Ecology of the Colubrid Snake Spilotes pullatus from the Atlantic Forest of Southeastern Brazil Author(s): Otavio A. V. Marques, Diego F. Muniz-Da-Silva, Fausto E. Barbo, Silvia R. Travaglia Cardoso, Danusa C. Maia, and Selma M. Almeida-Santos Source: Herpetologica, 70(4):407-416. 2014. Published By: The Herpetologists' League DOI: http://dx.doi.org/10.1655/HERPETOLOGICA-D-14-00012 URL: http://www.bioone.org/doi/full/10.1655/HERPETOLOGICA-D-14-00012 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Herpetologica, 70(4), 2014, 407–416 Ó 2014 by The Herpetologists’ League, Inc. ECOLOGY OF THE COLUBRID SNAKE SPILOTES PULLATUS FROM THE ATLANTIC FOREST OF SOUTHEASTERN BRAZIL 1,5 2 3 OTAVIO A. V. MARQUES ,DIEGO F. MUNIZ-DA-SILVA ,FAUSTO E. BARBO ,SILVIA R. TRAVAGLIA 4 4 1 CARDOSO ,DANUSA C. MAIA , AND SELMA M. ALMEIDA-SANTOS 1 Instituto Butantan, Laboratorio´ de Ecologia e Evolu¸ca˜o, Av. Dr. Vital Brazil, 1500, Sa˜o Paulo, 05503-900, SP, Brazil 2 Setor de Anatomia, Departamento de Cirurgia, Faculdade de Medicina Veterina´ria e Zootecnia, Universidade Sa˜o Paulo, Av. Orlando Marques de Paiva 87, 05508-270 Cidade Universita´ria, Sa˜o Paulo, SP, Brazil 3 Museu de Zoologia, Universidade de Sa˜o Paulo (MZUSP), P.B. 42494, 04218-970, Sa˜o Paulo, SP, Brazil 4 Instituto Butantan, Museu Biologico,´ Av. Dr. Vital Brazil, 1500, Sa˜o Paulo, 05503-900, SP, Brazil ABSTRACT: Few extensive studies have addressed the ecology of South American colubrids. Spilotes pullatus is a large and conspicuous colubrid snake with a broad distribution in South America. We analyzed the morphology, habitat use, diet, feeding behavior, and reproductive biology of S. pullatus in a subtropical area of distribution, specifically in the Atlantic Forest of southeastern Brazil. We compared its ecological traits with those of other South American colubrids to identify common characteristics and differences among these snakes. Spilotes pullatus inhabits primarily lowland areas and readily occurs in altered habitats. Male and female snakes were similar in median snout–vent length, but the largest known individuals of the species are males. This snake forages actively by day, searching primarily for small mammals and nestling birds (usually 0.36–7.37% of snake mass) on the ground or in vegetation. Observations of captive snakes showed that small prey are quickly swallowed alive, whereas large prey are constricted or pressed against the substrate and die before swallowing. The reproductive cycle of the females appears to be seasonal, with vitellogenesis occurring from the middle of the dry season to the onset of the rainy season. Mating was recorded at the end of the dry season and the onset of the rainy season and coincided with the onset of male– male combat. Such combat behavior includes partial entwining of the anterior portions of the body and a consistent, upright position of the trunk. Recruitment of newborns occurs at the end of the rainy season and during the dry season. Spilotes pullatus shows unique characteristics but also shares several ecological traits with other South American colubrids. Key words: Diet ecology; Habitat use; Reproduction; Subtropical region; Yellow Ratsnakes THE COSMOPOLITAN family Colubridae is reported to feed on a wide range of verte- diverse in North and Central America but brates (cf. Beebe, 1946; Cunha and Nasci- few representatives are found in South mento, 1978; Murphy, 1997; Martins and America (Greene, 1997). However, certain Oliveira, 1998), although several researchers colubrids are conspicuous elements of the have stated that its prey consists primarily of snake fauna in most portions of this region. birds and their eggs (e.g., Amaral, 1978; Spilotes pullatus is the most widely distributed Loiselle and Hoppes, 1983). Subsequent colubrid in South America and is abundant in studies found that this snake feeds on habitats such as the Brazilian Atlantic Forest smaller-sized prey such as juvenile mammals (Peters and Orejas-Miranda, 1970; Marques, and nestling birds (Marques and Sazima, 1998; Hartmann et al., 2009). Despite its 2004). Data on reproduction are scarce and conspicuousness and wide distribution, S. anecdotal, rarely documented (e.g., Hauzman pullatus has never been the subject of a et al., 2005), and insufficient to characterize detailed study covering the principal aspects the reproductive cycle or fecundity of the of its ecology. species. Defensive behaviors have been pre- Spilotes pullatus grows to a snout–vent viously described (Rossman and Williams, length (SVL) of .1500 mm. This snake may 1966; Sazima and Haddad, 1992), but other be exclusively diurnal and is usually described behavioral characteristics, including feeding as arboreal (Amaral, 1978; Dixon et al., 1993; and reproduction, are virtually unknown. In Martins and Oliveira, 1998). The species is this paper we provide information on the habitat use, daily activity, body size, repro- 5 CORRESPONDENCE: email, otavio.marques@butantan. ductive behavior, reproductive cycles, fecun- gov.br dity, diet, and feeding behavior of S. pullatus 407 408 HERPETOLOGICA [Vol. 70, No. 4 FIG. 1.—Specimen localities of individual Spilotes pullatus used in this study. Gray area represents the Atlantic Forest biome within South America (inset). Darker gray areas indicate forest remnants. in the subtropical Atlantic Forest, where it is Minas Gerais (PUC-MG), Centro Universita´r- locally abundant. io Serra dos Orga´ ˜os de Teresopolis´ (UNI- FESO), and Museu de Historia´ Natural da MATERIALS AND METHODS Universidade Estadual de Campinas (ZUEC). Specimens and Life-history Data The examined samples included only speci- mens collected in southeastern Brazil, from Our study is based on the dissection of Minas Gerais (208S) to Parana´ (258S). This preserved specimens from herpetological col- area lies within the Atlantic Forest domain, lections and on observations in the field and in captivity. We examined 178 preserved speci- with an elevational range of 0–2000 m above mens from the following museum collections: sea level (asl; Fig. 1). This portion of the Funda¸ca˜o Nacional Ezequiel Dias (FUNED), Atlantic Forest has two seasons: rainy, with Instituto Butantan (IBSP), Museu de Cienciasˆ higher rainfall and temperatures, and dry, eTecnologiadaPontifıcia´ Universidade with less rainfall and lower temperatures. The Catolica´ de Porto Alegre (MCT), Museu de rainy season comprises austral spring (Octo- Historia´ Natural Capa˜o da Imbuia (MHNCI), ber–December) and summer (January– Museu Nacional da Universidade Federal do March) whereas the dry season comprises Rio de Janeiro (MNRJ), Museu de Zoologia autumn (April–June) and winter (July–Sep- Joa˜o Moojen da Universidade Federal de tember; Nimer, 1989). Vi¸cosa (MZUFV), Museu de Cienciasˆ Natur- We collected the following data for each ais da Pontifıcia´ Universidade Catolica´ de specimen: (1) SVL; (2) tail length (TL); (3) December 2014] HERPETOLOGICA 409 sex; (4) juvenile or adult—males were adult if postures during combat. All behavioral obser- they had enlarged testes and opaque deferent vations from feeding trials and field encoun- ducts (Shine, 1982), and females were adult if ters are archived on a DVD housed at they had either ovarian follicles in vitellogen- Laboratoırio` de Ecologia e Evolu¸ca˜oof esis or oviductal eggs (Shine, 1980); (5) for Instituto Butantan. females, diameter of the largest ovarian follicles, diameter of the largest egg, number Reproductive Data of ovarian follicles in vitellogenesis (.10 mm), We obtained data on oviposition from four and number of oviductal eggs; and (6) gravid females received by Instituto Butantan. stomach or intestinal contents (or both). All The eggs were incubated in moist vermiculite food items in the stomach were removed, at room temperature (24–278C). Within 12 h identified to the lowest possible taxonomic of oviposition, we measured both females and level, and measured when intact or nearly their eggs and calculated relative clutch mass undigested. Following Shine (1994), the (RCM clutch mass/maternal body mass; degree of sexual size dimorphism (SSD) was Seigel and¼ Ford, 1987). We measured hatch- calculated as: lings within 24 h of emergence from their eggs. We defined clutch size as the number of 1 mean adult SVL of the larger sex SSD Àð Þ oviductal eggs or large vitellogenic ovarian ¼ mean adult SVL of the smaller sex . ð Þ follicles ( 10 mm) in preserved females (n 13) as well as the number of eggs laid by live¼ Behavioral Data females (n 4). We used linear regression to ¼ Captive individuals (15 adults: SVL . 1280 examine the relationship between maternal mm, 13 juveniles: SVL , 950 mm) were SVL