Neotropical Hylid Frogs, Genus Smilisca Part 8

Nine recently metamorphosed young were found on vegetation at the edges of streams in April. These specimens have snout-vent lengths of 13.1 to 15.7 mm. (14.9 mm.) and in life were pale greenish tan or olive-tan above and white below. The hands, feet, and thighs were pale yellowish tan.

_Remarks._--The foregoing synonymies indicate that confusion has existed in the application of various names, to this species, as well as in use of the names _sordida_ and _gabbi_ to include the species that we describe and name _Smilisca sila_. Correct allocation of the names involved was possible only after studying and comparing the type specimens, for the descriptions given by the various authors are not sufficiently explicit to determine the nature of many essential features.

The presence of a rounded snout and a long white throat in males distinguishes _S. sordida_ from _S. sila_, which has a high truncate snout and short dark throat in males. The two syntypes of _Hyla sordida_ Peters, 1863, (ZMB 3141) are males having snout-vent lengths of 36.9 and 37.0 mm. The two syntypes of _Hyla gabbi_ Cope, 1876 (USNM 30658-9), are females having snout-vent lengths of 52.8 and 53.7 mm., respectively.

Also included in the collections made by Gabb is eastern Costa Rica are two males (USNM 30685-6), which Cope (1876) named and described as _Hyla nigripes_. These specimens are soft and faded, but are recognizable as the same as _Hyla sordida_ Peters; the syntypes of _Hyla nigripes_ have snout-vent lengths of 37.6 and 37.7 mm. We have examined one of the syntypes of _Hyla salvini_ Boulenger, 1882 (BMNH 1947.2.24.13), a female having a snout-vent length of 54.6 mm. We are convinced that all of these type specimens are representatives of one species, the earliest name for which is _Hyla sordida_ Peters, 1863. The type localities for three of the named species are in Costa Rica--_H. gabbi_ from Sipurio on the Caribbean lowlands, _H. nigripes_ from the Caribbean slopes of Pico Blanco, and _H. salvini_ from Cartago on the Meseta Central. The type locality of _H. sordida_ was given as "Veraguas" by Peters (1863). At that time Veraguas was often considered to be most of western Panama.

Though we have not seen Panamanian specimens other than the types of _S.

sordida_ and one specimen from the Pacific lowlands of western Panama, the species probably occurs on the Caribbean slopes of western Panama.

The species has been taken on the Caribbean lowlands of Costa Rica within a few kilometers of Panama; collecting on the Caribbean slopes in the provinces of Bocas del Toro and Veraguas should reveal the presence of _Smilisca sordida_ there.

_Distribution._--_Smilisca sordida_ is found along the Pacific slopes and lowlands from Guanacaste, Costa Rica, southeastward to extreme western Panama, to elevations of about 1200 meters on the Meseta Central in Costa Rica, and on the Caribbean slopes and lowlands of Costa Rica and probably adjacent Panama (Fig. 5). One specimen purportedly comes from "Rio Grande, Nicaragua."

[Ill.u.s.tration: FIG. 5. Map showing locality records for _Smilisca sordida_.]

_Specimens examined._--412, as follows: NICARAGUA: "Rio Grande"

(? Depto. Zelaya), MCZ 2634.

COSTA RICA: =Alajuela=: Between Atena and Salto de San Mateo, USC 6185; 8 km. N Ciudad Quesada, USC 7155 (4); La Fortuna, USC 7153 (20); 3 km. E La Fortuna, USC 7150; San Carlos, USNM 29969; Sarchi, KU 32990-9, 36792-3.

=Cartago=: Cartago, BMNH 1947.2.24.13; headwaters of Rio Pacuare, USC 119; Inst.i.tuto Interamericano de Ciencias Agricolas, Turrialba, KU 37012, USC 420, 437; Rio Reventazon, Turrialba, MCZ 29268: 10 km. N Rio Reventazon bridge, USC 7073; 5 km. SW Rio Reventazon bridge on Paraiso-Orosi road, USC 669; Turrialba, UMMZ 118405, USC 455, USNM 29936-9.

=Heredia=: Puerto Viejo, KU 36791.

=Guanacaste=: Las Canas, USC 7164; Santa Cecilia, MCZ 7924-5; Tilaran, USC 7161 (5).

=Limon=: Bambu, USC 7171 (2), 7183 (13); La Lola, USC 820 (6), 6083-94, 8064, 8071; Pandora, USC 7188 (7), 7189, 7190 (3), 7191 (5); Pico Blanco, USNM 30685-6; Rio Lari, 14-16 km. SW Amubre, USC 7179, 7180 (10); Sipurio, USNM 30658-9; Suretka, KU 36764, 36765 (skeleton), 36766-78.

=Puntarenas=: 6 km. N Dominical, KU 91749-50, 91811 (young), 91812 (tadpoles); Esparta, MCZ 8028; 6 km. E Golfito, KU 91718-41, 91809 (young), 91810 (tadpoles), 91816-9 (skeletons), USC 7103 (23); Quebrada Agua Buena, 3 km. SW Rincon de Osa, USC 7236 (6); Quebrada Boruca, 22 km. E Palmar Norte, KU 64264; Rincon de Osa, Camp Seattle, UMMZ 123680-5, S-2792 (skeleton), USC 705 (5), 6023, 7254; Rio Barranca, USC 7119 (2); Rio Ceiba, 6 km. NW Buenos Aires, KU 91747-8, USC 7112 (7); Rio Ciruelitas, 16 km. NW Esparta, USC 7121 (3); Rio Claro, 14.2 km. NW Villa Neily, USC 7110 (4); Rio Ferruviosa, 7 km. S Rincon de Osa, USC 7235 (4); Rio Lagarto at Pan-American Hwy. (Guanacaste Border), USC 7122 (4); Rio La Vieja, 30 km. E Palmar Norte, KU 87684 (tadpoles), 91743-6, USC 7083 (2); Rio Oro, 28.5 km. NW Villa Neily, KU 91742; Rio Volcan, 10 km. W Buenos Aires, USC 7113; Rio Zapote, 7 km. E Palmar, USC 7100 (4); 3-5 km. W Palmar, USC 7101 (18); 7 km. SE Palmar, KU 64261-3; 1.2 km. NW Villa Neily, USC 8032; 3 km. NW Villa Neily, USC 7109 (20); 5 km. NW Villa Neily, USC 6176, 8035.

=San Jose=: Bajos de Jorco, KU 91813 (tadpoles); Escazu, KU 34863, 34869-75, USC 813; between Monrovia and La Hondura, 0.5 km. N Santa Rosa, USC 302 (2); Paso Ancho, Rio Jorco, UMMZ 122649 (6), USC 530 (3); Rio Jorco, near Desamparados, KU 91757-65, 91796-7, 91820-3 (skeletons), USC 228, 513, 7117 (7); Rio Peje, 10 km. SSE San Isidro el General, USC 7115 (3); Rio Tirivi, MCZ 7972; San Isidro el General, CNHM 101096, KU 28201, 32989, UMMZ 72024; 15 km. WSW San Isidro el General, KU 64245-56, 68473 (tadpoles), 68474 (young), 68475 (tadpoles), 86516, 91754-6, 91793-5, USC 7097 (6); 17.1 km. WSW San Isidro el General, USC 6047; 18 km. WSW San Isidro el General, USC 689; 20 km. WSW San Isidro el General, KU 64257-9, 64260 (skeleton), 68468 (young), 68469 (tadpoles), 68470 (young), 68471-2 (tadpoles), 68476 (young), 68633-4 (skeletons), 91751-3; San Jose, AMNH 7501-4, USC 298; Santa Rosa, Rio Virilla, USC 7145.

PANAMA: =Chiriqui=: Rio Jacu, 5.8 km. ESE Paso Canoas, KU 91905.

"Veraguas," ZMB 3141 (2).

a.n.a.lYSIS OF MORPHOLOGICAL CHARACTERS

Osteology

In attempting to a.s.say the taxonomic significance of skeletal differences we are faced with a dearth of data on the skeletons of frogs in general and hylids in particular. Recent reviews by Brattstrom (1957) and Hecht (1962, 1963) have been concerned with general salientian cla.s.sification and phylogeny, princ.i.p.ally at the family level. Savage and Carvalho (1953), Griffiths (1959), and Baldauf (1959) used osteological characters in determining the taxonomic status of the families Pseudidae, Brachycephalidae, and Bufonidae, respectively.

Carvalho (1954) presented osteological evidence for the generic separation of New World microhylids. Zweifel (1956) and Tihen (1962) used osteological characters at the levels of the species-group and species in their respective studies on _Scaphiopus_ and _Bufo_. Little has been recorded about the skeletons of the hylids. Goin (1961) mentioned dentigerous elements and cranial co-ossification in his synopsis of the genera of hylids. Copland (1957) in his review of the _Hyla_ of Australia, Funkhouser (1957) in her revision of _Phyllomedusa_, and Zweifel (1958) in his review of _Nyctimystes_ did not consider skeletal characters.

Some osteological studies on hylids have yielded worthwhile information.

Mittleman and List (1953) used osteological characters in defining the genus _Limnaoedus_: Starrett (1960) used cranial characters in combination with jaw musculature in defining the genus _Smilisca_, and Duellman (1964) used cranial characters in delimiting the _Hyla bistincta_ group. Brief descriptions of cranial structure were given for _Phrynohyas_ (Duellman, 1956) and _Ptychohyla_ (Duellman, 1963a); specific and s.e.xual differences in the skulls of _Hyla chaneque_ and _Hyla taeniopus_ were pointed out by Duellman (1965). Stokely and List (1954) described early cranial development in the hylid _Pseudacris triseriata triseriata_.

Because our knowledge of the skeleton in hylids is so incomplete, we are not attempting to place _Smilisca_ in the general scheme of hylid phylogeny on the basis of skeletal characters. Instead, our purposes are to describe the skeleton and its ontogenetic development in one member of the genus (_S. baudini_), and to make comparisons that show taxonomic differences in osteological characters among species of _Smilisca_.

The study of 68 dried skeletons and 25 cleared and stained preparations, including an ontogenetic series of _S. baudini_, has resulted in an understanding of the progressive development of skeletal elements and a knowledge of interspecific and intraspecific variation in these elements. Furthermore, investigations of the osteology have provided correlations between some cranial characters and certain aspects of external morphology.

_Descriptive Osteology of Smilisca baudini_

The following description is based primarily on an adult female (KU 68184):

_Skull._--The skull is large, solid, and broader than long; the greatest width is between the sutures of quadratojugal and maxillary on either side of the skull (Pls. 2-3). The maxillaries bear well-developed dorsal f.l.a.n.g.es, curve gently, join the moderately convex premaxillaries anteriorly and form a slightly truncate snout. The combined premaxillary width is about one-fourth the width of the skull. The premaxillaries are separated medially, and laterally from the maxillaries by sutures. Each premaxillary bears a dorsomedial alary process, which is anteriorly convex and four times as high as the depth of the lateral wing of premaxillary; each premaxillary also has a ventromedial palatine process that projects dorsally from the lingual edge of the premaxillary. The septomaxillaries are closely a.s.sociated dorsally with the premaxillaries immediately lateral to the prenasal processes.

The nasals are large, widest anteriorly and narrowing posteriorly, parallel to maxillaries, and not separated from the ethmoid by cartilage. The nasals bear long, delicate maxillary processes extending nearly to the maxillaries. Anteriorly, the nasals are widely separated by the partially ossified internasal septum, which is in contact with the premaxillaries between the prenasal processes; the anterior points of the nasals lie approximately one-half the distance between the anterior ends of the ethmoid and the premaxillaries. The ethmoid is large and completely ossified; the margins are smooth. The trunate anterior edge lies between the nasals and is in contact with the internasal septum. The frontoparietals are large, smooth-margined, and bear large supraorbital f.l.a.n.g.es curving posterolaterally at the rear of the orbit. A small, oval foramen involves the posterior part of the ethmoid and anterior portion of frontoparietals; continued ossification in older specimens fills in the foramen, thereby resulting in a solidly roofed cranium. The auditory regions are relatively ma.s.sive and bear narrow tegmen tympani; the distal ends of the tegmen tympani are medial to the lateral edge of the pterygoids in dorsal view. The squamosals are large; the long anterior arm is separated from the maxillary by a suture. The delicate, spindle-shaped columellae lie ventral to the tegmen tympani and squamosals, are spatulate distally, and have a broad basal attachment to the auditory region.

The vomers are moderately large and are in contact anteriorly with the premaxillaries and posteriorly with the ethmoid. Each vomer has two wide serrated f.l.a.n.g.es laterally. The tooth-bearing parts of the vomers are widely separated and at a slight angle to one another; the vomers terminate medially in two pointed processes on the ethmoid. The palatines are edentate, but bear strong ridges throughout their lengths.

They are broadly in contact with the maxillary, are narrow medially, and are attached by pointed processes to the medial part of the ethmoid.

The pterygoids are large, attached to the maxillaries immediately anterior and medial to the squamosal-maxillary connection, bear well-developed pedicles, which are broadly attached to the prootic, and a wide wing is in contact posteriorly with the distal two-thirds of the quadrate.

The angular makes up most of the lower jaw, bears a broad articular surface posteriorly, and has a small coronoid process on the lingual edge; anteriorly the angular is separated from the dentary and mentomecklian by Meckel's cartilage. The dentary lies external to the angular and extends from the mentomecklian to approximately the mid-length of the angular. The mentomecklians are ossified, but separated by cartilage medially.

_Hyoid._--The hyoid plate is curved, thin, and mostly cartilaginous, but calcined posteriorly (Fig. 6). The anterior cornua are slender, cartilaginous, and curve anteromedially from the hyoid plate and thence laterally and posteriorly, to attach to the posterior surface of the prootics. The lateral cornua are broad, flat, cartilaginous lateral extensions from the bases of the anterior cornua. The posterior cornua are bony, except distally.

[Ill.u.s.tration: FIG. 6. Ventral view of hyoid apparatus of an adult male _Smilisca baudini_ showing areas of muscle attachment: _Gen.

L._, attachment of geniohyoideus lateralis; _Gen. M._, attachment of geniohyoideus medialis; _Hyo._, attachment of hyoglossus; _Omo._, attachment of omohyoideus; _Pet._, petrohyoideus; _St._, attachment of sternohyoideus. KU 64220, 5.]

_Vertebral Column._--The atlas lacks transverse processes and a neural crest, whereas transverse processes are present on the other seven presacral vertebrae, and k.n.o.blike neural crests are present on the second, third, and fourth vertebrae; a faint neural ridge is visible on the fifth vertebra. The transverse processes are directed laterally on the second and sixth vertebrae, ventrolaterally on the third, posterolaterally on the fourth and fifth, and anterolaterally on the seventh and eighth. The processes are slightly expanded on the fourth, and more so on the fifth, vertebra. The sacral diapophyses are expanded and have a border of calcified cartilage laterally. There are two sacral condyles. The slender coccyx has a thin dorsal ridge on the anterior three-fourths of its length.

_Pectoral Girdle._--The omosternum is large, ovoid, and cartilaginous; the sternum is a thin cartilaginous sheet deeply notched posteriorly and is not differentiated into episternal and xiphisternal elements. The coracoids are robust, twice as stout as the clavicles. The epicoracoidal cartilages overlap in the usual arciferal manner, except that they are fused anteriorly between the slender clavicles. The clavicles are strongly arched. The clavicle, coracoid, and scapula on each side form a bony articulation at the glenoid fossa. A bifurcation of the ventral end of the scapula results in a large glenoid foramen. The scapula is flat and expanded dorsally; the suprascapula is broad, flat, and calcified in large adults. In young specimens no distinct ossification of the cleithrum or ossification of endochondral centers are evident.

_Arm and Hand._--The humerus is equally well-developed in both s.e.xes and has a prominent lateral crest. The radius and ulna are completely fused.

A bony prepollex is present in both s.e.xes. The metacarpals are about equal in length. The phalangeal formula is 2-2-3-3; the terminal phalanges are claw-shaped.

_Pelvic Girdle._--The ilia are long, slender, and slightly curved. A thin ridge projects laterally from the dorsal edge of the posterior one-half of each ilium. The ilial prominence is large and k.n.o.blike when viewed from above. The anterior edge of the ilial prominence is at the level of the anterior edge of the acetabular border. The dorsal acetabular expansion is small. The pubis is slender, and the ischium is elevated and robust.

_Leg and Foot._--The slightly curved femur has a distinct crest proximally on the posterior surface. The nearly straight tibio-fibula is slightly longer than the femur. The tibial and fibial elements are completely fused but have a distinct cleft between them. A small foramen exists at the mid-length of the tibio-fibula. The fibulare (calcaneum) is much more robust than the tibiale (astragalus). The prehallux is large and flat. The metatarsals of the third, fourth, and fifth digits are equal in length; the metatarsal of the second is somewhat shorter, and that of the first is much shorter. The phalangeal formula is 2-2-3-4-3; the terminal phalanges are claw-shaped.

_Developmental Cranial Morphology of Smilisca baudini_

The following description of development of the skull of _Smilisca baudini_ is based on the examination of 12 cleared and stained specimens. In table 3 the cranial bones are listed in the left hand column in the approximate order of their appearance in the young frogs.

Across the top of the table selected specimens designated by developmental stage or snout-vent length are listed. It should be noted that although each individual, from left to right, has an increasing number of ossified bones, the correlation with increasing size is imperfect; the precise ages of the individuals are unknown.

The first bones to appear are the septomaxillaries, frontoparietals, part of the exoccipital, and the parasphenoid in developmental stage 40.

The frontoparietals are represented by two slender ossifications dorsomedial to the orbits; the septomaxillaries are present as small ossifications anterior to the nasal capsules (Pl. 1A). The parasphenoid is present as a faint median ossification, and the exoccipital shows some ossification.

Table 3.--The Order of Occurrence of Cranial Ossifications in the Skull of Smilisca baudini. Where Numbers Are Divided by a Slash Mark, the Left and Right Symbols Correspond to the Left and Right Sides of the Skull, Respectively.

=====================+=====+=====+=====+=====+=====+=====+==== Bone |Stage|Stage|12.6 |13.9 |32.0 |27.0 |20.1 | 40 | 44 | mm. | mm. | mm. | mm. | mm.

---------------------+-----+-----+-----+-----+-----+-----+---- Frontoparietal | X | X | X | X | X | X | X Parasphenoid | X | X | X | X | X | X | X Septomaxillaries | X | X | X | X | X | X | X Exoccipitals | X | X | X | X | X | X | X Squamosals | -- | X | X | X | X | X | X Premaxillaries | -- | X | X | X | X | X | X Maxillaries | -- | X | X | X | X | X | X Nasals | -- | -- | X | X | X | X | X Pterygoids | -- | -- | X | X | X | X | X Vomers | -- | -- | -- | X | X | X | X Palatines | -- | -- | -- | X | X | X | X Quadratojugals | -- | -- | -- | X | X | X | X Ethmoid | -- | -- | -- | -- | X | X | X Columellas | -- | -- | -- | -- | X | X | X Supraorbital f.l.a.n.g.es | -- | -- | -- | -- | -- | X | X Prootics | -- | -- | -- | -- | -- | -- | X Vomerine Teeth | -- | -- | 1/1 | 4/3 | 5/5 | 3/3 | 5/4 Maxillary Teeth | -- | 0/7 | 3/5 | 6/5 |30/31|30/26|37/36 Premaxillary Teeth | -- | 2/4 | 3/3 | 5/5 | 7/6 | 8/6 | 8/7 ---------------------+-----+-----+-----+-----+-----+-----+----

The dentigerous bones are among the most rapidly developed, although not the first to appear. They are present in developmental stage 44 before metamorphosis is completed. The maxillaries bear a few teeth anteriorly and are ossified posteriorly to a point one-third of the distance from the anterior to the posterior edge of the orbit. Ossification lengthens the posterior termini of the maxillaries to the posterior edge of the orbit. In front of the anterior margin of the orbit, bone is proliferated dorsal to the main axes of the maxillaries and forms moderate dorsal maxillary f.l.a.n.g.es. The premaxillaries appear simultaneously with the maxillaries. Initially they are widely separated medially from each other, and laterally from the developing maxillaries; each bears two or three teeth, large dorsally blunt alary processes, and small palatine processes. The median and lateral edges of the prenasal processes lengthen heterochronously, causing the median edges to be longest and to lie slightly dorsal to the level of the septomaxillaries.

After the maxillaries and premaxillaries develop, the vomers appear as small horizontal ossifications anterior to the parasphenoid.

Ossification begins in the lateral f.l.a.n.g.es, then in the prevomerine processes, and lastly in the posterior dentigerous parts of the bones; the prevomerine processes are the last parts of the vomers to ossify completely.