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Morphology and Diet of Two Sympatric Colubrid Snakes, Chironius flavolineatus and Chironius Quadricarinatus (Serpentes: Colubridae)

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Morphology and Diet of Two Sympatric Colubrid Snakes, Chironius flavolineatus and Chironius Quadricarinatus (Serpentes: Colubridae) Amphibia-Reptilia 29 (2008): 149-160 Morphology and diet of two sympatric colubrid snakes, Chironius flavolineatus and Chironius quadricarinatus (Serpentes: Colubridae) Roberta Richard Pinto1,3,∗, Ronaldo Fernandes1,3, Otavio Augusto Vuolo Marques2,3 Abstract. The morphometry and diet of two sympatric species of Chironius (C. flavolineatus and C. quadricarinatus) from Brazilian Cerrado are described. The two snake species differ in external morphology, as Chironius flavolineatus was the largest species (body, tail and eyes) whereas C. quadricarinatus the heaviest. Each species also showed marked sexual size dimorphism. In terms of dietary ecology, both species feed exclusively on frogs with a heavy preference for hylids and may have tendency to eat small items, as noticed in other colubrine species. These two snake species showed a brownish colour pattern and exhibited no ontogenetic variation, suggesting that juveniles and adults use similar substrates. Chironius flavolineatus and C. quadricarinatus present a semi-arboreal habit, with active foraging behaviour, feeding in the ground most of time. Chironius flavolineatus uses higher vegetation for resting and, based on morphological results, seems to be more arboreal than C. quadricarinatus. Keywords: Cerrado, Chironius, food habits, morphometrics, Serpentes, sexual dimorphism, South America. Introduction Uruguay (Dixon, Wiest and Cei, 1993; Hol- lis, 2006). This genus is composed by diur- Snake morphology can be influenced by habitat nal, semi-arboreal, frog-eating snakes (Dixon, use, diet, and reproductive constraints (Vitt and Wiest and Cei, 1993; Marques and Sazima, Vangilder, 1983; Martins and Oliveira, 1999). 2004). Two of the species, C. flavolineatus (Jan, Often, body shape is related to substrate use 1863) and C. quadricarinatus (Boie, 1827) oc- (Cadle and Greene, 1994; Marques, 1998; Lil- cur mainly in the Brazilian Cerrado, a landscape lywhite and Henderson, 2001; Martins et al., with a predominance of open vegetation (Eiten, 2001). Thus, morphometric measurements can 1978; Ab’Saber, 2003; Faria and Araujo, 2004), provide insights on the substrate use and pos- and are broadly sympatric with each other. Chi- sibly ontogenetic and intraspecific differences ronius flavolineatus is distributed from east of in diet (Arnold, 2001; Hartmann and Marques, Marajó Island, State of Pará to savanna areas 2005). These measurements are easily obtained of northeastern Brazil, although it is more com- from preserved animals in scientific collections mon in Central, Northwestern, and Southwest- and show little difference in size and mass from ern Brazil whereas C. quadricarinatus occurs in live specimens (Reed, 2001). Central, Northwestern, and Southwestern Brazil The colubrid snake genus Chironius Fitzinger, (cf. Peters and Orejas-Miranda, 1970; Dixon, 1826 is endemic of the Neotropical region com- Wiest and Cei, 1993). prising 20 species distributed from Nicaragua to southern Brazil, northern Argentina and Some ecological information are available for Atlantic Forest species (Chironius bicarinatus, C. exoletus, C. fuscus, C. foveatus and C. laevi- 1 - Departamento de Vertebrados, Museu Nacional, Univer- collis) (Dixon, Wiest and Cei, 1993; Marques, sidade Federal do Rio de Janeiro, Quinta da Boa Vista, s/n, São Cristóvão, 20940-040 Rio de Janeiro, RJ, Brasil Eterovic and Sazima, 2001; Marques and Saz- 2 - Laboratório de Herpetologia, Instituto Butantan. Av. Vi- ima, 2004; Rodrigues, 2007) but, apart from tal Brasil, 1500, Butantan, 05503-900 São Paulo, SP, anecdotal information of C. flavolineatus and Brasil 3 - Fellow of Conselho Nacional de Desenvolvimento Cien- C. quadricarinatus (e.g. Dixon, Wiest and Cei, tífico e Tecnológico (CNPq) 1993; Feio et al., 1999; Argôlo, 2004; Marques ∗Corresponding author; e-mail: [email protected] et al., 2005), no study has been published on the © Koninklijke Brill NV, Leiden, 2008. Also available online - www.brill.nl/amre 150 R.R. Pinto, R. Fernandes, O.A.V. Marques ecology of these snakes. The present work pro- 1999). Interactions were checked in all tests and described vides new information on morphometry, sexual when present. All variates were natural log transformed. We used a significance index of P<0.05 for all analyses. dimorphism, diet, and inference of substrate use of these two sympatric species. Results Materials and methods Morphometrics We examined 338 specimens (Chironius flavolineatus n = Variation between sexes. — In terms of mor- 167; C. quadricarinatus, n = 171) housed in the follow- ing herpetological collections: Museu Nacional, Universi- phological variation, some differences between dade Federal do Rio de Janeiro (MNRJ), Rio de Janeiro, sexes in each snake species were evident. Fe- RJ; Instituto Butantan (IBSP), São Paulo, SP; Universi- males of both species were significantly larger dade Estadual de Campinas (ZUEC), Campinas, SP; Museu = de Ciências e Tecnologia, PUCRS (MCP), Porto Alegre, than their respective males (F1,252 13.53; RS; Coleção Herpetológica da Universidade de Brasília P<0.001; table 1). However the reverse (CHUNB), Brasília, DF; Museu de Zoologia da Univer- was found in both species when examining tail sidade Federal de Viçosa (MZUFV), Viçosa, MG; Museu de Ciências Naturais da PUC Minas (MCN-R), Belo Hor- length and eye size, as males had significantly izonte, MG. The examined specimens and localities are longer tails (F1,213 = 8.72; P<0.01; table 1) listed in the appendix. and larger eyes (F = 5.74; P<0.05; ta- The following data were taken from each specimen 1,249 (measures were modified from Vitt, 1987 and Oliveira, ble 1). In contrast, no sexual dimorphisms were 2003): (1) sex; (2) snout-vent length (SVL); (3) tail length found when examining variation in head size (TAL); (4) head length (HL); (5) eye diameter (ED); (6) and body mass. body mass (M); (7) reproductive maturity or immaturity; and (8) stomach contents. Males were considered mature if The proportions of tail length correspond they had enlarged testes and opaque defferent ducts (Shine, to 39.9% and 38.9% of total length in males 1982). Females were considered mature if they had either and females of C. flavolineatus, respectively, ovarian follicles in secondary vitellogenesis or oviduct eggs (Shine, 1980a); the total (TL = SVL + TAL) and trunk while in C. quadricarinatus this proportion was lengths (T = SVL − HL) were also calculated. 37.8% and 36.9% in males and females, respec- All food items in the stomach were removed and iden- tified (sensu previous Frost et al., 2006; Grant et al., 2006) tively. to the lowest possible taxonomic level. Additionally, each Variation between species. —Ourmor- item was measured and weighed. Vestigial items were also phological data showed consistent differences compared by linear regressions to complete specimens de- posited in Museu Nacional, UFRJ to estimate their length between snake species: Chironius flavolinea- and mass (cf. Hirai and Matsui, 2001). We performed sim- tus was larger (SVL) than C. quadricarinatus ple regression in order to verify a tendency of prey choice (F1,252 = 46.82; P<0.001), and the former (see Marques and Sazima, 2004; Hartmann and Marques, = 2005) for these snake species. For these regression analy- had longer tails (F1,213 129.98; P<0.001) ses, only adults (frogs and snakes) were used. than the latter species. Relative head size in C. We calculate sexual size dimorphism index (SSD) (cf. quadricarinatus appeared to be larger than in C. Shine, 1994) in order to recognize a tendency for male- = male combat in species. The degree of SSD was calculated flavolineatus (F1,249 84.53; P<0.001; ta- as (mean adult SVL of the larger sex/mean adult SVL of ble 1). However the marginally significant inter- the smaller sex) − 1 (see Gibbons and Lovich, 1990; Shine, action (F1,249 = 4.21; P = 0.04) may confound 1994). All linear measures were taken with a dial calliper to these results. As to body mass, C. quadricari- the nearest 0.01 mm, except for snout-vent and tail lengths, natus was significantly heavier than C. flavolin- which were taken with a flexible ruler to the nearest 1.0 mm. eatus (F1,179 = 20.10; P<0.001; table 1). Body mass was recorded to the nearest 0.01 g (cf. Mar- tins et al., 2001). Gravid females were excluded from this Chironius flavolineatus had larger eyes than C. analysis to avoid bias. The sample included only mature quadricarinatus (F1,249 = 30.82; P<0.001). specimens and statistics analyses were made using STATIS- TICA program for Windows version 6.0 (Statsoft, 2001). In- tersexual and interespecific variation were evaluated under Diet MANOVA, in the case of SVL, and MANCOVA, in case of TAL (with SVL as covariate), HL (with T as covariate), M Prey taxa. — Chironius flavolineatus and C. (with TL as covariate) and ED (with HL as covariate) (Zar, quadricarinatus fed exclusively on anurans, Morphology and diet of Chironius flavolineatus and C. quadricarinatus 151 Table 1. Morphometric aspects of adults Chironius flavolineatus and C. quadricarinatus. Mean ± SD. Measures in millimeter (mm). Mass in gram (g). Measures Chironius flavolineatus Chironius quadricarinatus Snout-vent length 714.28 ± 64.59 670.95 ± 77.18 645.16 ± 57.29 621.60 ± 69.11 (SVL) r = 606-894; r = 507-880; r = 478-812; r = 504-77; n = 68 n = 40 n = 91 n = 57 Tail length 450.95 ± 42.14 438.54 ± 51.00 375.36 ± 33.44 377.37 ± 38.48 (TAL) r = 350-566; r = 325-552; r = 300-471; r = 268-464; n = 57 n = 37 n = 72 n = 52 Total length 1158.35 ± 99.46 1100.27 ± 116.82 1016.04 ± 91.49 998.75 ± 99.71 (TL) r = 963-1382; r = 832-1384;
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