ISZ-532 Souza E Lima Et Al.Indd
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Iheringia, Série Zoologia DOI: 10.1590/1678-476620141043299307 Sexual dimorphism in Amphisbaena nigricauda (Reptilia, Squamata, Amphisbaenidae) from Southeastern Brazil Francco A. N. de Souza e Lima¹, João Luiz Gasparini2, Antonio de Padua Almeida3, Marcos V. C. Vital4 & Tamí Mott4 1. Instituto de Biociências, Universidade Federal de Mato Grosso, 78060-900, Cuiabá, MT, Brazil. 2. Departamento de Ecologia e Oceanografia, Universidade Federal do Espírito Santo, 29060-900Vitória, ES, Brazil. 3. Instituto Chico Mendes de Conservação da Biodiversidade – Reserva Biológica de Comboios, 29900-970, Linhares, ES, Brazil 4. Instituto de Ciências Biológicas e da Saúde, Universidade Federal de Alagoas, 57072-970 Maceió, AL, Brazil. ([email protected]) ABSTRACT. Amphisbaena nigricauda Gans, 1966 is a small, poorly known amphisbaenid endemic to the restinga of the states of Espírito Santo and Bahia, Brazil. We analyze 178 specimens collected in Vitória municipality, state of Espírito Santo, Brazil, to investigate whether this species show sexual dimorphism in pre-cloacal pores and in morphological characters. Sex was determined by a ventral incision and direct inspection of gonads. A PCA analysis was performed to generate a general body size measurement. A T test and the non-parametric Mann-Whitney test were used to assess whether this species show sexual dimorphism on five morphometric and five meristic characters, respectively. Sex could not be determined in 36 specimens because they were mutilated in the posterior portion of their bodies. The diagnosis of the species is redefined based on this sample size: the smallest number of body annuli changes from 222 to 192, the number of dorsal and ventral segments in an annulus in the middle of the body changes to 9–11/13–16 (instead of 10/16), and the autotomic tail annulus lies between annulus 7–10 (instead of 6–9). The number of tail annuli remained within the known range of variation of the species (19–24). None of the 80 females analyzed showed pre-cloacal pores, whereas within males 59 out of 62 specimens displayed four and two specimens displayed five pre-cloacal pores. A single male did not possess pre-cloacal pores, but showed irregular scales on its cloacal region. Sex-based difference based on presence or absence of pre-cloacal pores as well as males with wider head was seen in other Neotropical amphisbaenids. However, a pattern of body size differences between males and females has not been identified so far in the few amphisbaenid species studied in this regard. Further studies on this taxonomic group are still needed to elucidate the existence of general patterns of sexual dimorphism and to identify the selective pressures driving these patterns. KEYWORDS. Amphisbaenia, Espírito Santo, restinga, sexual dimorphism. RESUMO. Dimorfismo sexual em Amphisbaena nigricauda (Reptilia, Squamata, Amphisbaenidae) do Sudeste do Brasil. Amphisbaena nigricauda Gans, 1966 é uma pequena anfisbênia pouco conhecida endêmica da restinga dos estados do Espírito Santo e Bahia, Brasil. Analisamos 178 indivíduos coletados no município de Vitória, Espírito Santo, Brasil, para verificar se esta espécie apresenta dimorfismo sexual nos poros pré- cloacais e em caracteres morfológicos. O sexo foi determinado por uma incisão ventral e inspeção direta das gônadas. Uma análise de PCA foi realizada para gerar uma medida geral do tamanho do corpo. O test-T e o teste de Mann-Whitney não paramétrico foram utilizados para avaliar se esta espécie apresenta dimorfismo sexual em cinco caracteres morfométricos e cinco merísticos, respectivamente. O sexo não pode ser determinado em 36 indivíduos porque eles estavam mutilados na parte posterior do corpo. O diagnóstico da espécie é redefinido com base nesta amostra: o menor número de anéis corporais alterou de 222 para 192, o número de segmentos dorsal e ventral em um anel no meio do corpo mudou de 9-11/13-16 (ao invés de 10/16), e o anel autotômico na cauda encontra-se entre 7-10 (ao invés de 6-9). O número de anéis caudais permaneceu dentro do intervalo de variação conhecida para a espécie (19-24). Nenhuma das 80 fêmeas analisadas apresentou poros pré-cloacais, enquanto que, dentro os 62 machos, 59 apresentaram quatro e dois indivíduos cinco poros pré-cloacais. Um único macho não tinha poros pré-cloacais, mas apresentava escamas irregulares em sua região cloacal. Diferença sexual quanto à presença ou ausência de poros pré-cloacais, assim como machos apresentando cabeças mais largas que a fêmeas, foi observada em outros anfisbenídeos neotropicais. No entanto, um padrão de diferenças de tamanho corporal entre machos e fêmeas não tinha sido identificado até agora nas poucas espécies de anfisbênias estudadas. Outros estudos com este grupo taxonômico ainda são necessários para elucidar a existência de padrões gerais de dimorfismo sexual e identificar as pressões seletivas que resultam estes padrões. PALAVRAS-CHAVE. Anfisbênias, Espírito Santo, restinga, dimorfismo. Amphisbaenia is a monophyletic group (TOWNSEND and ecology are poorly known (VEGA, 2001; NAVEGA- et al., 2004) of fossorial reptiles (Squamata) represented GONÇALVES, 2009). The typically small number of known by 184 taxa (UETZ, 2014). Among the six families (VIDAL specimens also limits knowledge of morphological variation et al., 2008), the Amphisbaenidae include the majority in many species, including sex-based differences. (n = 169, 91.8%) of amphisbaenian species (UETZ, 2014) The morphometric studies of amphisbaenids that distributed mainly in Africa, Central and South America have been performed indicate that sexual dimorphism may (STRÜSSMANN & MOTT, 2009). Brazil harbors the highest be common. WEbb et al. (2000) compared total length and diversity of amphisbaenians worldwide (MOTT & VIEITES, head width of two African species Monopeltis anchietae 2009) with 69 species currently catalogued in the country (Bocage, 1873) and Zygaspis quadrifrons (Peters, 1862) (BÉRNILS & COSTA, 2012; ROBERTO et al., 2014). (Amphisbaenidae), observing that females of Monopeltis Due to amphisbaenians’ fossorial habits, collecting have wider head than males and females of Zygaspis have specimens is frequently difficult. Consequently, the larger body than males. Conversely, GIL et al. (1993) descriptions of many species are based on a limited number and MÁRTIN et al. (2012) observed that males of Blanus of specimens and almost all aspects of their basic biology cinereus (Vandelli, 1797) (Blanidae) and Trogonophis Iheringia, Série Zoologia, Porto Alegre, 104(3):299-307, 30 de setembro de 2014 300 SOUZA E LIMA et al. wiegmanni Kaup, 1830 (Trogonophiidae) respectively mm) endemic to the states of Espírito Santo and Bahia, have wider head than females. For Bipes biporus (Cope, Brazil (DIAS & ROCHA, 2005; SILVA-SOARES et al., 2011). 1894) (Bipedidae), head shape does not differ between The type series consists of three specimens (a female, sexes (KEARNEY, 2003). For Neotropical amphisbaenids, a juvenile and a male) collected in 1964 at Sooretama sex-based morphological differences were investigated Refuge (now the Reserva Biológica de Sooretama – Fig. for Amphisbaena alba Linnaeus, 1758 (COLLI & ZAMBONI, 1) in the municipality of Linhares (19°00’S, 40°08’W), 1999); Amphisbaena kingii (Bell, 1833) and Amphisbaena state of Espírito Santo, Brazil. A large series of this species munoai Klappenbach, 1960 (BALESTRIN & CAPPELLARI, was obtained in the municipality of Vitória, Espírito Santo 2011); Amphisbaena ibijara Rodrigues, Andrade & Lima, State by one of the authors (JLG) - one of the specimens 2003 and Leposternon polystegum (Duméril, 1851) (GOMES from this series was used to extend the species known et al., 2009); Leposternon wuchereri (Peters, 1879) and distribution ca. 135 km southeast (SILVA-SOARES et al., Leposternon microcephalum Wagler, 1824 (FILOGONIO et al., 2011). Here, we use this series of 178 specimens to analyze 2009); and Amphisbaena prunicolor (Cope, 1885) (MACIEL variation in morphological characters and to assess sex- et al., 2012). These studies generally found that females are based differences in this poorly known species. larger than males (exception to Leposternon microcephalum whereas total length do not differ, and L. polystegum MATERIAL AND METHODS whereas males are larger than females), following the same pattern found in other squamate reptiles (SHINE, 1994). All specimens of Amphisbaena nigricauda were Another sexual dimorphism detected in amphisbaenids collected from July 2005 to November 2006 when vegetation is related to the presence/absence of pre-cloacal pores: was suppressed by bulldozers during expansion of airport in contrast to males some female amphisbaenids such as facilities in the restinga (coastal sand-dune vegetation) of Amphisbaena kingii (VEGA, 2001), A. dubia L. Müller, 1924, Praia de Camburi (20°16’16”S, 40°16’35”W), Vitória, A. heathi Schmidt, 1936 (VANZOLINI, 2002), A. uroxena Espírito Santo, Brazil (Fig. 1). Vitória municipality Mott, Rodrigues, Freitas & Silva, 2008 and A. anaemariae comprises a main area located on an island within a bay, and Vanzolini, 1997 (MOTT et al., 2011) do not show pores. a northern portion located on the mainland, where Camburi Amphisbaena nigricauda Gans, 1966 is a small and is located. The climate is Aw Tropical (KÖPPEN, 1936) with slender amphisbaenid (maximum Snout Vent Length= 105 an annual mean temperature of 23°C and precipitation of Fig. 1. Geographic distribution of Amphisbaena nigricauda Gans, 1966: 1, type locality, Linhares municipality; 2, Vitória