Visual and Acoustic Communication in the Brazilian Torrent Frog, Hylodes Asper (Anura: Leptodactylidae) Author(S): Célio F

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Visual and Acoustic Communication in the Brazilian Torrent Frog, Hylodes asper (Anura: Leptodactylidae) Author(s): Célio F. B. Haddad and Ariovaldo A. Giaretta Source: Herpetologica, Vol. 55, No. 3 (Sep., 1999), pp. 324-333 Published by: Herpetologists' League Stable URL: http://www.jstor.org/stable/3893226 . Accessed: 24/01/2014 11:44

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OKADA, Y. 1931. The Tailless Batrachians of the Jap- borea (L.). Pp. 295-4336. In D. H. Taylor and S. I. anese Empire. Imperial Agricultural Experiment Gutmann (Eds.), The Reproductive Biology of Am- Station, Nishigahara, Tokyo, Japan. phibians. Plenum Press, New York, New York, U.S.A. RYAN, M. J., A. S. RAND, AND L. A. WEIGT. 1996. UEDA, H. 1994. Mating calls of the pond frog species Allozyme and advertisement call variation in the distributed in the Far East and their artificial hy- tuingara frog, Physalaemus pustulosus. Evolution brids. Scientific Report of the Laboratory for Am- 50:2435-2453. phibian Biology, Hiroshima University 13:197-232. SAS INSTITUTE. 1988a. SAS User's Guide: Basics. ZHAO, E-M., AND K. ADLER. 1993. Herpetology of Version 6 ed. SAS Institute Inc., Cary, North Car- China. Society for the Study of Amphibians and olina, U.S.A. Reptiles. Contributions to Herpetology 10:1-522. . 1988b. SAS User's Guide: Statistics. Version 6 ed. SAS Institute Inc., Cary, North Carolina, U.S.A. SCHNEIDER, H. 1977. Acoustic behavior and physiology Accepted: 24 September 1998 of vocalization in the European tree frog, Hyla ar- Associate Editor: Richard Howard

Herpetologica, 55(3), 1999, 324-333 C 1999 by The Herpetologists' League, Inc.

VISUAL AND ACOUSTIC COMMUNICATION IN THE BRAZILIAN TORRENT FROG, HYLODES ASPER (ANURA: LEPTODACTYLIDAE)

CELIO F. B. HADDAD13 AND ARIOVALDOA. GIARETTAA2 'Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720, USA 2Departamento de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas, C.P. 6109, 13083-970 Campinas, Sio Paulo, Brasil

ABSTRACT: We studied the signaling, territorial, and courtship behaviors of the diurnal frog Hylodes asper. Visual and acoustic communication were used during intraspecific interactions involving males, females, and subadults. Hylodes asper has a complex visual communication system, of which foot-flagging is the most distinctive display observed in the repertoire of visual signals. The splash zone produced by the waterfalls and torrents creates a high, nearly constant, humidity near the streams, reducing the risk of desiccation which enables the diurnal activity of H. asper Although the ambient sound pressure levels (SPL), measured at the calling sites, are similar to the SPL of the advertisement calls, the high-pitched calls of H. asper are spectrally different from the noise produced by the water current. Thus, the ambient noise produced by the water current may not interfere significantly with the acoustic communication of this species. The noise and the nearly constant and high humidity produced by the torrents and waterfalls, along with the availability of light, probably favored the evolution of contrasting colors and visual communication in H. asper. Males of H. asper excavate underwater chambers that are probably used to shelter the eggs and to prevent the clutch from being drifted downstream. Key words: Hylodes asper; Anura; Hylodinae; Visual communication; Acoustic communication; Reproductive mode; Atlantic Forest; Southeastern Brazil

AMONG amphibians, vocalization is munication by acoustic signals is effective highly developed in anurans, most species in several circumstances, including situa- of which have vocal structures capable of tions where vision is limited (Gerhardt, producing a variety of sounds that attract 1983). Acoustic communication must have mates, advertise territories, or express dis- been favored by the pump breathing tress (Duellman and Trueb, 1986). Com- mechanism (Duellman and Trueb, 1986) and by the nocturnal activity observed for the majority of anuran species. The 3 PRESENT ADDRESS: Departmento de Zoologia, In- evo- stituto de Biociencias, Universidade Estadual Paulista, lution of visual communication in some C.P. 199, 13506-900 Rio Claro, Sao Paulo, Brasil. species of frogs has apparently been fa-

This content downloaded from 186.217.234.230 on Fri, 24 Jan 2014 11:44:35 AM All use subject to JSTOR Terms and Conditions September 1999] HERPETOLOGICA 325 vored by the availabilityof ambient light h of observations, from March 1988- (Lindquist and Hetherington, 1996, and March 1994, from 0530-2000 h. The study references therein). Diurnal species of an- was conducted at Paranapiacaba, Munici- urans commonly use visual displays, ap- pio de Santo Andre (23047'S, 46018'W, 800 parently for communication (e.g., Durant m above sea level), and Picinguaba, Mun- and Dole, 1975; Wells, 1980), with limb icipio de Ubatuba (23023'S, 44?50'W, 50- signals being the most distinctive behavior 100 m above sea level), State of Sao Paulo, described (e.g., Davison, 1984; Harding, Brazil, in streams with waterfalls and ex- 1982; Heyer et al., 1990; Pombal et al., tensive rapids. 1994). The apparentuse of limb signals for Focal animal and all occurrence sam- visual communication in anuranshas been plings were used for behavioral records observed for the following genera: Brachy- (Lehner, 1979). Experimental manipula- cephalus (Brachycephalidae), Atelopus tions were restricte to the manual inser- (Bufonidae), Dendrobates (Dendrobati- tion of a mirror (15 x 10 cm) next to res- dae), Litoria (Hylidae), Hylodes (Lepto- ident males, to test the importance of vi- dactylidae), Taudactylus (Myobatrachy- sion during the territorial interactions. De- dae), and Staurois (Ranidae) (see revision scriptions of the behaviors are based on in Lindquist and Hetherington, 1996). In individuals observed and videotaped in the addition to these genera, leg signals are field. Individuals were not marked, but performed by males during territorial in- some of them were recognized in succes- natural teractions in two nocturnal species in the sive days by distinctive markings and color patterns. We recorded advertise- genus Phyllomedusa (Hylidae) (P. distinc- ment calls in a Nagra E tape recorder us- ta: Castanho, 1994; P. burmeisteri: obser- ing a Sennheiser ME 80 micro phone; oth- vations by C. F. B. Haddad). er vocalizations were recorde in a Sony The subfamily Hylodinae comprises TCM-74v tape recorder using a Sony car- frogs distributed among the genera Cros- dioid microphone. The sonograms were sodactylus, Hylodes, and Megaelosia. A produced in a Macintosh computer cou- great number of species in this subfamily pled to the MacRecorder Sound System is diurnal, and males of most species in the 2.0.5, using 8 bit resolution, 22 kHz sam- genera Crossodactylus and Hylodes have pling frequency, and FFT with 256 points. loud bird-like voices (Vielliard and Car- For the statistical analysis of the results, doso, 1996; Weygoldt and Carvalho e Sil- we used the Mann-Whitney rank sum test, va, 1992); Megaelosia is apparentlyvoice- with a = 0.05 (Zar, 1996). less (Giaretta et al., 1993). Although some species of Hylodinae are common along RESULTS small forest streams in south and south- Hylodes asper was acoustically active in eastern Brazil, little is known about their all months, showing a peak in activity dur- reproductive behavior (Heyer et al., 1990; ing the rainy season (October-March). Weygoldt and Carvalhoe Silva, 1992). Hy- During the night, males, females, and ju- lodes asper, which has a distribution from veniles of H. asper were observed resting south to southeastern Brazil, occurring in crevices or on branches and leaves up from Santa Catarina to Rio de Janeiro to 1.0 m above the ground, near streams. (Frost, 1985), is known for displayingboth Tadpoles were observed performing feed- acoustic signals and apparentvisual signals ing activities during the day and at night near mountain streams (Heyer et al., 1990; in the streams. Males started to emit ad- Hodl et al., 1997). In the present study, vertisement calls during sunrise and we describe the signaling, territorial,nest stopped during sunset. The communication of H. and courtship behaviors of this asper is based on visual and building, acoustic signals, as described below. diurnal frog. Visual Communication Performed by MATERIALS AND METHODS Isolated Males The behaviors of H. asper were studied During the day, males defended during 18 visits, totaling 45 days and 112 emerged rocks and logs as territories, used

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We quantified the foot-flagging behavior of 11 calling males and observed that both left and right legs are used with similar frequencies (the right leg was used 71 times and the left leg was used 89 times); however, they were not used with regular alternation. The males may call without any observable movement of the limbs (n = 58 calls for 11 observed males). Some- times the foot-flagging display (26 observations for eight males) and the movements of the toes (27 observations for two males) were performed by males that were not calling. We observed subtle, but ap- ment call. Note the inflated vocal sacs. parently deliberate, up-and-down movements of one of the arms in front of the white chest, for two isolated males. as calling and courtship sites, and for feeding activities. Males of H. asper observed Territoriality and Visual Communication from above are cryptically colored, resem- Performed by Interacting Males bling the dark substrate of their calling At sunrise, males start to emit territorial sites. However, when the male is observed calls (described below) near the nocturnal from the front, in the plane that he might shelters, approximately 2-6 m from the be observed by conspecifics, the white calling site. At sunset, the males again emit venter and bright vocal pouches contrast territorial calls while returning to the noc- with the dark substrate, probably enhanc- turnal shelters. During the day, territorial ing the visibility of the male. Some visual males usually climb the rocks and logs signals are associated with stereotyped be- near waterfalls and the fastest torrents to haviors that allow the exposure of the usu- watch the territory and signal from an el- ally concealed contrasting colored parts. evated position. Males call from these sites The most distinctive visual signal is the and consequently vocalizations are emitted movement of a hind limb,, which is gen- from the noisiest parts of the streams. erally displayed while calling (foot-flag- Males may return to the same calling site ging). When the male starts to call, hemay in successive days (n = 8 males) and may raise one hind lhmb and extend it up and use the same nocturnal shelter for more back in an arc-shape movement of approx- than a month (n = 1 male). Females ap- imately 450 from the substrate, maintain- parently do not defend territories; how- ing the body stationary. When the leg is ever, they were observed returning to the extended (Fig. 1) the toes separate and the same diurnal sites in successive days (n = silvery color of the dorsal surfaces of toes 4 females). Territorial males of H. asper and toe fringes become visible. The leg re- were observed attracting females and ac- turs to the male's side just after finishing tively hunting invertebrates inside the ter- the call, and during 1-2 s he wiggles the ritories. Males seem to have an acute vi- toes of both feet without moving the legs, sual sense of movements; we observed showing the silver coloration (see similar males moving 3 m, by jumping on rocks descriptions in Heyer et al., 1990; Hodp et and logs, to prey on small insects and spi- al., 1997). The movements of the silvery ders. After ingestion, the male returned to parts of the foot contrast sharply with the the calling site. When a territorial male dark coloration of the male's body and with perceives an intruder by sight or by hear- the dark substrate. Females of H. asper do ing the advertisement call (described be- not present this contrasting color patter low), he increases the rate of advertise- on the feet and were not observed per- ment calls and foot-flagging behavior. forming foot-flagging. We observed eight territorial interac-

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AA B

FIG. 2.-Territorial male of Hylodes asper (A) emitting territorial calls, (B) stretching the legs backwards, (C) lifting the body, and (D) prior to the emission of vocalization.

tions that finished before fights, eight that onds to more than 1 h (x = 26.5 min, SD culminated in fights between two males, = 36.6, range 3 s to 85 min, n = 5) and and one that culminated in a fight among may be subdivided into rounds (x = 2.5 three males. The interactions that finished rounds per fight, SD = 1.9, range 1-5, n before fighting involved males that were = 4). When two males interact for the pos- passing through areas alreadydefended by session of a territory, the progression can resident males. In these cases, the intrud- be described as follows: one or both males ers were pursued. During the pursuit, the start to emit advertisement calls with foot- territorial male begins emitting advertise- flagging; then one or both males start to ment calls plus foot-flagging, and chases emit territorial calls with subtle up-and- the intruder by using these behaviors as down movements of one of the arms in well as territorial calls. Sometimes during front of the white chest (n = 1); then one pursuit, the territorial male emits territo- or both males start to emit the territorial rial calls plus the behavior of stretchingthe calls with the behavior of stretching the legs backwards at ground level and, sub- legs backwards without raising and, subsequently, lifting the body (n = 6; Fig. 2); sequently, lifting the body (n = 7). One the intruder is chased until the frontiersof male jumps, and using its snout, tries to the territory.Fights may last for a few sec- beat against the rival; the other male tries

This content downloaded from 186.217.234.230 on Fri, 24 Jan 2014 11:44:35 AM All use subject to JSTOR Terms and Conditions 328 HERPETOLOGICA [Vol. 55, No. 3 to repel the attack by kicking the jumping calls and territorialcalls. The activitiesper- male. The males fight by trying to enter formed by the male inside the chamber between their rival and the substrate; the were not observed. After observation the lower male attempts to dislodge the upper chamber was inspected and contained no male by pushing him with the feet, arms, eggs. flanks, or dorsal surfaces of its head and body; the round is finished when one of Visual Communication and Courtship the males is thrown down into the stream Behavior (the loser may return for another round) We observed a total of 13 females being or when one of the males flees. courted by males. In nine cases, females We observed seven territorial interac- refused the males by fleeing during the tions between a subadult and an adult courtship ritual. Courtship can be de- male of H. asper Five interactions finished scribed as follows. When the male per- before fights and two culminated in fights ceives an approachingfemale, he faces her between a male and a subadult. The ter- and starts to emit the advertisement calls ritorial behaviors observed during these plus foot-flagging displays;the female sig- interactions involving an adult male and a nals acceptance by stretching one or both subadult were similar to those described legs backwardsat ground level (similar to above for territorial males, except that the the male in Fig. 2B) and performingsubtle subadults were never observed emitting up-and-down movements of one of the vocalizations or performing the foot-flag- arms in front of the white chest; the male ging behavior. However, subadults may and the female approach each other; the show the behavior of stretching the legs male emits a low intensity courtship call backwards at ground level and, subse- and then touches the female's snout with quently, lifting the body (n = 4; Fig. 2). his gular region; the male jumps among To test the importance of vision during the rocks and logs apparently attracting the territorial interactions, we introduced the female with advertisement calls and a mirror into the territories of eight calling foot-flagging displays;the male then dives males. Just two males continued calling af- into the flowing water, followed by the fe- ter this manipulation. One male did not male. One female consecutively repeated change his behavior and continued to call; these behaviorswith three different males, the other male stopped the advertisement staying undenrater for a few seconds with calls, faced the mirror, started to emit ter- each one. Underwater behaviors were not ritorial calls, stretched the legs backwards observed. One dissected female contained without raising and, subsequently, lifted several unpigmented oviductal eggs (x = the body (Fig. 2), then jumped against the 2.58 mm diameter, SD = 0.27, range 2.3- mirror three times beating with the snout. 3.18, n = 10). One male of H. asper apparently signaled to a female of Hylodes Diving Behavior of Males phyllodes that was crossing his territory; In October 1993, we observed a male the female did not respond to the male. diving several times into the torrent and entering an underwater chamber. The Vocalizations male was excavating the chamber by re- Males likely call to attract females and moving the sand amidst some submerged to defend territories. Four different vocal- rocks. The chamber was 20 cm in total ization types were observed. The most length and its opening was 6 cm wide and common is the advertisement call that was 17 cm below the water surface. The consists of high-pitched whistled trills. At average time spent by the male underwa- an air temperature of 24-25 C, the adver- ter was 256 s (SD = 91, range 162-468 s, tisement calls are composed of 33-46 n = 17) and the mean interval between notes (x = 41.1, SD = 4.4, n = 10). The dives was 546 s (SD = 397, range 240- mean duration of this vocalization is 2.22 1230 s, n = 10). Sometimes, between s (SD = 0.37, range 1.65-2.73, n = 10) dives, the male emitted advertisement and the mean duration of the notes is 27

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N 6 6t r r rf rr

wD 0 2 I M E

TIME 0.2s s

TIME- O-Ol1s_

FIG. 3.-Sonogram (upper) of part of the advertisement call and wave form (lower) of one note of the advertisement call of Hylodes asper; the wave form corresponds to the last note in the sonogram. The ambient noise produced by the torrents is mainly 0-2 kHz. Picinguaba, Ubatuba, Sao Paulo; air temperature was 24- 25 C.

ms (SD = 4, range 20-30, n = 36). Each ing foot-flagging behavior (x = 88.7 s, SD note is an ascending frequency-modulated = 58.1, range 44-313, n = 46 vocalizations sound with the energy concentrated on the of five males) were significantly higher (P third harmonic, between approximately 5 < 0.0001) than the intervals between ad- and 6.5 kHz; the energy on the fundamen- vertisement calls of males that were per- tal and second harmonic is low (Fig. 3). forming foot-flagging (x = 47.9 s, SD = The fundamental, around 2 kHz, is not vis- 8.9, range 35-67, n = 26 vocalizations of ible in the sonogram, and the second har- two males). monic can be seen by weak marks around Two vocalization types were emitted 4 kHz. The frequencies on the third har- during agonistic male-male interactions: monic are higher than the frequencies of the territorial calls and squeals (Fig. 4). the background noise produced by the tor- The territorial call is a note with a mean rents and waterfalls (Fig. 3). The intervals duration of 31 ms (SD = 6, range 20-40, between advertisement calls emitted by n = 10), that is a frequency-modulated males of H. asper that were not perform- peep with the energy distributed in three

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6 A A B A

X 2 ?~~0 . .. 0t {:?0 - 4

z w C' _ p'J'',-f

2 - P"

TIME 0.2s

FIG. 4.-Sonograms of vocalizations emitted during agonistic male-male interactions of Hylodes asper: (upper) "A"notes are territorial calls and "B" note is a squeal without harmonic structure; (lower) squeal with harmonic structure. The ambient noise produced by the torrents is mainly 0-2 kHz. Paranapiacaba, Santo Andr6, Sao Paulo; air temperature was 24-25 C. harmonic structures between 1.4 and 5.6 1998). The lower intervals between adver- kHz (Fig. 4 upper). Squeals emitted dur- tisement calls of males of H. asper that ing fighting were variable in duration (x = were performing foot-flagging suggest that 260 ms, SD = 90, range 170-460, n = 8) males that are calling and performing the and structure; some squeals show harmon- foot-flagging behavior are more excited ic structures (Fig. 4 lower) and in others than males that are just calling. The ad- the harmonics are not evident (Fig. 4 up- vertisement call of H. asper is similar to per). The fourth vocalization type is a the advertisement calls of several species short, low intensity courtship call (not tape in the genus Hylodes that, like H. asper, recorded), emitted when the male is close occur near torrents (e.g., Haddad et al., to the female during courtship. 1996; Heyer and Cocroft, 1986; Vielliard and Cardoso, 1996). The characteristics of DISCUSSION the advertisement calls of some studied Variable aggressive calls, as observed for species in the genus Hylodes may be sum- H. asper, have been described for other marized as follows: short and numerous frog species (e.g., Cardoso and Haddad, notes with harmonic structures and rapid 1984; Wells, 1988) and may signal the mo- raise and decay; energy concentrated on tivational state of the opponents during ag- the third harmonic that is free from the onistic encounters, helping to avoid the low noise frequencies of the environment; risks of physical combats (Martins et al., notes rhythmically spaced within the se-

This content downloaded from 186.217.234.230 on Fri, 24 Jan 2014 11:44:35 AM All use subject to JSTOR Terms and Conditions September 1999] HERPETOLOGICA 331 quences that are separated by long periods males, and subadults of H. asper have a of silence. These characteristics have an complex system of visual communication, adaptive significance in allowing the vocal being foot-flagging behavior just one of the signals to be heard in environments of displays observed in the repertoire of vi- high ambient water noise, facilitating the sual signals of this species. Males of Ate- localization of the calling male (Dubois lopus zeteki, a montane stream species and Martens, 1984; Haddad et al., 1996; from Panama, perform visual communi- Vielliard and Cardoso, 1996). cation using a subtle but apparently delib- Similar and convergent acoustic char- erate foot-raising behavior that is some- acteristics may be observed between frogs what different from the foot-flagging dis- and birds from torrents and waterfalls of play; besides this behavior, males of this the Atlantic Forest mountains of Brazil species display a stereotyped forelimb (Vielliard and Cardoso, 1996) and of the waving signal (Lindquist and Hethering- Himalayan Mountains (Dubois and Mar- ton, 1996). Brachycephalus ephippium tens, 1984). This general pattern of con- was considered a diurnal forelimb signal- vergence among unrelated groups in dif- ing anuran, occurring in stream microhab- ferent regions of the world demonstrates itats (Lindquist and Hetherington, 1996); the effects of noisy environments on mod- however, this species has direct develop- eling the acoustic communication in ani- ment (Pombal et al., 1994) and is more mals. Although the ambient sound pres- common in quiet and humid places of the sure levels (SPL), measured at the calling forest floor far from water bodies (personal sites, are similar to the SPL of the adver- observations). Consequently, the evolution tisement calls (Hbdl et al., 1997), the high- of visual communication in B. ephippium pitched calls of H. asper are spectrallydif- apparently was not related to the con- ferent from the noise produced by the wa- straints of the noisy environments of tor- ter current. Thus, the ambient noise pro- rents and waterfalls, but may have been duced by the water current may not related to the diurnal activity and apose- interfere significantly with the acoustic matic coloration of this species (Pombal et communication of this species. al., 1994). In the cases of Litoria and Phyl- Species of anuransliving near rain forest lomedusa, which are nocturnal species, it torrents and waterfalls are subject to a is more difficult to understand the selec- nearly constant, high relative humidity as tive pressures leading to the evolution of a result of the waterfall splash zone. visual communication. Species in both Therefore, these species are not subject to genera have contrasting color patterns on desiccation and could evolve a diurnal ac- the hind limbs, which is apparently used tivity pattern. The noise produced by tor- in nocturnal visual communication among rents along with the availabilityof light for territorial males (Litoria: Heyer et al., the diurnal species of torrent frogs may 1990; Richards and James, 1992; Phyllo- have favored the evolution of contrasting medusa: Castanho, 1994; observations by colors and visual communication. The vi- C. F. B. Haddad). sual display and exposure of the contrast- In the rheophilic subfamily Hylodinae, ing colors might conceivably attract pred- all known species of Megaelosia are appar- ators, but a frog on the edge of a mountain ently mute (Giaretta et al., 1993), some stream can easily escape from a predator species of Hylodes are mute (Heyer, 1982) by jumping into the swift waters (Heyer et or have a weak vocalization and bright col- al., 1990; Hodl et al., 1997; personal ob- ors (Gouvea, 1979), and Crossodactylus servations). gaudichaudii displays apparent visual sig- Torrent frogs of the genus Staurois, nals during territorial interactions (Wey- Taudactylus,and Hylodes display foot sig- goldt and Carvalho e Silva, 1992). These nals, apparently for visual communication observations and characteristics are indic- in a convergent way (Harding, 1982; Hey- ative that visual displays may be wide- er et al., 1990; Winter and MacDonald, spread among the species in this subfam- 1986; present study). However, males, fe- ily.

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We can tentatively reconstruct the as a protection against predators and to courtship behavior of H. asper as follows: prevent the eggs from drifting down- the male excavates an underwater cham- stream; subsequently, feeding tadpoles ber near his calling site; he calls from abandon the chamber and go into the emerged rocks and logs near torrent stream. This reproductive mode is uncom- streams and near his chamber; a gravid fe- mon among anuransand has only been ob- male approaches the male, attracted by his served for some Hylodinae frogs (Faria et acoustic and visual displays; after physical al., 1993; Weygoldt and Carvalho e Silva, contact, the male guides the female to the 1992; present study). underwater chamber; the female inspects the chamber and may accept or refuse to RESUMO reproduce with the male; the female may Os comportamentos de sinalizavao,ter- engage with another male to inspect his ritorial e de corte foram estudados para o chamber. In species in which the males anuro diumo Hylodes asper, com base nos construct nests for reproduction, the nest sistemas de comunicavdoacu'stica e visual. quality may be used by the females as a Estes sistemas de comunicaVdosao usados way to select males, which may be refused durante interaV6es intraespecfficasenvol- or accepted on the basis of the construc- vendo machos, femeas e subadultos. Hy- tion characteristics (e.g., Hylafaber: Mar- lodes asper tem um sistema de comuni- tins, 1993; H. leucopygia: observations by caVao visual complexo, destacando-se a C. F. B. Haddad). sinaliza,co realizadacom os membros pos- The reproductive modes in the subfam- teriores ("foot-flagging"),que e a mais dis- ily Hylodinae are not well known; only for tintiva dentro do repertorio de sinais vis- two species, one in the genus Crossodac- uais. Os borrifos d'agua, produzidos pelas tylus and another in the genus Hylodes, corredeiras e cachoeiras, criam uma umi- has the reproductive mode been identi- dade elevada e constante proximo aos ria- fied. In both cases, males excavate under- chos, reduzindo os riscos de dessecaVao,o water oviposition nests in the substrate of que possibilita a atividadediurna de H. as- mountain streams (Faria et al., 1993; Wey- per. Embora a intensidade do rufdo am- goldt and Carvalho e Silva, 1992). Mutual biental seja similar a da vocalizaVaode an- touches between male and female engaged uncio de H. asper, esta e espectralmente in courtship and/or the behavior displayed diferente do rufdo produzido pelas corre- by the male of guiding the female to the deiras e cachoeiras. Assim, o ruido am- oviposition site are typical of anuran spe- biental nao parece representar uma fonte cies in which the male constructs a con- importante de interferencia na comunica- cealed nest for the clutch, before the ar- Vaoacu'stica desta especie. 0 ruido e a um- rival of the female (e.g., Hyla leucopygia: idade elevada e constante gerados pelas Haddad and Sazima, 1992; observations by corredeiras e cachoeiras, juntamente com C. F. B. Haddad; Leptodactylus fuscus: a disponibilidadede luz, provavelmentefa- Martins, 1988). Hylodes phyllodes shows a voreceram a evolu:ao de coloravoes con- courtship behavior similar to that observed trastantes e comunicaVaovisual em H. as- for H. asper: the male touches the snout per Machos de H. asper escavam tocas su- of his mate with the gular region; the fe- baquaticas que provavelmente sao usadas male follows the male to the underwater para proteger a desova contra predadores nest (Faria et al., 1993). The unpigmented e prevenir que os ovos sejam carregados eggs observed in the dissected female of pela correnteza. H. asper are indirect evidence that the Acknowledgnents.-We thank A. d'Heursel, R. D. clutch is deposited in places protected Howard, R. Jaeger, E. D. Lindquist, and A. S. Rand from insolation. The observation that for critically reading the manuscript, J. R. Somera for males of H. asper excavate underwater the drawing, and R. P. Bastos and J. P. Pombal, Jr. for chambers strongly suggests that the repro- field assistance. The study at Picinguaba was made possible by the logistical support of Instituto Florestal ductive mode of this species is character- do Estado de Sao Paulo. C. F. B. Haddad acknowl- ized by eggs deposited inside the chamber edges FAPESP (proc. 95/9269-2) for financial support

This content downloaded from 186.217.234.230 on Fri, 24 Jan 2014 11:44:35 AM All use subject to JSTOR Terms and Conditions September 1999] HERPETOLOGICA 333 and CNPq for a research fellowship; A. A. Giaretta lantic forests of Brazil (Amphibia: Leptodactyli- acknowledges CNPq for the graduate fellowship. dae). Proceedings of the Biological Society of Washington 99:100-109. LITERATURE CITED HEYER, W R., A. S. RAND, C. A. G. CRUZ, 0. L. PEIXOTO, AND C. E. NELSON. 1990. Frogs of Bor- CARDOSO, A. J., AND C. F. B. HADDAD. 1984. Var- ac6ia. Arquivos de Zoologia, Sao Paulo, 31:231-410. iabilidade acustica em diferentes e in- populag6es HODL, W, M. T. RODRIGUES, G. M. ACQAQIO, P. H. tera,coes agressivas de Hyla minuta (Amphibia, An- LARA, D. PAVAN, L. C. SCHIESARI, AND G. SKUK. ura). Ciencia e Cultura 36:1393-1399. 1997. Foot-flagging display in the Brazilian stream- CASTANHO, L. M. 1994. 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