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 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 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_.
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 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 Analyzed 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 repetition 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-repetition 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-repetition 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 analyzed (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 deg. 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 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 in _Smilisca_, but even a crude
graph shows some general correlations. The widest range of temperatures
is associated with the recordings of _S. baudini_. Three individuals
recorded at a temperature of 30 deg. 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 deg.
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 deg. C. the pulse rate is
80-90, as compared with four recordings made at 25 deg. C. having pulse
rates of 120-135. Thirteen recordings of _S. sila_ made at 17 deg. C. have
pulse rates of 97-112 (average 105); one individual recorded at 26 deg. 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 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.
cyanosticta_ were 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 of _S.
cyanosticta_ and _S. phaeota_ closely resemble one another, but the
calls of both species differ markedly from that of _S. baudini_. The
geographic ranges of _S. cyanosticta_ and _S. phaeota_ are widely
separated.
The calls of the allopatric species _S. puma_ and _S. sila_ are not
greatly different. _Smilisca sordida_ has a distinctive call and occurs
sympatrically with _S. puma_ and _S. sila_. In the streams in southern
Costa Rica _S. sordida_ and _S. sila_ breed synchronously, but the
high-pitched modulated call of the former is notably different from the
lower, unmodulated call of _S. 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 in _Smilisca_; we have heard no calls that can be
definitely identified as territorial. Single notes of _S. baudini_,
_phaeota_, and _sila_ have 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 in _Hyla eximia_ and _Hyla
squirella_. Distress calls are known in several species of _Rana_ and in
_Leptodactylus pentadactylus_; such calls result from the rapid
expulsion of air over the vocal cords and with the mouth open. Distress
calls have been heard from _S. baudini_. At Charapendo, Michoacan,
Mexico, a male that had one hind limb engulfed by a _Leptodeira
maculata_ emitted several long, high-pitched cries. A clasping pair of
_S. baudini_ was found in a bush at the edge of a marshy stream 2
kilometers northeast of Las Canas, Guanacaste Province, Costa Rica. When
the pair was grasped, the female emitted a distress call.
Eggs
Eggs of _S. baudini_, _cyanosticta_, and _phaeota_ have been found in
the field, and eggs of _S. sila_ have been observed in the laboratory.
The eggs of _S. puma_ and _sordida_ are unknown. Insofar as known,
_Smilisca baudini_ is unique in the genus in depositing the eggs in a
surface film. Each egg is encased in a vitelline 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 of _S. cyanosticta_ and _phaeota_ are
deposited in clumps, and the eggs are larger than those of _S. baudini_.
Diameters of eggs of _S. cyanosticta_ are about 2.3 mm., and those of
the outer envelopes are about 4.0 mm. Artificially fertilized eggs of
_S. sila_ raised 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: 3 _S. baudini_--2620, 2940, 3320; 1 _S. cyanosticta_--910;
3 _S. phaeota_--1665, 1870, 2010; 1 _S. puma_--518; 3 _S. sila_--369,
390, 473; 3 _S. sordida_--524, 702, 856. These limited data indicate
that the large species (_S. baudini_, _cyanosticta_, and _phaeota_) have
more eggs than do the smaller species. The stream-breeding species (_S.
sila_ and _sordida_) 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 of _Smilisca_ has 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 genus _Smilisca_ are 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 of _Smilisca_ are compared below
and illustrated in Figures 11-15.
_Shape and Proportions._--The bodies of _S. baudini_, _cyanosticta_,
_phaeota_, and _puma_ are 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 of
_S. sila_ and _sordida_ are 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 in _S. baudini_,
_cyanosticta_, _phaeota_, and _puma_; in these species the caudal
musculature is moderately heavy, and the caudal fins are deep. The
caudal musculature is upturned distally in _S. baudini_ and _phaeota_,
and the dorsal fin extends anteriorly onto the body in these two species
and in _S. puma_. The tail is about twice as long as the body in _S.
sila_ and _sordida_. In both species the caudal fins are shallow in
comparison with the depth of the caudal musculature, especially in _S.
sordida_ (Fig. 14); in neither species does the dorsal fin extend
anteriorly onto the body.
[Illustration: FIG. 11. Tadpoles of _Smilisca baudini_: (A) Stage
21 (KU 62155) x 10; (B) Stage 25 (KU 68467) x 5; (C) Stage 30
(KU 60018) x 4; (D) Stage 41 (KU 60018) x 3.]
_Mouthparts._--The mouth of _S. sordida_ is completely bordered by two
rows of papillae, whereas in the other species the median part of the
upper lip is devoid of papillae. _Smilisca baudini_ and _puma_ have two
rows of papillae; _S. sila_ has one complete row (except medially on the
upper lip) and one incomplete row, and _S. cyanosticta_ and _phaeota_
have only one row (Fig. 15). All species have numerous papillae in the
lateral fold; the fewest lateral papillae are found in _S. cyanosticta_
and _phaeota_. 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 in _S. sila_ and _sordida_ and broadly
interrupted in the other species. The first upper row is strongly arched
in _S. puma_, moderately arched in _S. baudini_ and _sila_, and weakly
arched in the other species. In all species the third lower tooth-row is
the shortest, only slightly so in _S. sila_ and _sordida_, but only
about half the length of the second lower row in _S. puma_.
[Illustration: FIG. 12. Tadpoles of _Smilisca cyanosticta_:
(A) Stage 21 (KU 87648) (B) Stage 25 (KU 87651) x 5;
(C) Stage 30 (KU 87652) x 4; (D) Stage 40 (KU 87650) x 3.]