The Cranial Characters of the Brevicipitid Genus Cacosternum...

The Cranial Characters of the BrevicipitidGenus Cacosternum (Boulenger).

By

C. G. S. de Villiers, M.A., Ph.D.,Professor of Zoology, University of Stellenbosch, South Africa.

With 12 Text-figures.

THE present paper is a continuation of my work on thecranial characters of the two South African Brevicipitid generalacking the claviculo-procoracoidal arch in the pectoral girdle.The genus P h r y n o m e r u s (Noble) was discussed in a previouspaper in this Journal (vol. 73), to which the reader is referred fordetails of technique, which was, however, slightly varied forpurposes of the present research, inasmuch as double bulk-staining was resorted to. The nuclear stain, haemalum, wasapplied in the usual way, and after all traces of alum used fordifferentiation were washed out, the object was bulk-stainedfor twenty-four hours in a strong aqueous solution of Bismarckbrown and differentiated in ordinary tap-water for forty-eighthours. I have not yet experimented with bulk-staining for con-nective tissue and muscle; stains recommended for this purposeare fuchsin and light green or eosin respectively. The use ofvan Gieson in conjunction with Bismarck brown is consideredby many workers to lead to confusing results, so that purefuchsin is recommended for connective tissue and for decalcifiedbone. All material was decalcified with Ebner's solution inpreference to nitric acid, which is, however, used with greatsuccess for the same purpose by Professor Stadtmiiller ofGottingen, according to a personal communication from him.The material of C a c o s t e r n u m b o t t g e r i was kindly sup-plied by the Director of the Transvaal Museum; C a c o s t e r n u mc a p e n s e was collected by the author on the StellenboschFlats after the first rains in May 1928. The eighteen speci-mens collected are the only ones known besides the type

276 C. G. S. DB VILLIBRS

specimens collected by Mr. Eose of Cape Town. Three speci-mens of C a c o s t e r n u m n a m a q u e n s e were collected byDr. Herre of Stellenbosch University during the phenomenalNamaqualand rains of 1929; but owing to the rarity of thematerial, this species was not microtomized. Mr. Hewitt hasrecently upheld the species and recorded the existence of twospecimens referable to it in the collection of the South AfricanMuseum.

REVIEW OF THE EXISTENT LITERATURE ON THE GENUS.

The genus C a c o s t e r n u m was first described by Boulenger(1887, page 51). The new genus was referred to the Engyosto-matidae and the following osteological details were enumeratedas being characteristic of it: palate toothless, without dermalridges; tympanum hidden; no procoracoids; coracoids slender;sternum extremely small, cartilaginous; diapophyses of sacralvertebrae strongly dilated. The presence of strong subarticulartubercles of the fingers and toes, also present in P h r y n o -m e r u s , was mentioned. The first South African species to bedescribed was C. b o t t g e r i in Boulenger's catalogue of 1882,where it is referred to as A r t h r o l e p t i s b o t t g e r i (p. 118).Werner (1910) described a new species of C a c o s t e r n u m ,C. n a m a q u e n s e . Boulenger (1906-9) first called C. b o t t -ge r i by the name now generally used. No cranial charactersare mentioned in this work. Valuable osteological data aresupplied by Hewitt (1911) from which I select the following:(p. 215) 'maxillary and premaxillary teeth present, no vomerineteeth, palate without dermal ridges, tympanum hidden. In theskull a fronto-parietal foramen is present and the fronto-parietals are but feebly ossified'. Hewitt then regarded Caco-s t e r n u m as allied to the Dyscophids, on account of thepresence of teeth. Andersson (1911) merely notes the occurrenceof P h r y n o m e r u s and C a c o s t e r n u m in British EastAfrica, where the Swedish Zoological Expedition made a collect-ing tour in 1911. Methuen (1913, p. 123) classifies C. b o t t -ge r i under the sub-family Dyscophinae of the Engyostomatidae,probably on account of the presence of teeth on the maxilla.No cranial characters are mentioned. Hewitt (1919) discusses

CRANIUM OF CACOSTERNUM 277

in detail the affinities of the Cacosternum-Anhydro-phryne group (pp. 184r-7) and concludes that the absenceof procoracoids is of greater importance than the presence ofmaxillary teeth and stresses the affinities with the MalagasyDyscophids. The presence of a fronto-parietal fontanelle inBreviceps and Cacosternum is not considered by the authoras of great systematic importance. That part of Noble's work(1922) dealing with Cacosternum and its allies is of extremeimportance, as it discards the toothed ' Dyscophidae' as anindependent family and classes them with allied toothless formsunder the new family Brevicipitidae. Noble's paper of 1924contains interesting speculations on the origin of the EthiopianBrevicipitidae, which are referred to the older African faunawhich flourished when the mainland was still connected withMadagascar (pp. 277 and 278), and suggests possible affinitiesbetween the Cacosternum-Anhydrophryne group andthe Malagasy Anodonthyla, the affinities of which genusare further discussed by Noble (1926, pp. 2-4), the conclusionarrived at being that Anodonthyla is derived from a formwith divided, dentigerous vomer. In 1926 Hewitt contributedvaluable information regarding the morphology and systematicsof the genus Cacosternum: C. capense, the new Capespecies described by the same author in 1925, was shown topossess a divided coracoid, which may be of great value in acomparison of Cacosternum and Phrynomerus . Wer-ner's species (1910) of C. namaquense was upheld and foundto be allied to C. capense, from which it differs mainly inbeing toothless. A new sub-species of C. bot tger i , C. bot t -geri a lbiventer was described. C. namaquense, ofwhich Werner's specimens were supposed to be the only onesextant, was rediscovered by Dr. Herreat IKoeboes, Eichtersfeld,Namaqualand. The three specimens collected in October 1929agree in every detail with those described by Werner, whocollected them at Steinkopf. The new specimens are in theDepartment of Zoology of the University of Stellenbosch. Noble(1926 a, p. 4) again refers to the possible relationship of Caco-sternum and Anhydrophryne, and of the latter genus withthe genera Arthrolept is and Ar throlepte l la , without,

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278 C. G. S. DE VILMBRS

in the opinion of the author of this paper, making good his point.Nieden (1926, p. 11) groups Cacosternum under the Engyo-stomatidae and is therefore not aware of the discovery ofmaxillary teeth in the genus by Hewitt (1911). Power publisheda paper dealing with Cacosternum in 1927. On p. 250 hecomes to the remarkable conclusion that ' Cacosternum hasbufonid affinities', but bases his argument solely on the patternof the chitinous tooth-rows and the position of the anus. Thepresent author published a paper (1929 a) on the macroscopicdevelopment of C. capense, whose spawn and larvae areextremely common round Stellenbosch, and is of opinion thatthe larvae are in appearance and in habit as unlike Bufo larvaeas they possibly can be, and resemble much more closely thoseof the genus Pyxicephalus . Mr. Rose, the discoverer ofC. capense, gave a preliminary account of its habits andlife-history in 1926 (p. 437). The latest paper up to date, refer-ring to Cacosternum, is that of Noble (1927, pp. 116 and117), in which the following conclusions are reached: (1) Thepectoral girdles of Cacosternum and Phrynomerusagree closely; (2) the larvae of the former genus are ranid andunlike those of Phrynomerus ; (3) Anhydrophrynewas evolved from Arthrolepte l la , from which it differs bythe absence of a clavicle; (4) the close relationship of Caco-sternum and Anhydrophryne is stressed; (5) Caco-sternum is possibly also derived from Arthrolepte l la butis in any case ' closely related to ranids and not to other Brevici-pitids'. In a paper read before the British Association at theCape Town Session, the author of this paper has fully describedthe non-aquatic life-history of Arthroleptel la and hasproved that the genus is perfectly ranid. Contrary to whatNoble presupposes, it has no clavicle, but a procoracoid only.It was suggested that Arthrolepte l la , Cacosternum,and Anhydrophryne might have to be removed to theRanidae.

RESULTS OF OWN INVESTIGATIONS.

It is proposed in the following account to discuss chiefly thosefeatures of the cranial characters of the genus Cacosternum


in which it differs from P h r y n o m e r u s , the other SouthAfrican genus lacking a procoracoid. The following descriptionapplies in the main to C a c o s t e r n u m c a p e n s e : the dif-ference between it and the smaller species, C. bb ' t tge r i , willduly be noted. C. n a m a q u e n s e Avas not sectioned as thematerial is too rare.

THE OLFACTORY CAPSULE.

Both cartilagines praenasales are present as in P h r y n o m e -rus ; the superior is short, the inferior long and flexed beneaththe solum nasi, and forms the main support for the premaxilla.It is imbedded in the tubules of the large glandula intermaxil-laris. The same conditions prevail in 0 . b o t t g e r i . The twovestibular 'Wiilste' are both present and the plica obliqua isblunt and short and suspended from the cartilago obliqua asin P h r y n o m e r u s , not from the tectum nasi as in E a n a ;the same applies to C. b o t t g e r i . The recessus sacciformis,described by Gaupp for K a n a, was found to be absent inP h r y n o m e r u s . In C a c o s t e r n u m it is, however, present,but its anatomical relations are not the same as in E a n a .Gaupp described the organ on pages 625 and 633 of the thirdvolume of the ' Anatomie des Frosches' (1904). On page 625 weread: 'Der Wulst [i.e. the one taking the place of the cartilagoalaris] ist von unten und hinten her gewissermassen unter-miniert durch den Becessus sacciformis, der hinten in dieVestibularnische tibergeht, medial- und ventralwarts mit demInfundibulum und dem Cavum medium zusammenhangt.'Additional details are furnished on p. 633: 'Lateral von diesemWandwulst stiilpt sich ein schlaffwandiger Schleimhautblind-sack, der Recessus sacciformis, nach vorn und oben hin vor, derseinen Ausgang von der erwahnten Kommunikationsspalte undim Anschluss daran (nach vorn hin) auch noch von der lateralenKante des Cavum medium nimmt.' In P h r y n o m e r u s anevagination of the infundibulum and cavum medium is absent,but a sac-like recess is present in C a c o s t e r n u m , althoughit does not undermine the large' Wulst', is short and wide insteadof high and narrow as in R a n a (see Gaupp, loc. cit., fig. 140,p. 627), and does not communicate with the vestibule. The

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280 C. G. S. DE VILLIEBS

recessus in C. capense is figured in Text-fig. 1, from whichit will be seen that it originates from both infundibulum andcavum medium; it does not represent the point of communica-tion of the ductus nasolacrimalis with the cavum medium, as the

TEXT-FIG. 1.

blv

s nTransverse section through the three narial cavities of the left side in

C a c o s t e r n u m e a p e n s e . bl.v., blood-vessel; cv.i., cavuminferius; cv.m., cavum medium; cv.p., cavum principale ; gl.imx.,glandula nasalis intermaxillaris; g.n.l., glandula nasalis lateralis;inf., infundibulum; l.if., lamina inferior cristae intermediae;l.sp., lamina superior cristae intermediae; rc.m., recessus medialis;r.sc, recessus sacciformis; s.n., solum nasi; s.o.c, side of olfactorycapsule; spmx., septomaxillary.

latter receives the duct at its blind, lateral division, after therecessus sacciformis has disappeared from sections. It will beseen from the figure that the recess is surrounded by the septo-maxillary bone, which forms a capsule for it. In C. b o t t -geri the recess has exactly the same disposition as in 0.capense .

In P h r y n o m e r u s two remarkable prechoanal sacs weredescribed (loc. cit.); they were shown to be derived from anunpaired prechoanal sac in the young form. The apparatus iseasily derived from a fusion of the two ' Gaumenleisten' (Gaupp)or palatal ridges. In Cacos t e rnum, Text-fig. 2, there is an


unpaired preohoanal sac as in the young Phrynomerus , butthe choanae no longer open into, but just beyond it. In C.bottgeri the sac was filled with dense mucous material.

The premaxilla and maxilla have the usual relationswith neighbouring structures, but are not separated palatallyby the ventrally flexed crista subnasalis as in Phrynomerus .They are moreover toothed: the teeth consist of a functional

6c c

Transverse section through the head o f C a c o s t e r n u m c a p e n s ein the anterior region of the olfactory capsule, bc.cv., buccal cavity;cr.sb., criata subnasalis; g.n.m., glandula nasalis medialis; M.c,Meckel's cartilage; pch.s., prechoanal sac; pl.t., planum ter-minale; sjp.n., septum nasi; ten., tectum nasi. Other abbreviationsas for Text-fig. 1.

row (acrodont), and a few additional rows waiting to take theplace of the former. The premaxillary teeth of C. bot tger iare sketched in Text-fig. 3; they have the normal histologicalstructure of anuran teeth as described for Ran a by Krause(1923), and were discovered in the genus by Hewitt (1911).C. namaquense differs from the other species in beingtoothless. The vomer in C. capense is a very small boneinvesting the edge of the solum nasi region of the choana. Thereis no considerable prolongation of the bone into the narialcavity, as Cacosternum lacks the enormous cartilaginousaxis of the eminentia olfactoria, which the vomer invests in

282 C. G. S. DE VILLIERS

Phrynomerus . C. bot tger i has a comparatively largevomer, its size being due to the extent of the squame investingthe ventral surface of the solum nasi. The bone encapsules afew tubules of the glandula intermaxillaris. In both species thevomer is entirely edentulous, and separated from its fellow onthe other side by fibrous connective tissue. In G. capensethe two bones approach each other most closely. The pala-t ine is widely separated from the vomer, so that no vomero-

TEXT-FIG. 3.

pn pmx L

pwx

sk

Section through the left premaxilla of C a c o s t e r n u m b o t t g e r i .c.pn.i., cartilago praenasalis inferior; epm., epithelium of buccalcavity; pl.c., pulp cavity of tooth; pmx.l., left premaxilla;pmx.r., right premaxilla; pn.pmx.l., prenasal portion of leftpremaxilla; sk., socket of tooth; t., tooth. Other abbreviations asfor previous figures.

p a 1 a ti n e is formed as in Phrynomerus . The bone investsthe ventral surface of the processua antorbitalis as in Ranaand is of course quite edentulous. The septomaxil lary istopographically confined to the lamina superior cristae inter-mediae and, as stated above, encapsules the recessus sacci-formis. As in Phrynomerus , the bone terminates in frontof the planum terminale of the cartilago obliqua. The relationof nasals and os en ceinture in Cacosternum wasfirst remarked upon by Noble (1926), who pointed out that the


nasals are very small bones appearing on the sides of the largeos en ceinture, which latter is prolonged into the tectum nasi.At their maximal width a nasal in C a c o s t e r n u m covers aboutone-sixth of the tectum nasi, so that two-thirds of the latter areexposed; laterally the nasal does not articulate with the maxillaas in R a n a. This peculiarity is also met with in P h r y n o -m e r u s , but the posterior bay in the nasal is absent.

For the rest, the region of the olfactory capsule and associatedstructures differs very little from the well-known type met within the frog. The absence of an enlarged eminentia olfactoria andassociated cartilaginous axis encountered in P h r y n o m e r u sis probably to be interpreted as lack of specialization in thisdirection.

OSSIFICATIONS IN THE SPHENETHMOID EEGION.

In neither of the two species sectioned is the os en cein-ture ossified so far forwards as one might expect. The firsttraces of the bone are met with in the nasal septum at the levelof the choana and the posterior limits of the vomers. This isexactly the state of affairs in R a n a as well. The ossificationspreads to the tectum nasi at the region of the anterior limitsof the processus antorbitalis, but the ventral portion of thenarial skeleton only begins to show signs of ossification towardsthe posterior region of the processus antorbitalis, which is notpartially incorporated into the os en ceinture as in R a n a.These features are drawn in Text-fig. 4, a. In the region of theroots of the olfactory nerves (Text-fig. 4, b) the os en ceintureappears upon transverse section as a densely ossified troughwith no traces of cartilage in its walls. In P h r y n o m e r u s thefree dorsal ends of the trough persist as cartilage, which alsoconstitutes the central portion of its bottom. More posteriorlythese three tracts of cartilage also appear in C a c o s t e r n u m ;it is interesting to note that the appearance of the mid-ventraltract indicates the presence of a posterior ventral notch in theos en ceinture. This is not represented in R a n a. The anteriordivision of the os en ceinture in C. b o t t g e r i is similar inappearance to that of C. c a p e n s e , but the posterior portionis like that of P h r y n o m e r u s , inasmuch as no complete

284 C. G. S. DB VILLIERS

ossification occurs, the three tracts of cartilage persisting as inP h r y n o m e r u s .

It will be convenient to leave the discussion of the othercartilage bones to a later stage and to consider forthwith thef r o n t o - p a r i e t a l bones and the so-called fronto-parietal

TEXT-FIG. 4 6.

o e c en t

4a: Transverse section of the skull ofC. c apense cut posterior tothe antorbital process.

4 b: Transverse section through the region of the antorbital process ofC . c a p e n s e .

b.op.7i., branch of the optic nerve; cn.t., connective tissue; frp.,fronto-parietal; mx., maxilla; o.e.c, os en ceinture; op.n., opticnerve; pal., palatine; pr.aob., processus antorbitalis. Otherabbreviations as for previous figures.

fontanelle. Hewitt (1911) remarked upon the weak ossificationof the fronto-parietals and called attention to the presence ofthe fontanelle in C. b o t t g e r i . These two features are alsomet with in Cacos te rnum capense . The tips of thefronto-parietals are figured in Text-fig. 4, a; they are imbeddedin tough connective tissue which forms the roof of the brain case.The bones do not increase greatly in size in the interorbitalregion but are always joined by a wide expanse of connective

CRANIUM OF CACOSTBRNUM 285

tissue as in P h r y n o m e r u s ; they attain to their maximalsize in the region of the anterior limits of the otic capsule, buteven so they do not touch in the middle line, although they areconsiderably more strongly developed than in P h r y n o m e r u s .Conditions in C. b o t t g e r i correspond very closely to thosein C. c a p e n s e , but the fronto-parietals are even smaller andhardly project from the otic capsule into the connective-tissuecranial roof. This is almost exactly similar to the P h r y n o -m e r u s pattern.

The p r o - o t i c:—The optic foramen is bounded anteriorly bycartilage, but its postero-dorsal margin is formed by the p r o -o t i c bone. Exactly the same conditions prevail in C. b o t t -g e r i . All ossification of the septum dividing the cavity of theotic capsule from the brain-cavity disappears before the foramenacusticum and the foramen endolymphaticum are sectioned,whereas in B a n a and P h r y n o m e r u s the anterior boundaryof the former foramen is part of the p r o - o o t i c . Posteriorto the two foramina mentioned, the otic capsule is almostentirely cartilaginous. Weak ossification of the capsule was alsoa feature of P h r y n o m e r u s , in which the supra- and infra-cristal ossifications were likewise absent. C. b o t t g e r i hasthe same type of otic capsule as C. c a p e n s e , except that inthe latter species the posterior division contains much morepersistent cartilage than in the former.

The cranial roof consists of fibrous connective tissue in theorbital region; towards the anterior boundary of the oticcapsule the tip of the taenia tecti medialis is sectioned; whenthis spreads laterally and passes into what should represent thetaenia tecti transversalis, the cartilaginous cranial roof shows nomore foramina, so that as in P h r y n o m e r u s and A r t h r o -l e p t e l l a (de Villiers, 1929) the parietal foramen is absent andthe taenia tecti transversalis is confluent with the tectum syno-ticum. It is of course also possible to consider this state of affairsto be due to the a b s e n c e of the transverse taenia; but com-parative data are not available; Gaupp's original descriptionreferred to the European E a n a fusca. A remarkable feature ofthe tectum synoticum of O a c o s t e r n u m is its weak develop-ment towards the foramen magnum, where it possesses a deep

286 C. G. S. DB VILLIEES

notch filled with connective tissue (Text-fig. 5). The exoccipitalsare comparatively small; ventrally between them a portion ofthe planum basale persists as cartilage, which, however, showsno traces of a notochord.

The p a r a s p h e n o i d stretches from themid-A^entral divisionof the os en ceinture to the ventral occipital region, is a dagger-shaped bone as in E a n a and, as in that genus, possesses twoposterior notches separating the longitudinal portion from the

TEXT-FIG. 5.

t sn en t

ot

Transverse section through the posterior limits of the tectumsynoticum of C. c a p e n s e . br., brain; oi.c, otic capsule;t.sn., tectum synoticuni. Other abbreviations as for previousfigures.

lateral ones, which attain their greatest size at the level of theposterior region of the otic capsule. The cartilaginous cranialroof lacks a taenia transversalis in C. b d t t g e r i also. Thee x o c c i p i t a l s are comparatively large and the tectum synoti-cum has no bay dorsal to the foramen magnum. The para-sphenoid is dagger-shaped, but posteriorly the longitudinalportion is not marked off from the lateral ones by deep notches.

The morphology of the q u a d r a t o m a x i l l a r y and para-quadrate was reinvestigated by the author in A r t h r o l e p t e l l a(1929) and P h r y n o m e r u s (Quart. Journ. Micr. Sci., vol.73. C a c o s t e r n u m is most remarkable in possessing atotally unossified quadrate cartilage, whereas in other Anurangenera, including E a n a , as described by Gaupp, the quadrateossifies perichondrally and enchondrally and fuses with the


quadratomaxillary. The relations of the above-mentioned bonesin C a c o s t e r n u m are sketched in Text-fig. 6, a and b; a repre-sents a transverse section of the suspensorial region of the headand passes through the Eustachian tube. The quadratomaxil-lary occupies a position external to the chewing muscles, but

TEXT-FIG. 6 a AND 6.

an ty

Me

Transverse sections through the articular region of the skull ofC. c a p e n s e to show the relations of the quadratomaxillary tothe rest of the skeleton (muscles are ruled), an.ty., annulus tym-panicus; dmar., dermarticular; EX., Eustachian tube; hy., hyale;p.pt., processus pterygoideus; p.qd., pars quadrata processuspterygoidei; prq., paraquadrate; ptg., pterygoid; qmx., quad-ratomaxillary. Other abbreviations as for previous figures.

more posteriorly it gradually shifts in between these latter, andappears as an investing bone of the quadrate cartilage. It is,however, easily distinguishable from dermal bones by the factthat it is not separated from the quadrate cartilage by a con-nective-tissue lamella (Text-fig. 6, b). The bone shoots a fewdiminutive rootlets into the invested cartilage, but the charac-teristic cartilaginous structure of the latter is in no way affected.Exactly the same conditions prevail in C. b o t t g e r i .

The p a r a q u a d r a t e is a comparatively small bone in


C a c o s t e r n u m and is first encountered in sections at the levelof the closure of the optic foramen; it then lies external to thetemporal muscle and does not articulate anteriorly with anybone as it does in P y x i c e p h a l u s a d s p e r s u s . Uponreaching the transitional region between the processus oticusand the crista parotica, the paraquadrate forms a bony sheath

TEXT-FIG. 7 a, b, c, d.

.prq

vat

Consecutive transverse sections through the tympanic region ofC- c a p e n s e . (It is impossible to locate definitely the commonboundary of the crista parotica and the processus oticus. Thisregion is therefore labelled trn., transitional cartilage.) d.at., dorsalportion of annulus; epl., extraplectral enlargement of the parsexterna plectri; m.e., middle ear; p.ot., procesaua oticus; t.m.,tympanic membrane; v.at., ventral portion of annulus. Otherabbreviations as for previous figures.

for the latter. For a considerable stretch no connective tissueis present to separate the bone from the cartilage, which there-fore simulates perichondral cristal ossification. Enchondralossification of the cartilage is absent. The paraquadrate istypically triradiate as in all A n u r a known to me; the twotransverse posterior rays are normal investing bones of thequadrate cartilage and crista parotica. The relations of theparaquadrate, crista parotica, processus oticus and annulustympanicus are sketched in Text-fig. 7, a, b, c, d. C. b 611 g e r i


does not differ very much from 0 . c a p e n s e , but a stagecorresponding to Text-fig. 7, b, is missed out, so that the para-quadrate forms a groove, and not a sheath for the transitionalcartilage.

The p t e r y g o i d invests the dorsal and inner surfaces of theprocessus pterygoideus and possesses in its dorsal portion a well-developed marrow cavity. On the whole it may justly be main-tained that the pterygoid is much more strongly developeddorsal to the processus pterygoideus than in B a n a. Theanterior portion of the processus basalis is entirely ensheathedby the pterygoid, which is not in this region separated from thecartilage by connective tissue (Text-fig. 8, a). The two anteriorlydirected horns of the processus basalis are sectioned in Text-fig. 8, b; the tip of the lower touches the pterygoid bone, but itsupper division and the dorsal anterior horn of the processusbasalis are again separated from the investing pterygoid byconnective tissue. Text-fig. 8, b, shows the junction of theprocessus oticus and crista parotica, and Text-fig. 8, c, marks thefusion of this cartilage mass with the processus basalis. Pos-teriorly the pterygoid persists as a diminished bone on the innersurface of the pars quadrata. As far as comparative data areavailable, these conditions agree topographically quite well withthose in K a n a . C. b o t t g e r i agrees with C. c a p e n s eeven in the minutest details, the only point of difference beingthe circumstance that the lower anterior hom of the processusbasalis is not entirely ensheathed by the pterygoid.

THE AUDITORY APPARATUS

Typical transverse sections through the anterior region of theannulus tympanicus and middle ear are shown in Text-fig. 7, aand b; since the annulus has the form of a disk with a centralperforation, it will appear in transverse section as two cartilages,the ventral of which is the larger on account of the eccentricityof the perforation referred to above. The pars externa plectribegins to appear in Text-fig. 7, c as a longish cartilage imbeddedin the mesodermal portion of the tympanic membrane. Suchan extraplectral enlargement of the pars externa was alsoencountered in P h r y n o m e r u s . Text-fig. 8, a, b, and c,

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.

CRANIUM OP CACOSTERNUM 291

represent further sections of the auditory apparatus, not differ-ing essentially from Text-fig. 7, c, so far as the plectral andannular arrangements are concerned. It will, however, benoticed that the pars externa plectri shifts gradually to a moredorsal position, and in Text-fig. 9, a, its dorsal portion shows

TEXT-FIG. 9 a AND b.

pmp

Pr1

prtjP Pb

Consecutive transverse sections through the annular region ofC. c a p e n s e . j-v., jugular vein; p.e.p., pars externa plectri;p.m.p., pars media plectri; vd.at., ventral and dorsal portions ofannulus passing over into each other at the posterior limits of theannulus; VII, seventh cranial nerve. Other abbreviations as forprevious figures.

perichondral and enchondral ossification, although a marrowcavity is not developed. The section is in fact cut through thetransition from pars externa to pars media plectri, which is theonly part of the plectral apparatus to ossify in A n u r a. It willbe noticed further that the dorsal portion of the annulus hasnow disappeared from section, although it subsequently re-appears. The annulus is in fact not a complete ring as in R an a,but is discontinuous dorsally as in P h r y n o m e r u s. The open,crescentic form of the annulus seems to be quite common inA n u r a and particularly in Brevicipitid-Engyostomatidae.Since the region of the pars media plectri is now reached, atten-


tion should be called to the absence of a pars ascendens plectrieffecting a communication between the pars externa plectri andthe crista parotica. This cartilage was described by Gaupp forB a n a fu sca , but I have never come across it in South Africanfrogs and toads, so that its universal occurrence in A n u r ashould not be assumed. Text-fig. 9, b, represents a sectionthrough the body of the pars media, which is seen to consist ofa perichondral osseous sheath and a central, permanentlycartilaginous core. As the pars media approaches the oticcapsule, the ossification ceases to be exclusively peripheral andosseous substance may also be seen traversing the cartilage asin Text-fig. 10, a. The pars media is overlain by the jugular veinand the hyomandibular branch of the seventh nerve. Text-fig. 10, b, represents the point of maximal fusion of the parsmedia with the otic capsule; it will be noticed that the peri-chondral ossification is no longer sheath-like, but disappearstowards the inner aspect of the pars media, where it is in carti-laginous continuity with the otic capsule. For a short distancethe sheath-like pattern is represented again, Text-fig. 10, c, andall traces of ossification disappear at the level of the anteriorboundary of the operculum (Text-fig. 10, d), where the plectrumis represented by the pars interna. The plectral apparatus istherefore a continuous cartilaginous structure, but in the regionof the pars media it is perichondrally ossified.

The operculum has the bowl-like shape typical of A n u r a andis fused to the dorsal margin of the fenestra ovalis upon thedisappearance of the pars interna plectri. The fossa fenestraeovalis is large as in P h r y n o m e r u s . The operculum possessesa well-developed musculus opercularis, which is not, however,attached to a special cartilaginous tuberosity of the operculum.

C. b o t t g e r i has an auditory apparatus which differs quiteconsiderably from that of C. c a p e n s e . The annulus tym-panicus is very widely open dorsally, but the plectrum has muchthe same histological and anatomical structure as in the largerspecies. The operculum is, however, relatively much larger inthe smaller species and in its anterior division it is straightenedout, and more Avatch-glass shaped than bowl shaped. Theconsequence is that the fossa fenestrae ovalis and the ductus


fenestrae vestibuli both appear to be smaller than in the largerspecies, although the increase in height compensates for the

TEXT-FIG . 10 a, b, c, d.

Consecutive transverse sections through the sound conductingapparatus of C. c a p e n s e . opm., operculum; pb.p.m.p.,posterior boundary of the pars media; p.i.p., pars interna plectri;IX, ninth cranial nerve. Other abbreviations as for previousfigures.

decrease in breadth. Posteriorly the operculum acquires theusual bowl-like shape again (Text-fig. 11). The musculus oper-cularis is comparatively enormous and joined by means of an

NO. 294 u


aponeurosis to the musculus levator scapulae. The opercularmuscle is attached to the operculum, which develops a specialtubercle or tuberosity for this purpose: the tubercle is absent inC* capense although the muscle is present. According to

TEXT-FIG. 11.

spsc

m L

tb-

Transverse section through the opercular region of the ear ofC. b o t t g e r i . f.f.o., fossa fenestrae ovalis; f.o., f enestra ovalis;m.l.s., musoulus levator scapulae; m.op., musculus opercularis;spsc, suprascapula; tb., tubercle for opercular muscle. Otherabbreviations as for previous figures.

Versluys (1924) an operculum was evolved as a response toterrestrial life; C. bot tger i should therefore be more terres-trial than C. capense. Of the latter species I may definitelyaccentuate the aquatic habits and the same is probably trueof C. bot tger i .

The hyoid appara tus was imbedded and sectioned with

CRANIUM OF CACOSTBRNUM 295

the skull, but was also dissected out to make sure of the grossanatomy. It was found to be so similar to that of E a n a, thatit was not considered necessary to give a drawing of it. Thebay between the manubria is a little shallower than in E a n a,the processes alares taper slightly more towards their posteriortips, and the processes thyroidei are comparatively longer, sothat they are still encountered in section towards the posteriorlimits of the coracosternum. This arrangement is, however,quite secondary and is due to the forward position of the shouldergirdle in the genus. The hyale is fused to the base of the oticcapsule behind the processus basalis. The processes anterioresare absent. The hyoid apparatus in C. b o t t g e r i is verysimilar to that of C. c a p e n s e , but the thyroids are notprolonged posteriorly to such an extent; possibly the pectoralgirdle is not so considerably shifted forwards as in the largerspecies. The hyale, moreover, is not fused with the otic capsule,but merely articulates with it, in a fossa below the lower lip ofthe fenestra ovalis (Text-fig. 12). It should be further noted thatthe thyroid processes in both species possess well-developedmarrow cavities but end posteriorly in long cartilaginous tips.

The loAver jaw lacks all traces of the peculiar modificationsencountered in P h r y n o m e r u s , and agrees in all essentialdetails with that of E a n a. The mento-mandibular is, however,ossified perichondrally only in the form of a sheath to Meckel'scartilage, Avhereas in E a n a enchondral ossification is alsoinitiated. The same conditions prevail in C. b o t t g e r i as inC. capense .

COMPARISON OF THE SKULL OF CACOSTBRNUM WITH THAT

OF PHRYNOMERUS.

The reasons for investigating the skulls of P h r y n o m e r u sand C a c o s t e r n u m were (1) to give some new histologicaldetails of the A n u r a n skull in general, (2) to ascertain whetherthe two Brevicipitid (Engyostomatid) genera are allied, as theabsence of a procoracoid might lead one to expect, and (3) toattempt to enumerate some cranial characters by which thesetwo genera are both distinguishable from Eanids; in otherwords, to attempt to discover some specific Brevicipitid-Engyo- •

U2

296 C. G. S. DE VILLIEBS

stomatid cranial characters. It will probably be most convenientto tabulate the evidence under the headings of the variouscranial unities.

A. The vestibule of the olfactory organ. The vestibular' Wiilste' described by Gaupp for E a n a are developed in both

TEXT-FIG. 12.

Transverse section through the otic region of the skull of C . b 611 -ger i to show the method of articulation of the hyale. f-hy., fossain otic capsule for the hyale; j?.&., processus basalis. Otherabbreviations as for previous figures.

species of Cacosternum, and in Phrynomerus . Theplica obliqua is suspended in Eana from the tectum nasi; inthe Brevicipitids the plica is short and blunt and suspendedfrom the cartilago obliqua.

B. The prenasal cartilages are present in the Brevicipitids asin Sana ,

C. The premaxilla is toothed in C. bot tger i and C.cap ens e but edentulous in C. namaquense (Werner, 1910)


and Phrynomerus . [Noble has repeatedly maintained thatno great systematic value can be attached to the absence orpresence of teeth. The South African Heleophryne would,according to Noble, have to be considered as a 'toothedBufonid'].

D. The maxilla is separated from the outer palatal squameof the premaxilla in Phrynomerus only.

E. The eminentia olf actoria is very high in Phrynomerus ,normal in Cacosternum and Eana .

~F. The vomer in Phrynomerus is considerably prolongedinto the choana; in Eana and Cacosternum such dorso-ventral enlargement of the bone does not occur.

G. The palatine in Phrynomerus fuses •with the vomer toform a vomero-palatine, but in Eana and Cacosternumthe two bones are wide apart.

H. The recessus sacciformis is large in Eana , diminished inCacosternum, and purely vestigial in Phrynomerus .

I. The nasals in Phrynomerus and Eana leave littleof the anterior portion of the os en ceinture exposed, whereasin the Cacosternum-Anhydrophryne group the os enceinture is prolonged anteriorly between the nasals, which aresmall and laterally placed.

J. Phrynomerus has two prechoanal sacs, Cacoster-num an unpaired one, whereas in Eana the structure isabsent. The organ in the Brevicipitids is to be derived from aprechoanal fusion of the ' Gaumenleisten', and not improbablyrepresents buccal vestiges of Jacobson's organ, which is supposedto be reduced to the recessus medialis in Anura.

K. The os en ceinture is paired in Phrynomerus , andnotched posteriorly in Cacosternum, whereas in Eana it isgirdle-like as its name implies. The lateral trabecular derivatesbounding the fenestra parieto-frontalis are cartilaginous inPhrynomerus and C. bot tger i but ossified in C. capenseand Eana .

L. The parieto-frontal bones are mere lateral tracts inPhrynomerus and Cacosternurn, whereas in Eanathey are broad and closely approximated mid-dorsally. Whereasthe dorsal cranial roof in the latter genus is therefore bony, it


is formed by thick, densely fibrous connective tissue joining thetwo parieto-frontals in the two Brevicipitid genera.

M. The optic and pro-otic foramina are bounded anteriorlyand posteriorly by bone in Phrynomerus . In Cacoster-num the Eanid type prevails, in which the anterior marginof the optic foramen is not reached by the os en ceinture.

N. The otic capsule in Phrynomerus lacks the supra- andsub-cristal ossifications. Weak ossification of the otic capsule isalso a feature of Cacosternum, particularly of C. capense.

0. The transverse taenia of the Eanid cranial roof is absent inboth Brevicipitid genera and also in Ar throlepte l la .

P. The occipital region of the adult Anuran skull is remarkablyconstant in structure. The exoccipitals are joined ventrally bythe persistent planum basale. All traces of an intracranialnotochord disappear. In C. capense the foramen magnumpossesses a deep dorsal notch.

Q. The parasphenoid shows no appreciable variation.E. The paraquadrate is comparatively short in Phryno-

merus and inclined to fuse with or invade the crista, which isossified. In Cacosternum the crista is cartilaginous, en-capsuled, but not invaded by the paraquadrate although theseparating connective-tissue lamella disappears.

S. The pterygoid invades and fuses with the ossified peripheryof the processus basalis in Phrynomerus . This does nottake place in Cacosternum, in which the separating con-nective tissue merely disappears. No histological details areavailable for Ran a.

T. The quadratomaxillary invades the articular division ofthe quadrate process in Ran a (Gaupp), Ar throlepte l la ,and Phrynomerus . In Cacosternum the quadratecartilage is not ossified, but merely overlain directly by thequadratomaxillary.

U. The two Brevicipitid genera differ from Rana in theabsence of a processus ascendens plectri and in the incomplete-ness of the annulus tympanicus. They share these features withArthro lepte l la . The middle ear and Eustachian tube arepresent in all the three non-Eanid genera mentioned as well asin Rana. The plectrum and operculum are Eanid, except for


the following differences. The operculum is particularly largeand shallow in G. bot tger i , and develops a relatively largemusculus opercularis attached to a special tuberosity. I havenot seen an opercular muscle in Phrynomerus . The parsexterna plectri is enlarged to form an extraplectral imbeddedin the mesodermal layer of the tympanic membrane in the twoBrevicipitid genera, but not in Ran a. The pars media plectrilies ventral to the crista in Phrynomerus , but in Cacoster-n u m is closely applied to the ventral lip of the fenestra ovalisas in Ran a.

V. The hyalia are fused with the otic region of the skull exceptin C. bot tger i . The Brevicipitid genera lack the anteriorprocesses of the hyoid apparatus, present in Rana. The alarprocesses of Cacosternum are like those of Rana, butthey are enlarged and blade-like in Phrynomerus ; in thelatter genus, as well as in Cacosternum, the thyroidprocesses are met with in the pectoral region, a condition whichmay be due to the pectoral girdle being shifted forwards. Theoverlapping is most pronounced in C. capense.

W. In the lower jaw the mento-mandibular is exclusivelyperichondrally ossified in Cacosternum. In Rana andPhrynomerus enchondral ossification also takes place. Thelatter genus has a remarkably specialized mental region, withbackwardly directed diverticula of Meckel's cartilage and amodified gular musculature. These features are absent inCacosternum and Rana.

It is always dangerous to base affinities on the study of oneparticular system of organs only; it is therefore necessary tostate explicitly that no final conclusion regarding the mutualrelationships of Phrynomerus and Cacosternum can bearrived at by a comparison of their cephalic skeletons, but thatthe results embodied in this paper and the previous one onPhrynomerus may aid the solution of the problem. Thewhole question of the validity of the Brevicipitidae as an autono-mous family of the F i rmis te rn ia , and of the monophyleticorigin of the South African Brevicipitid genera, will be fullydiscussed in a dissertation by one of my students. I shall there-fore restrict myself to the cephalic skeleton.

300 C. G. S. DE VILLTERS

The most important feature which Phrynomerus andCacosternum have in common is the extreme reduction ofthe parieto-frontal bones, and the connective-tissue-like natureof the pretectal cranial roof. Whether the feature is met with inany other Brevicipitids, I cannot say. The otic region of bothgenera is characterized by the incompleteness of the annulustympanicus and the enlargement of the pars externa plectri toform an extraplectral cartilage embedded in the tympanicmembrane. Moreover, the pars ascendens, effecting a junction ofthe pars externa plectri and the crista parotica, is not developed.But these features, as well as the absence of a taenia tectitransversalis, are not exclusively Brevicipitid, as they have beenproved (de Villiers, 1929) also to occur in the Eanid Arthro-lepte l la . The hyoid apparatus lacks the anterior processesin Phrynomerus and Cacosternum, but again compara-tive data for other genera are not available, and the processesare also absent in an arciferous toad, Bufo angust iceps .The relations of membrane bones like the paraquadrate, quad-rato-maxillary and pterygoid, to the cartilages they invest areof great osteogenic interest but are probably not of systematicimportance.

Many features of the skull of Phrynomerus are indicativeof extreme specialization and cannot be used for comparisonwith Cacosternum; such are, e.g., the presence of a vomero-palatine, the absence of a recessus sacciformis, the enlargedeminentia olfactoria and the intrachoanal elongation of thevomer. But these features probably represent individualcharacteristics of Phrynomerus and probably do notrepresent specifically Brevicipitid modifications. As far ascomparative data are available, the skull of Anura, withthe exception of Aglossa, which have become secondarilyaquatic, is remarkably constant in structure, and great deviationfrom the Eanid type should not be expected and has not beenrecorded in the extant literature on the subject. But it is hopedthat the account of the anatomy of the microtomized skulls ofPhrynomerus and Cacosternum may help to reviveinterest in the osteology of one of the most primitive groups ofterrestrial vertebrates; their phylogeny may be obscure, but as

CRANIUM OF CACOSTBENUM 301

a group they are at any rate end-products of evolution and theirgenealogy is not obscured by phylogenetic neoteny, as is the casewith the Urodeles.Stellenbosoh,

April, 1930.

LITERATURE CITED.

For a more comprehensive list, the reader is referred to the Author'spaper on. P h r y n o m e r u s ; the following are additional references:Andersson, L. G. (1911).—"Reptiles, Batrachians, and Fishes collected by

the Swedish Expedition to British East Africa. 2. Batrachians", 'Sven-ska Vetensk. Akad. Handl,', vol. xlvii.

Boulenger, G. A. (1882).—'Catalogue of the Batrachia salientia siveecaudata in the collection of the British Museum', 2nd ed.

(1887).—"Description of new Reptiles and Batrachians in the BritishMuseum", Part III, 'An. and Mag. Nat. Hist.', vol. xx.

(1906-9).—"A revised list of the South African Reptiles and Batra-chians", 'An. S. Afr. Mus.', vol. v.

Gaupp, E. (1904).—'Die Anatomie des Frosches', Bd. 3.Hewitt, J. (1911).—"A Key to the species of the South African Batrachia

together with some notes on the specific characters and a synopsis of theknown facts of their distribution", 'Rec. Albany Mus.', vol. ii.

(1919).—"Anhydrophryne rattrayi, a remarkable new frog fromCape Colony", 'Rec. Albany Mus.', vol. iii.

(1925).—"On some new species of Reptiles and Amphibians fromSouth Africa", ibid.

(1926).—"Descriptions of some new species of Batrachians andLizards from South Africa", 'An. Natal Mus.', vol. v.

Krause, R. (1923).—"Mikroskopische Anatomie der Wirbeltiere in Einzel-darstellungen", Teil III, 'Amphibien'. Berlin, de Gruyter.

Methuen, P. (1913).—"The Percy Sladen Memorial Expedition to GreatNamaqualand, 1912-1913: Zoology", 'An. Trvl. Mus.', vol. iv.

Nieden, F. (1926).—"Anura I I : Engyostomatidae" : 49ste Lieferung des'Tierreichs'. Berlin, de Gruyter.

Noble, G. K. (1922).—"The Phylogeny of the Salientia: I. The osteologyand the thigh musculature; their bearing on classification and phylo-geny", 'Bui. Am. Mus. Nat. Hist.', vol. xlvi.

(1924).—"Contributions to the herpetology of the Belgian Congo,based on the collection of the American Museum Congo Expedition,1909-1915", 'Bui. Am. Mus. Nat. Hist.', vol. xlix.

and Parker, H. W. (1926).—"A synopsis of the Brevicipitid toads ofMadagascar", 'Am. Mus. Novitas', No. 232.

(1926 a).—"The Importance of larval characters in the classificationof South African Salientia", ibid., No. 237.

802 C. G. S. DB VILLIBRS

Noble, G. K. (1927).—"The value of life-history data in the study of theevolution of Amphibia", 'An. N. Yk. Ac. So.', vol. xxx.

Power, J. H. (1927).—"Some tadpoles from Griqualand West", 'Trans.Roy. Soc. S. Afr.', vol. xiv.

Versluys, J. en anderen (1924).—'Leerboek der vergelijkende Ontleed-kunde van de Vertebraten', Deel II. Utrecht, Oosthoek.

Villiers, C. G. S. de (1929).—"The Development of a Species of Arthrolep-tella from Jonkershoek, Stellenbosch", 'S. Afr. Journ. Sc.', vol. xxvi.

(1929 a).—"Some observations on the breeding habits of the Anuraof the Stellenbosch Flats, in particular of Cacosternum capense andBufo angusticeps", 'An. Trvl. Mus.', vol. xiii.

(1930).—" On the Cranial Characters of the South African Brevicipitid,Phrynomerus bifasciatus", 'Quar. Journ. Micr. Sci.', vol. 73.

Werner, F. (1910).—'Eeptilia et Amphibia aus den zoologischen undanthropologischen Ergebnissen einer Forschungsreise im westlichen undzentralen Siidafrika', Bd. IV.

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