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Sexual Dimorphism, Reproductive Biology, and Dietary Habits of Psammophiine Snakes (Colubridae) from Southern Africa Author(S): Richard Shine, William R

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Sexual Dimorphism, Reproductive Biology, and Dietary Habits of Psammophiine Snakes (Colubridae) from Southern Africa Author(S): Richard Shine, William R Sexual Dimorphism, Reproductive Biology, and Dietary Habits of Psammophiine Snakes (Colubridae) from Southern Africa Author(s): Richard Shine, William R. Branch, Jonathan K. Webb, Peter S. Harlow, and Terri Shine Source: Copeia, 2006(4):650-664. 2006. Published By: The American Society of Ichthyologists and Herpetologists DOI: http://dx.doi.org/10.1643/0045-8511(2006)6[650:SDRBAD]2.0.CO;2 URL: http://www.bioone.org/doi/ full/10.1643/0045-8511%282006%296%5B650%3ASDRBAD%5D2.0.CO%3B2 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. Copeia, 2006(4), pp. 650–664 Sexual Dimorphism, Reproductive Biology, and Dietary Habits of Psammophiine Snakes (Colubridae) from Southern Africa RICHARD SHINE,WILLIAM R. BRANCH,JONATHAN K. WEBB,PETER S. HARLOW, AND TERRI SHINE Slender-bodied, diurnal ‘‘sand snakes’’ of the genus Psammophis are widespread and abundant through Africa, but the general biology of these animals remains poorly known. For example, sexual dimorphism is unstudied because it is difficultto determine the sex of live specimens (uniquely among snakes, the male hemipenis is vestigial). Our dissections of 700 preserved specimens provide detailed ecological information on ten psammophiine species from southern Africa. Males grow larger than females in most taxa, especially in species of large absolute body size. However, sex differences in body proportions (relative head size, relative tail length) are minor. Females produce small clutches (generally ,10 eggs), with larger clutches in larger females in some but not all species. Psammophylax tritaeniatus differs from the nine Psammophis species studied in its higher fecundity and its primary reliance on mammalian rather than reptilian prey. Within Psammophis, five species (P. brevirostris, P. jallae, P. leopardinus, P. subtaeniatus, P. trigrammus) fed mostly on scincid lizards, two (P. namibensis, P. notostictus) fed mostly on lacertid lizards, and two (P. trinasalis, P. mossambicus) took approximately equal numbers of lizards and mammals. Although dietary composition thus varied with snake species and body size, conspecific males and females took similar prey types. Thus, despite reports of unusual mating systems in captive psammophiines, these snakes exhibit only minor sexual dimorphism in size, bodily proportions, and dietary habits. UR current understanding of snake ecology The phylogenetic relationships of psammo- O is derived disproportionately from a rela- phiine snakes have been clarified only recently. tively small subset of taxa that occur in North Bogert (1940) first grouped the genera Hemi- America and Europe, with much less information rhagerrhis, Cerastes (5Psammophylax), Malpolon, on adaptive radiations in other parts of the world Dromophis, Psammophis, and Rhamphiophis, based (e.g., Seigel and Ford, 1987). Although recent on the absence of hypapophyses on the posterior work has seen a significant reduction in this bias vertebrae, possession of small, unornamented, (Akani et al., 2002, 2003a, b), there remain many and fusiform hemipenes with an undivided speciose groups for which available published sulcus, and grooved posterior maxillary teeth. data are fragmentary at best. One of the best Subsequently, Broadley (1990) revived Dipsina examples involves the Psammophiinae, a lineage (Jan, 1863) to accommodate D. multimaculata of about 40 to 50 species of slender-bodied (previously placed in Rhamphiophis), and the snakes distributed through Africa, Madagascar, Madagascan genus Mimophis was shown to be Asia, and Europe (Broadley, 1977, 2002; Branch, allied to the group (Nagy et al., 2003). Although 1998; de Haan, 2003a). Most psammophiines are the monophyly of psammophiines is well-estab- diurnal, fast-moving terrestrial snakes, although lished (Kelly et al., 2003; Nagy et al., 2003, 2005), some are arboreal and others burrow in loose their familial relationships remain contentious, sand (Branch, 1998). Characteristic of relatively not least because of the lack of hemipenial open habitats rather than thick forests, the features. Although Rasmussen (1985) included psammophiines are active hunters that chase them within the Colubrinae, Cadle (1994) found down their prey (Branch, 1998). In both general significant albumin divergence between the two morphology (notably, slender body form) and groups, suggesting an earlier divergence. Psam- foraging modes, these snakes are highly conver- mophiines share high chromosomal numbers gent with distantly-related lineages of ‘‘whip- (Branch, 1980) with other, mainly African, snakes’’ in other parts of the world (e.g., the lineages such as the Lamprophiinae, Pseudoxyr- Australian elapid Demansia; the North American ophiinae, Atractaspididae, and Elapidae, and this colubrid Masticophis; the South American colu- grouping is maintained in recent molecular brids Leimadophis and Liophis;theEuropean colubroid phylogenies (Vidal and Hedges, 2002; Coluber: Stewart, 1971; Shine, 1980; Vitt and Nagy et al., 2003, 2005). There is conflict over the Vangilder, 1983). taxonomic levels (families or subfamilies) cur- # 2006 by the American Society of Ichthyologists and Herpetologists SHINE ET AL.—BIOLOGY OF PSAMMOPHIINE SNAKES 651 rently afforded lineages within this clade, but for tus), two are oviparous but with maternal convenience we continue to treat sand snakes attendance of the clutch (P. rhombeatus, P. multi- and their relatives as a subfamily within the squamis), and one is viviparous (P. variabilis: artificial ‘Colubridae,’ although we note that Broadley, 1977; De Villiers, 1995; Branch, 1998). Kelly (2005) has proposed familial status for the Lastly, observations of captive specimens suggest lineage, which probably had an Oligocene or a uniquely complex social system in psammo- early Miocene origin in northeastern Africa phiines (de Haan, 1984, 2003a, b). (Kelly, 2005). Frustratingly, little is known about the ecology Recent molecular studies (Kelly, 2005) have of these animals in the field, despite their shown that existing generic boundaries within abundance over a wide region. Recent detailed the psammophiines are confused. Rhamphiophis autecological studies in Nigeria have clarified the is polyphyletic, with ‘R.’ acutus sister to Psammo- biology of one species (Akani et al., 2002, 2003a), phylax, while Dromophis lineatus is nested within but our inability to determine the sex of living Psammophis (D. praeornatus was not assessed). psammophiines poses a major logistical problem Rhamphiophis and Malpolon together form the for investigation of sex differences in morphol- most basal psammophiine clade, while Hemirha- ogy and ecology. For this reason, dissection of gerrhis and Mimophis are sister taxa. There preserved specimens in museum collections remains confusion over species boundaries with- provides an ideal initial step for any investigation in the Psammophis phillipsi-mossambicus complex, of psammophiine ecology and especially, sexual particularly in the western regions. Kelly (2005; dimorphism. unpubl. obs.) has noted no significant genetic divergence between typical P. phillipsi and P. MATERIALS AND METHODS mossambicus, and Hughes and Wade (2004) have revived P. occidentalis for West African popula- We measured and dissected preserved speci- tions (to which many previous studies on P. mens of ten psammophiine species from south- phillipsi are probably referable, e.g., Akani et al., ern Africa (south of 17uS latitude, corresponding 2002, 2003a). Butler’s (1993) material is probably to the northern borders of Namibia, Botswana, composite, possibly including species currently and Zimbabwe) in the collections of the Trans- referred to P. occidentalis, P. mossambicus, and P. vaal Museum and the Port Elizabeth Museum in sibilans, and is here referred to as P. ‘phillipsi’. the Republic of South Africa, and the State We use the recent taxonomy of Broadley (2002), Museum of Namibia and the Directorate of with additional updates (Hughes and Wade, Wildlife Conservation (both in Windhoek, Nami- 2004; Kelly, 2005) for analyses in the current bia). Identification of all specimens was verified paper. (by WRB) at the time that we gathered ecological Psammophiine snakes display a series of un- and morphological data, and has been updated usual features in their reproductive biology. For with respect to subsequent taxonomic changes. example, the hemipenes of males are virtually For each animal we recorded snout–vent length vestigial tubelike structures, in strong contrast to (henceforth, SVL), tail length, head length the large and elaborately spinous hemipenes of (from the posterior margin of the lower jaw to most snake taxa (Dowling and Savage, 1960; the
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