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Breeding Biology and Advertisement Call of the Horned Leaf-Frog, Proceratophrys Appendiculata (Amphibia: Anura: Odontophrynidae)

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Breeding Biology and Advertisement Call of the Horned Leaf-Frog, Proceratophrys Appendiculata (Amphibia: Anura: Odontophrynidae) ZOOLOGIA 30 (4): 388–396, August, 2013 http://dx.doi.org/10.1590/S1984-46702013000400004 Breeding biology and advertisement call of the horned leaf-frog, Proceratophrys appendiculata (Amphibia: Anura: Odontophrynidae) Pedro Henrique dos Santos Dias1,2,4, Fabio Silva Fernandes dos Santos Hepp3, Ana Maria Paulino Telles de Carvalho e Silva2 & Sergio Potsch de Carvalho e Silva1 1 Instituto de Biologia, Universidade Federal do Rio de Janeiro. Avenida Brigadeiro Trompowsky, bloco A, Ilha do Fundão, 21941-590 Rio de Janeiro, RJ, Brazil. 2 Laboratório de Biossistemática de Anfíbios, Departamento de Zoologia, Universidade Federal do Estado do Rio de Janeiro. 22290-240 Rio de Janeiro, RJ, Brazil. 3 Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro. Quinta da Boa Vista, 20940-040 Rio de Janeiro, RJ, Brazil. 4 Corresponding author. E-mail: [email protected] ABSTRACT. We describe the breeding biology and the advertisement call of the horned leaf-frog, Proceratophrys appendiculata (Günther, 1873) in the Parque Nacional da Serra dos Órgãos, municipality of Teresópolis. The reproduc- tive period of P. appendiculata is short and is associated with the end of the winter and the beginning of the spring, when males call night and day under large rocks in sandy bottom rock streams. The amplexus is axillary and one female laid about 656 viscous eggs. The advertisement call of P. appendiculata is unique among congeners. The call lasts approximately two seconds, with about 85 pulses/call at a rate of 45 pulses/s and frequency around 0.620 kHz. It is one of the longest calls and lowest in dominant frequency. Moreover, the call of P. appendiculata is characterized by the greatest number of pulses so far registered, reaching 129 pulses in a single call. KEY WORDS. Atlantic Forest; calling activity; reproductive behavior. Breeding activity in most species of anurans begins with Two main phenetic groups are recognized within the emission of an advertisement call (GERHARDT 1994), which Proceratophrys according to the presence or absence of palpe- plays several roles in anuran reproductive behavior, for instance: bral appendages (CRUZ & NAPOLI 2010). Among the species that attract females to breeding sites, defend territories against other possess a long and single palpebral appendage are the species males, and stimulate female ovulation, among others (WELLS complexes of Proceratophrys appendiculata and P. boiei (IZECKSOHN 1977). et al. 1998, PRADO & POMBAL 2008, CRUZ & NAPOLI 2010). The advertisement call is species-specific, thus present- Proceratophrys appendiculata (Günther, 1873) is an en- ing an important mechanism of prezygotic reproductive isola- demic species of the southeastern Atlantic Forest, occurring tion (RYAN & RAND 1993, FUNK et al. 2009). Because of this amidst the leaf-litter (DIAS et al. 2013a). These are cryptic ani- property, the advertisement call and all behaviors associated mals (SAZIMA 1978) found scattered on the forest floor. Their with it are important tools in taxonomic (PADIAL et al. 2009, tadpoles develop in small streams inside the forest (DIAS & PADIAL & DE LA RIVA 2009, HEPP & CARVALHO-E-SILVA 2011) and CARVALHO-E-SILVA 2012). The breeding activity of the species is phylogenetic studies (COCROFT & RYAN 1995, ROBILLARD et al. 2006, poorly studied and its advertisement call has not been described. GOICOECHEA et al. 2010). The great morphological similarity observed among spe- The Neotropical Proceratophrys Miranda-Ribeiro, 1920 cies of P. appendiculata complex (PRADO & POMBAL 2008, DIAS et currently comprises 32 species distributed in Argentina, Bra- al. 2013a,b) and the discovery of several new species (CRUZ & zil, and Paraguay (ÁVILA et al. 2012, CRUZ et al. 2012, TEIXEIRA- NAPOLI 2010, ÁVILA et al. 2011, 2012, MARTINS & GIARETTA 2011, JR et al. 2012, DIAS et al. 2013a, FROST 2013, GODINHO et al. NAPOLI et al. 2011, CRUZ et al. 2012, TEIXEIRA-JR et al. 2012, DIAS et 2013). These species are commonly grouped within phenetic al. 2013a, GODINHO et al. 2013) – including cryptic species within groups or species complexes based on external morphologi- P. appendiculata (see DIAS et al. 2013a) – makes the description cal similarity (PRADO & POMBAL 2008, DIAS et al. 2013b), des- of the advertisement call of P. appendiculata very important pite molecular data indicating that these groups are not (MÂNGIA et al. 2010, DIAS et al. 2013b). Herein we describe the monophyletic (AMARO et al. 2009, TEIXEIRA-JR et al. 2012, DIAS advertisement call and aspects of the breeding biology of P. et al. 2013a). appendiculata. © 2013 Sociedade Brasileira de Zoologia | www.sbzoologia.org.br | All rights reserved. Breeding biology and advertisement call of the horned leaf-frog 389 MATERIAL AND METHODS Moura, Lacerda & Feio, 2013 – GODINHO et al. (2013); P. cururu Eterovick & Sazima, 1998 – ETEROVICK & SAZIMA (1998); P. The present study was conducted in the Parque Nacional concavitympanum Giaretta, Bernarde and Kokubum, 2000 – da Serra dos Órgãos (PARNASO), municipality of Teresópolis, SANTANA et al. (2010); P. cristiceps (Müller, 1883) – NUNES & JUNCÁ state of Rio de Janeiro, Brazil, from September 2004 to July (2006); P. huntingtoni Ávila, Pansonato & Strüssmann, 2012 – 2012, excepting the years of 2005 and 2007. We visited five ÁVILA et al. (2012); P. melanopogon (Miranda-Ribeiro, 1926) – breeding sites monthly for at least three nights and three days. MÂNGIA et al.(2010); P. moehringi Weygoldt & Peixoto, 1985 – During the breeding period, we stayed in the field for as long WEYGOLDT & PEIXOTO (1985); P. moratoi (Jim & Caramaschi, 1980) as the calling activity was taking place. Many other observa- – BRASILEIRO et al. (2008) and MARTINS & GIARETTA (2012); P. palustris tions were made sporadically in different dates and sites of the Giaretta & Sazima, 1993 – MARTINS & GIARETTA (2012); P. paviotii study area. We considered males calling, amplexed couples, Cruz, Prado & Izecksohn, 2005 – CRUZ et al. (2005); P. renalis egg clutches and tadpoles in initial development stage as indi- (Miranda-Ribeiro, 1920) – SANTANA et al. (2011); P. sanctaritae cators of breeding activity (GOSNER 1960, stages 25-26). Cruz & Napoli, 2010 – CRUZ & NAPOLI (2010); P. vielliardi Mar- Vocalizations were recorded with a Marantz PMD-670 tins & Giaretta, 2011 – MARTINS & GIARETTA (2011). and Tascam DR-07 digital recorders, at sample rate of 44.100 kHz and sample size of 16 bits and microphone Sennheiser RESULTS ME-67. The recordings were made in October, 2011 and Sep- tember, 2006 both with temperature of about 17.5°C. Sound Breeding Biology analyses and graphs were made with Raven Pro ver. 1.3 from The reproductive period of P. appendiculata was short and the Cornell Laboratory of Ornithology (Bioacoustics Research associated with the end of winter and spring, from July to Program). The following parameters were measured: call dura- November, although the males called only one or two months tion; number of pulses per call; pulse rate; pulse periods (mea- per year (Table I). sured from the beginning of one pulse to the beginning of the following one, thus encompassing the pulse duration and Table I. Month of calling activity of Proceratophrys appendiculata interpulse interval); dominant frequency; and fundamental per year in the period of 2004 to 2012. Breeding site not visited frequency. Numerical call parameters are given as a range, fol- in the years of 2005 and 2007. lowed by the Mean ± SD, Mode and N within parenthesis. Year Month The temporal parameters were measured directly from 2004 October the waveform and frequency parameters were measured directly from the audiospectrogram (with window function Hann, 2006 September amplitude logarithmic, window size 512 samples and overlap 2008 August 99%). We also counted the number of harmonically related 2009 September frequencies observed in the audiospectrogram and power spec- 2010 July and November trum (see HEPP et al. 2012). Technical terms and definitions 2011 October adopted follow LITTLEJOHN (2001) and HEPP & CARVALHO-E-SILVA (2011). Individuals recorded were collected, fixed in 10% forma- During the breeding season, males called continuously lin, and preserved in 70% ethyl alcohol. They are housed in at night and during the day in large choruses inside the forest, the Amphibian collection of the Laboratório de Biossistemática along shallow rocky streams with sandy bottoms (Fig. 1). Call- de Anfíbios of the Universidade Federal do Estado do Rio de ing activity began a few days after the first heavy rainfall within Janeiro (UNIRIO 2542-2543, 4471-4473) and in the Amphib- the period above mentioned. Males of P. appendiculata were ian collection of the Departamento de Zoologia of the only observed calling under large rocks or in small burrows Universidade Federal do Rio de Janeiro (ZUFRJ 8970-8971). The formed by vegetation and tree branches, always with their permit for collecting zoological material provided by Instituto bodies in contact with the water. Chico Mendes (ICMBio) and Instituto Brasileiro do Meio Males called at an approximately equal distance from Ambiente e dos Recursos Naturais e Renováveis (IBAMA) re- one another, which varied from one to two meters. A wave ceives the number12164-2. like chorus was observed along the streams, where one male Comparative acoustic data for other species were ob- called followed by the most adjacent male and so on down tained from the following references: Proceratophrys avelinoi and up the river. No satellite males were observed, and it seems Mercadal de Barrio & Barrio, 1993 – KWET & BALDO (2003) and that calling activity was also related to territorial defense. LIMA (2007); P. bigibbosa (Peters, 1872) and P. brauni Kwet & In a plot of 5 x 5 m, about eight to twelve males were Faivovich, 2001 – KWET & FAIVOVICH (2001); P. boiei (Wied- observed calling actively. This number decreased each day, and Neuwied, 1824) – HEYER et al. (1990); P. carranca Godinho, about three to four days after the first record of calling activ- ZOOLOGIA 30 (4): 388–396, August, 2013 390 P. H. dos S. Dias et al. ity, only two or three males were still calling.
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