Study on the Population Structure of the Paradoxical Frog, Pseudis Bolbodactyla (Amphibia: Anura: Hylidae), Using Natural Markings for Individual Identification
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ZOOLOGIA online ahead of print http://dx.doi.org/10.1590/S1984-46702013005000001 Study on the population structure of the paradoxical frog, Pseudis bolbodactyla (Amphibia: Anura: Hylidae), using natural markings for individual identification Werther P. Ramalho1,4, Rafael F. Jorge2, Leandro B. Baiocchi3, Alfredo P. Peña4 & Ricardo A. P. Pires4 1 Programa de Pós-Graduação em Ecologia e Manejo de Recursos Naturais, Universidade Federal do Acre. 69915-900 Rio Branco, AC, Brazil. E-mail: [email protected] 2 Programa de Pós-Graduação em Ecologia, Instituto Nacional de Pesquisas da Amazônia. Avenida André Araújo 2936, Petrópolis, 69011-970 Manaus, AM, Brazil. 3 Departamento de Biologia, Pontifícia Universidade Católica de Goiás. Avenida Universitária 1069, Setor Universitário, 74605-010 Goiânia, GO, Brazil. 4 Associação Brasileira para a Conservação das Tartarugas. Rua 4, 515, Ed. Parthenon Center, Sl. 1207, Centro, 74020-060 Goiânia, GO, Brazil. ABSTRACT. The goal of this study was to assess the population structure of Pseudis bolbodactyla Lutz, 1925 using natural markings to identify individuals. Recruitment, survival, and population size estimations were obtained using the Jolly- Seber stochastic method. A total of 166 individuals were captured, and the striped, spotted, and dotted patterns that make their recognition possible were recorded. Of the specimens captured, 27 were recaptured, including some at pre and post-metamorphic stages. The estimate maximum population size was 52. The indices of survival and recruitment varied among samplings. Sexual dimorphism in size and in the operational sex ratio were detected. Despite the limited scope of our characterization of the P. bolbodactyla population, our data might be useful in the interpretation and elaboration of new hypotheses about ecological processes acting on anuran populations. KEY WORDS. Amphibian; capture-recapture; Cerrado; photograph; estimate. Several methods have been used for marking and identi- designs on the inner surface of the thighs of these frogs serve fying anurans, for instance toe clipping, burning, tagging and as a fingerprint that makes it possible to unequivocally iden- banding (DONNELLY et al. 1994). These techniques, which im- tify them. Later, GARDA et al. (2010) suggested that these pat- port in various degrees of disfigurement, have been assessed in terns of stripes on the thigh area vary between and within order to determine their impacts on the survival of the marked populations of different species of Pseudis, allowing popula- animals, their efficacy, and the ethical issues involving the use tion studies to be conducted. of animals in scientific research (GOLAY & DURRE 1994, MEASEY Based on the patterns of the stripes on the ventral longi- 2001, DAVIS & OVASKA 2001, MCCARTHY & PARRIS 2004, FUNK et al. tudinal section of the thigh, GALLARDO (1961) divided the Pseudis 2005, FERNER 2007, CLEMAS et al. 2008). An alternative to these paradoxa (Linnaeus, 1758) species group into several sub-spe- methods is identification through photographs, a relatively cies, but this division was subsequently deemed unreliable (GARDA new technique that has been adopted by a number of research- et al. 2010). The species that comprise Pseudis Wagler, 1830 are ers, but is still looked upon with some suspicion (REBELO & distributed in South America, east of the Andes, from Venezuela LECLAIR 2003, BRADFIELD 2004, MIRANDA et al. 2005, FERNER 2007, to eastern Argentina and Uruguay (DARST & CANNATELLA 2004, CLEMAS et al. 2008, KENYON et al. 2010). It involves the utiliza- GARDA & CANNATELLA 2007, GARDA et al. 2010, FROST 2013). tion of organic physical markings (scratches, mutilations, or Species of Pseudis are extremely dependent on water and defects) and color patterns (stripes, spots, etc.) to distinguish display several morphologic, reproductive, and developmen- among individuals of the same species. The viability of this tal adaptations to aquatic environments that distinguish them technique depends on the quality of the markings and the time from other Hylidae (EMERSON 1988, GARDA & CANNATELLA 2007). it takes to compare images (FRISCH & HOBBS 2007). The dispersion of individuals to different water bodies occurs Identification through photographs was recently used mainly after heavy rains, although populations ordinarily tend by MIRANDA et al. (2005) for the identification of Pseudis cardosoi to remain within their own watershed (GALLARDO 1961).With Kwet, 2000 individuals. Their results showed that the variable the exception of Pseudis bolbodactyla Lutz, 1925, P. paradoxa, © 2013 Sociedade Brasileira de Zoologia | www.sbzoologia.org.br | All rights reserved. W.P. Ramalho et al. and Lysapsus limellum Cope, 1862, all paradoxical anuran spe- subject. Voucher specimens were deposited in the Herpetologi- cies are restricted to one watershed. However, this group is still cal Collection of the Pontifícia Universidade Católica de Goiás poorly sampled in most of the Central and North regions of (CEPB-NUROG; male: CN18 and female: UF08). South America (GARDA & CANNATELLA 2007). We assumed that the population studied varied due to Pseudis bolbodactyla has been found in four Brazilian mortality, birth rates, emigration, and immigration. Therefore, states: Bahia, Minas Gerais, Goiás, and Mato Grosso (CARAMASCHI the population size was estimated using the Stochastic Method & CRUZ 1998, TEIXEIRA et al. 2004, VAZ-SILVA et al. 2007, GARDA et of Jolly-Seber. This method was also used to estimate the prob- ROST ⌽ al. 2010, F 2013). It is medium sized when compared with ability of survival ( i, i+1) and recruitment (Bi, i+1) rates of the other species of Pseudis, and is characterized by a vestigial car- population between sampling sessions (LEBRETON et al. 1993, pal tubercle, head as wide as long, and dorsal skin sharply FERNANDEZ 1995). wrinkled (GALLARDO 1961, CARAMASCHI & CRUZ 1998, TEIXEIRA et Based on the observations of VAZ-SILVA et al. (2007), indi- al. 2004, GARDA et al. 2010). Very few studies have been con- viduals with yellowish throat regions were identified as adult ducted on the population ecology of P. bolbodactyla, and the males and those with whitish throat regions were considered existing ones are mainly focused on behavior, diet, and breed- adult females. Sexual dimorphism was verified using SVL and ing (BRANDÃO et al. 2003, TEIXEIRA et al. 2004, VAZ-SILVA et al. 2007). body mass measurements used as reference. In order to com- In this study, we present information on the biology and pare the SVL and body mass measurements between males and ecology of a population of P. bolbodactyla in an artificial pond females, a Student t-test was applied. Sexual Size Dimorphism located on the boundary of the Serra de Caldas Novas State (SSD) was analyzed by dividing the average SVL of females by Park, in the municipality of Caldas Novas, state of Goiás, Bra- the average SVL of males, where SSD > 0 = females larger than zil. The natural markings of individuals were recorded with males, and SSD < 0 = males larger than females (SHINE 1979, the aid of photographs. Based on our data, we endeavored to: MONNET & CHERRY 2002). 1) verify the existence of biometric variations among males, The operational sex ratio (OSR) was obtained by divid- females, and juveniles; 2) determine whether the variability in ing the number of males by the number of females present at length and weight of males and females is indicative of sexual the breeding sites (assuming that males and females breed ev- dimorphism; 3) verify whether there is a tendency for opera- ery year after reaching maturity) each night and by the grand tional sex ratio in the species; 4) estimate population size dur- total recorded in the samplings (EMLEN & ORING 1977, SILVA & ing the breeding season; and 5) evaluate whether photographic ROSSA-FERES 2010). The qui-square (2) (ZAR 1984) was used to identification methods using natural markings can be used in evaluate possible differences in sex ratio. population studies of P. bolbodactyla. The Pearson correlation coefficient (r) was used to verify the relationship between abundance and climatic variables, MATERIAL AND METHODS the abundance of males and females, the abundance and op- erational sex ratio, and the weight/length relation of the indi- This study was conducted at Lajeado farm (17°52’10.1"S/ viduals. All statistical analyses were conducted with a 48°41’26.5"W, 663 m a.s.l.; WGS84 datum), situated in the significance level of 0.05. buffer zone of Serra de Caldas Novas State Park, Goiás, Brazil (Fig. 1). Five excursions, lasting two days each, were conducted RESULTS to the research site between April and May, 2009, and January and May, 2010. The samples were collected from an artificial A total of 169 P. bolbodactyla specimens (88 males, 40 pond measuring about 280 m2, beginning at 6:00 p.m. and females, and 41 juveniles) were collected and photographed. lasting for a variable number of hours. Individuals were considered juveniles in the absence of sec- The anurans were captured manually, kept in buckets of ondary sexual characteristics. There was a positive correlation water, and taken to the laboratory for biometrics and photo- between the number of individuals and the following climatic graphic registration. The snout-vent length (SVL) was measured variables: precipitation (r = 0.92, gl = 4) and relative humidity with a caliper (0.1 mm precision) and their body mass with a (r = 0.89, gl = 4). Individuals were more abundant in April and Diamond model 500 digital