Journal of Herpetology, Vol. 42, No. 3, pp. 542–549, 2008 Copyright 2008 Society for the Study of Amphibians and Reptiles 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 Sa˜o Paulo and Rio de Janeiro. We were surprised to find out, while conducting herpetofaunal surveys at Estac¸a˜o Biolo´gica de Borace´ia (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 Sa˜o 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 Sa˜o 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 Sa˜o and similarity based groups of species. The first Paulo: Estac¸a˜o Biolo´gica de Borace´ia 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] Estac¸a˜o Biolo´gica de Borace´ia (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 Sa˜o 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 Sa˜o 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 Estac¸a˜o Biolo´gica de Borace´ia, State of bomba’’) at EBB, extending from behind the Sa˜o 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 Sa˜o 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 Estac¸a˜o the body wall were considered notes. The Ecolo´gica de Jure´ia–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 Ribeira˜o 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) Estac¸a˜o Biolo´gica de Borace´ia, (4) Reserva Biolo´gica de Paranapiacaba, (5) Reserva Florestal do Morro Grande, (6) Juquitiba, (7) Estac¸a˜o Ecolo´gica Jure´ia-Itatins, (8) Tapiraı´, and (9) Ribeira˜o Grande, State of Sa˜o 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.