Herpetology Notes, volume 11: 329-335 (2018) (published online on 22 April 2018)

Sexual dimorphism in two species of Sibynomorphus (Squamata, Dipsadidae) from Brazil

Tatiane Parnazio1 and Davor Vrcibradic1,*

Abstract. Snakes are usually sexually dimorphic in both morphology and pholidosis. Members of the Neotropical tribe Dipsadini (Dipsadidae) commonly have unusual patterns of sexual dimorphism regarding the numbers of ventral scales (higher in males or non-dimorphic). The northern (trans-Andean) species of Sibynomorphus apparently deviate from the typical dipsadine pattern, but there is little data currently available on the southern (cis-Andean) members of the genus. We tested for differences in some morphological and meristic characters between males and females of two cis-Andean species of Sibynomorphus [S. mikanii (Schlegel, 1837) and S. neuwiedi (Ihering, 1911)]. Preserved specimens from Brazilian institutional collections were analysed with respect to snout-vent length (SVL), relative length of the tail, and ventral and subcaudal scale counts. Both species had patterns of sexual dimorphism typical of most snakes with regard to SVL (larger in females), relative length of the tail and subcaudal scale counts (both greater in males). Regarding ventral counts, however, S. neuwiedi showed no sexual dimorphism (as is common among Dipsadini), whereas in S. mikanii females had a significantly greater number of ventrals than males (as in most snakes, including trans-Andean Sibynomorphus).

Keywords: Dipsadini, Dipsadinae, morphology, pholidosis, scalation, snake

Introduction et al., 1997). The larger size of females in most snake species is commonly attributed to an adaptive advantage Snakes can be sexually dimorphic in various of large size in enhancing reproductive success (e.g., phenotypic traits, such as the size of certain organs Semlitsch and Gibbons, 1982; Shine, 1994), as fertility and/or glands (Bonnet et al., 1998; Kissner et al., 1998), and/or production of larger-bodied offspring is generally degree of keeling of some scales (Layne and Steiner, positively related to female body size in squamate 1984; Maritz and Alexander, 2011), colour pattern reptiles (Fitch, 1985). On the other hand, the greater (Shine and Madsen, 1994; Marques and Sazima, 2003), relative length of the tail in males is due to the “extra head shape and dimensions (Camilleri and Shine, 1990; space” at the tail base for accommodating the hemipenes Shine, 1991) and, especially, body size and relative and their retractor muscles (Klauber, 1943; King, 1989), tail size, with females usually growing longer and/or though it may also have an adaptive function, such as bulkier and having proportionally shorter tails than aiding in the removal of other males during reproductive males (e.g., Klauber, 1943; Fitch, 1981; Pearson et al., aggregations (King, 1989; Shine et al., 1999). Such 2002; Pizzatto et al., 2008). morphological differences between sexes are usually Sexual dimorphism in body size in snakes could be paralleled by pholidosis, with females normally having explained by differences between the sexes in the costs higher numbers of ventral scales (reflecting their longer involved with reproduction (Shine, 1978; Madsen bodies) and males usually having more subcaudal scales and Shine, 1994; Rivas and Burghardt, 2001), though (reflecting their longer tails; Shine, 1993). in some cases it may also be related to ecological The tribe Dipsadini (sensu Harvey et al., 2008; segregation between the sexes (Shine, 1993; Branch family Dipsadidae, subfamily Dipsadinae) consists of the Neotropical genera Dipsas, Plesiodipsas, Sibon, Sibynomorphus and Tropidodipsas. It is a speciose group of nocturnal, predominantly arboreal molluscivorous snakes distributed from Mexico to northern Argentina 1 Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Estado do Rio de Janeiro. Av. (Peters, 1960; Wallach et al., 2014). Among the Dipsadini, Pasteur 458, Urca, 22240-290, Rio de Janeiro, Brazil sexual dimorphism in various traits has been reported * Corresponding author. E-mail: [email protected] for a number of species (e.g., Cadle, 2007; McCranie, 330 Tatiane Parnazio & Davor Vrcibradic

2007; Harvey and Embert, 2008; Pizzatto et al., 2008). collections of several institutions in Brazil, including the Notably, some studies have reported unusual patterns of Museu Nacional (MNRJ), the Universidade Federal do sexual dimorphism in the number of ventral scales for Rio de Janeiro (ZUFRJ), and the Universidade Federal species in the genus Dipsas, with males having ventral do Estado do Rio de Janeiro (UNIRIO; all in the city counts either higher than or equal to those of females of Rio de Janeiro), the Instituto Vital Brazil (IVB; in (Cadle, 2005; Harvey and Embert, 2008; Barros et al., Niterói, state of Rio de Janeiro), the Instituto Butantan 2012). Based on data from Kofron (1988, 1990), Cadle (IBSP) and the Museu de Zoologia da Universidade de (2007) speculated that the same phenomenon might also São Paulo (MZUSP; both in the city of São Paulo, state occur in species of Sibon and Tropidodipsas (=Sibon of São Paulo), and the Museu Paraense Emílio Goeldi sensu Kofron, 1985), and data from McCranie (2007) (MPEG; in Belém, state of Pará). Specimens identified seem to corroborate that hypothesis. Thus, a relatively in collections as S. mikanii septentrionalis or whose high number of ventrals in males (compared to females) provenance was from the general area of occurrence may be a widespread trait among the Dipsadini. The of that taxon in the states of Maranhão and Pará (see genus Sibynomorphus Fitzinger, 1843, however, does Freitas et al., 2014) and other adjacent states in northern not appear to follow this trend. This genus currently and northeastern Brazil were not included in the present consists of twelve recognized species and has a disjunct study, as the taxonomic status of that subspecies has distribution: six species are distributed east of the Andes not been assessed since its original description by and south of the Amazonian domain in Argentina, Brazil, Cunha et al. (1980) and there is the possibility that it Paraguay, Uruguay and Bolivia and the other six occur could be specifically distinct from the nominal form; west of the northern Andes in Ecuador and Peru (Cadle, thus, in order to prevent the risk of analysing data from 2007; Wallach et al., 2014). For the six trans-Andean a heterogeneous sample we only included specimens species, patterns of sexual dimorphism in pholidosis are assignable to S. m. mikanii as representatives of the not different from those presented by most Dipsadidae species in our analyses. and for snakes in general, with females tending to have Sexing of individuals was performed by making a more ventrals and less subcaudals in comparison to small incision at the base of the tail to check for the males (Cadle, 2007). As for the species occurring east of presence of hemipenial muscles, except when males the Andes, however, the little information available does had the hemipenes everted or in cases when animals not show a clear pattern regarding sexual dimorphism. had been previously opened (in which case sexing was Cunha et al. (1980) reported sexual dimorphism in the done by direct observation of the gonads). For each number of ventrals for S. mikanii septentrionalis Cunha, individual, the measurements of snout-vent length Nascimento and Hoge, 1980, with females tending to (SVL) and tail length (TL) were taken with the aid of have higher counts. On the other hand, data from a measuring tape with 1 mm precision, and counts of Scrocchi et al. (1993) for S. lavillai Scrocchi, Porto and ventral and subcaudal scales were performed under a Rey, 1993 suggest that males and females of that species stereomicroscope, following Dowling (1951). In some do not differ in ventral counts (see Cadle, 2007). specimens of S. mikanii the occurrence of “half-split” ventrals was observed, but those were not included In the present study we analyse the differences in in the counts; according to King (1959), these scales certain morphological (SVL and relative tail length) correspond to anomalous vertebral duplication and thus and meristic (numbers of ventral and subcaudal scales) should not be counted. Since the subcaudal scales of the characters between males and females of two common species analysed are divided, the counts were performed species of Sibynomorphus occurring east of the Andes following the trend of counting only the scales on one and south of the Amazon: S. mikanii and S. neuwiedi. side (in this case the right side) and including the single Our aim is to check whether those species have patterns terminal scale (Schmidt and Davis, 1941). of sexual dimorphism typical or atypical compared to Data normality was verified using the Kolmogorov- those observed in other snakes of the tribe Dipsadini. We Smirnov test. Differences between sexes in SVL and discuss our results in light of what is currently known of scale counts were tested by One-Way Analysis of the phylogenetic relationships of dipsadine snakes. Variance (ANOVA), and inter-sexual differences in relative tail length were tested by Analysis of Covariance Materials and Methods (ANCOVA) using SVL as the covariate. The degree For the present study we analysed preserved specimens of sexual size dimorphism (SSD) was estimated for of Sibynomorphus mikanii and S. neuwiedi from reptile each species by dividing the mean SVL of the larger Sexual dimorphism in two species of Sibynomorphus from Brazil 331 sex by that of the smaller sex, and subtracting 1.0 from Discussion the resulting value (see Shine, 1994). For analyses Our results confirm that females of both S. mikanii involving measurements of SVL and TL, we considered and S. neuwiedi grow larger than conspecific males. only sexually mature animals, based on the minimum This trend has been previously observed by Pizzatto et size (SVL) of reproductive males and females of each al. (2008) for these two species and for other species species reported by Pizzato et al. (2008). Statistical of the tribe Dipsadini (including another congener, S. analyses were performed using the language R (R Core ventrimaculatus). Cadle (2007) also observed a general Team, 2015). trend of females growing larger than males in the trans- Andean species of Sibynomorphus [except for S. vagus Results (Jan, 1863), in which no pattern was evident due to the A total of 202 individuals of S. mikanii and 148 of S. small sample size]. Males growing larger than females neuwiedi were analysed in the present study. Females or a lack of sexual dimorphism are often observed in had significantly greater mean SVLs than males in species in which fighting behaviour occurs between both species (S. mikanii: F1,139 = 77.70; p < 0.001; S. males during the breeding season (Shine, 1994). Male- neuwiedi: F1,105 = 56.98; P < 0.001; Table 1). The SSD male combat is not known to occur in dipsadines, except ratio was higher for S. neuwiedi (0.233) than for S. for Imantodes cenchoa (Linnaeus, 1758) (see Pizzatto et mikanii (0.213). al., 2008). Thus, it is not surprising that females are the Although females of both species had higher mean larger sex in Sibynomorphus spp. The indices of SSD absolute values of TL than males (Table 1), the analyses estimated in our study (0.21 for S. mikanii and 0.23 for of covariance showed that the length of the tail relative S. neuwiedi) were comparable to those (0.24 – 0.27) to SVL was greater in males for both S. mikanii (F1,1,138 reported for three species of Sibynomorphus (including

= 62.31; P < 0.001) and S. neuwiedi (F1,1,104 = 45.13; P the two studied herein) by Pizzatto et al. (2008), and < 0.001). This is also shown by the greater proportion of higher than those calculated for other species of tail length relative to body length (mean TL/SVL ratio) Dipsadini by those authors. These data suggest that in males of both S. mikanii (males: 25.3%; females: Sibynomorphus spp. (or at least the cis-Andean species 21.8%) and S. neuwiedi (males: 31.0%; females: 27.0 in this genus) are the most sexually dimorphic of the %). dipsadines. In S. mikanii, females had significantly higher numbers Both species were also sexually dimorphic in relative of ventral scales than males (F1,198 = 36.10; P < 0.001), tail length, with males having proportionally longer tails but in S. neuwiedi there was no significant inter-sexual than females. Unsurprisingly, this was also reflected in difference in the number of ventrals (F1,142 = 0.50; P = the subcaudal counts, which were also significantly 0.478; Table 1). Males had a higher mean number of higher for males. These results are also in agreement subcaudals compared to females in both S. mikanii with what has been reported by other authors for various

(F1,192 = 125.06; P < 0.001) and S. neuwiedi (F1,142 = species of Dipsadini (Cadle 2007, Pizzatto et. al., 2008, 94.85; P < 0.001) (Table 1). Harvey and Embert, 2008), indicating that members of

Table 1. Mean values (± 1 SD, with ranges and sample sizes in parentheses) of snout-vent length (SVL), tail length (TL), and numbers of ventral and subcaudal scales for Sibynomorphus mikanii and S. neuwiedi. Measurements of SVL and TL are given only for sexually mature individuals. Whenever there are statistically significant (P < 0.05) differences between sexes in relative Table 1. Mean values (± 1 SD, with ranges and sample sizes in parentheses) of snout-vent length (SVL), tail length (TL), and numbers of ventral and subcaudal scales for Sibynomorphus mikanii (for TL) or absoluteand S. valuesneuwiedi (for. Measurements the other variables)of SVL and TLthe are sex given with only the for larger sexually value mature is shownindividuals. in bold.Whenever there are statistically significant (P < 0.05) differences between sexes in relative (for TL) or absolute values (for the other variables) the sex with the larger value is shown in bold.

Species sex SVL (mm) TL (mm) Ventrals Subcaudals S. mikanii ♂♂ 348.1 ± 36.7 88.1 ± 10.2 162.8 ± 4.4 52.9 ± 3.0 (280–445, N = 61) (65–115, N = 61) (154–176, N = 87) (42–59, N = 83) ♀♀ 422.3 ± 57.3 92.0 ± 16.4 166.9 ± 5.0 47.4 ± 3.6 (339–571, N = 80) (64–150, N = 80) (157–181, N = 113) (39–59, N = 111) S. neuwiedi ♂♂ 406.1 ± 67.9 126.1 ± 25.2 171.7 ± 6.0 73.0 ± 4.2 (255–565, N = 45) (72–195, N = 45) (159–185, N = 54) (61–85, N = 54) ♀♀ 500.7 ± 61.1 134.9 ± 14.0 171.1 ± 5.2 65.0 ± 4.4 (415–688, N = 62) (101–170, N = 62) (159–183, N = 90) (56–76, N = 90)

1

332 Tatiane Parnazio & Davor Vrcibradic that tribe do not differ from the majority of snakes with on molecular data, the paraphyly of Dipsas relative to regard to sexual dimorphism in tail length and number Sibynomorphus and the polyphyly of Sibynomorphus of subcaudal scales. have been recovered in all of them (Zaher et al., 2009, Unlike the other traits mentioned above, the pattern of 2014; Vidal et al., 2010; Grazziotin et al., 2012; Pyron sexual dimorphism in number of ventral scales differed et al., 2015; Figueroa et al., 2016). Studies that included between the two species tested in our study: females of four to five species of this genus (Grazziotin et al., S. mikanii had a significantly higher mean number of 2012; Zaher et al., 2014; Pyron et al., 2015, Figueroa ventrals than males, whereas in S. neuwiedi the sexes did et al. 2016) have consistently recovered them in two not differ with respect to that trait (even though females clades, each having closer relationships with species had a significantly greater mean SVL than males). Data in other dipsadine genera than with each other (albeit from Peters (1960) also show largely overlapping ranges usually with weak support). Interestingly, S. neuwiedi of ventral counts for males (165-182) and females (167- and S. mikanii were never recovered within the same 181) of S. neuwiedi (at that time still regarded as a clade, even though the former was considered a subspecies of S. mikanii), although mean values were not subspecies of the latter until relatively recently (Hoge et given​​ in that work. Our analyses thus confirm that there al., 1981). Considering that in the genera Dipsas, Sibon is no relevant difference in the number of ventral scales and Tropidodipsas males tend to have either equal or between males and females of this species. However, greater ventral scale counts than females (which is Peters (1960) also gave overlapping ranges of ventrals unusual among snakes), this characteristic may possibly for males and females of S. mikanii, with the range for represent a synapomorphy of the Dipsadini. In this case, females (153-177) totally encompassing the range for the condition observed in S. mikanii (and, presumably, males (155-171), whereas our data revealed female- other species closely related to it) could represent a biased sexual dimorphism in that trait for this species. secondary reversal to the “normal” pattern (i.e. females Thus, considering only the ranges of values as evidence tending to have higher ventral counts), since this species for absence of sexual dimorphism can be misleading. is deeply embedded within the dipsadine clade (Zaher Peters (1960), however, included in his sample some et al., 2009, 2014; Grazziotin et al., 2012). The only specimens from the southern Brazilian state of Rio trans-Andean species of Sibynomorphus that has so far Grande do Sul which he considered “intermediate” been included in a molecular phylogeny is S. vagus, between typical mikanii and neuwiedi and for which which was not recovered as closely related to either he suggested that the epithet garmani could be used S. neuwiedi or S. mikanii (Figueroa et al., 2016). This to designate this population as a distinct subspecies would imply at least two independent occurrences of (although he considered his data insufficient to propose reversal to the “normal” pattern of sexual dimorphism such an action). Nevertheless, it has been since proposed in number of ventral scales in the Dipsadini. However, in an unpublished thesis (see Cadle, 2007, p. 185) that it is premature to make such inferences, since the S. garmani (Cope, 1887) should be regarded as a valid knowledge of relationships among dipsadine taxa is species (though it is still officially maintained in the still in a very incipient state, with the few phylogenies synonymy of S. mikanii; Wallach et al., 2014). Thus, available presenting conflicting results, low support Peters’s (1960) sample of S. mikanii mikanii may have for many clades, and low taxon coverage (Zaher et al., been a composite of more than one taxon (F. L. Franco, 2009, 2014; Vidal et al., 2010; Grazziotin et al., 2012; pers. comm.), which limits the utility of comparisons Pyron et al., 2015; Figueroa et al., 2016). Inclusion of with our data. It is also noteworthy that Cunha et al. more Sibynomorphus species (especially trans-Andean (1980) found female-biased sexual dimorphism in ones) in future phylogenetic studies may shed more ventral scale counts for S. m. septentrionalis, as we did light on the evolution of sexual dimorphism patterns in for the nominal subspecies. This suggests that the taxon the Dipsadini. septentrionalis may be related to mikanii rather than to neuwiedi (which was also considered a subspecies of mikanii by Cunha et al., 1980). Acknowledgments. We thank P. Passos and R. Fernandes The results above are interesting if we consider (MNRJ), A. Melgarejo (IVB), F. L. Franco (IBSP), A. L. Prudente (MPEG), D. S. Fernandes (ZUFRJ), and H. Zaher (MZUSP) for the current (and still very limited) knowledge about allowing us to access specimens deposited in collections under phylogenetic relationships within the Dipsadini. their care. Besides, F. L. Franco also reviewed the manuscript. We Although only two to five species of Sibynomorphus are also grateful to A. R. Martins and M. Soares for their helpful have so far been included in phylogenetic studies based suggestions to improve this work. Sexual dimorphism in two species of Sibynomorphus from Brazil 333

References Colubridae) and review of morphological characters of Dipsadini. Herpetological Monographs 22: 106–132. Barros, T.R., Jadin, R.C., Caicedo-Portilla, J.R., Rivas, G.A. Hoge, A.R., Laporta, I.L., Romano-Hoge, S.A. (1981 “1978/79”): (2012): Discovery of a rare snail-eater snake in Venezuela Notes on Sibynomorphus mikanii Schlegel 1837. Memórias do (Dipsadinae, Dipsas pratti), with additions to its natural history Instituto Butantan, 42/43: 175–178. and morphology. Zoosystematics and Evolution 88: 125–134. King, W. (1959): Vertebra duplication, an osteological anomaly Bonnet, X., Shine, R., Naulleau, G., Vacher-Vallas, M. (1998): widespread in snakes. Herpetologica, 15: 87–88. Sexual dimorphism in snakes: different reproductive roles King, R.B. (1989): Sexual dimorphism in snake tail length: favour different body plans. Proceedings of the Royal Society of sexual selection, natural selection, or morphological constraint. London B, Biological Sciences 265: 179–183. Biological Journal of the Linnean Society 38: 133–154. Branch, W.R., Shine, R., Harlow, P.S., Webb, J.K. (1997): Sexual Kissner, K.J., Forbes, M.R., Secoy, D.M. (1998): Sexual dimorphism dimorphism, diet and aspects of reproduction of the western in size of cloacal glands of garter snake, Thamnophis radix keeled snake, Pythonodispsas carinata (Serpentes: Colubridae). haydeni. Journal of Herpetology 32: 268–270. African Journal of Herpetology 46: 89–97. Klauber, L.M. (1943): Tail-length differences in snakes, with notes Cadle, J.E. (2005): Systematics of snakes of the Dipsas oreas on sexual dimorphism and the coefficient of divergence. Bulletin complex (Colubridae: Dipsadinae) in western Ecuador and Peru, of the Zoological Society of San Diego 18: 1–60. with revalidation of D. elegans (Boulenger) and D. ellipsifera Kofron, C.P. (1985): Systematics of the neotropical gastropod- (Boulenger). Bulletin of the Museum of Comparative Zoology eating snake genera Tropidodipsas and Sibon. Journal of 158: 67–136. Herpetology 19: 84–92. Cadle, J.E. (2007): The snake genus Sibynomorphus (Colubridae: Kofron, C.P. (1988): Systematics of neotropical gastropod-eating Dipsadinae: Dipsadini) in Peru and Ecuador, with comments snakes: the sartorii group of the genus Sibon. Amphibia-Reptilia on the systematics of Dipsadini. Bulletin of the Museum of 9: 145–168. Comparative Zoology 158: 183–284. Kofron, C.P. (1990): Systematics of neotropical gastropod eating Camilleri, C., Shine, R. (1990): Sexual dimorphism and dietary snakes: the dimidiata group of the genus Sibon, with comments divergence: differences in trophic morphology between male on the nebulata group. Amphibia-Reptilia 11: 207–233. and female snakes. Copeia 1990: 649–687. Layne, J.N., Steiner, T.M. (1984): Sexual dimorphism in occurrence Cunha, O.R., Nascimento, F.P., Hoge, A.R. (1980): Ofídios da of keeled dorsal scales in the eastern indigo snake (Drymarchon Amazônia XII. Uma subespécie nova de Sibynomorphus mikanii corais couperi). Copeia 1984: 776–778. do noroeste do Maranhão (Ophidia: Colubridae, Dipsadinae). Madsen, T., Shine, R. (1994): Costs of reproduction influence the Boletim do Museu Paraense Emilio Goeldi, Série Zoologia 103: evolution of sexual size dimorphism in snakes. Evolution 48: 1–15. 1389–1397. Dowling, H.G. (1951): A proposed standard system of counting Maritz, B., Alexander, G.J. (2011): Morphology, sexual dimorphism ventrals in snakes. British Journal of Herpetology 1: 97–99. and growth in the smallest viperid, Bitis schneideri (Reptila: Figueroa, A., McKelvy, A.D., Grismer, L.L., Bell, C.D., Lailvaux, Squamata: Viperidae). Journal of Herpetology 45: 457–462. S.P. (2016): A species-level phylogeny of extant snakes with Marques, O.A.V., Sazima, I. (2003): Bothrops jararacussu description of a new colubrid subfamily and genus. PloS ONE (Jararacussu). Sexual dichromastism. Herpetological Review 11(9):e0161070. doi:10.1371/journal.pone.0161070. 34: 62. Fitch, H.S. (1981): Sexual size differences in reptiles. Miscellaneous McCranie, J.R. (2007): A second new species of Sibon (Squamata: Publications of the Museum of Natural History, University of Colubridae) from La Mosquitia, Northeastern Honduras. Kansas 70: 1–72. Herpetologica 63: 213–218. Fitch, H.S. (1985): Clutch and litter size variation in New World Pearson, D.J., Shine, R.,Williams, A. (2002): Geographic variation reptiles. Miscellaneous Publications of the Museum of Natural in sexual size dimorphism within a single snake species (Morelia History, University of Kansas 76: 1–76. spilota, Pythonidae). Oecologia 131: 418–426. Freitas, M.A., Almeida, B.J.L., Almeida, M.S.M., Danin, Peters, J.A. (1960): The snakes of the subfamily Dipsadinae. T.S., Moura, G.J.B. (2014): Rediscovery and first record of Miscellaneous Publications of the Museum of Zoology, Sibynomorphus mikanii septentrionalis (Cunha, Nascimento & University of Michigan 114: 1–224. Hoge, 1980), (Squamata; Serpentes) for the state of Pará. Check Pizzatto, L., Cantor, M., Oliveira, J.L., Marques, O.A.V., List 10: 1246-1248. Capovilla, V., Martins, M. (2008): Reproductive ecology of Grazziotin, F.G., Zaher, H., Murphy, R.W., Scrocchi, G., Benavides, Dipsadine snakes, with emphasis on South American species. M.A., Zhang, Y.P., Bonatto, S.L. (2012): Molecular phylogeny Herpetologica 64: 168–179. of the New World Dipsadidae (Serpentes: Colubroidea): a Pyron, R.A., Guayasamin, J.M., Peñafiel, N., Bustamante, L., reappraisal. Cladistics 28: 437–459. Arteaga, A. (2015): Systematics of Nothopsini (Serpentes, Harvey, M.B., Embert, D. (2008): Review of Bolivian Dipsas Dipsadidae), with a new species of Synophis from the Pacific (Serpentes: Colubridae), with comments on other South Andean slopes of southwestern Ecuador. ZooKeys 541: 109– American species. Herpetological Monographs 22: 54–105. 147. Harvey, M.B., Rivas-Fuenmayor, G., Caicedo, J.R., Rueda- R Core Team. (2015): R: A language and environment for statistical Almonacid, J.V. (2008): Systematics of the enigmatic dipsadine computing. R Foundation for Statistical Computing, Vienna, snake Tropidodipsas perijanensis Alemán (Serpentes: Austria. 334 Tatiane Parnazio & Davor Vrcibradic

Rivas, J.A., Burghardt, G.M. (2001): Understanding sexual size Appendix 1. Specimens examined. dimorphism in snakes: wearing the snake’s shoes. Animal Behaviour 62: 1–6. Sibynomorphus mikanii Schmidt, K.P., Davis, D.D. (1941): Field book of snakes of the BRAZIL: GOIÁS: MNRJ 9352 (Alto Paraíso de United States and Canada. New York, USA, G. P. Putnam’s Goiás); MNRJ 7813 (Amaro Leite); MZUSP 17788 Sons. Scrocchi, G., Porto, M., Rey, L. (1993): Descripción de una especie (Buritinópolis); MZUSP 16900, 16903, 16905, 16909– nueva y situación del género Sibynomorphus (Serpentes: 10 (Cavalcante); MPEG 24945, 24948–50, 24952–53 Colubridae) en la Argentina. Revista Brasileira de Biologia 53: (Goiânia); MNRJ 7996–98 (Ipameri); MZUSP 3778 197–208. (Jataí); MZUSP 17690 (Luziânia); MZUSP 16728 Semlitsch, R.D., Gibbons, J.D. (1982): Body size dimorphism and (Mambaí); MNRJ 4882, MZUSP 11006, 16913, sexual selection in two species of water snakes. Copeia 1982: 16915, 20454–58, 20461–62, 20464–66 (Minaçu); 974–976. MZUSP 9046 (Nova Olinda); MNRJ 19217, 21183 Shine, R. (1978): Sexual size dimorphism and male combat in snakes. Oecologia 33: 269–277. (Ouvidor); MZUSP 12495 (Petrolina de Goiás); MNRJ Shine, R. (1991): Intersexual dietary divergence and the evolution 23607 (Pirenópolis). MATO GROSSO: ZUFRJ 780 of sexual dimorphism in snakes. American Naturalist 138: (Diamantino); MZUSP 3753 (Luciara); IBSP 50224 103–122. (Paranatinga); MPEG 21967 (Querência); IBSP 70729 Shine, R. (1993): Sexual dimorphism in snakes. In: Snakes: (Sinop). MATO GROSSO DO SUL: MZUSP 10140–42 Ecology and Behavior, p. 49-86. Seigel, R.A., Collins, J.T. 2nd (Campo Grande); MZUSP 10143 (Corumbá). MINAS Edition. New York, USA, McGraw-Hill. GERAIS: IVB 1627 (Albertina); MNRJ 18934, 19407, Shine, R. (1994): Sexual size dimorphism in snakes revisited. 21104 (Catas Altas); IBSP 79495 (Consolação); MNRJ Copeia 1994: 326–346. Shine, R., Madsen, T. (1994): Sexual dichromatism in snakes of 23717–18 (Contagem); MZUSP 14963 (Cristina); the genus Vipera: a review and a new evolutionary hypothesis. MZUSP 1631 (Delfinópolis); IBSP 81175 (Extrema); Journal of Herpetology 28: 114–117. MNRJ 15228, 15267, 15294–96, 15455, 15397, 17162, Shine, R., Olsson, M.M, Moore, I.T., Lemaster, M.P., Mason, R.T. 17191–92, 17260, 17772, 20230 (João Pinheiro); (1999): Why do male snakes have longer tails than females? MNRJ 1329–34, 1986 (Lagoa Santa); MNRJ 24523 Proceedings of the Royal Society of London B, Biological (Matias Barbosa); IBSP 84197 (Passos); MNRJ 18727, Sciences 266: 2147–2151. 18729 (Patos de Minas); ZUFRJ 1747 (Pedralva); Vidal, N., Dewynter, M., Gower, D.J. (2010): Dissecting the major American snake radiation: A molecular phylogeny of ZUFRJ 1214, 1237 (Porteirinha); IBSP 85496 (Pouso the Dipsadidae Bonaparte (Serpentes, Caenophidia). Comptes Alegre); MNRJ 9026 (Três Marias). PARANÁ: IBSP Rendus Biologies 333: 48–55. 78504 (Foz do Iguaçu); MNRJ 9087 (Nova Concórdia); Wallach, V., Williams, K.L., Boundy, J. (2014): Snakes of the IBSP 16354–55 (Uraí). SÃO PAULO: MNRJ 14027 World: A Catalogue of Living and Extinct Species. CRC Press, (Alumínio); MNRJ 19198 (Anhembi); MNRJ 19188 USA. (Araraquara); MNRJ 14025 (Atibaia); MNRJ 19927, Zaher, H., Grazziotin, F.G., Cadle, J.E., Murphy, R.W., Moura- 20477 (Bofete); MNRJ 18549, 19184–86, 19189–93, Leite, J.C. (2009): Molecular phylogeny of advanced snakes 19197, 19199–202, 19204–05, 19295, 19318, 20469, (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: a revised classification and descriptions of new 20476, 20502, 20510, 20736–37, 20800, 20864, 20876, taxa. Papéis Avulsos de Zoologia (São Paulo) 49: 115–153. 21605, 21614, 21737, 21749, 21752, 21771, 21808, Zaher, H., Grazziotin, F.G., Campagner, M., Jared, C., Antoniazzi, 21871, 21874, 21891, 21912, 21935, 21977, 21983, M.M., Prudente, A.L. (2014): Consuming viscous prey: a novel 21989, 21990, 22033, 22078, 22084, 22114, 22182, protein-secreting delivery system in neotropical snail-eating 22232, 22238, 22653–55, 22878–83, 23026 (Botucatu); snakes. BMC Evolutionary Biology 14: 58. IBSP 80744, 85202, 85412, 85552, MNRJ 17452 (Bragança Paulista); MNRJ 12734–35 (Carapicuíba); ZUFRJ 179, 247, 779 (Catanduva); MNRJ 14028 (Embu das Artes); MZUSP 11535 (Itanhaém); MNRJ 12738–39 (Itapevi); MZUSP 12350 (Itu); MNRJ 14026 (Jandira); MZUSP 10764 (Leme); MNRJ 17451 (Osasco); MNRJ 12736 (Porto Feliz); MZUSP 8629 (Piracicaba); MNRJ 19195 (Registro); MNRJ 21996, MZUSP 8285, 8288 (Ribeirão Preto); IBSP 78408, 81179, MNRJ 12737 (Santana de Parnaíba); IBSP 85032 (São Caetano do Sul). TOCANTINS: MZUSP Sexual dimorphism in two species of Sibynomorphus from Brazil 335

10749 (Cristalândia); IBSP 78452 (Figueirópolis); 19520 (Mendes); IVB 152, 154, 578–79, MNRJ 4873, MZUSP 12700–01 (Guaraí); MZUSP 14604, 15763 7519, 8283–84, 20873 (Nova Friburgo); MNRJ 22037, (Lajeado); MZUSP 10743–44, 10746, 10748, 10750 23632 (Nova Iguaçu); MNRJ 21836 (Paracambi); IVB (Porto Nacional); MZUSP 17670, 17872 (São Salvador 3079 (Paraíba do Sul); IVB 410, 896, MNRJ 9044, do Tocantins). 9343, MZUSP 5172 (Petrópolis); MNRJ 4890 (Piraí); MNRJ 14505 (Porciúncula); MNRJ 12444, 12646, Sibynomorphus neuwiedi 13181, 13119, 14054, 14100, 14433–34, 14674, 15333, 17112, 17868, 18399, 18425, 18478, 19095 (Resende); BRAZIL: ALAGOAS: MNRJ 19285 (Murici). MNRJ 11336, 17172, 19171–72, 19489, 20773, 23300, BAHIA: MNRJ 23073 (Itagibá); MNRJ 19618 23303 (Rio Claro); MNRJ 7803, 15105, 15578 (Rio (Trancoso). ESPÍRITO SANTO: MNRJ 8140 das Flores); IVB 244, MNRJ 18086 (Rio de Janeiro); (Cariacica); MNRJ 23363 (Guarapari); MNRJ 702, MNRJ 23218 (São Sebastião do Alto); IVB 608, 621, 23721(Santa Tereza); MNRJ 8139, 23720, 23722–23 644 (Três Rios); MNRJ 16495 (Valença); MNRJ 10038, (Venda Nova do Imigrante); MZUSP 14404 (PARNA 17317 (Volta Redonda). SANTA CATARINA: MNRJ do Caparaó). MINAS GERAIS: MNRJ 17855, 19969, 10635 (Blumenau); MNRJ 689–90, 692, 695 (Corupá); 24241, 24561 (Catas Altas); MNRJ 11332, 11335, 14624 MZUSP 15700–01 (Guaramirim); MZUSP 13230, (Espera Feliz); MNRJ 14127–28, 14504 (Faria Lemos); 17227 (Jaraguá do Sul); MNRJ 698 (Joinville); MNRJ IVB 1558 (São João do Manhuaçu). PARANÁ: MZUSP 20209 (Palhoça). SÃO PAULO: MNRJ 14040, MZUSP 8062 (Ipiranga). RIO DE JANEIRO: IVB 2317, MNRJ 12892, 12934 (Arujá); MZUSP 15257 (Bertioga); 7802, 7806, 8059, 9785, 23275–77, 24211, UNIRIO MNRJ 19187, 20719, 21911 (Botucatu); MNRJ 10634 55–59 (Angra dos Reis, Ilha Grande); IVB 2441, MNRJ (Igaratá); MZUSP 21248 (Itanhaém); MNRJ 14039 7791, 7800 (Bom Jardim); MNRJ 12346 (Cachoeiras (Jacupiranga); MZUSP 12833 (Mogi das Cruzes); de Macacu); MNRJ 7795–98 (Carmo); MNRJ 17842, MZUSP 12733 (Pariquera-Açu); MZUSP 20912 18596 (Casimiro de Abreu); MNRJ 15572, 15577 (Paraibuna); MNRJ 17459 (Salesópolis); MNRJ 10633, (Comendador Levy Gasparian); MNRJ 15592, 16538, MZUSP 12405, 18067 (São Bernardo do Campo); 17489, 18277 (Duque de Caxias); MNRJ 4887 MZUSP 15221 (São Miguel Arcanjo); MZUSP 12824 (Engenheiro Paulo de Frontin); MNRJ 24246 (Macaé); (Ubatuba). MNRJ 15943, UNIRIO 60 (Mangaratiba); MNRJ

Accepted by Andrew Durso