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Natural History of Holoaden Luederwaldti (Amphibia: Strabomantidae: Holoadeninae) in Southeastern of Brazil

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Natural History of Holoaden Luederwaldti (Amphibia: Strabomantidae: Holoadeninae) in Southeastern of Brazil ZOOLOGIA 27 (1): 40–46, February, 2010 Natural history of Holoaden luederwaldti (Amphibia: Strabomantidae: Holoadeninae) in southeastern of Brazil Itamar A. Martins Laboratório de Zoologia, Universidade de Taubaté. Avenida Tiradentes 500, 12030180 Taubaté, São Paulo, Brasil. Email: [email protected] ABSTRACT. This study reports the rediscovery of Holoaden luederwaldti Miranda-Ribeiro, 1920 and provides information on the distribution, sexual dimorphism, reproduction and vocalization of a population of this species in Campos do Jordão, São Paulo (southeastern Brazil). Sampling was carried out in the Parque Estadual de Campos do Jordão (PECJ) from October 2005 through December 2008. Collecting was conducted using pitfall traps with a drift-fence on different altitudinal gradients (1,540 m, 1,780 m and 2,000 m a.s.l.). Fifty-two specimens of H. luederwaldti were collected in the PECJ. The mean snout-vent length (SVL) was 36.17 mm for males and 42.61 mm for females, indicating sexual dimor- phism in body size. Holoaden luederwaldti occurred during the warm-rainy months. The population was distributed between 1500 and 2000 m, and the greater abundance was registered in well preserved forest areas. Mature females contained from 36 to 41 oocytes and the mean of oocyte diameter was 3.72 mm. The advertisement call of H. luederwaldti consists of simple notes composed of three harmonics. The record of the population of H. luederwaldti in the PECJ has reinforced the importance of investigating different areas of the forest when conducting faunal surveys. KEY WORDS. Advertisement call; Atlantic forest; fecundity; Holoaden; use of habitat. The anuran Strabomantidae HEDGES et al. (2008) contains Due to uncertainties about the distribution, status and 18 genera with 553 species, divided into two subfamilies, ecological requirements of H. luederwaldti this species was clas- Strabomantinae and Holoadeninae. Holoadeninae includes six sified as “data deficient” (DD) in the List of Threatened Brazil- genera – Noblella Barbour, 1930, Euparkella Griffits, 1959, ian Fauna (HADDAD 2005), in the list of threatened wild species Bryophryne Hedges, Duellman and Heinicke, 2008, of the state of São Paulo (SÃO PAULO 2008, Decreto 53.494), and Psychophrynella Hedges, Duellman and Heinicke, 2008, in the IUCN Red List (CRUZ & PEIXOTO 2004) . In the Red List of Barycholos Heyer, 1969, and Holoaden Miranda-Ribeiro, 1920 – the state of Rio de Janeiro (CARAMASCHI et al. 2000), H. luederwaldti with 40 species occurring in South America (HEDGES et al. 2008, is listed as “vulnerable”. FROST 2009). Euparkella and Holoaden are endemic to the Atlan- HADDAD (2005) noted that many species that are presently tic Forest in southeast Brazil (HEDGES et al. 2008). classified as “DD” may not be really threatened. Therefore, a Holoaden contains three species – Holoaden luederwaldti strong effort is necessary to evaluate the real situation of DD Miranda-Ribeiro, 1920, Holoaden bradei B. Lutz, 1958, and species in nature and expand knowledge of their distribution Holoaden pholeter Pombal, Siqueira, Dorigo, Vrcibradic and Rocha, and habitats (HADDAD 2005) by means of intensive field studies. 2008 – endemic to the montane Atlantic Forest (between 1,200 This study reports on the rediscovery of a population of and 2,500 m a.s.l.) of the states of São Paulo, Minas Gerais, and H. leuderwaldti in the Parque Estadual de Campos do Jordão Rio de Janeiro (LUTZ 1958, CRUZ & PEIXOTO 2004, POMBAL-JR et al. (PECJ), municipality of Campos do Jordão, state of São Paulo, 2008).Even though the first specimen of H. luederwaldti was col- southeastern Brazil. Information about sexual dimorphism, re- lected by H. Luederwaldt in 1905 (Municipality of Campos do productive biology, use of habitat, and vocalization is presented. Jordão, state of São Paulo, southeastern Brazil; type locality, 22°44’S, 45°36’W, 1,600 m a.s.l.), the species was only described MATERIAL AND METHODS in 1920, by Miranda-Ribeiro. The Amphibia Collection of the The municipality of Campos do Jordão is located in the Museu de Zoologia da Universidade de São Paulo houses 16 speci- Serra da Mantiqueira, at a mean altitude of 1,400 m a.s.l. The mens collected in Campos do Jordão, state of São Paulo, up to topography is very uneven, with some peaks higher than 2,000 1967, and one specimen collected in 1953 by C. Gans from m, and is cut by many streams arising from the Mantiqueira Cidade Azul, actually Campos do Jordão (POMBAL-JR et al. 2008). Range (PRADO & ABREU 1995). The Parque Estadual de Campos do Therefore, more than 40 years have elapsed with no new record Jordão (PECJ) (22°39’30”-22°42’58”S, 45°26’32”-45°27’27”W) is of H. luederwaldti from the type locality. located in the northern part of the municipality of Campos do © 2010 Sociedade Brasileira de Zoologia | www.sbzoologia.org.br | All rights reserved. Natural history of Holoaden luederwaldti in southeastern of Brazil 41 Jordão, at altitudes ranging from 1,030 to 2,007 m. The PECJ 5% (ZAR 1999). The parametric t-test was used for the analyses covers an area of approximately 8,300 ha, and occupies one- of sexual dimorphism between females and males. third of the total area of the municipality of Campos do Jordão. Collecting was carried out monthly in the PECJ, from RESULTS October 2005 to December 2008, lasting four days on average. I sampled 52 specimens of H. luederwaldti: 33 males, 11 The sampling was conducted using lines of pitfall traps with a females, and 8 juveniles (undetermined). The mean of SVL of drift fence installed at different altitudinal gradients in three the specimens were: males 36.17 ± 2.42 mm (31.02-40.48 mm), areas (spaced about 2.5 km): area I at 2,000 m, area II at 1,780 females 42.61 ± 2.48 mm (39.37-46.53 mm), and juveniles 26.76 m, and area III at 1,540 m a.s.l. (Tropical Rainforest). On each ± 1.43 mm (23.97-28.55 mm). The mean of SVL of females was altitudinal gradient area, three lines of pitfall traps with a 8 m bigger than males (t = 6.46; 1 df; p< 0.0001), indicating sexual drift-fence, containing 10 buckets (100 l), were installed, total- dimorphism in size (Fig. 1). No other sexually dimorphic char- ing 90 traps. Pitfall lines were installed with a distance of 150 acters, even in color patterns or morphological structures (Figs m between each other. 2-4) were observed. All the specimens collected had their snout-vent length (SVL) measured with a caliper, to a precision of 0.01 mm. Voucher specimens are housed in the Scientific Collection of the Laboratório de Zoologia of the Universidade de Taubaté 48 Max (CCLZU), Taubaté, São Paulo; in the Célio F.B. Haddad Collec- Min tion (CFBH) of the Departamento de Zoologia, Universidade 44 Mean+SD Mean-SD Estadual Paulista, UNESP, Rio Claro, São Paulo; and in the Museu Mean de Zoologia da Universidade de São Paulo (MZUSP). 40 The vocalization of H. luederwaldti was recorded with a 36 Marantz PMD-222 cassette recorder coupled to external semidirectional (ME 66) Sennheiser microphones. All recorded 32 calls were edited with a sampling rate of 44,100 Hz and 16 bit per sample in the mono pattern. The bioacoustic analyses were 28 performed on a computer using the program CoolEdit 96 Snout-vent length (mm) 24 (Syntryllium Software Corporation), with a 20,050 Hz sampling frequency. The 256 points option (Fast Fourier Transform, FFT) 20 Young Male Female and, when necessary, the 1024 points option was used, mainly in determining fundamental frequencies. Five parameters of Figure 1. Snout-vent length (SVL) of juvenile and adult male and the advertisement calls were quantified: frequency bandwidth, female specimens of H. luederwaldti recorded in the Parque Estadual fundamental frequency, dominant frequency, note duration, de Campos do Jordão, state of São Paulo, southeastern Brazil. and note repetition rate. For the analyses and bioacoustic in- terpretations, the terms used follow MARTINS & JIM (2003). The sex of adult specimens was determined from the Females with mature oocytes were observed in October snout-vent length (SVL), based on the smallest male with de- of 2005, 2006, and 2007, and in February and April of 2008. veloped testicles. Females were determined by visual inspec- The number of oocytes in the females varied between 36 and tion, through the transparence of the ventral skin and pres- 41 oocytes (37.4 ± 3.57, n = 5). The oocytes are large and un- ence of the oocytes. When necessary, abdominal incisions were pigmented (Fig. 5). The mean diameter of the oocytes was 3.72 made and the specimens observed by means of an optical ste- ± 0.8 mm (2.86-4.32 mm, n = 96). The oocytes were light yel- reomicroscope, which facilitated the confirmation of the sex. low, with a large quantity of vitelline (Fig. 5). A positive corre- The sex of the juveniles was considered undetermined. lation was observed between the number and diameter of oo- Females were dissected by ventral incision and had their cytes (Spearman’s correlation, rs = 0.95, p = 0.013) (Fig. 6). There ovaries removed. Contents of the ovaries were spread out in a was no correlation between the SVL of the females and the Petri dish, in order to count the oocytes in each ovary. The number of oocytes (rs = 0.35, p = 0.552), or the diameter of the largest diameter of the oocytes was measured, using a stereo- oocytes (rs = 0.16, p = 0.79). Females with mature oocytes also scopic microscope with an ocular micrometer. For each dis- had some smaller oocytes in the initial stages of development.
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