Visual signaling and reproductive biology in a nocturnal treefrog, genus Hyla (Anura: Hylidae) Marília T. Hartmann, Paulo A. Hartmann, Célio F.B. Haddad Departamento de Zoologia, Instituto de Biociências, UNESP, Caixa Postal 199, 13506-900 Rio Claro, São Paulo, Brasil e-mail: [email protected] Abstract. We investigated reproductive activity, courtship behavior, call structure, body size, clutch size, oviposition site, and reproductive mode of Hyla sp. (aff. ehrhardti). Males called in all months, but showed a peak of activity during the rainy season. Three pair formations were observed and courtship involved stereotyped behavioral sequences, including visual signaling. Males emitted three different vocalization types: advertisement calls, courtship calls, and a vocalization of unknown function. Females attained larger body sizes than males and deposited an average of 74.5 unpigmented eggs per clutch. Early larval stages are aquatic but restricted to water in constructed subterranean nests; subsequent to flooding of nests, exotrophic tadpoles live in ponds or streams. Courtship behavior in Hyla sp. (aff. ehrhardti) is complex and the diverse repertoire of limb movements, exhibited by males, probably provide visual stimuli to females in this nocturnal treefrog. Hyla sp. (aff. ehrhardti) belongs to the H. albomarginata group. Considering the reproductive modes in this group, the complexes of H. albosignata and of H. albofrenata can be considered more close related to each other than to the H. albomarginata complex.

Introduction Studies on tropical and temperate frog species have revealed a surprising diversity of social systems (Wells, 1977a), but many aspects of courtship have been neglected (Wells, 1977b). Most examples of complex courtship behavior reported to date came from studies on dendrobatid frogs (e.g., Wells, 1977b; Limerick, 1980; Roithmair, 1992; Juncá, 1998), perhaps because these conspicuous diurnal frogs are more easily observed than most nocturnal frogs. Behavioral patterns related to visual communication vary greatly among anuran taxa and have been observed during both agonistic and courtship interactions (see review in Hödl and Amézquita, 2001). Visual signaling is predominantly employed by diurnal species at sites with an unobstructed view (Endler, 1992). Visual communication by diurnal anurans has been observed in the genera Brachycephalus (Brachycephalidae), Atelopus (Bu© Koninklijke Brill NV, Leiden, 2004 Also available online - www.brill.nl

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fonidae), Dendrobates (Dendrobatidae), Hylodes (Leptodactylidae), Taudactylus (Myobatrachidae), and Staurois (Ranidae) (see review in Lindquist and Hetherington, 1996). Nocturnal species that use visual signals are cited rarely in the literature, being known in the hylid genera Litoria (Richards and James, 1992), Phyllomedusa (Haddad and Giaretta, 1999), and Hyla (Kluge, 1981), in the centrolenid genus Hyalinobatrachium (MacDiarmid and Adler, 1974), and in the ranid genus Rana (Emlen, 1968; Wiewandt, 1969; Wells, 1978). The treefrog Hyla sp. (aff. ehrhardti) is a common and vocally conspicuous member of the anuran community in the north coast of São Paulo State, in the Brazilian Atlantic Rain Forest. It occurs in forested habitats where males call at night from hillsides close to flooded areas. Hyla ehrhardti (see Faivovich et al., 2002) is known only from Santa Catarina State, Brazil (Frost, 1985), and has different vocalizations from the species studied here (personal obs.). However, external morphology of specimens from São Paulo is very similar to that of the specimens from the type locality in Santa Catarina. According to Cruz and Peixoto (1985), H. arianae (now a synonym H. ehrhardti) belongs to the H. albofrenata complex, in the H. albomarginata group (Cruz and Peixoto, 1985). Since the description made by Cruz and Peixoto (1985), this species was only cited in one taxonomic article (Faivovich et al., 2002). According to Cruz and Peixoto (1984, 1985), the Hyla albomarginata group is divided in three complexes: Hyla albomarginata complex (H. albomarginata, H. rufitela), Hyla albosignata complex (Hyla albosignata, H. callipygia, H. fluminea, H. leucopygia, and H. cavicola), and Hyla albofrenata complex (Hyla albofrenata, H. musica, H. arildae, H. ehrhardti [= H. arianae], and H. weygoldti). Both H. albosignata and H. albofrenata complexes are restricted to the Brazilian Atlantic Forest (Cruz and Peixoto, 1984, 1985; Frost, 1985; Gomes and Peixoto, 1997). This group is predominantly South American, and possibly is related to the Hyla granosa group (Duellman, 2001), but the relationships among these species of Hyla are obfuscated by a dearth of information on tadpoles, life history, and behavior. Natural history of these green species are nearly unknown, with the exception of H. leucopygia (Heyer et al., 1990; Haddad and Sazima, 1992; Haddad and Sawaya, 2000). Anecdotal information can be found for H. albofrenata (Heyer et al., 1990), H. arildae (Haddad and Sazima, 1992), H. cavicola (Cruz and Peixoto, 1984), H. callipygia (Gomes and Peixoto, 1997), and H. albosignata (Haddad and Sawaya, 2000). Our objective is to provide information on reproductive activity, body size, oviposition site, and clutch characteristics of Hyla sp. (aff. ehrhardti), a member of the H. albofrenata complex (sensu Cruz and Peixoto, 1985). We also describe the courtship behavior, call, and reproductive mode of this treefrog.

Materials and methods The study was carried out at Núcleo Picinguaba (44◦ 50 W, 23◦ 23 S, 10-150 m above sea level), Parque Estadual da Serra do Mar, in the municipality of Ubatuba, State of São Paulo, southeastern Brazil. The study area is

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located in the Atlantic Rain Forest (Morellato and Haddad, 2000); climate is characterized by warm temperatures and high humidity throughout the year, without a pronounced dry season. The population was sampled for 15 months (January 2000-March 2001; 3-10 days each month) and additional data were collected in July 2002. Sequence sampling with continuous tape recording was used for behavioral observations (Altmann, 1974). Descriptions of behaviors were based on individuals observed and photographed in the field. Vocalizations were recorded using a UHER 4000 tape recorder and a UHER M518A cardioid microphone. Air temperature was measured at the time of each recording. Sonograms and oscillograms of the vocalizations were produced with the program Cannary (version 1.2.4). Height above the ground was visually estimated for all males. In order to identify individual males, frogs were fitted with belts containing different combinations of small colored balls. Trees used as calling sites were marked with colored tape, and examined during each trip. Voucher specimens of adults, embryos, and tadpoles of Hyla sp. (aff. ehrhardti) were deposited in Célio F.B. Haddad collection (CFBH), Departamento de Zoologia, I. B., UNESP, Rio Claro, SP, Brazil. Sex was determined for each preserved specimen based on gonad observation. We measured SVL of preserved specimens to the nearest 0.1 mm with a caliper ruler and weighed individuals to the nearest 0.01 g with a balance. Gravid females were dissected and mean number of ovarian eggs, ovarian egg diameter, and ovary mass were determined. Egg diameter was measured to the nearest 0.1 mm with an ocular micrometer in a Zeiss stereomicroscope.

Results Activity and calling sites Calling males of Hyla sp. (aff. ehrhardti) were registered in all months between January 2000 and July 2002, but they showed a peak of activity during the rainy season (NovemberMarch). Pair formation was observed in January, February, and July. Reproduction occurred in the forest; males began to call approximately one hour before dusk. During the dry season, males called from vegetation next to flooded areas, generally from bromeliads that were 2.0 to 10 m above the ground (mean = 5.0 m, s = 2.4, n = 29). However, during the rainy period, males frequently called from bromeliads or leaves closer to the ground (mean = 2.0 m from the ground, s = 1.09, range = 0.5-4 m, n = 13). Body size Mean SVL of males (mean SVL ± s = 33.02 ± 1.19 mm, range 31.21-34.8 mm, n = 14) was significantly smaller (t = 4.27, P = 0.0005) than that observed for females (mean SVL = 35.27 ± 0.61 mm, range 34.34-36 mm, n = 6). Mean body mass of females (without eggs) was significantly less than body mass of males (mean body mass of females = 1.87 ± 0.2, range 1.77-2.15, n = 6; mean body mass of males = 2.35 ± 0.31, range = 2.04-2.79, n = 12; t = 3.01, P = 0.009). Vocalizations Males emitted three different vocalization types: advertisement call, courtship call, and a vocalization of unknown function, here named multi-note call. The most common was the advertisement call given at a mean rate of 22 calls/min (s = 7.73, range = 12-37,

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n = 12) at an air temperature of 25◦ C. The advertisement call was composed of one note with three harmonics having frequencies between 0.8-3.7 kHz: first harmonic between 0.81.2 kHz; second harmonic between 2.1-2.5 kHz; and third harmonic between 3.3-3.7 kHz (fig. 1a). The mean duration of the advertisement call was 85.64 ms (s = 16.77, range = 53.88-114.9, n = 46). The courtship call was structurally identical to the advertisement call, but was emitted at a lower intensity. This vocalization was observed only when the male noticed an approaching female. The multi-note call was composed of two or three notes with harmonic structure, and was emitted sporadically during the night. The mean duration of the multi-note calls was 586.3 ms (s = 124.05, range = 503.8-729, n = 3). Frequency was emitted between 0.91-5.09 kHz: first harmonic between 0.91-1.29 kHz, second harmonic between 1.87-2.7 kHz, and third harmonic between 4.85-5.09 (fig. 1b). Notes had a mean duration of 64.93 ms (s = 15.66, range = 41.70-86.18, n = 9). Visual communication and courtship behavior Three pair formations were observed. Courtship involved stereotyped behavioral sequences, summarized as follows: the male emitted advertisement calls, and the female responded approaching the male. When the male noticed the female, it started to emit courtship calls, and both began to move the limbs up and down. Male and female started a stereotyped behavior, alternating positions, sometimes being face to face, sometimes side by side. The first observed pair was about 3 m above the ground, the second pair was about 1.5 m high, and the third pair was next to the ground, approximately 1.0 m high. Courtship behavioral sequences were similar for the three pairs observed during the study. The following detailed behavioral description is based on one pair observed in January 2000: A female jumped to the leaf where a male was calling, and both positioned face to face. When the female approached, the male emitted courtship calls, and raised one hind leg and then returned to the normal position (fig. 2a). The female approached the male slowly and the male made rapid vertical up and down hindlimb movements. Female and male turned face to face and touched each other’s snouts. Then, the male turned his back to the female and extended the leg that was at her side, and touched her body with his foot (fig. 2b). The male raised the other leg, and passed the leg and foot across his body (fig. 2c). Then, the male raised his arms alternately, passing them over his eyes, and touched his own body (fig. 2d). The female approached the male, and touched his dorsum with her snout (fig. 2e). The male turned to the female to be face to face, and moved his hindlimbs up and down. The female raised her head, in an upright posture (sensu Hödl and Amèzquita, 2001), and placed it on the male’s head. The male also raised his head, and both assumed an upright posture with their heads at the same level (fig. 2f). The male moved one of his leg rapidly up and down (fig. 2f). The female lowered her head and touched the male’s gular region with her snout (fig. 2g). The male walked to the edge of the leaf; the female followed him and touched the male’s back with her snout. Then, side by side, male and female sat with their legs

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Figure 1. Sonogram (upper) and oscilogram (lower) of vocalizations of Hyla sp. (aff. ehrhardti): (a) advertisement call (Tair = 21◦ C) and (b) multi-note call (Tair = 19◦ C). Picinguaba, Ubatuba, São Paulo, Brazil.

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close together and the male put his foot on the female’s foot. The female moved and face to face, lifted her head and touched the male’s head with her gular region. The male lifted his head, almost to the same height of the female’s head, and touching the female’s dorsum with a hand, he inflated his vocal sac without emitting any sound. The female touched the male’s dorsum with her hand (fig. 2h). The male walked toward the edge of the leaf; the female followed him and touched his dorsum with her snout. The female walked onto the male’s back, being in a position similar to amplexus but without grasping the male (fig. 2i). The male lowered his body and walked forward, leaving the female behind him. Then, the female walked in front of the male; the male lowered his head and touched the female’s vent with his snout, moving one of his legs up and down. The male changed his position to be side by side with the female. The female lowered her head, moved one of the legs up and down, and the male passed his hand slowly over the female’s dorsum (fig. 2j). The pair repeated many of the steps of the courtship described above. After two hours of courtship, the male jumped on to the tree trunk, and started to walk to the ground. The female followed him slowly and touched the male with her snout. The male jumped on a leaf next to the ground and the female remained motionless. The male started to emit courtship calls and moved the hindlimbs up and down alternately. As the female remained motionless, the male turned in her direction and continued the courtship call, increasing the speed of the up and down movements of the hindlimbs. The female jumped towards the male and the male emitted courtship calls while raising one of his legs. The female approached the male and they performed mutual touches repeatedly, touching each other’s dorsum with their hands, until the male vigorously beat his snout against the female’s head twice. The male jumped to another leaf, making slow up and down movements with his legs, and emitted courtship calls until the female approached him (fig. 2k). The male reached a soil bank and emitted courtship call continuously from the ground until the female touched him. The male entered a previously constructed subterranean nest, but left his toes outside the nest, moving them continuously (fig. 2l). The female followed the male into the nest, and the pair could no longer be observed. The courtship lasted approximately six hours from the female arrival until the pair entered in the nest. The female of the third pair was observed inspecting a nest (entered and exited several times); she refused to reproduce with the male who continued to call inside the nest. We tried to induce courtship behavior once by offering a gravid female to a vocalizing male. The male stopped calling and courtship did not occur. Nests characteristics A total of two nests were observed. They were subterranean and associated with flooded areas and temporary ponds inside the forest. Nests were built in muddy soil or banks near water bodies and had elliptical to nearly circular apertures, with a corridor connecting to a subterranean chamber. The bottom of the chambers contained water that permeated from

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Figure 2. Behavioral sequence of the courtship behavior of Hyla sp. (aff. ehrhardti). Picinguaba, Ubatuba, São Paulo, Brazil. See text for details.

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the natural water bodies. One nest measured 15 cm from the aperture to the bottom, a width of 6 cm in the interior of the chamber, and contained ca 5.0 cm of water on the bottom. Clutches Based on mature ovarian eggs, females deposited an average of 74.5 unpigmented eggs per clutch (s = 12.06, range = 62-88, n = 5). Egg diameter, without jelly, ranged from 1.952.87 mm (mean = 2.31, s = 0.22, n = 56). Correlations between clutch size and female SVL (r = 0.19, P = 0.8, n = 5), and between clutch size and mass of females (r = 0.93, P = 0.06, n = 5) were not significant. One clutch observed in the field contained 70 unpigmented eggs, and mean diameter of eggs was 2.42 mm (s = 0.19, range = 2.242.91). Reproductive mode Tadpoles of Hyla sp. (aff. ehrhardti) were observed and collected by day and night in ponds next to the chambers used for egg deposition. Heavy rains caused a rise in the water level and flooded the nests, allowing the tadpoles to escape from the chambers to natural water bodies. Based on our observations, Hyla sp. (aff. ehrhardti) exhibits the following reproductive mode: unpigmented eggs and early larval stages in water in constructed subterranean nests; subsequent to flooding, exotrophic tadpoles in ponds or streams.

Discussion The courtship behavior observed for Hyla sp. (aff. ehrhardti) is more elaborate than that documented for most frogs. Except for the visual signaling, the courtship behavior of Hyla sp. (aff. ehrhardti) seems to be equivalent to that reported for other hylids in the Hyla albosignata complex (see Haddad and Sawaya, 2000). Courtship behavior is simple in most hylids: males call from breeding sites and receptive females usually choose their mates (Wells, 1977a). In contrast, courtship in Hyla sp. (aff. ehrhardti) involves not only advertisement calls emitted by males, but also complex visual and tactile stimuli, performed by both the male and female. After attraction of the female by the advertisement call, courtship behavior in Hyla sp. (aff. ehrhardti) can be divided in three stages: (1) preliminary female choice, (2) interactive courtship, and (3) acceptance or refusal of the male and/or subterranean nest by the female. Preliminary female choice seems to be based on advertisement and courtship calls. During the interactive courtship stage, diverse and repetitive displays produced by the male seem to stimulate the female to mate and probably play an important role in the selection of males performed by females. Males and females perform complex series of movements during courtship, probably to stimulate the female, encouraging her to follow the male to the nest. In the third stage, the female may reject a calling male and follow another one. Sometimes

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the female will reject the male after visiting his subterranean nest. The nest site is selected by the male but can be rejected by the female. Oviposition only occurs subsequent to entry by the male and female into the subterranean nest. Teyssedre and Halliday (1986) characterized courtship as a system of tonic communication, in which the stimulating effects of the repeated display elements emitted by a male accumulate within the female until they exceed a threshold above which she becomes most likely to mate. Courtship displays of males affect the mating decision of females (Andersson, 1994); thus it seems reasonable that anurans employ more than one type of communication during reproductive interactions, such as vocalizations, visual signals, and mutual touches. Persuasive displays probably evolved through sexual selection (Darwin, 1871; Andersson, 1994), which favors traits that increase mating success either by direct competition for mates and/or by differential attractiveness to partners. Frogs communicate primarily through vocalizations emitted by males. A major advantage of acoustic communication is the potential for encoding multiple messages within the same signal (Gerhardt, 1992). However, visual signals are easier to locate at short distances, where localization of sound is less accurate (Marler, 1967). Among species in the Hyla albomarginata group, H. leucopygia exhibits elaborate courtship (Haddad and Sawaya, 2000), but occurrence of visual signaling has not been reported. In Hyla sp. (aff. ehrhardti) the diverse repertoire of limb movements exhibited by males probably provides visual stimuli to females. Courtship in Hyla sp. (aff. ehrhardti) has greater duration compared to other amphibians, even those with elaborate courtship (e.g., Bourne, 1997; Heying, 2001; Ovaska and Rand, 2001). The long interaction between males and females may have at least three purposes: (1) to evaluate the reproductive condition of the mate, because elaborate behavior may indicate physiological condition and individual attributes, influencing acceptance or refusal of the mate; (2) to stimulate ovulation, as relative long periods of courtship may be necessary to trigger ovulation (e.g., Bourne et al., 2001); and/or (3) to lead the female from the calling site to the nest passing obstacles such as leaves, trunks, and roots that could obstruct progress to the nest. It is possible that females require extended stimuli to follow males to the nests. Previous descriptions of the calls of Hyla sp. (aff. ehrhardti) are not available. The advertisement call is similar to those described for H. albofrenata, H. albosignata (Heyer et al., 1990), and H. leucopygia (Haddad and Sawaya, 2000). Advertisement calls are well separated single notes, exhibiting harmonics. The multi-note call seems common in these species, because it also occurs in H. leucopygia (Haddad and Sawaya, 2000), H. callipygia (C.F.B. Haddad, unpublished data), and H. albofrenata (Lutz, 1973). In H. leucopygia, multi-note calls appear to be associated with excavation of the subterranean nests (Haddad and Sawaya, 2000). However, for Hyla sp. (aff. ehrhardti) we observed males emitting multi-note calls sporadically during the night; nest construction was not observed for this species. Sexual dimorphism in size was evident for Hyla sp. (aff. ehrhardti) and, on average, females attain larger body sizes than males. Female fecundity is generally used to explain

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their larger sizes (Shine, 1979). Males were not observed defending territories suggesting that they are not territorial. Lack of territoriality in this species agrees with the smaller size of males compared to females, because large male size is highly correlated to territoriality in anurans (Shine, 1979). For Hyla sp. (aff. ehrhardti), clutch size was not correlated to body size, nor was body mass. However, our small sample size could have influenced the results. We did not observe males excavating nests, but this behavior probably is similar to that described for H. leucopygia, where males were observed constructing nests using the snout for excavation (Haddad and Sawaya, 2000). Subterranean nests may be important as shelters that protect adults, eggs, and embryos from aquatic predators, as well as from visually oriented terrestrial predators (Haddad and Sawaya, 2000). Furthermore, this type of nest may also provide protection to eggs or larvae against desiccation (e.g., Richards, 1993). The reproductive mode of Hyla sp. (aff. ehrhardti) is similar to that recorded for H. leucopygia by Haddad and Sawaya (2000), and probably is widespread among the species of the H. albosignata and H. albofrenata complexes. Hyla cavicola and H. callipygia (both in the H. albosignata complex) vocalize inside subterranean nets (Cruz and Peixoto, 1984, Gomes and Peixoto, 1997). In the H. albomarginata complex, the reproductive mode is more generalized; eggs are deposited as a surface film in shallow water, and exotrophic tadpoles were observed in lentic water bodies (H. albomarginata, pers. obs.; H. rufitela, Duellman, 2001). Considering the reproductive modes in the H. albomarginata group, just the complexes of H. albosignata and of H. albofrenata can be considered close related. On the other hand, the H. albomarginata complex, that shows a more generalized reproductive mode, seems not to be closely related to the two previously mentioned complexes.

Acknowledgements. We thank M.E. Oliveira, M.J.C. Gondin, and L.O.M. Giasson for field work assistance and C.P.A. Prado for the English version. This study was conducted with the permission of the Instituto Florestal, Parque Estadual da Serra do Mar, Núcleo Picinguaba. Field collections of treefrogs were made under permit of the Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis — IBAMA. This study is part of the Ph. D. Thesis of the first author at the Programa de Pós — Graduação em Biologia, Área de Zoologia, Universidade Estadual Paulista, UNESP, Campus de Rio Claro. Financial support was provided by Fundação O Boticário de Proteção à Natureza/MacArthur Foundation and FAPESP. The authors are grateful to CNPq and Capes for the fellowships.

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Cruz, C.A., Peixoto, O.L. (1984): Espécies verdes de Hyla: o Complexo “Albosignata” (Amphibia, Anura, Hylidae). Arq. Univ. Fed. Rur. Rio de J. 7: 31-47. Cruz, C.A., Peixoto, O.L. (1985): Espécies verdes de Hyla: o Complexo “Albofrenata” (Amphibia, Anura, Hylidae). Arq. Univ. Fed. Rur. Rio de J. 8: 59-70. Darwin, C. (1871): The Descent of Man, and Selection in Relation to Sex. London, John Murray. Duellman, W.E. (2001): Hylid Frogs of Middle America. Ithaca, New York, Society for the Study of Amphibians and Reptiles. Emlen, S.T. (1968): Territoriality in the bullfrog, Rana catesbeiana. Copeia 1968: 240-243. Endler, J.A. (1992): Signal, signal conditions and the direction of evolution. American Naturalist 139: S36-S61. Faivovich, J., Cruz, C.A.G., Peixoto, O.L. (2002): Identifity of Hyla ehrhardti Muller, 1924 (Anura, Hylidae). J. Herpetol. 36: 325-327. Frost, D.R. (1985): Amphibians Species of the World. A Taxonomic and Geographical Reference. Lawrence, Kansas, Allen Press Inc. & Assoc. Syst. Coll. Gerhardt, H.C. (1992): Multiple messages in acoustic signals. Seminars in the Neurosciences 4: 391-400. Gomes, M.R., Peixoto, O.L. (1997): Hyla callipygia (Bocaina Treefrog). Herpet. Rev. 28: 92-93. Haddad, C.F.B., Giaretta, A.A. (1999): Visual and acoustic communication in the Brazilian Torrent Frog, Hylodes asper (Anura: Leptodactylidae). Herpetologica 55: 324-333. Haddad, C.F.B., Sawaya, R. (2000): Reproductive modes of Atlantic Forest hylid frogs: a general overview and description of a new mode. Biotropica 32: 862-871. Haddad, C.F.B., Sazima, I. (1992): Anfíbios anuros da Serra do Japi. In: História natural da Serra do Japi. Ecologia e preservação de uma área florestal no Sudeste do Brasil, p. 188-210. Morellato, L.P.C., Org., Campinas, Unicamp/Fapesp. Heyer, W.R., Rand, A.S., Cruz, C.A.G., Peixoto, O.L., Nelson, C.E. (1990): Frogs of Boracéia. Arq. Zool. 31: 231-410. Heying, H.E. (2001): Social and reproductive behaviour in the Madagascar poison frog, Mantella laevigata, with comparisons to the dendrobatids. Anim. Behav. 61: 567-577. Hödl, W., Amèzquita, A. (2001): Visual signaling in anuran amphibians. In: Anuran Communication, p. 121-141. Ryan, M.J., Ed., Washington and London, Smithsonian Institution Press. Juncá, F.A. (1998): Reproductive biology of Colostethus stepheni and Colostethus marchesianus (Dendrobatidae), with the description of a new anuran mating behavior. Herpetologica 54: 377-387. Kluge, A.G. (1981): The life history, social organization, and parental behavior of Hyla rosenbergi, a nest building gladiator frog. Michigan, Miscellaneious Publications, Museum Zoology, University of Michigan. Limerick, S. (1980): Courtship behavior and oviposition of the poison-arrow frog Dendrobates pumilio. Herpetologica 36: 69-71. Lindquist, E.D., Hetherington, T.E. (1996): Field studies on visual and acoustic signaling in the “earless” Panamian golden frog, Atelopus zeteki. J. Herpetol. 30: 347-354. Lutz, B. (1973): Brazilian species of Hyla. Austin, Texas, Univ. Texas Press. MacDiarmid, R.W., Adler, K. (1974): Notes on territorial and vocal behavior of neotropical frog of the genus Centrolenella. Herpetologica 30: 75-78. Marler, P. (1967): Animal communication signals. Science 157: 769. Morellato, L.P.C., Haddad, C.F.B. (2000): Introduction: The Brazilian Atlantic Forest. Biotropica 32: 786-792. Ovaska, K., Rand, A.S. (2001): Courtship and reproductive behavior of the frog Eleutherodactylus diastema (Anura: Leptodactylidae) in Gamboa, Panama. J. Herpetol 35: 44-50. Richards, S.J. (1993): Functional significance of nest construction by an Australian rainforest frog: a preliminary analysis. Mem. Qd. Mus. 34: 89-93. Richards, S.J., James, C. (1992): Foot-flagging displays of some Australian frogs. Mem. Qd. Mus. 32: 302. Roithmair, M.E. (1992): Territoriality and male mating success in the dart-poison frog, Epipedobates femoralis (Dendrobatidae, Anura). Ethology 92: 331-343. Shine, R. (1979): Sexual selection and sexual dimorphism in the Amphibia. Copeia 1979: 297-306. Teyssedre, C., Halliday, T. (1986): Cumulative effect of male’s displays in the sexual behaviour of the smooth newt Triturus vulgaris (Urodela, Salamandridae). Herpetological Monographs 10: 1-42. Wells, K.D. (1977a): The social behaviour of anuran amphibians. Anim. Behav. 25: 666-693.

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Received: December 30, 2002. Accepted: October 9, 2003.