Early development of the head and pharynx of Neoceratodus with a consideration of its phylogeny

J . Zool. (1965) 146,470-554

Early development of the head and pharynx of Neoceratodus with a consideration of its phylogeny

H A R O L D Fox Department of Zoology and Comparative Anatomy, University College, London

(Accepted 13 October 1964)

(With 4 plates and 42 figures in the text)

The development of the head and pharynx of larvae of Neoceratodus (ranging in length from 11.5 to 34.5 nun) was investigated from microscopic transverse serial sections. The structures studied included the chondrocranium and visceral arches, ossifications, cranial and anterior spinal nerves, musculature and vascular system. These components of Neoceratodus are compared with similar ones, likewise investigated, in Rana temporaria and Rana esculenta (33 and 26 mm long, respectively), and in various genera of Urodela, either previously investigated by the author or by reference to the earlier literature.

Some new homologues of the various morphological components of the head and pharynx of these groups are suggested.

On the basis of the larval structure an assessment is made of the classical view of a close phylogenetic relationship between Neocerarodus and the two amphibian groups. It is concluded that they share a common derivation from pro-dipnoan-amphibian stock- of crossopterygian ancestry-in the early Devonian: a conclusion which supports an earlier somewhat similar view of Goodrich.

It is further considered that there is evidence of a quasi parallel evolution between Neoceratodus and Urodela, though some assumed similarities in larval structure are spurious; nevertheless, in some ways, they are more similar than are Neoceratodus and members of the Anura.

A common origin of Neoceratodus (Dipnoi) and the amphibian groups supports the view of a monophyletic derivation of the Tetrapoda.

Contents

Introduction . . . . .. . . . . . . . . . . History of previous investigations on Neoceratodus . . . .

Larve . . . . . . * . . . .. . . . . Adults . . . . .. . . . . . . .. ..

Materials and methods . . .. . . . . . . . . Description of the head and pharynx of the larva of Neoceratodus

The chondrocranium and visceral skeleton . . . . . . Ossifications . . . . . . .. . . . . . . Musculature . . .. .. . . . . .. .. Arterial system . . . . .. . . . . .. .. Venoussystem . . . . .. . . . . . . . . Cranial and anterior spinal nervous system . . . .

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Page . . 471 .. 412 . . 472 .. 413 . . 474 . . 474 . . 474 .. 485 .. 489 .. 495 .. 502 .. 503

The head and pharynx of Rana temporaria and Rana esculenta 33 mm and 26 mm long respectively . . . . . . . . . . . . .. .. .. 516

The chondrocranium and visceral skeleton . . . . . . . . . . . . 516 Musculature . . . . . . .. . . . . . . . . . . . . 517 Arterial system . . . . . . .. . . . . . . . . . . . . 520 Cranial nerves . . . . . . . . . . . . . . . . . . . . 521

410

E M B R Y O L O G Y O F N E O C E R A T O D U S

Page Comparison of the head and pharynx of larvae of Neoceratodus Urodela and Anura 526

Chondrocranium and visceral skeleton . . . . . . . . . . . . 526 Cranial pharyngeal and anterior spinal nerves . . . . . . . . . . 531 Musculature . . . . . . . . . . . . . . . . . . . . 536 Arterial system . . . . . . . . . . . . . . . . . . . . 537

Phylogeny of the columella in Urodela from evidence in Neoceratodus . . . . 538 Discussion . . . . . . . . . . . . . . . . . . . . . . 540 Summary . . . . . . . . . . . . . . . . . . . . . . 544 Key to plate and figure lettering . . . . . . . . . . . . . . . . 545 References . . . . . . . . . . . . . . .. . . . . . . 548

47 1

Introduction

The aim of the present work is twofold: to describe the structure and development of various components of the head and pharynx of young stages of Neoceratodus, and to compare results with those in Urodela and Anura; which two groups have been considered to be closely allied to the Dipnoi. The cranial morphology of a variety of organ systems, in larvae of several genera of Urodela, has been investigated previously by the author first hand, and in order to obtain comparable and detailed information in Anura, young larvae of Rana were likewise investigated, with emphasis on the relationship of the cranial nerves and musculature to the skeleton.

Though caution is essential when comparing larvae of living specimens with fossil adult ancestral types (Watson, I926), ontogenetic analysis may reveal ancestral embryonic characteristics, and such information should justify speculation-from the standpoint of embryology alone-on the phylogeny of Dipnoi and Amphibia.

The following brief account of the literature on phylogenetic relationship of Dipnoi and Amphibia is not intended to be a comprehensive one. Further details can be obtained from the excellent reviews of Eaton (1959), Szarski (1962) and Parsons & Williams (1963).

It has been generally accepted that ancestral Dipnoi, like Dipterus (and Amphibia) presumably, originated from crossopterygian stock, in the early Devonian (Cope, 1892 ; Dollo, 1895; Baur, 1895; Haekel, 1911; Watson, 1912; Kesteven, 1931a, 1950; Save- Soderbergh, 1934, 1935; Gregory & Raven, 1941; Wickbom, 1945; Westoll, 1943a, 1949; Romer, 1946, 1956). Dipnoi are considered to be closely related to Amphibia (Wilder, 1887), but more especially to the Urodela (Save-Soderbergh, 1934, 1935; Kindahl, 1938; Rudebeck, 1945; Wickbom, 1945). Haekel (1870) actually derived all Amphibia from Dipnoi, but Holmgren (1949a,b), on evidence based mainly on fin structure, considered perennibranch urodeles only to originate directly from Dipnoi of Conchopma type, and Stegocephalia and all tetrapods to derive from Crossopterygii.

Kesteven (193 la, 1950) actually called dipnoans the most primitive known amphibians. Direct ancestry of Dipnoi in tetrapod phylogeny has been specifically denied by numer-

ous workers (Cope, 1882; Dollo, 1895; Baur, 1895; Winslow, 1898; Luther, 1913; Gregory & Raven, 1941 ; Jarvik, 1942, 1952, 1960; Lehman, 1955), and even that Dipnoi and Rhipidistia are not closely related (Jarvik, 1952). de Beer (1937), on embryological grounds, recognized the affinity between urodeles and Dipnoi, but found no justi- fication for the view that urodeles derive independently of the Anura from Dipnoi, and Gregory (1915) excludes them by virtue of their specialized dentition. Romer (1946, 1956)

412 H A R O L D F O X

calls the Dipnoi an evolutionary sideline, related to amphibian ancestors not in a parental, but in an avuncular position. Watson (1926) writes of parallel evolution-as did Baur (1895), Dollo (1895), Bridge (1904) and Gregory (1915)-of not distantly related stock; that Dipnoi, Osteolepids and Amphibia arose together from a common ancestry before the Middle Devonian (Watson & Gill, 1923); and that they were not long separated from a common ancestor at this time (Westoll, 19433).

The view that Dipnoi and Amphibia share a common stem was agreed by Boas (1880), Semon (1901b), Kellicott (1905), Edgeworth (1925), Kesteven (1931u), Szarsky, (1962) and Goodrich (1924) came to a similar conclusion, for he believed tetrapods to have arisen from the base of the dipnoan stem, before the latter had specialized like the later extinct and modern forms; a conclusion which in general is supported in the present work.

History of previous investigations on Neoceratodus Lar sue

In 1870 Gerard Krefft, Curator and Secretary of the Australian Museum, Sydney, first reported (and figured) “a giant amphibian allied to Lepidosiren” from the River Burnett of the Wide Bay District of Queensland, Australia. Others were subsequently found in the River Mary (Caldwell, 1884; Illidge, 1893). It was called Cerutodus Forsteri (Krefft), for its tritoral teeth plates were extremely similar to those of a genus of fossil forms so named by Agassiz (1833-43). The specific name celebrated its discoverer. Gunther (1871) soon described the internal and external structure of the adult, and clearly showed its relationship with other lung-fishes Lepidosiren and Protopterus, and Hancock & Atthay (1871) recognized its affinity with Dipterus. In order to distinguish living from fossil forms it was named Neocerutodus (Castlenau, 1876), or Epicerutodus (Teller, 1891), the former name is more widely used and probably more appropriate. It is also known as the Burnett or Dawson Salmon, Barramundi or Barramoondi, Flat-head, Djellah or Teebine (Gunther, 1871; O’Connor, 1898).

Eggs, larvae, which are extremely helpless soon after hatching (Bancroft, 191 l), and juvenile adults are rarely found, and since 1914 under the Fish and Oyster Act Neoceru- todus has been a protected animal though OConnor (1897), many years earlier, tried to protect them.

In October 1958, in answer to my request for young stages of larvae, Mr Tom C. Marshall, Government Ichthyologist of the Department of Harbours and Marine, Brisbane, wrote to me “. . . that no such material exists here in Queensland. I am surprised to know that you have some ranging from 11 -5 mm to 16 mm and in over 30 years I have never seen young Cerutodus”.

Nevertheless, eggs were reared for up to three months at the Burnett or in the laboratory by Caldwell (1884); for eight months by Illidge, according to Dean (1912) and Longman (1929), and one specimen by Bancroft (1918) up to two years. Ramsey (1876) was probably the first to study adults in captivity and later Caldwell (1884) first briefly described eggs (and larvae), to be about 2-5 mm in diameter (2.7 to 3 mm, Semon, 1893), surrounded by a gelatinuous capsule 3.5 mm thick, laid singly in water and strongly reminiscent of those of Amphibia, especially newts. Richard Semon, who arrived in Australia in 1891, by great perseverence accumulated a comprehensive series of young stages starting with the uncleaved egg. In the well-known Semon’s Forschungsreisen in Australien, between

E M B R Y O L O G Y O F N E O C E R A T O D U S 413

1893 and 1913 fourteen major publications deal with development and structure of a wide variety of organ systems of larvae and adults.

One of the earliest descriptions of the development of the chondrocranium, hyobranchial and occipital arch skeleton, up to Semon stage 47 (42 days post-hatching, 15.7 mm long) was given by Sewertzoff (1902). Subsequently, Krawetz (191 1) and Schmalhausen (1923a,b), in larvae up to Semon stage 48 (a little less than 63 days post-hatching, 17.8 rnm long), and de Beer (1926, 1930) in larvae 13 to 17 mm long, described aspects of the chondrocranium, visceral cartilages, upper jaw suspension and associated nerves and blood vessels. Edgeworth (191 1, 1923u, 1925, 1926a,b) described the development of the musculature of the head, and somewhat briefly its innervation-as did Luther (1913) on the trigeminal musculature and nerves V and VII-hyobranchial and quadrate cartilages. Recent work includes descriptions of the chondrocranium, hyoid, trigeminal and facial nerves and their associated blood vessels (Bertmar, 1959, 1961, 1962a, 1963), and of the occipital region, prootic musculature, arteries and hyoid (Fox, 1961c, 1962, 1963b,c,d). The larval vascular system was described first by Kellicott (1905), later by Greil (1908-13), and in part considered among previously mentioned publications. Aspects of the venous system of the head have recently been described by Bertmar (1965a).

The embryology of the brain was investigated by Sewertzoff (1902), Bing & Burckhardt (1905) and Rudebeck (1945); olfactory organs by Broman (1939) and Bertmar (19656), lateral line organs of the head by Pehrson (1949) and Holmgren & Pehrson (1949); the pronephros by Fox (1960, 1961b,c, 1962, 1963u), together with the mesonephros also (Kindahl, 1938). Furthermore, Wickbom (1945) studied chromosome structure of Neo- crratodus and compared it with that in Amphibia. Summaries on the larval head include those on its musculature (Edgeworth, 1935), cartilaginous skeleton and ossifications (Gaupp, 1906; Holmgren & Stensio, 1936; de Beer, 1937), hyoid arch (Bertmar, 1959), and aspects of the snout in dipnoan larvae (Thomson, 1963, 1965). Finally, early development of the egg and larva, pronephros, teeth and paired fins was described by Semon (1893, 1898, 190la,c,d).

Adults Many early papers are mainly of historical interest though reference to them may still

be made with profit. After Gunther’s (1871) descriptions, the brain (Huxley, 1876) and cranial nerves (Beauregard, 1881) were described. Others in this field include van Wijhe (1 882), Wilder (1887), Sanders (1889), Bing & Burckhardt (1905) and Holmgren & van der Horst (1925)-see also brief summary by Stensio 1963 : 78-82-and information on the occipital nerves was presented by M. Furbringer (1897) and K. Furbringer (1904). Fin musculature was soon to be investigated by Humphrey (1872), aspects of the glottis by Wiedersheim (1904), cephalic musculature by Jaquet (1899) and its innervation by Ruge (1897), Luther (1913), Edgeworth (1935) and Kesteven (1944).

The heart and truncus valves were examined by Lankester (1879), together with the aortic arches (Boas, 1880), and the whole vascular system by Spencer (1893). Boas rightly concluded that Neocerutodus possesses a primitive double circulation like tetrapods. Early papers include one by Ayers (1885) on the alimentary canal and its derivatives.

Krefft (1870), who first furnished details of the dentition, also briefly referred to the skull-the palate and the upper part are of bone-jaws and hyoid. Skull and dentition were described in more detail and figured by Gunther (1871), Huxley (1876)-who described


its autostylic jaw suspension-Bruhl (1880), Jaquet (1899), K. Furbringer (19O4), Kesteven (1931b) and Holmgren & Stensio (1936). Other publications include those on jaw suspension (Pollard, 1895), hyoid (Ridewood, 1894), visceral skeleton (van Wijhe, 1882), which structure was reviewed by Gaupp (1904), auditory organ (Retzius, 1881) and occipital arches (M. Furbringer, 1897), and various structures including the skull, branchial and shoulder skeletons (Kisselewa, 1929). The anatomy and homology of the skull, hyomandibula, blood vessels, nervous system, pituitary fossa, myodome, trigemino-facialis chamber and lateral line organs were considered by Allis (1914a,b, 1915, 1929a,b, 1930, 19326, 1934). Details of the adult anatomy are summarized among others by Goodrich (1909, 1930), Kerr (1919) and Young (1950); and the skull and its ossifications by de Beer (1937). Finally, the head of the extinct Chirodipterus of the Upper Devonian was described in 1935 by the late Save-Soderbergh, and subsequently his results were published by Jarvik & Stensio (1952).

Material and methods Morphological examination was made from transverse or, occasionally, horizontal or sagittal

microscopic serial sections 10 p thick. Larvae of Neoceratodus investigated, in terms of total length (the total number, if more than

one, is in brackets), include the following: 11.5 mm ( 3 ) , 13.5 mm (one transverse, the other a horizontal series), 14 mm, 15 mm, 16 mm (3), 27 mm and 34.5 mm. Reference was also made to a 42 mm sagittal series. Amphibian larvae used or referred to include: transverse series of Hynobius nebulosus, H . retardatus, H . (Salamandrella) keyserlingii, Cryptobranchus japonicus, Cryptobranchus alleghaniensis (37 mm), Salamandra maculosa (24 mm and 25 mm), Ambystoma mexicanum (25 mm), Rana temporaria (33 mm) and Rana esculenta (26 mm). All specimens were fixed in Bouin or Zenker’s fluid, and stained by Ehrlich’s haematoxylin and aqueous eosin, except for the specimens of Cryptobranchus japonicus, which were stained by Heidenhain’s Azan or Weigert and Pasini. Reconstructions of organs from transverse sections were made on graph paper and transferred and redrawn on Bristol board, to provide three-dimensional illustrations (Fox, 1954, 1959, 1963~).

Information of the Semon stages 1 to 48 (Semon, 1893, plates 1 to 8; 1901d, plates 30 to 34) referred to in this work has also been given by Kellicott (1905), Krawetz (191 1) and Edgeworth (1 923a, p. 356), and lllidge (1 893), Dean (1 906, I9 12) and Bancroft (1 91 8) relate larval length to ape.

Description of the head and pharynx of the larva of Neocerutodus

The chondrocranium and visceral skeleton In an 1 1 a5 mm specimen incipient procartilaginous blastemata exist in the regions of

the future trabeculae, quadrate and Meckel’s cartilages, hyoids-situated on each side behind the hyoid clefts and related to ganglion VII-and branchiale 1 and 2 (Figs 1 to 3). Trabecular procartilage, situated behind the blind nasal sac, leads dorso-posteriorly, alongside the fore-brain. In one 1 1 -5 mm specimen mandibular procartilage is already faintly demarcated into quadrate and Meckel’s constituents (Plate I(a)). Prospective branchiale 1 and 2 are situated behind open gill clefts 1 and 2, respectively, and a third cleft on either side has almost broken through. This result confirms Kellicott’s description (1905) of stage F (Semon stage 45) of Neocerutodus. There is a rudimentary ventral laryngeal downgrowth of the pharyngo-oesophageal epithelium, first recognizable in a 10-5 mm


t m o h.b.

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I 1 rnm

FIG. 1 . 11.5 mm (a) specimen of Neocerutodus. Lateral reconstruction of the front of the larva showing procartilaginous arches, levatores mandibulae and brain.

: incipient

FIG. 2. 11.5 mm (b) specimen of Neocerutodus. Lateral reconstruction of similar structures as in Fig. 1, but very slightly more advanced. The trabeculaecranii lie more horizontally, and incipient separation of quadrate and Meckel's cartilages has occurred.


specimen (Edgeworth, 1923~). Externally, the pharynx is protected by an operculum (Plate I(b)).

In a 13-5 mm stage cartilaginous trabeculae cranii meet in front below the fore-brain at a trabecular plate (Plate I(e)), and enclose a hypophysial fenestra (fenestra basicranialis of Krawetz, 191 l), bounded behind by achondrified basal plate (de Beer, 1926) (Figs 4 and 9). A procartilaginous lamina orbitonasalis, the ethmoidalfortsatz of Sewertzoff (1902) or processus antorbitalis of Krawetz (191 1) is present, to derive from the front of the trabecula.

FIG. 3. 11.5 rnm (a) specimen of Neocerutodus. Lateral reconstruction of the front of the larva, showing the relationship of the incipient cranial and anterior spinal nervous system to the levatores mandibulae and hyoideus, and incipient procartilages.

A taenia marginalis posterior has not yet joined the chondrified auditciy capsule (though junction had occurred in a 13 mm specimen of de Beer, 1926); hence the future foramen prootica-now the incisura sphenotica (Greil, 191 3)-between the pila prootica and the front of the auditory capsule has no roof. The quadrate cartilage is suspended auto- stylically and has ascending and otic processes-considered to derive phylogenetically from pre-trigeminus and post-trigeminus branchial ray bars, respectively, of the epimandi- bular portion of the mandibular arch (Allis, 19290, p. 99)-and a basal process (Sewertzoff, 1902; Krawetz, 1911 ; Edgeworth, 19230, 1925; de Beer, 1926; Holmgren & Stensio, 1936). There were no signs of any joint in the latter. The three processes are joined to the pila prootia, auditory capsule and lateral junction of the trabecula and parachordal cartilages, respectively (Plate I(f)).


There is thus an antrum petrosa lateralis (Druner, 1904; Schmalhausen, 19233), enclosed by these processes and the wall of the neurocranium. Bertmar (1963) describes it as a cavum epiptericum, with the ascending and basal processes having been fused with the chondrocranium from the 12.6 mm stage. Furthermore, the latter includes basal and basitrabecular processes. In the orbital cartilage there are a small foramen oculomotorius and a larger foramen sphenotrabeculare (Greil, 1913 ; Allis, 1930)-for the emergence of the ophthalmica magna artery and the pituitary vein-and behind, in the ventro-mesial surface of the auditory capsule there is a separate foramen jugulare as in Protopterus (Winslow, 1898), which transmits nerve IX (Fig. 4). Between the front of the lower jaws-associated with incipient teeth germs-there is a procartilaginous blastema of the intermandibular

FIG. 4. 13.5 mm stage of Neocerufodus. Lateral reconstruction of the neuro- and splanchnocranium and related levator musculature.

cartilage. Behind there is a well-developed and chondrified hyoid, comprising a median basihyale, hypohale, ceratohyale and rudimentary otoquadrate cartilage (Edgeworth, 1923~7, 1926a, 1935; Fox, 1963d). The latter is of varied nomenclature (Figs 4 and 15), i.e. a hyomandibula (Allis, 1915; K. Furbringer, 1904, p. 494, Plates 40, 41, Fig. 43; Krawetz, 1911; Greil, 1913, p. 1293, and Fig. 493), a pharyngohyale (Allis, 1915; Schmalhausen, 1923~; Fox, 19634, an infrapharyngohyale-suprapharyngohyale (Bertmar, 1962a), or an epihyale (Greil, 1913, p. 1398, and Fig. 544). Cartilaginous ceratobranchiale 1 and 2, incipiently chondrified ceratobranchiale 3 and blastemata 4 and 5 are recognized (Plate I(c)). There are now a blind spiracular (hyoid) cleft (Kellicott, 1905; Edgeworth, 1926a), four open gill clefts (and external gill filaments), and an incipient fifth, which is perforated in the 15 mm and subsequent stages. The trachea is first seen as a small posterior outgrowth of the larynx, which confirms the description of Edgeworth (1923~). Fore-fin rudiments, first recognizable in stage 45 (Semon, 1898), or 11.6mm specimen (Edgeworth, 19230) are now established.

In the 14 mm stage merely incipient trabecular horns (cornua) and a tiny lamina orbitonasalis are present, in the region of the nasal capsule (Figs 5 and 10). A delicate pila preoptica

32


of the orbital cartilage forms the anterior margin of an incipient foramen optica. The taenia marginalis posterior has joined the pila prootica to the auditory capsule, and thus there is a complete foramen prootica. Similarly are recognized foramina sphenoticus (between the processus ascendens and the processus oticus), sphenoticus minus, or profundus canal (Holmgren & Stensio, 1936), (between the processus ascendens and the pila prootica), and prooticum basicraniale or facialis (between the processus oticus and the auditory capsule) : homologues of the same-named foramina in amphibian larvae (Schmalhausen, 19233).

The sclerotic cartilage originates from two upper and one lower separate cartilages, which have enlarged and joined to become a delicate but complete ring around the eye in the 16 mm stage (Figs 5 , 6 and 28).

cehy I I 1 mm

FIG. 5. 14 mm stage of Neoc~ru~odus. Lateral reconstruction of similar structures as in Fig. 4, with incipient sclerotic cartilage.

The floor of the chondrocranium comprises a basal plate considered by Bertmar (1959) to be of segmental origin, and the under-surfaces of the paired auditory capsules, which meet on either side of the notochord (Fig. 10). Chondrilied hyoid, ceratobranchiale and epibranchiale 1 , 2 and 3, and procartilaginous ceratobranchiale 4 and 5 are developed (Fig. 16). Cartilage is now present in the fore-fin. Pelvic fin rudiments are found in the 16 mm stage, slightly earlier than in stage 48 (17.8 mm) reported by Semon (1898).

In the 15 mm specimen there are a pair of rudimentary trabecular horns but no nasal septum, and behind the nasal sac there is a tiny cartilaginous lamina orbitonasalis (Figs 6 and 11). The nasal sac, still with a single opening leading into the front of the roof of the mouth, is situated ventrally to it. The otoquadrate cartilage is in incipient cartilaginous continuity with the edge of the basal plate (Fig. 11). A primordium of the epihyale is now distinguishable.

In the 16 mm stage the trabecular horns have extended postero-laterally to the front of the anterior naris, for the primary nasal aperture of each side is now divided into anterior


and posterior nares (which agrees with the results of Bertmar (196%)’ in a specimen at the same stage) by the development of a so-called teleostomian nasal bridge (Allis, 1934, p. 367), both of which open into the front of the roof of the mouth. Recently however both Thomson (1965) and Bertmar (196%) have’challenged the view of the homology of the posterior nares in Dipnoi and Tetrapoda. A median rudimentary nasal septum originates from the anterior trabecular plate, in front of the fore-brain, to separate the nasal sacs. Whether it has an independent origin could not be ascertained for it is not discernible in the 15 mm specimen (Plate I(g)). The lamina orbitonasalis is situated posterolaterally to the posterior naris, trabecular plate and incipient cartilaginous nasal septum (Fig. 12). From the postero-dorsal region of the latter a backgrowth has extended towards a forward extension of the orbital cartilage-the incipient spheno-septa1 commissure-but as there is yet no junction there is thus no roof of the presumptive foramen olfactorius evehens (Fig. 28).

I.mo.

1 mrn q.c.

10 SD Imo.

FIG. 6. 15 mm stage of Neocerufodus. Lateral reconstruction showing further development of the neuro- and splanchnocranium.

A foramen trochlearis is now developed in the upper region of the orbital cartilage. A cartilaginous tectum synoticum extends across the mid-brain region to connect the auditory capsules. There is merely a single large aperture to the median wall of the auditory capsule, as in the older 27 mm and 34.5 mm stages of Neoceratodus (Plate II(c)), and Protopterus, which resembles fishes in this respect (Winslow, 1898). Behind the capsule, on each side, are occipital arches, occipito-spinal arches 1 and 2 and neural arch I, but occipito-spinal arch 1 is reduced (Krawetz, 1911; Fox, 1961c, 1962)’ and cannot be found in later stages. Incipient cartilaginous ribs are associated with occipito-spinal arches 1 and 2 (Figs 12 and 28).

Meckel’s cartilage is associated with a small intermandibular cartilage situated below the median symphysis (Fig. 18; Plate I(g)). The hyoid comprises a median basihyale (of


both sides), called a copula or glossohyale by Kisselewa (1929), hypohyale, ceratohyale, epihyale (the hyomandibula of Huxley (1876), van Wijhe (1882), Ridewood (1894), Sewertzoff (1902) and Schmalhausen (1923a), who also thought it to be an epihyale; interhyale of Edgeworth ( 1 923a, 19264 ; the symplectic of Krawetz (1 91 1) and opercular cartilage of Pollard (1895)), laterohyale Bertmar (1959), which is an undifferentiated extension of the epihyale at this stage, pharyngohyale (otoquadrate cartilage), whose inner end in the 15 mm stage has already joined the parachordal below the auditory capsule, and a small protuberance from the hind end of the quadrate cartilage, or future stylohyale (Fox, 1963d) (Fig. 28, Plate II(a), (e)). The stylohyale may well be the interhyale of Schmalhausen (19234. The epi-laterohyale cartilage has been termed a hyomandibula by Bertmar (1959).

The three cartilages above the ceratohyale figured by Goodrich (1930) in an 18.5 mm specimen may be the otoquadrate, epihyale and laterohyale, or possibly otoquadrate, epi- laterohyale and stylohyale.

As in the older stages, ceratobranchiale 1 4 each have a small related epibranchiale (pharyngobranchiale of Allis, 1915), but not the cartilaginous fifth (Holmgren & Stensio, 1936) (Fig. 18). Krawetz (191 1) described chondrified ceratobranchiale 1-4 and epibranchiale 1-3 at Semon stages 46/47 (13.9-15-7 mm long, 34 days after hatching), but his oldest larvae were similar to my 16 mm stage. A median dorso-ventrally flattened precardial plate of cartilage-the sternum of Greil (1913, Fig. 547, p. 1403)-is situated below the front of the heart and, as previously reported by Edgeworth (1923a), in this stage the paired geniocoracoideus and more laterally situated rectus cervicis muscles insert behind on it (Figs 18 and 28). Incipient pelvic fins are now present-normally they appear about six weeks after the pectorals (Bridge, 1904)-and these have a cartilaginous skeleton. There is a chondrified pelvic girdle in the 27 mm stage.

The chondrocranium, jaws, hyobranchial skeleton, occipital, reduced occipito-spinal 1, occipito-spinal2 and neural (spinal) 1 arches, of a larva of Neoceratodus of Semon stage 47 (equivalent to a specimen 15.7 mm long), are figured by Sewertzoff (1902, Fig. 2A, p. 597). It is generally similar in appearance to the 16 mm stage of the present work. However, no sclerotic cartilaginous ring (Fig. 28) nor ceratobranchiale 5 are shown, though the latter is described in an older specimen, and a tiny foramen jugulare is separated from a presumably erroneously considered and indeed not constant “fenestra ovalis”, a structure not represented in Neoceratodus. The occipital arch is illustrated as situated behind the 5th metotic segment (behind head segment 8). The hind end of the skull is situated behind the 5th extant metotic somite of the 7th metotic segment (for metotic somites 1 and 2 do not develop, Greil, 1913), and thus behind head segment 10 (see Fox, 1962).

In the 27 mm specimen a well-developed nasal capsule has a highly fenestrated roof, but no floor or posterior margin between the nasal cavity and the orbit, and therefore the orbito-nasal foramen is only feebly demarcated. Paired nasal capsules share a common medial, or nasal septum (Plate II(b)). The spheno-septa1 commissure is complete and dorsally encloses a fully demarcated foramen olfactorius (Fig. 7). The trabecular horn meets the spheno-septa1 commissure laterally to the anterior (external) nostril, and a well- developed lamina orbitonasalis is situated behind the posterior (internal) nostril (Figs 7 and 13). This post-nasal cartilage (Jarvik, 1942) is secondarily detached and independent in the adult.

A sclerotic ring is now strongly developed (Fig. 7). At the level of the front of the hypophysial fenestra a narrow epiphysial cartilage connects each orbital cartilage dorsally.

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482 H A R O L D FOX

Behind and extending from the top of the processus ascendens to the hind end of the auditory capsule, a tectum synoticum roofs the mid-hind-brain (Figs 7 and 13); anterior and posterior fontanelles are thus recognized. The medio-posterior region of the tectum synoticum juts backwards as a finger-like projection, almost to the level of the upper region of the occipital arch. The latter is well-developed but does not join its partner, and the upper part has not yet reached the hind surface of the auditory capsule over the hind- brain. Nor is there a dorsal neural (occipital) spine. Below and alongside the notochord the occipital arch is continuous in front with the cartilaginous “condyle”, at the occipito- vertebral junction. Occipito-spinal arch 2 and neural arches 1 and 2 each meet their respective partners of the other side over the spinal cord, below a median neural spine. Cartilaginous ribs are associated with these three arches, the first one being a cranial rib (Goodrich, 1909) (Fig. 7). Underneath the large auditory capsule an otoquadrate or post- palatine cartilage leads almost transversely and separates the rami hyomandibularis and palatinus facialis. The basal process is firmly fused to the basal plate and no joint is visible (Fig. 13). The intermandibular cartilage is now a centre of ossifications (Fig. 19), and in both upper and lower jaws in front there are practically separate teeth germs with dentine; further back, however, teeth are already fused as incipient grinding plates. The adult possesses a pair of vomerine teeth (Plate II(d), (k)), and a pair (on each side) of maxillo- mandibular dental plates (Gunther, 1871); the Vomerzahnplatte, Oberkieferzahnplatte (Pterygopalatinalzahnplatte) and Unterkieferzahnplatte respectively of Semon (19014, formed in the embryo by fusion of originally separate conical teeth.

In the 34.5 mm specimen the hypophysial fenestra is still larger than in the previous stage (Figs 8 and 14), but it is reduced in the adult, and recognized at the base of the sella turcica. Absence of a basicranial fenestra in all stages confirms the results of de Beer (1926). The anterior naris is situated behind and below the trabecular horn : in contrast in Amphibia it is situated in front of and above the latter.

Fenestrated nasal capsules are generally the same as in the previous stage only larger (Plate II(b), (d), (k)), but the upper labial (or subnasal) cartilages (Huxley, 1876)-superior labials of Jaquet (1899)-of each side, are situated mesial to and in between the anterior and posterior nares; extending to the latter (Figs 7, 8, 13 and 14; Plate II(d)). The lamina orbitonasalis and labia! cartilages probably correspond to the paired post-nasal cartilages and subnasal cartilages of Lepidosiren and Protopterus, respectively; the latter in Neocerutodus having become secondarily detached from the nasal capsule (Jarvik, 1942, p. 273).

A large tectum synoticum and a small epiphysial cartilage are developed (Fig. 14). Ultimately the entire roof is cartilaginous (Kesteven, 1931b, Figs. 1 and 2, 1944; de Beer, 1937). The occipital arches have extended forwards to join thepostero-mesial surfaces of the auditory capsules (Fig. 8). The upper fused regions of the occipital and occipito-spinal 2 arches together form the tectum posterius. As in the other stages the roots of the vagus ganglion enter the chondrocranium through a vagus foramen, behind the auditory capsule (Krawetz, 1911), bounded by the hind end of the latter and the occipital arch, when it is developed (Sewertzoff, 1902) (Figs 30 and 31). As in earlier stages a foramen jugulare or glossopharyngeal foramen is separate from and situated in front of the vagus foramen, in the latero-ventral wall of the auditory capsule (van Wijhe, 1882; Krawetz, 191 1 ; Holmgren & Stensio, 1936) (Plate II(f), (8)).

Meckel’s cartilages meet in front in a median symphysis, and the intermandibular cartilage


now comprises a matrix of spongy bone from which teeth emerge and lead to the lower surface of the mouth (Fig. 20). A similar but larger hyoid than jn the 27 mm stage now

A" I .

not.

----------I

1 mm

FIG. 9. 13-5 mm stage of Neoceratodus. Ventral reconstruction of the neurocranium.

C I

t.0. - -mat.

1 mm

FIG. 10. 14 mm stage of Neoceratodus. Reconstruction as in Fig. 9 showing further development of the neurocranium.

includes a separate stylohyale, but the epihyale-laterohyale components are still not separate (Fox, 19636) (Figs 8 and 31). In the 27 mm stage the outer end of the otoquadrate


cartilage in front joins the inner surface of the quadrate cartilage, and it ends behind as a small protuberance (Edgeworth, 1926a). In the 34.5 mm stage the front of the otoquadrate fuses with the hind surface of the basal process, and behind it fuses with the ventral surface of the auditory capsule (Plate II(h), (i)). The precardial plate is slightly larger in the 34.5 mm stage than in the preceding stage.

c.t.

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- b.p.

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1 mrn

FIG. 11. 15 mm stage of Neoceratodus. Reconstruction as in Fig. 9 showing further development of the neurocranium.

Ossifications Descriptions of the ossifications of the adult Neoceratodus have been given by Krefft

(1870), Gunther (1871), Huxley (1876), Jaquet (1899), K. Furbringer (1904), Goodrich (1925), Kisselewa (1929), Kesteven (1931b, 1944), de Beer (1937), Holmgren & Stensio (1936, Figs 287-289, pp. 374-376) and Holmgren (1949a).

Ossifications are all of membrane bone except where specifically stated. Merely a general account of these elements in a 34.5 mm specimen is given, for some of them are not clearly distinguishable and demarcated in such young stages. In front of the skull below the nasal septum small paired prevomers support vomerine teeth. Behind, the palato- pterygoids extend on either side laterally to the front of the large elongate flat parasphenoid (Lehman, 1955)-which protects almost the whole of the floor of the skull, and extends from the front of the optic foramen to the region in between the occipital arch and occipito- spinal arch 2 (4.26 mm), forking into two about 320 p from its posterior end-to terminate mesial to the basal process, where it joins the parachordal. Over the nasal capsules there is an anterior medial and unpaired nasale (or postrostral), and behind a median unpaired fronto-parietal and on each side supraorbitals (fronto-parietal mediale and laterale, Holmgren & Stensio, 1936), which cover the mid-brain and eyes. Further behind are postorbital and squamosal elements (intertemporal of de Beer, 1937), whose boundaries

FIG

. 12.

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E M B R Y O L O G Y OF N E O C E R A T O D U S 489

are not clear. The opercular fold includes an opercular and interopercular (Gaupp, 1904), which are not seen in the 27 mm stage. No ossifications are found in the sclerotic ring. The ceratohyale is enclosed by a thin cylinder of cartilage bone, which is incipient in the 27 mm specimen. Below the symphysis of Meckel‘s cartilage a splenial gives origin to the ventral teeth plates. Lateral to the lower jaw a small dentary extends for about 0-8 mm, and behind is a supra-angular 320 p long. A large coronoid is situated mesial to Meckel’s cartilage from the front of the jaw to its hind end. No exoccipitals-the only cartilage bones in the brain case (de Beer, 1937)-were recognizable.

The main differences between the skulls of the living adult Neoceratodus and a fossil dipnoan like Chirodipterus are : the different degrees of ossification in the endocranium, strongly ossified in the latter but practically entirely cartilaginous in the former, and the reduced number of dermal bones of Neoceratodus and fusion of the remaining ones into plates (Save-Soderbergh, 1952).

Musculature Alternative nomenclature of previous workers is given by Edgeworth (1925, 1935),

whose terminology is generally used in this present work. The arrangement in the 34.5 mm specimen is described; that in the 27 mm stage is similar but with smaller components (Figs I , 2 and 4 to 8, 15 to 20).

The large masseter comprises a mesial levator mandibulae anterior and a lateral levator mandibulae posterior-the temporalis and masseter, respectively (Greil, 19 13), or portio temporalis and portio lateralis of the adductors (Luther, 1913)-which insert above on the upper surface of the chondrocranium and the internal surface of the fronto-parietal mediale and laterale, and below, on the dorso-mesial (levator posterior) or dorso-lateral (levator anterior) surface of Meckel’s cartilage. Though separated by connective tissue in the adult, the two components are more easily distinguishable as separate structures in younger stages (Figs 1,2,4,5,6 and 8). In Protopterus and Lepidosiren a levator mandibulae externus is developed from the levator mandibulae posterior, and is represented in the former by the retractor anguli oris, and in the latter by the retractor anguli oris superficialis and profundus (Edgeworth, 1935). Both levator mandibulae muscles of Neoceratodus are considered to derive from mesenchyme of the mandibular segment (Edgeworth, 191 1, 1935), but the levator anterior and posterior muscles may be of the premandibular and mandibular segments, respectively (Fox, 1963b). The levator hyoideus, inserted on the auditory capsule below the crista parotica (Plate II(i)), mesial to the epihyale and post- lateral to the hyomandibular nerve, is a flattish strand which leads postero-ventrally to the top of the ceratohyale (Figs 7 and 8). A broad sheet-like constrictor hyoideus in the opercular fold inserts likewise on the auditory capsule, just behind and lateral to the levator hyoideus, and meets its opposite partner in the mid-ventral line. The anterior portion, though indistinguishable from the rest, is attached on each side to the ventro-anterior region of the ceratohyale and designated the interhyoideus (Edgeworth, 1935). In the median line the pair meet as an inscriptio, below the rectus cervicis and geniocoracoideus, above the intermandibularis posterior (Fig. 20). A retractor mandibulae-not described by Edgeworth (1926b, 1935)-which depresses the lower jaw inserts in front on the postero- ventral surface of Meckel’s cartilage and behind on the lateral surface of the ceratohyale (Figs 7, 8, 19 and 20).

The intermandibularis posterior musculature inserts below Meckel’s cartilage on each


side and meets in an inscriptio below the geniocoracoideus, at the front of the interhyoideus (Figs 19 and 20).

The rectus cervicis is attached to the lower surfaces of the hypohyale and ceratohyale, and in older stages probably the basihyale also : the hind end inserts partly on the precardial plate and thence merges with the trunk muscles. It is situated below the ceratohyoideus internus and the hyoid, above the geniocoracoideus, intermandibularis and interhyoideus muscles, mesial to the ceratohyale. In front the apparently single massive rectus cervicis includes a median vertical myocomma delimiting its two halves, which separate above the precardial plate (Figs 19 and 20). The median elongated geniocoracoideus inserts in front on the parasphenoid and perhaps on the intermandibular cartilage. It lies above the inscriptios of the intermandibularis and interhyoideus muscles, below and ending between the paired components of the rectus cervicis, just before their separation. The ceratohyoideus internus is inserted on the upper surface of the hypohyale, and is directed laterally to the rectus cervicis and mesially to the ceratohyale, to end on the lower surface of ceratobranchiale I (Fig. 20).

The levatores arcuum branchialum 1-6 insert above on the ventro-lateral surface of the auditory capsule below the crista parotica (levators 1,2), or at its hind end (levators 3-6). The first four lead almost vertically downwards, each to insert on the tops of ceratobranchiale 1-4, respectively, laterally to the epibranchiale. Levators 5 and 6, which behind merge ventrally with the coracobranchialis and hinder transversus musculature, may include a portion homologous with the dilator laryngeus and the beginning of the cucullaris muscle (Figs 7 and 8), for in urodeles the latter develops from the most caudal levator (Edgeworth, 1935).

A trapezius leads Laterally to the hinder levators, below the body surface, to the scapula. The first two of the narrow elongated constrictor branchialis muscles 1-4 are attached above to the auditory capsule and the others behind it. Constrictor branchialis muscles 1-4 are situated in the external gill filaments 1 4 , outside branchiale 1-4, respectively, and they end below closely associated with the coracobranchialis musculature.

Strap-like longitudinally arranged subarcuales recti 1-5 connect the ventral surfaces of the hyoid and branchiale (Figs 19 and 20). Subarcualis rectus 1 joins the ceratohyale to ceratobranchiale 1 , over the rectus cervicis and hind end of the ceratohyoideus internus. Subarcualis rectus 2 joins ceratobranchiale 1 and 2, extending from the hind end of the ceratohyoideus internus over the front of the coracobranchialis musculature. Subarcualis 3 extends from ceratobranchiale 2 to 3, inserting in front above the outer end of transversus ventralis 2 and coracobranchialis 3. Subarcualis rectus 4 joins ceratobranchiale 3 and 4, its front situated over transversus ventralis 3, and a tiny strip of subarcualis rectus 5 joins ceratobranchiale 4 and 5 .

The outer ends of the transversus ventralis 2-5 muscles are attached to the corresponding branchiale at their ventral surfaces, and their inner ends to corresponding raphes, joining their fellows of the opposite side. The inner portions of transversus ventralis 4 and 5 have extended forwards above the others to attach to the underlying rectus cervicis.

Transversus ventralis 2 extends transversely over the rectus cervicis and coracobranchialis muscles to branchiale 2. Transversus 3 meets its partner medially over transversus 2, and is directed outwards and slightly posteriorly to its attachment on ceratobranchiale 3. A thin independent transversus 4-only recognized in this 34.5 mm specimen --inserts on ceratobranchiale 4, and a massive transversus 5 inserts on ceratobranchiale 5,

E M B R Y O L O G Y O F N E O C E R A T O D U S 49 1

br.S

I It.

t I 1 .II

FIG. 15. 13.5 mm stage of Neoceratodus. Ventral reconstruction of the splanchnocranium and some of its associated ventral musculature.

,<..

I I

1 .I

FIG. 16. 14 mm stage of Neoceratodus. Reconstruction as in Fig. 15 showing further development of similar structures.

0 rbr 2

1 m m

FIG. 17. 15 mni stage of Neocerafodus. Reconstruction as in Fig. 15 showing further development of similar structures, especially of the ceratohyoideus internus muscles.

1m.C

C t h y .

cbr 2

t I

l m m

FIG. 18. 16 mm specimen of Neocerafodus. Reconstruction as in Fig. 15. Further development of the visceral cartilages and of some of the associated ventral musculature.

PLATE I.

s' 3

E d

PLATE I. Photomicrographs of Neocerutodus. All sections transverse, except for (c) and (d) which are horizontal

(a) 11-5 mm specimen 1 .1 mm from anterior end. Quadrate and Meckel's procartilage. (b) Specimen of Plate I(a), 1.9 mm from anterior end. Origin of the larynx. (c) 13.5 mni specimen 1.7 mm from ventral surface. External gills, hyobranchial skeleton and operculum. (d) Specimen of Plate I(c), 2.1 mm from ventral surface. Innervation of the levator mandibulae anterior by

(e) 13.5 mm specimen 0 3 mm from anterior end. Nasal sac and the sole internal narial opening. (f) Specimen of Plate I(e), 1.2 mm from anterior end. Processus basalis of quadrate cartilage, levator muscle and

(g) 16 mni specimen 0.5 mm from anterior end. Praeoptic ganglion against the nasal sac.

and 10 p thick.

the r. ophthalmicus profundus V.

trigeminal ganglion.

PLATE 11. Photomicrographs of Neocerutodus. All sections transverse and 10 p thick.

(a) Specimen of Plate I(g), 2.25 mm from anterior end. Otoquadrate cartilage below the auditory capsule. (b) 27 nini specimen 0.6 mm from anterior end. Median nasal septum alongside the anterior naris. (c) Specimen of Plate II(b), 3-7 mm from anterior end. Auditory capsule with no medial wall. (d) 34.5 mni specimen 1.1 mm from anterior end. Region of nasal capsule showing subnasal (labial) cartilage

situated mesial to the internal naris, and the relationship of the profundus and superior ophthalmicus facialis nerves.

(e) Specimen of Plate I(g), 2.2 mm from anterior end. Relationship of the hyomandibular nerve to the epihyale and the front of the auditory capsule.

(f) Specimen of Plate II(b), 4.2 mm from anterior end. Foiamen jugulare and nerve IX. (9) Specimen of Plate II(b), 4.4 mm from anterior end. Origin of vagus ganglion behind the auditory capsule. (h) Specimen of Plate II(d), 3.8 mm from anterior end. Emergence of the hyomandibular nerve over the

otoquadrate cartilage and head vein, and below the auditory capsule and stapedial artery, mesial to the epihyale. (i) Specimen of Plate II(d), 3.9 mm from anterior end. Origin of hyoidean and stapedial arteries over the

otoquadrdte cartilage. Levator hyoideus situated mesial to the epi-laterohyale. (j) Specimen of Plate II(d), 3.2 mm from anterior end. Strap of nerve tissue between levatores mandibulae

anterior and posterior, incorporating rami superior ophthalmicus and buccalis facialis, and rami maxillaris and mandibularis V. The neuromasts are recognized in grooves.

(k) Specimen of Plate II(d), 0.8 mm from anterior end. Relationship of the rami nasalis internus profundus V and superior ophthalmicus facialis, within the nasal capsule.

PLATE 111. Photomicrographs of transverse sections 10 p thick. (a) Hjnobius rrebulosus 32 mm long, 0 3 mm from anterior end. Region through broad internasal septum. (b) Specimen of Plate III(a), 0.4 mm from anterior end. Slightly in front of the internasal septum; the nasal

(c) Spccimen of Plate III(a), 0.8 mm from anterior end. Further behind the internasal septum the nasal

(d) Sulumundru muculosu 25 mm long, 0.5 mm from anterior end. Separate nasal capsules; the external naris is

(e) Suluniundru muculosu 24 mm long, 0.7 mm from anterior end. Region of nasal capsule with the r. nasalis

(f) Hynobius returdatus 27 mm long, 2.5 mm from anterior end. Medial wall and foramina of auditory capsule. (g) Specimen of Plate III(f), 2.8 mm from anterior end. Otoquadrate cartilage is incorporated into the floor

of the auditory capsule, forming the base of the facial canal, and separating the rami hyomandibularis and palatinus facialis.

(h) Specimen of Plate III(a), 1.6 mm from anterior end. Processus pterygoideus extended forwards below the orbit.

capsules have independent medial walls.

capsules are separate. Region of the foramen olfactorius evehens and olfactory nerve.

shown on one side.

internus profundus inside and the r. superior ophthalmicus facialis outside and above the capsule.

PLATE IV. Photomicrographs of transverse sections 10 fi thick.

(a) Cryptobrurtchu~ u//eg/iurrietisi~ 37 nini long, 1.8 mm from anterior end. Junction of the processus pterygoideus

(b) Specimen of Plate III(e), 3.2 rnrn from anterior end, showing the coluniella auris in the foramen ovale. (c) Rana teinporuriu 40 mni long, 1.2 rnrn from anterior end. Median internasal septum in the region of the nasal

(d) Rana esculerita 26 niin long. 0.97 nin i from the anterior end. Region of the rostra1 cartilages. (e) Specimen of Plate IV Fig.id), 1.04 nini from anterior end. Rostra1 region, slightly behind that of previous

(f) Rmia teniporuriu 33 nini long, 1.9 rnrn from anterior end. Region of processus muscularis quadratus,comiissura

with the trabecula cranii.

capsules.

figure.

quadratoaanialis anterior and the front of the enclosed masseter musculature.


to continue backwards as a constituent of the sphincter oesophagi (Edgeworth, 19266, 1935), which extends to the front of the larynx. A constrictor oesophagi surrounds the hinder laryngeal region. The coracobranchialis musculature is elongated and flattened, and develops from the outer ends of the transversus ventralis muscles. The front is situated beneath subarcualis rectus 2, latero-dorsal to the rectus cervicis, but no insertions on ceratobranchiale 1 and 2 were recognized. Coracobranchiales 3, 4 and 5 insert on ceratobranchiale 3-5, respectively (Fig. 19) just behind the outer ends of the transversus muscles

FIG. 19.27 mm stage of Neocerufodus. Reconstruction as in Fig. 15. Further development of similar components of previous stages.

3-5, and end behind on the pectoral girdle. Their topography is similar to that described by Edgeworth (1935), who recognized 4 coracobranchiales attached to ceratobranchiale 2-5, respectively, and ending likewise on the pectoral girdle.

In an 11 -5 mm stage incipient levatores mandibulae anterior and posterior are practically separate, though joined ventrally (Fox, 19636), to insert on the procartilaginous upper margin of Meckel’s cartilage. Dorsally they are situated laterally to the fore-brain and the trigeminal ganglion ; the levator posterior inserting against the presumptive quadrate cartilage (Figs 1 to 3). Incipient levator, constrictor and interhyoidei and intermandibularis

33

5

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muscles are recognized. Mandibular and hyoid muscles were first described at about Semon stages 40-42; 9.8-10.3 mm (Edgeworth, 191 1). Primordia of the ceratohyoideus internus, which leads over the front of the rectus cervicis to below presumptive branchiale 1, transversus ventralis 2, levatores arcuum branchialium 1-3 and the rectus cervicis are present.

In the 13.5 mm stage levatores mandibulae anterior and posterior are inserted above on the crista trabeculae and the otic process, respectively (Plate t(d),(f)). Other recognizable muscles include a geniocoracoideus, transversus ventralis 3 and 5, levatores arcuum branchialium 4 and 5, and blastemata of the retractor mandibulae and the eye muscles (Figs 5,6, 16 and 17).

In the 16 mm stage the geniocoracoideus is divided into two posterior “tails”, each one situated mesially and mesio-ventrally to the rectus cervicis and inserted on the precardial plate. The ceratohyoideus internus has now inserted on the upper surface of the hypohyale (Fig. 18). Incipient coracobranchiales are recognized, and there is further development of the hinder levator branchialis musculature. An incipient trapezius has developed slightly earlier than in a Semon stage 48; 17.8 mm specimen of Edgeworth (1911). Constrictor branchiales and subarcuales recti are first recognized in the 27 mm specimen.

Arterial system

For information on the circulatory system of the adult Neoceratodus reference may be made to the works of Boas (1880), Spencer (1893) and Goodrich (1911, 1930), among others; and for unhatched embryos and larvae Kellicott (1905), Greil (1908-13), Allis (1930) and Bertmar (1962b). There is a fairly strong similarity, in the region of the head and pharynx, between larva and adult (compare Figs 21,22,24 and 41, and the descriptions of Spencer, 1893, Plate 1, Fig. 2).

The following description is that for the 27 mm and 34.5 mm specimens. All arteries are paired except where stated.

The ventral conus arteriosis of the heart gives rise on each side to afferent epibranchial arteries 1-4 (often called 3-6); the first situated slightly further anterior of the others, for there is a short ventral lateral aorta. In the adult the conus is short and twisted, and the four afferent arteries originate at a similar level (Boas, 1880; Spencer, 1893). Each one leads outwards below ceratobranchiale 1-4 respectively into the external gill filaments, behind gill clefts 1-4, and subdivides into capillaries underneath the skin. All are situated in the floor of the pharynx, over the rectus cervicis and transversus ventralis musculature.

In association with the afferent vessels are the efferent epibranchial arteries 1-4 (likewise called 3-6 or “die vier Kiemenvenen” of Boas, 1880), which open into the lateral dorsal aorta (Figs 22 and 24).

Efferent epibranchial artery 1 is divided into two (like the others) on each side of ceratobranchiale 1 and afferent artery 1, and the anterior (lateral) and posterior (mesial) divisions ultimately are joined below the front of the latter cartilage. In the 34.5 mm specimen it is further divided into what are probably the lingual vessels of Spencer (1893). A lower vessel is distributed to the ventral surface, which comprises an anterior subdivision below the ceratohyale and hypohyale, mesial to Meckel’s cartilage and over the front of the intermandibularis muscle, and a posterior subdivision, distributed laterally to the ceratohyale and mesially to the retractor mandibulae to end amid the latter. An upper anterior

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vessel is distributed to the region mesio-dorsal to the ceratohyale, laterally and thence beneath the ceratohyoideus internus, over and in front of the rectus cervicis to end mesial to the ceratohyale and thyroid vesicles (Fig. 24). The divisions of efferent epibranchial artery 2 join below ceratobranchiale 2. The hypobranchial artery so-formed (Spencer, 1893) continues ventro-anteriorly for a short distance and thence turns sharply backwards, over transversus ventralis 2 and the rectus cervicis, mesial to the ventral lateral aorta, and below transversus ventralis 4 and 5. It is divided into lower and upper vessels to the heart and mesial surface of the rectus cervicis muscle, respectively (Fig. 24).

The divided efferent epibranchial artery 3, situated lateral and mesio-ventral to ceratobranchiale 3, is joined below to end over the coracobranchialis musculature. Above the epibranchiale 3 and ceratobranchiale 3 efferent artery 3 comprises a complex capillary sinus, which leads into the lateral dorsal aorta via a separate vessel at the level of the occipital artery.

Efferent epibranchial artery 4 is similar in arrangement to the preceding artery, but the paired divisions situated on either side of ceratobranchiale 4 end below the latter. It joins the lateral dorsal aorta just before the latter meets its partner of the other side.

Arising from the lateral dorsal aorta in the 27 mm specimen, but from the top of efferent artery 3 in the 34.5 mm specimen, an occipital artery leads upwards mesially to the occipital somites. It divides into an upper division distributed to hypoglossal nerve 3 and a lower one, situated mesially to the somite of the fifth metotic segment, to end in the region lateral to the base of the occipital arch (Figs 22 and 24).

A pulmonary artery originates from the hind surface of efferent artery 4, which in the 27 mm stage (Fig. 22) was traced below the hind end of the vagus ganglion, mesially to the sphincter oesophagi and ventro-lateral to the oesophagus. The artery of one side is distributed to the air sac, which is seen in transverse section to the left and ultimately above the gut. On the other side the pulmonary disappeared amidst the oesophageal musculature.

A hyoid artery from the lateral dorsal aorta forks into an upper stapedial artery- probably the anterior carotid of Spencer (1893), or temporalis (Greil, 1913)-and a lower hyoidean (Plate II(h), (i)), though the latter is vestigial in the 27 mm stage (Figs 21,22, and 24). The hyoidean artery leads posteriorly for a short distance over the otoquadrate cartilage, below the auditory capsule, laterally to the levator hyoideus and mesially to the laterohyale. The stapedial artery is situated over the otoquadrate and the facial nerve, mesial to the otic process, and emerges through the foramen sphenoticus below the trigeminal ganglion, to divide and supply the regions of the masseter and facial nerves (mandibular division), the eye (supraorbital division), and mesial to the posterior nares (nasal division) (Fig. 24; see Fox, 1963~).

Just before the lateral dorsal aorta (Plate II(h), (i)) enters the chondrocranium via the foramen hypophyseos as the internal carotid artery (Allis, 1929a, 1930) or posterior carotid (Spencer, 1893) it receives a mandibular artery, which when followed backwards is situated below the head vein, mesio-posterior to the quadrate cartilage, mesial to the stylohyale and the stylo-epihyale junction (27 mm specimen) and over the basal process (34.5 mm specimen). It ends over the top of the ceratohyale, mesial to the levator hyoideus.

In the 34-5 mm stage a small palatine artery originates from the lateral dorsal aorta, just behind the mandibular artery (Allis, 1930), and is directed forwards, below the post- palatine and mesially to the quadrate cartilages, and ventro-laterally to the hind end of the basal process, to supply the roof of the pharynx (Fig. 24).


Leading from the internal carotid artery at the level of the hypophysis is an ophthalmica magna artery, or orbital artery (Spencer, 1893), possibly the persistent relic of a premandibular efferent epibranchial artery (Allis, 1914b; Fox, 1963~). It emerges from the chondrocranium through the foramen ophthalmica magna (foramen sphenotrabeculare), mesial to the ramus ophthalmicus profundus V and masseter musculature, dorsal to the large orbital venous sinuses, close against the pila metoptica, amid the rectus muscles, and below the oculomotor nerves. It thence curves backwards over the optic and ventral oculomotor nerves and the inferior obliquus, to supply the posterior mesial surface of the eye (Figs 21, 22 and 24). Further forwards the internal carotid artery gives off a large dorsal carotis cerebralis artery, against the mid-brain, and its divisions among others include a carotis cerebralis anterior and a large carotis cerebralis posterior artery. The latter situated at the side and floor of the mid-brain joins its opposite partner as the artery basalis, which thence divides at the side or above the notochord, close to the hind-brain and spinal cord, to end below them as a capillary network.

In front, the internal carotid artery, situated over the origin of the optic nerve about half-way between the foramina optica and sphenotrabeculare, gives origin to the optic artery (arteria centralis retinae)-probably the equivalent of the anterior end, or part of it, of the internal carotid or lateral dorsal aorta (Fox, 1963~)-which leaves the chondrocranium through the optic foramen. The optic artery is distributed to the antero-mesial surface of the eye, inside the sclerotic cartilage. The remainder of the internal carotid artery ends as a delicate network of capillaries against the side of the fore-brain, behind the olfactory region (Fig. 24).

The front of the ventral lateral aorta-absent in the adult Neoceratodus (Spencer, 1893)- curves backwards over the ceratohyoideus internus and below the front of ceratobranchiale 1. It is thence recognized mesial to efferent epibranchial artery 1 below the front of the post-trematic division of glossopharyngeal nerve IX, lateral to the mandibular vein, rectus cervicis and ceratohyoideus internus, and ventro-lateral to the interhyoideus muscle within which it ends.

In the 27mm specimen (Fig. 22) at the level of the occipito-spinal arch 2 a coeliac artery from the dorsal aorta is directed to the liver, and about 200 p further behind a subclavian artery, situated over the rectus cervicis beneath the rib of occipito-spinal arch 2 and just behind the pronephros, leads to the fore-fin (Boas, 1880, Plate 15, Fig. 19).

Efferent epibranchial arteries 1-4 (though the last one is not clearly defined) are recognized in a 13.5 mm specimen, each one being a complex network of capillaries in its respective branchial arch. Small afferent epibranchial arteries originating from the ventral lateral aorta are also present.

In the 14 mm stage each efferent artery has divided into two, and as in the 13.5 mm specimen the mandibular, hyoid (forking into stapedial and hyoidean), internal carotid, ophthalmica magna, carotis cerebralis (network of capillaries which have sent a carotis cerebralis posterior to meet its fellow of the opposite side as the basilar artery), are recognized. Paired efferent arteries 1 and 2 of the 14 mm stage have joined below the front of ceratobranchiale 1 and 2, but the others still terminate in capillaries in the 15 mm stage. The ventral aorta has already turned backwards, to lead over the interhyoideus muscle.

By the 16 mm stage (Fig. 21) the arterial arrangement is similar, though the components are simpler and smaller, to that in the older stages. An optic artery has emerged through the optic foramen and an incipient hypobranchial artery of efferent epibranchial artery 2

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has curved back below transversus ventralis 2, over and thence mesially to the rectus cervicis toward the heart. A small pulmonary artery is present though it was not indicated in a specimen nine weeks post-hatching (Semon stage about 48, 17.8 mm long, Kellicott, 1905).

Venous system

In the 27 mm specimen (Figs 22 and 23) the head vein (vena capitis lateralis or anterior cardinal vein) from the ductus Cuvieri is directed anteriorly, lateral to the somites, over the vagus ganglion-between it and the ramus superior lateralis X-thence between the vagus and the outer somitic musculature and over epibranchiale 3 and 4 and the efferent epibranchial arteries. Lateral to the vagus ganglion it receives a post-cerebral vein, which is situated dorso-anteriorly and mesially to the auditory capsule, against the hind- brain. It drains blood by divisions from the upper regions of the levator muscles and dorso-posterior surface of the hind-brain, below the tectum synoticum.

In front the head vein is situated ventro-lateral to the auditory capsule, dorso-lateral to the foramen jugulare, over the glossopharyngeal ganglion, efferent epibranchial arteries, epibranchiale 1 and the lateral dorsal aorta (Fig. 21), and mesial to the levator hyoideus, hyoid and the ramus hyomandibularis facialis. Thence it is recognized over the otoquadrate cartilage, processus basalis, origin of the hyoidean and stapedial arteries but eventually mesial to the latter (Plate 1I(i)), below the facialis ganglion, mesial to the processus oticus, quadrate cartilage, trigeminal ganglion, processus ascendens and masseter musculature, and below the profundus nerve. The detailed description of its morphological relationships confirms that of de Beer (1926) and would seem to compare favourably with that given for a similar stage by Bertmar (1965a). In the orbit the head vein receives a pituitary vein, which has emerged from inside the chondrocranium, together with the ophthalmica magna artery, through the foramen sphenotrabeculare (Fig. 23). Thenceforth it receives : (a) a large upper orbital vein, directed masially to the truncus infraorbitalis, between the levatores mandibulae anterior and posterior and the head vein; (b) two smaller veins from the orbit; (c) a large ventro-posterior vein from the region lateral to Meckel’s cartilage and the base of the masseter musculature (probably the vena mandibularis of Bertmar (19651)). This vein drains blood by vessels above and below the ramus mentalis externus facialis, and from the proximal roots of the rami mentalis internus facialis and jugularis facialis, below the stylohyale ; ending lateral to the ceratohyale and interhyoideus musculature underneath the skin. The front of the orbital sinus now receives: (d) a large vein and several others from the dorso-mesial surface of the eye and the region mesial to the nasal sac, respectively, and it is ultimately situated lateral to the nasal capsule where this; (e) external nasal vein drains blood from the front of the snout, by vessels within the capsule (Fig. 23). The veins of the orbit are probably variable in arrangement in different specimens.

A large mandibular vein from the ductus Cuvieri leads forwards over hypoglossal nerves 2 and 3 and the rectus cervicis, mesial to the antero-lateral division of the truncus intestinalis X, below the ceratobranchiale, transversus ventralis musculature and afferent epibranchial arteries and thence lateral to the rectus cervicis. In front it is recognized mesially to the backwardly turned lateral ventral aorta, below efferent epibranchial artery 1, and it terminates mesially and thence below the ceratohyale, over the front of the interhyoideus (Figs 21 and 23).


The ductus Cuvieri receives : (a) a post-cardinal vein, associated with the pronephros and its duct; (b) a post-lateral vein which leads upwards through the pronephros laterally to the somitic and mesially to the pectoral musculature, at the level of the ramus superior lateralis X.

The sinus venosus receives: (c) a large postcaval vein, which penetrates the liver; (d) several pulmonary veins, including a pair of vessels on each side, which drain blood from the musculature of the oesophagus and the lower surface (right) and upper surface (left) of the air sac (Fig. 23).

The arrangement of the head vein in younger stages is generally similar but simpler and less clear. In a 13.5 mm stage however the left one is situated mesial to the vagus ganglion, not lateral to it as on the other side, underneath the hind end of the auditory capsule and over the top of the vagus. Further forwards it lies lateral to ganglion IX and ventro-lateral to the auditory capsule, like its opposite partner. The orbital sinuses likewise in general drain blood from regions of the orbit, mesially and below the nasal sac.

Post-cerebral, post-cardinal, mandibular and post-caval veins are already developed in this stage.

Cranial and anterior spinal nervous system

Most of the earlier descriptions in adult Neoceratodus by Beauregard (1881), van Wijhe (1 882), Sanders (1 SS9), Sewertzoff (1902), Bing & Burckhardt (1905) and Kesteven (1944) are incomplete, though important data on the occipital nerves have been provided by M. Furbringer (1897), K. Furbringer (1904) and Krawetz (191 1). Jarvik (1942) described the innervation of the snout of the larva based on investigations by Greil (1913), as did Thomson (1963), who also considered Protopterus and Lepidosiren. Various cranial nerves and their courses through related foramina were adumbrated in larvae by Krawetz (191 I), de Beer (1926) and Holmgren & Stensio (1936). Luther (1913) described the relationship of divisions of the trigeminal and facial nerves to the adductor muscles, Edgeworth (1935) contributed information on innervation of various muscles of the head, and Bertmar (1963) described the relationship of orbito-temporal nerves to cartilage structures in the vicinity. Specimens 27 mm and 34.5 mm long are here described, and where necessary younger stages also (Figs 25 to 31).

Olfactory nerve 1 emerges from the olfactory lobe through the foramen olfactorius evehens. It comprises a dorsal (posterior) root, which divides and is distributed below the profundus nerves to the dorsal and dorso-mesial surfaces of the nasal sac (Plate II(d)), and a ventral (anterior) root-nerve praeopticus or “new nerve of Dipnoi” (Sewertzoff, 1902), or nervus terminalis (Rudebeck, 1945)-which originates just in front of the anterior naris and is similarly distributed. A delicate dorsal root is always recognizable, though it is ill-defined in the 1 1 -5 mm stage, and a thicker ventral root also, which up to and including the 16 mm stage leads for a short distance into an olfactory ganglion, or praeoptic ganglion (Sewertzoff, 1902, Figs 4 and 5) ; situated mesially to the nasal sac (Plate I(g)). In the 16 mm stage the ventral olfactory root fibres are about 150 p long. The nervus terminalis in the adult Neoceratodus is complex in its internal distribution, and derives from two roots (Holmgren & van der Horst, 1925), an anterior vomero-nasalis and a posterior root which is probably the praeopticus of Sewertzoff. According to Bertmar (19653) the ganglion terminalis is the Ratselhafte or Rudimentarorgane of Broman (1939).

504 H A R O L D FOX

Optic nerve I1 from the ventral surface of the forebrain leads antero-dorsally through the foramen optica, and thence curves backwards again, ventrally to the r. ophthalmicus profundus V and between the oculomotor nerve divisions and the rectus muscles, to lead to the eye (Figs 30 and 31). A similar but less curved course occurs in younger specimens. The optic nerve primordium is hollow in the 11.5 mm specimen; its solid lens is cellular at its periphery and the eye is little differentiated.

A delicate oculomotor nerve 111 from the ventro-anterior surface of the mid-brain leads forwards within the chondrocranium for 200 p and 320 p in the 16 mm and 34.5 mm specimens respectively (Figs 25 and 31). It is divided above and below the r. ophthalmicus

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profundus V-with which it is closely associated-and is distributed to the usual rectus muscles and the inferior obliquus. In the 1 1 -5 mm stage the oculomotor nerve leads ventro- posteriorly, and just behind the premandibular vesicle (Edgeworth, 1935) it is distributed to the mesenchyme of the presumptive eye muscles (Fig. 3).

A slender trochlear nerve IV-probably first discovered in the adult by van Wijhe (1 882) and described by Sanders (1889)-is first recognizable in a 16 mm specimen (Fig. 29). It originates from the dorso-lateral surface of the mid-brain, above the origin of the oculomotor nerve (27 mm specimen), at the level of the pituitary (34.5 mm specimen). In the former it leads forwards within the upper region of the chondrocranium for 400 p, and emerges through a tiny foramen trochlearis to be distributed to the superior obliquus.


The abducens nerve VI-first suspected in the adult by van Wijhe (1882), and recognizable only in my 16 mm and 27 mrn specimens-originates from the ventral surface of the medulla; by 3 or 4 roots in the adult (Holmgren & van der Horst, 1925). It leads forwards, from a transverse level shared with the top of epibranchiale 1, over the basal plate, mesially and extremely close to the auditory ganglion and into the facial ganglion. Doubtless it is intimately associated with the roots of the facialis and trigeminal nerves, and presumably it leads into the orbit to innervate the rectus externus. It is extremely weakly developed, though of similar origin and distribution in the adult (Bing & Burckhardt, 1905).

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FIG. 26.14 mmstage of Neocerutodus. Reconstruction as in Fig. 25 of similar components of the head and pharynx. Sclerotic cartilage is omitted.

The trigeminal nerve V In the 27 mm and 34.5 mm specimens separate profundus, trigeminus and facialis

ganglionic components are not distinguishable (Figs 30 and 3 1). (1) The ramus ophthalmicus profundus V of the 27 mm specimen (Fig. 30) leads forwards

from the trigeminal ganglion mesial to the processus ascendens (Schmalhausen, 1923b; de Beer, 1926), between the upper and lower divisions of the oculomotor nerve, and over the optic nerve amidst the rectus muscles. A delicate branch is given off to the mesial surface of the eye, as in some younger specimens. About 400 in front of the processus ascendens a dorsal division is distributed laterally to the masseter musculature, to the upper surface of the head. At the level of the lamina orbito-nasalis the profundus has divided into : (a) an upper r. nasalis internus profundus V, which first distributes a dorso-anterior

506 H A R O L D FOX

branch against the foramen olfactorius, behind the nasal capsule to the skin of the upper surface. The main internal nasalis V nerve situated dorso-mesially to the nasal sac, within the nasal capsule, is divided into two in the 27 mm specimen (undivided in the 34.5 mm specimen). After giving off several dorsal branches through foramina in the roof of the nasal capsule, the main nerve is closely associated with the ramus superior ophthalmicus facialis VLI (Plate II(k)). A composite ramus nasalis internus profundus V-superior ophthalmicus facialis VII emerges through the front of the nasal capsule, to be distributed to the skin and lateral line organs of the snout; (b) a lower r. nasalis externus profundus V divides laterally to the nasal sac, within the nasal capsule, into (c) a deep profundus V

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FIG. 27. 15 ti1111 stage of Neoceratodus. Reconstruction as in Fig. 25 of similar components of the head and pharynx. Sclerotic cartilage omitted.

to join the truncus infraorbitalis. The resultant common nerve joins (d) another division of the r, nasalis externus profundus V, further forwards within the nasal capsule, the whole thence being distributed to the skin and sense organs at the antero-lateral margin of the snout (Fig. 30). No profundus-palatinus facialis division is recognized. Apart from individual variation the arrangement is similar in the 34.5 mm and 16 mm specimens (Figs 29 and 31), though simpler in the latter.

In the 13.5 mm, 14 mm and 15 mm specimens (Figs 25 to 27) the rami nasalis internus profundus V and superior ophthalmicus facialis VII are associated, but entirely separate. In a 13.5 mm specimen the profundus would seem to innervate the levator mandibulae anterior (Plate I(d)) (Fox, 19636).

In the 11.5 mm stage (Fig. 3), the profundus nerve is situated mesial to the eye, over the premandibular vesicle, to end amid the premandibular mesenchyme. Separate profundus

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and gasserian ganglia are not recognizable, though the mandibular nerve, which forks over the levator mandibulae posterior, is derived from the posterior region of the trigeminal ganglion, the whole of which can be distinguished from the facialis.

In the 34.5 mm specimen (Fig. 31), a massive trigemino-facialis ganglion bulges out of the prootic recess laterally to the processus ascendens.

(2) An upper ramus maxillaris V leads from the front of the large r. mandibularis V antero-laterally to the masseter masculature and the processus ascendens, mesial to the posterior surface of the eye, and mesio-dorsal to, separate from, but closely associated with the lower division of the truncus infraorbitalis (r. buccalis facialis VII). Thence the maxillary nerve crosses the floor of the orbit, over the lamina orbitonasalis and the lateral margin of the teeth plates, mesially to the nasal sac and below the lateral edge of the trabecula, to fuse with the ramus palatinus facialis VII. The result confirms the description given by Jarvik (1942, p. 281) based on the work of Greil (1913). The combined nerves finally disappear mesial to the nasal sac.

The origin and arrangement of the maxillary nerve in the 27 mm specimen is less clear (Fig. 30). Proximally at the origin of the maxillary V, mandibular V, buccalis and superior ophthalmicus facialis VII nerves, a number of extremely fine lateralis ? divisions of the buccalis nerve are distributed to the skin and sense organs; like the condition in the 34.5 mm specimen. Maxillary fibres may here be included, but separate maxillaris V and buccalis VII nerves of the truncus infraorbitalis are recognized however, beneath the eye and rectus muscles. The upper division, presumably mainly maxillary nerve, is distributed as in the 34.5 mm specimen.

The ventro-lateral predominantly buccalis facialis VII fibres (presumably including some maxillaris V elements) continues forwards, receives two divisions from the deep profundus V of the r. nasalis externus profundus V, and finally is situated mesial to the outer nasal capsule wall, lateral to the nasal sac, to be distributed to the neuromasts of the snout.

The arrangement of the maxillary V and buccalis VII nerves is simpler in the 16 mm and younger stages, which agrees with the description of Luther (1913), and here no actual junction between maxillary and palatine nerves is yet apparent (Figs 25 to 27 and 29).

(3) The ramus mandibularis V of the 34.5 mm specimen (Fig. 31) originates with the rami maxillaris V, superior ophthalmicus VII and buccalis facialis VII as an elongated strap of nerve tissue, situated between the levatores mandibulae anterior and posterior muscles (Plate Il(j)). On separation of the facialis and maxillaris nerves the remainder, or mandibular nerve, closely associated with a number of buccal branches, proceeds almost vertically downwards outside the masseter. It innervates the outer and inner surfaces, though the masseter also receives other nerves from the hinder region of the trigeminal ganglion. Lateral to Meckel’s cartilage the mandibular nerve divides into : (a) an anterior r. mentalis V; (b) a vertically situated r. intermandibularis V; (c) a r. mandibularis superior V, which originates just below the origin of the r. maxillaris V to lead postero-ventrally to the outer surface of the masseter muscle, mesially to the buccal nerve; (d) r. mandibularis interior V, which originates somewhat above the r. mentalis V and leads postero-laterally to the base of the levator mandibulae posterior, and thence over the top of the hinder upper surface of Meckel’s cartilage, to continue forwards mesial to the base of the masseter and the lower jaw. The r. mentalis V is situated dorso-mesial to the r. mentalis externus facialis and they unite, to proceed mesial to the dentary and lateral to Meckel’s cartilage to the


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median symphysis (Figs 30 and 3 1). Delicate branches emerge through minute foramina in the dentary, to lead to the skin and neuromasts at the side and front of the lower jaw. The r. intermandibularis V is directed laterally to Meckel’s cartilage and divides below into : (e) rami intermandibularis anterior V and (f) intermandibularis posterior V, which are distributed to the intermandibularis musculature, and in the process are intimately associated with terminal endings of the rami mentalis internus facialis and jugularis facialis. No fusion or exchange of fibres were recognized. The arrangement of the mandibular nerve is similar in the 27 mm specimen (Fig. 30), but rami mandibularis superior V and interior V were not clearly distinguished.

In the 16 mm stage (Fig. 29) rami mentalis V and mentalis externus facialis show incipient unification, but in younger specimens (Figs 25 to 27) they are entirely separate.

In the 1 1.5 mm stage the mandibular nerve forks over the levator mandibulae posterior; the inner division is probably the maxillary, and the outer the mandibular branch of the fifth nerve.

The facialis nerve VII In the 34-5 mm specimen (Fig. 31) the (1) ramus hyomandibularis facialis emerges

through the facialis foramen almost transversely from the facialis ganglion, mesio-ventrally to the inner front wall of the auditory capsule and the otic process (de Beer, 1926), over the outer edge of the basal plate and the otoquadrate cartilage (Plate II(h)). The latter forms the front, rear and ventral margins of the facial canal. The hyomandibular nerve is situated behind the spiracular cleft and in front of the epihyale and laterohyale (Edgeworth, 1926~)~ and proximally it divides into: (2) a ramus mandibularis externus facialis, further dividing into: (a) a ramus mentalis externus facialis, which leads forwards to join the r. mentalis V as previously described; (b) a ramus mentalis internus facialis, which leads backwards and thence curves forwards alongside the retractor mandibulae (which probably it innervates), dividing into upper and lower branches situated below the interhyoideus, retractor mandibulae and the hind end of Meckel’s cartilage, and distributed to the neuromasts of the lower surface.

(3) A delicate ramus mentalis interior facialis-which joins the outer r. mentalis internus facialis in the 27 mm specimen (Fig. 30), but is separate from it in the 34.5 mm specimen- penetrates and presumably innervates the retractor mandibulae, below the hind end of Meckel’s cartilage, latero-dorsal to the branches of the r. mentalis internus facialis and to the ceratohyale, and above the intermandibularis muscle.

(4) A ramus alveolaris facialis (r. mandibularis internus facialis) lies mesio-ventral to the hyoid, below the spiracular cleft, and curves forwards lateral to the ceratohyale and mesial to Meckel’s cartilage.

(5) A more lateral ramus jugularis facialis leads posteriorly and thence curves forwards, laterally to the stylohyale and the top of the retractor mandibulae. Anterior and posterior divisions supply the interhyoideus and probably lateralis components of the skin.

(6) A ramus palatinus facialis originates from the ventral surface of the facialis ganglion, in front of the otoquadrate cartilage, which separates it from the r. hyomandibularis facialis. The palatine nerve leads forwards below the basal process (de Beer, 1926), close against the basal plate and the mesial edge of the trabecula and above the parasphenoid, at the outer margin of the foramen hypophyseos. Mesial to the nasal sac and in front of the junction of the lamina orbitonasalis with the trabecula, it receives the maxillary

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E M B R Y O L O G Y O F N E O C E R A T O D US 513

nerve, which together are situated mesio-ventral but ultimately dorsal to, and innervate, the prevomerine teeth (Plate II(d)).

(7) The ramus buccalis facialis originates with the r. superior ophthalmicus facialis from the lateralis constituent of the facialis ganglion, and separates off ventrally from the upper part of the elongated strip of trigeminal and facial nerve components, against the lateral surface of the masseter musculature. Lateral to the r. mandibularis V its complex divisions associate with the r. maxillaris V to form the truncus infraorbitalis. Within the nasal capsule (lateral to the nasal sac) it receives branches of the deep profundus V, and thence is distributed to the skin and neuromasts of the ventral and lateral regions of the snout.

(8) The ramus superior ophthalmicus facialis separates from the top of the strip of nervous tissue previously mentioned, and leads forwards laterally to the top of the levator mandibulae anterior (Luther, 191 3), and over the sclerotic cartilage and rectus muscles, to supply lateral line organs of the front of the head. It enters the nasal capsule through one of the larger foramina '(Plate II(d), (k)), and thereafter is closely associated with the r. nasalis internus profundus V (Figs 29 to 31), an arrangement illustrated in specimens at Semon stage 48, as yet without a nasal capsule (Greil, 1913; Jarvik, 1942). The combined nerves emerge from the capsule through a dorsal mesial and anterior foramen, and the facialis components are distributed to neuromasts at the tip of the snout.

(9) A large Connective VII-IX-X from the trigemino-facialis ganglionic complex is directed latero-posteriorly to the auditory capsule, dorsomesially to the levator mandibulae posterior, to innervate the lateral line organs alongside, or the region between the masseter components and the crista parotica. It joins the vagus ganglion in the 27 mm and 34.5 mm specimens (Figs 30 and 31), mesial and lateral to the hinder end of the auditory capsule. In 16 mm and all younger stages, except for the 1 1 -5 mm specimens where it was not recognized, a similar connective also includes delicate nerves which join ganglion IX, lateral to the auditory capsule at the level of the foramen jugulare. In some cases the main trunk of the Connective would seem to join the lateralis constituent of the vagus ganglion, at about the level of hypoglossal nerve 1.

(10) In the 27 mm specimen (Fig. 30) a pair of posterior nerves (which anastomose), from the top of the r. hyomandibularis facialis, supply the interhyoideus musculature. The lower one is situated postero-lateral to the levator hyoideus and dorso-lateral to the ceratohyale, and the upper division mesial to the epihyale-stylohyale junction, dorso- lateral to the levator hyoideus, and lateral to the auditory capsule. A single fine, elongated, and similarly distributed nerve is recognized in the 34.5 mm specimen (Fig. 31), which probably represents the lower division of the previous specimen.

The glossopharyngeal nerve I X A ramus post-trematicus IX originates from the front of a separate ganglion IX, whose

roots enter the chondrocranium through a separate foramen jugulare (Plate II(f)), which is divided in the 16 mm stage (Fig. 29). It is directed ventro-anteriorly over the first epibranchiale and efferent epibranchial artery, mesially to levator arcus branchialis 1-which it innervates-lateral and ventro-lateral to ceratobranchiale 1, to innervate the ceratohyoideus internus by a separate branch. Below, a division is distributed to the region in between the rectus cervicis and the body surface, behind gill cleft 1 : and the main trunk thence continues alongside, then dorsally or laterally to the ceratohyoideus internus and ceratohyale, and divisions terminate over the hypohyale and basihyale, underneath the

5 14 H A R O L D FOX

skin. A shortish ramus pretrematicus 1X originates mesial to the post-trematic nerve and is situated below the auditory capsule, to end laterally to the epi- and ceratobranchiale 1. A ramus pharyngeus IX-recognized as a ventro-anterior trunk of ganglion IX-is situated lateral to epibranchiale 1 and the lateral dorsal aorta, thence over the roof of the pharynx and efferent epibranchial artery 1, and below the head vein, auditory capsule, otoquadrate cartilage, processus basalis, parasphenoid and basal plate (Figs 30 and 3 1). It is recognized near the foramen hypophyseos, and further forwards mesial to the teeth plates below the trabecular plate. In younger specimen (Figs 25 to 27 and 29), rami pre- and post-trematicus and pharyngeus IX are in general similarly arranged. Ganglion IX and the three rami though incipient are recognizable in the 11.5 mm stage (Fig. 3); r. post-trematicus IX likewise associated with branchial arch 1.

The vagus nerve X The vagus ganglion is in all cases entirely separate from the glossopharyngeal ganglion

(Figs 3,25 to 27 and 29 to 31 ; Plate II(g)). In the 34.5 mm specimen vagus branchial nerve 1 originates from the front and 2 and 3 from the ventro-lateral margin of the vagus ganglion ; each comprise pretrematic, post-trematic and pharyngeus rami, Vagus nerves 4 to 6 are post-trematic only. The post-trematic rami of vagus 1 , 2 and 3 lead laterally to epi- branchial2, 3 and 4 respectively, and lateral, ventro-lateral and ventral to ceratobranchiale 2, 3 and 4; behind their related gill clefts (Figs. 30 and 31).

Vagus ramus post-trematicus 1 leads forwards mesially to levator arcus branchials 2 and over efferent epibranchial artery 2. It innervates the levator arcus branchialis 2 and transversus ventralis 2 and ends over the rectus cervicis, underneath the floor of the mouth. Vagus ramus pretrematicus 1 originates just above the post-trematicus 1 and with its delicate pharyngeal ramus-which supplies the roof of the pharynx-leads forwards laterally to ganglion IX and the ventro-lateral margin of the auditory capsule, in front of gill cleft 2 and mesial to epibranchiale 1 and ceratobranchiale 1.

Vagus ramus post-trematicus 2 which originates about 200 p behind vagus 1 , innervates levator arcus branchialis 3 ; thenceforth it leads ventro-anteriorly to innervate transversus ventralis 3, and end in the floor of the mouth. Vagus rami pretrematicus 2 and pharyngeus 2 are directed ventro-anteriorly to the roof of the pharynx-below the branchial lymphoid mass, which is probably the thymus-in front of gill cleft 3.

Vagus ramus post-trematicus 3 originates about 140 p behind vagus 2 and leads backwards and thence forwards to innervate levator arcus branchialis 4. It ultimately is situated over afferent epibranchial artery 4, and innervates transversus ventralis muscles 5 and 6, and perhaps the coracobranchialis musculature. A vagus ramus pretrematicus 3 and more mesially situated ramus pharyngeus 3 lead forwards over the pharynx in front of gill cleft 4.

A stout vagus ramus post-trematicus 4 originates from the ventro-posterior margin of the vagus ganglion, behind vagus nerve 3, to lead over the top of ceratobranchiale 5 and probably innervate levator arcus branchialis 5. Two other more posterior vagus nerves, probably 5 and 6, are distributed to the region between the oesophagus and the sphincter oesophagi.

In the 16 mm and 27 mm specimens (Figs 29 and 30) vagus nerves 1-3 only are distinguished, and are similar to those of the older stage, except that pharyngeal components, as in younger stages, are not recognizable in the 16 mm stage. In the 13.5 mm, 14 mm and


15 mm specimens (Figs 25 to 27), nerve IX and vagus 1 each terminate in what would seem to be a tiny ganglion, below the fronts of ceratobranchiale 1 and 2, and against the outer margins of transversus ventralis 1 and 2 respectively. In the 16 mm stage (Fig. 29) a minute ganglion is also recognized associated with vagus nerve 11, beneath ceratobranchiale 3. Merely suggestions of incipient vagus nerves are recognized in the 11 - 5 mm stage (Fig. 3).

Just behind the auditory capsule, and originating from the hinder end of the vagus ganglion, a stout antero-dorsally directed ramus auricularis X divides and leads laterally to the auditory capsule, to supply the skin of the occipital region; likewise a large postero- dorsally directed ramus supratemporalis X is distributed to the neuromasts laterally to the occipital somites.

A large truncus intestino-accessorius X originates from the dorso-posterior region of the vagus ganglion, behind the vagus nerve 3 (Figs 30 and 31). It proceeds postero-ventrally over the hinder levator musculature-which it probably innervates-and thence forwards. It is divided into : (a) an upper anterior r. recurrens intestinalis X, which is situated below ceratobranchiale 4, over hypoglossal nerve 2 and lateral to the mandibular vein, and innervates the rectus cervicis and coracobranchialis musculature ; (b) a lower mesial anterior r. recurrens intestinalis X, which innervates transversus ventralis muscles 4 and 5 and the lower surface of the sphincter oesophagi; (c) a posterior r. superior laryngeus X leads to the dorso-lateral surface of the sphincter laryngei; (d) a posterior r. inferior laryngeus X ends on the ventral surface of the latter muscle; (e) the hind-end of the vagus ganglion is divided and continues backwards over the pulmonary artery to end dorso-laterally in the laryngeal musculature ; (f) delicate cardiac and (g) pulmonary divisions of the truncus, which are recognizable, though details are not clear at this stage.

An incipient truncus X in a 15 mm specimen, and its anterior and posterior divisions in a 16 mm specimen are already present (Figs 27 and 29).

Hypoglossal (occipital) occipito-spinal and spinal nerves Hypoglossal nerve 1 was not found in Neocerutodus by Sewertzoff (1902), but was

reported by M. Furbringer (1 897) and Krawetz (1 91 l), and by Agar (1906a) in Protopterus. It is first recognized in my 14 mm stage (Fig. 26) and comprises a minute ventral root, which innervates somite 1 (metotic segment 3).

Hypoglossal nerve 2 (like all succeeding nerves) is recognized in the 1 I a 5 mm and older stages (Figs 3,25 to 27 and 29 to 31), though it was not distinguished on the left side in the 11.5 mm stage or the right in the 13.5 mm specimen. It comprises a ventral root and innervates somite 2 (metotic segment 4).

Hypoglossal nerve 3, which like hypoglossal nerve 2 was described as a ventral root only (Sewertzoff, 1902), innervates somite 3 (metotic segment 5). In a 34.5 mm specimen (Fig. 31), on the right side the nerve includes a tiny ganglion. In the latter and a 27 mm specimen (Fig. 30) the closely associated hypoglossal nerves 2 and 3 curve forwards lateral to the head vein, below the coracobranchialis musculature and the outer divisions of the truncus X, to supply the rectus cervicis.

Occipito-spinal nerve 1 of the 6th metotic segment comprises a ventral root only in all specimens (Figs 3,25 to 27 and 30), except for the inclusion of a tiny ganglion on the right side of the 27 mm specimen, and a dorsal root also on both sides in 16 mm and 34.5 mm specimens (Figs 29 and 31).


Occipito-spinal nerve 2 of the 7th metotic segment comprises a ventral root and a tiny ganglion on the right side of an 11 -5 mm specimen (Fig. 3), and a dorsal root also, but no ganglion on the other side. In all other stages it comprises dorsal and ventral roots and a ganglion, like succeeding spinal nerves. In the 27 mm specimen (Fig. 30), occipito-spinal nerve 1 curves forwards ventro-laterally, over the region of the posterior nephrostomial tubule of the pronephros, and innervates the rectus cervicis (it joins hypoglossal nerve 3 in the 34.5mm stage) (Fig. 31). A division from occipito-spinal nerve 1 joins occipito- spinal nerve 2 and together with spinal nerve 1, of the 8th metotic segment, they are distributed to the fore-fin musculature, mesially to the rectus cervicis, below the rib of the occipito-spinal arch 2 (Fig. 30).

Spinal nerves 2 and 3 are distributed to the lateral plate musculature. M. Furbringer (1897) described 3 hypoglossal and 2 occipito-spinal nerves in front of

the first spinal nerve. In another smaller adult of Ceratodus in his possession, hypoglossal nerve 3 included a fine dorsal root and the succeeding nerves all comprised dorsal and ventral roots and a ganglion. Furthermore he described the innervation of the hypobranchial musculature (plexus cervicalis) to be by the hypoglossal nerves 1-3, and that of the fore-fin (plexus branchialis) by occipito-spinal nerves 1 and 2 and spinal nerve 1, which is essentially in agreement with the results in the present work.

The head and pharynx of Rana temporaria and Rana esculenta 33 mm and 26 mm long respectively

The chondrocranium and visceral skeleton A somewhat detailed analysis of various organ systems of the larval anuran head is

included in the present work, in order to provide comparisons, at first hand, with similar systems in Urodela and Neocerutodus. In particular consideration is given to the homologies between their nervous and muscular systems.

Important information on development in Rana is given in the works of Gaupp (1904, 1906), Stadtmiiller (1936), de Beer (1937), Pusey (1938), and Jarvik (1942) among others, and more recently Stephenson (1951~) considered Anura with special reference to the head in Leiopelma.

Trabeculae cranii are well developed in both specimens, and orbital cartilages also in R. temporaria, but there is no significant development in the region of the nasal capsule, though this is well developed in a 40 mm larva of R. temporaria (Plate IV(c)).

Foramina optica (complete in R. temporaria) and oculomotorius transmit optic and oculomotor nerves (and ophthalmica magna artery) respectively, and the taenia marginalis posterior has joined the pila prootica to the front upper surface of the auditory capsule (Figs 34and 35). Ascending and otic processes connect the quadrate cartilage to the chondrocranium (Gaupp, 1906), and a hinder process of the quadrate articulates with the base of the inner floor of the capsule; thus there are foramina prootica, sphenoticus and sphenoticus minus.

The quadrate cartilage is continued forwards as an elongated flattened cartilaginous process, to expand over the ceratohyale into a biflanged processus muscularis quadratus (Fig. 36; Plate lV(f)). From the median flange a commissura quadrato-cranialis anterior (R. temporaria, Gaupp, 1906)-and a posterior also in R. esculenta-join the trabecula,


considered to be part of the basal process of the quadrate (Pusey, 1938, 1943), or the homologue of the urodele pterygoid process (Edgeworth, 1925). A basal process is described in Leiopelma from cartilage of hyoid origin (Stephenson, 1951a). In front the inner flange of the quadrate cartilage ends as a processus quadrato-ethmoidalis, and the lateral one ends postero-lateral to Meckel’s cartilage as a processus (pars) articulo-quadratus. Mesio- ventral to the auditory capsule in R. temporaria, below the foramen ovale and the rudimentary columella (probably the pars interna plectri, or otostapes; the pars externa plectri, or hyostapes, and operculum develop later; de Beer, 1937) there is a foramen facialis. Behind the auditory capsule is an occipital arch, and in R. temporaria succeeding neural arches each possess a well-developed centrum, anterior and posterior zygapophyses and rudimentary ribs to vertebrae 2 and 3 (Fig. 34). A foramen hypophyseos is recognizable in R. esculenta but has disappeared in R. temporaria, for here there is a complete cartilaginous floor to the chondrocranium, with a separate pair of foramina to permit entrance of the internal carotid arteries.

A narrow roofing tectum transversum connects the orbital cartilages over the mid-brain in R. temporaria, but in both specimens, behind, a tectum synoticum, which connects the auditory capsules over the mid-hind-brain, leads forwards as a tania tectum medialis (Figs 34 and 35).

Paired fused suprarostral cartilages curve upwards on either side of the front of the snout. Close behind and mesially to them are similarly arranged paired infrarostrals (Figs 34 and 36), but these have a recognizable ventral junction. There is merely a suggestion of a basimandibular cartilage-or mandibular copula-only in R. temporaria. Behind (on each side) and in sequence are Meckel’s cartilage, and a large boat-shaped ceratohyale- notched at its outer end for the insertion of the orbitohyoideus muscle-which fuse with each other in the mid-line, to form the pars reuniens of the hypobranchial plate, and extend outwards, below the front of the processus muscularis quadratus. The hypobranchial plate and the pars reuniens may represent two fused hypohyale, and copulae 1 and 2 the basihyale and basibranchiale 1 (paired), respectively (de Beer, 1937).

Four ceratobranchiale, each possessing a large posteriorly directed cartilaginous spine, and the first a number of others also, extend laterally from their union with the “plate”, below and behind the gill clefts, to support the delicate gill region (Figs 33 to 35).

Musculature

For previous descriptions in Anura and other Amphibia reference may be made among others to the works of Luther (1914), Edgeworth (1935) and Kesteven (1944). All muscles are paired except where stated (Fig. 33).

Components of the large masseter musculature-the adductors of Luther (1914)- include a laterally situated levator mandibulae posterior, which inserts behind on the hinder dorsal surface of the quadrate cartilage, mesial to the otic process, at the level of origin of the r. hyomandibularis facialis, and a levator mandibulae anterior, which inserts on the ventro-mesial and anterior surface of the auditory capsule, just behind the origins of the hyomandibular and palatine nerves. Both muscles are directed forwards below the eye, outside (levator posterior), inside (levator anterior), thence ultimately fused together over the quadrate process. Further, the levator mandibulae posterior is separated into superficialis and profundus components. In front the solid masseter, in cross-section

518 H A R O L D FOX

cylindrical within a cup-shaped quadrate cartilage (Plate IV(f)), inserts on Meckel's and the suprarostral cartilages.

The intermandibularis musculature is divided into three (Edgeworth, 191 1, 1935). A short thick mandibulo-labialis, inserted behind and below the infrarostral cartilage at the lower surface of the mouth, is directed ventro-posteriorly to the skin below the geniocoracoideus, to end ventro-mesially to Meckel's cartilage. An intermandibularis anterior (submentalis) joins the infrarostral cartilages below. A large intermandibularis posterior

cehy.

m.c. \ cebrl A

a.arc.3

I I rnm

FIG. 32. 17 mm specimen of Hynobius nebulosus. Ventral reconstruction of the splanchnocranium and some of itslassociated ventral musculature. (Redrawn after Fig. 31, and see also Figs 30,32 and 33, Fox, 1959.)

(submaxillary) inserts in front on the ventro-lateral surface of Meckel's cartilage and leads postero-mesially, to meet its fellow of the other side in a median raphi below the geniocoracoideus ; in front of the ceratohyale and the hypobranchial plate. At metamorphosis with the loss of the horny teeth and the elongation of Meckel's cartilage the mandibulo- labialis atrophies, and the intermandibularis posterior spreads back as a solid sheet below the lower jaws.

A large solid longitudinally arranged geniocoracoideus inserts in front on the lower surface of the infrarostral cartilage, and extends backwards below the ceratohyale and


hypobranchial plate, and over the intermandibularis posterior to end on the undersurface of the “plate” at the transverse level of origin of ceratobranchiale 3.

The hyoid muscle plate separates into a sheet-like interhyoideus and an upper levator hyoideus; the latter further dividing into an orbitohyoideus and a closely associated

Imm

FIG. 33. 33 mm stage of Rana temporaria. Ventral reconstruction of the splanchnocranium, including the rostra1 cartilages, and some of its associated ventral musculature.

quadrato-hyo-angularis. The interhyoideus situated below the ceratohyale, branchiale, geniococoracoideus and other branchial muscles, inserts on the antero-lateral and ventral surfaces of the ceratohyale, to meet its opposite member below copula 2.

The quadrato-hyo-angularis inserts in front on the lateral edge of Meckel’s cartilage and curves backwards below the quadrate cartilage, to end on the antero-lateral and ventral surfaces of the ceratohyale, mesially to the orbitohyoideus muscle. The latter inserts in front on the edge of the lateral flange of the quadrate cartilage, about halfway between Meckel’s cartilage and the ceratohyale, and is directed backwards, laterally to the quadrato- hyo-angularis, to end on the postero-lateral surface of the ceratohyale.

A ceratohyoideus internus originates in front, over and halfway along the ceratohyale.


It is continued behind, over the interhyoideus and below ceratobranchiale 1, and ends on a ventral cartilaginous process of the hypobranchial plate, between ceratobranchiale 2 and 3.

A short subarcualis rectus 1 is inserted on the ceratohyale, thence it is situated over and laterally to the ceratohyoideus internus and inserts behind, on the ventro-mesial surface of ceratobranchiale 1. Behind the ceratohyoideus internus a composite subarcuales 2, 3 and 4 separately inserts on the hind surface of ceratobranchiale 2 and ventral surfaces of ceratobranchiale 3 and 4, respectively. In front of the latter insertion a rectus cervicis separates off ventro-mesially, to continue backwards lateral to the heart (Fig. 33).

Constrictor branchialis muscles 1-3 (or possibly 2-4) each lead outwards below, against and inserting on the top of its relevant ceratobranchiale. In the ventro-mesial situation the first inserts just laterally to the hinder end of the ceratohyoideus internus, the second against the junction of the hind end of the latter muscle and the front of subarcualis 2, and the third constrictor inserts near the separation of the front of the rectus cervicis.

Transversus ventralis 2 originates from the hind surface of copula 2. It is situated over the interhyoideus, below the hypobranchial plate, mainly mesial to the hind end of the geniocoracoideus and postero-laterally and below the thyroid vesicles, to end behind on a cartilaginous process of the “plate” between ceratobranchiale 2 and 3.

At the hind end of the branchial skeleton a large dilator laryngeusinserts on the laryngeal skeleton, and extends postero-laterally below the auditory capsule. It meets a transversus ventralis 4, which is joined to the top of ceratobranchiale 4 and extends below the pharynx, to fuse with the dilator laryngeus. Behind and surrounding the oesophagus and larynx are sphincters oesophagi and laryngei muscles, respectively.

Levator arcus branchialis 1 muscle from the lateral surface of the auditory capsule inserts on the upper ends of ceratobranchiale 1 and 2. Levators 2, 3 and 4, which are not clearly demarcated, are likewise inserted on ceratobranchiale 2-4, respectively.

Arterial system

In R . esculenta (Fig. 36) afferent epibranchial arteries 14-the first slightly in front of the others-originate from the truncus arteriosus of the heart, and subdivide into capillaries in the gill filaments. Antero-laterally to afferent artery 1 a large continuous hyoid artery joins the ventral and dorsal lateral aortae, ventro-mesial to the branchial lymphoid body. The truncus continues forwards (lateral ventral aorta) over the ceratohyoideus internus and interhyoideus muscles, thence mesially to the former and to the hyoid, to end lateral to the geniocoracoideus and the infrarostral cartilage.

In sequence behind the hyoid artery and from capillaries in the gill filaments, efferent epibranchial arteries 1-3 join the lateral dorsal aorta; the fourth, which leads into the third, comprising three pulmonary divisions, which originate from the front and rear regions of the lung, near the front of the liver and mesial to the pronephros.

At the level of neural arch 1 an anteriorly directed occipital artery from the lateral dorsal aorta is situated lateral to the hind-brain, mesial to the hind surface of the auditory capsule and the occipital arch, and thence over and lateral to the former, to lead mesial to the eye. It is recognized against the hinder region of the orbital cartilage, over the rectus muscles and profundus and olfactory nerves, to end mesial to the nasal sac (Fig. 36).

In front of the hyoid artery a mandibular artery, from the lateral dorsal aorta, leads forwards laterally to the palatine nerve, below the hind region of the levator mandibulae


anterior and over the levator mandibulae posterior. It is divided ventro-mesial to the r. maxillo-mandibularis V between the two main components of the masseter, and ends within the levator mandibulae posterior superficialis.

The internal carotid artery enters the chondrocranium through the foramen hypophyseos and gives rise to the following arteries : (a) an antero-dorsally directed carotis cerebralis anterior, to the region between the lobes of the fore-brain; (b) an ophthalmica magna artery, which is directed through a common foramen oculomotorius shared with the oculomotor nerve, and leads below the rectus superior and profundus nerve and over the rectus inferior and r. maxillo-mandibularis V to the median surface of the eye; just behind the optic nerve; (c) a carotis cerebralis posterior, which leads backwards to join its partner below the mid-brain, as the (d) basilar artery.

The main internal carotid artery-probably representing the arteria cranio-palatine of Gaupp (1906); see Allis (1930)-emerges from the chondrocranium in front, through a ventral foramen in the basal plate. It is situated mesial to the hind end of the trabecula, commissura quadrato-cranialis anterior and posterior, internal naris and nasal sac, and dorso-mesial to the processus quadrato-ethmoidalis, and ends at the front of the snout, mesially to the front of the trabeculae and within the suprarostral cartilaginous ring.

Cranial nerves

A description of the nerves of the snout of Rana is briefly summarized by Jarvik (1942), based on that in the works of Ecker, Wiedersheim & Gaupp (1899, pp. 128-156), where all the nerves of the head are described. For further information on the cranial nerves in Amphibia reference may be made to the works of Coghdl (1901), Gaupp (1904), Luther (1914), Edgeworth (1935) and Stadtmuller (1936). Where possible in the present work similar terminology to that used for Urodela has been employed (Fox, 1954, 1959).

In R. temporaria (Fig. 34) olfactory nerve 1 leaves the ventro-lateral margin of the olfactory lobe through the presumptive foramen olfactorius evehens, below the r. nasalis internus profundus V. Two divisions, which further divide, are distributed to the mesial and dorsal surfaces of the nasal sac, latero-dorsally to the trabecula.

Optic nerve I1 from the floor of the fore-brain emerges through a separate foramen optica to lead to the eye.

Oculomotor nerve I11 from the floor of the mid-brain leaves the chondrocranium with the ophthalmica magna artery, through a common foramen oculomotorius. An upper division above and a lower one below the r. ophthalmicus profundus V, are distributed to the recti superior, inferior and internus, and inferior obliquus. In R. temporaria what would seem to be a small division of the profundus-probably the trochlear nerve IV-leads to the superior obliquus; it is separate, originating in the upper mid-brain in R. esculenta.

Abducens nerve VI originates from the ventral surface of the medulla as in urodeles (Gaupp, 1911; see Fox, 1954), at the level of the hind region of the auditory capsule, and leads forwards over the basal plate, close against the mesial surface of the capsule. and auditory nerve, where it was traced into the trigeminal ganglion.

The trigetninal nerve V (1) The r. ophthalmicus profundus V (Figs 34 and 35) leads forwards from the antero-

ventral end of the trigemino-facialis ganglion, mesial to the processus ascendens and over the

X 0

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4

0

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hind end of the levator mandibulae anterior. Several upper branches to the skin, between the eye and chondrocranium, ramify with the r. superior ophthalmicus facialis. In the region of the incipient nasal capsule the profundus divides into: (a) a r. nasalis internus profundus V, distributed over the trabecula and olfactory nerve mesially to the nasal sac, which ends in the skin at the front of the snout; (b) a r. nasalis externus profundus V is distributed dorso-laterally to the nasal sac, mesially to the tip of the outer flange of the quadrate cartilage and over the masseter musculature ; (c) two ramus palatine-profundus V nerves, from the r. nasalis externus profundus V, join the palatine nerve ventro-mesially to the trabecula in the prenasal region.

(2) A large ramus maxillo-mandibularis V from the trigeminal ganglion emerges through the foramen sphenoticus, antero-laterally to the processus ascendens, over the levatores mandibulae anterior and posterior and below the rectus inferior. A mandibular division supplies the hinder masseter musculature and the main horizontally flattened nerve, situated below the optic nerve and over the masseter, subsequently divides into: (a) a powerful r. maxillaris V, which further subdivides into a r. maxillaris superior V, situated mesial to the processus muscularis quadratus, over the masseter, and distributed to the lateral skin over the nasal sac, and a r. maxillaris inferior V, situated lateral to the masseter, close against the r. mandibularis V, which ends beneath the skin laterally to the supra and infrarostral cartilages; (b) a r. mandibularis V, situated mesial to the processus muscularis quadratus, over the levator mandibulae anterior and thence laterally to the levator mandibulae posterior superficialis and profundus muscles, which it innervates. Further forwards other divisions lead antero-laterally and postero-mesially to Meckel’s cartilage, the former ending close to the ventral skin and presumably supplying the intermandibularis musculature.

The facialis nerve VII ( I ) The ramus hyomandibularis facialis VII emerges from the facialis ganglion antero-

laterally, below the articulation of the hinder end of the quadrate cartilage with the inner floor of the auditory capsule; separated from the origin of the palatine nerve by a hind portion of the levator mandibulae anterior. The hyomandibular nerve is recognized below and thence alongside the quadrate cartilage and the ceratohyale, and divides within the orbitohyoideus, which it innervates, into (a) an upper r. mentalis externus facialis, which penetrates the orbitohyoideus and ends underneath the skin below the processus articulo- quadratus; (b) a r. mentalis internus facialis, which divides lateral to the ceratohyale within the orbitohyoideus into a posterior division to the interhyoideus, and other ventral or ventro-posterior divisions to the neuromasts and skin; (c) a delicate r. alveolaris facialis? situated just behind the ceratohyale, leads for a short distance almost vertically downwards, below the quadrate cartilage, above the ceratohyale and close to the side of the mouth. A similar minute nerve in R. esculentu is situated mesial to the orbitohyoideus.

(2) A ramus palatinus facialis, from the ventral region of the facialis ganglion, at first is situated below the lateral margin of the basal plate and the inner margin of the levator mandibulae anterior.

It divides into: (a) a r. palatinus lateralis facialis, directed forwards below the commissura quadrato-cranialis anterior, lateral to the internal naris and mesial to the quadrate cartilage; (b) a r. palatinus internus facialis (which sends a division to the dorso-lateral roof of the mouth in R. temporaria (Fig. 34)), and this division joins a branch of the

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r. maxillaris V postero-mesially to the processus quadrato-ethmoidalis in R. esculenta (Fig. 35), situated lateral to and thence below the trabecular plate, mesial to the internal naris. It ultimately anastomoses with branches of the r. nasalis internus profundus V, and ends over the front of the roof of the mouth.

(3) A ramus buccalis facialis is directed antero-ventrally underneath the skin, laterally to the processus ascendens, dorso-laterally to the levator mandibulae posterior and over the quadrate cartilage. It is distinguishable ventro-lateral to the eye, over the hinder upper edge of the processus muscularis quadratus and the top of the orbitohyoideus, but not thereafter .

(4) A ramus superior ophthalmicus facialis arises together with two roots of the buccal nerve (only one root in R. esculenta, Figs 34 and 39, from the lateralis component of the facialis ganglion, below the front of the auditory capsule and just behind the processus ascendens. It leads almost vertically upwards, crossing the top of the foramen sphenoticus against the pila prootica, and thence forwards over the eye. It is distributed to neuromasts of the upper surface, ramifies with dorsal branches of the profundus nerve, and ends in front over the snout. Both rami superior ophthalmicus and buccalis facialis are better developed in R. esculenta (Fig. 35).

The glossopharyngeal nerve IX from the front of ganglion IX is situated lateral to the foramen ovale, below and receiving a branch from the VII-IX Connective. It divides into : (a) a descending ramus pretrematicus IX, situated mesial to and close against the large branchial lymphoid body, ending ventro-mesially to the front of the gill cleft 1; (b) a ramus post-trematicus IX, situated over and thence laterally to the lymphoid body, within the levator arcus branchialis 1, which it innervates. It continues along the ventro- mesial surface of ceratobranchiale 1, innervate the ceratohyoideus internus and terminates laterally to the dorso-anterior end of the ceratohyale. The large ganglion IX extends back behind the auditory capsule. Its roots to the hind-brain enter the chondrocranium between the capsule and occipital arch, together with those of the larger and more posterior vagus ganglion.

Comparison of the head and pharynx of larvae of Neoceratodus Urodela and Anura

Chondrocranium and visceral skeleton For a review of the similarities and differences of the chondrocranium and hyobranchial

skeleton of Dipnoi and Amphibia, reference may be made to the publication of de Beer (1937, pp. 458-461), and Figs 1,2,7,12 to 14, 18 to 20 and 30 to 40 and other illustrations (Fox, 1954, 1959, 1961c, 1962, 1963~).

The overall shape and arrangement of various cartilaginous components of Neoceratodus resemble those of Amphibia, particularly Urodela (Sewertzoff, 1902; de Beer, 1926). In all groups chondrification is precocious, though delayed in the nasal and orbital regions of R. temporaria and R. esculenta (Figs 34 and 35). The chondrocranium is platytrabic and widely spaced trabeculae enclose at first a hypophyseal foramen, which ultimately is reduced by further chondrification.

Paired nasal capsules develop in a similar way, each sharing a common medial wall (planum verticale) in Neoceratodus-like Chirodipterus (Save-Soderbergh, 1952)-and Anura (Plate IV(c)). In contrast there are separate medial capsule walls in most Urodela,


an arrangement confirmed in larvae of Ambystoma mexicanum (25 mm), Salamandra maculosa (24 mm), Cryptobranchus japonicus (32 mm), C. alleghaniensis (37 mm), Hynobius retardatus (37 mm) and Hynobius nebulosus (32 mm). Nevertheless, de Beer (1937, p. 461) reported a medial nasal septum in Salamandra, as has Amphiuma means (Higgins, 1920), and in Hynobius nebulosus (32 mm) though the capsules are separate in front and behind, they share a broad internasal septum. Each nasal capsule has an open floor-the fenestra narina-which is large in Neoceratodus, bounded behind by a similarly derived lamina

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FIG. 37. 30 mm specimen of Crjptobrunehus japonieus. Lateral reconstruction of the front of the neurocranium

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and splanchnocranium and associated cranial nerves. (Redrawn in part after Fig. 14, Fox, 1954.)

orbitonasalis; the roof of the nasal capsule in Neoceratodus is highly fenestrated, much more so than in Amphibia.

The cornua trabeculae of Amphibia are ventral to the external anterior nares (Plate III(d)), not dorsal to them as in Neoceratodus.

In all groups trigemial and facial nerves and blood vessels maintain similar relationships with the autostylic quadrate cartilage and its processes (Figs 22 to 24,29 to 31, 34, 35 and 37 to 40). All are monimostylic, though Hynobius nebulosus and H . (Salamandrella) keyserlingii secondarily become semistreptostylic in the larva, and Plethodon and Ranodon in the adult (Edgeworth, 1925).


There is still doubt on the homology of the basal process of Anura; its processus muscularis quadratus is unique (Plate IV(f)).

A complete cartilaginous pterygoid process, fused in front with the trabecula just behind the lamina orbitonasalis, is found in Cryptobranchus japonicus (Fig. 37), and C. alleg- huniensis (Plate IV(a)) (Aoyama, 1930; Edgeworth, 1923c; Fox, 1954), and an incomplete one in Suluniandra maculosa (Stadtmiiller, 1924, 1936), Hynobius nebulosus (Plate III(h) ; Fig. 38), H. (Salamandrella) keyserlmgii (Fox, 1959, 1963~)-though Edgeworth ( 1 9 2 3 ~ )

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FIG. 38.32 mm specimen of Hynobius nebulosus. Similar reconstruction of comparable components as in Fig. 37. (Redrawn in part after Fig. 28, Fox, 1959.)

found the pterygoid process complete in Hynobius-Ranodon sibiricus (Edgeworth, 1925), a 69 mm specimen of Ambystoma punctatunz (Winslow, 1898) and a 65 mm specimen of Pleurodeles waltlii (Eyal- Giladi & Zinberg, 1964). A true process is not present in Rana and in Neoceratodus. In Semon stages 45 and 46 ( 1 1.6 mm and 13-9 mm long) however a transitory one is reported by Greil(l913, pp. 1124, 1155, Figs 240 to 422), but it is not figured in Semon stage 48 (17.8 mm long). In Protopterus and Lepidosiren it is represented by a fibrous stand (Agar, 1906a).


An otoquadrate cartilage of the hyoid, situated below the cartilaginous floor of the auditory capsule in Neoceratodus, forms part of the capsule floor mesially to the facial foramen in Urodela (Plate II(a), (h), (i); Plate III(g)) (Fox, 1963d).

The hyoid comprises a separate ceratohyale, hypohyale and medial basihyale (developed from the pair of each side) in Urodela, but an epihyale, laterohyale and stylohyale are also included in Neoceratodus. In Rana the arrangement is extremely specialized as previously described (Fig. 33). In Ambystoma and Triton the dorsal end of the ceratohyale connects with the quadrate cartilage by a ligament, which may chondrify at its attachment to the latter as the processus hyoideus (de Beer, 1937). Furthermore, in some Urodela such as Hynobius nebulosus (Fig. 38) and Salamandra maculosa a cartilaginous (or cellular) stilus from the columella joins the quadrate cartilage (Kingsbury & Reed, 1909; Fox, 1963d); the columella joins it by a ligament in Rana.

There is no medial wall to the auditory capsule in Neoceratodus, in contrast to that in Amphibia whose chondrified inner surface includes a number of separate foramina for the passage of the anterior and posterior divisions of the auditory nerve, and for the endo- lymphatic and perilymphatic ducts (Plate II(c) ; Plate III(f), (g) ; Plate IV(b)) (Stadtmiiller, 1924,1936; Pusey, 1943; Fox, 1954, Fig. 17,1959, Figs 20 to 22). Neither is there a foramen ovale (Figs 23 and 24)-though its region is claimed to be discernible in Neoceratodus and Protopterus because of the presence of a transparent covering of cartilage (Holmgren, 1949a)-nor a columella or a later developed operculum which are features of amphibian development (Plate IV(b); Figs 37 to 40) (Kingsbury & Reed, 1909; Schmalhausen, 1923a; de Beer, 1937; Fox, 1962).

In Neoceratodus nerve IX emerges from the brain through a foramen jugulare in the ventro-lateral margin of the auditory capsule (Fig. 30), not behind it as in Amphibia (Fox, 1959). A cartilaginous tympanic ring on which the tympanic membrane is stretched is peculiar to members of the Anura (de Beer, 1937).

The entire roof is completely cartilaginous in Neoceratodus, but large vacuities are found in Amphibia.

In larval Rana only, Meckel’s cartilage is short and transversely arranged (Fig. 33), and between the infrarostrals, which together with the suprarostral cartilages support horny teeth, there is a median basimandibular cartilage.

An intermandibular cartilage, which ossifies, and labial cartilages develop only in Neoceratodus, but as in Urodela Meckel’s cartilage is generally similar in shape and arrangement.

Behind the 5 open gdl clefts of larval and adult Neoceratodus are 5 ceratobranchiale, which end freely ventrally (Figs 20, 28, 31 and 41) and support the gill filaments (Jaquet, 1899), the first four branchiale each possessing a dorsal epibranchiale (K. Furbringer, 1904): three pharyngobranchiale and one basibranchiale (van Wijhe, 1882), or 2 basibranchiale (Huxley, 1876) have been described in adults. In contrast most larvae of Urodela (and Anura) possess 4 ceratobranchiale behind 4 open gill clefts (Figs 32 to 35, 39,40 and 42), with usually hypobranchiale 1 and 2, and occasionally a third in Hynobius nebulosus (Fig. 32) (Fox, 1959), Cryptobranchus (Menopoma) alleghaniensis (Edgeworth, 1923b), H . Ieechii (Matumoto, 1932), Salamandra maculosa (Driiner, 1901 ; Stadtmiiller, 1936) and Onychodactylus (Okajima, 1922). Ocasionally there are 3 arches as in Necturus; the larval Eleutherodactylus nubicola has no internal or external gills or aquatic stage and merely 3 blind gill pouches and 3 ceratobranchiale (Lynn, 1942), and Leiopelma has 5


ceratobranchiale (Stephenson, 1951a). It is of interest that Glyptolepis, a Porolepiform Crossopterygian, possessed 4 and sometimes 5 branchiale, behind the ceratohyale and hypohyale of the hyoid, with ceratobranchiale and hypobranchiale 1-4, a basibranchiale and a urobranchiale (Jarvik, 1961). In Urodela anterior and posterior copulae are probably the homologues of basibranchiale 1 and 2 (basihyale and basibranchiale 1 in Rana), and the urobranchiale may be of independent origin (Aoyama, 1930), or developed as a ventro-posterior outgrowth of the second basibranchiale (Edgeworth, 1920). Furthermore, the hyobranchial skeleton of older urodele larvae includes radii anteriores and posteriores (see Eyal-Giladi & Zinberg, 1964), of obscure origin (de Beer, 1937). Older anuran larvae have antero-lateral and postero-lateral cartilages present.

Commissura terminales of Amphibia (Figs 32 and 33), which are absent in Neoceratodus (Fig. 20), may represent epibranchiale. Traces of vestigial and blind gill clefts behind the fourth open one exist in larvae of Cryptobranchus, Menopoma, Hynobius, Salamandrella, Salamandra, Amphiuma, Ambystoma, Triton and Rana (Kingsley, 1892; Driiner, 1901, 1904; Makuschok, 1911, 1912; Edgeworth, 1920; Fox, 1954, 1959). There are no traces of extra gill clefts behind the fifth open one in Neoceratodus.

During metamorphosis there is a radical rearrangement and reduction of branchial elements in Amphibia (Gaupp, 1904; Stadtmiiller, 1936). Caducibranchiata usually retain two branchiale as in Pleurodeles (Eyal-Giladi & Zinberg, 1964), Rhyacotriton (Cloate, 1961) and Pseudotriton (Joubert, 1961), or merely one in Spelerpes (Smith, 1920), though Perennibranchiala such as Proteus, Necturus, Siren and Amphiuma have more (Stadtmiiller, 1936). However, the adult Cryprobranchus (Menopoma) alleghaniensis retains 4 ceratobranchiale and a third hypobranchiale (Edgeworth, 1923b), or even a fourth (Druner, 1904), and an open gill cleft.

A laryngo-tracheal skeleton (or cartilago lateralis) of arytenoid (larval Anura) and tracheal elements also (larval Urodela), like that of Hynobius (Edgeworth, 1920; Fox, 1959) is not found in Neoceratodus and other living Dipnoans.

Sclerotic cartilage develops extremely early in Neoceratodus (Figs 5,6 and 28), and Urodela (in a 14mm specimen of Hynobius), but much later in Anura. It is well developed and persistent in Neoceratodus and many Amphibia such as C. alleghaniensis, Ambystoma, Necturus, Rhyacotriton (Cloate, 1961) and Rana, but usually disappears at metamorphosis in Triton and Salamander (Stadtmuller, 1924).

The number and arrangement of the anterior neural cartilages incorporated into the hind region of the skull, and their associated nerve components differ in Dipnoi and Amphibia (Fox, 1954, 1957, l959,1961a,c, 1962). The head of Urodela (Goodrich, 191 1)- and probably Anurans (Elliot, 1907; van der Steen, 1930)-includes six segments; a hypoglossal foramen, which is present in a few urodeles like Cryptobranchus japonicus, C. (Menopoma) alleghaniensis, Hynobius nebulosus and Salamandra maculosa (Figs 38 and 39), transmits a hypoglossal nerve and marks the boundary between preoccipital and occipital arches, situated behind metotic segments 5 and 6, respectively. A preoccipital arch is not recognized in Anura (Figs 34 and 3 3 , but an occipital arch in its topographical and general arrangement is similar to that of Urodela. In contrast the head of Protopterus includes 9 and Neoceratodus 10 segments (Figs 30 and 31).

Neoceratodus has lost the nyotomes of first two metotic somites. Larvae of Anura retain the second, and urodeles also have a small upper portion of the somite of metotic segment 2 . In Hynobius keyserlingii traces of a rudimentary first metotic somite and its associated


cartilaginous arch are recognized for a short time; a most primitive arrangement (Regel, 1961, 1964 and personal communication).

Neoceratodus has also lost the first four metotic cartilaginous occipital arches, and by the 16 mm stage has practically lost occipito-spinal arch 1 of metotic segment 6, for the occipital arch is situated behind metotic segment 5 of head segment 8 (Fig. 28). However in development cartilaginous elements of the third prootic and the first and second metotic segments are retained, which constitute the basal plate (Bertmar, 1959). Amphibia, in contrast, have discarded the first two of their three metotic occipital cartilaginous arches, or in some primitive urodeles merely the first (see Table I), and even this is vestigial in Hynobius keyserlingii.

The first vertebra or atlas is modified in a similar manner in all modern adult Amphibia, and its facets fit against paired condyles of the skull (Parsons & Williams, 1963). The hind region of the cranial notochord is chondrified and attached to the atlas to form the tuberculum interglenoidale (odontoid process), which articulates with the basal plate between the condyles. There is thus a cranio-vertebral joint. In contrast to this arrangement in Urodela and Anura, Dipnoi have a persistent notochord. Transition from the skull to the vertebral column is “gentle” and there is no cranio-vertebral joint (de Beer, 1937, p. 385).

The dispositions of the fore and hind-limb (or fin) blastemata, or of the pectoral and pelvic girdles, were analysed by virtue of their relationship to the spinal ganglia. The latter were used to clarify numeration of body segments counted from the front of the head.

Fore-limb (or fin) elements belong to the region of segments 6-8 in Rana, 7-12 in Hynobius nebulosus, Ambystoma rnexicanum, Cryptobranchus (Menopoma) alleghaniensis and Salamandra maculosa, and 6-10 in 16 mm and 27 mm specimens of Neoceratodus. Hind limb (or fin) elements belong to the region of segments 15-18, 21-27 and 35-38 of the same groups, respectively.

Cranial pharyngeal and anterior spinal nerves Cranial nerves I, 11,111, IV and VI are in genera1 similar in arrangement and distribution,

though there would seem to be close association between the trochlear nerve IV and r. ophthalmicus profundus V in Rana, and termination of the abducens nerve VI was recognized only in Urodela (Figs 31 and 38).

A particularly well developed and complex profundus supplies the skin of the snout in Urodela (Jarvik, 1960) and Neoceratodus-and Chirodipterus also (Save-Soderbergh, 1952)-though no divisions leading to the palatine nerve were recognized in Neoceratodus, a feature seen prenasally in Rana (Figs 34 and 35) and Osteolepiformes like Eusthenopteron, and post-nasally in Urodela (Figs 38 to 40) and Porolepiformes like Glyptolepis and Porolepis (Jarvik, 1942, 1961), or to the truncus infraorbitalis in some specimens of Ambystoma-usually found in Urodela and Neoceratodus (Figs 30,31 and 37 to 39)--or to the maxillo-mandibular and buccal nerves in Rana.

In Urodela the r. superior ophthalmicus facialis is separate (Figs 37 to 40; Plate III(c),(e)) -earlier described in Ambystoma (Coghdl, 1901), and confirmed in the latter and in Salamandra in the present work (also see Fox, 1954, 1959)-and unlike the r. nasalis internus profundus V it does not enter the nasal capsule. Likewise these nerves are separate in Rana (Figs 34 and 35). In contrast, in Neoceratodus they anastomose within the capsule, and they are large and closely associated in Chirodipterus (Save-Soderbergh, 1952, Plate 2, Fig. 2), and in front they emerge from the capsule together.

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The maxillary, mandibular and facial nerves are in general topographically similar in Neoceratodus and Urodela (Figs 29 to 31 and 37 to 40). The weakly developed maxillary nerve innervates the skin at the side of the upper jaw as described by Jarvik (1942, 1960). It is intimately associated with the r. buccalis facialis-the truncus infraorbitalis-in Salamandra and Ambystoma (Figs 39 and 40), rather less so in Cryptobranchus, Hynobius and Neoceratodus (Figs 29 to 31, 37 and 38). In the last named the maxillary nerve crosses the floor of the orbit to join the palatine nerve, mesially to the internal naris. Likewise in Hynobius a division of the truncus infraorbitalis is similarly directed, to emerge from the nasal capsule mesially to the nasal sac, via a small foramen, to innervate the skin of the snout.

A r. mandibularis interior V of Neoceratodus leads over the top of Meckel's cartilage and is probably equivalent to the r. alveolaris V, sometimes recognized in Urodela. The rami mentalis V and mentalis externus facialis are separate in Hynobius, Salamandra and Ambystoma (Figs 38 to 40), or fused together in Cryptobranchus and older larvae of Neoceratodus (Figs 30,31 and 37). The r. mentalis V leads mesial to the dentary in larvae of Ambystoma and Sulamandra-results which confirm those of Herrick (1894) and Coghill (1902) for the former and Francis (1934) for the latter-but does not do so in Crypto- branchus japonicus and Hynobius nebulosus.

Only Neoceratodus possessed a r. mentalis interior facialis, which supplies the retractor mandibulae (a muscle not found in Urodela), and there is no r. palatinus lateralis facialis.

In Urodela the r. jugularis facialis innervates the interhyoideus, digastricus, lateral line organs and the ceratohyoideus externus (Fig. 32) (branchio-hyoideus externus (Edgeworth, 1935) of Perenibranchiala and larval Caducibranchiata, which disappears at metamorphosis), a muscle reported in the primitive anuran Ascaphus (Pusey, 1943). In Neoceratodus this nerve and other divisions of the hyomandibular supply similar structures -reading levator hyoideus for digastricus-except for a ceratohyoideus externus.

In contrast Rana (Figs 34 and 35) possesses a strongly developed r. maxillo-mandibularis V; the maxillary is much more strongly developed than in Urodela and Neoceratodus, and supplies the skin laterally to the nasal sac and rostra1 cartilages. The mandibular divisions supply similar elements as in other groups. A typical truncus inf'raorbitalis is not recognized (Jarvik, 1942, p. 332), but even though the facialis nerve differs from that of the other groups in form and arrangement, nevertheless, like Urodela, there is a r. palatinus lateralis facialis and an anastomosis between the palatinus internus and the profundus nerves.

Possible homologues of the urodele rami mentalis externus and internus facialis supply the orbitohyoideus, interhyoideus, skin and neuromasts. A delicate r. alveolaris facialis ?- but no r. jugularis facialis-is recognized. Rami superior ophthalmicus and buccalis facialis nerves are retained in the adult Neoceratodus (van Wijhe, 1882; Kesteven, 1931b; Edgeworth, 1935), but these are lost in most Amphibia which metamorphose.

A VII-IX Connective is present in all groups. In Neoceratodus an independent ganglion IX (in contrast to Amphibia) enters the skull through a separate foramen jugulare in the lateral margin of the auditory capsule, as in Cephalaspids like Kiaeraspis (Stensio, 1927), Eusfhenopteroti (Jarvik, 1954) and Chirodipterus (Save-Soderbergh, 1952), which is probably a primitive feature. It is of interest that in Leiopelma the combined trunk of nerves IX and X appears to cut into the wall of the auditory capsule, but never pierces it, and it is outside the capsular cavity (Stephenson, 1951a). The arrangement in Cyclostomes and in Amphibia, where nerves IX and X enter the skull behind the auditory capsule, may thus be a secondary development (Holmgren, 1943, p. 141).

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Distribution of nerve IX is similar in all groups, except that in Urodela it supplies the ceratohyoideus externus.

The arrangement of the vagus nerves is not clear in Rana, but inNeoceratodus and Urodela (Hynobius and Cryptobranchus) vagus 1 4 nerves supply levators 2-5, respectively; vagus nerves 5 and 6 of Neoceratodus supply the oesophageal musculature, and vague nerves 5-7 of Urodela supply levator 6, dilator laryngeus and trapezius muscles respectively. Furthermore, vagus nerves 1-3 of Neoceratodus innervate transversus ventralis muscles 2, 3 and 4 and 5, respectively.

Distribution of the truncus intestino-accessorius X in Neoceraiodus has been described (see above). In Hynobius similarly, a r. recurrens intestinalis X innervates transversus ventralis IV (like other Urodela, Driiner, 1901, 1904), and constrictor arcuate muscles (subarcuales recti), and other truncus divisions supply the gut, trachea, larynx and heart.

Spinal nerves 1 and 2, probably including some truncus fibres-the hypobranchialis- lead forward to supply the rectus cervicis (thoracicohyoideus), geniocoracoideus (geniohyoideus) and the intermandibularis muscles, and thus encroach on anterior regions not normally reached in Neoceratodus. In Urodela several lateralis nerves supply neuromasts along the upper and lower regions of the body; in larvae of Neoceratodus a single upper one only, originated from the top of the vagus ganglion.

Fore-fins of Neoceratodus are supplied by occipito-spinal nerves I, I1 and spinal nerve 1 (Fig. 30); fore-limbs of Urodela by spinal nerves 3-5 (in each case of head segments 9-1 1 inclusive). In contrast, those of Rana and other Anura are supplied by spinal nerves 2 and 3 (head segments 8 and 9) (Table I and Fox, 1962).

Musculature

The masseter of Neoceratodus, comprising the levator mandibulae anterior and posterior, is represented in its most primitive condition in vertebrates (Edgeworth, 1926b, 1935). In Urodela in addition a levator mandibulae externus develops from the levator mandibulae anterior-the three adductors of Luther (1914Fand in Anura there are levatores mandibulae externus, subexternus, lateralis and articularis, with the outer levator mandibulae posterior divided into upper superficialis and lower profundus components, respectively (Edgeworth, 1935, p. 44).

In Urodela the levator hyoideus grows forwards from the top of the hyoid, to insert secondarily on the hind surface of Meckel’s cartilage, as the sole depressor mandibulae or digastricus (Edgeworth, 1935; Schmalhausen, 1955; Fox, 1959, 1963b). The levator hyoideus and retractor mandibulae of Neoceratodus presumably represent the orbitohyoideus and the quadrato-hyo-angularis of Rana.

A constrictor hyoideus, like the coracobranchialis of Neoceratodus and Fishes, is not represented in Amphibia.

An intermandibularis posterior is present in Neoceratodus but there is an intermandibularis anterior also in Hynobius nebulosus (Fox, 1959), Ambystoma, Necturus, Plethodon, Diemnjctilus and Anura (Kesteven, 1944), and in Salarnandra, Amphiuma and some members of the Cryptobranchidae (Edgeworth, 1935). In Rana in addition a mandibulo-labialis is recognized.

The similar large paired rectus cervicis muscles of Neoceratodus and Urodela are smaller in Rana, and situated farther back (Figs 15 to 20, 32 and 33).


A median geniocoracoideus of Neoceratodus is presumably derived from paired components, clearly recognizable in Amphibia (Figs 18 to 20, 32 and 33).

The ceratohyoideus internus of all groups is probably the homologue of the heretofore missing transversus ventralis 1, which changes its morphological relationships in ontogeny to insert secondarily in front on the hyoid (Figs 15 to 20). In 14 mm and 17 mm specimens of Hynobius nebulosus it inserts in front on the antero-mesial surface of gill cleft 1, just above the ceratohyoideus externus (Fig. 32), but in 22 mm and 32 mm specimens there is an attachment at the junction of the hypohyale and the ceratohyale (Fox, 1959, Figs 32 and 33). Its more primitive origin, development and final arrangement in larvae of Neoceratodus may be compared with these features in Hynobius and Rana.

In Hynobius from an extremely early age the ceratohyoideus internus is situated longitudinally, not transversely or almost so as in Neoceratodus. Ontogeny in the latter quite clearly demonstrates a phylogenetic trend, which is only barely noticeable in Urodela. Transversus ventralis muscles 2-5 (thus the whole sequence 1-5) are present in Neocera- todus; numbers 2 and 4 only in Rana, the former to disappear at metamorphosis and the latter by the time the larva is 11 mm long (Edgeworth, 1935, p. 162), though it is still present in my 33 mm specimen. Except in Necturus and Proteus which retain a transversus ventralis 3, only the fourth is developed in Urodela (Edgeworth, 1920).

There are 4 levator branchialis muscles followed by a dilator laryngeus in Anurans (Edgeworth, 1935); 6 in Neoceratodus, the last ones probably including a dilator laryngeus constituent, and 5 levators and a separate dilator laryngeus and trapezius (as in Neocera- todus) in Cryptobranchus and Hynobius (Fox, 1954, 1959).

Four constrictor branchialis muscles are found in Neoceratodus-not 5 as described by Edgeworth, who may have confused the fifth with the posterior levators-and 3 in Rana, though Edgeworth described 4 constrictors. Adductor arcuate muscles 2 and 3 (subarcuales obliquus of Edgeworth) are present in Urodela, which could possibly be the homologues of the constrictor branchiales.

Five subarcuales recti are present in Neoceratodus, but not the fifth in Rana or the first also in Urodela.

Arterial system The arterial system of the head and pharynx of tadpoles of Amphibia is quite fish-like

(Figs 36 and 42, and Fox, 1959, Figs 4 ,9 and 25), and can easily be derived from that of Neoceratodus by selective elimination or minor alteration of existing components (Figs 21, 22,24 and 41). Modification of the gill region, loss of one member of the pair of each of the forked efferent epibranchial arteries, and of the hypobranchial artery, and shortening of the lateral ventral aorta and of the truncus, will, in general transform the larval system of Neoceratodus into that of an Amphibian. Each anterior efferent fork is considered to be the homologue of the comparable single efferent of Rana (Spencer, 1893). Again the relatively minor changes in the structure of the heart of Neoceratodus, like the complete and not partial separation of the auricles in Amphibia, will enhance the performance of the system for double circulation.

Neoceratodus and Amphibia, in their larval arterial systems, thus demonstrate a similar basic segmental pattern (Figs 41 and 42), some of whose components having been modified, or reduced or eliminated in phylogeny, and again particularly in Amphibia in ontogeny, for a more successful adaptation to a terrestrial existence.


Phylogeny of the columella in Urodela from evidence in Neoceratodus

Van der Westhuizen (1961, p. 68) concluded that the majority of previous investigations favoured the view of the non-participation of the hyoid in the development of the sound conducting apparatus of Amphibia (Barry, 1956), and that evidence of hyoid derivation is exiguous.

Nevertheless on comparative morphological grounds he suggested that in anurans the operculum, pars interna and media plectri are of capsular origin, that the pars externa

q; 1

o r n o

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FIG. 41. Diagrammatical scheme of various components of the head and pharynx of the larval Neoceratodus.

plectri and annulus tympanicus are developed from a common blastema derived from the palatoquadrate, and that part of the auditory capsule which incorporates the infrapharyngohyale gives origin to the pars interna and media plectri, as well as the floor of the fenestra ovalis and the otic ledge in adults.

More recently in an experimental analysis in Ambystoma punctatum, Toerien (1963) concluded that the presence of the auditory capsule influences the shape but not the existence of the columella foot-plate, that the latter and the stilus share origin with the visceral skeleton, and that the columella is most likely hyoidal. Both workers surveyed the literature.

The pharyngohyale (Schmalhausen, 1923~) of Neoceratodus comprises supra and

E M B R Y O L O G Y O F N E O C E R A T O D US 539

infrapharyngohyale elements homologous with the lateral commissure in telestomes (Bertmar, 1959, 1962a, 1963). It is the otoquadrate cartilage (Edgeworth, 1923a), and the homologue of a structure incorporated into the floor of the auditory capsule (post-palatine cartilage) of Urodela (Fox, 19636). Thus the columella of Urodela cannot be equivalent to the pharyngohyale of Neocerutodus, as thought by Schmalhausen (1923a), nor to the lateral commissure of teleostomes suggested by Bertmar (1962a), for it coexists in space and time with an otoquadrate cartilage.

The hyomandibula (or epihyale-laterohyale, which is never found in Urodela) of Neoceratodus is considered to be the extra columella or stilus (Schmalhausen, 1923a), or even the columella itself (Stadtmiiller, 1936)-a more plausible view. Nevertheless an

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FIG. 42. Similar scheme as in Fig. 41 of larval Amphibia, especially Urodela (see Fox, 1959). For a more elaborate interpretation of the formation of the jaws and trabeculae, mainly based on palaeontological evidence, see summary bylJarvik (1965, pp. 25-27).

epi-laterohyale of Neocerutodus and a columella of Urodela are each situated lateral to the levator hyoideus and mesial to the depressor mandibulae respectively-muscles which are known to be homologous. If a columella is indeed hyoidal (Kingsbury & Reed, 1909; Marcus, 1910; Gazagnaire, 1932; Edgeworth, 1935; de Beer, 1937), then in Urodela it is either the homologue of a laterohyale extension of the epihyale of Neoceratodus, which chondrifies against the foramen ovale, and in order to fulfil its function as a sound- conducting organ would of necessity need to be situated mesial to the depressor mandibulae; or it is a new formation developed sui generis (Fox, 1963d). That the columella cannot be pharyngohyale in origin would seem to be supported by the results of Stephenson (195 la), according to which in Leiopelma the top of the hyoid becomes the otohyoid ledge, below the auditory capsule, like the otoquadrate cartilage of Neocerutodus.


Bertmar (1959) concluded that the stylohyale of Neoceratodus originated from hyoidal and sub-epidermal blastemata, which together with the epi- latero- cerato- hypo- and basihyale comprise the hyoid. In contrast Fox (1963d) concluded that the stylohyale would seem to develop from the quadrate cartilage as a backgrowth, which becomes incorporated into the hyoid, though because of its topographical situation, it may well have originated from hyoidal tissue.

Examination of the origin, development, structure and topography of the other hyoidal elements in general was found to confirm the results of Bertmar.

Discussion

Many structures of larvae of Urodela and Neoceratodus show similarities (Lists 3, 5). Some of these are, however, illusory as revealed on closer examination. In addition to a number of fundamental differences in the skeleton, vascular, muscular and nervous systems (List 61, differences occur in origin of the pronephric tubules, and further some pronephroi of urodeles, in contrast to those of Neoceratodus and Protopterus, comprise more than two nephrostomial units (Fox, 1962, 1963a). Neoceratodus (11.5 mm to 16 mm long) had a pronephric individual cell volume size range which differed far more from that of Cryptobranchus, a urodele, than from Rana esculenta (Fox, 1960, 1961b). Rudebeck (1945, p. 146) stated that differences between fore-brains of Urodela and Anura are not enough to infer that they have a different phylogenetic history; and thus one should not in this particular instance ascribe preferential relationships between Urodela and Dipnoi.

There are a greater number of body segments in Neoceratodus than in urodeles, and the location of the hind-fin (and girdle) bears no relation to that of compatible elements in Amphibia. It is of interest that the freezing point of blood of adult Neoceratodus is almost the same as that of the frog (Dakin, 1931).

Again urodeles possess a balancer and no operculum, the reverse of the condition in Neocera todus.

Consideration of the main differences between on the one hand larvae of Neoceratodus, and on the other urodeles and Anura, leads to the rejection of the view of a direct ancestry of the Amphibia from Dipnoi.

In List 6 are included differences in: the segmentation number of the head, nasal capsules, teeth, and in Neoceratodus the loss of certain other occipital components, lower branchial cartilage elements, and branchial structures behind the fifth branchial bar (laryngo-tracheal cartilages and vestigal gill clefts, Fox, 1954, 1959), all of which are unlikely to have disappeared to reappear anew in Amphibia.

However, larvae of Neoceratodus, Urodela and Anura have a wide range of characters in common (Lists 3 to 5), which, though many doubtless have evolved in parallel since the Devonian, must surely emphasize a common relationship or derivation. In particular the autostylic jaw suspension, and the practically identical relationships of nerves V and VII and blood vessels to the quadrate processes in Neoceratodus and Amphibia (particularly in the urodeles), platytraby, details of the heart and vascular system and the structure of the brain lend support to this view. If as is likely their rhipidistian crossopterygian ancestors lacked many of these characters-certainly they did not possess an autostylic jaw suspension like Dipterus (Traquair, 1878; Dollo, 1895), though it is foreshadowed in Eusthenopteron (Jarvik, 1954)-then a diphyletic origin would demand their independent


aquisition in Dipnoi and Amphibia, which seems an unlikely possibility. However, if indeed there were a pro-dipnoan-amphibian common stem presumably separation soon occurred, for Porolepis and Dipnorhynchus and the later Osteolepis and Dipterus already exist in the Early and Middle Devonian respectively (Westoll, 1949). The latter worker described a rapid evolutionary shift in Dipnoi of the Devonian, which would account for the presence of the highly developed Dipterus in this period. The Upper Devonian Chirodipterus in particular is astonishingly similar in structure to Neoceratodus (especially young stages), especially in the shape of the skull and of the brain, and in the presence and course of the blood vessels and nerves (Save-Soderbergh, 1952, p. 23). Dipnoans thus have not substantially changed for 300 million years (Jarvik, 1960). Thomson (1963) concluded that apart from some differences in the nasal capsules, between larvae of Neoceratodus on the one hand, and Protopterus and Lepidosiren on the other, the nervous and vascular systems of the snout together with those of Chirodipterus were remarkably constant. Soon after separation from their amphibian kin dipnoan forms presumably radiated into the now-extinct genera, and the three still-living ones (whose skull ossifications are greatly reduced for the chondrocranium is largely cartilaginous), possessing specialized teeth plates and archipterygial fins derived from tribasal rhipidistian paddles (Gregory & Raven, 1941 ; Westoll, 1943~).

Two main views prevail at present on the origin of amphibian tetrapods; that they are monophyletic (Goodrich, 1909, 1930; de Beer, 1937; Westoll, 1943a,b; Stephenson, 1951b; Eaton, 1959; Schmalhausen, 1959; Szarski, 1962; Parsons & Williams, 1963; Reig, 1964; among others), or diphyletic, mainly supported by the Swedish palaeontologists (Save- Soderbergh, 1934, 1935; Holmgren, 1949a,b; Lehman, 1955; Jarvik, 1942, 1960, 1961, 1965). Wintrebert (1922) derived Urodela directly from fishes and Herre (1935) concluded that each amphibian order arose independently from a different group. Jarvik favours a separate origin of urodeles from Porolepiformes, like Porolepis, and Anura from Osteolepi- formes, like Osteolepis or Eusthenopteron, on evidence mainly from comparative morphology of the snout. Kulczycki (1960) however concluded that the main differences in the ethmoid region between Porolepis and Eusthenopteron are due to differences in proportion. Thomson (1962) furthermore concluded that these two groups of rhipidistians are more closely related than Jarvik believes, and that characters which are used to justify separate phylogeny of Urodela and Anura are present in both groups.

Possession of the common characters shared in larvae of Urodela and Anura (List l), which differ in practically every case from comparable ones-when present-in Neo- ceratodus, would therefore require that either these characters evolved within a single amphibian stock, after separation from Dipnoi had occurred, or that pentadactyly, nature of the head segmentation, characteristics of the ear, columella and fenestra ovalis among others, all originated independently in separately evolved amphibian stocks.

The conclusion in the present work that Dipnoi and Amphibia share a common origin- even if it was extremely early in phylogeny and of short duration in terms of geological time-implies a monophyletic derivation of Amphibia, though many differences in structure between adults (Evans, 1944), and larvae of modern Urodela and Anura now clearly separate them into distinct groups (List 2). Yet the head of embryos of the primitive anuran Leiopelma includes many features typical of Urodela (Stephenson, 1951~). There are no rostra1 cartilages, processus muscularis quadratus and its specialized attached jaw muscles, and commissura terminales. A true processus pterygoideus is retained. There

36


is an otohyoid ledge, or floor to the hyomandibular canal, of hyoid origin, which is probably equivalent to the otoquadrate cartilage of Neoceratodus, and part of the floor of the auditory capsule in urodeles (Fox, 1963d). The nasal capsules are widely separated, though a broad internasal septum ultimately develops-also seen in Hynobius-and there is a tectum synoticum, but no taenia tecti medialis. The course of the hyomandibular nerve is more comparable to urodeles than to anurans (Stephenson, 1951b). Furthermore a vestigial fifth ceratobranchiale is present, a feature seen to occur, though rarely, in Pleurodeles (Signoret, 1956). Pusey (1943) has also shown Ascaphus to possess features in common with urodeles. Leiopelriia in its slow intracapsular development shows little of the extreme specialization of anuran tadpoles, seen in Rana.

Stephenson concluded that this direct development, similar to that of urodeles, is the primary mode, and that the anuran tadpole stage and striking metamorphosis, or indirect development, are derived from it.

In adaptation to a suctorial method of feeding the larval Rana possesses an elaborate specialized skeleton, musculature and nervous system in the head and pharynx, developed from a more primitive unspecialized condition, represented in Leiopelma and caducibranch urodeles. Many of the character differences of List 2 can be accounted for on this hypo- thesis.

It is therefore suggested that a common pro-Dipnoan-Amphibian stock originated from early rhipidistian crossopterygians in the lower Devonian, and soon separated into two streams. The first has practically disappeared and is merely represented by the three genera of living Lung-fishes. The second stream radiated into various Amphibia throughout the Devonian and Carboniferous ; the modern forms no doubt arising in the Jurassic (A. Nevo, 1956; E. Nevo, 1964; Griffiths, 1956; Hecht & Estes, 1960), or even earlier for the Salientia in the lower Trias (Griffiths, 1963). In larvae of Neoceratodus, Urodela and Anura the overall basic patterns of various morphological component systems are fish-like and similar. Each comparable system in the three groups has evolved independently, within its own milieu, showing a greater or a lesser degree of specialization. The sum total of these changes gives rise to the modern forms, and has resulted in the promotion of the pronounced phylogenetic divergence between larvae of Anura and Urodela, with an apparent and somewhat lesser divergence between Urodela and Neoceratodus, so that in some respects, superficially at any rate, they have evolved in parallel.

It is the relative stability of form of these groups rather than their changes that is so impressive, for despite the long period of hundreds of millions of years when highly organized amniotes dominate the vertebrate landscape, living larvae of Dipnoi and Amphibia bear witness to their extremely ancient heritage.

List I . Main cltaracters in coninion in larvae of Urodela and Anura

I . Head segmentation: 6 segments to the head. 2. Autostylic jaw suspension (though this feature is

3. Pentadactyly. 4. Position of the trabecular horns: ventral to the

external nares. 5. Columella auris. 6. Fenestra ovalis in lateral wall of avditory capsule.

found in Neoceratodus).

7. Medial wall of cartilage and foramina to the

8. Nerve IX emerges from the brain behind auditory

9. Ganglia IX and X fused together.

auditory capsule.

capsule, with nerve X.

} Szarski (1962) 10. Similarity of skin structure. 1 1 . Similarity of pelvic girdles. 12. Structure and mode of development of the lachryinal

13. Structure and arrangement of the heart, pharyngeal duct.

and head arterial system.

E M B R Y O L O G Y O F N E O C E R A T O D U S

List 1-continued 7. Primitive double circulation.

543

14. 15.

16. 17.

1.

2.

3.

4.

c

Basic pattern of the pronephric system. Paired occipital condyles, odontoid process and cranio-vertebral joint. Presence of respiratory post-branchial cartilages. Similarity in structure of the lungs.

List 2. Main characters which differ in larvae of Urodela and Anura

Supra and infra-rostra1 cartilages in Anura (though not in Leiopelma). Median nasal septum (Anura); separate medial walls to nasal capsules. (Urodela), though not in Amphiuma (Higgins, 1920). Processus muscularis quadratus of the quadrate cartilage and its transformation (Anura). Shape and arrangement of Meckel’s cartilage and the hyobranchial skeleton.

J. No sign of the otoquadrate cartilage in Anura

6. Absence of basicranial fenestra (Anura). 7. Presence of annular tympanic ring (Anura). 8. Precocious development of sclerotic cartilage

9. Absence of tracheal cartilage, only arytenoids in

(except Leiopelma).

(Urodel a).

Anura (Edgeworth, 1920, p. 126). 10. Position of the profundus-palatine anastomosis. 11. Arrangement of the nerves V and VII. 12. Differences in intimate form and structure of

pronephros.

musculature of the head and pharynx.

(Anura).

13. Differences in arrangement and content of the

14. Shortened body and reduced number of vertebrae

15. Segmental position of the hind limb elements. 16. Balancers present (Urodela). 17. Opercular cavity (Anura). 18. Post-notochordal tail in Urodela (Percy, 1962). 19. Dramatic metamorphic climax in Anura.

List 3. Main characters in common in larvae of Neoceratodus Anura and Urodela

1. Autostylic jaw suspension. 2. Platytrabic chondrocranium. 3. Relationship of nerves V and VII and blood vessels

to the processes of the quadrate cartilage. 4. Pharyngohyale (otoquadrate) fused to the basal

plate below the auditory capsule (Neoceratodus): incorporated in capsule floor (Urodela); equivalent to the otohyoid ledge (Leiopeha).

5. Internal and (external) nares. 6. Pulmonary artery (on each side) from efferent

artery 4, to air-sac or lung, whose inner surface is divided into alveoli.

8. Posterior vena cava. 9. Anterior abdominal and renal portal veins.

10. Larynx originates as a median ventral outgrowth of the pharynx.

11. Paired cerebral hemispheres. Similarity in ontogeny and morphology of telencephalon (Rudebeck, 1945).

12. Loss of certain components of at least two metotic somites.

13. Pronephros and mesonephros of Neoceratodus and Amphibia (especially Urodela) are generally similar in appearance and development.

14. Size of cells (but pronephric cell size of Crypto- branchus japonicus is much larger than that of other Amphibia and Neoceratodus).

15. Closed spiracular gill cleft. 16. Fore-limb (or fore-fin) elements originate in similar

region of body segments. 17. External gill filaments.

List 4. Main characters in common in larvae of Neoceratodus and Anura in addition to those

of List 3 1. Common medial nasal septum (but note Amphiuma). 2. Absence of basicranial fenestra. 3. Aspects of pharyngeal musculature, i.e. levator

hyoideus and retractor mandibulae (Neoceratodus), equivalent to the orbitohyoideus and quadrato- hyo-angularis (Anura). Constrictor branchiales muscles.

4. Opercular fold covers gill region.

List 5 . Main characters in common in larvae of Neoceratodus and Urodela in addition to

those in List 3 1. Overall shape of larva, including long body and tail. 2. Overall shape and arrangement of chondrocranium

3. Precocious development of sclerotic cartilage (from

4. General arrangement of cranial nerves. 5. Fore-fins (Neoceratodus) and fore-limbs (Urodela)

supplied by occipital and/or spinal nerves from head segments 9-1 1 inclusive.

6. Similarity of chromosome structure of the cells (Wickbom, 1945).

7. Commonly two nephrostomial tubules and nephro- stomes to the pronephros.

and hyobranchial skeleton.

3 centres of chondrification).

List 6 . Main differences recognized between larvae of Neoceratodus and Amphibia (Urodela and Anura) 1. Head segmentation: 6 segments in Amphibia; 9 in

2. Early development of fused teeth plates in Neo- Protopterus; 10 in Neoceratodus.

ceratodus.


List 6-continucti

ceratodus).

goideus in primitive Urodela and Leiopeha.

margin of the auditory capsule (Neoceratodus).

3. Nasal capsules (very highly fenestrated in Neo-

4. Complete (or almost complete) processus ptery-

5. Situation of foramen jugulare: in the ventro-lateral

6. Labial (subnasal) cartilages in Neoceratodus. 7. Occipital region. 8. Notochord unconstricted and surrounded by a thick

fibrous sheath, and the vertebrae have no centrum (Neoceratodus).

9. Complete cartilaginous roof to the skull (Neo- ceratodus).

10. Great reduction in the number of head ossi6cations (Neoceratodus).

1 1 . Hyoid arch includes extra dorsal elements (Neo- ceratodus).

12. Columella auris and:operculurn in Amphibia. 13. Foramen ovale in auditory capsule of Amphibia. 14. No medial wall or perforate foramina to auditory

15. Laryngo-tracheal cartilages in Amphibia. 16. Loss of certain ventral components of the branchial

skeleton and possession of dorsal epibranchialia (Neoceratodus).

capsule in Neoceratodus.

17. Five branchial bars and gill clefts (Neoceratodus).

18. Archipterygial fins in Neocerutodus and pentadactyl limbs in Urodela and Anura.

19. Single twisted air bladder (though paired in other Lung-fish) in Neoceratodus.

20. Aspects of the arterial system. 21. Lateral line organs in grooves (Neocerutodus), but

on the surface of the body in larvae of Amphibia. 22. Arrangement and origin (in detail) of the pronephric

tubules (Fox, 1962). 23. No profundus-palatine anastomosis, mesially to the

nasal sac in Neocerafodus up to 35 mni long but present in Amphibia.

24. Close association between rami nasalis internus profundus V and superior ophthalmicus facialis VII, within the nasal capsule (Neoceratodus).

25. Ganglia IX and X separate in Neoceratodus. 26. Nerve IX emerges from the skull through a separate

foramen jugulare, and nerve X emerges behind the auditory capsule in Neoceratodus. Both nerves emerge behind the auditory capsule in Amphibid.

27. Location of the hind-fin (or hind-limb) elements is in different numerical segments in all groups.

28. Spiral valve in intestine of Neocerutodus. 29. Metamorphosis in most Amphibia with loss of

lateral line organs, closure of gill clefts and reduction and reorganization of the hyobranchial skeleton.

Summary

A study was made of the structure of the head and pharynx of larvae of Neoceratodus 11.5 to 34.5 mm long, and Rana teriiporaria and R . esculenta 33 mm and 26 mm long respectively, from transverse microscopic serial sections.

Morphological structures considered in some detail include the neuro- and splanchnocranium, musculature, vascular system, cranial, anterior occipital and spinal nerves. Results were compared with those of previous work in larvae of Urodela.

Some of the more important, and in some cases newly considered, homologies among the various components include : (a) Levatores mandibulae anterior and posterior belong to the premandibular and mandibular head segments respectively. (b) Ceratohyoideus internus is the equivalent of transversus ventralis 1. (c) Retractor mandibulae of Neo- ceratodus is equivalent to the quadrato-hyo-angularis of Rana. (d) Levator hyoideus of Neoceratodus is equivalent to the depressor mandibulae of Urodela, and the orbitohyoideus of Rana. (e) Otoquadrate cartilage of Neoceratodus is the homologue of the pharyngohyale (or at least the top of the hyoid) of fishes; the mesio-ventral floor of the auditory capsule or post-palatine cartilage of Urodela, and the otoquadrate ledge of Leiopelma. (f) Epi- laterohyale of Neoceratodus may be the equivalent of the columella of Urodela : alterna- tively the latter cartilage may originate sui generis. ( g ) The stylo-hyale of the hyoid of Neoceratodus seems to originate from the hind-surface of the quadrate cartilage. (h) Occipito-spinal components of Neoceratodus, Urodela and Anura are tabulated in order to compare their equivalences in phylogeny. In terms of loss of some of these components Neoceratodus is more specialized than amphibians. (i) The stapedial artery of


Neocerutodus (and tetrapods) is considered to be the homologue of a pretrematic efferent epibranchial artery of the hyoid artery, whose post-trematic vessel is represented by a hyoidean (opercular) artery. (j) The ophthalmica magna artery is considered to be a relic of the efferent epibranchial artery of the premandibular segment, situated in front of the mandibular artery of the second head segment. (k) The arteria centralis retinae (optic artery) is considered to be equivalent to either the whole of part of the front of the lateral dorsal aorta.

In Neoceratodus there is no median wall to the auditory capsule, neither is there a foramen ovale nor columella. Nerve IX, whose ganglion is separate from that of the vagus, emerges from the brain through a separate foramen jugulare in the latero-ventral wall of the auditory capsule. In contrast in Amphibia ganglia IX and X are closely apposed, and their nerves share a common foramen behind the auditory capsule.

Differences and similarities of various characters of Neocerutodus, Urodela and Anura have been listed. On the basis of such larval comparisons it is considered that Dipnoi and the two amphibian groups share a common origin: reference to fossil history suggests that separation soon occurred in the early part of the Devonian. Such a view implies a monophyletic origin of Urodela and Anura.

Though structural affinities between Neocerutodus and Urodela are recognized, many putative similarities are not as close as some have formerly believed. All groups have diverged from one another in evolution-Anura in particular-and the apparent closer relationship between Neocerutodus and Urodela may be ascribed to a quasi parallel phylogenetic development of particular morphological components.

It is a pleasure for me to record my appreciation to Mrs Kirkham-Jones, who supplied me with specimens of Neoceratodus from the J. P. Hill Collection, lodged in the Department of Embryology, University College, London; to Professor M. Abercrombie for reading parts of the manuscript and for the generous facilities provided in the Department of Zoology; and to Dr K. S. Thomson, now at Yale, and Dr G . Bertmar of Stockholm, for the stimulating conversations on tetropod phylogeny.

My warm thanks are also due to Mr H. Barker for his technical assistance, and to Mr C. Atherton, who prepared the admirable photomicrographs of the plates.

K E Y T O PLATE A N D F I G U R E LETTERING

a.arc.2,3

a.c.c.a. a.e.a.1,2,3,4 a.1.d.a. a.na. au . a.v. b s . b.p. b.r.b.VI1 b.r.0.p.V

bhy. br. 1-5

8 . C .

adductor arcuate muscles 2,3 auditory capsule anterior carotis cerebralis artery afferent epibranchial artery 1 4 anterior end of lateral dorsal aorta anterior naris auricle of heart auditory vesicle buccal cavity basal plate branch of ramus buccalis facialis branch of ramus ophthalmicus profundus V basihyale branchiale 1-5

c.VII-IX

c.VII-x

c . VII-IX-x

c.VII-1Xe

c.a. c.arc.l-4 c .b .14 c.c.a. ce. cebr.1-5 ce.ext.

Connective between ganglia of facialis and glossopharyngeus nerves Connective between ganglia of facialis and vagus nerves Connective between ganglia of facialis, glossopharyngeus and vagus nerves excised end of facialis-glossopharyngeus Connective columella auris constrictor arcuate muscles 1-4 constrictor branchialis muscles 1 4 carotis cerebralis artery centrum of vertebra ceratobranchiale 1-5 ceratohyoideus externus muscle

546

cehy. mint .

c0.a. c.p. c.q.a. c.q.p.

~0.b.1-5 C0.t. con. cop. C.S.

C.t. cr.t. d.a. d.c. d.o.sp.n.l,2 d.1. d.m.

d.r.0.p.V

e.a.a.1 e.a.p.1 e.a.s.1 e s . e.col. e.e.a.l-4 e.g.f.l-4 e.n.v. ebr.14 ehy. ex.n. eye f.b. f.g. f0.a. f0.a.c.

fo.ap. f0.f. f0.g. f0.h. fo.hy. fo.na. fo.n.cap. fo.0c. fo.01. fo.om. fo.0p. fo.0v. f0.p. fo.p.0.

co.

H A R O L D F O X

ccratohyale ceratohyoideus internus muscle conus arteriosus coeliac artery crista parotica commissura quadratocranialis anterior commissura quadratocranialis posterior coracobranchialis muscles 1-5 commissura terminales condyle copula columella stilus cornu trabecula crista trabecula dorsal aorta ductus Cuvierii dorsal root occipito-spinal nerves 1,2 dilator laryngeus muscle depressor mandibulae (digastricus) muscle dorsal branch of ramus ophthalmicus profundus V efferent epibranchial anterior artery 1 efferent epibranchial posterior artery 1 efferent epibranchial superior artery 1 epiphysial cartilage ethmoidal column efferent epibranchial arteries 1-4 external gill filaments 1-4 external nasal vein epibranchiale 1 4 epi hyale external naris eye cavity fore-brain fore-gut foramen anterior foramen of medial wall of auditory capsule foramen apicale foramen facialis foramen glossopharyngeus (jugulare) foramen hypoglossus foramen hypophyseos foramen narina foramina of nasal capsule foramen oculomotorius foramen olfactorius evehens foramen for ophthalmica mama artery foramen optica foramen ovale foramen for pituitary vein common foramen for pituitary vein and ophthalmica magna artery

fo.pa. fosp. f0.sp.m. fo.tr. g.c.1-8 ga.V,VII,VI11, IX,X ga.V-V1 I ga.lXe

ga.Xe ga.0.sp.n. 1,2 ga.p. ga.sp.n.1-3 gco. ghy. h.a. h.a.c. h.b. h.n.1,2,3 h.p. hd.a. ht. hy. hy.a. hybr. 1-3 hWw. i.c.a. inis. in.111

in.lV

in.IX

in.n. inh. int. int.a. int.p. ir.c. 1. 1.c.v. I.cap.

1.d.a. 1.1.0.

1.m.a. I m p . 1.m.p.p.

1.m.p.s.

1.o.n. 1.s.n.X

foramen palatinus foramen sphenoticus foramen sphenoticus minus foramen trochlearis gill clefts 1-8 ganglia tigeminus, facialis auditory, glossopharyngeus and vagus trigemino-facialis ganglion excised end of glossopharyngeal ganglion excised end of vagus ganglion ganglia of occipito-spinal nerves 1,2 praeoptic ganglion ganglia of spinal nerves 1-3 geniocoracoideus muscle geniohyoideus muscle hyobranchial artery hind end of auditory capsule hind-brain hypoglossal nerves 1-3 hypobranchial plate hyoid artery heart hyoid arch hyoidean artery hypobranchiale 1-3 hypohyale internal carotid artery intermandibular cartilage insertion of oculomotor nerve in mid- brain insertion of trochlear nerve in mid- brain insertion of glossopharyngeal nerve in hind-brain internal naris interhyoideus muscle intermandibularis muscle intermandibularis anterior muscle intermandibularis posterior muscle infrarostral cartilage lung lateral cardinal vein lateral (and ventral) margin of nasal capsule lateral dorsal aorta lateral line organ levator mandibulae anterior muscle levator mandibulae posterior muscle levator mandibulae posterior profundus muscle levator mandibulae posterior superficialis muscle lamina orbito-nasalis lateralis superior vagus nerve


I.V.S.

le. lev.br.1-6 lev.hy. Ihy. Ix. m.a. m.b. 1n.c. m.1. m.m. m.0. m.p.c. m.v. ma.c. med.c. med.w.c. n.II,llI,lV,VI, v I I, I XI x n.111 s.r. n.111 i.r. n.c. n a p . n.cap.f.,m.,r.

n.f. ns . n.se. nsp. 1-3 n.sp.occ.sp.a.2

n.v.s. n.a.1-3 na.c. not. 0.a. 0.1.

0.m.a. 0.n. o.sp.n.l,2 O.V. O.V.S. 0cc.a. occ. sp.a.l,2 0cc.v. OP. 0p.a. 0rb.c. orh. 0t.c. p.a. p.a.q. p.b. p.b.p.

lateral venous sinus lens of eye levator arcus branchialis muscles 1-6 levator hyoideus muscle laterohyale larynx mandibular artery mid-brain Meckel's cartilage mandibulo-labialis muscle masseter muscle mouth opening Meckel's procartilage mandibular vein mandibular cartilage medial region of auditory capsule medial wall of auditory capsule optic, oculomotor, torchlear, abducens, facialis, glossopharyngeus and vagus nerves superior ramus of oculomotor nerve inferior ramus of oculomotor nerve nerve cord nasal capsule floor, medial wall and roof of nasal capsule narial funnel nasal sac nasal septum neural spines of vertebrae 1-3 neural spine to occipito-spinal vertebral arch 2 nasal venous sinus neural arches 1-3 narial canal not ochord occipital artery olfactory lobe ophthalmica magna artery olfactory nerve occipito-spinal nerves 1,2 orbital vein orbital venous sinus occipital arch occipito-spinal arches 1,2 occipital vein operculum optic artery orbital cartilage orbit ohyoideus muscle otoquadrate cartilage processus ascendens pars articularis quadrati processus basalis presumptive basal plate

p.c.c.a. p.cehy. p.cop. P.C.S. P.C.V. p.fo.01 p.hyphy. p.1. p.1.m.a.

p.m.q. p.na. p.0. p.0cc.a. P.P. p.p.c. p.p.j.

p.p.0. P.Pt. p.q.e. p.re. p.t. p.v. p.v.a. P.V.C. p.v.1. p.v.r. p.2.n.a. 1-4

phx. phy. p1.t. pr. pr.c. pre.2.n.a. 1,3 prv. pu1.a. pv.t. q.c. q.h.a. 4.P. 9.p.c. r.1,2 r.3.4 r.al.Vl1 r.b.VI1 r.b.VI1-d.p.V

r.c. r.d.p.V

r.dg.

posterior carotis cerebralis artery process of ceratohyale post-copula postcardinal sinus post-cerebral vein presumptive foramen olfactorius presumptive hypohyale pars laryngeus profundus branch to the levator mandibulae anterior Processus muscularis quadratus posterior naris processus oticus preoccipital arch pila prootica post-palatine cartilage junction of processus pterygoideus and trabecula cranii pila preoptica processus pterygoideus processus quadratoethmoidalis pars reuniens pars trachealis pituitary vein posterior ventral aorta post-caval vein (posterior vena cava) pulmonary vein (left side) pulmonary vein (right side) post-zygapophyses of neural arches 1-4 pharynx pharyngohyale planum tectale pronephric tubules precardial cartilage prezygapophyses of neural arches 1,3 prevomer pulmonary artery prevomerine teeth quadrate cartilage quadrato-hyo-angularis muscle quadrate process quadrate procartilage ribs to occipito-spinal arches 1,2 ribs to neural arches 1 2 ramus alveolaris facialis ramus buccalis facialis ramus of buccal nerve and deep profundus (of r. nasalis externus profundus V) rectus cervicis muscle deep profundus nerve of ramus nasalis externus profundus V ramus from Connective VII-IX to digastricus muscle

548

r.fo.sp. r.h.Vll r.hy.VJ1

r.in.V r.in.a.V r.in.p.V. r.j.Vl1 r.ni.V r.m.V-Vl1

r.ma.V r . nid. i . V rman. r.mand.V r.max.V r.m.e.VI1 r.m.i.V

r.m.i.VI1 r.m.int.V r.m.int.VII r.m.md.V r.m.p.V

r.m.pal. r.n.a.2,3 r.n.cap. r.n.e.V r.n.i.V r.0.p.V r.p.lX r.pal.Vl1 r.pa1.p.V r.ph.IX r.p.m.VI1

r.p.p.V

r.p.pal. r.pre.lX r.s.o.VI1 r.s.o.VIle

rect .int . ,cxt .,

roof of foramen sphenoticus ramus hyomandi bularis facialis ramus hyomandibularis posterior facial is ranius intcrmandibularis V ramus intermandibularis anterior V ramus intermandibularis posterior V ranius jugularis facialis ramus mentalis V common trunk of rami mentalis V and mentalis cxternus facialis ramus to masseter muscle ramus mandibularis internus V retractor mandibulae muscle ramus rnandibularis V ramus maxillaris V ramus mentalis externus facialis rainus mandibularis internus V ( I 1.5 mm Neocerutodus) ramus mentalis internus facialis ranius rnandibularis interior V ramus mentalis interior facialis ranius maxillo-mandibularis V ramus of maxillary nerve to ramus palatine facialis ramus maxillo-palatine ribs of neural arches 2,3 roof of nasal capsule ramus nasalis externus profundus V ramus naralis internus profundus V ramus ophthalmicus profundus V ramus post-trematicus IX ramus palatine facialis ramus palatine-profundus V ramus pharyngeus IX ramus of palatine nerve to ranius niaxillaris V ramus of r. nasalis internus profundus V to palatine nerve ramus profundus-palatine ramus pretrematicus 1X ranius superior ophthalniicus facialis excised end of ramus superior ophthalmicus facialis rectus internus, externus, inferior and

inf.sup. s.a. s.r.1-5 S.V.

sc.c. ~c.c. 1,2,3 sc.c.r. shy. som. sp.c. sp.cebr.14 sp.n.1-3 srx. sub.a. t.X t .c. t.c.X t.co.X

t.inf. t.1.p.X t.ni.p. t.p. t.r.p. t.r.c.X t.S. t.t. t.t.X

t . t .m. thor.

t r. v.2-5 u.1.c. v.a. v.b.n.1-5 V.C.I.

v.g.c.8-lO v.1.r.

v.ph. 1,2 v.pre. 1,2 v.post. 1-4 v.r. ve.

H A R O L D F O X

R E F E R E N C E S

superior muscles stapedial artery subarcuales recti muscles 1-5 sinus venosus sclerotic cartilage incipient sclerotic cartilages 1-3 sclerotic cartilaginous ring stylohyale somite sphenoseptal commissure spines to ccratobranchiale 1-4 spinal nerves 1-3 supra-rostra1 cartilage subclavian artery truncus intcstino-accessorius X trabecula cranii truncus cardiac X truncus division to coracobranchialis musculature truncus infraorbitalis truncus laryngeus posterior X taenia marginalis posterior trabecular plate truncus division to palatine ncrve truncus division to rectus cervicis tectum synoticum tectum transversum truncus division to transversus ventralis musculature 4 and 5 taenia tecti medialis thoraciocohyoideus muscle (= rectus cervicis) transversus ventralis muscles 2-5 upper labial cartilage ventral aorta vagus branchial nerves 1-5 vena capitis lateralis (head vein) vestigial gill clefts 8-10 vagus rami to laryngeal and oesophageal musculature vagus pharyngeal nerves 1,2 vagus pretrcmaticus nerves 1,2 vagus post-trematicus nerves 1-4 vestigial rib ventricle of the heart

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Early development of the head and pharynx of Neoceratodus with a consideration of its phylogeny

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