Part 18

The developmental data on the four species show no significant variations; consequently, we will describe the development of only one species, Smilisca phaeota (Table 11, Figs. 13 and 16).

Stage 21.--Bulging cream-colored yolk mass, transparent cornea, and moderately long, unbranched filamentous gills, and oral suckers present; mouth having irregular papillae on lower lip; teeth and beaks absent; caudal myomeres distinct; pigmentation uniform over body and caudal musculature; caudal fin transparent with scattered small flecks.

Stage 25.--Operculum complete; gills absent; sinistral spiracle apparently functional; cloacal tail-piece, nasal capsules, and external nares present; gut partly formed; mouth bordered by single row of papillae, except medially; small papillae present in lateral fold of lips; two upper and three lower tooth-rows present, but not fully developed; beaks apparently fully developed; depth of dorsal and ventral fins less than depth of caudal musculature: tip of tail upturned; pigment on body most dense on dorsum and sides; faint, nearly pigmentless crescent-shaped mark on posterior edge of body; concentrations of pigment forming small spots on tail.

Stage 28.--Mouthparts complete; limb bud about half as long as thick; other structural features and coloration closely resemble those in stage 25.

Stage 30.--Limb bud approximately twice as long as thick; body as deep as wide; dorsal fin deepest just posterior to body; ventral fin deeper than caudal musculature; tail sharply upturned distally; anal tube dextral; brown pigment sparse on flanks.

Table 11.--Growth and Development of Tadpoles of Smilisca phaeota. (Means Are Given in Parentheses After the Observed Ranges.)

==================================================================== Stage | N | Total length | Body length | Tail length -------------------------------------------------------------------- 15 | 10| -- | 1.9-2.1 (1.97) | -- 16 | 8| -- | 2.0-2.2 (2.07) | -- 18 | 4| -- | 2.2-2.6 (2.31) | -- 21 | 3| 7.9-8.6 (8.21) | 4.1-4.5 (4.31) | 3.8-4.1 (3.92) 25 | 10| 8.7-10.6 (9.69) | 4.5-4.8 (4.64) | 4.3-6.0 (5.05) 26 | 11| 12.3-16.1 (14.01) | 4.2-6.3 (5.60) | 6.7-9.8 (8.41) 27 | 10| 13.0-15.7 (14.28) | 4.9-6.2 (5.40) | 7.7-10.5 (8.88) 28 | 13| 13.9-20.9 (15.62) | 5.2-8.3 (5.75) | 8.5-12.6 (9.85) 29 | 8| 17.8-22.3 (19.79) | 6.3-8.4 (7.19) | 11.5-14.0 (12.60) 30 | 9| 20.3-24.8 (22.85) | 8.1-10.5 (9.32) | 10.5-15.5 (13.53) 31 | 5| 24.1-28.5 (26.61) | 9.4-11.2 (10.59) | 14.7-17.3 (16.02) 34 | 5| 24.8-29.4 (27.31) | 9.2-11.6 (10.73) | 15.6-18.5 (16.80) 36 | 3| 30.0-30.1 (30.07) |10.1-12.2 (11.15) | 18.9-20.0 (19.44) 37 | 4| 28.9-34.1 (31.75) |11.5-12.4 (11.88) | 17.4-22.5 (19.88) 38 | 1| 28.98 |12.88 | 16.10 39 | 2| 35.6-36.9 (36.25) |14.00 | 21.6-22.9 (22.25) 40 | 2| 32.3-39.8 (36.05) |14.00 | 18.3-21.8 (20.05) 43 | 2| 21.5-23.0 (22.25) |14.2-14.8 (14.45) | 6.8-8.8 (7.80) 44 | 4| -- |14.5-15.6 (15.08) | -- 46 | 11| -- |12.7-16.7 (14.26) | -- --------------------------------------------------------------------

Table 12.--Growth and Development of Tadpoles of Smilisca sordida. (Means Are Given in Parentheses After the Observed Ranges.)

=======+===+==================+==================+================= Stage | N | Total length | Body length | Tail length -------+---+------------------+------------------+----------------- 25 | 6 | 25.5-28.0 (26.1) | 9.0-9.5 (9.3) | 16.2-18.5 (16.7) 33 | 2 | 28.5-30.0 (29.3) | 10.2-10.5 (10.4) | 18.0-19.8 (18.9) 36 | 8 | 29.5-34.5 (32.3) | 10.2-11.7 (10.8) | 19.3-23.0 (21.5) 37 | 7 | 31.6-37.5 (34.6) | 11.0-12.5 (11.5) | 21.6-25.0 (23.2) 41 | 3 | 33.0-37.2 (35.2) | 11.6-12.2 (11.9) | 21.4-25.2 (23.2) 43 | 1 | ---- | 12.4 | ---- 46 | 9 | ---- | 13.1-15.7 (14.9) | ---- -------+---+------------------+------------------+-----------------

Stages 34, 36, 37, and 38.--Stage 34, foot paddle-shaped with four toe buds; stage 36, five toe buds; stages 37 and 38, lengthening of toes. In all four stages, spiracle persistent, and pigmentation resembling that of early stages.

Stage 39.--Metatarsal tubercle present; greatest total length (36.9 mm.) attained.

Stage 40.--Subarticular tubercles prominent; skin over forelimbs transparent; cloacal tail-piece and spiracle absent; outer tooth-rows degenerating; caudal fins shallower than in preceding stages; distal part of tail nearly straight; size of dark markings on tail decreased; pigment present on hind limb.

Stage 43.--Forelimbs erupted; larval mouthparts absent; corner of mouth between nostril and eye; transverse bands present on hind limbs; tail greatly reduced (about 8 mm. in length).

Stage 44.--Sacral hump barely noticeable; tail reduced to a stub; corner of mouth at level of pupil of eye; dorsal surfaces pale olive-green; venter white.

Changes proceed in a definite pattern during the growth and development of tadpoles. Larval teeth are absent in hatchlings; the inner tooth-rows develop first, and the third lower row last. At metamorphosis the third lower row is the first to be lost. The tail increases gradually in length relative to the body. In stage 25 the tail is 52.1 per cent of the total length, and in stage 36, 64.6 per cent. In later stages the tail becomes relatively shorter through resorption. Duellman and Klaas (1964:320) noted a great size-variation in Triprion tadpoles in stage 25. No such variation is apparent in any stage of any of the species of Smilisca studied.

The growth and development of the other species of Smilisca do not differ significantly from that of S. phaeota. The tadpoles of S. sila and sordida from streams have relatively longer tails at hatching. For example, in tadpoles of S. sordida the average length of tail is 64.0 per cent of the body-length in stage 25, and in stage 37, 67.0 per cent.

Behavior

The tadpoles of S. baudini, cyanosticta, phaeota, and puma are pelagic inhabitants of shallow ponds. Early stages of S. baudini in which external gills are present have been observed to hang vertically with the gills spread out at the surface of the water, a behavior noted by Zweifel (1964:206) in tadpoles of Phrynohyas venulosa, which also develop in warm, standing water having a relatively low oxygen-tension. When disturbed the pelagic tadpoles usually dive and seek shelter amidst vegetation or in mud on the bottom. This behavior was observed in S. baudini, cyanosticta, and phaeota by day and at night. No tadpoles of S. puma were observed by day; those seen at night were near the surface of small water-filled depressions in a grassy marsh; they responded to light by taking refuge in the dense grass. Perhaps tadpoles of this species are negatively phototactic and remain hidden by day.

The stream-inhabiting tadpoles of S. sila and sordida live in clear pools in rocky streams, where they were observed to cling by their mouths to rocks in the stream and to seek shelter amidst pebbles or beneath rocks and leaves on the bottom. These tadpoles are not found in shallow riffles.

We have not found tadpoles of two species of Smilisca in the same body of water and therefore cannot offer observations on ecological relationships in sympatric situations.

PHYLOGENETIC RELATIONSHIPS

Identifiable hylid remains are known from the Miocene to the Recent, but these fossils are mostly fragmentary and provide little useful information regarding the phylogenetic relationships of living genera. Frogs of the genus Smilisca are generalized and show no striking adaptations, either in their structure or in their modes of life history.

Interspecific Relationships

In attempting to understand the relationships of the species of Smilisca we have emphasized osteological characters. The phylogeny suggested by these characters is supported by other lines of evidence, including external morphology, tadpoles, and breeding calls.

Our concept of the prototype of the genus Smilisca is a moderate-sized hylid having: (1) a well-developed frontoparietal fontanelle, (2) frontoparietal lacking lateral processes, (3) no bony squamosal-maxillary arch, (4) a fully ossified ethmoid, (5) paired subgular vocal sac, (6) moderately webbed fingers and toes, (7) relatively few supernumerary tubercles on the digits, (8) eggs deposited in clumps in ponds, (9) anteroventral mouth in tadpoles bordered by one row of labial papillae, but median part of upper lip bare, (10) tail relatively short and deep in tadpoles, and (11) a breeding call consisting of a series of like notes.

Two phyletic lines evolved from this prototype. The first of these was the stock that gave rise to the baudini group. The evolutionary changes that took place in this line included increase in size, development of a lateral curvature of the maxillary, and an increased amount of cranial ossification, especially in the dermal roofing bones. This phyletic line retained the larval characters and breeding call of the prototype. The second phyletic line gave rise to the sordida group and diverged from the prototype in the development of an angular maxillary and a breeding call consisting of a primary note followed by secondary notes. The frogs in this phyletic line retained the moderate size of the prototype and did not develop additional dermal bone. Our concept of the phylogenetic relationships is shown graphically in Figure 17.

Within the baudini group one stock retained separate nasals and did not develop a bony squamosal-maxillary arch, but broad lateral processes developed on the frontoparietals. The tadpoles remained unchanged from the primitive type. This stock evolved into S. phaeota. In the other stock the nasals became fully ossified and a bony squamosal-maxillary arch developed. One branch of this second stock retained tadpoles having only one row of labial papillae and did not develop lateral processes on the frontoparietals; this branch evolved into S. cyanosticta. The other branch diverged and gave rise to S. baudini by developing relatively shorter hind legs, large lateral processes on the frontoparietals, and tadpoles having two rows of labial papillae.

Within the sordida group the cranial features remained unchanged in one line, which gave rise to S. sila, whereas in a second line the nasals were reduced, and their long axes shifted with the result that they are not parallel to the maxillaries; the amount of ossification of the ethmoid was reduced, and the tadpoles developed two rows of labial papillae. In this second line one branch retained the pond-breeding habits and gave rise to S. puma, whereas a second branch became adapted to stream-breeding and gave rise to S. sordida.