baudini_; _A. M. E. S._, adductor mandibulae externus
superficialis; _A. M. P. S._, adductor mandibulae posterior
subexternus; _Col._, columella; _D. M._ depressor mandibulae;
_M. B. T. N._, mandibular branch trigeminal nerve;
_Sq._, squamosal. KU 64214, x5.]
[Illustration: FIG. 10. Ventral view of throat musculature in an
adult male _Smilisca baudini_ (Superficial musculature on left,
deep musculature on right); _A. C._ anterior cornua of hyoid;
_Gen. L._, geniohyoideus lateralis; _Gen. M._, geniohyoideus
medialis; _Hyo._, hyoglossus; _Omo._, omosternum; _Pet._,
petrohyoideus; _S._, submentalis; _Sm._, submaxillaris;
_St._, sternohyoideus; _V. S._, vocal sac. KU 64220, x 2.5.]
_Throat Musculature._--The frogs that comprise the genus _Smilisca_ are
characterized by paired subgular vocal sacs, essentially the same as
those in _Triprion_ (Duellman and Klaas, 1964). The following
description is based on _Smilisca baudini_ (Fig. 10).
M. submentalis lies in the anterior angle of the lower jaw, is thick,
and consists of transverse fibers extending between the dentaries. M.
submaxillaris is thin and arises from the whole of the inner surface of
the lower jaw, except for the anterior angle occupied by M. submentalis.
Anteriorly M. submaxillaris is broadly attached by fascia to M.
hyoglossus and M. geniohyoideus, which lie dorsal to M. submaxillaris.
Medially this attachment continues posteriorly for about one-half the
length of the hyoglossus. Posteriorly M. submaxillaris is folded and
attached to M. sternoradialis of the pectoral girdle. The vocal sacs are
formed by a pair of posterolateral evaginations of M. submaxillaris; a
broad connection between the pouches allows free passage of air between
the pouches.
The deeper throat musculature is essentially the same as that described
for _Phrynohyas spilomma_ by Duellman (1956), except for slight
differences in the place of attachment on the hyoid.
Skin
_Structure_
The skin of _Smilisca_ is typical of that of most hylids in organization
and structure. _Smilisca sila_ is distinguished from other members of
the genus by the presence of small wartlike protrusions and peculiar
white, pustular spots on the dorsum. The wartlike structures are
composed of three or four epidermal cells, which protrude from the
surface of the epidermis; the structures are covered by a slightly
thickened layer of keratin. The white pustules are slightly elevated
above the surrounding skin. Internally they consist of aggregations of
swollen, granular, pigment-cells (perhaps lipophores) lying between the
epidermis and the melanophores.
_Biochemical Variations_
Dried skins of all species of _Smilisca_ were sent to Jose M. Cei,
Instituto Nacional de Cuyo, Mendoza, Argentina, for biochemical
screening by means of the chromatographic techniques described by
Erspamer and Cei (1963). The species in the _baudini_ group have
detectable amounts of penta-hydroxi-trypatamine, whereas only a trace is
present in the other species. Furthermore, species in the _baudini_
group differ from _S. sila_ and the _sordida_ group in lacking, or
having only a trace of, tryptophan-containing polypeptides. These
superficial biochemical tests support the arrangement of species as
ascertained by conventional taxonomic characters.
External Morphological Characters
The features of external morphology that were studied in connection with
the taxonomy of the genus _Smilisca_ are discussed below.
_Size and Proportions_
The frogs of the genus _Smilisca___ are medium to large tree frogs. The
three species comprising the _baudini_ group (_S. baudini_,
_cyanosticta_, and _phaeota_) are notably larger than _S. puma_, _sila_,
and _sordida_ (Table 6). The largest specimen that we examined is a
female of _S. baudini_ having a snout-vent length of 90 mm. _Smilisca
puma_ is the smallest species; the largest male has a snout-vent length
of 38 mm. and the largest female, 46 mm.
Table 6.--Comparison of Sizes and Certain Proportions of the Species
of Smilisca. (Means in Parentheses Below Observed Ranges; Data for
Males Only.)
================+====+===========+=============+===========+
| | Snout-vent|Tibia length/| Tympanum/ |
Species | N | length | snout-vent | eye |
----------------+----+-----------+-------------+-----------+
| | | | |
_S. baudini_ |140 | 47.3-75.9 | 42.1-53.6 | 56.1-94.4 |
| | (58.7) | (47.8) | (73.5) |
| | | | |
_S. cyanosticta_| 40 | 44.6-56.8 | 51.9-59.7 | 62.7-88.4 |
| | (50.7) | (56.0) | (71.4) |
| | | | |
_S. phaeota_ | 50 | 40.8-65.5 | 50.9-60.2 | 62.7-85.5 |
| | (53.9) | (55.5) | (76.6) |
| | | | |
_S. puma_ | 20 | 31.9-38.1 | 48.2-53.1 | 52.1-72.2 |
| | (34.7) | (51.3) | (64.9) |
| | | | |
_S. sila_ | 33 | 31.6-44.8 | 49.7-58.1 | 47.6-58.3 |
| | (37.7) | (54.8) | (53.2) |
| | | | |
_S. sordida_ | 55 | 31.9-44.6 | 50.5-57.1 | 46.5-57.1 |
| | (37.9) | (53.4) | (49.1) |
----------------+----+-----------+-------------+-----------+
No outstanding differences in proportions exist between species,
although certain proportions are sufficiently different in some species
to warrant mention. _Smilisca baudini_ is a more squat and stocky frog
than other members of the genus; this is reflected in the somewhat
shorter hind legs (Table 6). The size of the tympanum relative to that
of the eye is highly variable within samples of a given species. Even
so, noticeable differences in the tympanum/eye ratio are apparent.
Members of the _baudini_ group have the largest tympani, whereas _S.
sila_ and _sordida_ have the smallest, and _S. puma_ is intermediate
(Table 6).
_Shape of Snout_
Although all members of the genus have rather truncate snouts, subtle
differences exist among the species (Pl. 12). _Smilisca sila_ has the
shortest snout; that of _S. baudini_ is only slightly longer. The snouts
of _S. cyanosticta_ and _puma_ are nearly square in lateral profile,
whereas those of _S. phaeota_ and _sordida_ are slightly inclined. The
shape of the snout is relatively uniform within each species and
displays no noticeable sexual dimorphism, except in _S. sordida_, in
which there are sexual differences and geographic variation (see p.
324).
_Hands and Feet_
The characters of the hands and feet are among the most taxonomically
important external features in _Smilisca_. Consistent differences exist
in relative lengths of the digits, size of subarticular tubercles, size
and number of supernumerary tubercles, size and shape of the inner
metatarsal tubercle, and amount of webbing (Pls. 4 and 5). In the
_baudini_ group the series of species (_baudini-phaeota-cyanosticta_)
show a progressive increase in amount of webbing in the hand and a
decrease in number, and corresponding increase in size, of supernumerary
tubercles. The amount of webbing in the feet of _S. baudini_ and
_phaeota_ is about the same, but the webbing is slightly more extensive
in _S. cyanosticta_. _Smilisca puma_ is unique in the genus in lacking
webbing in the hand; furthermore, this species is distinctive in having
many large subarticular tubercles on the hand and a relatively small
inner metatarsal tubercle. The two stream-inhabitants, _S. sila_ and
_sordida_, have shorter and stouter fingers than the other species. The
webbing is most extensive in both the hands and feet of these species,
which also are distinctive in having many small supernumerary tubercles
on the feet.
_Ontogenetic Changes_
Minor ontogenetic changes in structure involve the shape of the snout,
relative size of the eye, development of the tympanum, and amount of
webbing in the hand. In recently metamorphosed young the snout is more
rounded than in adults; the canthus and loreal concavity are not
evident. Usually the tympanum is not differentiated in recently
metamorphosed young, and the eye is proportionately large. The webbing
in the feet is completely developed at metamorphosis, but young
individuals have noticeably less webbing in the hand than do adults of
the same species.
Coloration
Some of the most distinctive characters of the species of _Smilisca_ are
color and pattern of the living frogs. Although many chromatic features
are lost or subdued in preserved specimens, the patterns usually
persist.
_Metachrosis_
Change in color, well known in frogs, is common in hylids, especially in
species having green dorsal surfaces (_Phyllomedusa_ is a notable
exception). The non-green _Smilisca_ (_puma_, _sila_, and _sordida_)
changes color, but this mostly is a change in intensity of color. In
these species the markings usually are most distinct at night;
frequently by day the frogs become pallid. The most striking examples of
metachrosis in _Smilisca_ are found in the _baudini_ group, in which the
dorsal ground-color changes from green to tan; correlated with the
change in ground-color may be a corresponding change in the dorsal
markings, but the dorsal markings may change to the opposite color.
Chromosomes
Chromosomes of all six species of _Smilisca_ were studied by means of
the propriono-orcein squash technique described by Duellman and Cole
(1965). Karyotype analysis was attempted for several species by means of
intraperitoneal injections of colchicine, which affected the mitotic
cells as desired, but the testes examined contained too few mitotic
cells to allow accurate determination of karyotypes.
Haploid (_n_) chromosome numbers were determined from cells in
diakinesis, metaphase I, and metaphase II of meiosis. Diploid (2_n_)
chromosome numbers were determined from cells in late prophase and
metaphase of mitosis. Chromosome counts from as few as 23 meiotic cells
of _S. phaeota_ and as many as 80 cells of _S. sordida_ reveal a
constant haploid (_n_) number of 12; counts of chromosomes in one to
five mitotic cells in all species, except _S. sila_, reveal that the
diploid (2_n_) number is 24.
NATURAL HISTORY
Breeding
Like most hylid frogs _Smilisca_ is most readily collected and observed
when individuals congregate for breeding.
_Time of Breeding_
_Smilisca_ breeds primarily in quiet water and reaches its height of
breeding activity at times of plentiful rainfall,--usually from May
through October. Through most of its range _Smilisca baudini_ breeds in
those months, but in some places where abundant rain falls in other
seasons, the species breeds at those times. For example, in southern El
Peten and northern Alta Verapaz, Guatemala, _Smilisca baudini_ has been
found breeding in February and March. The other pond-breeding species
(_S. cyanosticta_, _phaeota_, and _puma_) live in regions lacking a
prolonged dry season, and possibly they breed throughout the year, but
breeding activity seems to be greatest in the rainiest months.
The two stream-breeding species (_S. sila_ and _sordida_) breed in the
dry season when the streams are low and clear, principally in December
through April. At high elevations the species sometimes breed in the
rainy season; also, individuals sometimes breed in the short dry season
(summer canicula) in July and August.
At several localities species have been found breeding at different
times of the year: _S. baudini_ in March and July at Chinaja, Guatemala;
_S. phaeota_ in April and August at Palmar Sur, Costa Rica; _S. puma_ in
February and July at Puerto Viejo, Costa Rica; and _S. sila_ in
February, April, and August at El Volcan, Panama. These observations
indicate only that the population breeds at more than one time in the
year, but do not provide any evidence on the breeding cycles of the
individual frogs. This is one important aspect of the natural history of
_Smilisca_ for which we lack data.
_Breeding Sites_
All members of the genus _Smilisca_ presumably deposit their eggs in
water.
_Smilisca baudini_ usually breeds in temporary rain pools; often these
are nothing more than shallow, muddy puddles. In other instances the
sites are extensive ditches or large flooded areas (Pl. 8, Fig. 1). This
species is an opportunistic breeder, and males gather at any of a wide
variety of suitable breeding sites that are formed by torrential rains
in the early part of the rainy season. _Smilisca baudini_ nearly always
breeds in open pools having bare earthen edges. Frequently congregations
of _S. baudini_ are found at such small pools, but are absent from
nearby large ponds surrounded by vegetation.
Little is known of the breeding habits of _S. cyanosticta_, which
inhabits humid forests on foothills and lowlands. Apparently its
breeding sites are not unlike those of _S. phaeota_, which usually are
pools surrounded by vegetation (Pl. 8, Fig. 2), although sometimes males
of _S. cyanosticta_ call from open muddy puddles. In uplands, where
standing water is uncommon, this species breeds in quiet pools in
streams.
_Smilisca puma_ breeds in grass-choked ponds and marshes, where the
males call from bases of dense clumps of grass in the water (Pl. 9, Fig.
1).
_Smilisca sila_ and _S. sordida_ differ noticeably from other species in
the genus by breeding exclusively in streams, where males usually call
from rocks or gravel bars in or at the edges of streams (Pl. 9, Fig. 2);
sometimes individuals perch on bushes overhanging streams. In the
streams, or parts of streams, utilized by these frogs the water is
clear, shallow, and has a slow gradient; occasional males have been
found calling along cascading mountain streams.
Breeding choruses composed of ten or more species of frogs are not
uncommon in Middle America, but _Smilisca_ usually breeds alone or with
one or two other species and at the most five others. This tendency
towards solitary breeding possibly is the result of selection of
breeding sites that are unsuitable to many other species of frogs.
Nevertheless, many other species of frogs have been found at the
breeding sites with the various species of _Smilisca_; these breeding
associates (Table 7) are most numerous for _S. baudini_, which has a
broad geographic range, including a variety of habitats.
_Breeding Behavior_
_Calling sites._--All species of _Smilisca_ usually call from the
ground, including rocks and gravel bars; some individuals sit in shallow
water near the edge of the pool or stream. Sometimes males of _S.
baudini_, _sila_, and _sordida_ call from low bushes or trees near the
breeding site. One _S. baudini_ was observed calling while it was
floating on the surface of a pond. _Smilisca cyanosticta_, _phaeota_,
and _puma_ call from secluded places at the edge of the water or in the
water, whereas _S. baudini_, _sila_ and _sordida_ call from open
situations.
Table 7.--Breeding Associates of the Various Species of Smilisca.
==============================+========+============+========+=====+=====+========
Associate |_S. |_S. |_S. |_S. |_S. |_S.
|baudini_|cyanosticta_|phaeota_|puma_|sila_|sordida_
------------------------------+--------+------------+--------+-----+-----+--------
_Rhinophrynus dorsalis_ | X | - | - | - | - | -
_Leptodactylus bolivianus_ | - | - | X | - | - | -
_Leptodactylus labialis_ | X | - | X | - | - | -
_Leptodactylus melanonotus_ | X | - | X | X | X | -
_Leptodactylus occidentalis_ | X | - | - | - | - | -
_Leptodactylus quadrivittatus_| - | - | X | - | - | -
_Leptodactylus pentadactylus_ | - | - | X | X | - | X
_Engystomops pustulosus_ | X | - | X | - | - | -
_Bufo canaliferus_ | X | - | - | - | - | -
_Bufo cavifrons_ | - | X | - | - | - | -
_Bufo coccifer_ | X | - | - | - | - | -
_Bufo coniferus_ | - | - | X | - | - | -
_Bufo cristatus_ | - | X | - | - | - | -
_Bufo gemmifer_ | X | - | - | - | - | -
_Bufo haematiticus_ | - | - | 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_
==============================+========+============+========+=====+=====+========
Associate |_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_
==============================+========+============+========+=====+=====+========
Associate |_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 spaced 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 establishing 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 spacing 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.