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Feeding Ecology of Sidewinder Rattlesnakes, Crotalus Cerastes (Viperidae)

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Feeding Ecology of Sidewinder Rattlesnakes, Crotalus Cerastes (Viperidae) Herpetologica, 72(4), 2016, 324–330 Ó 2016 by The Herpetologists’ League, Inc. Feeding Ecology of Sidewinder Rattlesnakes, Crotalus cerastes (Viperidae) 1 2 MICHAEL M. WEBBER,TEREZA JEZKOVA , AND JAVIER A. RODRIGUEZ´ -ROBLES School of Life Sciences, University of Nevada, Las Vegas, 4505 Maryland Parkway, Las Vegas, NV 89154, USA ABSTRACT: Dietary studies are important for understanding predator–prey relationships and species interactions because they provide information on the trophic resources available to predators and their potential impact on prey populations. We relied on stomach contents of museum specimens and literature records to examine ontogenetic (size-related), sexual, seasonal, and geographic variation in the feeding habits of Sidewinders, Crotalus cerastes. Sidewinders fed primarily on lizards and slightly less frequently on mammals; birds and snakes were rarely consumed. The vast majority of C. cerastes consumed single prey items ingested head-first. Juvenile and adult female Sidewinders consumed lizards and mammals with similar frequency. We observed an ontogenetic shift in feeding patterns of adult male C. cerastes because they included more mammals in their diets, compared with juvenile males. Sidewinders are classic ambush (sit-and-wait) predators and, as predicted by theory, actively foraging lizards and mammals comprise a considerable fraction of their prey. We documented seasonal shifts in the feeding patterns of Sidewinders, with snakes consuming a greater proportion of lizards during early spring and autumn, and a greater percentage of mammals during late spring and summer. This dietary shift likely results from seasonal changes in the activity patterns of C. cerastes, because individuals can be diurnally active during early spring and autumn but are predominantly nocturnal during late spring and summer. Adult male and female Sidewinders from the Mojave and the Sonoran deserts consumed similar proportions of lizards and mammals. Our findings regarding the trophic habits of C. cerastes contribute to our understanding of the ecology of terrestrial, venomous predators. Key words: Diet; Foraging; Mojave Desert; Prey; Serpentes; Sonoran Desert; Variation DIET IS a fundamental aspect of an animal’s biology. movements occur in early spring and in the autumn, Foraging and feeding are critical ecological tasks that supply particularly during the morning or late in the afternoon the energy required for growth, maintenance, and repro- (Ernst and Ernst 2003). Sidewinders exhibit a classic ambush duction (Pianka 2000). Dietary studies are important for foraging strategy in which they wait in a cratered or coiled understanding predator–prey relationships because they position for suitable prey to come into close proximity (Secor provide information on predators’ fundamental trophic 1994a). resources and their potential impact on prey populations Herein, we tested specific hypotheses regarding the (Martınez-Guti´ errez´ et al. 2015). Foraging and feeding feeding ecology of C. cerastes, and assessed geographic behavior influence basic organismal features, including variation in the diet of this snake. Several species of large- habitat selection (Custer and Galli 2002), movement patterns bodied snakes incorporate a greater proportion of larger prey (Vedder 1984; Kreiter and Wise 2001), thermoregulatory in their diets, compared with smaller-bodied individuals regimes (Regal 1966; Lang 1979), and ultimately fitness (e.g., Mackessy 1988; Santos et al. 2007; Glaudas et al. 2008). (Selman and Houston 1996). Elucidating the underlying Accordingly, we predicted that Sidewinders experience an causes of variation in these traits thus provides valuable ontogenetic (size-related) shift in feeding behavior, in which information regarding the overall biology of a predator and snakes incorporate larger prey into their diets as the serpents its trophic niche within an ecosystem (Young et al. 2010; increase in body size (Klauber 1972; Secor 1994a). Brasil et al. 2011; Thoren´ et al. 2011; Rosca et al. 2013). Knowledge of the predominant foraging mode of a predator Sidewinders, Crotalus cerastes Hallowell 1854, are allows assessments of how aspects of the animal’s feeding relatively small-bodied serpents (50–60-cm adult snout–vent biology may covary with foraging mode (Huey and Pianka length [SVL]; Ernst and Ernst 2003) that inhabit sandy 1981). Sidewinders are ambush foraging predators; there- washes, dunes, and flatlands of the warm deserts of fore, we predicted that they predominantly feed upon southwestern North America (Campbell and Lamar 2004; actively foraging (mobile) species. The aforementioned Fig. 1). The species is reported to be moderately sexually temporal change in the activity patterns of Sidewinders led dimorphic, with females attaining larger body sizes than to the prediction that they primarily eat diurnal prey (lizards) males (Reiserer 2001; Campbell and Lamar 2004). Males when the snakes are active during the day, and switch to achieve sexual maturity at a smaller body size (SVL ¼ 34 cm) mainly crepuscular and nocturnal prey (mammals) when the than females (SVL ¼ 38 cm), based on the body size of the serpents are predominantly active at night. Finally, we smallest reproductive individual of each sex (Reiserer 2001). investigated geographic variation in the feeding ecology of C. Sidewinders can be found near or within rodent burrows, or cerastes. coiled in self-constructed depressions (a behavior known as ‘‘cratering’’) beneath desert vegetation (Secor 1994a; Steb- MATERIALS AND METHODS bins 2003). The snakes are usually considered nocturnal; We checked the stomach contents of individual C. almost all summer activity takes place at night, but diurnal cerastes by making a midventral incision in 1086 specimens from the following institutions: California Academy of 1 Sciences, San Francisco (CAS; n ¼ 142); Natural History PRESENT ADDRESS: Department of Ecology & Evolutionary Biology, P.O. Box 210088, University of Arizona, Tucson, AZ 85721, USA Museum of Los Angeles County, Los Angeles, California 2 CORRESPONDENCE: e-mail, [email protected] (LACM; n ¼ 344); Museum of Vertebrate Zoology, 324 WEBBER ET AL.—FEEDING ECOLOGY OF CROLATUS 325 University of California, Berkeley (MVZ; n ¼ 295); and the Department of Ecology and Evolutionary Biology, Univer- sity of Arizona, Tucson (UAZ; n ¼ 305). We did not examine type specimens or especially soft, brittle, or otherwise fragile specimens, and we excluded individuals that might have been fed in captivity before being preserved. Our data set also incorporates published dietary reports of C. cerastes (cf. Rodrıguez-Robles´ 1998) after accounting for redundancy between accounts (e.g., Klauber 1931, 1972). When possible for each snake, we recorded the following variables: locality data, date of collection, body size (SVL, 6 1.0 cm), body mass (6 0.1 g), sex (determined by inspection of the reproductive tract), taxonomic identity of the prey, direction of prey ingestion (inferred from orientation in the gut), number of prey items, and prey mass (6 0.1 g). We weighed snakes and their intact or slightly digested prey after blotting and draining them briefly in a towel to remove excess fluid. Body measurements of partially digested items were estimated by comparison with intact conspecifics of similar size available at the Marjorie Barrick Museum of Natural History, University of Nevada, Las Vegas (MBM; the MBM collection was acquired by the MVZ in September 2009). We relied on this limited data set (n ¼ 15) to obtain an estimate of mean relative prey mass (RPM), the ratio of prey mass to predator mass. Most prey items were considerably digested, and in those instances we assigned an average adult mass obtained from preserved specimens or from literature records to species of lizards (Miller 1951; Vitt et al. 1981; Degenhardt et al. 1996; Turner 1998; Wright 2002; Newbold 2005; Mosher and Bateman 2014), mammals (Burt and Grossenheider 1980; Jameson and Peeters 2004), and birds (Alsop 2001) consumed by C. cerastes, an approach used in prior studies (e.g., Clark 2002; FIG. 1.—Approximate distribution of Sidewinders, Crotalus cerastes (grey Weatherhead et al. 2009; Dugan and Hayes 2012). Based on shading; after Campbell and Lamar 2004), and approximate boundaries of the distribution of these estimates of prey mass, we divided the Mojave and Sonoran deserts (dotted lines) in southwestern North America. Circles indicate the georeferenced locations of male (filled circles) prey into smaller (,30 g) and larger (30 g) prey, and female (open circles) snakes that contained prey in their stomachs. irrespective of prey type. The smaller prey category consisted of lizards (e.g., Coleonyx variegatus [Western Banded Gecko], 2.7 g; Urosaurus spp. [tree and brush southwestern Arizona (Funk 1965), southern Nevada (Clark lizards], ,3.8 g), mammals (e.g., Chaetodipus spp. [Pocket 1968), and southeastern California (Secor 1994a). We Mice], ,23 g; Reithrodontomys megalotis [Western Harvest combined these data with records from our examination of Mice], 11.5 g), and birds (e.g., Cardellina pusilla [Wilson’s a larger number of specimens from across the species’ Warblers], 8.5 g). The larger prey category included lizards distribution to investigate geographic variation in feeding (e.g., Dipsosaurus dorsalis [Desert Iguanas], 39.8 g; patterns of Sidewinders. Specifically, the distribution of C. Gambelia wislizenii [Long-nosed Leopard Lizards], 36.4 g), cerastes extends into two physiographic regions of
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