prootic arteries of larvae of dipnoi and amphibia

Prootic arteries of larvae of Dipnoi and Amphibia

HAROLD FOX (Department of Zoology and Conlparative Anatomy, University College, London)

(Received, October 1962)

Introduction

Six aortic arterial vessels develop in Gnathostomes designated I-VI respectively; a rather unfortunate numeration because the first aortic vessel is said to belong to the second or mandibular head segment. The first two aortic arches do not develop to a great extent, for even in lower fishes the respiratory activity of these mandibular and hyoid arches is reduced, and there is a corresponding reduction in their arterial vessels.

In fishes and amphibian larvae the next four afferent arteries from the lateral ventral aorta subdivide into capillaries in the external gill filaments, to ramify with similar ones of corresponding efferent vessels from the lateral dorsal aorta.

When the external gill filaments atrophy short circuit vessels connect afferent and efferent vessels, to provide arterial continuity between lateral ventral, and dorsal aortae.

Elucidation of the fate of these aortic vessels, from fishes throughout the tetrapods to man, and their subsequent reduction in ontogeny and phylogeny, provides a stimulating achievement in the history of comparative morphology (see KERR 1919; GOODRICH 1930).

The present contribution is concerned with the prootic aortic vessels in larvae of Dipnoi and Amphibia. I t includes information on the origin and distribution of the mandibular artery, and furthermore would seem to demonstrate unequivo- cally that the so-called stapedial artery of Gnathostomes-which has a varied no- menclature and has been so successfully exploited in determining the homology of the stapes in higher tetrapods-derives from the hyoid arterial arch.

23 - A . Z. 1963 Acta Zoologica 1963. Bd. X L I V

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Material and methods Many of the specimens here investigated have been used in previous work (Fox

1954, 1957, 1959, 1961 a. b, 1962 a, b, 1963 a, b ) , where acknowledgement to various generous donors has already been made. These genera include the fol- lowing, whose range of size, in terms of total length is shown in brackets :

Neoceratodus ( 13.5-34.5 mm.) ; Protopterus aethiopicus (18-30 mm.) ; Hynobius nebulosus ( 17-32 mm.) ; Hynobius retardatus ( 2 7 and 37 mm.) ; Hynobius (Salamandrclla) beyserlingii ( 18-21 mm.) ; Pleurodrles waltlii ( 10 and 17 mm.) ; Salamandra maculosa (16-26 mm.) ; Cryptobranchus japonicus ( 17-32 mm.) ; Cryptobranchus alleghaniensis (37 mm.) ; Necturus maculatus ( 17-29 mm.) ; Desmognathus fuscus ~ Z I S C U S (20 and 28 mm.) ; Desmognathus yuadrimaculatus (18 mm.) ; Plcthodon cinereus ( 19 mm.) ; Eurycea bislineata (28 and 33 mm.) ; Triturus cristatus carnifex (9-16 mm.) ; Rana temporaria ( 9 mm. to the completely metamorphosed form-stages 29 to 54, Cambar and Mar- rot 1954: see Fox 1962 b ) .

All specimens were sectioned transversely at 10 1" and stained by a variety of routine histological dyes. The illustrations in the text were made by the graphic method ; reconstructions were transferred to Bristol board and redrawn to providc a three-dimensional view of the various morphological components under consideration ( FOX 1954, 1959).

Description of results T H E D I P N O I

The efferent mandibular artery of larvae of Neoceratodus, as in all other specimens examined, originates from the lateral dorsal aorta-just before the latter enters the chondrocranium via the foramen hypophyseos ( ALLIS 1929 a and b) as the internal carotid artery-close to the origin of the palatine nerve, ventro- lateral to the basal plate and ventro-mesial to the trigeminal ganglion. I t leads backwards and slightly outwards and is situated below the the head vein (vena capitis lateralis) and the ramus hyomandibularis facialis, mesio-posterior to the quadrate cartilage, mesial to the stylohyale ( BERTMAR 1959) and to the stylohyale- epihyale junction in the 27 mm. stages and over the basal process in a 34.5 mm. specimen (Text-figs. 1, 2; Plate 1, fig. C ) .

In a 13.5 mm. specimen and in all older ones, a hyoid artery, which in all cases originates from the lateral dorsal aorta, forks into a lower hyoidean (or opercular) vessel, which descends into the operculum below the head vein, mesially to the levator hyoideus muscle and mesio-dorsally to the top of the ceratohyale; and an upper stapedial artery, which originates from the top of the hyoidean artery. I t leads forwards over the incipient otoquadrate cartilage ( EDGEWORTH 1923

Prootic arteries oj larvae oj Dipnoi and Amphibia D.a. D.0.

C.T n.c.

"YC. \ -In' t '

' \ e.e.1. e.e.lV.

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Figure 1. Lateral view of the chondrocranium and some associated blood vessels of a larva of Neoceratodus 16 mm. Ions.

1935; Fox 1963 b) and the facial nerve, lateral. dorsal and thence latero-dorsal to the head vein, mesial to the otic process and lateral to the trigemino-facialis ganglion. The stapedial artery emerges from the chondrocranium through the foramen sphenoticus ( D E BEER 1937), over the front of the otic process and the common root of the rami superior ophthalmicus facialis and buccalis facialis, and continues forwards into the orbit, laterally to the ascending process and below the ramus superior ophthalmicus facialis, amidst the masseter musculature.

The arrangement and distribution of the divisions of the hyoid artery in the 14 mm., 15 mm. and 16 mm. specimens of Ncoceratodus are similar. In the latter the stapedial artery was traced laterally to the levator mandibulae anterior (Fox 1963 a ) , and forwards over the eye and sclerotic cartilage, to the mesial antorbital region, to terminate just behind the nasal region against the front of the pila preoptica (Text-fig. 1 ; Plate 1 ; fig. A ) .

Merely a vestigial hyoidean artery is recognized on either side in a 27 mm. specimen, but a better developed vesse1 in a 34.5 mm. stage leads posteriorly for a short distance, over the otoquadrate cartilage and below the auditory capsule. lateral to the levator hyoideus and mesial to the laterohyale (Plate 1, fig. B) . In a 27 mm. specimen the stapedial artery supplies several branches to the trigemino- facialis ganglion, outside the chondrocranium, and thence traverses the orbit, to descend mesially to the rami nasalis internus profundus V and superior ophthal- inicus facialis and the posterior naris, close to the forebrain; at the junction of the lamina orbitonasalis and the trabecula cranii.

In a 34.5 mm. Ncoccratodus the stapedial artery traverses the quadrate carti-

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Harold Fox lage in its own separate canal, situated over the head vein (Plate 1, fig. C ) . It emerges from the canal through the foramen sphenoticus and below the trige- minus ganglion, and just behind the ascending process supplies several vessels to the mesial surface of the externally-situated masseter musculature and neigh- bouring nerves. Proceeding between the proximal common root of the rami superior ophthalmicus facialis and buccalis facialis it divides within the masseter into : ( a ) a lower ventro-laterally descending mandibular division, distributed laterally to the buccalis facialis and mandibularis-maxillaris V complex and the masseter behind the eye; and ( b ) an upper supraorbital vessel, which as in the 27 mm. specimen is situated mesially to the eye and over the large venous sinuses, dorsal and thence mesial to the ramus ophthalmicus profundus V. Several small vessels lead either mesially or laterally to the superior ophthalmicus facialis nerve, to the upper antero-lateral surface of the head. Thence it is situated below the ramus nasalis profundus V and ends mesially to the posterior naris (Text-fig. 2 ) .

The description in general would seem to agree with that of GREIL (1913), who found the stapedial artery (arteria temporalis) to arise from the dorsal end of the hyoid arch, and to supply the temporal and masseter musculature.

In an 18 mm. specimen of Protopterus aethiopicus the mandibular artery leads forwards ventro-laterally to the trigemino-facialis ganglion, over the front of the hyoid and below the hind end of the incipient quadrate cartilage. In a 21 mm. specimen it proceeds postero-laterally (Plate 1, Fig. G ) , but thence also curves forwards laterally to the front of the ceratohyale between the quadrate and Meckel’s cartilages. A posterior division leads below the quadrate cartilage and basal process, and the origin of the mandibular nerve. In a 30 mm. stage the mandibular artery originates just behind the palatine nerve. A small division leads underneath the hind end of the quadrate cartilage, and a posterior one to the dorso-lateral roof of the pharynx, mesially to the levator hyoideus muscle and basal process, and below the facial nerve.

A stapedial artery only is recognized on both sides in a 21 mm. specimen, about 450 ,IL behind the mandibular artery (Plate 1, fig. F ) .

In a 29 mm. stage its course is similar to that in Neoccratodus, though situated ventrally or laterally to the head vein. In the orbit it was traced below the common trunk of the lateralis facialis nerves and mesially to the masseter musculature, to finally disappear amid the latter.

T H E U R O D E L A

In general a recognizable mandibular artery is similar in all urodele larvae examined. I t was not found in all specimens of Salamandra maculosa, a 37 mm. Cryptobranchus alleghaniensis, a 19 mm. Plethodon cinereus, and all stages of Necturus maculatus smaller than 24 mm. long. In Hynobius (Salamandrella) key-

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Prootic arteries oj larvae oj Dipnoi and Amphibia

Figure 2 . Lateral view of the chondrocranium and some associated blood vessels of 3 larva of Neoceratodus 34.5 mm. long.

serlingii it originates just in front of the otoquadrate cartilage, at the level of the palatine foramen (Plate 2 , fig. K ) ; about 60 j i in front of these structures in Necturus 29 mm. long.

As in Hynobius nebulosus and Hynobius retardafus it leads postero-ventrally. or posteriorly; in a 22 mm. H . nebulosus against the mesio-posterior surface of the basal process-not over it as in Neoceratodus-mesial or mesio-ventral to the quadrate cartilage and digastricus and mesio-dorsal to the top of the ceratohyale (Plate 2, fig. 1). Thence it curves forwards behind and thenceforth lateral to the quadrate and Meckel's cartilages (Text-fig. 3).

In a 32 mm. Hynobius nebulosus the mandibular artery first leads forwards for about 100 j( before curving backwards, finally to be distributed in the typical manner. The artery is first recognized in a 17 mm. Cryptobranchus japonicus and likewise in 19 mm. and 19.5 mm. stages includes a small posterior division, directed beneath the front of the hyoid blastema. In a 26 mm. and older stages of Cryptobranchus japonicus it proceeds for about 670 ,IC postero-mesially to the quadrate cartilage, laterally or ventro-laterally to the palatine artery. Thence it curves forwards mesially to the ramus mentalis externus facialis, latero-dorsally and laterally to the quadrate and Meckel's cartilages to supply the masseter musculature. This artery was erroneously confused with the hyoid artery in an earlier investigation (Fox 1954). A mandibular artery originates 280 j c , 380 i", 170 ,p and 550 p in front of the stapedial artery in 20 and 28 mm. specimens of Desmo-

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Harold Fox p.0.

C

Figure 3. Lateral view of the chondrocranium and some associated blood vessels of a larva of Hynobius (Safamandref fa) keyserlingii 21 mm. long.

gnatllus fuscus fuscus, a 16 mm. Triturus cristatus carnifex and the two specimens of Hynobius retardatus.

In a 28 mm. Desmognathus and an 18 mm. Desmognathus quadrimaculatzu a mandibular artery is recognized below the otoquadrate cartilage, or the hind end of the basitrabecular process (29 mm. Necturus) , or below the basal plate (33 mm. Eurycea bislineata).

A well developed stapedial artery is recognized in all urodeles examined except for one 19 mm. specimen of H . (Salamandrella) keyserlingii, a 10 mm. and one member of a pair of 17 mm. specimens of Pleurodeles waltlii, a 24 mm. Sala- mandra maculosa, and specimens of Cryptobranchus japonicus and Triturzis cristatus carnifex smaller than the 26 mm. and the 14 mm. stages respectively. Recognition was uncertain in a 33 mm. Eurycea bislineata. No hyoid artery was discovered in any specimen af Necturus.

In a 22 mm. Hynobius nebulosus, like other urodeles, a stapedial artery originates from the lateral dorsal aorta below the auditory capsule, ventro-laterally to the columella. It proceeds ventro-mesially and thence mesially to the columella stilus (32 mm. H . nebulosus), laterally or dorso-laterally but ultimately ventrally to the head vein, over the facial nerve and mesially to the otic process (Plate 2, fig. K) . It emerges through the foramen sphenoticus mesially or dorso-mesiallv to the masseter musculature, and is distributed between the latter and the proximal common ramus mandibularis-maxillaris V, below the ramus superior ophthalmicus facialis (Text-figs. 3, 4; Plate 2, figs. H, J ) .

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Prootic arteries oj larvae o j Dipnoi and Amphibia C.S.

co I

p.a.

35 1

I i.c.a.

Figure 4. Lateral view of the chondrocraniurn and some associated blood vessels of a 1arv;i of Hynobius nebulosus 32 rnrn. long.

The arrangement and distribution of the stapedial artery are similar in urodcles. though there is some variability especially in relation to the head vein, columella and stilus (or strand). Occasionally in Tr i turus it may lead forwards below the facial nerve.

O n emergence from the chondrocranium an upper division was traced to the hind region of the orbit ( H . retardatus, H . (Sa lnmandrr l la ) keyserlingii) , or to the rami maxillaris V and buccalis facialis and the venous sinuses (Salarnandru maculosa), or to the trigeminal ganglion and associated nerves just bclow the origin of the truncus infraorbitalis ( Cryptobrnnchus japonict~s) . A lower division was found to be distributed to the masseter musculature ( H . rctardatus, H . (Sola- mandrel la) keyserlingii) , and over or just anterior to thc ramus mandibularis V, laterally or into the masseter muscle ( Cryptobranclius japonicus, Drsmognatli I / 1

~ U S C U S ~ U S C U S , Pleurodeles waltlii, Plethodon cinereus, and Triturus cristatus carni- f e x ) . In Cryptobranchus alleghaniensis an upper supraorbital vessel supplies the trigeminal ganglion, a central infraorbital leads o17er the ramus mandibularis \' to descend mesially to it, ventro-laterally to the masseter below the truncus infraorbitalis, and a lower mandibular vessel supplies the masseter musculature laterally to the mandibular nerve.

In a 21 mm. H . (Salamandrel la) keyserlingii, or on the left side of a 17 mm. specimens of Pleurodeles waltlii a hyoid artery, which leads forwards ventro- laterally to the columella and ventrally to the head vein, forks into: a hyoidean (opercular) artery distributed mesially to the digastricus, ventrally to the ramus

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Harold Fox jugularis facialis and thence vertically downwards between the digastricus and the top of the ceratohyale; and a stapedial, distributed like that of Hynobius nebuEosus (Plate 2, fig. J ) .

In a 19.5 mm. Cryptobranchus japonicus, on both sides 650 ,u behind the mandibular artery, a small hyoidean artery only is present, supplying the roof of the pharynx. Merely incipient stapedials are recognized in a 22 mm. C. japonicus. A tiny hyoidean was recognized in a 9 mm. Triturus, 170 ,I& behind the mandibular artery, and it is strongly suspected in Plethodon cinereus, for a delicate vessel originates from the lateral dorsal aorta about 40 ,IL (left), and 70 E L (right), behind the stapedial artery, to lead for a short way towards the front of the columella stilus.

T H E A N U R A

*4 mandibular artery is recognized from the 9 mm. (stage 29) to the metamorphosed specimen (stage 54). In the former at the level of the hypophysis it proceeds outwards, mesially to the mandibular nerve, and in 16 mm. and 33 mm. specimens (stages 41 and 47) it divides into: a dorso-lateral vessel, distributed to the roof of the pharynx mesio-ventral to the eye and mesial to the processus muscularis quadrati, an upper inner vessel to the levator mandibulae anterior and a lower one to the orbito-hyoideus (levator hyoideus). In stages 49 to 51 (larvae shortening in length from 35 mm. to 33 mm.) a similar upper division (becoming progressively smaller) and a lower division likewise lead on the one hand to the dorsal surface of the levator mandibulae anterior and super- ficialis, below the optic nerve, and on the other hand underneath the masseter muscle and thence mesial and mesio-ventral to the processus muscularis quadrati, to fork into anterior and posterior vessels distributed to the orbito-hyoideus muscle. The mandibular artery of stages 53 and 54 is located 570 p and 600 ,LC respectively behind the front surface of the auditory capsule (comparable distance of the hyoid artery in stage 53 is 1190 p ) . In stage 54 upper and lower mandibular vessels are separate just behind the region where the internal carotid enters the chondrocranium, and they terminate in a degenerate network of vessels behind the origin of the facial nerve.

In a 9 mm. specimen an incipient stapedial artery originates 80 ! i in front of a small separate hyoidean artery. No stapedial artery was recognized in an 11 mm. or a 16 mm. specimen (stages 31 and 41). In the latter and in stage 47 a hyoidearl artery leads ventro-laterally to the branchial lymphoid body (first recognized in stage 41), to the anterior region of the operculum.

A small stapedial artery, present in stages 47, 49 (where it is 120 p behind the hyoidean) and 50, but not recognizable thereafter, leads mesial to and thence over the lymphoid body, ventro-lateral to the VII-IX Connective and the head vein. In contrast a stapedial artery is present in Bufo vulgaris japonicus at metamor-

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Prootic arteries OJ larvae o j Dipnoi and Amphibia

phosis (fig. 78, DE BEER 1926), situated below the head vein, over the post-palatine commissure, laterally to the auditory capsule and mesially to the otic process. In stages 49 to 52 a hyoid artery divides below the lymphoid body into a small anterior and a large posterior hyoidean vessel, alongside the top of branchiale I. In stage 53, only the hyoidean vessel is recognized as a complete arterial arch, which leads forwards and thence backwards to join the truncus arteriosus.

Other gill capillaries and filaments are reduced and efferent and afferent epibranchial arterial arches I (carotid), I1 (systemic) and I V (pulmo-cutaneous) are likewise complete.

In stage 54 however no hyoidean artery was recognized, but the others are further enlarged.

Discussion An efferent mandibular artery (hyomandibular artery of MAURER 1888), is

recognized in larvae of Dipnoi, Urodela and Anura and particularly in the two latter groups it can be traced to the outer surface of the lower jaw. In some urodeles and Dipnoi it may well substitute for the weakly developed, or absent hyoidean artery. The morphological relations of the mandibular artery in young larvae of these two groups are extremely similar, and it is of interest to find that in 17 mm., 19 mm. and 19.5 mm. specimens of Cryptobranchus japonicus, and 21 mm. and 30 mm. specimens of Protopterus aethiopicus it forks into anterior and posterior divisions, like efferent epibranchial arteries I-IV of specimens of Neocerutodus (Text-figs. 1 , 2 ) used in the present work (see also KELLICOTT 1905 and GREIL 1913. Likewise the artery divides in R a m , though in a some- what complicated manner to supply the jaw musculature. The condition in larvae of Dipnoi and urodeles may be a primitive one; that of a vestigial efferent branchial vessel with pretrematic and post-trematic divisions, for Agnathan Ostra- roderms possessed complete and functional branchial arches, with epibranchial arterial vessels and open gill clefts in premandibular, mandibular and hyoid segments ( STENSIO 1927; WATSON 1954). The mandibular artery still maintains its relationship with the quadrate-Meckel’s cartilage-a derivative of the mandibular branchial skeleton.

Among Gnathostomes an artery is recognized, usually to arise from the lateral dorsal aorta (the so-called internal carotid), or by branching from the top of the hyoidean aortic arch, and can be traced from Selachians to mammals (de Beer 1926).

This artery has been called a facialis in reptiles, birds and mammals (RATHKE 1857; VERSLUYS 1898, 1904; SCHMALHAUSEN 1923; GOODRICH 1916), a petrosa lateralis in amphibia ( DRUNER 1904), carotis externus (or external carotid) in fishes (ALLIS 1914 b) and Lapidosiren (ROBERTSON 1913), auricular in chick (TWINING 1906), temporalis in Ceratodus (GREIL 1913; ALLIS 1914a and b ) ,

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P L A T E 1

All photomicrographs are of transverse sections 10 / i thick. Nose-to-cloaca1 length of specimens is in brackets. Figure A. Photomicrograph of specimen of Neoceratodus 16 mm. long (10.28 nitn.), showing the origin of the hyoidean and stapedial arteries; 2.32 mm. from the tip of the snout, Figure B. Photomicrograph of specimen of Neoceratodus 34.5 mm. long (17 .55 mni.), sliow- ing the origin of the hyoidean and stapedial arteries by division of the hyoid artery; 3.88 mm. from the tip of the snout. Figure C. Photomicrograph of same specimen as in figure B, showing the origin of the mandibular artery from the lateral dorsal aorta, over the basal process and below the head vein; and the location of the stapedial artery within the quadrate cartilage; 3.67 mm. froin the tip of the snout. Figure D. Photomicrograph of same specimen as in figure B, showing the origin of the ophthalniica magna artery from the internal carotid artery; 3.18 mm. from the tip of the snout. Figure E. Photomicrograph of same specimen as in figure B, showing the emergence of the

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Harold Fox ophthalmica magna artery through the foramen spheno-trabeculare; 2.85 mm. from the tip of the snout. Figure F. Photomicrograph of specimen of Protopterus aethiopicus 21 mm. long ( 12.45 mm.), showing the origin of the stapedial artery from the lateral dorsal aorta; 2.43 mm. from the tip of the snout. Figure G . Photomicrograph of same specimen as in Figure F, showing the origin of the mandibular artery from the lateral dorsal aorta; 2.04 mm. from the tip of the snout.

P L A T E 2. Figure H. Photomicrograph of a specimen of Hynobius nebulosus 32 mm. long (14.4 mm.) , showing the origin of the stapedial artery from the lateral dorsal aorta, ventro-mesially to the columella; 2.99 mm. from the tip of the snout. Figure I. Photomicrograph of same specimen as in figure H, showing the origin of the mandibular artery from the lateral dorsal aorta; 2.53 mm. from the tip of the snout. Figure J. Photomicrograph of specimen of Hynobius (Salamandrel la) keyserlingii 2 1 mm. long (9.02 mm.), showing the origin of the hyoidean and stapedial arteries from the hyoid artery; 2.06 mm. from the tip of the snout. Figure K. Photomicrograph of same specimen as in figure J, showing the origin of the mandibular artery from the lateral dorsal aorta; 1.84 mm. from the tip of the snout.

and Cryptobranchus japonicus ( OSAWA 1902), carotis facialis in lizards, temporo- orbitalis in crocodiles, temporomaxillaris in Testudo and Chelone ( SHINDO 1914), orbitalis ( DE BEER 1926), and stapedial, especially in mammals ( TANDLER 1902; SHINDO 1914)) and in Gecko (Hafferl, 1921), and in Sphenodon (O'DONOGHUE 1920; see GOODRICH 1930).

The artery has an extremely constant relationship with the auditory ossicles, especially the stapes which it often pierces (see VERSLUYS 1904 in Lacertilia, and DE BEER 1926).

I t divides into three in reptiles (SHINDO 1914; O'DONOGHUE 1920), birds (TWINING 1906)) and mammals (TANDLER 1902)) and in man the supraorbital and infraorbital vessels arise from a common stem, which together with the mandibular division originate from the internal carotid artery, and generally are distributed with the divisions of the trigeminal nerve.

The stapes first appears as a ring, the annulus stapedis, which encircles the stapedial artery. Ultimately part of the artery which joins the internal carotid atrophies, though it is retained in the rat, and the remainder anastomoses with the external carotid to form the meningeal artery.

In larvae of Neoceratodus, Hynobius (Salamandrel la) keyserlingii and Pleuro- delcs zualtlii a dorsal artery originates as an anterior fork from the top of the hyoidean, whose arrangement and distribution leave no doubt that it is the homologue of the stapedial of higher forms. Presumably in Gnathostomes when it arises directly from the internal carotid, it does so owing to the loss, either during ontogeny or phylogeny, of the hyoidean division of the hyoid artery. Like the constant arrangement of the efferent epibranchial arteries I-IV of Neoceratodus, and the occasional condition of the mandibular artery in larvae of Protopterus and Crypto- branchus, the hyoid artery therefore divides into two. The stapedial artery may

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thus be a pretrematic efferent aortic vessel, once associated with an open hyoid gill cleft of more primitive gnathostomal Acanthodians or Agnathan Ostracoderms: a view which would seem to receive some support from a consideration of its topography, in an illustration of a selachian embryo (Text-fig. 276, GOODRICII 1930).

Many components of the premandibular segment of the Gnathostome head arc well known. Can a premandibular aortic artery, or part of it, of Agnatha be likewise recognized? The lateral dorsal aorta of Neoceratodus after giving rise to an efferent mandibular artery enters the chondrocranium as the internal carotid artery. I t soon gives off: an ophthalmica magna artery, which emerges through the foramen spheno-trabeculare to the eye (Text-figs. 1, 2 ; Plate 1 , figs. D, E ) . and further forwards a dorsally directed carotis cerebralis artery to the brain. Thence all of the internal carotid (16 mm. and 27 mm. specimens), or part of it (34.5 mm. specimen) emerges through the optic foramen, with the optic nerve, as the optic artery or arteria centralis retinae (DE BEER 1926), (Text-figs. 1, 2 ) .

The ophthalmica magna artery of Neoceratodus, situated in front of the mandibular artery and behind the trabecula cranii, originating from the extension of the lateral dorsal aorta, distributed mesially to the levator mandibulae anterior and posterior-of premandibular and mandibular segments (Fox 1963 a ) --could well be the homologue of the efferent epibranchial artery of the premandibular segment (see ALLIS 1914 b). This conclusion agrees in part with that of HOLM- GREN (p. 122, 1943), though his ophthalmice magna in selachian embryos is con- sidered to be the premandibular afferent epibranchial artery.

The optic artery, or part of it, could well be the anterior termination of the lateral dorsal aorta.

No ventral afferent epibranchial arteries of the premandibular, mandibular or hyoid segments were recognized in any of the young specimens of Dipnoi and urodeles examined in this work, but then the optic, ophthalmic and the stapedial arteries are retained almost from the beginning of ontogeny throughout phylogeny, to subserve as a vascular supply to the eyes, facial musculature and nervous system

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Summary 1. Features of the prootic arterial system and associated structures of larvae of

Dipnoi, Urodela and Anura were investigated from transverse microscopic sections.

2. A stapedial artery is presumed to be a pretrematic derivative of the efferent hyoid artery; loss of the post-trematic hyoidean in ontogeny or phylogeny would erroneously suggest the stapedial to derive directly from the lateral dorsal aorta.

3. An efferent mandibular artery supplies the lower jaw. The forked arrangement of the hyoid and the mandibular arteries, like that of the hinder efferent epibranchials I-IV of Nuoceratodus, suggests a primitive pre- and post-trematic arterial structure ; a relic of their earlier epibranchial ancestry.

4. It is tentatively suggested that the ophthalmica magna artery is the homologue of the premandibular efferent epibranchial artery, and that either the wholc or part of the anterior termination of the lateral dorsal aorta gives rise to the optic artery (arteria centralis retinae).

Acknowledgements Sincere thanks are due to Dr. A. d’A Bellairs of St. Mary’s Hospital Medical

School for his advice; and to Mr. C. Atherton, who prepared the photomicrographs with equipment from the Department of Genetics U.C.L., generously pro- vided by Professor H. Gruneberg.

References ALLIS, E. P., 1914 a. The pituitary fossa and trigemino-facialis chamber in Ceratodus

forsteri . Anat. .4nz. 46, 625-637. - 1914 b. The pseudobranchial and carotid arteries in Ceratodus forsteri . Anat. Anz. 46,

6 3 8-647. - 1929 a. Concerning the pituitary fossa, the myodonie and the trigeinino-facialis chamber

in recent gnathostome fishes. J . Anat. Lond. 63, 95-141. - 1929 b. Concerning the course of the efferent mandibular artery in Ceratodus. J. Anat.

Lond. 63, 282. I~ERTMAR, G., 1959. On the ontogeny of the chondral skull in Characidae with a discussion

on the chondrocranial base and the visceral chondrocranium in fishes. Acta Zool. Stockh. 40, 203-364.

CAMBAR, R. and MARROT, BR., 1954. Table chronologique du dCveloppement de la Grenouille agile ( R a n a dalmatina Bon.). Bull. biol. 88, 168-177.

DE BEER, G. R., 1926. Studies on the vertebrate head, 11. The orbitotemporal region of the skull. Quart. J. niicr. Sci. 70, 264-370.

- 1937. The development of the vertebrate skull. Oxford University Press. DRUNER, L., 1904. Studien zur Anatomie der Zungenbein-, Kiemenbogen- und Kehlkopf-

niusculatur der Urodelen 11. Zool. Jb. 19, 361--G90.

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Prootic arteries oj larvae oj Dipnoi and Amphibia EDGEWORTH, F. H., 1923. O n the development of the hypobranchial, branchial, and laryn-

geal muscles of Ceratodus. With a note on the development of the quadrate and epihyale. Quart. J. micr. Sci. 67, 325-368.

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Harold Fox STEXSIO, E. A., 1927. The Downtonian and Devonian vertebrates of Spitzbergen. I. Fam.

TANDLER, J., 1902. Zur Entwicklungsgeschichte der Kopfarterien bei den Mammalia. Morph.

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- 1904. Entwicklung der Columella auris bei den Lacertilien. Zool. Jb. 19, 107-188. WATSON, D. M. S., 1954. A consideration of Ostracoderms. Phil. Trans. B, 238, 1-25.

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Explanation of abbreviations on Text and Plate figures

ax . a.n. b.t.

cb. I

c.e. c.c.a. c.p. C.S. C.t.

C.

co.

d. d.a. ep. e.c.a. ex. I, Lab. f.b. f.oc. f.01. f.op. f.ov. fsp. f.st. f.s.0.

hb. I hd.a. hy.a. h.b. in. i.c.a. 1. I.C.

auditory capsule abducens nerve basitrabecular process ceratohyale ceratobranchiale I columella ceratohyoideus externus carotis cerebralis artery crista parotica columella stilus cornu trabecula digastricus muscle dorsal aorta epihyale external carotid artery

11, IV efferent epibranchial arteries foramen abducentis fore-brain foramen oculomotorius foramen olfactorius foramen opticus foramen ovale foramen sphenoticus foramen spheno-trabeculare common foramen sphenotra- beculare-oculomotorius hypobranchiale I hyoidean artery hyoid artery hind-brain interhyoideus muscle internal carotid artery lateroh y a k labial cartilage

1.d.a. 1.h. 1.m.a. 1.m.p. 1.11. Lon. n1.a. m.b.

m.m. II1.C.

I l l . 11.

not . 11.a. I n.c. n.cp. n.s.

0p.a. 0.a. 0.m.a. 0s. I, I1 pu1.a. p.a. p.b. p.n.

p.0.

q- r.c. s.a. t.s. V.C.I.

0.

rw

lateral dorsal aorta levator hyoideus muscle levator mandibulae anterior levator mandibulae posterioi lateralis facialis nerve lamina orbitonasalis mandibular artery mid-brain Meckel’s cartilage masseter muscle maxillo-mandibularis rierve notochord neural arch I nerve cord nasal capsule nasal septum otoquadrate cartilage optic artery occipital arch ophthalmica magna artery occipito-spinal arches I, I1 pulmonary artery ascending process basal process ramus ophthalmicus profundus V. otic process pterygoid process quadrate cartilage rectus cervicis stapedial artery tectum synoticum vena capitis lateralis

16

prootic arteries of larvae of dipnoi and amphibia

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