Comparative OsteologyThe genusSmiliscais characterized by the following combination of cranial osteological characters: (1) A large amount of bone is involved in the skull and a minimal amount of cartilage and/or secondarily ossified cartilage; co-ossification is absent. (2) The skulls are uniformly broad with angular lateral margins, and truncate anteriorly. (3) An internasal septum and quadratojugals are present. (4) A well-developed squamosal minimally extends one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally is separated from the maxillary by a suture. (5) The ethmoid is large; the distance between the anterior end of the ethmoid and the anterior edge of the premaxillary varies between 15 and 20 per cent of the total length of the skull.On the basis of cranial osteology two species-groups can be recognized within the genusSmilisca. Thesordidagroup, comprisingS. sordidaandpuma, is characterized by a broad skull in which the lateral margins of the maxillaries are relatively straight anterior to the orbit. The moderate-sized nasals are rounded anteriorly, and bear relatively short, sometimes blunt, maxillary processes. The long axes of the nasals are not parallel to the maxillaries. The ethmoid isproportionatelysmall in thesordidagroup. The bony part of the ethmoid terminates near the anterior edge of the orbits and does not extend anteriorly between the nasals; the entire anterior margin of the ethmoid is separated from the nasals by cartilage. The squamosals are generally small. They are narrow in dorsal view, and minimally extend one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally, two-thirds the distance. The tegmen tympani are relatively small (Fig. 8).Fig. 8.Dorsal views of the skulls of the species ofSmilisca: (A)S. baudini(KU 68184); (B)S. puma(KU 68636); (C)S. phaeota(KU 41090); (D)S. sila(KU 80625); (E)S. cyanosticta(KU 55938), and (F)S. sordida(KU 36765). ×1.5.In contrast to the tendency for reduction of cranial parts in thesordidagroup, thebaudinigroup, constituted byS. cyanosticta,phaeota, andbaudini, is characterized by more ossification of the cranial elements. The skull is broad; the lateral margins are less angular and are gently curved, rather than straight as in thesordidagroup. The nasals tend to be larger with the long axes parallel to the maxillary. Anteriorly the nasals are pointed, and posteriorlythey bear long, delicate palatine processes extending to the maxillary. The ethmoid is fully ossified, extends anteriorly between the nasals, and laterally is separated by a suture from the nasals if the latter are fully ossified. The squamosals are large, and wide in dorsal view. They minimally extend one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally are sutured to the maxillary. The tegmen tympani are massive.Smilisca silais intermediate between the two species-groups described. The skull is broad; the lateral margins are gently curved, and have a pronounced angularity just anterior to the palatines which results in a broad, truncate snout. The nasals are moderate in size; because of the anterior angularity of the lateral margins, the long axes of the nasals lie parallel to the maxillary. The nasals are only slightly pointed anteriorly, and posteriorly they bear short, blunt palatine processes and medial processes in contact with the lateral corners of the ethmoid. The ethmoid is fully ossified, but does not extend anteriorly between the nasals. The squamosals are moderate in size and extend one-fourth the distance from the dorsal end of the quadrate to the maxillary. The tegmen tympani are relatively large, but proportionately short.The cranial characters utilized in the analysis of species groups (general shape, nature of the nasals, ethmoid, squamosals, and tegmen tympani), together with other characters, such as the relative height and shape of the prenasal processes, the extent of the internasal septum, and the nature of the vomers, frontoparietals, maxillaries and pterygoids are useful in distinguishing the various species (Table 4, Fig. 8), as well as in establishing relationships within the species-groups.Within thesordidagroup,S. sordidaandS. pumacan be distinguished by the following characters: The bony part of the ethmoid terminates posterior to the anterior edge of the orbit and is thus widely separated from the nasals by cartilage inS. puma. InS. sordidathe bony part of the ethmoid always terminates at a level equal to, or slightly in front of the anterior edge of the orbit; therefore, less cartilage exists between the ethmoid and nasals inS. sordidathan inS. puma. The width of the premaxillary comprises about 30 per cent of the width of the skull inS. sordidaand 20 per cent inS. puma. The proportion of the length of the skull anterior to the bony part of the ethmoid inS. sordidais approximately 21 per cent, as compared with about 29 per cent inS. puma. The prenasal processes are convex inS. sordidaand straight inS. puma.The marked ontogenetic variation inS. sordidais considered in more detail in the account of that species, but it is pertinent to the present discussion to note that with respect to some features of the skull some young breeding specimens ofS. sordidaare intermediate in appearance between large females ofS. sordidaand adults ofS. puma. In some breeding males (usually the smaller individuals) ofS. sordidathe bony part of the ethmoid terminates at the anterior edge of the orbit and is widely separated from the nasals by cartilage. In small individualsS. sordida, especially in males, and in adults ofS. pumathe tegmen tympani are relatively short, whereas in adult females ofS. sordidathese elements are long and slender. In the smaller specimens ofS. sordidaand inS. pumathe squamosal is small; it extends only about one-fourth of the distance to the maxillary in the smallerS. sordidaand about one-half the distance inS. puma. The more massive squamosal in large adult females ofS. sordidaextends at least two-thirds of the distance to the maxillary.Table 4.—Comparative Cranial Osteology of Smilisca.CharacterS. baudiniS. cyanostictaS. phaeotaS. pumaS. silaS. sordidaAlary ProcessesFour times as high as lateral wing of premaxillary; anteriorly convex.Three times as high as lateral wing of premaxillary; anteriorly convex.Two and one-half times as high as lateral wing of premaxillary; anteriorly convex.Two times as high as lateral wing of premaxillary; straight.One and one-half times as high as lateral wing of premaxillary; straight.Two and one-half times as high as lateral wing of premaxillary; slightly convex anteriorly.NasalsLong, wide anteriorly, narrowing posteriorly; attached to ethmoid.Long, widest posteriorly; attached to ethmoid.Long, widest anteriorly and posteriorly, bearing posteromedial process; not attached to ethmoid.Short, narrow, not attached to ethmoid.Short, wide, bearing small posteromedial processes; not attached to ethmoid.Moderately long narrowest anteriorly and posteriorly; not attached to ethmoid.EthmoidLong; entirely ossified; smooth margins.Long, entirely ossified; smooth margins.Long, entirely ossified; smooth margins.Short, about two-thirds ossified; irregular margins.Moderately long; entirely ossified; smooth marginsShort; one-half to entirely ossified; irregular margins.FrontoparietalSmall, ovid fontanelle present or absent; long, pointed postorbital processes curving along posterior border of orbit.Large fontanelle, two and one-half times as long as wide; narrow supraorbital flanges with irregular margins.Fontanelle absent; large supraorbital flanges having straight edges and extending posterolaterally.Keyhole-shaped fontanelle; smooth margins; flanges absent.Large, ovoid fontanelle; smooth margins; flanges absent.Large, elongate fontanelle; smooth margins; flanges absent.SquamosalLarge: anterior arm in contact with maxillary.Large; anterior arm in contact with maxillary.Large; anterior arm extending 1/2-2/3 way to maxillary.Small; anterior arm extending 1/2 way to maxillary.Moderately large; anteriorarm extending 1/4 way to maxillary.Moderately small; anterior arm extending 1/4-2/3 way to maxillary.Within thebaudinigroup, the skull ofS. cyanostictais the most generalized of the three species; the cranial characters are intermediate betweenS. phaeotaandS. baudini. The lateral margins of the skull inS. cyanostictaare gently curved, and have an angularity anterior to the palatine-maxillary suture; the anterior margins are less angular inS. phaeota, which has a broader snout. Posteriorly inS. baudinithe margins are slightly curved medially, and the greatest width of the skull is between the quadratojugal-maxillary sutures on either side of the skull. The frontoparietals ofS. cyanostictabear slightly irregular lateral margins and a large fontanelle. There is a tendency for obliteration of the fontanelle with increasing age in bothS. baudiniandS. cyanosticta; the lateral margins of the frontoparietals bear large supraorbital flanges in both of these species. InS. phaeotathe flanges are most prominent; they extend posterolaterally with straight margins along two-thirds of the length of the orbit and terminate in rather blunt points. The broad interorbital flanges result in a relatively broad external interorbital distance. InS. baudinithe flanges are curved posterolaterally around the orbit and terminate in sharp, thin points. The tegmen tympani of all three species are massive. InS. cyanostictathe proötics slope posteriorly, whereas they slope anteriorly inS. baudiniandS. phaeota.The skulls ofS. cyanostictaandS. baudiniare alike in certain respects. The squamosals of both species are large and connected to the maxillary by a bony connection; the squamosals ofS. phaeotaare large, but extend only two-thirds of the distance from the dorsal end of the quadrate to the maxillary. InS. baudiniandS. cyanostictathe nasals are separated throughout their lengths from the ethmoid, whereas the nasals ofS. phaeotaare separated from the ethmoid by cartilage. The latter separation is due to an incomplete ossification of the nasals inS. phaeota. The bony part of each nasal is constricted in the middle of the long axis of the bone, and the nasals are widest anteriorly; posteriorly each nasal bears a medial process, which is narrowly separated from the lateral edge of the ethmoid.Table 5.—Variation in the Number of Teeth in the Species of Smilisca. (All Are Males; N = Number of Jaws, or Twice the Number of Individuals; Means Are Given in Parentheses After the Observed Ranges.)SpeciesNMaxillaryPremaxillaryVomerineS. baudini2049-65 (56.0)9-16 (13.6)5-9 (7.2))S. cyanosticta850-64 (57.9)10-12 (10.8)4-11 (7.1))S. phaeota2050-68 (58.1)10-15 (12.1)5-9 (7.3))S. puma660-67 (63.6)11-13 (12.0)4-7 (5.3))S. sila848-60 (52.9)10-14 (11.3)5-7 (5.7))S. sordida1239-55 (44.2)7-11 (9.3)4-6 (5.2)The teeth of all species ofSmiliscaare spatulate and bifid. The numbers of maxillary, premaxillary, and vomerine teeth are summarized in Table 5. Smaller and presumably younger specimens of all species ofSmiliscahave fewer teeth than do larger specimens of the same species. This correlationbetween size and number of teeth does not exist as an interspecific trend within the genus; for example, the smallest species in the genus,S. puma, has the highest number of maxillary teeth. In small specimens of a given species wide gaps are present between the maxillary teeth posteriorly; in large specimens the gaps are filled by teeth, beginning anteriorly and progressing posteriorly, until the maxillary dentition is continuous.MusculatureNo extensive study of the muscular system was undertaken, but certain muscles know to be of taxonomic importance were studied.Jaw Musculature.—Starrett (1960) pointed out the unique jaw musculature inSmilisca. In this genus M. depressor mandibulae consists of two parts, one arising from the dorsal fascia and one from the posterior arm of the squamosal. Two muscles arise from the anterior arm of the squamosal and insert on the lateral face of the mandible. Of these muscles, M. adductor mandibulae posterior subexternus lies medial to the mandibular branch of the trigeminal nerve; the other, M. adductor mandibulae externus superficialis, lies lateral to the same nerve (Fig. 9). In most other hylids the latter muscle is absent. No significant variation in the position of the muscles was noted in the various species ofSmilisca, though M. adductor mandibulae originate somewhat more anteriorly inS. baudiniandS. cyanostictathan in the other members of the genus, all of which have a shorter anterior arm of the squamosal that does not reach the maxillary. The two separate parts of M. depressor mandibulae are not so widely separated in members of thesordidagroup as in thebaudinigroup.Fig. 9.Lateral view of the left jaw ofSmilisca baudini;A. M. E. S., adductor mandibulae externus superficialis;A. M. P. S., adductor mandibulae posterior subexternus;Col., columella;D. M.depressor mandibulae;M. B. T. N., mandibular branch trigeminal nerve;Sq., squamosal. KU 64214, ×5.Fig. 10.Ventral view of throat musculature in an adult maleSmilisca baudini(Superficial musculature on left, deep musculature on right);A. C.anterior cornua of hyoid;Gen. L., geniohyoideus lateralis;Gen. M., geniohyoideus medialis;Hyo., hyoglossus;Omo., omosternum;Pet., petrohyoideus;S., submentalis;Sm., submaxillaris;St., sternohyoideus;V. S., vocal sac. KU 64220, × 2.5.Throat Musculature.—The frogs that comprise the genusSmiliscaare characterized by paired subgular vocal sacs, essentially the same as those inTriprion(Duellman and Klaas, 1964). The following description is based onSmilisca baudini(Fig. 10).M. submentalis lies in the anterior angle of the lower jaw, is thick, and consists of transverse fibers extending between the dentaries. M. submaxillaris is thin and arises from the whole of the inner surface of the lower jaw, except for the anterior angle occupied by M. submentalis. Anteriorly M. submaxillaris is broadly attached by fascia to M. hyoglossus and M. geniohyoideus, which lie dorsal to M. submaxillaris. Medially this attachment continues posteriorly for about one-half the length of the hyoglossus. Posteriorly M. submaxillaris is folded and attached to M. sternoradialis of the pectoral girdle. The vocal sacs are formed by a pair of posterolateral evaginations of M. submaxillaris; a broad connection between the pouches allows free passage of air between the pouches.The deeper throat musculature is essentially the same as that described forPhrynohyas spilommaby Duellman (1956), except for slight differences in the place of attachment on the hyoid.SKINStructureThe skin ofSmiliscais typical of that of most hylids in organization and structure.Smilisca silais distinguished from other members of the genus by the presence of small wartlike protrusions and peculiar white, pustular spots on the dorsum. The wartlike structures are composed of three or four epidermal cells, which protrude from the surface of the epidermis; the structures are covered by a slightly thickened layer of keratin. The white pustules are slightly elevated above the surrounding skin. Internally they consist of aggregationsof swollen, granular, pigment-cells (perhaps lipophores) lying between the epidermis and the melanophores.Biochemical VariationsDried skins of all species ofSmiliscawere sent to José M. Cei, Instituto Nacional de Cuyo, Mendoza, Argentina, for biochemical screening by means of the chromatographic techniques described by Erspamer and Cei (1963). The species in thebaudinigroup have detectable amounts of penta-hydroxi-trypatamine, whereas only a trace is present in the other species. Furthermore, species in thebaudinigroup differ fromS. silaand thesordidagroup in lacking, or having only a trace of, tryptophan-containing polypeptides. These superficial biochemical tests support the arrangement of species as ascertained by conventional taxonomic characters.External Morphological CharactersThe features of external morphology that were studied in connection with the taxonomy of the genusSmiliscaare discussed below.Size and ProportionsThe frogs of the genusSmiliscaare medium to large tree frogs. The three species comprising thebaudinigroup (S. baudini,cyanosticta, andphaeota) are notably larger thanS. puma,sila, andsordida(Table 6). The largest specimen that we examined is a female ofS. baudinihaving a snout-vent length of 90 mm.Smilisca pumais the smallest species; the largest male has a snout-vent length of 38 mm. and the largest female, 46 mm.Table 6.—Comparison of Sizes and Certain Proportions of the Species of Smilisca. (Means in Parentheses Below Observed Ranges; Data for Males Only.)SpeciesNSnout-ventlengthTibia length/snout-ventTympanum/eyeS. baudini14047.3-75.942.1-53.656.1-94.4(58.7)(47.8)(73.5)S. cyanosticta4044.6-56.851.9-59.762.7-88.4(50.7)(56.0)(71.4)S. phaeota5040.8-65.550.9-60.262.7-85.5(53.9)(55.5)(76.6)S. puma2031.9-38.148.2-53.152.1-72.2(34.7)(51.3)(64.9)S. sila3331.6-44.849.7-58.147.6-58.3(37.7)(54.8)(53.2)S. sordida5531.9-44.650.5-57.146.5-57.1(37.9)(53.4)(49.1)No outstanding differences in proportions exist between species, althoughcertain proportions are sufficiently different in some species to warrant mention.Smilisca baudiniis a more squat and stocky frog than other members of the genus; this is reflected in the somewhat shorter hind legs (Table 6). The size of the tympanum relative to that of the eye is highly variable within samples of a given species. Even so, noticeable differences in the tympanum/eye ratio are apparent. Members of thebaudinigroup have the largest tympani, whereasS. silaandsordidahave the smallest, andS. pumais intermediate (Table 6).Shape of SnoutAlthough all members of the genus have rather truncate snouts, subtle differences exist among the species (Pl. 12).Smilisca silahas the shortest snout; that ofS. baudiniis only slightly longer. The snouts ofS. cyanostictaandpumaare nearly square in lateral profile, whereas those ofS. phaeotaandsordidaare slightly inclined. The shape of the snout is relatively uniform within each species and displays no noticeable sexual dimorphism, except inS. sordida, in which there are sexual differences and geographic variation (see p. 324).Hands and FeetThe characters of the hands and feet are among the most taxonomically important external features inSmilisca. Consistent differences exist in relative lengths of the digits, size of subarticular tubercles, size and number of supernumerary tubercles, size and shape of the inner metatarsal tubercle, and amount of webbing (Pls. 4 and 5). In thebaudinigroup the series of species (baudini-phaeota-cyanosticta) show a progressive increase in amount of webbing in the hand and a decrease in number, and corresponding increase in size, of supernumerary tubercles. The amount of webbing in the feet ofS. baudiniandphaeotais about the same, but the webbing is slightly more extensive inS. cyanosticta.Smilisca pumais unique in the genus in lacking webbing in the hand; furthermore, this species is distinctive in having many large subarticular tubercles on the hand and a relatively small inner metatarsal tubercle. The two stream-inhabitants,S. silaandsordida, have shorter and stouter fingers than the other species. The webbing is most extensive in both the hands and feet of these species, which also are distinctive in having many small supernumerary tubercles on the feet.Ontogenetic ChangesMinor ontogenetic changes in structure involve the shape of the snout, relative size of the eye, development of the tympanum, and amount of webbing in the hand. In recently metamorphosed young the snout is more rounded than in adults; the canthus and loreal concavity are not evident. Usually the tympanum is not differentiated in recently metamorphosed young, and the eye is proportionately large. The webbing in the feet is completely developed at metamorphosis, but young individuals have noticeably less webbing in the hand than do adults of the same species.ColorationSome of the most distinctive characters of the species ofSmiliscaare color and pattern of the living frogs. Although many chromatic features are lost or subdued in preserved specimens, the patterns usually persist.MetachrosisChange in color, well known in frogs, is common in hylids, especially in species having green dorsal surfaces (Phyllomedusais a notable exception). The non-greenSmilisca(puma,sila, andsordida) changes color, but this mostly is a change in intensity of color. In these species the markings usually are most distinct at night; frequently by day the frogs become pallid. The most striking examples of metachrosis inSmiliscaare found in thebaudinigroup, in which the dorsal ground-color changes from green to tan; correlated with the change in ground-color may be a corresponding change in the dorsal markings, but the dorsal markings may change to the opposite color.ChromosomesChromosomes of all six species ofSmiliscawere studied by means of the propriono-orcein squash technique described by Duellman and Cole (1965). Karyotype analysis was attempted for several species by means of intraperitoneal injections of colchicine, which affected the mitotic cells as desired, but the testes examined contained too few mitotic cells to allow accurate determination of karyotypes.Haploid (n) chromosome numbers were determined from cells in diakinesis, metaphase I, and metaphase II of meiosis. Diploid (2n) chromosome numbers were determined from cells in late prophase and metaphase of mitosis. Chromosome counts from as few as 23 meiotic cells ofS. phaeotaand as many as 80 cells ofS. sordidareveal a constant haploid (n) number of 12; counts of chromosomes in one to five mitotic cells in all species, exceptS. sila, reveal that the diploid (2n) number is 24.NATURAL HISTORYBreedingLike most hylid frogsSmiliscais most readily collected and observed when individuals congregate for breeding.Time of BreedingSmiliscabreeds primarily in quiet water and reaches its height of breeding activity at times of plentiful rainfall,—usually from May through October. Through most of its rangeSmilisca baudinibreeds in those months, but in some places where abundant rain falls in other seasons, the species breeds at those times. For example, in southern El Petén and northern Alta Verapaz, Guatemala,Smilisca baudinihas been found breeding in February and March. The other pond-breeding species (S. cyanosticta,phaeota, andpuma) live in regions lacking a prolonged dry season, and possibly they breed throughout the year, but breeding activity seems to be greatest in the rainiest months.The two stream-breeding species (S. silaandsordida) breed in the dry season when the streams are low and clear, principally in December through April. At high elevations the species sometimes breed in the rainy season; also, individuals sometimes breed in the short dry season (summer canicula) in July and August.At several localities species have been found breeding at different times of the year:S. baudiniin March and July at Chinajá, Guatemala;S. phaeotain April and August at Palmar Sur, Costa Rica;S. pumain February and July at Puerto Viejo, Costa Rica; andS. silain February, April, and August at El Volcan, Panamá. These observations indicate only that the population breeds at more than one time in the year, but do not provide any evidence on the breeding cycles of the individual frogs. This is one important aspect of the natural history ofSmiliscafor which we lack data.Breeding SitesAll members of the genusSmiliscapresumably deposit their eggs in water.Smilisca baudiniusually breeds in temporary rain pools; often these are nothing more than shallow, muddy puddles. In other instances the sites are extensive ditches or large flooded areas (Pl. 8, Fig. 1). This species is an opportunistic breeder, and males gather at any of a wide variety of suitable breeding sites that are formed by torrential rains in the early part of the rainy season.Smilisca baudininearly always breeds in open pools having bare earthen edges. Frequently congregations ofS. baudiniare found at such small pools, but are absent from nearby large ponds surrounded by vegetation.Little is known of the breeding habits ofS. cyanosticta, which inhabits humid forests on foothills and lowlands. Apparently its breeding sites are not unlike those ofS. phaeota, which usually are pools surrounded by vegetation (Pl. 8, Fig. 2), although sometimes males ofS. cyanostictacall from open muddy puddles. In uplands, where standing water is uncommon, this species breeds in quiet pools in streams.Smilisca pumabreeds in grass-choked ponds and marshes, where the males call from bases of dense clumps of grass in the water (Pl. 9, Fig. 1).Smilisca silaandS. sordidadiffernoticeablyfrom other species in the genus by breeding exclusively in streams, where males usually call from rocks or gravel bars in or at the edges of streams (Pl. 9, Fig. 2); sometimes individuals perch on bushes overhanging streams. In the streams, or parts of streams, utilized by these frogs the water is clear, shallow, and has a slow gradient; occasional males have been found calling along cascading mountain streams.Breeding choruses composed of ten or more species of frogs are not uncommon in Middle America, butSmiliscausually breeds alone or with one or two other species and at the most five others. This tendency towards solitary breeding possibly is the result of selection of breeding sites that are unsuitable to many other species of frogs. Nevertheless, many other species of frogs have been found at the breeding sites with the various species ofSmilisca; these breeding associates (Table 7) are most numerous forS. baudini, which has a broad geographic range, including a variety of habitats.Breeding BehaviorCalling sites.—All species ofSmiliscausually call from the ground, including rocks and gravel bars; some individuals sit in shallow water near the edge of the pool or stream. Sometimes males ofS. baudini,sila, andsordidacall from low bushes or trees near the breeding site. OneS. baudiniwas observed calling while it was floating on the surface of a pond.Smilisca cyanosticta,phaeota, andpumacall from secluded places at the edge of the water or in the water, whereasS. baudini,silaandsordidacall from open situations.Table 7.—Breeding Associates of the Various Species of Smilisca.AssociateS. baudiniS. cyanostictaS. phaeotaS. pumaS. silaS. sordidaRhinophrynus dorsalisX—————Leptodactylus bolivianus——X———Leptodactylus labialisX—X———Leptodactylus melanonotusX—XXX—Leptodactylus occidentalisX—————Leptodactylus quadrivittatus——X———Leptodactylus pentadactylus——XX—XEngystomops pustulosusX—X———Bufo canaliferusX—————Bufo cavifrons—X————Bufo cocciferX—————Bufo coniferus——X———Bufo cristatus—X————Bufo gemmiferX—————Bufo haematiticus——X—XXBufo kellogiX—————Bufo luetkeniX—————Bufo marinusX—XXXXBufo marmoreusX—————Bufo mazatlanensisX—————Bufo melanochloris——X—XXBufo perplexusX—————Bufo typhonius——X—X—Atelopus varius————XXDiaglena reticulataX—————Diaglena spatulataX—————Table 7.—ContinuedAssociateS.baudiniS.cyanostictaS.phaeotaS.pumaS.silaS.sordidaHyla boulengeri——X———Hyla colymba————X—Hyla ebraccataX—X———Hyla elaeochroa——XX——Hyla eximiaX—————Hyla legleri—————XHyla microcephalaX—X———Hyla phlebodes——XX——Hyla pictaX—————Hyla robertmertensiX—————Hyla rosenbergi——X———Hyla rufioculis—————XHyla smithiX—————Hyla staufferiX—————Hyla walkeriX—————Phrynohyas inflataX—————Phrynohyas spilommaX—————Phrynohyas venulosaX—————Phyllomedusa callidryasX—X———Phyllomedusa dacnicolorX—————Phyllomedusa moreletiXX————Pternohyla fodiensX—————Smilisca baudiniXX————Smilisca cyanostictaXX————Smilisca phaeota——X———Smilisca puma———X——Table 7.—ConcludedAssociateS.baudiniS.cyanostictaS.phaeotaS.pumaS.silaS.sordidaSmilisca sila————XXSmilisca sordida——X—XXTriprion petasatusX—————Cochranella fleischmanni————XXCentrolene prosoblepon————X—Gastrophryne elegansX—————Gastrophryne olivaceaX—————Gastrophryne ustaX—————Hypopachus alboventerX—————Hypopachus caprimimusX—————Hypopachus inguinalisX—————Hypopachus maculatusX—————Hypopachus oxyrrhinusX—————Hypopachus variolosusX—————Rana palmipesX—XX——Rana pipiensX—————Rana warschewitschi——X—XXChorus structure.—Limited observations on some of the species ofSmiliscashow a definite organization of the calling behavior of individuals.Smilisca baudiniandS. phaeotacall in duets. This is especially noticeable inS. baudini, in which the members of a duet often call from sites separated by only a few centimeters. The call ofS. baudiniconsists of a series of like notes (see description of call in following section); the duration of each note is about equal to the interval between notes. Normally one individual utters one note, pauses, and utters a single note again, or series of two or three notes. If there is no response, the first individual often waits several seconds or even several minutes and then repeats the call. The second individual usually responds after the first or second note of the sequence. The notes of the second individual usually are spaced so that they are emitted in the intervals between the notes of the first individual. This can be shown diagrammatically by havingthe figure "1" represent notes of the first individual and figure "2," the notes of the second; an empty interval is represented by "0":
Comparative Osteology
The genusSmiliscais characterized by the following combination of cranial osteological characters: (1) A large amount of bone is involved in the skull and a minimal amount of cartilage and/or secondarily ossified cartilage; co-ossification is absent. (2) The skulls are uniformly broad with angular lateral margins, and truncate anteriorly. (3) An internasal septum and quadratojugals are present. (4) A well-developed squamosal minimally extends one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally is separated from the maxillary by a suture. (5) The ethmoid is large; the distance between the anterior end of the ethmoid and the anterior edge of the premaxillary varies between 15 and 20 per cent of the total length of the skull.
On the basis of cranial osteology two species-groups can be recognized within the genusSmilisca. Thesordidagroup, comprisingS. sordidaandpuma, is characterized by a broad skull in which the lateral margins of the maxillaries are relatively straight anterior to the orbit. The moderate-sized nasals are rounded anteriorly, and bear relatively short, sometimes blunt, maxillary processes. The long axes of the nasals are not parallel to the maxillaries. The ethmoid isproportionatelysmall in thesordidagroup. The bony part of the ethmoid terminates near the anterior edge of the orbits and does not extend anteriorly between the nasals; the entire anterior margin of the ethmoid is separated from the nasals by cartilage. The squamosals are generally small. They are narrow in dorsal view, and minimally extend one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally, two-thirds the distance. The tegmen tympani are relatively small (Fig. 8).
Fig. 8.Dorsal views of the skulls of the species ofSmilisca: (A)S. baudini(KU 68184); (B)S. puma(KU 68636); (C)S. phaeota(KU 41090); (D)S. sila(KU 80625); (E)S. cyanosticta(KU 55938), and (F)S. sordida(KU 36765). ×1.5.
Fig. 8.Dorsal views of the skulls of the species ofSmilisca: (A)S. baudini(KU 68184); (B)S. puma(KU 68636); (C)S. phaeota(KU 41090); (D)S. sila(KU 80625); (E)S. cyanosticta(KU 55938), and (F)S. sordida(KU 36765). ×1.5.
In contrast to the tendency for reduction of cranial parts in thesordidagroup, thebaudinigroup, constituted byS. cyanosticta,phaeota, andbaudini, is characterized by more ossification of the cranial elements. The skull is broad; the lateral margins are less angular and are gently curved, rather than straight as in thesordidagroup. The nasals tend to be larger with the long axes parallel to the maxillary. Anteriorly the nasals are pointed, and posteriorlythey bear long, delicate palatine processes extending to the maxillary. The ethmoid is fully ossified, extends anteriorly between the nasals, and laterally is separated by a suture from the nasals if the latter are fully ossified. The squamosals are large, and wide in dorsal view. They minimally extend one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally are sutured to the maxillary. The tegmen tympani are massive.
Smilisca silais intermediate between the two species-groups described. The skull is broad; the lateral margins are gently curved, and have a pronounced angularity just anterior to the palatines which results in a broad, truncate snout. The nasals are moderate in size; because of the anterior angularity of the lateral margins, the long axes of the nasals lie parallel to the maxillary. The nasals are only slightly pointed anteriorly, and posteriorly they bear short, blunt palatine processes and medial processes in contact with the lateral corners of the ethmoid. The ethmoid is fully ossified, but does not extend anteriorly between the nasals. The squamosals are moderate in size and extend one-fourth the distance from the dorsal end of the quadrate to the maxillary. The tegmen tympani are relatively large, but proportionately short.
The cranial characters utilized in the analysis of species groups (general shape, nature of the nasals, ethmoid, squamosals, and tegmen tympani), together with other characters, such as the relative height and shape of the prenasal processes, the extent of the internasal septum, and the nature of the vomers, frontoparietals, maxillaries and pterygoids are useful in distinguishing the various species (Table 4, Fig. 8), as well as in establishing relationships within the species-groups.
Within thesordidagroup,S. sordidaandS. pumacan be distinguished by the following characters: The bony part of the ethmoid terminates posterior to the anterior edge of the orbit and is thus widely separated from the nasals by cartilage inS. puma. InS. sordidathe bony part of the ethmoid always terminates at a level equal to, or slightly in front of the anterior edge of the orbit; therefore, less cartilage exists between the ethmoid and nasals inS. sordidathan inS. puma. The width of the premaxillary comprises about 30 per cent of the width of the skull inS. sordidaand 20 per cent inS. puma. The proportion of the length of the skull anterior to the bony part of the ethmoid inS. sordidais approximately 21 per cent, as compared with about 29 per cent inS. puma. The prenasal processes are convex inS. sordidaand straight inS. puma.
The marked ontogenetic variation inS. sordidais considered in more detail in the account of that species, but it is pertinent to the present discussion to note that with respect to some features of the skull some young breeding specimens ofS. sordidaare intermediate in appearance between large females ofS. sordidaand adults ofS. puma. In some breeding males (usually the smaller individuals) ofS. sordidathe bony part of the ethmoid terminates at the anterior edge of the orbit and is widely separated from the nasals by cartilage. In small individualsS. sordida, especially in males, and in adults ofS. pumathe tegmen tympani are relatively short, whereas in adult females ofS. sordidathese elements are long and slender. In the smaller specimens ofS. sordidaand inS. pumathe squamosal is small; it extends only about one-fourth of the distance to the maxillary in the smallerS. sordidaand about one-half the distance inS. puma. The more massive squamosal in large adult females ofS. sordidaextends at least two-thirds of the distance to the maxillary.
Within thebaudinigroup, the skull ofS. cyanostictais the most generalized of the three species; the cranial characters are intermediate betweenS. phaeotaandS. baudini. The lateral margins of the skull inS. cyanostictaare gently curved, and have an angularity anterior to the palatine-maxillary suture; the anterior margins are less angular inS. phaeota, which has a broader snout. Posteriorly inS. baudinithe margins are slightly curved medially, and the greatest width of the skull is between the quadratojugal-maxillary sutures on either side of the skull. The frontoparietals ofS. cyanostictabear slightly irregular lateral margins and a large fontanelle. There is a tendency for obliteration of the fontanelle with increasing age in bothS. baudiniandS. cyanosticta; the lateral margins of the frontoparietals bear large supraorbital flanges in both of these species. InS. phaeotathe flanges are most prominent; they extend posterolaterally with straight margins along two-thirds of the length of the orbit and terminate in rather blunt points. The broad interorbital flanges result in a relatively broad external interorbital distance. InS. baudinithe flanges are curved posterolaterally around the orbit and terminate in sharp, thin points. The tegmen tympani of all three species are massive. InS. cyanostictathe proötics slope posteriorly, whereas they slope anteriorly inS. baudiniandS. phaeota.
The skulls ofS. cyanostictaandS. baudiniare alike in certain respects. The squamosals of both species are large and connected to the maxillary by a bony connection; the squamosals ofS. phaeotaare large, but extend only two-thirds of the distance from the dorsal end of the quadrate to the maxillary. InS. baudiniandS. cyanostictathe nasals are separated throughout their lengths from the ethmoid, whereas the nasals ofS. phaeotaare separated from the ethmoid by cartilage. The latter separation is due to an incomplete ossification of the nasals inS. phaeota. The bony part of each nasal is constricted in the middle of the long axis of the bone, and the nasals are widest anteriorly; posteriorly each nasal bears a medial process, which is narrowly separated from the lateral edge of the ethmoid.
The teeth of all species ofSmiliscaare spatulate and bifid. The numbers of maxillary, premaxillary, and vomerine teeth are summarized in Table 5. Smaller and presumably younger specimens of all species ofSmiliscahave fewer teeth than do larger specimens of the same species. This correlationbetween size and number of teeth does not exist as an interspecific trend within the genus; for example, the smallest species in the genus,S. puma, has the highest number of maxillary teeth. In small specimens of a given species wide gaps are present between the maxillary teeth posteriorly; in large specimens the gaps are filled by teeth, beginning anteriorly and progressing posteriorly, until the maxillary dentition is continuous.
Musculature
No extensive study of the muscular system was undertaken, but certain muscles know to be of taxonomic importance were studied.
Jaw Musculature.—Starrett (1960) pointed out the unique jaw musculature inSmilisca. In this genus M. depressor mandibulae consists of two parts, one arising from the dorsal fascia and one from the posterior arm of the squamosal. Two muscles arise from the anterior arm of the squamosal and insert on the lateral face of the mandible. Of these muscles, M. adductor mandibulae posterior subexternus lies medial to the mandibular branch of the trigeminal nerve; the other, M. adductor mandibulae externus superficialis, lies lateral to the same nerve (Fig. 9). In most other hylids the latter muscle is absent. No significant variation in the position of the muscles was noted in the various species ofSmilisca, though M. adductor mandibulae originate somewhat more anteriorly inS. baudiniandS. cyanostictathan in the other members of the genus, all of which have a shorter anterior arm of the squamosal that does not reach the maxillary. The two separate parts of M. depressor mandibulae are not so widely separated in members of thesordidagroup as in thebaudinigroup.
Fig. 9.Lateral view of the left jaw ofSmilisca baudini;A. M. E. S., adductor mandibulae externus superficialis;A. M. P. S., adductor mandibulae posterior subexternus;Col., columella;D. M.depressor mandibulae;M. B. T. N., mandibular branch trigeminal nerve;Sq., squamosal. KU 64214, ×5.
Fig. 9.Lateral view of the left jaw ofSmilisca baudini;A. M. E. S., adductor mandibulae externus superficialis;A. M. P. S., adductor mandibulae posterior subexternus;Col., columella;D. M.depressor mandibulae;M. B. T. N., mandibular branch trigeminal nerve;Sq., squamosal. KU 64214, ×5.
Fig. 10.Ventral view of throat musculature in an adult maleSmilisca baudini(Superficial musculature on left, deep musculature on right);A. C.anterior cornua of hyoid;Gen. L., geniohyoideus lateralis;Gen. M., geniohyoideus medialis;Hyo., hyoglossus;Omo., omosternum;Pet., petrohyoideus;S., submentalis;Sm., submaxillaris;St., sternohyoideus;V. S., vocal sac. KU 64220, × 2.5.
Fig. 10.Ventral view of throat musculature in an adult maleSmilisca baudini(Superficial musculature on left, deep musculature on right);A. C.anterior cornua of hyoid;Gen. L., geniohyoideus lateralis;Gen. M., geniohyoideus medialis;Hyo., hyoglossus;Omo., omosternum;Pet., petrohyoideus;S., submentalis;Sm., submaxillaris;St., sternohyoideus;V. S., vocal sac. KU 64220, × 2.5.
Throat Musculature.—The frogs that comprise the genusSmiliscaare characterized by paired subgular vocal sacs, essentially the same as those inTriprion(Duellman and Klaas, 1964). The following description is based onSmilisca baudini(Fig. 10).
M. submentalis lies in the anterior angle of the lower jaw, is thick, and consists of transverse fibers extending between the dentaries. M. submaxillaris is thin and arises from the whole of the inner surface of the lower jaw, except for the anterior angle occupied by M. submentalis. Anteriorly M. submaxillaris is broadly attached by fascia to M. hyoglossus and M. geniohyoideus, which lie dorsal to M. submaxillaris. Medially this attachment continues posteriorly for about one-half the length of the hyoglossus. Posteriorly M. submaxillaris is folded and attached to M. sternoradialis of the pectoral girdle. The vocal sacs are formed by a pair of posterolateral evaginations of M. submaxillaris; a broad connection between the pouches allows free passage of air between the pouches.
The deeper throat musculature is essentially the same as that described forPhrynohyas spilommaby Duellman (1956), except for slight differences in the place of attachment on the hyoid.
SKIN
Structure
The skin ofSmiliscais typical of that of most hylids in organization and structure.Smilisca silais distinguished from other members of the genus by the presence of small wartlike protrusions and peculiar white, pustular spots on the dorsum. The wartlike structures are composed of three or four epidermal cells, which protrude from the surface of the epidermis; the structures are covered by a slightly thickened layer of keratin. The white pustules are slightly elevated above the surrounding skin. Internally they consist of aggregationsof swollen, granular, pigment-cells (perhaps lipophores) lying between the epidermis and the melanophores.
Biochemical Variations
Dried skins of all species ofSmiliscawere sent to José M. Cei, Instituto Nacional de Cuyo, Mendoza, Argentina, for biochemical screening by means of the chromatographic techniques described by Erspamer and Cei (1963). The species in thebaudinigroup have detectable amounts of penta-hydroxi-trypatamine, whereas only a trace is present in the other species. Furthermore, species in thebaudinigroup differ fromS. silaand thesordidagroup in lacking, or having only a trace of, tryptophan-containing polypeptides. These superficial biochemical tests support the arrangement of species as ascertained by conventional taxonomic characters.
External Morphological Characters
The features of external morphology that were studied in connection with the taxonomy of the genusSmiliscaare discussed below.
Size and Proportions
The frogs of the genusSmiliscaare medium to large tree frogs. The three species comprising thebaudinigroup (S. baudini,cyanosticta, andphaeota) are notably larger thanS. puma,sila, andsordida(Table 6). The largest specimen that we examined is a female ofS. baudinihaving a snout-vent length of 90 mm.Smilisca pumais the smallest species; the largest male has a snout-vent length of 38 mm. and the largest female, 46 mm.
No outstanding differences in proportions exist between species, althoughcertain proportions are sufficiently different in some species to warrant mention.Smilisca baudiniis a more squat and stocky frog than other members of the genus; this is reflected in the somewhat shorter hind legs (Table 6). The size of the tympanum relative to that of the eye is highly variable within samples of a given species. Even so, noticeable differences in the tympanum/eye ratio are apparent. Members of thebaudinigroup have the largest tympani, whereasS. silaandsordidahave the smallest, andS. pumais intermediate (Table 6).
Shape of Snout
Although all members of the genus have rather truncate snouts, subtle differences exist among the species (Pl. 12).Smilisca silahas the shortest snout; that ofS. baudiniis only slightly longer. The snouts ofS. cyanostictaandpumaare nearly square in lateral profile, whereas those ofS. phaeotaandsordidaare slightly inclined. The shape of the snout is relatively uniform within each species and displays no noticeable sexual dimorphism, except inS. sordida, in which there are sexual differences and geographic variation (see p. 324).
Hands and Feet
The characters of the hands and feet are among the most taxonomically important external features inSmilisca. Consistent differences exist in relative lengths of the digits, size of subarticular tubercles, size and number of supernumerary tubercles, size and shape of the inner metatarsal tubercle, and amount of webbing (Pls. 4 and 5). In thebaudinigroup the series of species (baudini-phaeota-cyanosticta) show a progressive increase in amount of webbing in the hand and a decrease in number, and corresponding increase in size, of supernumerary tubercles. The amount of webbing in the feet ofS. baudiniandphaeotais about the same, but the webbing is slightly more extensive inS. cyanosticta.Smilisca pumais unique in the genus in lacking webbing in the hand; furthermore, this species is distinctive in having many large subarticular tubercles on the hand and a relatively small inner metatarsal tubercle. The two stream-inhabitants,S. silaandsordida, have shorter and stouter fingers than the other species. The webbing is most extensive in both the hands and feet of these species, which also are distinctive in having many small supernumerary tubercles on the feet.
Ontogenetic Changes
Minor ontogenetic changes in structure involve the shape of the snout, relative size of the eye, development of the tympanum, and amount of webbing in the hand. In recently metamorphosed young the snout is more rounded than in adults; the canthus and loreal concavity are not evident. Usually the tympanum is not differentiated in recently metamorphosed young, and the eye is proportionately large. The webbing in the feet is completely developed at metamorphosis, but young individuals have noticeably less webbing in the hand than do adults of the same species.
Coloration
Some of the most distinctive characters of the species ofSmiliscaare color and pattern of the living frogs. Although many chromatic features are lost or subdued in preserved specimens, the patterns usually persist.
Metachrosis
Change in color, well known in frogs, is common in hylids, especially in species having green dorsal surfaces (Phyllomedusais a notable exception). The non-greenSmilisca(puma,sila, andsordida) changes color, but this mostly is a change in intensity of color. In these species the markings usually are most distinct at night; frequently by day the frogs become pallid. The most striking examples of metachrosis inSmiliscaare found in thebaudinigroup, in which the dorsal ground-color changes from green to tan; correlated with the change in ground-color may be a corresponding change in the dorsal markings, but the dorsal markings may change to the opposite color.
Chromosomes
Chromosomes of all six species ofSmiliscawere studied by means of the propriono-orcein squash technique described by Duellman and Cole (1965). Karyotype analysis was attempted for several species by means of intraperitoneal injections of colchicine, which affected the mitotic cells as desired, but the testes examined contained too few mitotic cells to allow accurate determination of karyotypes.
Haploid (n) chromosome numbers were determined from cells in diakinesis, metaphase I, and metaphase II of meiosis. Diploid (2n) chromosome numbers were determined from cells in late prophase and metaphase of mitosis. Chromosome counts from as few as 23 meiotic cells ofS. phaeotaand as many as 80 cells ofS. sordidareveal a constant haploid (n) number of 12; counts of chromosomes in one to five mitotic cells in all species, exceptS. sila, reveal that the diploid (2n) number is 24.
NATURAL HISTORY
Breeding
Like most hylid frogsSmiliscais most readily collected and observed when individuals congregate for breeding.
Time of Breeding
Smiliscabreeds primarily in quiet water and reaches its height of breeding activity at times of plentiful rainfall,—usually from May through October. Through most of its rangeSmilisca baudinibreeds in those months, but in some places where abundant rain falls in other seasons, the species breeds at those times. For example, in southern El Petén and northern Alta Verapaz, Guatemala,Smilisca baudinihas been found breeding in February and March. The other pond-breeding species (S. cyanosticta,phaeota, andpuma) live in regions lacking a prolonged dry season, and possibly they breed throughout the year, but breeding activity seems to be greatest in the rainiest months.
The two stream-breeding species (S. silaandsordida) breed in the dry season when the streams are low and clear, principally in December through April. At high elevations the species sometimes breed in the rainy season; also, individuals sometimes breed in the short dry season (summer canicula) in July and August.
At several localities species have been found breeding at different times of the year:S. baudiniin March and July at Chinajá, Guatemala;S. phaeotain April and August at Palmar Sur, Costa Rica;S. pumain February and July at Puerto Viejo, Costa Rica; andS. silain February, April, and August at El Volcan, Panamá. These observations indicate only that the population breeds at more than one time in the year, but do not provide any evidence on the breeding cycles of the individual frogs. This is one important aspect of the natural history ofSmiliscafor which we lack data.
Breeding Sites
All members of the genusSmiliscapresumably deposit their eggs in water.
Smilisca baudiniusually breeds in temporary rain pools; often these are nothing more than shallow, muddy puddles. In other instances the sites are extensive ditches or large flooded areas (Pl. 8, Fig. 1). This species is an opportunistic breeder, and males gather at any of a wide variety of suitable breeding sites that are formed by torrential rains in the early part of the rainy season.Smilisca baudininearly always breeds in open pools having bare earthen edges. Frequently congregations ofS. baudiniare found at such small pools, but are absent from nearby large ponds surrounded by vegetation.
Little is known of the breeding habits ofS. cyanosticta, which inhabits humid forests on foothills and lowlands. Apparently its breeding sites are not unlike those ofS. phaeota, which usually are pools surrounded by vegetation (Pl. 8, Fig. 2), although sometimes males ofS. cyanostictacall from open muddy puddles. In uplands, where standing water is uncommon, this species breeds in quiet pools in streams.
Smilisca pumabreeds in grass-choked ponds and marshes, where the males call from bases of dense clumps of grass in the water (Pl. 9, Fig. 1).
Smilisca silaandS. sordidadiffernoticeablyfrom other species in the genus by breeding exclusively in streams, where males usually call from rocks or gravel bars in or at the edges of streams (Pl. 9, Fig. 2); sometimes individuals perch on bushes overhanging streams. In the streams, or parts of streams, utilized by these frogs the water is clear, shallow, and has a slow gradient; occasional males have been found calling along cascading mountain streams.
Breeding choruses composed of ten or more species of frogs are not uncommon in Middle America, butSmiliscausually breeds alone or with one or two other species and at the most five others. This tendency towards solitary breeding possibly is the result of selection of breeding sites that are unsuitable to many other species of frogs. Nevertheless, many other species of frogs have been found at the breeding sites with the various species ofSmilisca; these breeding associates (Table 7) are most numerous forS. baudini, which has a broad geographic range, including a variety of habitats.
Breeding Behavior
Calling sites.—All species ofSmiliscausually call from the ground, including rocks and gravel bars; some individuals sit in shallow water near the edge of the pool or stream. Sometimes males ofS. baudini,sila, andsordidacall from low bushes or trees near the breeding site. OneS. baudiniwas observed calling while it was floating on the surface of a pond.Smilisca cyanosticta,phaeota, andpumacall from secluded places at the edge of the water or in the water, whereasS. baudini,silaandsordidacall from open situations.
Chorus structure.—Limited observations on some of the species ofSmiliscashow a definite organization of the calling behavior of individuals.Smilisca baudiniandS. phaeotacall in duets. This is especially noticeable inS. baudini, in which the members of a duet often call from sites separated by only a few centimeters. The call ofS. baudiniconsists of a series of like notes (see description of call in following section); the duration of each note is about equal to the interval between notes. Normally one individual utters one note, pauses, and utters a single note again, or series of two or three notes. If there is no response, the first individual often waits several seconds or even several minutes and then repeats the call. The second individual usually responds after the first or second note of the sequence. The notes of the second individual usually are spaced so that they are emitted in the intervals between the notes of the first individual. This can be shown diagrammatically by havingthe figure "1" represent notes of the first individual and figure "2," the notes of the second; an empty interval is represented by "0":