Life History Aspects of Oxyrhopus trigeminus (Serpentes: Dipsadidae) from Two Sites in Southeastern Brazil

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1 Journal of Herpetology, Vol. 46, No. 1, pp. 9 13, 2012 Copyright 2012 Society for the Study of Amphibians and Reptiles Life History Aspects of Oxyrhopus trigeminus (Serpentes: Dipsadidae) from Two Sites in Southeastern Brazil LAURA R. V. ALENCAR, 1 CONRADO A. B. GALDINO, 2 AND LUCIANA B. NASCIMENTO 2,3,4 1 Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, Cidade Universitária, São Paulo, São Paulo, Brazil, CEP Programa de Pós-graduação em Zoologia, Pontifícia Universidade Católica de Minas Gerais, Avenida Dom José Gaspar, 290, Coração Eucarístico, Belo Horizonte, Minas Gerais, Brazil, CEP Museu de Ciências Naturais; Departamento de Ciências Biológicas, Pontificia Universidade Católica de Minas Gerais, Avenida Dom José Gaspar, 290, Coraçáo Eucarístico, Belo Horizonte, Minas Gerais, Brazil, CEP ABSTRACT. We studied the reproduction, sexual dimorphism, and diet of Oxyrhopus trigeminus from two sites in southeastern Brazil. Oxyrhopus trigeminus from Irapé Power Plant (IPP) contained vitellogenic follicles and eggs in both rainy and dry seasons and clutch size was not correlated with female snout vent length (SVL). Sexual dimorphism was evident. Females attain larger SVL but males have longer tails. We found three females from Santa Clara Power Plant (SPP) with vitellogenic follicles, all of them collected in the dry season. Mean SVLs of adult females from IPP and SPP were mm and 786 mm, respectively. Mean SVL of adult males from IPP was mm and the single adult male from SPP was 507 mm. The diet of O. trigeminus from IPP included rodents (46.7%), lizards (33.3%), and birds (20%). The volume of individual prey items was not correlated with snake SVL. The diet of O. trigeminus from SPP included rodents (37.5%), lizards (37.5%), birds (12.5%), and marsupials (12.5%). It seemed that an ontogenetic shift may occur in individuals of this snake species from IPP. Many clades within the family Dipsadidae (sensu Zaher et al., 2009), such as the tribe Pseudoboini, remain poorly studied (Pizzatto, 2005). The pseudoboine snake Oxyrhopus trigeminus has a broad geographical distribution in Brazil, ranging from Marajó Island in the state of Pará (north) to the state of Rio de Janeiro (south). Oxyrhopus trigeminus occurs throughout much of the Cerrado, Caatinga, Atlantic Forest, and southern Amazon domains (Peters and Orejas-Miranda, 1970; Zaher and Caramaschi, 1992). Previous studies indicate that Oxyrhopus trigeminus is an oviparous, terrestrial, and predominantly nocturnal snake (Marques et al., 2005). Vitt and Vangilder (1983) found hatchlings in July and females with large vitellogenic follicles in December in the Caatinga domain in northeastern Brazil. The diet of O. trigeminus consists of mammals and lizards (Vitt and Vangilder, 1983; Rocha et al., 2005; França et al., 2008). Data on the life history of O. trigeminus are needed to understand geographic patterns in the ecology of this species. Herein, we provide information on the life history of two populations of O. trigeminus from southeastern Brazil. We studied timing of reproduction, clutch size and its relation to female SVL, sexual size dimorphism in SVL, and tail length (TL) for Oxyrhopus trigeminus from a population in southeastern Brazil. Additional data for a second population are also provided. We also describe the diet of these populations and evaluate a possible ontogenetic shift in prey consumption. MATERIALS AND METHODS Our study was conducted on snakes sampled at two localities, separated by ca. 250 km, in southeastern Brazil within the limits of the Irapé and Santa Clara Power Plants in the State of Minas Gerais, Brazil (Fig. 1). The Irapé Power Plant (IPP) is located on the Jequitinhonha River in a transitional zone between the Cerrado, Atlantic Forest, and Caatinga domains (16u459S, 42u329W). The area contains a mosaic of Cerrado habitat, semideciduous and deciduous forests, riparian pluvial forest, grazing lands for cattle, and cultivated areas (Enerconsult Engenharia/CEMIG, unpubl. data; Feio and Caramaschi, 1995). Most of the precipitation occurs from October to March with a drier period from April to September. 4 Corresponding Author: luna@pucminas.br DOI: / The highest average temperature of the region in 2004 was 29uC and the lowest 11uC (Enerconsult Engenharia/Cemig, unpubl. data). The Santa Clara Power Plant (SPP) is located on the Mucuri River where the Mucuri (Bahia State), Nanuque, and Serra dos Aimorés municipalities come together (17u539S, 40u119W). This area was previously Atlantic Forest but is now pasture with islands of remnant forest. The climate is seasonal with the peak of rainfall from November to April (Pompeu and Martinez, 2006). The highest average temperature of the region in 2004 was 33.5uC and the lowest 21.5uC (SIMGE, 2009). We examined 83 specimens of O. trigeminus deposited in the herpetological collection of the Museu de Ciências Naturais, Pontifícia Universidade Católica de Minas Gerais, Brazil (MCNR). Specimens from IPP and SPP (Appendix I) were collected during a faunal monitoring program from February 2004 to July 2006 and from August 2001 to May 2003, respectively. We measured SVL and TL to the 0.01 cm for each specimen using a tape measure. Individuals were dissected and sex and reproductive condition were determined by gonadal inspection. We considered males to be reproductively active if they contained turgid testes and opaque and convoluted epididymides (Shine, 1977a; Ibarguengoytía et al., 2006). Females were considered reproductive if they contained vitellogenic follicles larger than 10 mm or oviductal eggs (Shine, 1977b; Pizzatto and Marques, 2002). Minimum size at maturity was estimated for the sample as the smallest reproductive individual of each sex. In many snake species, some early developing follicles will not be recruited and, thus, will not completely develop to eggs (Seigel and Ford, 1987). Hence, we estimated the maximal potential clutch size (MPC) by counting the number of vitellogenic follicles, oviductal eggs, or both. The assumption of normality was tested using the Shapiro- Wilk test, and we performed an F test to compare variances among groups. Wherever assumptions were not met we used appropriate transformations. We tested for sexual dimorphism in body size (SVL) of adults with a Student s t-test. Differences between the sexes in TL of adult individuals were evaluated using an analysis of covariance (ANCOVA) with SVL as the covariate. We tested for the association between female SVL and clutch size (both ln transformed; King, 2000) with a simple linear regression. Composition of the diet was determined by direct inspection of stomachs. We measured the length and width of food items

2 10 L. R. V. ALENCAR ET AL. FIG. 1. Map showing the location of the two hydroelectric power plants at Minas Gerais State where life history aspects of Oxyrhopus trigeminus were studied. using a measuring tape (length; nearest 1.0 mm) and a dial calliper (width; nearest 0.5 mm). Prey volume was estimated using the formula for the volume of a prolate spheroid: V 5 2/ 3p(L/2)(W/2) 2, where V is prey volume, W is prey width, and L is prey length. The direction of food ingestion was recorded whenever possible. All prey items were removed and identified to the lowest taxonomic level possible. The presence of ontogenetic change in diet of O. trigeminus was evaluated by using a Student s t-test and using type of prey (ecto- or endothermic) as a factor and SVL as the dependent variable. We used a simple linear regression analysis to test for the effect of snake size (ln transformed SVL) on the ln transformed cubic root of the volume of individual prey items. RESULTS Oxyrhopus trigeminus from the IPP. We analyzed 59 individuals of O. trigeminus and were able to determine sex and maturity for 53 individuals: 16 adult females, 13 adult males, and 24 juveniles. Mean SVL of adult females was mm (range, 629 to 808 mm, N 5 14) and mean SVL of adult males, with one standard error, was mm (range, 474 to 621 mm, N 5 9). Adult females had larger SVLs than did adult males (t ; P, 0.001); however, TL increased more rapidly with SVL for males than for females (slopes test: F 1, ; r ; P ; Fig. 2). Reproductive females were found during the rainy season; seven females with vitellogenic follicles and two with oviductal eggs (January, February, and November 2005; January 2006) and, during the dry season; four females with vitellogenic follicles and one with oviductal eggs (June 2004, 2005, and July 2006). Mean MPC was follicles or eggs (or both; N 5 13), range one to 11. Maximal potential clutch size was not correlated with female SVL (r s ; P 5 0.1; N 5 11). Reproductive males were collected during both rainy (N 5 5) and dry seasons (N 5 5). The smallest reproductive female (629 mm SVL) was larger than the smallest reproductive male (474 mm SVL). Of 59 individuals dissected for stomach content analysis, 25.4% contained a prey item in the stomach. All contained only one prey item. Rodents were the most frequent prey item found (46.7%) followed by lizards (33.3%) and birds (20%; Table 1). All prey were swallowed head-first. We did not find a significant ontogenetic shift in the diet of this population (t ; P ), although juveniles

3 LIFE HISTORY OF OXYRHOPUS TRIGEMINUS 11 marsupials (12.5%) (Table 1). Adults of O. trigeminus from SPP contained rodents, birds, and marsupials as prey, whereas juveniles contained only lizards. Because of the small sample size, we were not able to test the relationship between prey volume and snake SVL and the occurrence of an ontogenetic shift in the diet of this population. Intact prey were swallowed head-first (N 5 5). FIG. 2. Sexual dimorphism in tail length (males N 5 9 and females N 5 13) of Oxyrhopus trigeminus from Irapé Power Plant, Minas Gerais State, Brazil. consumed a higher proportion of lizards than did adults (66.7% and 33.3%, respectively). Prey volume was not related to individual snake SVL (r ; P ; N 5 12). Five females that had food items in the stomach were reproductive and one of them contained oviductal eggs. Oxyrhopus trigeminus from SPP. Twenty-four individuals of O. trigeminus were analyzed from SPP. We were able to determine sex and maturity for 21 individuals; six adult females, two adult males, and 13 juveniles. Mean SVL of adult females was mm (range, 694 to 848 mm, N 5 6). We found three females with vitellogenic follicles at dry season (May 2003). One adult male was too damaged to be measured and the other was 507 mm in SVL. Based upon testis development, both males were reproductive and were collected in the rainy season. Because of the small sample size, we were not able to evaluate sexual dimorphism and the relationship between female SVL and clutch size in this population. Seven (29.2%) of the 24 individuals dissected for stomach analysis contained prey. Rodents and lizards were the most frequent prey (37.5% each) followed by birds (12.5%) and DISCUSSION The pattern of sexual size dimorphism found for O. trigeminus from IPP (females larger than males) is similar to that described for other snakes (Shine, 1993; Gregory, 2004; Pinto and Fernandes, 2004). This pattern has also been observed in closely related species including Oxyrhopus guibei (Pizzatto and Marques, 2002) and species of the genera Clelia, Boiruna, and Mussurana (Pizzatto, 2005). It is argued that females with larger body size should produce a clutch with larger eggs or more eggs, and sexual dimorphism may exist due to the reproductive benefits associated with larger female size (Fairbairn, 1997). The larger TL of males results partly from accommodation of the hemipenes in the base of the tail but may also reflect selection for hemipenis size resulting from higher relative reproductive success in males with relatively larger hemipenes (King, 1989; Shine et al., 1999). Females of O. trigeminus from IPP are capable of producing eggs during rainy and dry seasons, indicating that reproduction can occur throughout the year, a pattern also known for O. guibei from a seasonal habitat in southeastern Brazil (Pizzatto and Marques, 2002). However, in that case, females with vitellogenic follicles or oviductal eggs were more abundant at the end of dry season, and most oviposition occurred during the onset of the rainy season. Contrary to other well-studied snakes with variable clutch size (Pizzatto and Marques, 2002; Alves et al., 2005), MPC was not related to female SVL in O. trigeminus from IPP. Nonetheless, only larger females were capable of producing large clutches. Thus, despite the nonsignificant result of the regression analysis, SVL likely has influence on clutch size in O. trigeminus. The nonsignificant result should be viewed with caution because it could have been influenced by our sample size or could be from the inclusion of vittelogenic follicles in the analyses. Lizards and rodents were the most frequent items in the diet of O. trigeminus from both localities, similar to the diet reported elsewhere for this species (Vitt and Vangilder, 1983; França et al., 2008). Similarities between the prey items that we report and those reported earlier include Necromys lasiurus, Ameiva TABLE 1. Analyses of stomach contents of Oxyrhopus trigeminus from the Irapé Power Plant (IPP) and Santa Clara Power Plant (SPP), Minas Gerais State, Brazil. Number in parentheses corresponds to the number of specimens examined in each site. N 5 number of occurrence of each item; P 5 percentage of occurrence of each item. Family Prey Item IPP (59) SPP (24) N P(%) N P(%) Rodents Cricetidae Akodon sp Necromys lasiurus Nectomys squamipes Oligoryzomys sp Marsupials Didelphidae Didelphis albiventris Lizards Gekkonidae Hemidactylus mabouia 2 25 Teiidae Ameiva ameiva 3 20 Tropiduridae Tropidurus hispidus Tropidurus sp Undetermined Birds Furnariidae Synallaxis sp Emberezidae Coryphospingus sp Undetermined Total

4 12 L. R. V. ALENCAR ET AL. ameiva, and species of the genus Tropidurus (Vitt and Vangilder 1983; Franca et al. 2008). The semi-aquatic rodent Nectomys squamipes (Martins-Hatano et al., 2001) and one marsupial, Didelphis albiventris, were found in the diet of O. trigeminus from SPP. We suggest that, due to differences in habitat use between predator and prey, predation on N. squamipes was incidental. To our knowledge, these are the first records of N. squamipes and a marsupial as prey of O. trigeminus. Our data also provide the first record of birds being consumed by O. trigeminus. The birds were identified as adult Synallaxis sp. (Furnariidae) and Coryphospingus sp. (Emberizidae). These species forage on the ground (Sick, 2001), which may facilitate predation by the terrestrial O. trigeminus. Snake SVL was not correlated with prey volume in O. trigeminus from IPP. No relationship between SVL and prey volume has been found for other snake species, probably resulting from large snakes continuing to eat small prey (Arnold, 1993). Shine (1977c) proposed that this trend arises because capture and ingestion costs could be smaller in relation to the energy content of prey. Our results may also be biased due to low sample size. Ontogenetic shifts in diet are common in snake species (Mushinsky et al., 1982; Martins et al., 2002; Hartmann et al., 2003). Although we could not find a significant difference in the diets of juvenile and adult O. trigeminus from IPP, our limited data indicate that juveniles took a higher proportion of lizards and fewer endothermic prey than did adults in both localities. However, our sample size is small and these results should be considered preliminary. Further, Andrade and Silvano (1996) found an ontogenetic shift in diet, from ectothermic to endothermic prey, for O. guibei. Pizzato and Marques (2002) found that female O. guibei did not feed while gravid, as in other snakes (Shine, 1980). Nonetheless, we found a gravid female O. trigeminus from IPP that had fed on an Ameiva ameiva, which may indicate that females of O. trigeminus are able to feed even when gravid. Acknowledgments. We are grateful to L. Vitt and M. Martins for critically reading the manuscript; D. Fernandes and P. Fatorelli for their suggestions on the drafts of the manuscript; S. A. Talamoni, E. Câmara, R. Dutra and F. Lira for the identification of the mammals and B. Garzón for the identification of the birds; M. P. Gaiarsa for help with the map; R. R. Carvalho for the information about the Power Plants; and V. Calixto, F. Braga, F. Natali, F. Pinto, and R. Campos for the kind help at lab analyses. CAB Galdino currently receives a grant from CNPq (proc /2010-6). LB Nascimento receives financial support from FIP/PUC Minas (Fundo de Incentivo à Pesquisa of Pontifícia Universidade Católica de Minas Gerais) and FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais). LITERATURE CITED ALVES, F. Q., A. S. ARGÔLO, AND J. JIM Biologia reprodutiva de Dipsas neivai Amaral e Dipsas catesbyi (Sentzen) (Serpentes, Colubridae) no sudeste da Bahia, Brasil. Revista Brasileira de Zoologia 22: ANDRADE, R. O., AND R. M. SILVANO Comportamento alimentar e dieta da falsa-coral Oxyrhopus guibei Hoge & Romano (Serpentes, Colubridae). Revista Brasileira de Zoologia 13: ARNOLD, S. J Foraging theory and prey size predator size relations in snakes. In R. A. Seigel and J. T. Collins (eds.), Snakes, Ecology and Behavior, pp McGraw-Hill, New York. FAIRBAIRN, D. J Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics 28: FEIO, R. N., AND U. 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5 LIFE HISTORY OF OXYRHOPUS TRIGEMINUS 13 ZAHER, H., F. GRAZZIOTIN, J. E. CADLE, R. W. MURPHY, J. C. MOURA-LEITE, AND S. BONATO Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: a revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia 49: Accepted 20 January APPENDIX Specimens Examined Oxyrhopus trigeminus MINAS GERAIS: UHE IRAPÉ (MCNR 1685, MCNR 1694, MCNR 916, MCNR 917, MCNR , MCNR 1042, MCNR 1310, MCNR 1314, MCNR 1321, MCNR 1335, MCNR , MCNR 1562, MCNR 1576, MCNR 1592, MCNR 1595, MCNR 1604, MCNR 1622, MCNR , MCNR , MCNR 1686, MCNR 1705, MCNR 1722, MCNR 1733, MCNR 1759, MCNR 1776, MCNR 1779, MCNR 1791, MCNR 1845, MCNR 1848, MCNR 1850, MCNR 1861, MCNR 1876, MCNR 1878, MCNR 1914, MCNR 1918, MCNR , MCNR 2245, MCNR 2261, MCNR 2270, MCNR 2275, MCNR 2285, MCNR , MCNR 2359, MCNR 2374, MCNR , MCNR 2523). Oxyrhopus trigeminus MINAS GERAIS: UHE SANTA CLARA (MCNR 235, MCNR 246, MCNR 249, MCNR 526, MCNR , MCNR , MCNR 1420, MCNR 2224, MCNR , MCNR 2232).