Volume 18, No. 6, pp. 505-545, 7 figs., 4 pls.

Published December 2, 1969

UNIVERSITY OF KANSAS Lawrence, Kansas

PRINTED BY ROBERT R. (BOB) SANDERS, STATE PRINTER TOPEKA, KANSAS 1969

The Systematics of the Frogs of the _Hyla rubra_ Group in Middle America

BY

JUAN R. LEÓN

CONTENTS

PAGE

INTRODUCTION 508 Acknowledgments 508 Materials and Methods 509

THE HYLA RUBRA GROUP 509 Key to Species and Subspecies 510 Key to Known Tadpoles 511

ACCOUNTS OF SPECIES AND SUBSPECIES 511 _Hyla boulengeri_ (Cope) 511 _Hyla foliamorta_ Fouquette 520 _Hyla rubra_ Laurenti 524 _Hyla elaeochroa_ Cope 525 _Hyla staufferi_ Cope 532 _Hyla staufferi staufferi_ Cope 537 _Hyla staufferi altae_ Dunn 540

EVOLUTIONARY HISTORY 540

LITERATURE CITED 543

INTRODUCTION

The tree frogs of the _Hyla rubra_ group are abundant and form a conspicuous element of the Neotropical frog fauna. Representatives of the group occur from lowland México to Argentina; the greatest diversity is reached in the lowlands of southeastern Brazil (Cochran, 1955). The group apparently originated in South America; the endemic Central American species evolved from stocks that invaded Middle America after the closure of the Colombian Portal in the late Pliocene.

Dunn (1933) partially defined the _rubra_ group as it occurs in Central America. Cope (1865, 1876, 1887), Brocchi (1881), Boulenger (1882), Günther (1901), Noble (1918), Kellogg (1932), Dunn and Emlen (1932), Stuart (1935), and Gaige (1936) dealt with the Middle American species now considered to make up the _rubra_ group. More recently, Taylor (1952, 1958), Fouquette (1958), Starrett (1960), and Duellman (1960, 1963, 1966a) studied aspects of the taxonomy and biology of the species of this group. The five species of the _rubra_ group in Central America have received ten different names. One species, _Hyla staufferi_, has received five names (two subspecies are recognized herein). _Hyla boulengeri_ was named in the genus _Scytopis_, but the type species of _Scytopis_ is a member of the genus _Phrynohyas_ Fitzinger, 1843 (Duellman, 1956.)

Little has been published concerning the ecology, life history, osteology, and mating calls of the Middle American species of this group. The purpose of the present report is to describe the species occurring in Middle America and to comment on their distributions, ecology, cranial osteology, and mating calls, and in so doing provide evidence for the evolutionary history of the species inhabiting Middle America.

Acknowledgments

For permission to examine specimens in their care, I am grateful to Drs. Richard G. Zweifel, American Museum of Natural History (AMNH); Robert F. Inger, Field Museum of Natural History (FMNH); Ernest E. Williams, Museum of Comparative Zoology (MCZ); Hobart M. Smith, University of Illinois Museum of Natural History (UIMNH); Charles F. Walker, University of Michigan Museum of Zoology (UMMZ); Jay M. Savage, University of Southern California (USC); James A. Peters, United States National Museum (USNM); Richard J. Baldauf, Texas Cooperative Wildlife Collection (TCWC); and W. Frank Blair, Texas Natural History Collection (TNHC). KU refers to specimens in the Museum of Natural History, University of Kansas. For the loan of tape-recordings of mating calls I thank Drs. W. Frank Blair, University of Texas, and Richard G. Zweifel, American Museum of Natural History.

I am indebted to the Ford Foundation-Universidad de Oriente (Venezuela) Science Project for a scholarship which enabled me to study for two years at The University of Kansas, foster institution of the project. I have benefited by being able to work in the Museum of Natural History at The University of Kansas and I am grateful to Dr. E. Raymond Hall, Director, for providing space and equipment.

I gratefully acknowledge the assistance and advice of Dr. William E. Duellman, who suggested and directed this work, made available specimens under his care and gave much of his time in reading the manuscript and suggesting improvements. I am grateful to Dr. Frank B. Cross who critically read the manuscript and made many editorial suggestions. I am indebted to Linda Trueb for assistance with the osteological aspects of this study; she helped to clarify many confusing points. I am grateful to Charles W. Myers for making available his field notes on these frogs in Panamá, to Arthur C. Echternacht for reading part of the manuscript, and to John D. Lynch for many suggestions and helpful criticisms. The illustrations were executed by David M. Dennis.

Materials and Methods

For the purposes of the present study I examined 1383 preserved specimens, 50 skeletons, and 9 lots of tadpoles. External characteristics used in the analysis of variation are those currently employed in the study of anuran systematics. Twelve measurements and six proportions were taken in the manner described by Duellman (1956). Only the most important references are given in the synonymies, except those of the two subspecies of _Hyla staufferi,_ which are more nearly complete. The taxonomic history of each frog is discussed under _Remarks_ in each account. The cranial osteology was studied by using skeletons and cleared and stained specimens of all species. Developmental stages of tadpoles were determined from Gosner's (1960) table. Personal field work in Central America in the summer of 1966 provided an opportunity to make observations on the ecology, calling sites, and color in life; these data were supplemented by field notes from, and discussions with, Dr. William E. Duellman and Charles W. Myers.

The mating calls of the frogs were recorded in the field on Magnemite and Uher Tape Recorders by Dr. Duellman in the course of his work on the hylid frogs of Middle America--supported by grants from the National Science Foundation (G-9827 and GB-1441). These recordings, plus those borrowed from other institutions, provided 50 tapes for analysis of the mating calls. The calls were analyzed on a Vibralyzer (Kay Electric Company).

THE HYLA RUBRA GROUP

_Definition._--The species forming the group are small to moderate-sized tree frogs (maximum snout-vent length of males of various species 20-49 mm.), distinguished from other groups in the genus _Hyla_ as follows: Brown, grayish brown, or yellowish tan above; thighs plain, marbled with dark brown, or having vertical bands; vocal sac single, median, subgular; snout flat, protruding, rounded or pointed; webbing between fingers reduced or absent; web between first and second toes reduced to fringe on second toe, rest of toes about half webbed; tarsal fold reduced or absent; shanks robust; inner metatarsal tubercle larger than outer; prevomerine teeth on transverse ridges between small to large sized choanae; skull generally longer than wide; nasals large (length more than 40 per cent total length of skull) and having pointed maxillary processes; maxillary bearing small ventromedial palatine process; quadratojugal slender, always joined to maxillary by bony suture; auditory region of proötic slender and short; delicate spatulate columella ventral to crista parotica, broad basally, compressed anterolaterally, slightly rounded distally; anterior arm of squamosal extending about half distance to maxillary; sphenethmoid wider than long; frontoparietal fontanelle present or absent; prevomerine, premaxillary, and maxillary teeth present; prevomer with two lateral processes forming incomplete bony margin to internal nares; tadpoles having pointed xiphicercal tail, snout short, rounded; 2/3 tooth rows; dorsal fin deeper than ventral fin; sinistral spiracle; short dextral anal tube not reaching edge of ventral fin; mating calls consisting of single long note or series of short notes.

_Composition._--This group contains about 24 currently recognized species, most of which occur in Brazil. Only five species--_boulengeri,_ _elaeochroa_, _foliamorta_, _rubra_, and _staufferi_ with two subspecies--occur in Central America. _Hyla boulengeri_ and _rubra_ are widespread in South America, and _foliamorta_ occurs in Colombia, whereas the other species are known only from Middle America.

_Distribution._--The species of the _Hyla rubra_ group range from the lowlands of northern Argentina and Bolivia to southern Tamaulipas and Guerrero, México.

_Comments._--In Central America two subgroups of species can be recognized. _Hyla boulengeri_ and _H. foliamorta_ are distinctive in the large size of adults (snout-vent lengths 41-49 mm.); both have prominent bars on the thighs, a well-defined interorbital triangular mark, blotches or spots dorsally, and large choanae. _Hyla elaeochroa,_ _H. rubra,_ and _H. staufferi_ are smaller (snout-vent lengths 29-40 mm.); they have the thighs weakly barred or vermiculate anteriorly and posteriorly or unmarked, an ill-defined interorbital triangular mark, linear markings dorsally, and small choanae.

Key to Species and Subspecies

1. Larger frogs (males to 49 mm. snout-vent length); thighs strongly barred; supratympanic fold black; dorsum blotched or spotted 2

Smaller frogs (males to 40 mm. snout-vent length); thighs weakly barred or plain; supratympanic fold pale brown; dorsum usually having linear pattern 3

2. Dorsum tuberculate; snout subacuminate; vocal sac flecked with brown; tarsal fold rudimentary; web absent between fingers; black spots absent in scapular region _H. boulengeri_

Dorsum smooth; snout pointed; vocal sac dark gray; tarsal fold absent; trace of web between fingers; two or more elongate dark spots in scapular region _H. foliamorta_

3. Snout-vent length more than 30 mm.; tympanum 2/3 to 3/4 diameter of eye; prevomerine elevations about size of choanae 4

Snout-vent length less than 30 mm.; tympanum less than 1/2 diameter of eye; prevomerine elevations smaller than choanae 5

4. Thighs mottled posteriorly; discs on fingers about 1/2 size of tympanum; faint dark line from nostril to eye _H. rubra_

Thighs faintly barred or plain posteriorly; discs on fingers about size of tympanum; distinct dark line from nostril to eye _H. elaeochroa_

5. Dorsum brown with irregular dorsolateral stripes and interrupted paravertebral stripes; two transverse bars on shanks; interorbital bar present _H. staufferi staufferi_

Dorsum gray with complete dorsolateral and paravertebral stripes; longitudinal stripe on shank; interorbital bar absent _H. staufferi altae_

Key to Known Tadpoles

1. Entire lower beak black; beaks moderate-sized, serrate; dorsal fin high, extending to middle of back 2

No more than half of lower beak black; beaks small, finely serrate; dorsal fin lower, barely extending onto body 3

2. Papillae present only laterally _H. boulengeri_ Papillae present laterally and ventrally _H. foliamorta_

3. Distinct brown stripe from nostril to eye; two stripes below eye, _H. elaeochroa_

Faint stripe from nostril to eye; no stripe below eye _H. staufferi_

ACCOUNTS OF SPECIES AND SUBSPECIES

_Hyla boulengeri_ (Cope)

_Scytopis boulengeri_ Cope, Bull. U.S. Natl. Mus., 32:12, December 1, 1887 [Holotype.--USNM 13974, from "Nicaragua"; J. A. McNiel, collector].

_Hyla boulengeri:_ Günther, Biologia Centrali-Americana, Reptilia and Batrachia, p. 267, June 1901. Noble, Bull. Amer. Mus. Nat. Hist, 38:339, June 1918. Taylor, Univ. Kansas Sci. Bull., 35:856, July 1, 1952.

_Diagnosis._--Size large (Male to 49 mm., Female to 53 mm.); skull as long as wide; frontoparietal fontanelle present; snout subacuminate; canthus not pronounced; choanae large; tongue cordiform, slightly longer than broad; interorbital triangle tubercular; skin on dorsum tuberculate; tarsal fold reduced or absent; thighs, shanks, and tarsi boldly barred with dark brown and pale yellow-green in life.

_Description._--Head flattened, longer than wide; snout projecting beyond lower lip; loreal region oblique; canthus not pronounced; length of eye less than interorbital distance; tympanum large, about 70 per cent of diameter of eye; interorbital triangle distinct; arms short; fingers lacking web; palmar tubercle tripartite; subarticular tubercles distinct; long tubercle on base of first finger; discs truncate; legs long; tarsal fold reduced or absent; inner metatarsal tubercle rounded, larger than outer, both elevated; subarticular tubercles distinct; one phalanx free of web on second, third, and fifth toes, three free on fourth toe (Fig. 1A and B); skin tuberculate on dorsum, less so on flanks; skin of belly granular, that on chest and throat weakly granular; tongue cordiform, longer than wide, free and notched behind; vocal slits large, lateral to tongue.

In life, dorsum tan or brown with dark spots on snout, head, and scapular region; interorbital triangle and blotch posteriorly on dorsum dark brown; flanks pale green; groin pale green or orange, mottled with dark brown; thighs tan or brown above with dark transverse bars on anterior and posterior surfaces; spaces between bars green or orange; inner surfaces of shanks and outer surfaces of tarsi brown and orange; foot brown above; forelimbs brown and pale green above, weakly barred; belly creamy white with scattered brown spots; vocal sac creamy white flecked with brown; lower jaw brown with white spots on lips (Pl. 1A).

In preservative, head and dorsum dark brown with triangular spot between eyes; dark spots on head and scapular region and dark brown blotch posteriorly on dorsum; flanks creamy white with brown spots; groin creamy white mottled with dark brown; thighs brown above with dark brown transverse bars on anterior and posterior surfaces; inner surfaces of shanks and outer surfaces of tarsi barred with pale brown; dorsal surface of foot mottled brown and creamy white; ventral surface of foot and toes pale brown; forelimbs faintly barred with pale brown; belly white with a few pale brown spots; vocal sac flecked with pale brown; lower jaw marked with small white spots on lips.

_Variation._--Geographic variation is evident in the snout-vent length, tibia length, and foot length, all in relation to snout-vent length, and the relative size of the tympanum to the eye (Table 1). The largest specimens are from the humid Pacific lowlands of Costa Rica; individuals from the Caribbean lowlands of Costa Rica, Canal Zone, and South America are smaller. A general trend for increase in size extends from South America to the Pacific lowlands of Costa Rica.

Most variation in color does not seem to be correlated with geography; color variation is nearly as great within a given population as between separated populations. However, most specimens from Rincón de Osa, Puntarenas Province, Costa Rica, are dusky brown, but a few are darker. In comparison with specimens from the Caribbean lowlands of Central America, specimens from the Pacific slopes in Costa Rica have a darker interorbital triangle. In some specimens from the latter area rugosities are present on the borders of the interorbital triangle, on the snout, on the upper eyelid, and on the heel. Specimens from the Caribbean lowlands are less tuberculate, and most individuals from there lack rugosities on the tarsus. Living individuals from Puerto Viejo, Heredia Province, Costa Rica, and from the Canal Zone, Panamá, are brown above with a metallic green tint. Rugosities are present on the posterior edges of the forelimbs in some specimens from throughout the range. In most respects, specimens from the Canal Zone resemble those from the Caribbean lowlands of Costa Rica more than they resemble those from the Pacific lowlands of Costa Rica, but some individuals from the Canal Zone are less metallic above and have small white spots dorsally on the body, head, and limbs.

A moderate amount of color change from night to day has been noted. At night, a male from Puerto Viejo, Heredia Province, Costa Rica, was grayish tan above with slightly darker markings; the flanks were pale yellowish green. By day, the dorsum was brown with darker markings, and the throat was pale gray with white flecks; the rest of the venter was creamy white. The groin was pale green with black mottling; the anterior and posterior surfaces of the thighs and inner edges of the tarsi were greenish yellow with black bars.

TABLE 1.--Geographic Variation in Size and Proportions in Males of _Hyla boulengeri_. (Means in parentheses below observed ranges.)

========================================================================= | | Snout-vent| Tibia | | | | length | length/ |Tympanum/|Foot length/ Locality | N | (mm.) | snout-vent| eye | snout-vent --------------------+----+-----------+-----------+---------+------------- Costa Rica: Tilarán | 23 | 37.4-48.7 | 0.52-0.58 |0.62-0.76| 0.39-0.45 | | (43.8) | (0.55) | (0.71) | (0.42) | | | | | Costa Rica: Rincón | 10 | 41.4-46.1 | 0.54-0.60 |0.68-0.80| 0.40-0.45 de Osa | | (44.0) | (0.57) | (0.74) | (0.43) | | | | | Costa Rica: Alajuela| 13 | 35.6-43.1 | 0.55-0.60 |0.63-0.78| 0.41-0.46 Province | | (39.8) | (0.57) | (0.69) | (0.44) | | | | | Costa Rica: Puerto | 25 | 37.5-42.9 | 0.51-0.62 |0.63-0.79| 0.38-0.46 Viejo | | (41.6) | (0.55) | (0.71) | (0.43) | | | | | Costa Rica: Suretka | 9 | 38.7-42.0 | 0.56-0.58 |0.53-0.72| 0.35-0.45 | | (41.0) | (0.56) | (0.62) | (0.42) | | | | | Panamá: Canal Zone | 16 | 36.7-42.9 | 0.52-0.58 |0.70-0.78| 0.40-0.44 | | (39.0) | (0.54) | (0.74) | (0.42) | | | | | Venezuela: Santomé | 4 | 35.5-40.9 | 0.45-0.48 |0.63-0.67| 0.36-0.40 | | (38.5) | (0.46) | (0.65) | (0.38)

TABLE 2.--Comparison of Mating Calls in the _Hyla rubra_ Group. (Means in parentheses below observed ranges.)

============================================================================ | |Notes| | | | Major frequencies | | per |Duration| Pulses|Fundamental| (cps) | |call | of note| per | frequency |--------------------- Species | N |group| (sec.) | second| (cps) | Lower | Upper ---------------+---+----+---------+-------+-----------+---------+----------- H. boulengeri | 8 | 1 | 0.24- | 80-120| 70-74 |1400-1820|2520-3182 | | | 0.47 | (101)| (71) | (1611) | (2840) | | | (0.35) | | | | | | | | | | | H. foliamorta | 7 | 1 | 0.23- | 50-60 | 52-61 | 912-1026|2736-3477 | | | 1.86 | (51) | (56) | (918) | (3055) | | | (0.69) | | | | | | | | | | | H. elaeochroa |15 | 2-95| 0.12- | 40-50 | 48-65 |1254-1586|2562-3477 | | (19)| 0.24 | (42) | (57) | (1499) | (2911) | | | (0.17) | | | | | | | | | | | H. s. staufferi|18 | 2-77| 0.13- |100-130| 96-130 |1582-1872|1962-3744 | | (23)| 0.23 | (120) | (106) | (1743) | (3056) | | | (0.18) | | | | | | | | | | | H. s. altae | 7 | 2-22| 0.14- |110-130| 104-117 |1853-2106|3379-4056 | | (11)| 0.18 | (120) | (112) | (2008) | (3775) | | | (0.15) | | | |

_Cranial Osteology._--The skull of _Hyla boulengeri_ is as long as it is wide, and is flat; the premaxillary is small and bears 13 to 17 teeth (mean for 6 specimens, 14.9). The alary processes of the premaxillaries are widely separated, concave posteriorly, and vertical. Ventrally, the premaxillary is connected to the prevomer by bony tissues. The maxillary is slender and bears 70 to 91 teeth (mean for 6 specimens 78.1). The pars facialis of the maxillary is laterally convex and about four times as high as the pars dentalis.

The nasal is large (its length about 40 per cent of total length of skull), and pointed anteriorly and posteriorly in dorsal view. The nasals are separated anteromedially by the cartilaginous septum nasi. One or two protuberances are present on the midlateral concavity of the nasal. Posteriorly, the nasal overlaps the sphenethmoid and articulates with the palatine. Dorsally the sphenethmoid is large, pentagonal, and completely ossified. The frontoparietal is elongate, smooth, and bears a small supraorbital process on the anterior edge of the orbit. A keyhole-shaped frontoparietal fontanelle is present; the fontanelle is narrow anteriorly and wide posteriorly.

The bony part of the proötic is separated dorsally from the squamosal by the cartilaginous crista parotica. The squamosal is small, its anterior arm slender and pointed. The posterior arm of the squamosal is pointed terminally and articulates with the proötic medially.

The prevomer is large and elongate. Anteriorly the prevomer is connected to the maxillary-premaxillary articulation; posteriorly, the prevomer is separated from the sphenethmoid by cartilage. Each prevomer bears six to nine teeth. The palatine is present and edentate. The anterior end of the parasphenoid is broad (less pointed than in _Hyla foliamorta_). The pterygoid is slender and well developed.

_Natural History._--_Hyla boulengeri_ inhabits humid lowland tropical forests and breeds in temporary ponds. Clasping pairs and gravid females were observed at Puerto Viejo, Heredia Province, Costa Rica, on June 21, 1966. Males were calling from depressions in decaying logs and stumps, in forked stems, and from leaves of broad-leafed plants near the pond. Males were observed in late July and early August calling from _Calathea_ and _Heliconia_ leaves at the edge of a pond in the wet forest of the Osa Peninsula. William E. Duellman informed me that he collected calling males in January at El Real, Darién, and in March at Almirante, Bocas del Toro, Panamá. Taylor (1952) found calling males in June at Turrialba, Cartago Province, Costa Rica, and Dunn (1931a) observed males calling in July, November, and December in Panamá. Gravid females have been found from April to August. Breeding activities of _Hyla boulengeri_ always seem to be associated with temporary ponds; in Central America breeding apparently takes place throughout most of the year.

The mating call of _Hyla boulengeri_ consists of one short, moderately low-pitched note. Each note has a duration of 0.24 to 0.47 second and is repeated at intervals of one second to several minutes. The notes have 80 to 120 pulses per second, a fundamental frequency of about 70 cycles per second, and a dominant frequency of 2,840 cycles per second (Table 2, Pl. 3A).

The eggs are deposited in a mass in the water. No information is available concerning early development. Tadpoles in advanced stages of development were found in a temporary pond at Rincón de Osa, Puntarenas Province, Costa Rica. The pond was about 10 cm. deep, had a muddy bottom and lacked vegetation. Three recently metamorphosed young were found in mid-August, 1966, on grass at the edge of another temporary pond in the forest.

_Tadpoles_--Twelve tadpoles are available. These were collected at Rincón de Osa, Puntarenas Province, Costa Rica. The maximum size represented is 34.0 mm., total length (stage 42 of development).

A typical tadpole in stage 36 of development (KU 104295) has a body length of 12.0 mm., tail length of 20.0 mm., and total length of 32.0