1-0-1-2-1-2-1-2-1-2-1-2Usually a chorus is initiated by one duet and is quickly picked up by other individuals also calling in duets. A numerical representation of a chorus of eight frogs would approximate the following organization:1-0-1-2-1-2-1-2-1-2-1-2-1-23-0-3-4-3-4-3-4-3-4-3-4-35-6-5-6-5-6-5-6-5-6-5-67-8-7-8-7-8-7-8-7-8-7-8After the first one or two duets are initiated, the second individuals in the following duets usually call immediately after their respective partners have given the first notes. The other noteworthy aspect about the organization is that the entire chorus usually stops abruptly. Normally the first duet stops calling shortly before the others, but this is not invariable. Often one duet or one individual will emit several notes after the rest of the frogs have become silent. An interval of several minutes sometimes elapses before the chorus begins again. Successive choruses apparently are initiated by the same duet. Responses can be initiated artificially by imitating the call, and sometimes any loud noise will start a chorus.Similar duets have been observed inS. phaeota. In this species the intervals are often much longer than the notes, and if two males are calling in close proximity, their calls can be mistaken for those of one individual.Smilisca phaeotadoes not congregate in large numbers; usually only two males call from one restricted site.Smilisca silahas a call consisting of a primary note followed by one or more secondary notes. Males often call in duets, but not necessarily so. In a duet, the first male usually utters only primary notes until the second individual responds; then each individual produces a rapid series of secondary notes.Smilisca pumaalso produces primary and secondary notes. Although individuals sometimes call alone, duets, trios, or quartets were more common. The chorus is initiated by one individual uttering primary notes until joined by the second, third, and fourth frogs. In one quartet in a marsh 7.5 kilometers west of Puerto Viejo, Costa Rica, on February 19, 1965, the same individual initiated four consecutive choruses. Each time the second member of the chorus was the same; the third and fourth frogs joined the chorus nearly simultaneously.Individuals ofS. sordidaare usually irregularly situated along a stream. No duets or other combinations of individuals are apparent in the chorus structure, but once an individual calls, a frog nearby calls almost immediately; then a frog near the second individual calls, and so on. The resulting series of calls gives the impression that the sound is moving along the stream as successive individuals join the chorus and the first callers become quiet. It is not known if the same individual initiates successive choruses or if the order of calling is the same in subsequent choruses.These limited observations on chorus structure inSmiliscashow the presence of behavioral organization. The methods of establishing the organization and the significance of the call-order in breeding have yet to be discovered.Calling males ofS. baudiniare often close together; some individuals have been observed almost touching one another, but no indication of territorialityor aggressive behavior has been witnessed. The more distant spacing of the stream-breeding speciesS. silaandS. sordidamay be a function of calling-territories, but no direct evidence is available to substantiate this supposition.Sex recognition and amplexus.—Observations onSmilisca baudiniindicate that the calls of males attract females. At Tehuantepec, Oaxaca, México, a female was first observed about two meters away from a male calling at the edge of a rain pool; in a series of short hops she progressed directly towards the male, although vegetation obscured him until she was less than a meter away. When she approached to within about 20 centimeters of the male, he took notice of her, moved to her, and clasped her. At Chinajá, Alta Verapaz, Guatemala, a female swam directly across a pool about three meters wide to a calling male. Her line of movement took her within a few centimeters of a silent male, to whom she paid no attention. She stopped just in front of the calling male, which immediately clasped her. At a large muddy pond 4 kilometers west-northwest of Esparta, Puntarenas, Costa Rica, a female was observed swimming toward a small submerged tree; a male was calling from a branch about one meter above the water. The female climbed to a branch about 20 centimeters below the male, which upon seeing her there immediately jumped down and clasped her. These few observations ofS. baudinishow that in this species females are capable of locating calling males by means of phono-orientation; visual reception on the part of females seems to be secondary. Contrariwise, males apparently become aware of the proximity of females by seeing them; once a male sees a female he usually tries to clasp her. Possibly the males receive stimuli by means of chemo-reception, but in each observed instance the male obviously looked at the female.Amplexus is axillary in all members of the genus. Normally amplexing males hunch their backs and press their chins to the females' backs. Clasping pairs are usually found at the edge of the water, but sometimes amplexus takes place in trees or bushes.Egg deposition.—Oviposition has been observed only inSmilisca baudini. On the night of June 28, 1961, at Chinajá, Alta Verapaz, Guatemala, a clasping pair was observed at the edge of a shallow rain pool. After sitting for several minutes in shallow water, the female (with male on her back) swam part way across the pool and grasped an emergent stick with one hand. The female's body was nearly level with the surface of the water, and her hind legs were outstretched as deposition commenced; eggs were extruded rapidly. After a few seconds the female moved slowly to another twig a few centimeters away and deposited more eggs. This process was repeated until the female was spent. The spawn resulted in a surface film covering roughly one square meter. It is doubtful if this type of egg deposition occurs in any other species in the genus, especially those that lay their eggs in streams.Breeding CallThe breeding calls of the six species ofSmiliscaare alike in their explosive nature. Calls are emitted quickly with a short burst of air filling the vocal sac, which immediately deflates. Phonetically the calls can be described as a single "wonk" or series of such notes inS. baudiniandS. cyanosticta, a low growl inS. phaeota, a relatively high pitched rattle inS. sordida, and a lowsquawk usually followed by one or more rattling secondary notes inS. pumaandS. sila. Quantitatively, the calls of the six species differ in number of notes, duration of notes, and in pitch (Table 8, Pls. 10 and 11). Although no measurements were taken on the intensity of the calls, we observed in the field that each of the species has a loud voice. The call ofS. baudiniseems to carry farther than any of the others.Table 8.—Comparison of Breeding Calls in Smilisca. (Observed Range Given in Parentheses Below Mean. In Species Having Primary and Secondary Notes, Only the Primary Notes Are Analyzed Here.)SpeciesNNotes percall groupDuration ofnote (seconds)Pulses persecondFundamentalfrequency (cps)Major frequencies (cps)LowerUpperS. baudini208.00.11174.7166.23512507(2-15)(0.09-0.13)(140-195)(135-190)(175-495)(2400-2725)S. cyanosticta101.20.38147.0145.18411894(1-2)(0.25-0.45)(110-180)(135-160)(480-975)(1600-2100)S. phaeota101.60.31116.0143.0372—(1-2)(0.10-0.45)(100-130)(110-165)(330-495)S. puma283.70.13208.2145.67431868(2-10)(0.06-0.35)(187-240)(125-200)(495-980)(1456-2240)S. sila152.40.16108.5103.08992218(1-6)(0.06-0.28)(97-120)(90-115)(665-1180)(1980-2700)S. sordida191.70.29104.7123.112162694(1-6)(0.18-0.45)(78-135)(90-140)(1150-1540)(2340-2990)Call rate.—The rate at which call-groups are produced varies from one every few seconds to one in several minutes. InS. baudini,cyanosticta,phaeota, andsordida, call-groups are produced as frequently as every 12 seconds, but usually more time elapses between call groups. InS. sordida, five or more minutes sometimes elapse between call-groups. The interval is somewhat less inS. phaeota. Calls are repeated at much shorter intervals inS. puma(5-55 seconds) andS. sila(4-20 seconds).Notes per call-group.—Except forS. pumaandS. sila, the series of notes produced in any given call of a species ofSmiliscais essentially the same; there is no differentiation into primary and secondary notes.Smilisca cyanostictaandS. phaeotaemit only one or two relatively long notes per call-group, whereasS. baudiniandS. sordidaproduce as many as 15 and 6 notes, respectively. Males ofS. pumaandS. silaoften produce only the primary note; sometimes this is done several times before the secondary notes are produced. For example, oneS. puma(KU 91711; tape No. 379) produced the following number of notes in consecutive call-groups: 1, 1, 1, 1, 2, 2, 3, 1, 4; secondary notes are present in only four of the nine call-groups. A typical series of consecutive call-groups inS. sila(KU 91852; Tape No. 385) has 1, 1, 1, 2, 4, 2 notes per call-group; secondary notes are present in only half of the call-groups.Smilisca pumaapparently always produces at least two primary notes before emitting secondary notes; sometimes only primary notes are produced in one series of calls. The number of secondary notes following a given primary varies from one to nine; the modal number is one, and the mean is three in 27 call-groups.Smilisca silafrequently begins a series of calls with two or more primary notes, but sometimes the first primary note is followed immediately by two or more secondary notes. The number of secondary notes following a given primary varies from one to five; the modal number is one, and the average is two in 13 call-groups.Duration.—The average duration of call-groups consisting of two or more notes is 1.18 seconds inS. baudini; 1.02 incyanosticta, 0.91 inphaeota, 1.32 inpuma, 1.48 insila, and 1.29 insordida. Although there is considerable variation in the lengths of the notes (only primary notes inS. pumaandsilaare considered here),S. cyanosticta,phaeota, andsordidahave noticeably longer notes than do the other species (Table 8). The secondary notes are longer than the primary notes inS. puma(average 0.27 secs. as compared with 0.13 secs.) and inS. sila(average 0.25 secs., as compared with 0.16 secs.).Note repetition rate.—The rate at which notes in call-groups containing two or more notes are produced varies inS. baudinifrom 2.5 to 7.1 (average, 3.7) calls per second;cyanosticta, 1.8-2.1 (1.9);phaeota, 2.0-2.4 (2.2);puma, 1.9-2.9 (2.2);sila, 1.3-2.4 (1.8); andsordida, 1.5-2.6 (2.1).Smilisca baudini, which has notes of short duration (0.09 to 0.13 seconds), has the fastest note-repetition rate. Although the individual notes ofS. cyanostictaandS. phaeotaare relatively long (average, 0.38 and 0.31 seconds, respectively), the intervalsbetween the notes is short; consequently, their note-repetition rates do not differ greatly from those ofS. pumaandS. sila, which have shorter notes (average, 0.13 and 0.16 seconds, respectively) but longer intervals between notes.Pulse rate.—Pulses vary in frequency from 78 to 240 per second in the calls analyzed (only primary notes inS. pumaandS. sila), but the variation in any given species is much less than that in the entire genus (Table 8).Smilisca pumais outstanding in having a high pulse rate, which is approached only by that ofS. baudini. Even in the species having the lowest pulse rates, the pulsations are not audible. The secondary notes produced byS. pumaandS. silahave a slower pulse rate than the primary notes; often the pulses are audible. InS. pumathe pulse rate of secondary notes is sometimes as low as 48 pulses per second, and inS. silastill lower (as low as 40 pulses per second). The upper limits of pulse rate in the secondary notes in these species merge imperceptibly with the rates of the primary note; consequently, on the basis of pulse rate alone it is not always possible to distinguish primary from secondary notes.Frequency.—Smiliscaproduces noisy (as opposed to more musical) calls, and the energy is distributed throughout the frequency spectrum; the calls are poorly modulated, except inS. sordida, in which two usually discrete bands of frequency are present (Pl. 11C). For the most part the calls ofSmiliscaconsist of little modified energy of the fundamental frequency and of its harmonics, some of which are emphasized.The upper frequency range varies within each species and even within the calls of one individual.Smilisca phaeotahas the lowest upper frequencies; no calls ranged above 4400 cycles per second (cps.), and half of the calls never exceeded 3000 cps.Smilisca cyanostictaproduces calls in which the upper frequency is below 7000 cps. and usually below 6000 cps. Likewise,S. pumaproduces calls that are below 7000 cps., whereasS. silahas frequencies of up to 8400 cps. In bothS. baudiniandS. sordida, the highest frequencies attained are about 9100 cps. Variation in the highest frequencies in a series of consecutive calls by one individual frog was noted in all species. Such variation is especially prevalent inS. puma; for example one individual (KU 87771; Tape No. 376) recorded at a temperature of 24° C. at 7.5 kilometers west of Puerto Viejo, Heredia Province, Costa Rica, on July 31, 1964, produced three consecutive primary notes having upper frequencies of about 6000, 4000, and 4000 cps., respectively. Apparently in a given species the production of the higher frequencies in some notes and not in others is correlated with the amount of distention of the vocal sac and is not dependent upon the structure or tension of the vocal cords.Although the dominant frequency inS. sordidais lower than that inS. baudiniandS. cyanosticta, the call of the former is audibly higher-pitched. This is due primarily to the emphasis on certain harmonics at a high frequency (sometimes as high as 9000 cps.) inS. sordida, whereas inS. baudiniand other species, if harmonics are present at those frequencies, they are not emphasized.The fundamental frequencies are as low as 90 cps. inS. silaandS. sordidaand as high as 200 cps. inS. puma(Table 8). The fundamental frequency seemingly is relatively unimportant in determining the general pitch of the call, a characteristic most dependent on the dominant frequency and emphasized harmonics in the higher-frequency spectrum. In none of the species is thefundamental the dominant frequency. In the low-pitched call ofS. phaeotathe dominant frequency is the third harmonic (the second harmonic above the fundamental frequency, which is the first harmonic). In all other species a much higher harmonic is dominant; for examples, inS. cyanostictaharmonics from 10 to 15 are dominant; inS. baudini, 15-19; andS. sila, 20-30.A glance at the audiospectrographs and their accompanying sections (Pls. 10 and 11) reveals the presence of two emphasized bands of frequency in all species exceptS. phaeota, in which only the lower band is present. These two bands of emphasized harmonics are part of a continuous, or nearly continuous, spread of energy throughout the frequency spectrum, except inS. sordidain which the bands are usually distinct. As shown in the sections, certain harmonics in each of the bands are emphasized with nearly equal intensity. Therefore, with the exception ofS. phaeota, the calls ofSmiliscaare characterized by two major frequencies, one of which is the dominant frequency and the other is a subdominant frequency (Table 8). The upper major frequency is dominant in all calls inS. baudiniandS. cyanosticta, but either major frequency may be dominant in other species. The upper major frequency is dominant in 65 per cent of calls byS. puma, 87 per cent inS. sila, and 68 per cent inS. sordida. Individuals of these three species sometimes produce a series of calls in which the dominant frequency changes from one of the major frequencies to the other. Four consecutive notes emitted by an individual ofS. sordidarecorded 13 kilometers east-northeast of Golfito, Puntarenas Province, Costa Rica, had dominant frequencies of 910, 1950, and 750 cps., respectively. In each case, an alternation of major frequencies took place in respect to dominance. An individual ofS. pumafrom 7.5 kilometers west of Puerto Viejo, Costa Rica, produced a primary note followed by one secondary note; each note had major frequencies at 600 and 1800 cps.; the dominant frequency of the primary note was at 1800 cps., whereas in the secondary note the dominant frequency was at 600 cps. The difference in emphasis on the major frequencies is so slight that shift in dominance is not audible.Effect of temperature on calls.—The present data are insufficient to test statistically the correlation between temperature and variation within certain components of the calls inSmilisca, but even a crude graph shows some general correlations. The widest range of temperatures is associated with the recordings ofS. baudini. Three individuals recorded at a temperature of 30° C. at Tehuantepec, Oaxaca, had pulse rates of 180 pulses per second and fundamental frequencies of 160-180 cps., as compared with an individual recorded at a temperature of 17° C., which had a pulse rate of 140 and a fundamental frequency of 135 cps. All individuals ofS. baudinirecorded at higher temperatures had faster pulse rates and higher fundamental frequencies. Pulse rates differ in the other species in the genus but less strikingly (probably owing to narrower ranges of temperatures at which recordings were made). In five recordings ofS. sordidamade at 20° C. the pulse rate is 80-90, as compared with four recordings made at 25° C. having pulse rates of 120-135. Thirteen recordings ofS. silamade at 17° C. have pulse rates of 97-112 (average 105); one individual recorded at 26° C. has 120 pulses per second. Seemingly no correlation exists between temperature and other characteristics of the calls, such as duration and rate of note-repetition.The breeding call as an isolating mechanism.—Blair (1958), Bogert (1960), Duellman (1963a),Fouquette(1960), Johnson (1959), and others have providedevidence that the breeding calls of male hylids (and other anurans) serve as isolating mechanisms in sympatric species. In summarizing this discussion of the breeding calls ofSmiliscawe want to point out what seem to be important differences in the calls that may prevent interspecific hybridization in sympatric species ofSmilisca.The genus is readily divided into two species-groups on morphological characters; this division is supported by the breeding calls. In the species of thebaudinigroup the calls are unmodulated and lack secondary notes. In thesordidagroup the calls either have secondary notes or are modulated.Smilisca baudinioccurs sympatrically withS. cyanostictaandS. phaeota; where they occur together, both species sometimes breed in like places at the same time. We are not aware of these species breeding synchronously at exactly the same site, althoughS. baudiniandS. cyanostictawere calling on the same nights and less than 100 meters apart in Oaxaca in June, 1964. Regardless of their respective breeding habits, sympatric species have calls that differ notably. Except for the higher fundamental and dominant frequencies, the calls ofS. cyanostictaandS. phaeotaclosely resemble one another, but the calls of both species differ markedly from that ofS. baudini. The geographic ranges ofS. cyanostictaandS. phaeotaare widely separated.The calls of the allopatric speciesS. pumaandS. silaare not greatly different.Smilisca sordidahas a distinctive call and occurs sympatrically withS. pumaandS. sila. In the streams in southern Costa RicaS. sordidaandS. silabreed synchronously, but the high-pitched modulated call of the former is notably different from the lower, unmodulated call ofS. sila.The data indicate that the calls of related sympatric species differ more than the calls of related allopatric species. We postulate that these differences evolved to support the reproductive isolation of the sympatric species. The data are insufficient to determine geographic variation in the calls and to determine if differences in the calls are enhanced in areas of sympatry as compared with the allopatric parts of the ranges.Other calls.—As stated previously, there is no direct evidence of territoriality inSmilisca; we have heard no calls that can be definitely identified as territorial. Single notes ofS. baudini,phaeota, andsilahave been heard by day, just prior to rains, or during, or immediately after rains. Such calls can be interpreted as "rain calls," which are well known inHyla eximiaandHyla squirella. Distress calls are known in several species ofRanaand inLeptodactylus pentadactylus; such calls result from the rapid expulsion of air over the vocal cords and with the mouth open. Distress calls have been heard fromS. baudini. At Charapendo, Michoacán, México, a male that had one hind limb engulfed by aLeptodeira maculataemitted several long, high-pitched cries. A clasping pair ofS. baudiniwas found in a bush at the edge of a marshy stream 2 kilometers northeast of Las Cañas, Guanacaste Province, Costa Rica. When the pair was grasped, the female emitted a distress call.EggsEggs ofS. baudini,cyanosticta, andphaeotahave been found in the field, and eggs ofS. silahave been observed in the laboratory. The eggs ofS. pumaandsordidaare unknown. Insofar as known,Smilisca baudiniis unique in the genus in depositing the eggs in a surface film. Each egg is encased in avitelline membrane, but individual outer envelopes are lacking. The eggs are small; the diameter of recently-deposited eggs is about 1.3 mm. and that of the vitelline membrane is about 1.5 mm. The eggs ofS. cyanostictaandphaeotaare deposited in clumps, and the eggs are larger than those ofS. baudini. Diameters of eggs ofS. cyanostictaare about 2.3 mm., and those of the outer envelopes are about 4.0 mm. Artificially fertilized eggs ofS. silaraised in the laboratory have diameters of about 2.4 mm.; the diameter of the outer envelopes is about 4.9 mm.In order to determine the reproductive potential of the six species, ovulated eggs were removed from females and counted. The numbers of eggs recorded are: 3S. baudini—2620, 2940, 3320; 1S. cyanosticta—910; 3S. phaeota—1665, 1870, 2010; 1S. puma—518; 3S. sila—369, 390, 473; 3S. sordida—524, 702, 856. These limited data indicate that the large species (S. baudini,cyanosticta, andphaeota) have more eggs than do the smaller species. The stream-breeding species (S. silaandsordida) have relatively few eggs by comparison with the pond-breeders. Possibly this is a function of size of eggs rather than a correlation with the site of egg-deposition.TadpolesThe acquisition of tadpoles of all of the species ofSmiliscahas made possible the use of larval characters in erecting a classification and in estimating the phylogenetic relations of the several species. Furthermore, developmental series of tadpoles of four species allow a comparison of the growth and development in these species. Throughout the discussion of tadpoles we have referred to the various developmental stages by the Stage Numbers proposed by Gosner (1960).General StructureTadpoles of the genusSmiliscaare of a generalized hylid type, having 2/3 tooth-rows, unspecialized beaks, mouth partly or completely bordered by papillae, lateral fold present in the lips, spiracle sinistral, anal tube dextral, and caudal musculature extending nearly to tip of caudal fin. Although minor differences exist in coloration, proportions, and mouthparts, no great modifications of the basic structure are present.Comparison of SpeciesThe larval characters of the species ofSmiliscaare compared below and illustrated in Figures 11-15.Shape and Proportions.—The bodies ofS. baudini,cyanosticta,phaeota, andpumaare rounded and about as wide as deep; the eyes are moderately large and directed dorsolaterally, and the nostrils are about midway between the bluntly rounded snout and the eyes. The mouths are medium-sized and directed anteroventrally. The bodies of tadpoles ofS. silaandsordidaare slightly compressed dorso-ventrally. The snout is moderately long and sloping; the eyes are larger and directed more dorsally than in the other species, and the nostrils are closer to the eyes than the snout. The mouths are moderately large and directed ventrally.The tail is about half again as long as the body inS. baudini,cyanosticta,phaeota, andpuma; in these species the caudal musculature is moderately heavy, and the caudal fins are deep. The caudal musculature is upturned distally inS. baudiniandphaeota, and the dorsal fin extends anteriorly onto the body in these two species and inS. puma. The tail is about twice as long as the body inS. silaandsordida. In both species the caudal fins are shallow in comparison with the depth of the caudal musculature, especially inS. sordida(Fig. 14); in neither species does the dorsal fin extend anteriorly onto the body.Fig. 11.Tadpoles ofSmilisca baudini: (A) Stage 21 (KU 62155) × 10; (B) Stage 25 (KU 68467) × 5; (C) Stage 30 (KU 60018) × 4; (D) Stage 41 (KU 60018) × 3.Mouthparts.—The mouth ofS. sordidais completely bordered by two rows of papillae, whereas in the other species the median part of the upper lip is devoid of papillae.Smilisca baudiniandpumahave two rows of papillae;S. silahas one complete row (except medially on the upper lip) and one incomplete row, andS. cyanostictaandphaeotahave only one row (Fig. 15). All species have numerous papillae in the lateral fold; the fewest lateral papillaeare found inS. cyanostictaandphaeota. Although all species have two rows of teeth in the upper jaw and three rows in the lower jaw, specific differences in the nature of the rows exist between certain species. The second upper tooth-row is narrowly interrupted medially inS. silaandsordidaand broadly interrupted in the other species. The first upper row is strongly arched inS. puma, moderately arched inS. baudiniandsila, and weakly arched in the other species. In all species the third lower tooth-row is the shortest, only slightly so inS. silaandsordida, but only about half the length of the second lower row inS. puma.Fig. 12.Tadpoles ofSmilisca cyanosticta: (A) Stage 21 (KU 87648) (B) Stage 25 (KU 87651) × 5; (C) Stage 30 (KU 87652) × 4; (D) Stage 40 (KU 87650) × 3.The beaks are well developed and finely serrate in all species. The lower, broadly V-shaped, beak is slender inS. puma, rather robust inS. baudiniandsila, and moderately heavy in the other species. The lateral processes of the upper beak are shortest inS. pumaand longest inS. baudiniandsordida. In the latter the inner margin of the upper beak and lateral process have the form of a shallow S, whereas in the other species the inner margin of the upper beak forms a continuous arch with the lateral processes (Fig. 15).Fig. 13.Tadpoles ofSmilisca phaeota: (A) Stage 21 (KU 68479) × 14; (B) Stage 25 (KU 68480) × 5; (C) Stage 30 (KU 68482) × 4; (D) Stage 40 (KU 68483) × 3.Coloration.—The tadpoles ofSmiliscalack the bright colors or bold markings characteristic of some hylid tadpoles; even so, the subdued colors and arrangement of pigments provide some distinctive markings by which the species can be distinguished from one another. The species comprising thebaudinigroup (S. baudini,cyanosticta, andphaeota) are alike in having the body brown or grayish brown dorsally and transparent with scattered brown pigment ventrally. A cream-colored, crescent-shaped mark is present on the posterior edge of the body; this mark is usually most noticeable inS. baudiniand least so inS. cyanosticta. Other differences in coloration in members of thebaudinigroup are relative and subtle.Smilisca phaeotausually is morepallid thanbaudini, andcyanostictausually is darker thanbaudini; both species have larger dark markings on the tail than doesS. phaeota.Smilisca baudinihas a dark streak on the middle of the anterior one-fourth of the tail (Figs. 11-13).Smilisca pumais distinctive in having a grayish brown body and dark gray reticulations on the tail.Smilisca silaandsordidaare distinctive in having pairs (sometimes interconnected) of dark marks on the dorsal surfaces of the caudal musculature, and in dorsal view the tail appears to be marked with dark and pale creamy tan transverse bars. These dark marks, as well as the small flecks on the tail, are brown inS. silaand red insordida.Smilisca silahas dark brown flecks on the dorsal surface of the body and small white flecks laterally; these markings are absent inS. sordida(Fig. 14).Descriptions of the coloration of living tadpoles are given in the accounts of the species.Fig. 14.Tadpoles ofSmilisca; (A)S. puma, Stage 30 (KU 91807); (B)S. sila, Stage 25 (KU 80260);S. sordida, Stage 30 (KU 68475). All × 3.5.Growth and DevelopmentInformation on the growth and development of Middle American hylids is scanty. Adequate descriptions have been published forPhyllomedusa annae(Duellman, 1963b),Phrynohyas venulosa(Zweifel, 1964), andTriprion petasatus(Duellman and Klaas, 1964). Material is available for adequate descriptions of the developmental stages of four species ofSmilisca(Tables 9-12, Figs. 11-13). Because none of the tadpoles was raised from hatching to metamorphosis, the rate of growth and duration of the larval stages are unknown.Fig. 15.Mouthparts of tadpoles ofSmilisca; (A)S. baudini(KU 60018); (B)S. puma(KU 91807); (C)S. cyanosticta(KU 87625); (D)S. sila(KU 80620); (E)S. phaeota(KU 68482); (F)S. sordida(KU 68475). All ×17.Table 9.—Growth and Development of Tadpoles of Smilisca baudini. (Means Are Given in Parentheses After the Observed Ranges.)StageNTotal lengthBody lengthTail length21105.1-5.4 (5.22)2.6-2.7 (2.54)2.5-2.7 (2.58)24106.0-6.5 (6.20)2.3-2.6 (2.45)3.5-3.9 (3.69)25107.2-8.3 (7.78)3.0-3.3 (3.14)4.2-5.0 (4.64)271018.5-21.5 (20.22)8.0-9.0 (8.38)10.4-13.0 (11.84)291021.5-24.5 (22.60)8.5-10.0 (9.25)12.5-14.5 (13.35)37328.5-31.0 (30.00)11.0-12.5 (11.67)17.5-19.0 (18.00)381035.0-37.5 (35.50)12.0-13.5 (12.80)21.5-24.0 (22.70)40234.0-37.0 (35.50)12.5-13.5 (13.00)21.5-23.5 (22.50)411034.0-37.0 (35.50)12.5-13.5 (13.00)21.5-23.5 (22.50)42324.0-30.0 (27.00)12.5-13.0 (12.67)11.5-17.0 (14.33)45614.0-24.0 (17.58)12.5-14.0 (13.37)1.5-10.0 (4.17)4623——12.0-15.5 (13.34)——Table 10.—Growth and Development of Tadpoles of Smilisca cyanosticta. (Means Are Given in Parentheses After the Observed Ranges.)StageNTotal lengthBody lengthTail length21105.8-6.5 (6.28)2.8-3.1 (3.00)3.0-3.5 (3.28)25107.9-9.2 (8.44)2.7-3.2 (2.96)4.8-6.0 (5.48)30722.5-25.0 (23.50)8.5-9.5 (9.00)14.0-15.5 (14.57)361027.0-30.0 (28.75)9.5-11.5 (10.80)17.0-18.5 (17.95)42226.0-27.0 (26.50)10.0016.0-17.0 (16.50)462—14.00—Hatchlings of three species (S. baudini,cyanosticta, andphaeota) are available. These larvae have non-functional eyes and large oral suckers. By the time the larvae have developed to stage 21, external gills are present, the caudal musculature and caudal fin have been differentiated, and the head is distinguishable from the body. In stage 21 oral suckers and a large amount of yolk are still present.The developmental data on the four species show no significant variations; consequently, we will describe the development of only one species,Smilisca phaeota(Table 11, Figs. 13 and 16).Stage 21.—Bulging cream-colored yolk mass, transparent cornea, and moderately long, unbranched filamentous gills, and oral suckers present; mouth having irregular papillae on lower lip; teeth and beaks absent; caudal myomeres distinct; pigmentation uniform over body and caudal musculature; caudal fin transparent with scattered small flecks.Fig. 16.Relative rate of growth in tadpoles ofSmilisca phaeotaas correlated with developmental stages. Formulas for the limb bud refer to its length (L) in relation to basal diameter (D).Stage 25.—Operculum complete; gills absent; sinistral spiracle apparently functional; cloacal tail-piece, nasal capsules, and external nares present; gutpartly formed; mouth bordered by single row of papillae, except medially; small papillae present in lateral fold of lips; two upper and three lower tooth-rows present, but not fully developed; beaks apparently fully developed; depth of dorsal and ventral fins less than depth of caudal musculature: tip of tail upturned; pigment on body most dense on dorsum and sides; faint, nearly pigmentless crescent-shaped mark on posterior edge of body; concentrations of pigment forming small spots on tail.Stage 28.—Mouthparts complete; limb bud about half as long as thick; other structural features and coloration closely resemble those in stage 25.Stage 30.—Limb bud approximately twice as long as thick; body as deep as wide; dorsal fin deepest just posterior to body; ventral fin deeper than caudal musculature; tail sharply upturned distally; anal tube dextral; brown pigment sparse on flanks.Table 11.—Growth and Development of Tadpoles of Smilisca phaeota. (Means Are Given in Parentheses After the Observed Ranges.)StageNTotal lengthBody lengthTail length1510—1.9-2.1 (1.97)—168—2.0-2.2 (2.07)—184—2.2-2.6 (2.31)—2137.9-8.6 (8.21)4.1-4.5 (4.31)3.8-4.1 (3.92)25108.7-10.6 (9.69)4.5-4.8 (4.64)4.3-6.0 (5.05)261112.3-16.1 (14.01)4.2-6.3 (5.60)6.7-9.8 (8.41)271013.0-15.7 (14.28)4.9-6.2 (5.40)7.7-10.5 (8.88)281313.9-20.9 (15.62)5.2-8.3 (5.75)8.5-12.6 (9.85)29817.8-22.3 (19.79)6.3-8.4 (7.19)11.5-14.0 (12.60)30920.3-24.8 (22.85)8.1-10.5 (9.32)10.5-15.5 (13.53)31524.1-28.5 (26.61)9.4-11.2 (10.59)14.7-17.3 (16.02)34524.8-29.4 (27.31)9.2-11.6 (10.73)15.6-18.5 (16.80)36330.0-30.1 (30.07)10.1-12.2 (11.15)18.9-20.0 (19.44)37428.9-34.1 (31.75)11.5-12.4 (11.88)17.4-22.5 (19.88)38128.9812.8816.1039235.6-36.9 (36.25)14.0021.6-22.9 (22.25)40232.3-39.8 (36.05)14.0018.3-21.8 (20.05)43221.5-23.0 (22.25)14.2-14.8 (14.45)6.8-8.8 (7.80)444—14.5-15.6 (15.08)—4611—12.7-16.7 (14.26)—Table 12.—Growth and Development of Tadpoles of Smilisca sordida. (Means Are Given in Parentheses After the Observed Ranges.)StageNTotal lengthBody lengthTail length25625.5-28.0 (26.1)9.0-9.5 (9.3)16.2-18.5 (16.7)33228.5-30.0 (29.3)10.2-10.5 (10.4)18.0-19.8 (18.9)36829.5-34.5 (32.3)10.2-11.7 (10.8)19.3-23.0 (21.5)37731.6-37.5 (34.6)11.0-12.5 (11.5)21.6-25.0 (23.2)41333.0-37.2 (35.2)11.6-12.2 (11.9)21.4-25.2 (23.2)431——12.4——469——13.1-15.7 (14.9)——Stages 34,36,37, and38.—Stage 34, foot paddle-shaped with four toe buds; stage 36, five toe buds; stages 37 and 38, lengthening of toes. In all four stages, spiracle persistent, and pigmentation resembling that of early stages.Stage 39.—Metatarsal tubercle present; greatest total length (36.9 mm.) attained.Stage 40.—Subarticular tubercles prominent; skin over forelimbs transparent; cloacal tail-piece and spiracle absent; outer tooth-rows degenerating; caudal fins shallower than in preceding stages; distal part of tail nearly straight; size of dark markings on tail decreased; pigment present on hind limb.Stage 43.—Forelimbs erupted; larval mouthparts absent; corner of mouth between nostril and eye; transverse bands present on hind limbs; tail greatly reduced (about 8 mm. in length).Stage 44.—Sacral hump barely noticeable; tail reduced to a stub; corner of mouth at level of pupil of eye; dorsal surfaces pale olive-green; venter white.Changes proceed in a definite pattern during the growth and development of tadpoles. Larval teeth are absent in hatchlings; the inner tooth-rows develop first, and the third lower row last. At metamorphosis the third lower row is the first to be lost. The tail increases gradually in length relative to the body. In stage 25 the tail is 52.1 per cent of the total length, and in stage 36, 64.6 per cent. In later stages the tail becomes relatively shorter through resorption. Duellman and Klaas (1964:320) noted a great size-variation inTripriontadpoles in stage 25. No such variation is apparent in any stage of any of the species ofSmiliscastudied.The growth and development of the other species ofSmiliscado not differ significantly from that ofS. phaeota. The tadpoles ofS. silaandsordidafrom streams have relatively longer tails at hatching. For example, in tadpoles ofS. sordidathe average length of tail is 64.0 per cent of the body-length in stage 25, and in stage 37, 67.0 per cent.
1-0-1-2-1-2-1-2-1-2-1-2
Usually a chorus is initiated by one duet and is quickly picked up by other individuals also calling in duets. A numerical representation of a chorus of eight frogs would approximate the following organization:
1-0-1-2-1-2-1-2-1-2-1-2-1-23-0-3-4-3-4-3-4-3-4-3-4-35-6-5-6-5-6-5-6-5-6-5-67-8-7-8-7-8-7-8-7-8-7-8
After the first one or two duets are initiated, the second individuals in the following duets usually call immediately after their respective partners have given the first notes. The other noteworthy aspect about the organization is that the entire chorus usually stops abruptly. Normally the first duet stops calling shortly before the others, but this is not invariable. Often one duet or one individual will emit several notes after the rest of the frogs have become silent. An interval of several minutes sometimes elapses before the chorus begins again. Successive choruses apparently are initiated by the same duet. Responses can be initiated artificially by imitating the call, and sometimes any loud noise will start a chorus.
Similar duets have been observed inS. phaeota. In this species the intervals are often much longer than the notes, and if two males are calling in close proximity, their calls can be mistaken for those of one individual.Smilisca phaeotadoes not congregate in large numbers; usually only two males call from one restricted site.
Smilisca silahas a call consisting of a primary note followed by one or more secondary notes. Males often call in duets, but not necessarily so. In a duet, the first male usually utters only primary notes until the second individual responds; then each individual produces a rapid series of secondary notes.
Smilisca pumaalso produces primary and secondary notes. Although individuals sometimes call alone, duets, trios, or quartets were more common. The chorus is initiated by one individual uttering primary notes until joined by the second, third, and fourth frogs. In one quartet in a marsh 7.5 kilometers west of Puerto Viejo, Costa Rica, on February 19, 1965, the same individual initiated four consecutive choruses. Each time the second member of the chorus was the same; the third and fourth frogs joined the chorus nearly simultaneously.
Individuals ofS. sordidaare usually irregularly situated along a stream. No duets or other combinations of individuals are apparent in the chorus structure, but once an individual calls, a frog nearby calls almost immediately; then a frog near the second individual calls, and so on. The resulting series of calls gives the impression that the sound is moving along the stream as successive individuals join the chorus and the first callers become quiet. It is not known if the same individual initiates successive choruses or if the order of calling is the same in subsequent choruses.
These limited observations on chorus structure inSmiliscashow the presence of behavioral organization. The methods of establishing the organization and the significance of the call-order in breeding have yet to be discovered.
Calling males ofS. baudiniare often close together; some individuals have been observed almost touching one another, but no indication of territorialityor aggressive behavior has been witnessed. The more distant spacing of the stream-breeding speciesS. silaandS. sordidamay be a function of calling-territories, but no direct evidence is available to substantiate this supposition.
Sex recognition and amplexus.—Observations onSmilisca baudiniindicate that the calls of males attract females. At Tehuantepec, Oaxaca, México, a female was first observed about two meters away from a male calling at the edge of a rain pool; in a series of short hops she progressed directly towards the male, although vegetation obscured him until she was less than a meter away. When she approached to within about 20 centimeters of the male, he took notice of her, moved to her, and clasped her. At Chinajá, Alta Verapaz, Guatemala, a female swam directly across a pool about three meters wide to a calling male. Her line of movement took her within a few centimeters of a silent male, to whom she paid no attention. She stopped just in front of the calling male, which immediately clasped her. At a large muddy pond 4 kilometers west-northwest of Esparta, Puntarenas, Costa Rica, a female was observed swimming toward a small submerged tree; a male was calling from a branch about one meter above the water. The female climbed to a branch about 20 centimeters below the male, which upon seeing her there immediately jumped down and clasped her. These few observations ofS. baudinishow that in this species females are capable of locating calling males by means of phono-orientation; visual reception on the part of females seems to be secondary. Contrariwise, males apparently become aware of the proximity of females by seeing them; once a male sees a female he usually tries to clasp her. Possibly the males receive stimuli by means of chemo-reception, but in each observed instance the male obviously looked at the female.
Amplexus is axillary in all members of the genus. Normally amplexing males hunch their backs and press their chins to the females' backs. Clasping pairs are usually found at the edge of the water, but sometimes amplexus takes place in trees or bushes.
Egg deposition.—Oviposition has been observed only inSmilisca baudini. On the night of June 28, 1961, at Chinajá, Alta Verapaz, Guatemala, a clasping pair was observed at the edge of a shallow rain pool. After sitting for several minutes in shallow water, the female (with male on her back) swam part way across the pool and grasped an emergent stick with one hand. The female's body was nearly level with the surface of the water, and her hind legs were outstretched as deposition commenced; eggs were extruded rapidly. After a few seconds the female moved slowly to another twig a few centimeters away and deposited more eggs. This process was repeated until the female was spent. The spawn resulted in a surface film covering roughly one square meter. It is doubtful if this type of egg deposition occurs in any other species in the genus, especially those that lay their eggs in streams.
Breeding Call
The breeding calls of the six species ofSmiliscaare alike in their explosive nature. Calls are emitted quickly with a short burst of air filling the vocal sac, which immediately deflates. Phonetically the calls can be described as a single "wonk" or series of such notes inS. baudiniandS. cyanosticta, a low growl inS. phaeota, a relatively high pitched rattle inS. sordida, and a lowsquawk usually followed by one or more rattling secondary notes inS. pumaandS. sila. Quantitatively, the calls of the six species differ in number of notes, duration of notes, and in pitch (Table 8, Pls. 10 and 11). Although no measurements were taken on the intensity of the calls, we observed in the field that each of the species has a loud voice. The call ofS. baudiniseems to carry farther than any of the others.
Call rate.—The rate at which call-groups are produced varies from one every few seconds to one in several minutes. InS. baudini,cyanosticta,phaeota, andsordida, call-groups are produced as frequently as every 12 seconds, but usually more time elapses between call groups. InS. sordida, five or more minutes sometimes elapse between call-groups. The interval is somewhat less inS. phaeota. Calls are repeated at much shorter intervals inS. puma(5-55 seconds) andS. sila(4-20 seconds).
Notes per call-group.—Except forS. pumaandS. sila, the series of notes produced in any given call of a species ofSmiliscais essentially the same; there is no differentiation into primary and secondary notes.Smilisca cyanostictaandS. phaeotaemit only one or two relatively long notes per call-group, whereasS. baudiniandS. sordidaproduce as many as 15 and 6 notes, respectively. Males ofS. pumaandS. silaoften produce only the primary note; sometimes this is done several times before the secondary notes are produced. For example, oneS. puma(KU 91711; tape No. 379) produced the following number of notes in consecutive call-groups: 1, 1, 1, 1, 2, 2, 3, 1, 4; secondary notes are present in only four of the nine call-groups. A typical series of consecutive call-groups inS. sila(KU 91852; Tape No. 385) has 1, 1, 1, 2, 4, 2 notes per call-group; secondary notes are present in only half of the call-groups.Smilisca pumaapparently always produces at least two primary notes before emitting secondary notes; sometimes only primary notes are produced in one series of calls. The number of secondary notes following a given primary varies from one to nine; the modal number is one, and the mean is three in 27 call-groups.Smilisca silafrequently begins a series of calls with two or more primary notes, but sometimes the first primary note is followed immediately by two or more secondary notes. The number of secondary notes following a given primary varies from one to five; the modal number is one, and the average is two in 13 call-groups.
Duration.—The average duration of call-groups consisting of two or more notes is 1.18 seconds inS. baudini; 1.02 incyanosticta, 0.91 inphaeota, 1.32 inpuma, 1.48 insila, and 1.29 insordida. Although there is considerable variation in the lengths of the notes (only primary notes inS. pumaandsilaare considered here),S. cyanosticta,phaeota, andsordidahave noticeably longer notes than do the other species (Table 8). The secondary notes are longer than the primary notes inS. puma(average 0.27 secs. as compared with 0.13 secs.) and inS. sila(average 0.25 secs., as compared with 0.16 secs.).
Note repetition rate.—The rate at which notes in call-groups containing two or more notes are produced varies inS. baudinifrom 2.5 to 7.1 (average, 3.7) calls per second;cyanosticta, 1.8-2.1 (1.9);phaeota, 2.0-2.4 (2.2);puma, 1.9-2.9 (2.2);sila, 1.3-2.4 (1.8); andsordida, 1.5-2.6 (2.1).Smilisca baudini, which has notes of short duration (0.09 to 0.13 seconds), has the fastest note-repetition rate. Although the individual notes ofS. cyanostictaandS. phaeotaare relatively long (average, 0.38 and 0.31 seconds, respectively), the intervalsbetween the notes is short; consequently, their note-repetition rates do not differ greatly from those ofS. pumaandS. sila, which have shorter notes (average, 0.13 and 0.16 seconds, respectively) but longer intervals between notes.
Pulse rate.—Pulses vary in frequency from 78 to 240 per second in the calls analyzed (only primary notes inS. pumaandS. sila), but the variation in any given species is much less than that in the entire genus (Table 8).Smilisca pumais outstanding in having a high pulse rate, which is approached only by that ofS. baudini. Even in the species having the lowest pulse rates, the pulsations are not audible. The secondary notes produced byS. pumaandS. silahave a slower pulse rate than the primary notes; often the pulses are audible. InS. pumathe pulse rate of secondary notes is sometimes as low as 48 pulses per second, and inS. silastill lower (as low as 40 pulses per second). The upper limits of pulse rate in the secondary notes in these species merge imperceptibly with the rates of the primary note; consequently, on the basis of pulse rate alone it is not always possible to distinguish primary from secondary notes.
Frequency.—Smiliscaproduces noisy (as opposed to more musical) calls, and the energy is distributed throughout the frequency spectrum; the calls are poorly modulated, except inS. sordida, in which two usually discrete bands of frequency are present (Pl. 11C). For the most part the calls ofSmiliscaconsist of little modified energy of the fundamental frequency and of its harmonics, some of which are emphasized.
The upper frequency range varies within each species and even within the calls of one individual.Smilisca phaeotahas the lowest upper frequencies; no calls ranged above 4400 cycles per second (cps.), and half of the calls never exceeded 3000 cps.Smilisca cyanostictaproduces calls in which the upper frequency is below 7000 cps. and usually below 6000 cps. Likewise,S. pumaproduces calls that are below 7000 cps., whereasS. silahas frequencies of up to 8400 cps. In bothS. baudiniandS. sordida, the highest frequencies attained are about 9100 cps. Variation in the highest frequencies in a series of consecutive calls by one individual frog was noted in all species. Such variation is especially prevalent inS. puma; for example one individual (KU 87771; Tape No. 376) recorded at a temperature of 24° C. at 7.5 kilometers west of Puerto Viejo, Heredia Province, Costa Rica, on July 31, 1964, produced three consecutive primary notes having upper frequencies of about 6000, 4000, and 4000 cps., respectively. Apparently in a given species the production of the higher frequencies in some notes and not in others is correlated with the amount of distention of the vocal sac and is not dependent upon the structure or tension of the vocal cords.
Although the dominant frequency inS. sordidais lower than that inS. baudiniandS. cyanosticta, the call of the former is audibly higher-pitched. This is due primarily to the emphasis on certain harmonics at a high frequency (sometimes as high as 9000 cps.) inS. sordida, whereas inS. baudiniand other species, if harmonics are present at those frequencies, they are not emphasized.
The fundamental frequencies are as low as 90 cps. inS. silaandS. sordidaand as high as 200 cps. inS. puma(Table 8). The fundamental frequency seemingly is relatively unimportant in determining the general pitch of the call, a characteristic most dependent on the dominant frequency and emphasized harmonics in the higher-frequency spectrum. In none of the species is thefundamental the dominant frequency. In the low-pitched call ofS. phaeotathe dominant frequency is the third harmonic (the second harmonic above the fundamental frequency, which is the first harmonic). In all other species a much higher harmonic is dominant; for examples, inS. cyanostictaharmonics from 10 to 15 are dominant; inS. baudini, 15-19; andS. sila, 20-30.
A glance at the audiospectrographs and their accompanying sections (Pls. 10 and 11) reveals the presence of two emphasized bands of frequency in all species exceptS. phaeota, in which only the lower band is present. These two bands of emphasized harmonics are part of a continuous, or nearly continuous, spread of energy throughout the frequency spectrum, except inS. sordidain which the bands are usually distinct. As shown in the sections, certain harmonics in each of the bands are emphasized with nearly equal intensity. Therefore, with the exception ofS. phaeota, the calls ofSmiliscaare characterized by two major frequencies, one of which is the dominant frequency and the other is a subdominant frequency (Table 8). The upper major frequency is dominant in all calls inS. baudiniandS. cyanosticta, but either major frequency may be dominant in other species. The upper major frequency is dominant in 65 per cent of calls byS. puma, 87 per cent inS. sila, and 68 per cent inS. sordida. Individuals of these three species sometimes produce a series of calls in which the dominant frequency changes from one of the major frequencies to the other. Four consecutive notes emitted by an individual ofS. sordidarecorded 13 kilometers east-northeast of Golfito, Puntarenas Province, Costa Rica, had dominant frequencies of 910, 1950, and 750 cps., respectively. In each case, an alternation of major frequencies took place in respect to dominance. An individual ofS. pumafrom 7.5 kilometers west of Puerto Viejo, Costa Rica, produced a primary note followed by one secondary note; each note had major frequencies at 600 and 1800 cps.; the dominant frequency of the primary note was at 1800 cps., whereas in the secondary note the dominant frequency was at 600 cps. The difference in emphasis on the major frequencies is so slight that shift in dominance is not audible.
Effect of temperature on calls.—The present data are insufficient to test statistically the correlation between temperature and variation within certain components of the calls inSmilisca, but even a crude graph shows some general correlations. The widest range of temperatures is associated with the recordings ofS. baudini. Three individuals recorded at a temperature of 30° C. at Tehuantepec, Oaxaca, had pulse rates of 180 pulses per second and fundamental frequencies of 160-180 cps., as compared with an individual recorded at a temperature of 17° C., which had a pulse rate of 140 and a fundamental frequency of 135 cps. All individuals ofS. baudinirecorded at higher temperatures had faster pulse rates and higher fundamental frequencies. Pulse rates differ in the other species in the genus but less strikingly (probably owing to narrower ranges of temperatures at which recordings were made). In five recordings ofS. sordidamade at 20° C. the pulse rate is 80-90, as compared with four recordings made at 25° C. having pulse rates of 120-135. Thirteen recordings ofS. silamade at 17° C. have pulse rates of 97-112 (average 105); one individual recorded at 26° C. has 120 pulses per second. Seemingly no correlation exists between temperature and other characteristics of the calls, such as duration and rate of note-repetition.
The breeding call as an isolating mechanism.—Blair (1958), Bogert (1960), Duellman (1963a),Fouquette(1960), Johnson (1959), and others have providedevidence that the breeding calls of male hylids (and other anurans) serve as isolating mechanisms in sympatric species. In summarizing this discussion of the breeding calls ofSmiliscawe want to point out what seem to be important differences in the calls that may prevent interspecific hybridization in sympatric species ofSmilisca.
The genus is readily divided into two species-groups on morphological characters; this division is supported by the breeding calls. In the species of thebaudinigroup the calls are unmodulated and lack secondary notes. In thesordidagroup the calls either have secondary notes or are modulated.
Smilisca baudinioccurs sympatrically withS. cyanostictaandS. phaeota; where they occur together, both species sometimes breed in like places at the same time. We are not aware of these species breeding synchronously at exactly the same site, althoughS. baudiniandS. cyanostictawere calling on the same nights and less than 100 meters apart in Oaxaca in June, 1964. Regardless of their respective breeding habits, sympatric species have calls that differ notably. Except for the higher fundamental and dominant frequencies, the calls ofS. cyanostictaandS. phaeotaclosely resemble one another, but the calls of both species differ markedly from that ofS. baudini. The geographic ranges ofS. cyanostictaandS. phaeotaare widely separated.
The calls of the allopatric speciesS. pumaandS. silaare not greatly different.Smilisca sordidahas a distinctive call and occurs sympatrically withS. pumaandS. sila. In the streams in southern Costa RicaS. sordidaandS. silabreed synchronously, but the high-pitched modulated call of the former is notably different from the lower, unmodulated call ofS. sila.
The data indicate that the calls of related sympatric species differ more than the calls of related allopatric species. We postulate that these differences evolved to support the reproductive isolation of the sympatric species. The data are insufficient to determine geographic variation in the calls and to determine if differences in the calls are enhanced in areas of sympatry as compared with the allopatric parts of the ranges.
Other calls.—As stated previously, there is no direct evidence of territoriality inSmilisca; we have heard no calls that can be definitely identified as territorial. Single notes ofS. baudini,phaeota, andsilahave been heard by day, just prior to rains, or during, or immediately after rains. Such calls can be interpreted as "rain calls," which are well known inHyla eximiaandHyla squirella. Distress calls are known in several species ofRanaand inLeptodactylus pentadactylus; such calls result from the rapid expulsion of air over the vocal cords and with the mouth open. Distress calls have been heard fromS. baudini. At Charapendo, Michoacán, México, a male that had one hind limb engulfed by aLeptodeira maculataemitted several long, high-pitched cries. A clasping pair ofS. baudiniwas found in a bush at the edge of a marshy stream 2 kilometers northeast of Las Cañas, Guanacaste Province, Costa Rica. When the pair was grasped, the female emitted a distress call.
Eggs
Eggs ofS. baudini,cyanosticta, andphaeotahave been found in the field, and eggs ofS. silahave been observed in the laboratory. The eggs ofS. pumaandsordidaare unknown. Insofar as known,Smilisca baudiniis unique in the genus in depositing the eggs in a surface film. Each egg is encased in avitelline membrane, but individual outer envelopes are lacking. The eggs are small; the diameter of recently-deposited eggs is about 1.3 mm. and that of the vitelline membrane is about 1.5 mm. The eggs ofS. cyanostictaandphaeotaare deposited in clumps, and the eggs are larger than those ofS. baudini. Diameters of eggs ofS. cyanostictaare about 2.3 mm., and those of the outer envelopes are about 4.0 mm. Artificially fertilized eggs ofS. silaraised in the laboratory have diameters of about 2.4 mm.; the diameter of the outer envelopes is about 4.9 mm.
In order to determine the reproductive potential of the six species, ovulated eggs were removed from females and counted. The numbers of eggs recorded are: 3S. baudini—2620, 2940, 3320; 1S. cyanosticta—910; 3S. phaeota—1665, 1870, 2010; 1S. puma—518; 3S. sila—369, 390, 473; 3S. sordida—524, 702, 856. These limited data indicate that the large species (S. baudini,cyanosticta, andphaeota) have more eggs than do the smaller species. The stream-breeding species (S. silaandsordida) have relatively few eggs by comparison with the pond-breeders. Possibly this is a function of size of eggs rather than a correlation with the site of egg-deposition.
Tadpoles
The acquisition of tadpoles of all of the species ofSmiliscahas made possible the use of larval characters in erecting a classification and in estimating the phylogenetic relations of the several species. Furthermore, developmental series of tadpoles of four species allow a comparison of the growth and development in these species. Throughout the discussion of tadpoles we have referred to the various developmental stages by the Stage Numbers proposed by Gosner (1960).
General Structure
Tadpoles of the genusSmiliscaare of a generalized hylid type, having 2/3 tooth-rows, unspecialized beaks, mouth partly or completely bordered by papillae, lateral fold present in the lips, spiracle sinistral, anal tube dextral, and caudal musculature extending nearly to tip of caudal fin. Although minor differences exist in coloration, proportions, and mouthparts, no great modifications of the basic structure are present.
Comparison of Species
The larval characters of the species ofSmiliscaare compared below and illustrated in Figures 11-15.
Shape and Proportions.—The bodies ofS. baudini,cyanosticta,phaeota, andpumaare rounded and about as wide as deep; the eyes are moderately large and directed dorsolaterally, and the nostrils are about midway between the bluntly rounded snout and the eyes. The mouths are medium-sized and directed anteroventrally. The bodies of tadpoles ofS. silaandsordidaare slightly compressed dorso-ventrally. The snout is moderately long and sloping; the eyes are larger and directed more dorsally than in the other species, and the nostrils are closer to the eyes than the snout. The mouths are moderately large and directed ventrally.
The tail is about half again as long as the body inS. baudini,cyanosticta,phaeota, andpuma; in these species the caudal musculature is moderately heavy, and the caudal fins are deep. The caudal musculature is upturned distally inS. baudiniandphaeota, and the dorsal fin extends anteriorly onto the body in these two species and inS. puma. The tail is about twice as long as the body inS. silaandsordida. In both species the caudal fins are shallow in comparison with the depth of the caudal musculature, especially inS. sordida(Fig. 14); in neither species does the dorsal fin extend anteriorly onto the body.
Fig. 11.Tadpoles ofSmilisca baudini: (A) Stage 21 (KU 62155) × 10; (B) Stage 25 (KU 68467) × 5; (C) Stage 30 (KU 60018) × 4; (D) Stage 41 (KU 60018) × 3.
Fig. 11.Tadpoles ofSmilisca baudini: (A) Stage 21 (KU 62155) × 10; (B) Stage 25 (KU 68467) × 5; (C) Stage 30 (KU 60018) × 4; (D) Stage 41 (KU 60018) × 3.
Mouthparts.—The mouth ofS. sordidais completely bordered by two rows of papillae, whereas in the other species the median part of the upper lip is devoid of papillae.Smilisca baudiniandpumahave two rows of papillae;S. silahas one complete row (except medially on the upper lip) and one incomplete row, andS. cyanostictaandphaeotahave only one row (Fig. 15). All species have numerous papillae in the lateral fold; the fewest lateral papillaeare found inS. cyanostictaandphaeota. Although all species have two rows of teeth in the upper jaw and three rows in the lower jaw, specific differences in the nature of the rows exist between certain species. The second upper tooth-row is narrowly interrupted medially inS. silaandsordidaand broadly interrupted in the other species. The first upper row is strongly arched inS. puma, moderately arched inS. baudiniandsila, and weakly arched in the other species. In all species the third lower tooth-row is the shortest, only slightly so inS. silaandsordida, but only about half the length of the second lower row inS. puma.
Fig. 12.Tadpoles ofSmilisca cyanosticta: (A) Stage 21 (KU 87648) (B) Stage 25 (KU 87651) × 5; (C) Stage 30 (KU 87652) × 4; (D) Stage 40 (KU 87650) × 3.
Fig. 12.Tadpoles ofSmilisca cyanosticta: (A) Stage 21 (KU 87648) (B) Stage 25 (KU 87651) × 5; (C) Stage 30 (KU 87652) × 4; (D) Stage 40 (KU 87650) × 3.
The beaks are well developed and finely serrate in all species. The lower, broadly V-shaped, beak is slender inS. puma, rather robust inS. baudiniandsila, and moderately heavy in the other species. The lateral processes of the upper beak are shortest inS. pumaand longest inS. baudiniandsordida. In the latter the inner margin of the upper beak and lateral process have the form of a shallow S, whereas in the other species the inner margin of the upper beak forms a continuous arch with the lateral processes (Fig. 15).
Fig. 13.Tadpoles ofSmilisca phaeota: (A) Stage 21 (KU 68479) × 14; (B) Stage 25 (KU 68480) × 5; (C) Stage 30 (KU 68482) × 4; (D) Stage 40 (KU 68483) × 3.
Fig. 13.Tadpoles ofSmilisca phaeota: (A) Stage 21 (KU 68479) × 14; (B) Stage 25 (KU 68480) × 5; (C) Stage 30 (KU 68482) × 4; (D) Stage 40 (KU 68483) × 3.
Coloration.—The tadpoles ofSmiliscalack the bright colors or bold markings characteristic of some hylid tadpoles; even so, the subdued colors and arrangement of pigments provide some distinctive markings by which the species can be distinguished from one another. The species comprising thebaudinigroup (S. baudini,cyanosticta, andphaeota) are alike in having the body brown or grayish brown dorsally and transparent with scattered brown pigment ventrally. A cream-colored, crescent-shaped mark is present on the posterior edge of the body; this mark is usually most noticeable inS. baudiniand least so inS. cyanosticta. Other differences in coloration in members of thebaudinigroup are relative and subtle.Smilisca phaeotausually is morepallid thanbaudini, andcyanostictausually is darker thanbaudini; both species have larger dark markings on the tail than doesS. phaeota.Smilisca baudinihas a dark streak on the middle of the anterior one-fourth of the tail (Figs. 11-13).
Smilisca pumais distinctive in having a grayish brown body and dark gray reticulations on the tail.Smilisca silaandsordidaare distinctive in having pairs (sometimes interconnected) of dark marks on the dorsal surfaces of the caudal musculature, and in dorsal view the tail appears to be marked with dark and pale creamy tan transverse bars. These dark marks, as well as the small flecks on the tail, are brown inS. silaand red insordida.Smilisca silahas dark brown flecks on the dorsal surface of the body and small white flecks laterally; these markings are absent inS. sordida(Fig. 14).
Descriptions of the coloration of living tadpoles are given in the accounts of the species.
Fig. 14.Tadpoles ofSmilisca; (A)S. puma, Stage 30 (KU 91807); (B)S. sila, Stage 25 (KU 80260);S. sordida, Stage 30 (KU 68475). All × 3.5.
Fig. 14.Tadpoles ofSmilisca; (A)S. puma, Stage 30 (KU 91807); (B)S. sila, Stage 25 (KU 80260);S. sordida, Stage 30 (KU 68475). All × 3.5.
Growth and Development
Information on the growth and development of Middle American hylids is scanty. Adequate descriptions have been published forPhyllomedusa annae(Duellman, 1963b),Phrynohyas venulosa(Zweifel, 1964), andTriprion petasatus(Duellman and Klaas, 1964). Material is available for adequate descriptions of the developmental stages of four species ofSmilisca(Tables 9-12, Figs. 11-13). Because none of the tadpoles was raised from hatching to metamorphosis, the rate of growth and duration of the larval stages are unknown.
Fig. 15.Mouthparts of tadpoles ofSmilisca; (A)S. baudini(KU 60018); (B)S. puma(KU 91807); (C)S. cyanosticta(KU 87625); (D)S. sila(KU 80620); (E)S. phaeota(KU 68482); (F)S. sordida(KU 68475). All ×17.
Fig. 15.Mouthparts of tadpoles ofSmilisca; (A)S. baudini(KU 60018); (B)S. puma(KU 91807); (C)S. cyanosticta(KU 87625); (D)S. sila(KU 80620); (E)S. phaeota(KU 68482); (F)S. sordida(KU 68475). All ×17.
Hatchlings of three species (S. baudini,cyanosticta, andphaeota) are available. These larvae have non-functional eyes and large oral suckers. By the time the larvae have developed to stage 21, external gills are present, the caudal musculature and caudal fin have been differentiated, and the head is distinguishable from the body. In stage 21 oral suckers and a large amount of yolk are still present.
The developmental data on the four species show no significant variations; consequently, we will describe the development of only one species,Smilisca phaeota(Table 11, Figs. 13 and 16).
Stage 21.—Bulging cream-colored yolk mass, transparent cornea, and moderately long, unbranched filamentous gills, and oral suckers present; mouth having irregular papillae on lower lip; teeth and beaks absent; caudal myomeres distinct; pigmentation uniform over body and caudal musculature; caudal fin transparent with scattered small flecks.
Stage 21.—Bulging cream-colored yolk mass, transparent cornea, and moderately long, unbranched filamentous gills, and oral suckers present; mouth having irregular papillae on lower lip; teeth and beaks absent; caudal myomeres distinct; pigmentation uniform over body and caudal musculature; caudal fin transparent with scattered small flecks.
Fig. 16.Relative rate of growth in tadpoles ofSmilisca phaeotaas correlated with developmental stages. Formulas for the limb bud refer to its length (L) in relation to basal diameter (D).
Fig. 16.Relative rate of growth in tadpoles ofSmilisca phaeotaas correlated with developmental stages. Formulas for the limb bud refer to its length (L) in relation to basal diameter (D).
Stage 25.—Operculum complete; gills absent; sinistral spiracle apparently functional; cloacal tail-piece, nasal capsules, and external nares present; gutpartly formed; mouth bordered by single row of papillae, except medially; small papillae present in lateral fold of lips; two upper and three lower tooth-rows present, but not fully developed; beaks apparently fully developed; depth of dorsal and ventral fins less than depth of caudal musculature: tip of tail upturned; pigment on body most dense on dorsum and sides; faint, nearly pigmentless crescent-shaped mark on posterior edge of body; concentrations of pigment forming small spots on tail.Stage 28.—Mouthparts complete; limb bud about half as long as thick; other structural features and coloration closely resemble those in stage 25.Stage 30.—Limb bud approximately twice as long as thick; body as deep as wide; dorsal fin deepest just posterior to body; ventral fin deeper than caudal musculature; tail sharply upturned distally; anal tube dextral; brown pigment sparse on flanks.
Stage 25.—Operculum complete; gills absent; sinistral spiracle apparently functional; cloacal tail-piece, nasal capsules, and external nares present; gutpartly formed; mouth bordered by single row of papillae, except medially; small papillae present in lateral fold of lips; two upper and three lower tooth-rows present, but not fully developed; beaks apparently fully developed; depth of dorsal and ventral fins less than depth of caudal musculature: tip of tail upturned; pigment on body most dense on dorsum and sides; faint, nearly pigmentless crescent-shaped mark on posterior edge of body; concentrations of pigment forming small spots on tail.
Stage 28.—Mouthparts complete; limb bud about half as long as thick; other structural features and coloration closely resemble those in stage 25.
Stage 30.—Limb bud approximately twice as long as thick; body as deep as wide; dorsal fin deepest just posterior to body; ventral fin deeper than caudal musculature; tail sharply upturned distally; anal tube dextral; brown pigment sparse on flanks.
Stages 34,36,37, and38.—Stage 34, foot paddle-shaped with four toe buds; stage 36, five toe buds; stages 37 and 38, lengthening of toes. In all four stages, spiracle persistent, and pigmentation resembling that of early stages.Stage 39.—Metatarsal tubercle present; greatest total length (36.9 mm.) attained.Stage 40.—Subarticular tubercles prominent; skin over forelimbs transparent; cloacal tail-piece and spiracle absent; outer tooth-rows degenerating; caudal fins shallower than in preceding stages; distal part of tail nearly straight; size of dark markings on tail decreased; pigment present on hind limb.Stage 43.—Forelimbs erupted; larval mouthparts absent; corner of mouth between nostril and eye; transverse bands present on hind limbs; tail greatly reduced (about 8 mm. in length).Stage 44.—Sacral hump barely noticeable; tail reduced to a stub; corner of mouth at level of pupil of eye; dorsal surfaces pale olive-green; venter white.
Stages 34,36,37, and38.—Stage 34, foot paddle-shaped with four toe buds; stage 36, five toe buds; stages 37 and 38, lengthening of toes. In all four stages, spiracle persistent, and pigmentation resembling that of early stages.
Stage 39.—Metatarsal tubercle present; greatest total length (36.9 mm.) attained.
Stage 40.—Subarticular tubercles prominent; skin over forelimbs transparent; cloacal tail-piece and spiracle absent; outer tooth-rows degenerating; caudal fins shallower than in preceding stages; distal part of tail nearly straight; size of dark markings on tail decreased; pigment present on hind limb.
Stage 43.—Forelimbs erupted; larval mouthparts absent; corner of mouth between nostril and eye; transverse bands present on hind limbs; tail greatly reduced (about 8 mm. in length).
Stage 44.—Sacral hump barely noticeable; tail reduced to a stub; corner of mouth at level of pupil of eye; dorsal surfaces pale olive-green; venter white.
Changes proceed in a definite pattern during the growth and development of tadpoles. Larval teeth are absent in hatchlings; the inner tooth-rows develop first, and the third lower row last. At metamorphosis the third lower row is the first to be lost. The tail increases gradually in length relative to the body. In stage 25 the tail is 52.1 per cent of the total length, and in stage 36, 64.6 per cent. In later stages the tail becomes relatively shorter through resorption. Duellman and Klaas (1964:320) noted a great size-variation inTripriontadpoles in stage 25. No such variation is apparent in any stage of any of the species ofSmiliscastudied.
The growth and development of the other species ofSmiliscado not differ significantly from that ofS. phaeota. The tadpoles ofS. silaandsordidafrom streams have relatively longer tails at hatching. For example, in tadpoles ofS. sordidathe average length of tail is 64.0 per cent of the body-length in stage 25, and in stage 37, 67.0 per cent.