Mem. lnst. Butantan v. 53, n. 2, p. 197-204, 1991

THE NEST AND THE TADPOLE OF HYLA WAVRIN/, PARKER (AMPHIBIA, ANURA)

Marcia MARTINS" Gloria MOREIRN •

ABSTRACT: The recently ressurrected H. wavrini was observed at seve­ral locali ties in Brazilian Amazonia. Males call in apparent aggregations from the ground to 6 m above grou nd at the margins of streams, rivers, and lakes in " igap6" and " varzea" !inundation forests ot black and white water, respectively) habitats, apparently throughout the year. At the Re­serva Biol6gica Rio Trombetas, Para, Brazil, we found that H. wavrini builds nests for egg deposition like Lhe other species o·f the H. boans group. The four nests f·ound were less elaborated than those of H boans, H. faber, and H. rosenberg1 and were observed withtn small pools below trees at the margins of an "igap6" lake. Tadpoles leave the nests in five days and larval period is apparent ly very short, probably related to the high density of predatory fishes in the lake. Tadpoles are similar to those of the other species of the H. boans groupf. have cryptic coloration, and live in very shallow waters where they htde beneath the detnlus layer. An encounter call was emitted by a male when a playback of the adver­tisement call was played close to il; th1s and the spacing observed among calling males suggest that H. wavnni males are territorial, such as those of the well studied H. faber and H. rosenbergi. Although sympratic in several Amazonian localities, H. boans and H. wavrini were never found syntopic probably due to habita1 separation (H. boans breeds in streams in fores ts not subjected to seasonal floods).

KEYWORDS: Amphibia, Hyla wavrmi, reproduction.

• Labon:u6r1o de Zoologla, 08/ICB, Universldade do Amazonas, Campus Universitllrto. 69068 Manaus, AM, Brosil • • Departamento de Ecologla, ln5ltluto Nacional da PesQutsas da AmazOnia, Catxa Postal 4 78:, 69083 Manaus AM,

Brosil Rocabiclo para pubhcJc~o orn 19.? 1991 c .:~caito Dm 06.6 1991

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INTRODUCTION

The Hyla boans group (nest building gladiator frogs l1,l2) encompasses large species of Hyla. some of them known to construct sand or clay nests where eggs are laid !see brief reviews in 6.1 1•18·19). Awaning a taxonomic revision or the spe­cies related to H. boans and those or the closely allied H. circumdaca group, we conseNatively consider in the boans group only those species known to build nests tor egg deposition (see IB.19).

A large species of the H. boans group quite distinct in morphology, calls, and calling habitat f rom the widespread Amazonian H. boans was observed by us in several Amazonian localities in the recent years. This lead us ro suspect that this ·1rog was a distinct species. Independently M.S. Hoogmoed (pers. comm.) con­cluded that these and other specimens from several Amazonian localities were actually Hyla wavrini Parker, 1936, and recently resurrected this n.ame9. This au· thor distingu ished H. wavrini from H. boans by using several morphological and calling characteristrcs (see table 2 in9).

Hyla wavrini males call from low perches in " igap6" and "var.zea" habitats (see Methods) where they were suspected to reproduce ("; pers. obs.l Howe­ver, Hoogmoed9 found no nest or egg clutch of /-/. wavrini in several localities 1'1e observed calling males, and suggested that "it seems ( ... )likely that eggs are di­rectly deposited on or in the water"9. Recently we found a call ing aggregation of Hyla wavrini at the Reserva Biol6gica do Rio Trombetas, Para, Brazil, where we found egg clutches, nests, and tadpoles of this species. We here presen t additio­na l observat iOns on callmg habitat of H. wavrini, describe its nests and tadpoles, and compare lhem with those of related species.

METHODS

Observations on calling sites of H. wavrini were made at several Amazonian localities (table 1), all of them in " igap6" and " var.zea" (inundation forests or black and white water, respectively14) habitats. Observations and collections at the Reserva Biol6gica do Rio Trombetas (1 °22'S, 56°52' W, elev. ca. 50 m) were made from 27 October to 4 November and 3 and 4 December, 1990. The study site was Lagoinha, a medium sized lea. 3 ha), shallow "igap6 '' lake connected to the Rio Trombetas during high waters and becomes isolated during the dry sea­son (August-October); the lake is located about 300 m behind the buildings of the reseNe. Observations on nests, tadpoles, and calling males were made in di­verse periods of the day (from 0800h to 2200h l. We marked the calling sites of 13 males at night and looked for nests and egg clutcthes at these sites by day. In one nest (with eggs deposited in the night of 28/29 October) we collected sam­ples of premetamorphs in 29 and 30 October and 1 November and fixed them in 5% formalin. Eggs and embryos were measured to Lhe nearest 0.1 mm under a dissecting microscope. Tadpoles were collected by day at the margins of the lake and fixed in 5% formalin. To confirm tadpole identification, three individuals in stages 41-43 were mantained in laboratory until metamorphosis. Developmen­tal stages of tad poles are those of Gosner8 . Specimens from all localities cited here are deposited in the herpetological collections of Departamento de Ecolo­gia, Institute Nacional de Pesquisas da Arnaz6nia, Manaus, Brazil.

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FIG. 1 - Schematic representalion of a nest of Hyla wavrini (diameter ca. 40 em) found within roots and leaf litter below an island of "igap6" trees at lake Lagoinha, Reserva Biol6gica R1o Trombetas. Par~. Brazil. Finely dotted areas represent water: larger dots represent eggs. Drawn after a photograph.

b

FIG. 2 - Latera l view (a) and mouth (bl of a Hyla wavrmi tadpole !stage 37) collected at lake Lagoinha, Reserva B'ol6gica Rio Trombetas, Par~. Braz1l. Honzomal bars correspond to 3 mm

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RESULTS

~ales of H. wavrini were observed and/or heard calling at several localities in Brazilian Ama7onia, from Rio Branco (Amazonas) to Amapa (Table 1); calling acti­vii.V W<JS ohserved I)Oth in dry and wet seasons (Table 1l throughoul thrs geogra­phical range In alllocahtres, males called rn habitats subjected to seasonal floods Oakes, nvers, and streams rn " igap6" and "v<:h.zea") . Densities of calling males seem to be higher in lakes rhan in rivers or streams.

During our stav at the Rio Trombetas, Hyla wavrini males called all nights. Ca l­ling activity began at 1730h (ca. 30min before dusk) on most evenings and, atter a pO(Ik at approximately 1900-2000h, dirnrnished through the night. Males called 1-1 1 80 DO calls per minute, although some of them emrlted very long and spaced calls in the evening hours. Males called from lhFJ ground (over leaf litter or par­tially submerged in shallow small pools) to 6 m above ground (on branches of " igapo" trees) nearly regularly spaced in apparent aggregations throughout " iga­p6" margins; some areas where calling males were absent were nearly identical to those where males aggrega ted. In these apparent aggregations, distances bet­ween call in9 males varied from approx. 4-15 m, although in 3 November two ma­les called 1.5 m apart for some 30 min until one ot them moved away. When calling close to eacl1 other, males alternated their calls. In 31 November we recorded a long series of the advertisement call of a male and made playbacks some 2m from the same. At the first playback the male immediately emited a senes of 35 encounter calls (Wells, 1977 ) w ith shorter and, apparently, lower pitched notes rhan those of the advertisement call . Further playbacks to this and another male fai led to elicrt responses other than call alternation.

On 1st November, of thirteen ca lling si:es marked in the previous nights, 10 had call ing males (probably the same individua ls) and three were vacan t; further­more one male was cal ling in a site where no male called in the previous nights.

We found fo11r nests (hereafter numbered 1-4 according to day of first obser­vntionl with pre-metamorphs of 1-1. wavrini at calling sites marked in previous nights lbosides these, an aditional depression very similar to a nest was 'found at a cal­ling site). All nests found were water fi lled, roughly round depressions (Fig. 1) with diameters of about 30 - 50 ern, located within shallow irregu lar pools in small islands of " rgap6" vegetation. Nests nos. 1 and 4 were found in 29 October and 4 November, respectively, in o3 site where a male called throughout the observa­tioll perrod. Nest no. 4 was abou t lm rrom nest 110. 1. Nest no. 1 was loca ted rn the leaf li tter-water rntertace, had a water surface or 54x37 em, and was some 4 em deep; nest limits were easily noted by rough walls of mud leaf litter. Nest no. 4 was located within partially submerged roots of an "igap6'' tree and was limited by the roots and by leaf litter (Fig. 1 ). When found, nests nos. 1 and 4 lrNI eggs and embryos in stages 10-11 and 17-18, respectively. Nests nos. 2 and 3 were found in 1 and 3 November, respectively, in a site where a male called also throughout the observa tions. Nest no. 3 was nearly 2.5 m from nest no. 2. They were both located in the leaf litter whithin irregularly shaped depressions and had almost no walls in their limits. When fou nd, both nests nos. 2 and 3 had embryos in stages 21 -23. In 3 November we found a water filled depression that wns very similar to Lhe nests above: a round r.a. 40 ern drameter depression limi-

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ted by muddy and lea r litw walls (some 1-2 em high) loca ted In the leal litter· -water interface. A tadpole of H. wavnni (ca. 30 mrn) m stage 25 was found rn this nest.

We did not countetl eggs in clutches of H. wavrini dunng our stay at Trombe­tas. However lhe clutches of H wr~vnnt observed had ev1dently more egqs than those of H faber (mnge 1614-3576 eggs. x = 2276 eggstS). Eggs are black and surrounded by two transparent jelly-l1ke capsules. Diameler of ex ternal capsules, 1nternal capsules, and eggs were 3.2-3.5 mm, 2.2-2.4 mm, and 1. 6-1.8 mm. res­pect ively. Eggs are deposited as a roughly round monolayer film on the water sur­face and are hold together by their sticky capsules. Suppcsing that eggs are deposited arround 0300h (the mean 11me of egg deposition in lhe related H tosenbergt11l. embryos collected rn a clutch of 28/29 October (nest no. ll were rn stages 18-19 (4.5-4.9 mml rn ca. 40 hand in slages 23-24 !8.2-9.2 mm) rn ca. 90 h. In 3 Oc tober, all tadpoles had abandoned nest no. 1. A nest found in 4 December 1990 had 1056 embryos in stages 20-22, one tadpole in stage 25 (ca. 25 mm), and five freshwater shnmps.

Tadpoles of H. wavnni were found rn shallow small pools and abandoned nests w1thin the 1slands of "1gap6" 1rccs and 1n the marg1ns of a sandy beach at lhe lake. At the sand beach, mdtviduals of d1verse s1zes ('10-35 mm) and stages 125-421 flushed from under a detritus layer at the shallows (1-2 cml as an observer walked near the margins; after swimming a few cenrimeters these tadpoles retreated un­der debris or stopped unretreated. Dorsal coloration i~ cryptic and tadpoles are hardly found w hen 1mmob1le on the bottom.

The follow1ng descnpt1on 1s based on a " typ1cal" tadpole (INPA 1371. collec­ted at lagotnha, Rio Trombetas, Par~. Braz1. 1n 30 November 19901 in develop­mental stage 37. Body length 12.7 mm; total length 34 7 mm; body in dorsal v1ew ovoid, wider (8 .1 mml posteriorly; body in lateral view elongate. dorsoventrally depressed, slightly deeper (5.3 mml posteriorly, throat concave; snout 1n dorsa l view rounded, in lateral v1ew slightly truncate; eyes large, dorsolateral, facing la­terally; diStance helween eyes 2.8 mtn. from eve to nostrrl 0 .9 mm; e·.,..e d1ameter (2.1 mml slightly greater than the distance between nostrils; spiracle sinistral, 1ts opening on midline (Fig. 2al; cloacal tube sron. conical. Caudal musculature MO­

derately robust. gradually tapering to round tip; deepest point of tail 6.1 mm; dor­sal fin originating on body, deeper at m1dlength of ta1l; ventral fin deeper at midlength of tail; depth of dorsal f1n slightlv greater than caudal musculature at midlength of tail; depth of ven tral fin srm1lar to caudal musculature at m1dlength of tail (F1g. 2al Mouth medium-sized, ventra-terminal; well developed l1ps, upper and lower lips with one rcw of small papillae; lower lip wtth symmetrical folds; upper and lower beaks narrow, finely serrate; lower beak V-shaped; two rows of denttcles on the upper lip. the outermost cont1nuous and the innermost interrup­lcd at the m1ddlc; three conunuous rows of denticles on the lower lip IF1g. 21:>). In preserva tive the dorsum 1S brownish tan with darker reticulation; lhroat and an­lerior part of belly like dorsum. posterior part of belly whitish. slighlly translucid; caudal musculature and fins cream with Irregular brown reticulation. In life the body, caudal musculature. and fins are a httle green1sh.

Three metamorphosing tadpoles !stages 43-45) had snout-vent length !SVU of 14, 15, and 17 mm. Recently metamorphosed H. wavnnihas a brown dorsum very similar to the colors of adult.s.

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TABLE 1

Locali ties and dates of observations on calling activity of Hyla wavrini males. The driest months of each locality are indicated.

Locahry

Rio Branco near mouth. Amazonas (AM) Parana AmaJau, AM Rio Jauaperi. AM Anavilhanas, Rio Negro, AM R1o Cuieiras. AM Manaus. AM R1o Trombetas. Po1fl IPAI

Alter do Chao. PA

lgarape do Bispo, Amapa

DISCUSSION

Date

08 Jun 1989 10 Jun 1989 07 Jun 1989

22-24 Mar -988 10 Aug ' 986 20 Nov ·ggo

27 Oct to 04 Dec 1990

17 Sep and 29 Nov 1988 22 Jut 1989

D·•est months

Aug Sop Aug-Sep Aug-Sep Jun-Oct Jun-Oct Jun Oct Aug Oct

Aug-Oc t

Sep-Nov

f-fyfa wavrini is w idespread in northern Amazonia. occurnng from Taracufl. R10 Uaupes, Amazonas9 , throughout the Amazon Basin, reachmg lgarape do B1soo. just south of Macapa, Amapa (pers. obs l At the present state of knowledge, its range seems to be w ithin that of H. boans (see fig. 1 in9) which occurs m sou­thern Central Amenca and throughout Amazonia. In fact, both spec ies are sympa­tric at several Amazonian localities (9; pers. obs.l. although they were never found to be syntop1c. Hyfa boans breeds in "terra f1rme" (forests not subject 10 munda­tionsJ streams while H. wavrim breeds at lakes, streams, and nvers in "igap6" and "varzea" habitats. This habitat separation may prevent syntopy and, conse­quently, hybridization. Another difference between these two related species IS

that H boans breeds dunng the dry season (22; pers. obs) while H. wavnm seems to breed both 1n the dry and wet seasons (thiS study!.

The spacmg observed among calling males. tho1r apparen t fidelity to call ing sites, and the presence of an encounter call in the vocal repertoire indicate that H. wavrini males are territorial. Hoogmoed9 observed scars, probably caused by prepollical spines. in the dorsum of a male H. wavrim and speculated that males of this spec1es may fight as 1n H. faber and H. rosenbergi, the only two well stu­died species of the boans group l2,16,l8.19 . Thus, as for nest buildtng behavior, figh­ting behavior may be Widespread in the boans group; suggestively, Kluge 11·1' treats the H. boans group as "nest build1ng gladiator frogs".

The habit of building nests for egg depos1110n was observed in H. biobeba 10,

H. boans1A5-13, H. faber1·15•17.1B. T9, H. pardalis 16, H. rosenbergi12• and H. wavrini (this study). The nests of H. wavrini described herein have walls less elaborated than those of H. boans fpers obs.J. H faber (e.g ., fig. 6 1n 19• and H. rosenbergi (e.g .. ftg 27 in 12). However, Kluge 12 and Martins 18 suggest that the matenal used to build nests and, consequently, the1r architecture. in H. rosenberg i and H faber. respectively, is rela ted to the nature and hardness of the substrate (e.g., some H. faber males build nests just by pushing away the aquatic vegetation in pond margins 18).

The developmenta l rate of H. wavnm 1nit1al premetamorph1c stages observed at Trombetas is faster than those observed by Martins18 for H. faber and by Kluge 1' for H. rosenbergi. Furthermore. metamorphosing young 1-f. wavnm (SVL

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14-17 rnm) are smaller than those of H. rosenbergi ISVL 19-22 mml and H faber (SVL 31 -37 mml. These differences suggest that total developmental penod of H. wavrini ;s shorter than those of the latter species (40 days in H. rosenbergi 12;

8-9 months in H. faber 18). Rapid developmental period may increase the proba­bility of tadpoles escaping preda tion and/or water drying in temporary ponds. but in permanent ponds it may also permit escape from large predators21. We ob­served high densi ty of fishes at Lagoinha (probably because of the low waters. see2°). Short developmental penod associated with the defensive tactics (crypsis. hiding behaviour. and preference for very shallow water) observed in H. wavrini tadpoles may reflect the h1gh density of preoators in the hab1tats w here tadpoles grow.

In general. the tadpoles of Hyla wavrini are similar to those known for the other members of the boans group Major differences for tadpoles 1n similar stages are the following: the tadpoles of H biobeba are larger (66 mm m stage 3711, have two rows of pap1llae bordenng upper and lower lips, and no fold and four rows of denticles in the lower lip, the innermost interrupted at midlength; the tadpoles of H. boans are slightly larger (43 mm in stage 3861 and have four rows of denti­cles in the lower hp; those of H. faber are larger 180 mm in stage 37 181. those of H. pardalis are slightly larger (43 mm 1n stage 38 11. have no row of papil ae in the upper lip, and the mnermost row of den ticles in the lower lip is interrupted at mid length; and those of H. rosenbergi have four rows of denticles in the lower lip.

Additional observations on the reproductive biology of H. wavrini and H boans. ideally at localities where the two spec1es are sympatric (see9). would clarify how these two closely related species face the constraints associated w their different breeding habitats (inundatiOn forests and streams in "terra f1rme", respectively).

ACKNOWLEDGEMENTS

W e thank Silvia Egler, Marcelo Gordo. Celio Haddad. and J. P. Pombal Jr. for helpful sugges110ns on earlier drafts of the manuscript; IBAMA for permiSSIOn to work at Trombetas; and CNPq for financ1al support to M . Martins.

RESUMO. Hyla wavrmi, especie recem-revalidada. foi observada em di­versas localidades da Amazonia brasileira. Machos camam em aparen­tes agregacoes. do chao ate 6 m de altura. em margens de nachos. rios e lagos Cln ambientes de igap6 e varzea (florestas inundclveiS de agua preta e agua branca. respect•vamentel. aparentemente duranLe todo o ano. Na Reserva B•ol6g1ca Rio Trombetas. Para, Brasil. observamos que H. wavnni constr6i n.nhos para a desova. como as outras especies do grupo H boans. Ouatro ninhos encomrados eram menos elaborados que aqueles de H. boans. H faber e H. rosenbergi e estavam entre pe­quenas po(fas sob arvores nas margens de um lago de igap6. Os g~ri­nos abandonam os n.nhos em cerca de c•nco d•as e o perlodo larvarro e aparcn temente mUltO breve, provavelmentc dcv1d0 ll grande dens1da de de pcixes predadores no lago. Os g~rinos sao semelhantes llqueles das outras especies do grupo H. boans. tem colora<;ao cripuca e vivem em aguas muito rasas onde se escondem sob uma camada de detritos Um "grito de encontro" foi em111do porum macho ouando um "play­back" do canto de advertencia 101 tocado pr6x•mo a ele; estc fato e o espacamento observado entre machos que contavam sugercm que ma­chos do H. wavrini sao territoriais. como em cluas esp~c•es pr6ximas.

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MARTINS, M & MOREIRA, G Tne nest and the tacpole of Hyla wavrini, Parker (Amphibia, Anura) Mem. lnst. Butantan. v 53, n 2. p 197·204, 1991

bem estudadas. H fabet e H rosenbergi. Embora Slmpc\tncas err dl· versas localidades da Amazon1a, H. boans e H. wavnnr n!!o foram en­contradas em sintop1a, provavelmente devido a separa~ao por habitats (H. boans reproduz-se em riachos de ilorestas nao sujei1as a inurda­<;oes peri6dicasl.

UNITERMOS: Amphib1a. H. wavrrnt; reproduc;ao.

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