artery; vev, velar vein; vl, lateralis branch of vagus; vn, ventricle; w,, ,JS 3, first ventral nerve-root, second and third ditto ; zs, rudiment of otic process of the hyomandibular. VEETEBRATE HEAD 291 sac it runs between the latter and the wall of the brain. These relations will be obvious from Text-fig. 1, and show that the term vena capitis medialis is accurately descriptive. Text-fig. 2 is a reconstruction of a slightly older embryo (Stage J) from the left side; the vena medialis can be seen passing on the inside of the nerves and of the auditory sac. Just behind the oculomotor nerve the veins of each side communicate by the hypophysial vein. Between the glosso-

TEXT-FIG. 2.

Reconstruction of Stage J (Scyllium) from the left side. pharyngeal and vagus there appears the rudiment of a new vein, external to the medialis, which will form part of the vena capitis lateralis of the adult. In Text-fig. 3 (Stage K) the vena capitis lateralis is present external to the facial, but it has not yet joined with the posterior portion between the glossopharyngeal and the vagus. This stage is shown in section in Text-fig. 4 ; there is only the medialis in the region of the glossopharyngeal. It is important to observe that in the region of the vagus the new vein is at this stage still internal to the nerve. For this reason it is here denoted ' secondary vein ' until it acquires its definitive external position. 292 G. R. DE BEER

TEXT-FIG. 3.

Reconstruction of Stage K (ScyIlium) from the dorsal side.

TEXT-FIG. 4.

Selected sections through Scyllium, Stage K, in the regions of (a) trigeminal, (6) facial, (c) auditory nerve, {d) auditory vesicle, (e) glossopharyngeal, •(/) slightly behind (e), (g) vagus, (7i) first postotic myotome. VERTEBRATE HEAD 293

TEXT-FIG. 5.

Reconstruction of 21 mm. Heterodontus pliilippi from the left side.

TEXT-FIG. 6.

Selected sections through Stage 0, Scyllium, in the regions of (a) trigeminal, (6) facial, (c) and (d) auditory capsule, (e) glossopharyngeal, (/) vagus. 294 G. R. DE BEER Text-fig. 5 is taken from* a reconstruction of an embryo of Heterodontus in Stage L. The lateralis has joined the medialis just in front of the facial and in front of and behind the glossopharyngeal. By looping round, and the branches joining on the outer side, the first branch of the vagus has been TEXT-FIG. 7.

Keconstruction of Scyllium from the dorsal side (the brain is removed), showing the vena capitis lateralis. enclosed by the lateralis. The medialis is still the principal vein. The secondary vein has become lateralis. Anteriorly the medialis forms the orbital sinuses. A more ventrally situated sinus (inferior orbital sinus) lies median to the oculomotor nerve ; the superior orbital sinus, when it extends forwards, will lie external to this nerve. The medialis (and its anterior prolongation the inferior VERTEBRATE HEAD 295 orbital sinus) lies internal to the ventral cranial nerves (oculomotor, pathetic) except the abducens. The latter issues from the brain very nearly in the median line, and consequently the vein must lie external to it. That this is secondary is suggested by the relations of the postotic nerve-roots to the medialis as shown in Text-fig. 1 g, where the nerve lies dorsal and external to the vein. At a later stage (Text-fig. 6) the medialis dwindles away, being compressed between the developing auditory sac and the brain.

TEXT-FIG. 8.

Reconstruction of Scyllium (26 mm.) from the left side.

Text-fig. 7, which is a reconstruction from the dorsal side, shows how the medialis ends blindly posteriorly ; the lateralis is now the functional vein of the head. By looping round, nearly all the branches of the vagus are enclosed in the vein. Anteriorly the superior orbital sinus connects with the medialis behind the maxillo-mandibulary branch of the .trigeminal, forming a lateralis in this region. The hypophysial vein comes off from the medialis median to the trigeminal. At 26 mm. (Scyllium, Text-fig. 8) the lateralis is fully formed and lies external to all the branches of the vagus, and indeed to all the nerves except the ophthalmic branches of the trigeminal and facial. The only portion of the medialis 296 G. R. DE BEER remaining lies median to the trigeminal, and from it the hypophysial vein arises. The trigeminal and facial nerves thus come to be separated by a vein, and it is part of this vein which enters the skull in Heterodontus between these tAvo nerves (see 13). At 33 mm. (ScyIlium, Text-fig. 9) cartilage is developed. The lateralis lies outside the auditory capsule and dorsal to the hyomandibular but ventral and internal to the hyomandibular

TEXT-KIO. 9.

suos ros

eha \ hm

Reconstruction of Scyllium (33 mm.) from the left side. muscle. The hypophysial vein runs inwards anterior to the pila antotica joining the sphenolateral cartilages with the parachordals, and under the tip of the notochord. Text- fig. 10 gives transverse sections through the regions of the nerves at the stage from which Text-fig. 9 was reconstructed. Text-fig. 11 is a reconstruction from the dorsal surface of a 70 mm. embryo of Heterodontus. As well as the hypophysial vein, there are two others which pierce the skull. One of these pierces the skull slightly anterior and ventral to the optic foramen and runs for a short distance along the floor, VERTEBRATE HEAD 297 which it pierces, and then enters the olfactory capsule. The other pierces the skull by the same foramen through -which the ramus ophthalmicus profundus passes. In tracing the development of the venous system of the head it has been shown that the primitive vein becomes squashed by the development of the auditory sac. It is replaced by the definitive lateral vein, and in two ways. First,

TEXT FIG

Selected sections through Scyllixim (33 mm.) in the regions of (a) trigemitml, (6) facial, (c) and (d) auditory capsule, (e) hyomandibular, (/) vagus. rudiments of the lateralis appear, which later become connected up. Next this vein laps round the vagus branches by making small and progressive encroachments. Eventually that portion which was median to the vagus disappears. The possibility of forming a lateralis vein is conditioned by the fact that in the head region the myotomes are either small or absent. As soon as the postotic myotomes are reached the vein lies median to them. 298 G. R. DE BEER (b) The Arteries. (i) Development.—The early stages of development of the arteries have been described by Dohrn (15), Eaffaele (27), and others, to whom references will be found in Hochstetter's

TEXT-FIG. 11.

Reconstruction of Hetero'dontus (70 mm.) from the dorsal side, the roof of the skull removed. (20) work. Other workers who have investigated the conditions of the arteries in Selachians include Allis (6), Ayers (10), Carazzi (11), Hyrtl (21), and Parker (24). In an 11mm. embryo of Heterodontus (Text-fig. 12a) VERTEBBATB HEAD 299 the condition of the arteries is simple. There are a dorsal and a ventral aorta communicating through each arch by a single branchial vessel. At 21mm. (Text-fig. 126) the spiracular anterior demibranch has appeared. The vessel in the hyoid arch has split into two, an afferent and an efferent. The efferent hyoidean artery is connected with the mandibular artery ventral to the demibranch by a cross commissure running beneath the spiracle. The spiracle is much reduced in size and has moved dorsally. The vessel in the first branchial arch has likewise split into two, but both portions connect both with the dorsal and ventral aortae. Anteriorly the dorsal aorta is continued forwards as the internal carotid. This gives off an artery running along together with the optic nerve into the eyeball (the arteria centralis retinae), a small artery to the olfactory capsule, and then curves back, running under the floor of the brain as the arteria basilaris. At 25 mm. (Text-fig. 12 c) there is little change in the hyoid arch, but the efferent hyoid artery gives off a branch passing back beneath the first gill-slit towards the first efferent branchial artery, which at this stage it does not yet reach. Where the efferent artery from the spiracular demibranch joins the internal carotid an artery is given off which runs into the eye, the arteria ophthalmica magna. Slightly further posteriorly the internal carotid gives off the orbital artery, which runs forwards dorsal to the efferent artery of the spiracular demibranch but ventral to the ophthalmica magna. In the first branchial arch there are now three vessels. The anterior one is the anterior efferent branchial artery, connected with the dorsal aorta, and at this stage still communicating ventrally with the ventral aorta. The next one is the afferent branchial artery, leading out of the ventral aorta ; and behind it is the posterior efferent branchial artery. The two efferent branchial arteries are connected half-way up their length by a cross commissure which runs median to the afferent branchial vessel. At 45 mm. (Text-fig. 12 d) the efferent hyoid and anterior NO. 270 X 300 G. R. DE BEER

TEXT-FIG. 12. ophma da cc

Diagrammatic representation of the development of the arteries in Heterodontus. (a) 11 mm., (b) 21 mm., (c) 25 mm., (d) 45 mm., (e) 70 mm. VERTEBRATE HEAD 301 efferent branchial vessels communicate beneath the first gill- slit. The efferent vessels have lost all connexion with the ventral aorta, but communicate with a vessel which is the rudiment of the hypobranchial artery. The afferent artery to the spiracular demibranch arises from the anterior continuation of this hypobranchial artery, not from the ventral aorta. Up to and including this stage the spiracular demibranch has been supplied by two arteries, one the true mandibular vessel, and the other a cross commissure from the efferent hyoid artery. The true mandibular vessel lies median to the ramus rnandi- bularis externus facialis, and lateral to the ramus mandibularis internus facialis, confirming Allis (6). The cross commissure runs median to both these nerves. Since the afferent mandibular vessel arises no longer from the ventral aorta but from the hypobranchial artery, it transmits only blood which has already been through another gill. The spiracular demibranch therefore no longer functions as a true respiratory organ, but is a pseudobranch. At 70 mm. (Text-fig. 12 e) the true afferent mandibular vessel has disappeared, the pseudobranch being supplied solely by the cross commissure which becomes known as the afferent pseudobranchial artery. The anterior prolongation of the hypobranchial artery becomes the external carotid. (ii) Eelations of the Arteries.—Before proceeding to the consideration of the relations of the various arteries it must be pointed out that with regard to the nomenclature there prevails the wildest confusion. Many authors, among whom may be mentioned Allis (1, 2, 3, 4), Ayers (10), Carazzi (11), Dohrn (15), Greil (17), Hyrtl (21), Muller (23), Parker (24), and Wright (23), apply the same name to different vessels, and call the same vessel by different names. In the following table an attempt is made to give the relative equivalents of terms used by the different authors: Efferent pseudobranchial (Allis) = Anterior carotid (Parker) = Part of afferent spiracular and carotis interna anterior (Dohrn). X 2 802 G. E. DB BEER Afferent mandibular = Primary afferent pseudobranehial (of A m i a, Allis) = Hyoidea (Wright) = Pseudobranchialis (Parker) = Thyreo-spiracularis and part of afferent spiracular (Dohrn). Centralis retinae (Dohrn) = Optic (Allis) = Ophthalmica minor (Miiller) = Ophthalmica (Greil). Ophthalmica magna = Choroidalis (Dohrn) = Orbitalis (Greil). Orbitalis (Carazzi) = Temporalis (Greil) = Posterior carotid (Parker) = Carotis facialis (Bathke) = External carotid (Allis). The internal carotid is the anterior prolongation of the dorsal aorta. It runs median to the trabecula cranii and then rises between them so as to lie dorsal to the trabecular plate (Text-figs. 9 and 11). The external carotid is the anterior prolongation of the ventral aorta, which may shift its connexion to the hypobranchial artery (Text-fig. 12 e). The efferent pseudobranehial artery represents the dorsal portion of the true mandibular vessel. In Heterodontus and all Sela- chians it runs upwards median to the orbital artery and passes dorsal to the trabecula cranii to join the internal carotid. In all other vertebrates it passes ventral to the trabecula. This point will be referred to again below. It passes lateral to the ramus palatinus facialis. The afferent mandibular vessel, which arose first from the ventral aorta and later from the hypobranchial artery to run to the pseudobranch, disappears. It represents the ventral portion of the true mandibular vessel. The arteria centralis retinae arises from the internal carotid at the point where the latter passes over the optic nerve. VERTEBRATE HEAD 303 It accompanies the optic nerve through the optic foramen into the eyeball (Text-fig. 11). The ophthalmica magna arises from the efferent pseudobranchial artery near the junction of the latter with the internal carotid. It runs laterally into the eyeball, passing dorsal to the orbital artery and anterior to the maxillary and buccal nerves. The orbital artery arises from the internal carotid before the latter pierces its foramen into the cranial cavity. The orbital artery pierces a small lateral projection from the parachordal and emerges median and ventral to the facial ganglion. It does not, therefore, enter the cranial cavity. It runs forwards along the edge of the pterygoquadrate, passing dorsal to the efferent pseudobranchial and ventral to the ophthalmica magna (Text-figs. 11 and 12). It runs anterior to the ramus palatinus facialis, and at first lies dorsal and lateral to the maxillary and buccal nerves ; further forward it curves round the latter, lying behind and ventral to them. The relations of the branchial vessels to nerves and cartilages have been described in the writer's work on Heterodontus (13), to which the reader is referred. The nomenclature of the carotids in these and other forms deserves- perhaps a little amplification. While the internal carotid is always the prolongation of the dorsal aorta, when most of its blood is derived from the mandibular arch it is sometimes called anterior internal carotid; if most is derived from the hyoid or posterior arches, it is a common plus internal carotid. The so-called common carotid, which is difficult to define since it is an intermediate portion of the dorsal aorta and has been ascribed different limits along that vessel by different authors, may be regarded as that portion of the dorsal aorta which lies between the junctions of the latter vessel with the mandibular and hyoid vessels. It is not homologous with the common carotid of higher vertebrates, which is a ventral vessel. 304 G. R. DE BEER

3. TELEOSTOMES. (a) A m i a c a 1 v a. (i) The Venae Capitis.—The primitive vena capitis medialis is present in embryos of Ami a 6 mm. long (Test- figs. 13 and 14). It passes median and ventral to all the dorsal nerve-roots and between the auditory sac and the brain. Even at this early stage, however, it is not the sole vein of the head,

TEXT-FIG. 13.

Reconstruction from the ventral side of Amia calva (6 mm.). for a small secondary vein is present, which, leaving the medialis just anterior to the facial nerve, runs lateral to the latter and to the auditory sac, but median to both glossopharyngeal and vagus, behind which it rejoins the medialis. The medialis is still the principal vessel at this stage, and it gives off the hypophysial vein median to the trigeminal. At 7 mm. (Text-fig. 15) the medialis has disappeared behind the trigeminal, so that from there posteriorly the secondary VEBTEBBATE HEAD 305 vein is the only one present. It has lapped round the glossopharyngeal and now lies external to it, but it is still internal to the vagus. Median to the trigeminal the median's gives off the hypophysial vein which runs dorsal to the external rectus muscle, for the latter is already extending backwards under the brain. A reconstruction from the left side of a slightly later stage is shown in Text-fig. 16, with the cartilage omitted.

TEXT-FIG. 14.

Selected sections through Amia (6 mm.) in the region of {a) trigeminal, (6) slightly behind (a), (c) facial, {d) auditory nerve, (e) auditory vesicle, (/) gloesopharyngeal, (g) vagus, (h) first postotic myotome. At 11 mm. the cartilage of the skull is already well developed. The secondary vein is enclosed by the prefacial cartilaginous commissure, so that it issues from the skull by the facial foramen lying dorsal to the nerve. Here it gives off a small vein which accompanies the facial through the hyomandibular foramen. Prom the point of its emergence from the skull there starts a vein whieh, though in contact with the secondary vein, does not yet communicate with it and ends blindly in front. This vein passes external to both glossopharyngeal 306 G. R. DE BEER and vagus, and then comes into contact with the secondary vein again behind the vagus. Prom its relations to the nerves

TEXT-FIG. 15.

Reconstruction from the ventral side of A mi a (8 mm.

TEXT-FIG. 16.

Reconstruction from the left side of Amia (9 mm.). this vein is the vena capitis lateralis. Reconstructions of this stage from the left side in Text-fig. 17, from the inside in 1 mm.). 17.—Reconstruction from the left side of Amia (1 TEXT-FIG. 308 G. R. DB BEER Text-fig. 18, from behind in Text-fig. 19, and from above in Text-fig. 21 will make this description clearer. Text-fig. 20 is a reconstruction of the cartilage alone for greater ease of

TEXT-FIG. 18. tr oc pa f I 1

Reconstruction from the inside of Amia (11 mm.).

TEXT-FIG. 19.

Reconstruction from behind of Amia (11 mm.). The skull has been cut transversely in the region of the hyomandibular. comparison of the relations. Selected sections are reproduced in Text-fig. 22. The secondary vein thus does not become the lateralis, as it does in Selachians. Attention is called to the relations which the secondary vein and vena capitis lateralis bear to the hyomandibular. Both pass VERTEBRATE HEAD 809 ventral and median to this cartilage. The lateralis runs lateral to the hyomandibular muscle, the secondary vein median to that muscle. Eeconstructions of a 50 mm. stage are given in Text-figs. 28 and 24. There is not much change in the relations of the veins. The lateralis extends forwards beyond the hyomandi-

TEXT-FIQ. 20. £;&$\ tp

The skull of Amia (11 mm.) from the dorsal side. bular into the orbital sinus. The median's just anterior to the point where the hypophysial vein is given off divides into two, the oculomotor nerve passing between the branches. (ii) The Belations of the Arteries.—The internal carotid passing forward rises in a notch in the trabecula (Text-figs. 20 and 21), which eventually becomes closed to form a foramen. It sends a tiny branch ventral to the trabecular plate, but itself passes dorsal to this cartilage and gives off the 310 G. R. DE BEER posterior cerebral artery, the centralis retinae, and the anterior cerebral. Just before the internal carotid rises over the trabecula it receives the efferent pseudobranchial artery which passes ventral to the trabecula. Prom the point of junction

TEXT-FIG. 21. jlCU

Reconstruction of A mi a (11 mm.) from the dorsal side. the ophthalmica rnagna arises, passing up the median face of the trabecula and over it to the eye. At 50 mm. the efferent pseudobranchial no longer runs into the internal carotid, but continues straight into the ophthalmica rnagna (Text-fig. 24). The efferent pseudobranchial artery runs external to the ramus palatinus facialis. The primary afferent pseudobranchial artery at the 11 mm. VERTEBRATE HEAD 311 stage runs down from the pseudobranch and gives off a vessel which runs back into the operculum lateral to the hyomandibular. It continues downwards, lying between the pterygoquadrate and the hyomandibular and between the rarni

TEXT-FIG. 22.

£ Selected sections through Ami a (11 mm.) in the regions of (a) tri- geniinal, (6) facial, (c) orbital artery, (d) and (e) hyomandibular, (/) glossopharyngeal, (g) and (h) vagus, (i) first postotic myotome. externus and internus mandibularis facialis. It passes external to the symplectic and on to the anterior surface of the ceratohyal, where it gives off a branch which runs forwards external to Meckel's cartilage. It then splits into two portions which reunite and run into the hypobranchial artery (Text-fig. 17). 812 G. R. DE BEER

TEXT-FIG. 23.

Reconstruction of Amia (50 mm.) from the right side.

TEXT-'FIG. 24.

Reconstruction of Amia (50 mm.) from the front. VERTEBRATE HEAD 313 At 50 mm. the primary afferent pseudobranchial artery has been replaced by a secondary afferent artery given off as a branch from the orbital artery (see Allis, 1 and 2). The orbital artery arises from the internal carotid at about the level of

TEXT-FIG. 25.

7> 9,s/ 0

Diagrammatic representation of the development of the arteries of Amia: (a) 6 mm., (6) 11 mm., wrong interpretation, (c) correct interpretation. the facial foramen. It pierces the parachordal and runs lateral to the ramus palatinus facialis and ventral to the medialis vein and the trigeminal nerve (Text-fig. 18), with which it emerges from the skull (Text-fig. 24). The afferent hyoid artery arises from the ventral aorta, as do the afferent branchials. The efferent hyoid artery runs 314 G. E. DE BEER ventral to the lateralis and secondary veins and joins the dorsal aorta close to the orbital artery. The hypobranchial arteries join in the middle line ventral

TEXT-FIG. 26.

Reconstruction of the ventral arteries of A mi a (11 mm.) from the dorsal side. to the afferent hyoid artery and connect with a mandibular sinus (Text-fig. 26). Behind the afferent hyoid artery they join dorsal to the ventral aorta, and then run back ventral -to the afferent branchial vessels. Posteriorly the hypobranchial VERTEBRATE HEAD 315 arteries connect with the ductus cuvieri on each side. This connecting vessel (which is functional and contains blood corpuscles) is shown in Text-figs. 17 and 26. Of the functions of this connexion it is hard to be certain. The pressure of the blood must be higher in the hypobranchial arteries than in the ductus cuvieri, so that the direction of flow would be to the latter vessel. The result of this would be a supply to the heart of blood more oxygenated than would otherwise be the case, possibly to meet the respiratory requirements of the heart itself, for with branchial respiration the heart is entirely venous. The connexion could not be traced at 50 mm. (iii) Development of the Arteries.—The efferent pseudobranchial artery lies anterior to the spiracle, and therefore certainly represents the dorsal portion of the original mandibular vessel. Ventrally the spiracular slit is not open, but a deep depression shows its position, and the primary afferent pseudobranchial artery, running along the ceratohyal, lies behind this depression (Text-fig. 26). The question therefore presents itself, is the afferent pseudobranchial artery the ventral portion of the mandibular vessel which has slipped back, as Allis (1) suggests (represented diagrammatically in Text- fig. 25c), there being one hyoid vessel (the afferent and efferent hyoid vessels being a continuation the one of the other) ? Or is the afferent pseudobranchial vessel a cross commissure from a hyoid vessel as in Heterodontus, the hyoid vessel having split ventrally into two (represented diagrammatically in Text-fig. 25 b) ? In embryos 6 mm. long there is present a single vessel in each of the first two visceral arches, the mandibular and the hyoid (Text-fig. 25 a). Beneath the spiracle these pre- and post- spiracular vessels are connected by a cross commissure. At the 11 mm. stage the hyoid vessel is interrupted, the dorsal portion being the efferent hyoid artery. If the second alterna- tive be true, then the ventral portion would be split into two, as in the branchial arches, one connecting with the ventral aorta, the other with the hypobranchial artery. The presence NO. 270 Y 316 G. R. DE BEER in the hyoid arch of the afferent hyoid artery does not preclude the possibility of the afferent pseudobranchial artery being derived from the primitive post-spiracular vessel, and connected with the mandibular vessel by the cross commissure of the previous stage. But this rests on the assumption that a break has occurred in the mandibular vessel and that the ventral portion has either disappeared or lost connexion with the dorsal portion. A careful search through a series of embryos of 7, 7-5, 8, 8-5, and

TEXT-FIG. 27. Orb A

T6 Ppq NC Reconstruction of Salmo trutta (20 mm.) from the left side.

9 mm. has not revealed any such interruption : the mandibular vessel is continuous the whole time. The cross commissure loses connexion with the post-spiracular vessel and extends back into the operculum. The primary afferent and efferent pseudobranchial arteries therefore represent the original mandibular vessel. The relations of the rami internus and externus facialis to this vessel (Text-fig. 25 c) are similar to those in H e t e r o d o n t us for the mandibular vessel.

(6) Salmo trutta. (i) The Venae Capitis.—In 20mm. trout embryos the primitive vena capitis medialis has already long since disappeared, except in the region of the trigeminal where it gives VERTEBRATE HEAD 817 off the hypophysial vein. As in A mi a, the secondary vein is enclosed by the prefacial cartilaginous commissure, and it emerges through the facial foramen, but ventral to the rarnus hyomandibularis facialis, not dorsal and external to it as in

TEXT-FIG. 28.

Reconstruction of Sal mo (20 mm.) from the dorsal side.

Ami a. Thereafter it continues backwards outside the skull and internal to the glossopharyngeal and the vagus. The vena capitis lateralis starts at the point of exit of the secondary vein from the skull (and in contact with it) and courses back- external to the facial, glossopharyngeal, and vagus, to re- establish connexion with the secondary vein behind the latter nerve (Text-figs. 27, 28, and 29). Y 2 318 G. H. DE BEER Both the lateralis and the secondary vein pass internal to the hyomandibular and separated from one another by the hyomandibular muscle, as in Ami a. The lateralis is similar

TEXT-FIG. 29.

Selected sections through Sal mo (20 mm.) in the regions of (a) trigeminal, (6) orbital artery, (c) facial, (d) and (e) hyomandibular, (/) glossopharyngeal, (g) vagus, (h) first postotic myotome. to that vessel in A m i a, but the secondary vein differs froni that form in that it passes internal instead of external to the facial. The hypophysial vein runs dorsal to the external rectus muscle, which extends back in the myodome. The oculomotor runs in between two branches of the medialis vein. (ii) The Arteries.—The efferent pseudobranchial artery VERTEBRATE HEAD 819 runs under the trabecula, as in Ami a, to join the internal carotid. The ophthalmica magna runs over the trabecula out to the eyeball. Allis (7) quotes Dohrn as saying that at an early stage in the trout the ophthalmica magna runs under the trabecula. I have examined embryos 6 mm. 8 mm., 10 mm., 20 mm., and 50 mm. long, but have not found this. The orbital artery leaves the internal carotid and pierces the parachordal beneath the facial nerve. It runs forward

TBXT-FIO. 30.

. - tr

hmF

Reconstruction of Cottus bubalis (11 clays) from the front. along the upper face of the cartilage ventral to the external rectus muscle and across the orbit. The arteries in the trout are on the whole very similar to those of Ami a. (c) Cottus bubalis. The Venae Capitis.—In the Teleostomes so far examined all the veins have been found to lie median to the hyomandibular ; the medialis of course, the secondary vein, and the lateralis were all covered over by the hyomandibular. In Cottus bubalis (11 days, Text-figs. 30 and 81) the conditions are fairly similar to those obtaining in A m i a and the trout. The medialis disappears behind the trigeminal 320 G. E. DB BEER owing to the development of the auditory capsule, and is replaced by a secondary vein and the lateralis, both inside the hyoniandibular. But lateral to the hyoniandibular there

TEXT-FIG. 31.

Selected sections through Cottus (11 days) iu the regions of (a) trigeminal, (6) and (c) hyoniandibular, (d) glossopharyngeal.

is a small vein which, running into the orbital sinuses in front, joins the other two veins behind, in the region of the glossopharyngeal.

4. DIPNOI. Ceratodusforsteri. (i) The Venae Cap it is.—In a 18 mm. embryo of Ceratodus (Text-figs. 32, 33, 34, and 35) the cartilage is VERTEBRATE HEAD 321

TEXT-ITO. 32.

Reconstruction of Geratodus forsteri (13 mm.) from the left side. From a wax model.

TEXT-FIG. 33.

Reconstruction of Ceratodus (13 ram.) from the inside. 322 G. R. DE BEER already well developed. The figures reproduced here are from a wax reconstruction. Anteriorly the head veins start from the orbital sinuses and run back. They divide into two, one branch passing

TEXT-FIG. 34.

gl---'

Reconstruction of Ceratodus (13 mm.) from the dorsal side. The roof of the auditory capsule and of the foramen prootioum have been removed on the left side. lateral to and the other median to the processus ascendens. The branch enclosed by the processus ascendens lies beneath the ranius ophthalmicus profundus, and gives off the hypophysial vein medially. Behind the processus ascendens both branches of the vein unite and pass back median to the trigeminal and facial nerves VERTEBRATE HEAD 323 and to the processus oticus, dorsal to the processus palatobasalis. The hyomandibular element is very small at this stage (Text-fig. 42 a), and the vein passes external to it and internal

TEXT-FIG. 35.

Selected sections through Ceratodus (13 mm.) in the regions of (a) vagus, (b) glossopharyngeal, (c) facial, (d) palatobasal process, (e) processus ascendens, (/) orbital sinus. to the hyomandibular muscle. Lateral to this muscle there is a cord of dense tissue of which Greil (17) says : ' Ein verdickter Zellenstrang zieht von der dorsalen Kante des Keratohyals zum seitlichen Eand des Labyrinthknorpels und stellt wohl die Anfange kleiner Vorknorpelher.de dm-' (p. 1399). The presence of these structures lateral to the vein is of interest and will be referred to again. The vein continues backwards external to the glossopharyngeal, and it laps round both sides of the vagus. The vein at this stage is therefore lateralis as far forward as the facial, then medialis. (ii) The Arteries.—The efferent pseudobranchial vessel 324 G. R. DE BEEE (mandibular) runs up between the pterygoquadrate and the ceratohyal, and joins the internal carotid, passing under the trabecula. The ophthalmica magna arises somewhat further forward from the internal carotid and passes out to the eye over the carotid, piercing a small foramen in the side Avail of the skull. Still further forward the arteria centralis retinae leaves the internal carotid and accompanies the optic nerve into the eyeball. The orbital artery leaves the internal carotid behind the junction between the latter and the efferent pseudobranchial. It passes ventral and lateral to the vein and to the facial, and median to the processus oticus. It then curves up slightly so as to lie lateral to the ganglia and between the ramus buccalis and the superficial ophthalmic, and continues into the orbit.

5. CYCLOSTOMES. Petromyzon. (i) The Venae Gapitis.—Little or nothing remains to be discovered with regard to the blood-vessels of lampreys after Cori's (12) careful work and Hatta's (18) monumental paper. The reconstructions given here in Text-figs. 36, 37, and 38 are not intended to supplement or contradict the works of these authors, but merely to give the relations of only the most important vessels for comparison with other forms. Text-figs. 36 and 37 are from an 8 mm. embryo of Petro- myzon planeri, and the most striking thing about it is that the principal vein is the lateralis. It passes back over the eye, trigeminal and facial nerves, auditory sac and glossopharyngeal nerve, and branchial branches of the vagus. It lies median to the ramus communicans between the facial and vagus nerves. Behind the vagus the vein descends so as to lie ventral to the lateralis ganglion of the vagus, and it then joins two other veins. One of these is the vena capitis medialis, which runs forwards median to the vagus and glossopharyngeal. But it does not reach as far forward as the facial, for it curves VERTEBRATE HEAD 325

TEXT-FIG. 36.

Keconstruction of Petromyzon planeri (8 mm.) from the left side.

TEXT-FIG. 37.

Selected sections through Petromyzon (8 mm.) in the regions of (a) in front of eye, (6) eye, (c) trigeminal, [d) facial, (e) glossopharyngeal, (/) vagus, (g) first postotic myotome. 326 G. R. DE BEER down in the hyoid arch, i. e. the anterior wall of the first branchial basket, between that basket and the velar recess. In so doing the vein passes down lateral to the dorsal aorta, but in the arch it lies median to the hyoid artery. The other vein is known as the facial. It starts far forward in the lateral body-wall and connects with the mandibular vessel from the ventral aorta. It passes back lateral to all other veins, arteries, or cartilages. Behind the vagus it connects with the vein formed by the fused medialis and lateralis

TEXT-FIG. 38.

Reconstruction of Ammocoete of Petromyzon fluviatilis from the left side. by a connecting vein which passes median to the ramus branchialis vagi. Behind this the facial vein continues its course connected with the lateralis in the intervals between the branchial baskets. In an Ammocoete larva of Petromyzon fluviatilis the conditions are not dissimilar (Text-fig. 38). The lateralis vein connects with a dorsal occipital sinus and passes back median to the ramus communicans and lateral to the glossopharyngeal and vagus. Behind the ramus branchialis vagi there emerge two conjoined ventral nerve-roots. The more anterior of these left the brain level with the glossopharyngeal, the other level with the vagus. These two roots run back VERTEBBATE HEAD 327 within the connective tissue investment to the neural tube, and emerge behind the branchialis branch of the vagus. They then curve outwards and forwards, passing lateral to the lateralis vein, and are distributed to the first two postotic myotoraes (segments numbers four and five). The existence of these nerves and their relations to the veins are insisted upon here because it has often been stated that the anterior postotic myotomes of Petromyzon lack nerve-roots. The nerves described here appear to be the same as those which Johnston (22) describes in Petromyzon dorsatus, bub which he says are absent in other species. They can readily be found in serial transverse sections of Ammocoetes without neuro- logical technique. Anteriorly the facial vein has for a short distance become split into two. It connects down the mandibular (velar) arch, no longer with the ventral aorta but with a vessel to which the latter has given rise by splitting. It is from this vessel, which lies lateral to the cartilages of the branchial basket, that the vena capitis median's arises, passing up the hyoid arch. The venous system of P e t r o m y z on is peculiar, and can with difficulty only be compared with that of other forms. The existence of the facial veins in the head is a peculiar feature. They are possibly homologous with the lateral veins of fish, and persist in the head because there is no maxillomandibular articulation to crowd them out. The early appearance of the lateralis is perhaps the most striking feature. (ii) The Arteries.—At the 8mm. stage the arterial and venous sytems are not clearly separated, for the facial vein connects with the ventral aorta by the mandibular vessel. In the Ammocoete the mandibular vessel has split into two. One of the so-formed elements connects with the facial vein as described above. The other connects with the internal carotid, passing ventral to the trabecula (anterior parachordals of Sewertzoff, 30). The ventral connexion between this mandibular vessel and the ventral aorta is difficult to make out. Near the point where the mandibular vessel joins the internal 328 G. E. DB BEER carotid a small artery is given off which passes up median to the cartilage and up towards the brain. This is Cori's carotis cerebralis and Demme's (14 a) internal carotid. The main branch of the internal carotid continues forwards (Demme's external carotid) beneath the cartilage and rises up laterally to them. If these cartilages are the true trabeculae, then the small artery passing up median to them is the true internal carotid, and the so-called internal carotid is something else. If on the other hand the cartilages are anterior parachordals, as suggested by Sewertzoff (30), then the main artery can still hardly be the true internal carotid, since it does not enter the cranial cavity.

6. CONSTANT RELATIONS. In the forms which have been examined some structures have been found to bear constant relations to the neighbouring structures. Among these is the vena capitis medialis (except for the curious variation in cyclostomes). It passes median to the dorsal nerve-roots and to the auditory sac. Median to the trigeminal it gives off the hypophysial vein, which enters the skull anterior to the pila antotica and passes dorsal to the internal carotid and the external rectus muscle, when it extends back into a myodome. The vena capitis lateralis bears constant relations to the nerves (lying outside them) but not to the cartilages, as will be shown below. It is, however, always lateral to the auditory sac. With regard to the arteries, the ophthalmica magna passes dorsal to the trabecula, as does the centralis retinae. The orbital artery emerges from the internal carotid behind the pila antotica, either through its own foramen or with the trigeminal nerve. The efferent pseudobranchial artery (mandibular vessel) passes external to the ramus palatinus facialis on its way to the internal carotid, although its relations with the trabeculae vary. These constant relations are diagrammatically represented in Text-fig. 39. VERTEBRATE HEAD 329

7. INCONSTANT RELATIONS. (a) The Mandibular Vessel.—It has already been noticed that in Selachians the efferent pseudobranchial vessel joins the internal carotid by passing over the trabecula, whereas in all the other groups it passes under the trabecula. This is a discrepancy which needs explanation. The two types are shown in Text-fig. 40 c and a. Since the Selachians are the

vcfn

Diagram of the constant relations of veins and arteries to the cartilages. only forms (Allis, 7 and 9, mentions Amiurus as being of this type though a Teleost; in this case, however, the condition is secondary) in which the vessel goes over the trabecula, and in all other craniates it passes under that cartilage with constant regularity, it is probable that the Selachian condition is secondary. How, then, can it have been derived from the other type ? It might be supposed that the great cranial flexure characteristic of Selachians and the angle which the trabeculae make with the long axis may be responsible for the pseudobranchial artery slipping in between 330 G. R. DE BEER the trabeculae and parachordals before they fuse. But Amniotes also have the cranial flexure, and the relations in them are not the same as in Selachians. Besides, at the first appearance of the trabeculae the artery is already dorsal to the cartilage. Additional evidence against this view is found when the ophthalmica magna is considered. In Selachians this artery comes off from the efferent pseudobranchial, some distance away from the internal carotid; in the other forms it comes off close to the internal carotid. This looks as if the vessel between the internal carotid and the beginning of the ophthalmica magna in Selachians, and the base of the ophthalmica

TEXT-FIG. 40.

Relations of the trabecula cranii to the arteries in (a) non-Selachians, (c) Selachians, (6) hypothetical intermediate condition assuming that the cartilage remained unchanged. magna in the other groups, were the same vessel. The efferent pseudobranchial artery would have fused with the ophthalmica magna lateral to the trabecula, and the original junction of the efferent pseudobranchial with the internal carotid would have been lost, in producing the Selachian type (Text-fig. 406). To account for the difference there must be a change in the relations of either the vessels or the cartilage. Recently Allis (9), while maintaining that the vessels remain unchanged, has advanced a most ingenious explanation. Starting from the conditions in a branchial arch he notes that in the sharks the efferent vessel joins the aorta over and in front of the pharyngobranchial, whereas in Teleostomes it passes behind the pharyngobranchial (Text-fig. 41 a and b). Now turning to the polar cartilage (see Pehrson, 25, van Wijhe, 32), in sharks VERTEBRATE HEAD 331 the efferent pseudobranchial artery passes over and in front of it to join the internal carotid (Text-fig. 41c), in Teleo-

(a) Relations of the branchial cartilages to the arteries in Hetero- dontus (Selachian). The dotted lines represent the positions which the trabecula and parachordal would occupy if the figure were dealing with the mandibular arch and the polar cartilage were the pharyngomandibular. (6) Relations of the branchial cartilage to the arteries in Amia (Teleostome). (c) Relations of the trabecula, polar cartilage, parachordal, and arteries in Squalus (30 mm.) (as interpreted, by van Wijhe). (d) Relations of the trabecular, polar cartilage, parachordal, and arteries in Amia (12 mm.) (as interpreted by Pehrson). (e) Hypothetical interpretation of the mandibular arch in the Teleostome if the arch be of the sigma type. stomes it passes beneath. If the polar cartilage represents the pharyngeal element of the mandibular arch, then its NO. 270 Z 332 G. B. DE BEER relations to the mandibular vessel are directly comparable with the relations of the pharyngobranchial to the branchial vessel in the two respective groups. If now the trabecula attaches itself to the polar cartilage from in front, forming a single rod with it, that rod will lie under the mandibular vessel in sharks and over it in Teleostomes, which will give the required relations. In other words, Allis regards the change as brought about by the mandibular vessel passing between the polar cartilage and the trabecula, but that it is really passive to the movements of the cartilages. In Text- fig. 41 a and b the dotted lines indicate the positions which the trabecula and parachordal would occupy assuming the polar cartilage to correspond to the pharyngobranchial. Allis attributes the difference as ' evidently due to the fact that the internal carotid (lateral dorsal aorta) has not here (in the Teleostome) been crowded inwards to the median line by the fusion of the pharyngomandibulars (polar cartilages) of opposite sides, and that the latter cartilages have not fused with the axial skeleton until after they and the pharyngo- premandibulars (trabeculae) have both acquired a position in the horizontal plane of the parachordals. Because of this the ventral end of the pharyngomandibular, in swinging upwards, has passed posterodorsal to the efferent artery of its arch '. It is comprehensible that the fusion of the polar cartilages of opposite sides and the consequent approximation of the internal carotids in Selachians would result in pulling the efferent mandibular vessel inwards and backwards so that it ' crosses the anterior edge of the polar cartilage definitely dorsal to its ventral end '. Thus when the trabecula fuses with this ventral end of the polar cartilage the bar thus formed underlies the mandibular vessel. But I do not see how the ventral end of the polar cartilage in swinging upward can pass posterodorsal to the efferent artery of its arch in Teleo- stomes. If the mandibular arch must be of the sigma type. i.e. with the pharyngeal element directed backwards, the necessary relations would be obtained if the ventral end of VERTEBRATE HEAD 333 the pharyngomandibular were to swing forwards and outwards. But if this were so (Text-fig. 41 e) then the mandibular vessel would lie anterior to the epimandibular or palatoquadrate. The fact that it lies posterior to the processus palatobasalis would have to be explained by its slipping through backwards between the pharyngeal and epal elements of the mandibular arch. If on the other hand the mandibular arch in T e 1 e o s t o m e s were of the V type, and the pharyngomandibular acquires connexion with the trabecula and parachordal (Text-fig. 41 b), no rotation would be required. Beyond analogous cases of looping there is no direct evidence for the change being brought about by the looping of the mandibular vessel, and in the present state of knowledge it appears to me that Allis's view or sDme modification of it is the more probable explanation. He makes a strong case for the polar cartilage being a pharyngomandibular. Whether the trabecula is a pharyngopremandibular or not is open to question, but this question does not really affect the problem at issue here. (b) The Hyomandibular.—In Selachians (Text-fig. 42b) the hyomandibular articulates with the auditory capsule half- way between the notochord and the lateral edge of the capsule. External to it, originating from the edge of the capsule, is the hyomandibular muscle, and between the latter and the hyomandibular passes the lateralis vein. InTeleostomes (Text-fig. 42 c) the hyomandibular articulates with the auditory capsule right at its lateral edge. Median to it is the hyomandibular muscle and the two veins, secondary and lateralis. The hyomandibular therefore bears different relations both to the veins and to the muscles in the two groups. Not only this, but its relations to the ramus hyomandibularis facialis are different, for in Selachians this nerve passes back dorsal and external to the hyomandibular (Text-fig. 9), Avhereas in most Teleostomes it pierces the hyomandibular (Text- figs. 19, 21, 22, 23, 24, 27, 28, 29, and 31). 334 0. B. DB BEER The change of relations is accompanied by a change of function in the two groups. In Selachians the hyomandibular is either the simple skeletal element of the dorsal portion of the hyoid arch, or it assists in suspending the pterygoquadrate. In Teleostomes the hyomandibular, firmlyunite d with the opercular, is responsible for supporting the operculum. The operculum is lateral to the remaining visceral arches, so that it is not surprising that the hyomandibular in these forms should arise from the lateral edge of the auditory capsule. The possibility at once suggests itself that the hyomandi- bulars in the two groups are not really the same element (Allis and Woskoboinikoff, quoted by Schmalhausen, 29). Pollard (25 a) also came to this conclusion, but as he regards the spiracle and facial nerve as variable with regard to the cartilage, his views cannot be accepted. It is a familiar fact that the mandibular arch frequently has two or more articulations with the neurocranium (Text- fig. 42 e). Of these the processus palatobasalis is the original top of the arch. It lies median to the vein and to the nerves. The other, processus oticus, articulates with the skull in a more lateral position ; it lies external to the vein and to the nerves. In origin the processus oticus is probably, as Allis suggests, a modified branchial ray. May not the hyoid arch also have two articulations ? The hyomandibular of Selachians, articulating with the skull in a mesial position, median to the veins and nerves, is comparable with the proeessus palatobasalis of the mandibular arch and the pharyngobranchials of the other visceral arches, and represents the true primitive position of articulation of the hyoid arch. Whether it represents the pharyngo- or epi-elements is another question. The hyomandibular of Teleostomes, however, would represent a ' processus oticus hyomandibularis '. In the mandibular arch either of the two processes may be reduced. In Heptanchus there is a processus oticus and a palatobasalis; in Heterodontus there is apparently a palatobasalis without an oticus. The schematic hyomandibular would then be represented in VERTEBRATE HEAD 835 Text-fig. 42 d. That the two processes are not found simul- taneously must be due to the fact that the double articulation would not allow sufficient mobility for the operculum. In Ceratodus, however, it would appear that this ideal schematic condition is realized (Text-fig. 42 a). At the 13 mm.

TEXT-FIG. 42.

hmms

Relations of the hyomandibular cartilage in (a) Ceratodus, (b) Scyllium, (c) Amia, (d) schematic hyomandibular with otic process to compare with (e) palatobasal and otic articulations of the mandibular arch. stage there is a very small hyomandibular articulating half- way between the notochord and the edge of the auditory capsule, median to the vein and the muscle. This cartilage is the oto-quadrate cartilage of Edgeworth, the hyomandibular of Krawetz (22 a), Eidewood (27 a). Huxley's (20 a) and van Wijhe's (32 a) hyomandibular may be the same element, but I am not sure. Lateral to the muscle is the strand of radi- 386 G. R. DE BEER nientary procartilage described by Greil in the passage already quoted. This latter structure would be the processus oticus hyomandibularis, while the hyomandibular figured in Text- fig. 42 a would represent the true original cartilage of that name. The presence of a small extra vessel outside the hyomandibular in Cottus cannot be of much importance. Edgeworth (16) considers the development of the hyomandibular in C e r a t o d u s. What I have called the hyomandibular he terms the' oto-quadrate cartilage '. Lateral to it he describes an interhyal, which is obviously the structure produced by the ' Zellenstrang ' of Greil (cited above). He does not, however, give the relations which it bears to the vena capitis, although from his statement that it lies between the lateral edge of the auditory capsule and the hyosuspensorial ligament it is probable that it is lateral to the vein. Since the observations set forth in this paper were made I have come across Schmalhausen's (29) work. He definitely shows the lateral hyomandibular cartilage in Ceratodus (lateral to the vein) at the same time as the median one (my hyomandibular). He also states that the same conditions obtain in embryonic stages of A c i p e n s e r. He agrees with me in tracing the Selachian and Teleo- s t o m e from an intermediate form, but it does not appear to me that his interpretation of the changes is the correct one. Starting from the assumption that the hyomandibular so called is really the epihyal in the different fish, he supposes that the different types may have been brought about by a change in the position of articulation of the epihyal with the skull. It is probable that the hyomandibular of Selachians is the epihyal (see Sewertzoff, 31), but if this same structure can be regarded as capable of developing a new articulation with altogether different relations to the surrounding structures, the criteria of homology must be somewhat strained. It is to me more probable that the primitive position of articulation should be occupied by the true dorsal portion of the hyoid arch, i. e. pharyngohyal or epihyal or both, and that, as Allis suggests (see below), the lateral articulation of Ceratodus VERTEBRATE HEAD 337 (and T e 1 e o s t o in e s) represents a modified gill-ray, comparable to the processus oticus of the palatoquadrate. There remains the problem of the relations of the hyomandibular to the ramus hyomandibularis facialis. In the Selachian it passes over and external to the cartilage, as do the other branchial nerves to the branchial cartilages in all fish. This is the primitive condition. In the Teleostome when the nerve pierces the so-called hyomandibular it is improbable that it has acquired this position by eating through the cartilage. No intermediate stages are known either in phylogeny or in development. Allis's (5 and 8) suggestion to account for this is the probable explanation, and it fits in with the remarks already made here about the hyomandibular. He regards the Teleostome hyomandibular as having two heads. The anterior of these is an interarcual cartilage lying over and outside and in front of the nerve. The posterior is a modified hyal ray or dorsal extra-hyal cartilage lying behind the nerve. The two have become fused together and enclose the nerve between them. Swinnerton (31 a) describes the development of these two heads in Gasterosteus. In Polypterus the ramus hyomandibularis, which nor- mally divides into mandibularis and hyoideus half-way down the hyoid arch, divides before it has passed the hyomandibular (so called), the mandibular branch passing in front of it, the hyoideus behind (Allis, 8 a). This would result if a hyal ray, originally below the fork of these nerves, were to extend dorsally and articulate with the auditory capsule. In the adult Acipenser there is only one head to the so-called hyomandibular, the one corresponding to the anterior one of other Teleostomes, so that in this form the ramus hyomandibularis facialis lies behind and beneath the cartilage.

8. CONCLUSIONS. In this study an attempt has been made to trace the homologies between certain arteries, veins, and cartilages in the fish. In discussing relations it is necessary to start from some 388 G. E. DE BEER fixed point to which reference can be made. When relations differ in different forms, either one or the other of the two elements in question may have been responsible for the change, and it becomes necessary to inquire which. In the case of the efferent pseudobranchial artery and the trabecula it is not yet certain which has moved, although the probability is that it is the cartilage. With regard to the hyomandibular, the changed relations involving not only the veins but also the muscle and nerve render the problem easier to solve by imagin- ing that it was the cartilage that changed. Detailed comparisons between the vessels of different forms nearly always break down. For instance, the orbital artery may arise from the internal carotid or from the hyoid artery, or even from the first efferent branchial (Ceratodus). Some such variation may account for the fact that it is anterior to the palatine nerve in Selachians and posterior to it in T e 1 e o- stomes. The ophthalmica magna may arise from the internal carotid or from the efferent pseudobranchial. Blood-vessels are therefore capable of changing their relations and connexions, as has been shown by Broman (10 a). Bather than its detailed connexions, it is the general position and relations of a vessel which are the best clue to its honio- logies, which may be only partial. This is at one with Eoux's (28) discovery that the rudiments of the blood-vessels are self- differentiating, inherited, and therefore susceptible to analysis by homology ; whereas their later development is conditioned by dependent differentiation. So the orbital artery, which is probably derived from the dorsal commissural vessel joining the efferent branchials, may, if more of the latter vessel persists, join the first efferent branchial. If less persists, it will join the efferent hyoid artery, or even the internal carotid itself. Changes in relations are not always effected in the same way. The transition from median's to lateralis in Selachians is from one vein direct to the other, without the intervention of a separate and distinct secondary vein as in Teleostomes. The relations of the secondary vein itself differ in Ami a and Sal mo. VERTEBRATE HEAD 339

9. SUMMARY. In a paper of this nature it is difficult to epitomize the results any more briefly than has been clone in the actual text. Only a few of the more important conclusions will be summarized. 1. The vena capitis median's is the primitive head vein. It is replaced by the vena capitis lateralis by different methods in the different groups. 2. The relations of the efferent pseudobranchial artery to the trabecula cranii differ in Selachians and the remaining Craniates. This may be explained by vessel-looping in the Selachian or by the different relations of the polar cartilage. 3. The relations of the hyomandibular to the veins, hyomandibular muscle, aad facial nerve in the different groups suggest that the hyomandibular (i) of Selachians is a true hyomandibular, (ii) of Teleosts and Amia a compound of an interarcual cartilage and a processus oticus hyomandibularis, the latter being a modified extra-hyal. 4. The schematic condition of the true hyomandibular with the processus oticus hyomandibularis is shadowed in C e r a- todus, embryonic stages. 5. A certain number of constant relations exist, as set forth on p. 328. 10. LIST OF LITERATURE CITED. 1. Allis, E. P.—" Muscles and nerves in Amia calva ", ' Journ. Morph.', 12, 1897. 2. "Pseudobranchial circulation in Amia calva", ' Zool. Jahrb. Abt. Anat.', 14, 1901. 3. "Pseudobranchial and carotid arteries in Gnathostonie fish", ibid., 27, 1909. 4. ——" Pseudobranchial and carotid arteries in Esox, &c.", ' Anat. Anz.', 41, 1912. 5. " The homologies of the hyomandibular of Gnathostorne fish ", ' Journ. Morph.', 26, 1915. 6. " The so-called Mandibular artery, &c", ibid., 27, 1916. 7. "The Myodome and trigejnino-facialis chamber", ibid., 32, 1919. 340 G. R. DE BEER

8. Allis, E. P.—" On the origin of the hyomandibular ", ' Anat. Eec.', 15, 1918. 8 a. "The cranial anatomy of Polypterus", ' Journ. Anat.', 57, 1922. 9. " Are the polar and trabecular cartilages . . . &c. ? " ibid., 58, 1923. 10. Ayers, H.—" Morphology of the Carotids ", ' Bull. Mus. Comp. Zool. Harvard', 17, 1889. 10a. Broman, I.—" Uber die Entwicklung, Wanderung und Variation der Bauchaortenzweige ", ' Anat. Hefte', 2. Abt., 16, 1906. 11. Carazzi, D.—" Sul systema arterioso di Selache maxima ", 'Anat. Aiiz.', 26, 1905. 12. Cori, C. I.—" Das Blutgefasssysteni des jungen Ammocoetes ", ' Arb. Zool. Inst. Wien ', 16, 1906. 13. de Beer, G. R.—"Contributions to the development of the head of Heterodontus ", ' Quart. Journ. Micr. Sci.', 68, 1924. 14. " The prootic Somites of Heterodontus and of Amia ", ibid., 68, 1924. 14 a. Demine, R.—' Das arterielle Gefasssystem von Acipenser ruthenus ', Wien, 1860. 15. Dohrn, A.—" Studien zur Urgeschichte des Wirbeltierkorpers", ' Mitt. Zool. Stat. Neapel', 9, 1890. 16. Edgeworth, F. H.—" Note on the development of the quadrate and epihyal", ' Quart. Journ. Micr. Sci.', 67, 1923. 17. Greil, A.—" Entwicklungsgeschichte von Ceratodus ", Semon's ' Forschungsreise ', Jena, Denkschr. 4, 1913. 18. Hatta, A.—" Entwicklung des Blutgefasssystems des Neunauges ", ' Zool. Jahrb., Abt. Anat.', 44, 1923. 19. Hochstetter, F.—" Venensystem der Amphibien und Fische ",' Morph. Jahrb.', 13, 1888. 20. "Die Entwicklung des Blutgefasssystems ", Hertvig's ' Hand- buch der Entwicklungslehre ', 6, Jena, 1906. 20a. Huxley, T. H.—" Contributions to morphology. Icthyopsida I ", ' Proc. Zool. Soc.', 1878. 21. Hyrtl, J.—" Die Kopfarterie der Haifische ", ' Denkschr. Wien. Akad.', 32, 1872. 22. Johnston, J. B.—"The cranial nerve components of Petrornyzon ", ' Morph. Jahrb.', 34, 1905. 22a. Rrawetz, L.—" Entwicklung des Knorpelsohadels von Ceratodus >:, ' Bull. Soc Imp. Nat. Moscou ', 24, 1911. 23. Miiller, J.—" Vergleichende Anatomie der Myxinoidea ", ' Abh. K. Akad. Wiss. Berlin', 1839. 24. Packer, T. J.—"On the blood-vessels of Mustelus", 'Phil. Trans. Roy. Soc.', 1886. VERTEBRATE HEAD 841

25. Pehrson, T.—"Some points in the development of Teleostoniian fishes",' Acta Zool.', 3, 1922. 25 a. Pollard, H. B.—" The suspension of the jaws in fish ", ' Anat. Anz.', 10, 1895. 26. Rabl, P.—" tlber die Entwicklung des Venensystems der Selachier ", ' Festschr. f. Leuckart', 1892. 27. Raffaele, D. F.—" Ricerche sullo sviluppo del sistema vasculare nei Selacei ", ' Mitt. Zool. Stat. Neapel', 10, 1892. 27«. Ridewood, W. G.—"On the hyoid arch in Ceratodus ", ' Proc. Zool. Soc.', 1894. 28. Roux, W.—' Gesammelte Abhandlungen fiber Entwicklungsmechanik der Organismen ', 1895. 29. Schmalhausen, J. J.—" Der Suspensorialapparat der Ksche ", ' Anat. Anz.', 56, 1923. 30. Sewertzoff, A. N.—" Recherches sur l'origine des vertebres in- ferieurs ",' Arch. Russ.', 1916. 31. " Die Morphologie des Visceralapparates der Elasraobranchien ", ' Anat. Anz.', 56, 1923. 31 a. Swinnerton, H. H.—" The Morphology of the Teleostean head skeleton ", ' Quart. Journ. Micr. Sci.', 45, 1902. 32. Van Wijhe, J.—" Friihe Entwicklungsstadien des Kopf- und Rumpf- skeletts von Acanthias ",' Bijdr. t. d. Dierkunde', 22, 1922. 32a. "Uber das Visceralskelett und die Nerven des Kopfes der Ganoiden und von Ceratodus ", ' Nied. Arch. Zool.', 5, 1882. 33. Wright, J. R.—" On the hyomandibular clefts and Pseudobranchs of Lepidosteus and Amia ", ' Journ. Anat. and Phys.', 19, 1885.