Advertisement Call, Vocal Activity, and Geographic Distribution of Brachycephalus Hermogenesi (Giaretta and Sawaya, 1998) (Anura, Brachycephalidae)

Advertisement Call, Vocal Activity, and Geographic Distribution of Brachycephalus hermogenesi (Giaretta and Sawaya, 1998) (Anura, Brachycephalidae)

1 VANESSA K. VERDADE, MIGUEL T. RODRIGUES,JOSE´ CASSIMIRO,DANTE PAVAN,NORALY LIOU, AND MARTHA C. LANGE

Departamento de Zoologia, Instituto de Biocieˆncias, Universidade de Sa˜o Paulo, Caixa Postal 11461, CEP 05422–970, Sa˜o Paulo, Brazil

ABSTRACT.—Brachycephalus hermogenesi is an endemic leaf litter inhabitant of the Atlantic forest of southeastern Brazil, whose original distribution included a restricted area near the boundaries of the States of Saõ Paulo and Rio de Janeiro. We were surprised to find out, while conducting herpetofaunal surveys at Estaçaõ Biolo´gica de Boraceía (EBB), that the background forest insect–like sound we have been searching for corresponded to calling individuals of the species. Males call during the day at high densities, hidden under the leaf litter. Individuals do not answer playback, seem to move very infrequently, and seem to ignore nearby calling activity. We gathered data on annual and daily vocal activity of the species at EBB, observing a total of 1,549 calls given by 31 focal individuals in November 2003 and 2005. The call varies from short single note calls to calls composed of groups of two to seven similar notes emitted at regular intervals. We also extend the known distribution of the species southward to the State of Saõ Paulo.

Brachycephalus hermogenesi is a member of the ossification (absent in Brachycephalus alipioi, family Brachycephalidae as recently rearranged Brachycephalus brunneus, and Brachycephalus to include the genus Brachycephalus and species izecksohni, Ribeiro et al., 2005; Pombal and formerly placed in the subfamily Eleutherodac- Gasparini, 2006), originally described in the tylinae of the family Leptodactylidae (for details genus Brachycephalus (Izecksohn, 1971; Pombal on major changes in frog taxonomy see Frost et et al., 1998). The other assembles leptodactylid- al., 2006, Grant et al., 2006). The family is form, dull colored species, without ossified presently defined only by molecular synapo- structures on dorsum, formerly attributed to morphies because no morphological characters the genus Psyllophryne (Izecksohn, 1971; Giar- proved to be unique to sustain the group (Frost etta and Sawaya, 1998). Brachycephalus and et al., 2006). Species of Brachycephalidae share Psyllophryne were considered synonyms by similar natural history habits and reproductive Kaplan (2002) based on the histology of scapu- mode: most species are leaf litter inhabitants, lar girdle that revealed the presence of an lay large terrestrial eggs, and have direct omosternum in Brachycephalus, putting down development (Lynch, 1971; Frost et al., 2006). the single published character differentiating The genus Brachycephalus includes 11 species, the genera, omosternum present in Psyllophryne all endemic to the Atlantic forest of eastern and absent in Brachycephalus. Our preliminary Brazil (Frost, 2007; Sociedade Brasileira de molecular studies suggest it was an assertive Herpetologia, 2007). These species present decision (T. Mott, V. K. Verdade, M. T. diminutive size (e.g., Brachycephalus didactylus Rodrigues, and J. Cassimiro, unpubl. data). has been considered one of the smallest terres- Brachycephalus hermogenesi (Fig. 1) belongs to trial vertebrate, not reaching 10 mm; Estrada the dull colored assemblage. The species was and Hedges, 1996), digital reduction, sternum originally described from Picinguaba, at the absent, and epicoracoid cartilages ossified and Parque Estadual da Serra do Mar, with distri- fused to the coracoids and clavicles (Izecksohn, bution records restricted to Ubatuba municipal- 1971; Pombal et al., 1998). ity of the State of Saõ Paulo, and Parati The monophyly of the genus has not been municipality in the adjacent State of Rio de adequately tested, and relationships among the Janeiro. The species was later collected in two species are also unclear. There are two informal new localities in the plateau of State of Saõ and similarity based groups of species. The first Paulo: Estaçaõ Biolo´gica de Boraceía and Re- assembles bufoniform species, generally bear- serva Florestal de Morro Grande (Dixo and ing bright colors, and most presenting dorsal Verdade, 2006; Pimenta et al., 2007). In 2003, while conducting herpetofaunal surveys at 1 Corresponding Author. E–mail: [email protected] Estaçaõ Biolo´gica de Boraceía (EBB), the most VOCAL ACTIVITY OF BRACHYCEPHALUS HERMOGENESI 543

frogs at 70% of them. Unfortunately, this method is biased to favor male collection. The specimens were identified by comparison to the type series and original descriptions. Appendix 1 lists specimens examined and vouchers deposited at the Museu de Zoologia da Universidade de Saõ Paulo (MZUSP). The abbreviations for the herpetological collections consulted are as follows: MD and TP (M. Dixo private collection); MZUSP (Museu de Zoologia da Universidade de Saõ Paulo); ZUEC (Museu de Histo´ria Natural da Universidade de Cam- pinas-UNICAMP). Calling activity was studied on two occasions (November 2003 and November 2005), both at the EBB. Calling individuals were heard and FIG.1. Brachycephalus hermogenesi. Live specimen collected along the Pump trail (‘‘trilha da collected at Estaçaõ Biolo´gica de Boraceía, State of bomba’’) at EBB, extending from behind the Saõ Paulo. guest house to the Pump stream. Calls were recorded using a tape recorder (Sony TCM 5000–EV) and a Sennheiser ME–66 directional intensively studied frog site in the Atlantic microphone. The microphone was placed 70 cm forest of southern Brazil, our interest was in front of the calling frog. The tape recordings directed to discover the source of a very were digitized at a sampling frequency of common diurnal acoustic signal that did not 44.1 kHz and 16 bits resolution using Sound respond to playback experiments. To our Ruler Software version 0.9.6.1 (Gridi-Papp, surprise, the call turned out to be conveyed by 2007). In an effort to detect variation in some B. hermogenesi, a species until then unrecorded of the parameters of the advertisement call of from EBB. Our discovery led us to gather data the species, 31 focal individuals were observed on natural history and variation of vocal activity for 10 min while calling. We considered a call to of the species. In this paper, we present these be a group of notes conveyed by the same new data as well as new locality records, individual at regular intervals. Additionally, extending its geographical distribution. from February 2003 to August 2004, we visited EBB monthly and estimated the total number of MATERIALS AND METHODS calling males along the Pump trail on one randomly chosen day for each seven-day trip. We collected B. hermogenesi at EBB (23u389S, To quantify the temporal and spectral features 45u509W) and Juquitiba (23u579S, 47u039W), in of the advertisement call, we generated audio the State of Saõ Paulo. Additionally, while spectrograms, oscillograms, and power spectra. examining the herpetological collection of Sound units produced by a single contraction of MZUSP, we found specimens from Estaçaõ the body wall were considered notes. The Ecolo´gica de Jureía–Itatins (24u279S, 47u149W). acoustic variables considered were call dominant We also had the opportunity to examine the frequency, call length, call rate, call rise time, material under study by T. H. Condez, R. T. number of notes per call, and note repetition rate. Bruscagin, and M. Dixo that revealed the Acoustic terminology follows Cocroft and Ryan presence of B. hermogenesi in Ribeiraõ Grande (1995). Means are given 6 1 SD. (24u059S, 48u229W) and Tapiraı´ (23u579S, To understand the pattern of distribution of 47u309W) (unpubl. data). calling individuals and the calling activity during The herpetofaunal surveys were conducted the day, 10 spots (P1 to P10) were selected along using active collection during the day and night, the trail. During four days (7 and 8 November and pitfall traps. The pitfall traps were placed in 2003; 27 and 28 November 2005), in one-hour series of six stations, four pitfalls each, using a intervals (from 0600–1700 h), the number of linear or star configuration (for details on pitfall calling individuals at each spot was estimated trap methodology, see Heyer et al., 1994) at five on the basis of data obtained simultaneously by different sampling points inside EBB (Pump two observers previously trained to estimate trail A and B, Pilo˜es, and Guaratuba road A and calling individuals. The spots were chosen based B). The best way to collect these frogs was to on declivity, depth of leaf litter, and type of select the probable area of the calling site, and vegetation coverage and were separated by a collect the leaf litter. At the laboratory, we minimum distance of 150 m. P1 and P2 were searched each leaf litter sample twice and found located in areas with low inclination, shallow leaf 544 V. K. VERDADE ET AL.

FIG. 2. Collecting sites of Brachycephalus hermogenesi: (1) Parati, State of Rio de Janeiro, (2) Picinguaba, (3) Estaçaõ Biolo´gica de Boraceía, (4) Reserva Biolo´gica de Paranapiacaba, (5) Reserva Florestal do Morro Grande, (6) Juquitiba, (7) Estaçaõ Ecolo´gica Jureía-Itatins, (8) Tapiraı´, and (9) Ribeiraõ Grande, State of Saõ Paulo (SP). Open symbol indicate extended distribution. MG: State of Minas Gerais. PR: State of Parana´. RJ: Rio de Janeiro. litter, and many terrestrial bromeliads. P3 and P4 leaf litter at EBB and Reserva Biolo´gica de were located in areas with medium inclination, Paranapiacaba. The call is similar to that of shallow leaf litter, and covered by a complex Leptodactylus marmoratus (Heyer et al., 1990; system of stems. P5, P6, P7, and P8 were located Haddad et al., 2001), but it sounds insect-like, in flat areas with deep leaf litter and few acuter, weaker, and usually constituted by a terrestrial bromeliads. P9 and P10 were near the group of four similar notes emitted in regular Pump stream, in areas with low declivity, deep time (pic-pic-pic-pic). The abundance of calling leaf litter, and covered by bamboo. individuals of B. hermogenesi at EBB was very high (Fig. 3), their advertisement call being the background sound in the forest during the day. RESULTS Calling individuals do not answer playbacks and Including the new localities, and that from seem to ignore nearby calling activity. We Reserva Biolo´gica de Paranapiacaba, Santo observed individuals calling about 6 cm from Andre´ (23u479S, 46u199W; Verdade et al., in each other, with no detectable variation observed press), the range of the species (Pimenta et al., in calling pattern in the field. The calling 2007) was extended approximately 120 km individuals reacted to disturbances caused by southward and 180 km westward in the State the observer and stopped calling even on careful of Saõ Paulo, including areas from sea level up approaches 1–2 m from the calling sites. It was to 800 m (Fig. 2). We also found a specimen impossible to see individuals calling on the forest from Ilha do Cardoso (25u089S, 47u589W) at the floor, and all our attempts to record and collect MZUSP collection that may refer to B. hermo- vouchers failed. The only visual-acoustic record genesi, but we hesitate to extend further the associated with a voucher was obtained with a range of the species as the specimen is young frog constrained inside a plastic bag (MZUSP and in poor condition. 138345, snout–vent length 5 8mm). Individuals were found calling during the day The specimens seem to move very infrequently. and night on the forest floor, hidden under the Apparently, the same individual was observed at VOCAL ACTIVITY OF BRACHYCEPHALUS HERMOGENESI 545

FIG. 3. Average estimated number of calling individuals of Brachycephalus hermogenesi at each of the 10 sites studied from November 2003 and November 2005 at Estaçaõ Biolo´gica de Boraceía. the same place in successive days. This opinion is recordings are similar in terms of call dominant also supported by our collecting data. We are frequency (6.8 kHz 6 0.8; N 5 5). The call aware that these frogs may escape the pitfalls, but length varies along with the number of notes, in such a high density, we expected a few 0.2 sec 6 0.01 for single-note calls (N 5 22), individuals captured in pitfall traps. Despite the 1.4 sec 6 0.13 for four notes complex calls (N 5 commonness of the call we collected only two 2), and 1.9 6 0.26 for five notes complex calls (N individuals with pitfalls during our two years of 5 3). The call rise time is 0.01 sec; the call rate is fieldwork at EBB (almost 14,000 buckets/day). 0.19 calls per sec; and the note repetition rate is Along the trail we studied, frogs were more 1.09 per sec. The notes are very similar and common in areas with dense soil coverage, decrease in intensity if located at the end of especially with abundant falling branches and complex calls. logs (P3, P4, P9, P10) or deep leaf litter (P6, P7, P8). Their abundance was lower in areas with extensive coverage of terrestrial bromeliads DISCUSSION (Fig. 3). There was a slight decrease in vocal Brachycephalus hermogenesi seemed to be the activity between 1000 h and 1200 h and after most common frog of the leaf litter anuran 1600 h in 2003, but the pattern was not found in community at EBB during our field observa- 2005 (Fig. 4). We heard a few scattered individ- tions. This high density is congruent with the uals calling during the night as well. one reported for B. didactylus at Ilha Grande, We observed a total of 562 calls given by 14 State of Rio de Janeiro (Van Sluys et al., 2001), individuals in November 2003, and 987 calls and for other species in the genus (Ribeiro et al., given by 17 individuals in November 2005. The 2005). This is surprising, especially considering frogs call all year long at EBB, with a significant that they were first recorded at EBB in 2003 (D. decrease in calling activity during April to July, Pavan, M. T. Rodrigues, V. K. Verdade, unpubl. corresponding to the driest and coldest seasons data), one of the best surveyed localities for (Fig. 5). The calls may be simple, constituted by frogs of the Atlantic forest. The EBB has also a single note, or complex, composed of groups experienced frog population declines between of two to seven similar notes (Fig. 6). The most 1979 and 1981 (Heyer et al., 1988, 1990; Bertoluci common calls were the simple and the four and Heyer, 1995). Some of the species affected notes complex call (Fig. 7). We only have good by the declines were Leptodactylus marmoratus, records from five complex calls given by the Eleutherodactylus guentheri, and Eleutherodactylus same male, unfortunately not captured. All parvus, all with terrestrial reproduction, the first 546 V. K. VERDADE ET AL.

FIG. 4. Average estimated number of calling individuals of Brachycephalus hermogenesi per hour during data collection from November 2003 and November 2005 at Estaçaõ Biolo´gica de Boraceía. with endotrophic tadpoles and the others, direct ephippium (Pombal et al., 1994; Pombal, 1999), developers. Considering that B. hermogenesi pre- we might not expect such high abundances. It sent terrestrial reproduction, possibly with direct may be that the species went unnoticed at EBB development, as observed for Brachycephalus before the declines, its call was misidentified as

FIG. 5. Total estimated number of male Brachycephalus hermogenesi calling along the Pump trail at Estaçaõ Biolo´gica de Boraceía from February 2003 to August 2004. VOCAL ACTIVITY OF BRACHYCEPHALUS HERMOGENESI 547

FIG. 6. Sequence of five advertisement calls of Brachycephalus hermogenesi (Estaçaõ Biolo´gica de Boraceía; air temperature 20uC; voucher not captured): (A) Oscillogram of the sequence, (B) Oscillogram, (C) Spectrogram, and (D) Power spectrum of the first call of the sequence.

FIG. 7. Distribution of number of notes per call given by males of Brachycephalus hermogenesi during the observations made in November 2003 (562 calls of 14 males) and November 2005 (987 calls of 17 males) at Estaçaõ Biolo´gica de Boraceía. 548 V. K. VERDADE ET AL. that of an insect, or it arrived in the area after the T. H. Condez, and R. T. Bruscagin for sharing declines. One possible way to check for its unpublished data; P. Narvaes and the anony- presence and possibly its abundance before the mous reviewers who critically read the manu- population declines at EBB would be to check script; the Instituto de Biocieˆncias da Universi- bird call recordings made at the station prior to dade de Saõ Paulo (IB-USP) and MZUSP for 1979. We would expect to hear its call in the logistics; the Fundaçaõ de Amparo a` Pesquisa background of sound recordings if B. hermogenesi do Estado de Saõ Paulo (FAPESP) for financial were present before declines in such high support; and the Brazilian environmental orga- numbers as it currently occurs. nization, IBAMA, for collection permits. The advertisement call of B. hermogenesi is very distinct from that of B. ephippium (Pombal et al., 1994; Haddad et al., 2001), the only other LITERATURE CITED Brachycephalus species for which there is a call ALVES, A. C. R., L. F. RIBEIRO,C.F.B.HADDAD, AND S. F. description available. The call sounds like a buzz REIS. 2006. Two new species of Brachycephalus in B. ephippium, is much longer (2–6 min), is (Anura: Brachycephalidae) from the Atlantic forest ´ composed of notes with five to 15 pulses, and in the Parana State, Southern Brazil. Herpetologica 62:221–233. emphasizes frequencies ranging from 3.4– BERTOLUCI, J., AND W. R. HEYER. 1995. Boraceía update. 5.3 kHz (Pombal et al., 1994). Heyer et al. (1990) Froglog 14:3. described the call of Brachycephalus nodoterga as a COCROFT, R. B., AND M. J. RYAN. 1995. Patterns of weak buzz but were not able to locate calling advertisement call evolution in toads and chorus individuals. Ribeiro et al. (2005) heard the frogs. Animal Behaviour 49:283–303. advertisement calls of B. brunneus and B. DIXO, M., AND V. K. VERDADE. 2006. Herpetofauna da izecksohni and Alves et al. (2006) those of serrapilheira da Reserva de Morro Grande, Cotia, Brachycephalus ferruginus and Brachycephalus pom- Saõ Paulo. Biota Neotropica 6. Accessed 21 May bali but did not describe them along with the 2006. Available at http://www.biotaneotropica. + species descriptions. From the information on org.br/v6n2/pt/abstract?article bn00706022006. ESTRADA, A. R., AND S. B. HEDGES. 1996. At the lower natural history available (Heyer et al., 1990; size limit in tetrapods: a new diminutive frog from Pombal et al., 1994; Ribeiro et al., 2005; Alves et Cuba (Leptodactylidae: Eleutherodactylus). Copeia al., 2006), it is worth noting that the species 1996:852–859. behave differently while calling: B. nodoterga and FROST, D. R. 2007. Amphibian Species of the World: an B. hermogenesi hide under the leaf litter; and B. Online Reference. Version 4.0. American Museum brunneus, B. ephippium, B. ferruginus, B. izecksohni, of Natural History, New York. Accessed 23 and B. pombali remain exposed. One would October 2007. Available at http://research.amnh. expect these differences to be related to color org/herpetology/amphibia/index.html. pattern (the brightly colored species calling FROST, D. R., T. GRANT,J.FAIVOVICH,R.H.BAIN,A. ´ while exposed, and the dull colored species HAAS,C.F.B.HADDAD,R.O.DE SA,A.CHANNING, M. WILKINSON,S.C.DONNELLAN,C.J.RAXWORTHY,J. calling while hidden under the leaf litter), but A. CAMPBELL,B.L.BLOTTO,P.MOLER,R.C.DREWES, this is not the case. The bright colored species call R. A. NUSSBAUM,J.D.LYNCH,D.M.GREEN, AND W. while exposed, but among the dull colored ones, C. WHEELER. 2006. The amphibian tree of life. the males call either while hidden or exposed. Bulletin of the American Museum of Natural Such a pattern may result from different evolu- History 297:1–370. tionary histories among members of the genus GIARETTA, A. A., AND R. J. SAWAYA. 1998. Second species and needs to be explored further. of Psyllophryne (Anura: Brachycephalidae). Copeia The new data presented is congruent to the 1998:985–987. proposal of Pimenta et al. (2007) that would GRANT, T., D. R. FROST,J.P.CALDWELL,R.GAGLIARDO,C. F. B. HADDAD,P.J.R.KOK,D.B.MEANS,B.P. change the status of the species at the Global NOONAN,W.E.SCHARGEL, AND W. C. WHEELER. 2006. Amphibian Assessment (GAA) list (International Phylogenetic systematic of dart-poison frogs and Union for Conservation of Nature et al., 2006) their relatives (Amphibia: Athesphatanura: Den- from ‘‘vulnerable’’ (VU) to ‘‘Least Concern’’ (LC). drobatidae). Bulletin of the American Museum of Natural History 299:1–262. Acknowledgments.—We are thankful to all GRIDI-PAPP, M. 2007. Sound Ruler. Accessed 3 October graduate students (more than 20) who were 2007. Available at http://soundruler.sourceforge.net. part of the field trip that collected the data HADDAD,C.F.B.,J.G.R.GIOVANELLI,L.O.M.GIASSOM, AND presented, especially to G. R. R. Brito, who tape L. F. TOLEDO. 2001. Guia Sonoro dos Anfı´bios Anuros recorded the calls. We also thank F. M. Souza da Mata Atlaˆntica. Sound Guide of the Atlantic Forest Anurans. Biota Fapesp, Saõ Paulo, Brazil. and E. R. Bilo for granting access to the type HEYER, W. R., A. S. RAND,C.A.G.CRUZ, AND O. 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