Habitat Use by the Pumpkin Toadlet, Brachycephalus Ephippium (Anura, Brachycephalidae), in the Atlantic Rain Forest of Brazil
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Bol. Asoc. Herpetol. Esp. (2013) 24(2) 11 Habitat use by the pumpkin toadlet, Brachycephalus ephippium (Anura, Brachycephalidae), in the Atlantic Rain Forest of Brazil Mauro Sérgio Cruz Souza Lima1, Jonas Pederassi2 & Carlos Alberto dos Santos Souza3 1 UFPI - Universidade Federal do Piauí, Campus Amilcar Ferreira Sobral, BR 343, Km 3,5 – Meladão - CEP 64.800-000, Floriano/PI, Brazil. C.e.: [email protected] 2 UFRJ - Universidade Federal do Rio de Janeiro, Museu Nacional, Departamento de Vertebrados, Quinta da Boa Vista, São Cristóvão, 20940-040 Rio de Janeiro, RJ, Brasil. 3 UFJF – Universidade Federal de Juiz de Fora, Campus Martelos, Post-graduation Program on Biological Sciences Behaviour and Animal Biology. Martelos, CEP: 36.036-330, Juiz de Fora - MG. Brasil. Fecha de aceptación: 14 de octubre de 2013. Key words: bioindicator, Cunhambebe State Park, Poisson’s distribution, pumpkin toadlet. RESUMEN: La ocupación del hábitat y el comportamiento circadiano de las especies a menudo están relacionados con las condiciones ambientales. El objetivo de este trabajo es describir el uso de los hábitats y la actividad circadiana en el anuro Brachycephalus ephippium en el estado de Rio de Janeiro, Brasil. Se observó la frecuencia de ocupación de seis hábitats y se analizaron las diferencias entre las estaciones seca y lluviosa. El análisis causal de ocupación mostró un período de actividad de siete horas, con diferencias según los hábitats. La incidencia de luz natural resultó un factor importante en el período de actividad de la especie. Sugerimos que la especie es un buen bioindi- cador ya que las características del hábitat (e.g., cobertura arbórea) afectan directamente la inciden- cia de luz natural y ello puede afectar la ocupación de B. ephippium. Originally, the Atlantic Forest occupied 1.5 million km2 and in mid-2000 it was redu- ced to only 7% of its original area (Myers et al., 2000; Tabarelli et al., 2005). Scientific concerns Photo Jonas Pederassi Jonas Photo over ecosystems and biomes disappearance made researchers discover in frogs natural allies that can indicate the quality of the envi- ronment (Becker et al., 2007; Dixo et al., 2009; Hayes et al., 2010; Toledo et al., 2010). The amphi- bian Brachycephalus ephippium (Spix, 1824) is a small orange or chrome-yellow frog (Figure 1), with about 2 cm in snout-vent length and only two functional fingers and three toes (Izecksohn & Carvalho-e-Silva, 2001), and has its type locality in the municipality of Piquete, São Paulo, Brazil (Bokermann, 1966). The genus Brachycephalus is endemic from the region ranging from the state of Figure 1. B. ephippium in the study area. Espírito Santo to Paraná (Pombal-Jr et al., 1998; Figura 1. B. ephippium en el área de estudio. 12 Bol. Asoc. Herpetol. Esp. (2013) 24(2) Pombal-Jr & Izecksohn, 2011), being the species found in one specific habitat and N is the total B. ephippium currently distributed in moun- sample that was made in transects (Bodenheimer, tainous regions of the Atlantic Forest in Rio 1955 Apud Neto et al. 1976). The presence of the de Janeiro, São Paulo and Minas Gerais (Frost, species per habitat was considered Constant 2013). As for its natural history, it is a species (C > 50%), Accessory (50% > C > 25%) and restricted to mature forests where it inhabits Accidental (C < 25%). To test if habitat use diffe- the leaf litter (Pombal-Jr et al., 1994; Pombal-Jr, red between dry and wet season, constancy of 1999, 2003, 2010; IUCN, 2011). habitat occupation was analyzed using a Student’s Although the basic natural history of B. ephip- t-test. For casual or probabilistic analysis of the pium has been studied in Brazil, its dynamic occupational behavior, we modeled the variables behavioral occupation of the environment using Poisson distribution (pr(x) = µx e-µ / x!) in has not been examined yet. In this study, we Excel. The decay of the hypothesis was measured describe habitat uses of B. ephippium, to through a χ2 test. Biotic and abiotic correlations identify and determine the relationship bet- were tested using the nonparametric Spearman ween the abiotic elements and the occupatio- correlation coefficient. nal behavior of B. ephippium. With the biotic and abiotic data collected The study area was included inside the Parque during the rainy season we developed an eco- Estadual Cunhambebe (Cunhambebe State logical model of habitat occupation for B. ephip- Park), in the state of Rio de Janeiro, Brazil. The pium. The model was developed using the Park has an area of 380 km2, corresponding to software Vensim® (Ventana Systems, 2013), four municipalities: Mangaratiba, Angra dos Reis, which created the mathematical equations, Rio Claro and Itaguaí. The specific area of study algorithms and the causal diagram. corresponds to 1 km2 within the park located in We observed 37 individuals of B. ephip- Angra dos Reis (22°53'S / 44°14'W – Datum pium and its habitat use in the study area was UD55; 635 masl). Eight field visits per year were constant under leaf litter, accessory on shrub conducted between 2008 and 2009, on January and litter, and accidental on bromeliads, tree (rainy season) and July (dry season), accumula- trunks on soil, and in burrows. The record of ting a total of 192 hours of sampling effort. two amplexus under the leaf litter supports During the fieldwork, we recorded the habitat the condition of this habitat as the most com- type where individuals were observed, conside- mon for the species in the area. According to ring for the study six different categories: (1) Student’s t-test, the constancy of occupation shrubs, (2) litter, (3) bromeliads, (4) tree trunks of habitats by B. ephippium was not different on soil, (5) under leaf litter, and (6) in burrows. between the dry and rainy season (t15 = 0.28; Additionally, two abiotic conditions were recor- P = 0.57). This result is partially in concor- ded: relative humidity and temperature. Relative dance with a previous study which showed humidity (RH) and temperature were measured that these diurnal frogs occupied bushes, drif- using the thermo-hygrometer Instrutherm® with ting over the burlap when the RH reaches a precision ± 5% RH and ± 1°C respectively. 100% and remaining in the leaf litter during The constancy of habitat occupation of the dry season (Pombal-Jr. et al., 1994). Our B. ephippium was determined by C = (p.100) / N, measures of RH varied between 77.1% and where p is the number of times the species was 98% (dry and wet season respectively). No Bol. Asoc. Herpetol. Esp. (2013) 24(2) 13 correlations were detected between the habi- predicted by the model did not differ in rela- χ2 tat categories considered and the abiotic fac- tion to the observed data ( 6 = 0.47; P = 0.92). tor measured (R2 = 0.19 to temperature and When we build the ecological model based R2 = 0.057 to relative humidity). on the collected data, we observed that rainy The two amplexus observed were like the or dry conditions do not interfere in the spe- ones previously described: initially inguinal cies occurrence. According to the Poisson and later becoming axillary (Pombal-Jr et al., probability model for both sampling periods, 1994). The exposure period of the species was the specimen occupation, as a function of the only diurnal (between 8 a.m. and 3 p.m.) environments, did not present any changes. indicating a correlation between daily tempe- The habitat behavior of occupancy for the rature increases and the species exposure to sample period of drought and increased rain- the environment which, in this study, ranged fall across the two years of study is linked to between 16.5ºC and 26.9°C (R2 = 0.93, the course of a 24-h day. 21.48 ± 3.37°C). A causal diagram of occupational dynamics When we applied the observation period of by B. ephippium is supported by the model, each occupied habitat to the Poisson model, we which features key elements (daytime and grouped a seven-hour probability of occurrence night time) and the period element limited to where B. ephippium would be successively vie- a 24-hour cycle. The causal diagram shows the wed in each habitat: 1.16 hour on shrubs, 0.19 circadian cycle of B. ephippium in the studied hour on the litter, 0.05 hour on bromeliads, area (Figure 2). The ecological interaction 0.66 hour on tree trunk on soil; 3.67 hours dynamics of B. ephippium, over a 24-hour under leaf litter and 1.33 hour in burrow. cycle, points, according to the model, to a When we compare the exposure periods daily cycle that starts at 8 a.m. in the morning to the habitat constancy of occupation, we and continues until 3 p.m., reducing the acti- found equivalent results. However, the use of vity in the afternoon (Figure 3). Interestingly, the term “accidental” should be considered as the light starts to reduce at 3 p.m. because of a consequence of the short-time occupation the forest canopy and, meanwhile, the activity and not a randomness condition. The values of the species is reduced. The habitat occupa- Figure 2. Causal activity diagram of B. ephippium. Figure 3. Activity model of B. ephippium in a 24-h cycle. Figura 2. Diagrama de actividad causal de B. ephippium. Figura 3. Modelo de actividad de B. ephippium en un ciclo Flux/flujo: ; Connectors/-es: ; Stock: de 24 h. 14 Bol. Asoc. Herpetol. Esp. (2013) 24(2) tion systematically starts at 8 a.m. in the mor- and dark phases (Daan et al., 2001). The endoge- ning of the following day, when the light pene- nous circadian rhythms makes physiological trates the canopy and reaches the litter.