Neotropical Hylid Frogs, Genus Smilisca Part 11
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Table 7.--Breeding a.s.sociates of the Various Species of Smilisca.
==============================+========+============+========+=====+=====+======== a.s.sociate |_S. |_S. |_S. |_S. |_S. |_S.
|baudini_|cyanosticta_|phaeota_|puma_|sila_|sordida_ ------------------------------+--------+------------+--------+-----+-----+-------- _Rhinophrynus dorsalis_ | X | - | - | - | - | - _Leptodactylus bolivia.n.u.s_ | - | - | X | - | - | - _Leptodactylus l.a.b.i.alis_ | X | - | X | - | - | - _Leptodactylus melanonotus_ | X | - | X | X | X | - _Leptodactylus occidentalis_ | X | - | - | - | - | - _Leptodactylus quadrivittatus_| - | - | X | - | - | - _Leptodactylus pentadactylus_ | - | - | X | X | - | X _Engystomops pustulosus_ | X | - | X | - | - | - _Bufo ca.n.a.liferus_ | X | - | - | - | - | - _Bufo cavifrons_ | - | X | - | - | - | - _Bufo coccifer_ | X | - | - | - | - | - _Bufo coniferus_ | - | - | X | - | - | - _Bufo cristatus_ | - | X | - | - | - | - _Bufo gemmifer_ | X | - | - | - | - | - _Bufo haemat.i.ticus_ | - | - | X | - | X | X _Bufo kellogi_ | X | - | - | - | - | - _Bufo luetkeni_ | X | - | - | - | - | - _Bufo marinus_ | X | - | X | X | X | X _Bufo marmoreus_ | X | - | - | - | - | - _Bufo mazatlanensis_ | X | - | - | - | - | - _Bufo melanochloris_ | - | - | X | - | X | X _Bufo perplexus_ | X | - | - | - | - | - _Bufo typhonius_ | - | - | X | - | X | - _Atelopus varius_ | - | - | - | - | X | X _Diaglena reticulata_ | X | - | - | - | - | - _Diaglena spatulata_ | X | - | - | - | - | - ------------------------------+--------+------------+--------+-----+-----+--------
Table 7.--_Continued_ ==============================+========+============+========+=====+=====+======== a.s.sociate |_S. |_S. |_S. |_S. |_S. |_S.
|baudini_|cyanosticta_|phaeota_|puma_|sila_|sordida_ ------------------------------+--------+------------+--------+-----+-----+-------- _Hyla boulengeri_ | - | - | X | - | - | - _Hyla colymba_ | - | - | - | - | X | - _Hyla ebraccata_ | X | - | X | - | - | - _Hyla elaeochroa_ | - | - | X | X | - | - _Hyla eximia_ | X | - | - | - | - | - _Hyla legleri_ | - | - | - | - | - | X _Hyla microcephala_ | X | - | X | - | - | - _Hyla phlebodes_ | - | - | X | X | - | - _Hyla picta_ | X | - | - | - | - | - _Hyla robertmertensi_ | X | - | - | - | - | - _Hyla rosenbergi_ | - | - | X | - | - | - _Hyla rufioculis_ | - | - | - | - | - | X _Hyla smithi_ | X | - | - | - | - | - _Hyla staufferi_ | X | - | - | - | - | - _Hyla walkeri_ | X | - | - | - | - | - _Phrynohyas inflata_ | X | - | - | - | - | - _Phrynohyas spilomma_ | X | - | - | - | - | - _Phrynohyas venulosa_ | X | - | - | - | - | - _Phyllomedusa callidryas_ | X | - | X | - | - | - _Phyllomedusa dacnicolor_ | X | - | - | - | - | - _Phyllomedusa moreleti_ | X | X | - | - | - | - _Pternohyla fodiens_ | X | - | - | - | - | - _Smilisca baudini_ | X | X | - | - | - | - _Smilisca cyanosticta_ | X | X | - | - | - | - _Smilisca phaeota_ | - | - | X | - | - | - _Smilisca puma_ | - | - | - | X | - | - ------------------------------+--------+------------+--------+-----+-----+--------
Table 7.--_Concluded_ ==============================+========+============+========+=====+=====+======== a.s.sociate |_S. |_S. |_S. |_S. |_S. |_S.
|baudini_|cyanosticta_|phaeota_|puma_|sila_|sordida_ ------------------------------+--------+------------+--------+-----+-----+-------- _Smilisca sila_ | - | - | - | - | X | X _Smilisca sordida_ | - | - | X | - | X | X _Triprion petasatus_ | X | - | - | - | - | - _Cochranella fleischmanni_ | - | - | - | - | X | X _Centrolene prosoblepon_ | - | - | - | - | X | - _Gastrophryne elegans_ | X | - | - | - | - | - _Gastrophryne olivacea_ | X | - | - | - | - | - _Gastrophryne usta_ | X | - | - | - | - | - _Hypopachus alboventer_ | X | - | - | - | - | - _Hypopachus caprimimus_ | X | - | - | - | - | - _Hypopachus inguinalis_ | X | - | - | - | - | - _Hypopachus maculatus_ | X | - | - | - | - | - _Hypopachus oxyrrhinus_ | X | - | - | - | - | - _Hypopachus variolosus_ | X | - | - | - | - | - _Rana palmipes_ | X | - | X | X | - | - _Rana pipiens_ | X | - | - | - | - | - _Rana warschewitschi_ | - | - | X | - | X | X ------------------------------+--------+------------+--------+-----+-----+--------
_Chorus structure._--Limited observations on some of the species of _Smilisca_ show a definite organization of the calling behavior of individuals. _Smilisca baudini_ and _S. phaeota_ call in duets. This is especially noticeable in _S. baudini_, in which the members of a duet often call from sites separated by only a few centimeters. The call of _S. baudini_ consists 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 s.p.a.ced so that they are emitted in the intervals between the notes of the first individual. This can be shown diagrammatically by having the figure "1" represent notes of the first individual and figure "2," the notes of the second; an empty interval is represented by "0":
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:
1-0-1-2-1-2-1-2-1-2-1-2-1-2 3-0-3-4-3-4-3-4-3-4-3-4-3 5-6-5-6-5-6-5-6-5-6-5-6 7-8-7-8-7-8-7-8-7-8-7-8
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 in _S. 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 phaeota_ does not congregate in large numbers; usually only two males call from one restricted site.
_Smilisca sila_ has 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 puma_ also 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 of _S. sordida_ are 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 in _Smilisca_ show the presence of behavioral organization. The methods of establis.h.i.+ng the organization and the significance of the call-order in breeding have yet to be discovered.
Calling males of _S. baudini_ are often close together; some individuals have been observed almost touching one another, but no indication of territoriality or aggressive behavior has been witnessed. The more distant s.p.a.cing of the stream-breeding species _S. sila_ and _S.
sordida_ may be a function of calling-territories, but no direct evidence is available to substantiate this supposition.
_s.e.x recognition and amplexus._--Observations on _Smilisca baudini_ indicate that the calls of males attract females. At Tehuantepec, Oaxaca, Mexico, 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 Chinaja, 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 of _S. baudini_ show 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 in _Smilisca baudini_. On the night of June 28, 1961, at Chinaja, 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 sp.a.w.n 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 of _Smilisca_ are 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 in _S.
baudini_ and _S. cyanosticta_, a low growl in _S. phaeota_, a relatively high pitched rattle in _S. sordida_, and a low squawk usually followed by one or more rattling secondary notes in _S. puma_ and _S. sila_.
Quant.i.tatively, 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 of _S.
baudini_ seems 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 a.n.a.lyzed Here.)
==============+====+=======+===========+=========+=========+=======================+ | | Notes | | | Funda- | Major | Species | | per | Duration | Pulses | mental | frequencies (cps) | | N | call | of note | per |frequency+-----------+-----------+ | | group | (seconds) | second | (cps) | Lower | Upper | --------------+----+-------+-----------+---------+---------+-----------+-----------+ _S. | 20 | 8.0 | 0.11 | 174.7 | 166.2 | 351 | 2507 | baudini_ | | (2-15)|(0.09-0.13)|(140-195)|(135-190)| (175-495) |(2400-2725)| | | | | | | | | _S. | 10 | 1.2 | 0.38 | 147.0 | 145.1 | 841 | 1894 | cyanosticta_| | (1-2) |(0.25-0.45)|(110-180)|(135-160)| (480-975) |(1600-2100)| | | | | | | | | _S. phaeota_ | 10 | 1.6 | 0.31 | 116.0 | 143.0 | 372 | -- | | | (1-2) |(0.10-0.45)|(100-130)|(110-165)| (330-495) | -- | | | | | | | | | _S. puma_ | 28 | 3.7 | 0.13 | 208.2 | 145.6 | 743 | 1868 | | | (2-10)|(0.06-0.35)|(187-240)|(125-200)| (495-980) |(1456-2240)| | | | | | | | | _S. sila_ | 15 | 2.4 | 0.16 | 108.5 | 103.0 | 899 | 2218 | | | (1-6) |(0.06-0.28)| (97-120)| (90-115)| (665-1180)|(1980-2700)| | | | | | | | | _S. sordida_ | 19 | 1.7 | 0.29 | 104.7 | 123.1 | 1216 | 2694 | | | (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. In _S. baudini_, _cyanosticta_, _phaeota_, and _sordida_, call-groups are produced as frequently as every 12 seconds, but usually more time elapses between call groups. In _S. sordida_, five or more minutes sometimes elapse between call-groups. The interval is somewhat less in _S. phaeota_.
Calls are repeated at much shorter intervals in _S. puma_ (5-55 seconds) and _S. sila_ (4-20 seconds).
_Notes per call-group._--Except for _S. puma_ and _S. sila_, the series of notes produced in any given call of a species of _Smilisca_ is essentially the same; there is no differentiation into primary and secondary notes. _Smilisca cyanosticta_ and _S. phaeota_ emit only one or two relatively long notes per call-group, whereas _S. baudini_ and _S. sordida_ produce as many as 15 and 6 notes, respectively. Males of _S. puma_ and _S. sila_ often produce only the primary note; sometimes this is done several times before the secondary notes are produced. For example, one _S. 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 in _S. 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 puma_ apparently 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 sila_ frequently 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 in _S. baudini_; 1.02 in _cyanosticta_, 0.91 in _phaeota_, 1.32 in _puma_, 1.48 in _sila_, and 1.29 in _sordida_.
Although there is considerable variation in the lengths of the notes (only primary notes in _S. puma_ and _sila_ are considered here), _S.
cyanosticta_, _phaeota_, and _sordida_ have noticeably longer notes than do the other species (Table 8). The secondary notes are longer than the primary notes in _S. puma_ (average 0.27 secs. as compared with 0.13 secs.) and in _S. sila_ (average 0.25 secs., as compared with 0.16 secs.).
_Note repet.i.tion rate._--The rate at which notes in call-groups containing two or more notes are produced varies in _S. baudini_ from 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); and _sordida_, 1.5-2.6 (2.1). _Smilisca baudini_, which has notes of short duration (0.09 to 0.13 seconds), has the fastest note-repet.i.tion rate. Although the individual notes of _S. cyanosticta_ and _S. phaeota_ are relatively long (average, 0.38 and 0.31 seconds, respectively), the intervals between the notes is short; consequently, their note-repet.i.tion rates do not differ greatly from those of _S.
puma_ and _S. 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 a.n.a.lyzed (only primary notes in _S. puma_ and _S. sila_), but the variation in any given species is much less than that in the entire genus (Table 8). _Smilisca puma_ is outstanding in having a high pulse rate, which is approached only by that of _S. baudini_. Even in the species having the lowest pulse rates, the pulsations are not audible.
The secondary notes produced by _S. puma_ and _S. sila_ have a slower pulse rate than the primary notes; often the pulses are audible. In _S.
puma_ the pulse rate of secondary notes is sometimes as low as 48 pulses per second, and in _S. sila_ still 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._--_Smilisca_ produces noisy (as opposed to more musical) calls, and the energy is distributed throughout the frequency spectrum; the calls are poorly modulated, except in _S. sordida_, in which two usually discrete bands of frequency are present (Pl. 11C). For the most part the calls of _Smilisca_ consist 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 phaeota_ has the lowest upper frequencies; no calls ranged above 4400 cycles per second (cps.), and half of the calls never exceeded 3000 cps. _Smilisca cyanosticta_ produces calls in which the upper frequency is below 7000 cps. and usually below 6000 cps. Likewise, _S. puma_ produces calls that are below 7000 cps., whereas _S. sila_ has frequencies of up to 8400 cps. In both _S. baudini_ and _S. 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 in _S. 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 in _S. sordida_ is lower than that in _S. baudini_ and _S. 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.) in _S.
sordida_, whereas in _S. baudini_ and other species, if harmonics are present at those frequencies, they are not emphasized.
The fundamental frequencies are as low as 90 cps. in _S. sila_ and _S.
sordida_ and as high as 200 cps. in _S. 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 the fundamental the dominant frequency. In the low-pitched call of _S. phaeota_ the 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, in _S. cyanosticta_ harmonics from 10 to 15 are dominant; in _S. baudini_, 15-19; and _S. 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 except _S. 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 in _S. sordida_ in 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 of _S. phaeota_, the calls of _Smilisca_ are 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 in _S. baudini_ and _S. cyanosticta_, but either major frequency may be dominant in other species. The upper major frequency is dominant in 65 per cent of calls by _S. puma_, 87 per cent in _S. sila_, and 68 per cent in _S. 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 of _S. sordida_ recorded 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 of _S. puma_ from 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 s.h.i.+ft 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 in _Smilisca_, but even a crude graph shows some general correlations. The widest range of temperatures is a.s.sociated with the recordings of _S. 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 of _S. baudini_ recorded 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 of _S. sordida_ made 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 of _S. sila_ made 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-repet.i.tion.
_The breeding call as an isolating mechanism._--Blair (1958), Bogert (1960), Duellman (1963a), Fouquette (1960), Johnson (1959), and others have provided evidence 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 of _Smilisca_ we want to point out what seem to be important differences in the calls that may prevent interspecific hybridization in sympatric species of _Smilisca_.
The genus is readily divided into two species-groups on morphological characters; this division is supported by the breeding calls. In the species of the _baudini_ group the calls are unmodulated and lack secondary notes. In the _sordida_ group the calls either have secondary notes or are modulated.
_Smilisca baudini_ occurs sympatrically with _S. cyanosticta_ and _S.
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, although _S. baudini_ and _S.
Neotropical Hylid Frogs, Genus Smilisca Part 11
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