lower, broadly V-shaped, beak is slender in _S. puma_, rather robust in
_S. baudini_ and _sila_, and moderately heavy in the other species. The
lateral processes of the upper beak are shortest in _S. puma_ and
longest in _S. baudini_ and _sordida_. In the latter the inner margin of
the upper beak and lateral process have the form of a shallow S, whereas
in the other species the inner margin of the upper beak forms a
continuous arch with the lateral processes (Fig. 15).
[Illustration: FIG. 13. Tadpoles of _Smilisca phaeota_: (A) Stage 21
(KU 68479) x 14; (B) Stage 25 (KU 68480) x 5; (C) Stage 30 (KU
68482) x 4; (D) Stage 40 (KU 68483) x 3.]
_Coloration._--The tadpoles of _Smilisca_ lack the bright colors or bold
markings characteristic of some hylid tadpoles; even so, the subdued
colors and arrangement of pigments provide some distinctive markings by
which the species can be distinguished from one another. The species
comprising the _baudini_ group (_S. baudini_, _cyanosticta_, and
_phaeota_) are alike in having the body brown or grayish brown dorsally
and transparent with scattered brown pigment ventrally. A cream-colored,
crescent-shaped mark is present on the posterior edge of the body; this
mark is usually most noticeable in _S. baudini_ and least so in _S.
cyanosticta_. Other differences in coloration in members of the
_baudini_ group are relative and subtle. _Smilisca phaeota_ usually is
more pallid than _baudini_, and _cyanosticta_ usually is darker than
_baudini_; both species have larger dark markings on the tail than does
_S. phaeota_. _Smilisca baudini_ has a dark streak on the middle of the
anterior one-fourth of the tail (Figs. 11-13).
_Smilisca puma_ is distinctive in having a grayish brown body and dark
gray reticulations on the tail. _Smilisca sila_ and _sordida_ are
distinctive in having pairs (sometimes interconnected) of dark marks on
the dorsal surfaces of the caudal musculature, and in dorsal view the
tail appears to be marked with dark and pale creamy tan transverse bars.
These dark marks, as well as the small flecks on the tail, are brown in
_S. sila_ and red in _sordida_. _Smilisca sila_ has dark brown flecks on
the dorsal surface of the body and small white flecks laterally; these
markings are absent in _S. sordida_ (Fig. 14).
Descriptions of the coloration of living tadpoles are given in the
accounts of the species.
[Illustration: FIG. 14. Tadpoles of _Smilisca_; (A) _S. puma_,
Stage 30 (KU 91807); (B) _S. sila_, Stage 25 (KU 80260);
_S. sordida_, Stage 30 (KU 68475). All x 3.5.]
_Growth and Development_
Information on the growth and development of Middle American hylids is
scanty. Adequate descriptions have been published for _Phyllomedusa
annae_ (Duellman, 1963b), _Phrynohyas venulosa_ (Zweifel, 1964), and
_Triprion petasatus_ (Duellman and Klaas, 1964). Material is available
for adequate descriptions of the developmental stages of four species of
_Smilisca_ (Tables 9-12, Figs. 11-13). Because none of the tadpoles was
raised from hatching to metamorphosis, the rate of growth and duration
of the larval stages are unknown.
[Illustration: FIG. 15. Mouthparts of tadpoles of _Smilisca_;
(A) _S. baudini_ (KU 60018); (B) _S. puma_ (KU 91807);
(C) _S. cyanosticta_ (KU 87625); (D) _S. sila_ (KU 80620);
(E) _S. phaeota_ (KU 68482); (F) _S. sordida_ (KU 68475).
All x17.]
Table 9.--Growth and Development of Tadpoles of Smilisca baudini.
(Means Are Given in Parentheses After the Observed Ranges.)
====================================================================
Stage | N | Total length | Body length | Tail length
--------------------------------------------------------------------
21 |10 | 5.1-5.4 (5.22) | 2.6-2.7 (2.54) | 2.5-2.7 (2.58)
24 |10 | 6.0-6.5 (6.20) | 2.3-2.6 (2.45) | 3.5-3.9 (3.69)
25 |10 | 7.2-8.3 (7.78) | 3.0-3.3 (3.14) | 4.2-5.0 (4.64)
27 |10 | 18.5-21.5 (20.22) | 8.0-9.0 (8.38) |10.4-13.0 (11.84)
29 |10 | 21.5-24.5 (22.60) | 8.5-10.0 (9.25) |12.5-14.5 (13.35)
37 | 3 | 28.5-31.0 (30.00) |11.0-12.5 (11.67) |17.5-19.0 (18.00)
38 |10 | 35.0-37.5 (35.50) |12.0-13.5 (12.80) |21.5-24.0 (22.70)
40 | 2 | 34.0-37.0 (35.50) |12.5-13.5 (13.00) |21.5-23.5 (22.50)
41 |10 | 34.0-37.0 (35.50) |12.5-13.5 (13.00) |21.5-23.5 (22.50)
42 | 3 | 24.0-30.0 (27.00) |12.5-13.0 (12.67) |11.5-17.0 (14.33)
45 | 6 | 14.0-24.0 (17.58) |12.5-14.0 (13.37) | 1.5-10.0 (4.17)
46 |23 | ---- |12.0-15.5 (13.34) | ----
--------------------------------------------------------------------
Table 10.--Growth and Development of Tadpoles of Smilisca
cyanosticta. (Means Are Given in Parentheses After the
Observed Ranges.)
======================================================================
Stage | N | Total length | Body length | Tail length
----------------------------------------------------------------------
21 | 10| 5.8-6.5 (6.28) | 2.8-3.1 (3.00) | 3.0-3.5 (3.28)
25 | 10| 7.9-9.2 (8.44) | 2.7-3.2 (2.96) | 4.8-6.0 (5.48)
30 | 7| 22.5-25.0 (23.50) | 8.5-9.5 (9.00) |14.0-15.5 (14.57)
36 | 10| 27.0-30.0 (28.75) | 9.5-11.5 (10.80) |17.0-18.5 (17.95)
42 | 2| 26.0-27.0 (26.50) | 10.00 |16.0-17.0 (16.50)
46 | 2| -- | 14.00 | --
----------------------------------------------------------------------
Hatchlings of three species (_S. baudini_, _cyanosticta_, and _phaeota_)
are available. These larvae have non-functional eyes and large oral
suckers. By the time the larvae have developed to stage 21, external
gills are present, the caudal musculature and caudal fin have been
differentiated, and the head is distinguishable from the body. In stage
21 oral suckers and a large amount of yolk are still present.
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.
[Illustration: FIG. 16. Relative rate of growth in tadpoles of
_Smilisca phaeota_ as correlated with developmental stages.
Formulas for the limb bud refer to its length (L) in relation to
basal diameter (D).]
_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_.
_baudini_
\ _cyanosticta_
\ /
+ _phaeota_ _sordida_
\ / /
+ puma_ /
\ \/ _sila_
\ /_____/
\ /
\ /
\ /
|
|
Prototype
[Illustration: FIG. 17. Hypothesized phylogenetic relationships
of the species of _Smilisca_.]
Certain aspects of this proposed phylogeny warrant further comment.
Features such as the deposition of additional bone that roofs the skull
or that forms lateral projections from the frontoparietals, like those
in _S. baudini_ and _phaeota_, are minor alterations of dermal elements
and not basic modifications of the architecture of the skull.
Consequently, we hypothesize the independent development of these dermal
changes in _S. baudini_ and _phaeota_. Similar kinds of dermal
modifications have evolved independently in many diverse groups of
frogs.
Likewise, we propose the parallel development of stream-adapted tadpoles
in _S. sordida_ and _sila_; in both cases the tadpoles adapted to
changing environmental conditions (see following section on evolutionary
history). Tadpoles of _S. sordida_ already had two rows of labial
papillae before entering the streams; subsequently the tadpoles
developed complete rows of papillae, ventral mouths and long tails
having low fins. Possibly the tadpoles of _S. sila_ had two rows of
labial papillae prior to their adapting to stream conditions; in the
process of adapting they developed ventral mouths and long tails having
low fins. Similar modifications in tadpoles have occurred in many
diverse groups of Middle American hylids, such as _Plectrohyla_,
_Ptychohyla_, the _Hyla uranochroa_ group, and the _Hyla taeniopus_
group.
Our lack of concern about coloration is due to the fact that, with the
exception of the blue spots on the flanks and posterior surfaces of the
thighs in some species, the coloration of _Smilisca_, consisting of a
pattern of irregular dark marks on a paler dorsum and dark transverse
bars on the limbs, is not much different from that of many other
Neotropical hylids. Blue is a structural color, rare among Amphibia,
which is achieved by the absence of lipophores above the guanophores.
Thus, the incident light rays at the blue end of the spectrum are
reflected by the guanophores without interference by an overlying yellow
lipophore screen. According to Noble (1931), lipophores are capable of
amoeboid movement that permits shifts in their positions, between or
beneath the guanophores. We do not know whether this behavior of
lipophores is widespread and is effected in response to environmental
changes, or whether it is a genetically controlled attribute that is
restricted in appearance. If the latter is the case we must assume that
the prototype of _Smilisca_ possessed such an attribute which was lost
in _S. baudini_, _phaeota_, and _puma_. The development of blue spots is
not constant in _S. sordida_ and _S. sila_; in _S. cyanosticta_ the
spots range in color from blue to pale green.
The coloration of the tadpoles is not distinctive, except for the
presence of dorsal blotches on the tails of _S. sila_ and _sordida_.
However, the similarity in pattern cannot be interpreted as indicating
close relationships because nearly identical patterns are present in
_Hyla legleri_ and some species of _Prostherapis_. This disruptive
coloration seems to be directly associated with the pebble-bottom,
stream-inhabiting tadpoles.
In the _baudini_ group, _S. phaeota_ and _cyanosticta_ are allopatric,
whereas _S. baudini_ occurs sympatrically with both of those species.
The call of _S. baudini_ differs notably from the calls of _S. phaeota_
and _cyanosticta_, which are more nearly alike. Although in the
phylogenetic scheme proposed here _S. sila_ is considered to be more
distantly related to _S. puma_ than is _S. sordida_, the calls of _S.
sila_ and _puma_ more closely resemble one another than either resembles
that of _S. sordida_. _Smilisca sila_ and _puma_ are allopatric, whereas
_S. sordida_ is broadly sympatric with both of those species. We assume
that in their respective phyletic lines the differentiation of both _S.
baudini_ and _sordida_ was the result of genetic changes in
geographically isolated populations. Subsequently, each species
dispersed into areas inhabited by other members of their respective
groups. Selection for differences in the breeding calls helped to
reinforce other differences in the populations and thereby aided in
maintaining specificity.
Evolutionary History
With respect to temporal and spatial aspects of evolution in _Smilisca_,
we have tried to correlate the phylogenetic evidence on _Smilisca_ with
the geologic data on Middle America presented by Lloyd (1963), Vinson
and Brineman (1963), Guzman and Cserna (1963), Maldonado-Koerdell
(1964), and Whitmore and Stewart (1965). Likewise, we have borne in mind
the evidence for, and ideas about, the evolution of the Middle American
herpetofauna given by Dunn (1931b), Schmidt (1943), Stuart (1950, 1964)
Duellman (1958, MS), and Savage (MS).
According to Stuart's (1950) historical arrangement of the herpetofauna,
_Smilisca_ is a member of the Autochthonous Middle American Faunal
Element, and according to Savage's (MS) arrangement the genus belongs to
the Middle American Element, a fauna which was derived from a
generalized tropical American unit that was isolated in tropical North
America by the inundation of the Isthmian Link in early Tertiary, that
developed _in situ_ in tropical North America, and that was restricted
to Middle America by climatic change in the late Cenozoic.
Savage (MS) relied on the paleogeographic maps of Lloyd (1963) to
hypothesize the extent and centers of differentiation of the Middle
American Faunal Element. According to Lloyd's concept, Middle America in
the Miocene consisted of a broad peninsula extending southeastward to
about central Nicaragua, separated from the Panamanian Spur of
continental South America by shallow seas. A large island, the Talamanca
Range, and remnants of the Guanarivas Ridge formed an archipelago in the
shallow sea. The recent discovery of remains of mammals having definite
North American affinities in the Miocene of the Canal Zone (Whitmore and
Stewart, 1965) provides substantial evidence that at least a peninsula
was continuous southeastward from Nuclear Central America to the area of
the present Canal Zone in early mid-Miocene time. South America was
isolated from Central America by the Bolivar Trough until late
mid-Pliocene.
Thus, in the mid-Tertiary the broad peninsula of Nuclear Central
America, which consisted of low and moderately uplifted regions having a
tropical mesic climate, provided the site for the evolution of
_Smilisca_. It is not possible to determine when the genus evolved, but
to explain the differentiation of the species it is unnecessary to have
the ancestral _Smilisca_ present prior to the Miocene.