Chapter IV: Part 4

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=====================+=====+=====+=====+=====+=====+=====+====
Bone |Stage|Stage|12.6 |13.9 |32.0 |27.0 |20.1
| 40 | 44 | mm. | mm. | mm. | mm. | mm.
---------------------+-----+-----+-----+-----+-----+-----+----
Frontoparietal | X | X | X | X | X | X | X
Parasphenoid | X | X | X | X | X | X | X
Septomaxillaries | X | X | X | X | X | X | X
Exoccipitals | X | X | X | X | X | X | X
Squamosals | -- | X | X | X | X | X | X
Premaxillaries | -- | X | X | X | X | X | X
Maxillaries | -- | X | X | X | X | X | X
Nasals | -- | -- | X | X | X | X | X
Pterygoids | -- | -- | X | X | X | X | X
Vomers | -- | -- | -- | X | X | X | X
Palatines | -- | -- | -- | X | X | X | X
Quadratojugals | -- | -- | -- | X | X | X | X
Ethmoid | -- | -- | -- | -- | X | X | X
Columellas | -- | -- | -- | -- | X | X | X
Supraorbital Flanges | -- | -- | -- | -- | -- | X | X
Prooetics | -- | -- | -- | -- | -- | -- | X
Vomerine Teeth | -- | -- | 1/1 | 4/3 | 5/5 | 3/3 | 5/4
Maxillary Teeth | -- | 0/7 | 3/5 | 6/5 |30/31|30/26|37/36
Premaxillary Teeth | -- | 2/4 | 3/3 | 5/5 | 7/6 | 8/6 | 8/7
---------------------+-----+-----+-----+-----+-----+-----+----

The dentigerous bones are among the most rapidly developed, although not the first to appear. They are present in developmental stage 44 before metamorphosis is completed. The maxillaries bear a few teeth anteriorly and are ossified posteriorly to a point one-third of the distance from the anterior to the posterior edge of the orbit. Ossification lengthens the posterior termini of the maxillaries to the posterior edge of the orbit. In front of the anterior margin of the orbit, bone is proliferated dorsal to the main axes of the maxillaries and forms moderate dorsal maxillary flanges. The premaxillaries appear simultaneously with the maxillaries. Initially they are widely separated medially from each other, and laterally from the developing maxillaries; each bears two or three teeth, large dorsally blunt alary processes, and small palatine processes. The median and lateral edges of the prenasal processes lengthen heterochronously, causing the median edges to be longest and to lie slightly dorsal to the level of the septomaxillaries. After the maxillaries and premaxillaries develop, the vomers appear as small horizontal ossifications anterior to the parasphenoid. Ossification begins in the lateral flanges, then in the prevomerine processes, and lastly in the posterior dentigerous parts of the bones; the prevomerine processes are the last parts of the vomers to ossify completely.

Initially the frontoparietals are present as thin rods of ossification dorsomedial to the orbits; the frontoparietals extend from the anterior to the posterior end of the orbit by developmental stage 44. The anterior ends of the bones remain thin and pointed; ossification progresses medially from the midpoint of the length of the orbit and posteriorly to the level of the exoccipital; a median center of ossification joins the frontoparietals posteriorly, thereby forming the posterior border of the frontoparietal fontanelle. The supraorbital flanges of the frontoparietals do not appear until all other cranial bones are ossified, or nearly so. The most rapid ossification begins laterally at the posterior edge of the orbit and decreases anteriorly over the posterior half of the orbit. This differential rate of proliferation of bone results in the pattern of development of the supraorbital flanges shown in figure 7. The nasals appear as thin slivers of bone half way between the anterior ends of the frontoparietals and the end of the snout. As ossification proceeds the nasals assume a triangular shape in dorsal view. The anterior ends are pointed; the lateral margins are parallel to the maxillaries. The posteromedial points do not reach the lateral margins of the ethmoid, and the maxillary processes extend about three-fourths the distance from the bodies of the nasals to the maxillaries. Following the union of the frontoparietals posteriorly, the nasals widen anteriorly and are narrower at the midpoints of their long axes than anteriorly or posteriorly. With further ossification the maxillary processes extend to the maxillaries and form complete bony anterior margins to the orbits; the mid-parts of the nasals widen (Pl. 1B).

The parasphenoid is the first of the palatal bones to appear. At metamorphosis the bone is well developed; the anterior tip is situated just in front of the anterior edge of the orbit, and posteriorly the lateral processes extend laterally beyond the ossified parts of the auditory region. The pterygoids do not appear until metamorphosis, when ossification is evident in only the mid-parts of the posterolateral arms. Ossification follows in the mid-parts of the anterolateral arms and occurs last in the pterygoid pedicles. The palatines do not appear until all three arms of the pterygoids are at least partly ossified. Ossification proceeds rapidly from the maxillaries medially to the unossified ethmoid, which is the last of the cranial bones to appear. Initially it is extremely shallow; dorsally it is widely separated from the nasals, and ventrally the posterior margin meets the anterior point of the parasphenoid. In dorsal view, ossification proceeds anteriorly between the nasals and posteriorly, ventral to the frontoparietals; ventrally, ossification proceeds posteriorly dorsal to the parasphenoid.

The ventral arms of the squamosal and the supraoccipital region of the exoccipital are the first occipital bones to appear. Ossification follows in the regions of the semicircular canals and occipital condyles. The dorsal end of the ventral arm of the squamosal and the posterior arm of the squamosal ossify as a unit at the same time the quadratojugal appears. Shortly thereafter the anterior arm of the squamosal ossifies, the distal part of the columella appears, and the anterior and lateral parts of the auditory region ossify.

The angular and dentary of the lower jaw appear concurrently with the dentigerous bones. Initially, the angular is short and broad; the articular surface is absent, and the anterior end is slightly overlapped by the dentary. The mentomecklians do not ossify until approximately the same time that the quadratojugal appears in the upper jaw.

_Comparative Osteology_

The genus _Smilisca_ is characterized by the following combination of cranial osteological characters: (1) A large amount of bone is involved in the skull and a minimal amount of cartilage and/or secondarily ossified cartilage; co-ossification is absent. (2) The skulls are uniformly broad with angular lateral margins, and truncate anteriorly. (3) An internasal septum and quadratojugals are present. (4) A well-developed squamosal minimally extends one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally is separated from the maxillary by a suture. (5) The ethmoid is large; the distance between the anterior end of the ethmoid and the anterior edge of the premaxillary varies between 15 and 20 per cent of the total length of the skull.

On the basis of cranial osteology two species-groups can be recognized within the genus _Smilisca_. The _sordida_ group, comprising _S. sordida_ and _puma_, is characterized by a broad skull in which the lateral margins of the maxillaries are relatively straight anterior to the orbit. The moderate-sized nasals are rounded anteriorly, and bear relatively short, sometimes blunt, maxillary processes. The long axes of the nasals are not parallel to the maxillaries. The ethmoid is proportionately small in the _sordida_ group. The bony part of the ethmoid terminates near the anterior edge of the orbits and does not extend anteriorly between the nasals; the entire anterior margin of the ethmoid is separated from the nasals by cartilage. The squamosals are generally small. They are narrow in dorsal view, and minimally extend one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally, two-thirds the distance. The tegmen tympani are relatively small (Fig. 8).

In contrast to the tendency for reduction of cranial parts in the _sordida_ group, the _baudini_ group, constituted by _S. cyanosticta_, _phaeota_, and _baudini_, is characterized by more ossification of the cranial elements. The skull is broad; the lateral margins are less angular and are gently curved, rather than straight as in the _sordida_ group. The nasals tend to be larger with the long axes parallel to the maxillary. Anteriorly the nasals are pointed, and posteriorly they bear long, delicate palatine processes extending to the maxillary. The ethmoid is fully ossified, extends anteriorly between the nasals, and laterally is separated by a suture from the nasals if the latter are fully ossified. The squamosals are large, and wide in dorsal view. They minimally extend one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally are sutured to the maxillary. The tegmen tympani are massive.

_Smilisca sila_ is intermediate between the two species-groups described. The skull is broad; the lateral margins are gently curved, and have a pronounced angularity just anterior to the palatines which results in a broad, truncate snout. The nasals are moderate in size; because of the anterior angularity of the lateral margins, the long axes of the nasals lie parallel to the maxillary. The nasals are only slightly pointed anteriorly, and posteriorly they bear short, blunt palatine processes and medial processes in contact with the lateral corners of the ethmoid. The ethmoid is fully ossified, but does not extend anteriorly between the nasals. The squamosals are moderate in size and extend one-fourth the distance from the dorsal end of the quadrate to the maxillary. The tegmen tympani are relatively large, but proportionately short.

The cranial characters utilized in the analysis of species groups (general shape, nature of the nasals, ethmoid, squamosals, and tegmen tympani), together with other characters, such as the relative height and shape of the prenasal processes, the extent of the internasal septum, and the nature of the vomers, frontoparietals, maxillaries and pterygoids are useful in distinguishing the various species (Table 4, Fig. 8), as well as in establishing relationships within the species-groups.

Within the _sordida_ group, _S. sordida_ and _S. puma_ can be distinguished by the following characters: The bony part of the ethmoid terminates posterior to the anterior edge of the orbit and is thus widely separated from the nasals by cartilage in _S. puma_. In _S. sordida_ the bony part of the ethmoid always terminates at a level equal to, or slightly in front of the anterior edge of the orbit; therefore, less cartilage exists between the ethmoid and nasals in _S. sordida_ than in _S. puma_. The width of the premaxillary comprises about 30 per cent of the width of the skull in _S. sordida_ and 20 per cent in _S. puma_. The proportion of the length of the skull anterior to the bony part of the ethmoid in _S. sordida_ is approximately 21 per cent, as compared with about 29 per cent in _S. puma_. The prenasal processes are convex in _S. sordida_ and straight in _S. puma_.

The marked ontogenetic variation in _S. sordida_ is considered in more detail in the account of that species, but it is pertinent to the present discussion to note that with respect to some features of the skull some young breeding specimens of _S. sordida_ are intermediate in appearance between large females of _S. sordida_ and adults of _S. puma_. In some breeding males (usually the smaller individuals) of _S. sordida_ the bony part of the ethmoid terminates at the anterior edge of the orbit and is widely separated from the nasals by cartilage. In small individuals _S. sordida_, especially in males, and in adults of _S. puma_ the tegmen tympani are relatively short, whereas in adult females of _S. sordida_ these elements are long and slender. In the smaller specimens of _S. sordida_ and in _S. puma_ the squamosal is small; it extends only about one-fourth of the distance to the maxillary in the smaller _S. sordida_ and about one-half the distance in _S. puma_. The more massive squamosal in large adult females of _S. sordida_ extends at least two-thirds of the distance to the maxillary.

Table 4.--Comparative Cranial Osteology of Smilisca.

Within the _baudini_ group, the skull of _S. cyanosticta_ is the most generalized of the three species; the cranial characters are intermediate between _S. phaeota_ and _S. baudini_. The lateral margins of the skull in _S. cyanosticta_ are gently curved, and have an angularity anterior to the palatine-maxillary suture; the anterior margins are less angular in _S. phaeota_, which has a broader snout. Posteriorly in _S. baudini_ the margins are slightly curved medially, and the greatest width of the skull is between the quadratojugal-maxillary sutures on either side of the skull. The frontoparietals of _S. cyanosticta_ bear slightly irregular lateral margins and a large fontanelle. There is a tendency for obliteration of the fontanelle with increasing age in both _S. baudini_ and _S. cyanosticta_; the lateral margins of the frontoparietals bear large supraorbital flanges in both of these species. In _S. phaeota_ the flanges are most prominent; they extend posterolaterally with straight margins along two-thirds of the length of the orbit and terminate in rather blunt points. The broad interorbital flanges result in a relatively broad external interorbital distance. In _S. baudini_ the flanges are curved posterolaterally around the orbit and terminate in sharp, thin points. The tegmen tympani of all three species are massive. In _S. cyanosticta_ the prooetics slope posteriorly, whereas they slope anteriorly in _S. baudini_ and _S. phaeota_.

The skulls of _S. cyanosticta_ and _S. baudini_ are alike in certain respects. The squamosals of both species are large and connected to the maxillary by a bony connection; the squamosals of _S. phaeota_ are large, but extend only two-thirds of the distance from the dorsal end of the quadrate to the maxillary. In _S. baudini_ and _S. cyanosticta_ the nasals are separated throughout their lengths from the ethmoid, whereas the nasals of _S. phaeota_ are separated from the ethmoid by cartilage. The latter separation is due to an incomplete ossification of the nasals in _S. phaeota_. The bony part of each nasal is constricted in the middle of the long axis of the bone, and the nasals are widest anteriorly; posteriorly each nasal bears a medial process, which is narrowly separated from the lateral edge of the ethmoid.

Table 5.--Variation in the Number of Teeth in the Species of
Smilisca. (All Are Males; N = Number of Jaws, or Twice the Number
of Individuals; Means Are Given in Parentheses After the Observed
Ranges.)

=================+====+==============+==============+===========
Species | N | Maxillary | Premaxillary | Vomerine
-----------------+----+--------------+--------------+-----------
_S. baudini_ | 20 | 49-65 (56.0) | 9-16 (13.6) | 5-9 (7.2)
_S. cyanosticta_ | 8 | 50-64 (57.9) | 10-12 (10.8) | 4-11 (7.1)
_S. phaeota_ | 20 | 50-68 (58.1) | 10-15 (12.1) | 5-9 (7.3)
_S. puma_ | 6 | 60-67 (63.6) | 11-13 (12.0) | 4-7 (5.3)
_S. sila_ | 8 | 48-60 (52.9) | 10-14 (11.3) | 5-7 (5.7)
_S. sordida_ | 12 | 39-55 (44.2) | 7-11 (9.3) | 4-6 (5.2)
-----------------+----+--------------+--------------+-----------

The teeth of all species of _Smilisca_ are spatulate and bifid. The numbers of maxillary, premaxillary, and vomerine teeth are summarized in Table 5. Smaller and presumably younger specimens of all species of _Smilisca_ have fewer teeth than do larger specimens of the same species. This correlation between size and number of teeth does not exist as an interspecific trend within the genus; for example, the smallest species in the genus, _S. puma_, has the highest number of maxillary teeth. In small specimens of a given species wide gaps are present between the maxillary teeth posteriorly; in large specimens the gaps are filled by teeth, beginning anteriorly and progressing posteriorly, until the maxillary dentition is continuous.

Musculature

No extensive study of the muscular system was undertaken, but certain muscles know to be of taxonomic importance were studied.

_Jaw Musculature._--Starrett (1960) pointed out the unique jaw musculature in _Smilisca_. In this genus M. depressor mandibulae consists of two parts, one arising from the dorsal fascia and one from the posterior arm of the squamosal. Two muscles arise from the anterior arm of the squamosal and insert on the lateral face of the mandible. Of these muscles, M. adductor mandibulae posterior subexternus lies medial to the mandibular branch of the trigeminal nerve; the other, M. adductor mandibulae externus superficialis, lies lateral to the same nerve (Fig. 9). In most other hylids the latter muscle is absent. No significant variation in the position of the muscles was noted in the various species of _Smilisca_, though M. adductor mandibulae originate somewhat more anteriorly in _S. baudini_ and _S. cyanosticta_ than in the other members of the genus, all of which have a shorter anterior arm of the squamosal that does not reach the maxillary. The two separate parts of M. depressor mandibulae are not so widely separated in members of the _sordida_ group as in the _baudini_ group.

_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.

_Sex 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 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.

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Neotropical Hylid Frogs, Genus SmiliscaChapter IV: Part 4

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