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Reproductive Ecology of Dipsadine Snakes, with Emphasis on South American Species

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Reproductive Ecology of Dipsadine Snakes, with Emphasis on South American Species Herpetologica, 64(2), 2008, 168–179 E 2008 by The Herpetologists’ League, Inc. REPRODUCTIVE ECOLOGY OF DIPSADINE SNAKES, WITH EMPHASIS ON SOUTH AMERICAN SPECIES 1,4,5 2 3 4 LI´GIA PIZZATTO ,MAURI´CIO CANTOR ,JULIANA LIMA DE OLIVEIRA ,OTAVIO A. V. MARQUES , 2 3 VINICIUS CAPOVILLA , AND MARCIO MARTINS 1Po´s-Graduac¸a˜o em Ecologia, Depto. de Zoologia, Universidade Estadual de Campinas, CP 6109, 13083-970, Campinas, SP, Brazil 2Graduac¸a˜o em Cieˆncias Biolo´gicas, Depto. de Zoologia, Universidade Estadual de Campinas, CP 6109, 13083-970, Campinas, SP, Brazil 3Departamento de Ecologia, Instituto de Biocieˆncias, Universidade de Sa˜o Paulo, Rua do Mata˜o, Travessa 14 s/n, 05508-090, Sa˜o Paulo, SP, Brazil 4Laborato´rio Especial de Ecologia e Evoluc¸a˜o, Instituto Butantan, Av. Dr. Vital Brazil 1500, 05503-900, Sa˜o Paulo, SP, Brazil ABSTRACT: A relatively large amount of variation occurs in the reproductive ecology of tropical snakes, and this variation is generally regarded as being a consequence of seasonality in climate and prey availability. In some groups, even closely related species may differ in their reproductive ecology; however, in others it seems to be very conservative. Here we explore whether characters related to reproduction are phylogenetically constrained in a monophyletic group of snakes, the subfamily Dipsadinae, which ranges from Mexico to southern South America. We provide original data on reproduction for Leptodeira annulata, Imantodes cenchoa, and three species of Sibynomorphus from southern, southeastern and central Brazil, and data from literature for other species and populations of dipsadines. Follicular cycles were seasonal in Atractus reticulatus, Dipsas albifrons, Hypsiglena torquata, Leptodeira maculata, L. punctata, Sibynomor- phus spp. and Sibon sanniola from areas where climate is seasonal. In contrast, extended or continuous follicular cycles were recorded in Dipsas catesbyi, D. neivai, Imantodes cenchoa, Leptodeira annulata, and Ninia maculata from areas with seasonal and aseasonal climates. Testicular cycles also varied from seasonal (in H. torquata) to continuous (in Dipsas spp., Leptodeira annulata, L. maculata, N. maculata and Sibynomorphus spp.). Most dipsadines are small (less than 500 mm SVL), and females attain sexual maturity with similar relative body size than males. Sexual dimorphism occurred in terms of SVL and tail length in most species, and clutch size tended to be small (less than five eggs). Combat behavior occurs in Imantodes cenchoa, which did not show sexual size dimorphism. Reproductive timing, for both females and males, varied among species but in general there were no differences between the tribes of Dipsadinae in most of the reproductive characteristics, such as mean body size, relative size at sexual maturity, sexual size and tail dimorphism, duration of vitellogenesis or egg-carrying in oviducts. Key words: Dipsadinae; Fecundity; Follicular cycle; Reproduction; Sexual size dimorphism; Sexual tail dimorphism; Testicular cycle REPRODUCTIVE cycles of snakes vary from colubrid snake from tropical Australia (Tropi- highly seasonal to continuous. In temperate donophis mairii), abiotic factors such as areas, snakes usually reproduce only during seasonal availability of moist incubation con- the warmer months (usually spring) and many ditions were more important than biotic species present nonannual cycles. In tropical factors (e.g., higher predation on eggs or areas, however, cycles tend to be more hatchlings, or food availability for hatchlings) variable (Fitch, 1982; Seigel and Ford, on influencing reproductive timing. 1987). This higher variability can be partially Recent studies on the evolution of ecolog- explained by greater climatic complexity ical characters in Neotropical snakes have (Greene, 1997) and food availability in tropical shown that characters related to defense areas (Santos et al., 2005; Seigel and Ford, against predators seem to have diversified 1987). Climatic factors may be an important apparently quickly in Neotropical snakes, with variable affecting seasonality in reproductive a large amount of variation within clades (e.g., cycles of tropical snakes (Pizzatto and Martins, 1996). In contrast, habitat and Marques, 2002, 2006). For example, Brown microhabitat use, as well as diet and many and Shine (2006) provided evidence that, for a other characters related to feeding, seem to be conservative, i.e., they have experienced few changes during the lineage’s history and, 5 CORRESPONDENCE: e-mail, [email protected] consequently, the snake groups studied show 168 June 2008] HERPETOLOGICA 169 little contemporary variation in these charac- characters, such as sexual maturity and ters (e.g., Martins et al., 2001, 2002). Charac- dimorphism, body sizes, reproductive cycles ters related to reproduction in Neotropical and clutch size in snakes of the tribe snakes seem to be relatively conservative in Dipsadini; and (2) investigate how those some phylogenetic lineages (Almeida-Santos characters differ between the tribes Dipsadini and Saloma˜o, 2002; Almeida Santos at al., and Leptodeirini. 2006; Marques, 1996; Marques et al., 2006; Pizzatto and Marques, 2007; Pizzatto et al., MATERIALS AND METHODS 2007a, 2008), although in other groups even Original data on adult Leptodeira annulata closely related species may differ widely in (n 5 181), Imantodes cenchoa (n 5 36), their reproductive ecology (e.g., Marques, Sibynomorphus mikanii (n 5 144), S. neu- 1996). Despite the efforts to study the wiedi (n 5 126), and S. ventrimaculatus (n 5 reproductive biology of tropical snakes in the 111) were obtained from specimens deposit- last few decades (e.g., Balestrin and Di- ed in the collections of Instituto Butantan Bernardo, 2005; Marques, 1996; Pizzatto and (IB), Museu de Histo´ria Natural da Uni- Marques, 2002; Vitt, 1987), it is still not versidade Estadual de Campinas (ZUEC), possible to recognize patterns in many groups, Universidade Federal de Santa Maria especially in areas where species diversity is (ZUFSM), Pontifı´cia Universidade Cato´lica high, such as in the Neotropics (but see do Rio Grande do Sul (MCP), and Museu de Almeida-Santos and Saloma˜o, 2002). Histo´ria Natural do Capa˜o da Imbuia The subfamily Dipsadinae (Vidal et al., (MHNCI). Specimens of L. annulata were 2000; Zaher, 1999) is composed of small, collected in a range of localities between 11u slender snakes which occur from Mexico to 479 Nand23u 359 S, and 39u 439 Eand56u southern South America (Ferrarezzi, 1994; 059 W; those of I. cenchoa are from 21u 119 N Zaher, 1999). The monophyletism of Dipsa- to 26u 559 Sand45u 249 Eto52u 069 W; S. dinae is suggested by both morphological and mikanii from 20u 169 Nto23u 589 Sand45u molecular data (Cadle, 1984; Vidal et al., 2000; 429 Eto51u 209 W; S. neuwiedi from 20u 219 Wallach, 1995; Zaher, 1999), and the subfam- Nto25u 009 Sand40u 399 Eto49u 429 W; ily is apparently the sister group of all other and S. ventrimaculatus from 27u 289 Nto30u xenodontines (Vidal et al., 2000). Two appar- 529 Sand51u 019 Eto54u 289 W. For each ently monophyletic clades comprise the Dip- snake we collected data on: (1) snout–vent sadinae: the tribes Dipsadini, composed of length (SVL), (2) length of the right testis, (3) aglyphous, relatively smaller, earthworm/mol- diameter of deferent duct, proximal to the lusk-eating snakes (e.g., Adelphicos, Atractus, cloaca, (4) diameter of the largest ovarian Geophis, Ninia, Tropidodipsas, Sibon, Dipsas follicle or oviductal egg, and (5) number of and Sibynomorphus), and Leptodeirini, which well developed follicles in secondary vitello- is composed of aglyphous or opisthoglyphous, genesis (.10 mm) and eggs. relatively larger, lizard/frog-eating snakes Gravid S. mikanii and S. neuwiedi received (e.g., Eridiphas, Hypsiglena, Imantodes, Lep- at Instituto Butantan (IB) were kept in todeira and Pseudoleptodeira (see Cadle, captivity until oviposition. Data on other 1984; Cadle and Greene, 1993; Ferrarezzi, species of dipsadines were obtained from 1994; Martins and Oliveira, 1999; Rodrı´guez- published papers. In these cases we used only Robles et al., 1999; Vidal et al., 2000; Vitt, information that confirmed reproductive tim- 1996; Zaher, 1999). ing and fecundity in each species. Many As a further attempt to understand the published sources were not used because they extent to which reproductive characters of represent only a few, or casual, records that Neotropical snakes are conservative (cf. Al- were not conclusive or comparable to our meida-Santos and Saloma˜o, 2002), we here data. Data on testicular cycles of Hypsiglena explored the variation in reproductive ecology torquata, Leptodeira maculata, L. punctata in the subfamily Dipsadinae based on original and Ninia maculata came from histological and literature data. Specifically, our aim is to: analyses (Diller and Wallace, 1986; Goldberg, (1) conduct an overview of reproductive 2001, 2004a,b). 170 HERPETOLOGICA [Vol. 64, No. 2 Females were considered mature if they Yoshida, 1993). Variation in testis length and had follicles in secondary vitellogenesis, ovi- diameter of deferent duct (dependent vari- ductal eggs (cf. Shine, 1978) or folded ables) were compared among seasons (factors) oviducts (which indicate recent oviposition). using ANCOVA because both variables were Males were considered mature when they had significantly correlated to snake SVL (covari- turgid testes and convoluted deferent ducts ate) (Zar, 1999). (cf. Shine, 1980; Slip and Shine, 1988). A sexual size
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