ON T H E RELATIONS O F T H E HYOID AND OTIC ELEMENTS OF THE SKELETON IN THE

BATRACHIA.'

E. D. COPE.

THE characters of the hyoid bones of many Batrachia have been described by Dr. Parker and Professor Wiedersheim,a and their otic elements have received much attention from the same authors. In both fields, however, much remained to be done. The otic elements of the Salientia have been extensively described by Parker, but no especial attention bas been devoted to those of the Urodela by either author, except incidentally to other objects, In the present paper I desire to call attention to these elements in the Urodela, and to contribute thereby to the general theory of the morphology of the inferior arches of the skull. Whether light be thrown on the vexed question of the homologies of the suspensors of the inferior arches of the skull or not, it is desirable to see what this intermediate group of vertebrata contributes to its solution. I go over the types seriatim, commencing with the lowest.

GANOCEPHALA.

In the genus Trimerorhachis (Cope) there appears to be a distinct opisthotic bone in addition to the intercalare, as in the fishes. In form it is much like the prootic, but in reversed position ; its anterior thin edge forming a suture with the pos- terior thin edge of the latter. The two together form on their inferior surface a spout-like groove, which extends outwards,

1 Read before the United States National Academy of Sciences, April, 1888. Ab- stract published in Amei-ican Nafzwalist, 188S, p. 464.

1 On t l e Structure and DezIeiopent of the Skzii of the Common Frog, Transactions of the Royal Society, London, 1870, p. 137; On f l e Styurtwe and Dmeloptnent of the SkziZi in the Hatrachia, loc. cit., 1875, p. 601 ; On the Sfyucture and Deuelop~nent of the Sku12 in the Urolfelous Aniphidin, loc. cit., 1876, p. 529.

Das K@fsLdet dcr ci-odelen: hforphologiscles yahrbucl, 1877, pp. 352, 459.

298 COPE. [VOL. 11.

terminating at the narrow truncate extremity of the two bones. A t the base of the opisthotic, and between it and the parasphe- noid, is situated the fenestra ovale. This is closed by the extremity of a columella auris, whose proximal part at least may be homologized with the stapes, since no other element corre- sponding with the latter is visible. The columella is then directed outwards, backwards, and upwards to the notch which is formed between the adjacent borders of the intercalars and suspensorium, where it terminates without having displayed any segmentation. This notch, which is present in all the Permian Batrachia known to me except Acheloma, may have been occu- pied by a membranum tympani, and that the Ganocephala had, like the Salientia, distinct external organs of hearing, thus dif- fering from the Qoteida and Urodela.

RHACHITOMI.

The only genus in which I have observed ossicula auditus is Zatrachys (Cope). Here the parts resemble nearly those de- scribed in Trimerorhachis. The columella is curved outwards and backwards, and terminates at the notch external to the 0s intercaZare, which was, I suspect, covered by a membranum tym- pani as in the Salientia.

PROTEIDA.

In Necturus (PI. XXII., Fig. I) the stapes is osseous and has its columella directed abruptly forwards. It articulates with a cor- responding process of the squamosal bone, which extends pos- teriorly to meet it from the posterior bone of the latter. The quadrate part of the suspensorium of the mandible is exten- sively osseous. The distal extremity of the ceratohyal is not articulated with anything, but is connected with the quadrate by the hyosuspensorial ligament, and with the angle of the mandible by the mandibulo-hyoid ligament, as has been pointed out by Huxley.2

In Proteus the relation of the stapes to the squamosal is similar in general to that in Necturus, but the connection

1 Transacfions American Phiiosop/rical Society, 1886, p. 290. Proceedings Zoiilogical Society, London, 1S74, p. 192, PI. XXIX. Professor

Huxley does not describe or figure the relation of the stapes to the squamosal bone.

299 No. 2.1 NYOlDS AND 0TlC.S OF BATRACHlA.

between the anterior process of the former and the posterior process of the latter is accomplished by an intervening bit of ligament. The quadrate cartilage is little or not ossified in Proteus. The ceratohyal is not articulated at its distal end, but the latter is attached to the squamosal by two ligaments, the superior and inferior hyosuspensorials (Pl. I., Fig. 2) . The at- tachment is higher up than in Necturus, as the ceratohyal is longer.

URODELA.

Trematodera.

In Cryptobranchus the columella of the stapes is directed forwards, and terminates in a cartilaginous stem. This is artic- ulated with the suspensorium of the mandible at its proximal part, at the line of junction between the squamosal bone and the quadrate cartilage. The latter is not ossified. The distal end of the ceratohyal is not prolonged, and it is connected with the distal half of the posterior border of the quadrate cartilage by a wide hyosuspensorial ligament. This ligament is inter- rupted by a subtriangular cartilage, the hyosuspensorial carti- lage.

I have not examined the genus Megalobatrachus.

Amphiidmoidea.

In Amphiuma the stapes is lateral in position, and its short columella is directed outwards. It is continued as a cartilage to the truncate posterior apex of the osseous quadrate bone, with which it articulates by a suture. The quadrate is extensively osseous. The distal extremity of the ceratohyal is long and free, and is connected with the middle of the posterior border of the quadrate by an elongate hyosuspensorial ligament.

Apoda.

Merrem Pseudophidia De Blainville. In Typhlonectes (compressicaudus) the stapes is osseous,

and is lateral in position. Its columella is short, and is directed forwards, and is connected by ligament with the posterior border of the quadrate. The distal end of the ceratohyal is entireIy free from the manibular suspensorium.

Gymnophiom Mull.

300 COPE. [VOL. 11.

In Dermophis (mexicanus) the stapes is lateral in position, and is osseous. Its columella is robust and osseous, and extends forwards, abutting against the posterior border of the quadrate, with which it forms a close movable articulation. The quadrate is completely osseous, and is freely articulated proximally with the cranium. The ceratohyal is free, and not connected with the suspensorium.

Pseudosauria.

De Blainville ; Myctodeva, J. Mtiller. This elitensive group is most conveniently considered by

families. In the Amblystomidae the columella of the stapes is replaced

by the stapedius muscle. This is directed posteriorly, and away from the suspensorium. The ceratohyal is short distally, and its extremity is articulated to the distal part of the posterior border of the quadrate cartilage. The quadrate cartilage is ossified distally, but not proximally.

In the Plethodontidae the stapes has the same character as in the Amblystomidae, except that in some specimens a slender car- tilaginous process is seen to be directed towards the quadrate car- tilage in PZethodoiz gZa&tosus and SQehpes rzcber. This is probably the persistence of the larval condition of both this fam- ily and of the Amblystomidae. In the larva (Pl. I., Figs. 7, 9) the columella of the stapes is directed forwards, and is con- nected with the proximal part of the quadrate cartilage by a short cartilaginous rod. In the larva of Chondrotus tenebroszcs the connection is completed for a short distance by ligament. Thus the larvae of these two families present the character of the mature members of the suborders Trematodera, Amphiu- moidea, and Pseudophidia. The quadrate in the Plethodontidae is ossified in its proximal part only. The ceratohyal has its distal extremity curved forwards, and articulated by distinct suture with the quadrate cartilage or bone ; in Plethodon glztti- noszis it is inserted in a fossa (Pl. I., Fig. 14).

In Desmognathidze the characters are as in Plethodontidze. In Salamandridae the position of the stapes is as in the

previous families, but the relations of the extremity of the ceratohyal are as in the larvae of those animals, or as in the

301 No. 2.1 HYOIDS AND OTICS OF BATRACHIA.

Amphiumoidea. The extremity is connected with the quadrate bone by a hyosuspensorial ligament. In Salamandra the cera- tohyal and the ligament are of moderate length.

In the Yleurodelidae the arrangement is as in the Salamandri- dae. In sotne of the species the ceratohyal is greatly elongate. I n the DiemyctyZus torosus the free.extremity of the ceratohyal ex- tends to the inferior line of the occipital condyle, carrying with it the hyosuspensorial ligament. This ligament is elongate, and arises from the proximal part of the posterior border of the quad- rate cartilage (Pl. II., Fig. 3). In the D. viridesceizs this pecu- liarity is carried still further. The ceratohyal extends to the lateral crest of the exoccipital, and is received into a fossa of its inferior surface, as has been pointed out to me by my friend Dr. E. E. Galt. The hyosuspensorial ligament extends from the proximal part of the quadrate cartilage beneath the ridge men- tioned to the apex of the ceratohyal (Plate II., Fig. 4).

TRACHYSTOMATA.

In Siren the stapes is osseous. Its columella is replaced by the stapeclius muscle, which extends posteriorly. I t has no connection with the suspensorium. The quadrate is cartilagi- nous. The ceratohyal is large and is much produced distally. I t is connected with the posterior part of the quadrate, the ex- occipital, and the stapes by a wide hyosuspensorial ligament. I t is inserted on the anterior side of the ceratohyal oppo- site the quadrate, and is interrupted by a hyosuspensorial cartilage, as in Cryptobranchus.

SALIENTIA. Laurenti. Anura Dumkril. The stapes in this order resembles that of the Urodela. I t is

an oval disc without distinct process, and gives insertion to a stapedius muscle near its centre. But this order differs totally from the other existing orders, in the presence of a chain of ossicuZa auditus, which extends from the border of the stapes to the dermal membranum tympani. There are three of these, which have been named the interstapedial, the mesostapedial, and the epistapedial. The interstapedial is a bony style with a cartilaginous basis which originates alongside of the anterior

302 COPE. [VOL. 11.

border of the stapes, in a shallow cup-like expansion which abuts against the cranial wall. The shaft is cylindric. The meso- stapedial is a cartilage which is attached to the narrow extremity of the interstapedial much as an anther of a flower is attached to its filament. The proximal part of this element is shorter than the distal, and is connected with the superior part of the quadrate by a ligament, the mesostapedial. The distal part is deflected at a strong angle to the interstapedial, and is frequently somewhat spatulate by reason of an expansion distally. Its ex- ternal face is flat and is applied to the internal face of the epi- stapedial. The latter is a cartilaginous disk which closes the tympanic chamber externally. It fits like a lid on the cartilagi- nous annulus tympanicus, which extends beyond it all round. The annulus tympanicus is a thin and wide cartilaginous ring with a thickened margin, which is not continuous, but is inter- rupted at its superior outline. This interruption is occupied by the distal end of the interstapedial, and the proximal part of the mesostapedial. The distal part of thc latter extend verti- cally across the median foramen. These structures have been described and figured by Parker (I.c.), who has found them to be generally similar in all the families of the order, I have examined all the principal types, and give figures of them in the genera Xenopus, Discoglossus, Stereocyclops, Scaphiopus, Bufo, Hyla, and Rana (Pl. 11.) Figs. 7-12; P1. III., Fig. I).

The ceratohyal is slender at the point of connection with the skull. This is just in front of and external to the cartilaginous base of the interstapedial. It is continuous with the cranial wall in some species. I t is involved, just distal to its origin, in the annular Zigaamentum tymnfani, which forms the posterior wall of the tympanic chamber; but it has no structural connection with it.

The development of the Saliential skull has been studied by various authors, especially by Dug& Huxley, and Parker. I have examined series of Rana virescens, R. cZamata, and R. cates- briaea for the purpose of determining the homologies of the auricular bones of this order, by a study of their development. It has been shown that the ceratohyal cartilage is, for the greater part of the life of the tadpole, articulated with the quadrate car- tilage, first on its inferior, and then later on its posterior face. Professor Parker believes that it is a dismemberment of the dis-

No. 2.1 HYOZDS AND OTICS OF BATRACHZA. 303

tal half of the third ventral arch of the skull, and that the supe- rior half of the same becomes fused later with the second arch, thus forming the quadrate cartilage as it exists in adult Salientia. On approaching maturity, the ceratohyal leaves this connection, and is attached to the base of the skull as above described. My observations coincide with those of Parker in that the ossicula auditus do not appear until a later period of larval life in the genus Rana. But they appear before the ceratohyal has aban- doned its articulation with the quadrate cartilage. They then arise as follows: the epistapedial occupies from the first its normal position as a disk of cartilage at the flexure of the quad- rate cartilage. The interstapedial, on the other hand, arises as a bud from the normal position of its base, and gradually extends itself anteriorly. It early appears as cartilage with a short, free membranous extremity. The latter becomes the mesostapedial cartilage. These elements gradually elongate until they reach the epistapedial. For a time they reach no farther than the quadrate cartilage, and they rest on it, as in the Proteida and larvae of Urodela.

CONCLUSIONS.

From what has preceded, the following conclusions may be derived : - Fi~st. The relations of the stapes to the quadrate cartilage or

bone are of two types in the Urodela. The one is possessed by the Proteida, Trematodera, Amphuimoidea, and Pseudophidia ; the other by the Pseudosauria and Trachystomata. The larval structure in the Pseudosauria, and inferentially in the Trachy- stomata, is identical with the structure characterizing the adults of the other division. This is confirmatory of the opinion which I have expressed 1 as to the origin of the genus Siren. This is to the effect that Siren is an animal which is descended from a land salamander, and that its immediate ancestor became aquatic again at a comparatively late period of geological time. My opinion was at first suggested by the conditiolf of the bran- chi= in very young animals, where they are functionally abor- tive, and do not become respiratory organs until later in life, the largest animals having the best developed gills. The characters

=American Naturizlisf, 1885, p. 1226.

304 COPE. [VOL. 11.

of the stapes confirm this view, since they are those of land salamanders, as distinguished from those of aquatic habitat.

Second. There are also three types of relation between the ceratohyal arch and the skull. In the one there is no connection between the two, as in the Pseudophidia. Secondly, the con- nection is by ligament. This is seen in Proteida, Trachysto- mata, and all Pseudosauria except the Amblystomidae and Pletho- dontide. The last two families embrace the third type, in which the ceratohyal is articulated by suture with the quadrate. This last type is the most specialized, since the larve of those families display the connection between the ceratohyal and the skull similar to that seen in the types first and second. Thus the Salamandridze, which are superior to the Plethodontidae in their osseous carpus and tarsus, and opisthocelous vertebrae, have the hyoid connected with the skull, as in the larvae of the latter.

Third. At a stage in the history of the development of the Salientia, the relations of the stapes and of the ceratohyal to the skull are the same as in a transitibnal stage of the Urodele family of Plethodontidze ; or, taken separately, the relations of the stapes are those of Proteida, Trematodera, and larval Pseu- dosauria, while the relation of the ceratohyal is as in adult Pletho- dontidze and Amblystomidze. This is when the interstapedial cartilage connects the stapes with the posterior face of the quadrate cartilage, and where the ceratohyal articulates with the posterior face of the quadrate at its distal part.

Fozirth. It is not probable that the epistapedial forms an integral part of a single primitive element, which includes the other ossicda nzcdiius, as it originates independently of the interstapedial and mesostapedial. F@. The interstapedial and mesostapedial do not, at any

time in the history of the development of the genus Rana, form any part of the ceratohyal or meckelian ventral arches. As the incus and malleus of the Mammalian ossicda nzcditzts are seg- mented from the proximal parts of these arches, embryology indicates that they are not homologous with the ossicula of the Salientia. From this point of view, the latter form a special line of development, distinct from that displayed by the Mam- malia, unless the developmental record has been greatly falsi- fied by cznogeny. From the embryological standpoint, it

305 No.2.1 HYOZDS AND OTXCS OF BATRACHXA.

follows that the ossicuZa auditus of the Batrachia Salientia must be excluded from the discussion of the homologies of the Mam- malian ossicula.

Sixth. But the characters of the Ganocephala and Rhachi- tomi permit the following reflections, since the latter order is the one from which the Salientia derive their descent. The existence of a well-developed columella auris, which is unseg- mented, in the former orders, apparently like that of the Lacer- tilia, suggests that the segmentation seen in the Salentia is a specialization of later origin. This columella has also the posi- tion of the proximal part of the ceratohyal in the adult frog and the larval salamander. As the position of this element in all but the youngest tadpoles is a result of coenogeny, it may be inferred that the ossiczda auditus of both the Rhachitomi and the Salientia represent the separated proximal end of that arch, and hence be truly homologous with the incus of the Mam- mal. The probability that this is the case is increased by the character of this element in the Pelycosaurian genus Clepsy- drops,l- where the columella extends to the cranial wall, leav- ing the stapes to one side. This is exactly comparable to the relation between the interstapedial and the stapes seen in the Salientia, except that the two elements are not actually con- nected, as in Clepsydrops. Palaeontology then modifies the evi- dence from embryology, and renders it probable that the columella auris of the Permian genera, the interstapedial, and the incus are homologous elements, and originated by segmen- tation from the proximal end of a ventral cranial arch, probably the ceratohyal.

Seventh. It follows from what has preceded, that the con- dition of the representatives of the ossicuZa auditus in the Urodela is one of degeneration.

Eighth. It becomes probable, but not certain, from the posi- tion of the tympanic disk in the Rhachitomi, at the proximal base of the quadrate bone, that the episiapedial cartilage has originated as a segmentation from the proximal extremity of the quadrate cartilage, and is therefore truly homologous with the Mammalian malleus. This is, however, nothing more than a probability. For a considerable part of the material described in the preceding pages I am indebted to the United States National Museum.

1 See Pmccrdings American PhtiZosophiraZ Socicty, 1884, p. 41, PI. I., Fig. 2.

COPE.

EXPLANATION OF PLATE XXII.

The relations of the quadrate, stapedial, and hyoid apparatus. In Figs. I, 3, 9,

Figures twice natural size, excepting I, 3 , 4 7, and 8, which are natural size, and

FIG. I. Nrdurus rnacuIafus; squamosal removed. FIG. 2. Proteus anguinus. FIG. 3. Cryptobranchus aZlegheniensis; the middle of the squamosal removed,

FIG. 4. Amphiunza means: a, from behind. FIG. 5. TyphIonccics comprcssicaudw ; from the Belize. FIG. 6. Dermophis mexicanus; with the quadrate bone turned up, exposing its

inferior face, and that of the quadrat0 jugal; qa, the same with the quadrate in normal position. From Mexico.

14, 15, and 76, the squamosal bone has been removed.

10, I I, and 12, which are three times natural size.

the extremities remaining.

FIG. 7. Chondrotus ienebrosus ; larva 250 mm. FIG. 8. Chondrotus fenedrosus; adult. FIG. 9. Arnblystoinn tigrinum ; larva; squamosal removed. FIG. 10. Amdlystomn purzctaturn; adult. FIG. I I. Hemidactyliurn sadaturn. FIG. 12. Bafvachoseps attenuafus. FIG. 13. Cyrinophilus porphyrih'cus. FIG. 14. Pletlrodon glurinosus : squamosal removed. FIG. 15. Aufodax Zugubris; squamosal removed. FIG. 16. Spclerpes ruber; squamosal removed

COPE.

EXPLANATION OF PLATE XXIII.

The relations of the quadrate, stapedial, and hyoid apparatus in Urodela and Sali-

FIG I. Dennognatktu nigru; a, stapes separate and enlarged, the squamosal

FIG. 2. Sufamundra m u d a l u f ; the squamosal separated. FIG. 3. Die?nyc&&s lorosus, squamosal removed; P, separate squamosal. FIG 4. Dietnyctyfm viridescens, three times natural sue; the squamosal removed.

FIG. 5. siren kacerrina + ; squamosal in place. FIG. 6. DiscogZossus $ictus, partly posterior view; (I, ear bones, and origin of

ceratohyal, enlarged. FIG. 7. Bufo lcntip'nosus amrricanus, the squamosal removed; u, the squamo-

sal separate. FIG. 8. Scu$hiopm hammondii, the squamosal removed; (I, the squamosal; b,

the ear bones. FIG. 9. HyIugrutiosu, the squamosal removed; a, the squamosal; S, the ear

bones and cartilages in profile, the cartilages of the tympanum divided by vertical section; c, the ear bones and cartilages undivided, external view.

entia.

in place.

Figures twice natural size, with separate details larger.

a, the squamosal, external side; b, apex of ceratohyal, with hyoquadrate ligament.

FIG. 10. Xmoptu cukurutus, partly from behind, with quamod in place. FIG. XI. S~reocycZops incrussutm, squamosal in place; a, stapes and ear bones

FIG. 12. Ran0 pretiosu, squamosal in place; u, ear bones and vert idy divided and cartilages.

aailpga.

310 COPZ.

EXPLANATION OF PLATE XXIV.

FIG. I. Rura vircsccns, adult, X 2; a, squamosal bone; S, ear bones without epiatapedial.

FIG. 2. R a m vircscens, larva with hind legs, and developed fore legs concealed, the skull X 2; a, the hyoid apparatus from below, x 4. FIG. 3. Runa cafcsbcyana, larva further advanced than that represented in Fig. 2;

showing the first appearance of the auditory cartilages at ST and AT. FIG. 4. Trinrerorkackis in-is of the Permian bed of Texas; part of skdl from

below, showing columella at st. ; natural sue. FIG. 5 . Trimerorkackis insignis basicranial axis from below, without stapes;

natural size. FIG. 6. ZWackys s@rutus, upper posterior part of skull from above; natural

sue. FIG. 7 . Zatvackys s ~ r u f u s , inferior view of external part of posterior part of

skull of individual represented in Fig. 6; showing columella.

EXPLANATION OF LF3TERING.

AT., Annulus tympanicus; B.O., basioccipital; C.Br., Ceratobranchial; C.H., Ceratohyal; C. Tr.. Cornu trabeculi; E.S., Epistapedial; Efk., Ethmoid; Ex.O., Ex- occipital; F.P., Frontoparietal; Hm., Hyomandibular; H. Q., Hyosuspensorial liga- ment; Int, Intercalare; LSt., Interstapedial; ’j? Jugal; LI., Lower labial cartilage; MA, Meckel’s cartilage; Mx., Maxillary; Mn., Mandible; M.S., Mesostapedial; O.C., Occipital condyle; P., Parietal; Par., Parasphenoid; Px., Rerygoid; Pm., Premaxillary ; Pob., Postorbital arch; Q., Quadrate; Q. C., Quadrate cartilage; S., St., Stapes; Sq., Squamosal; SI., Superior labial cartilage; T., Trabeculum; Ty., Posi- tion of Membranum tympani.

Cartilage, blue; ligament and membrane, yellow; bone, white.