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Gape Size and Evolution of Diet in Snakes: Feeding Ecology of Erycine Boas

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Gape Size and Evolution of Diet in Snakes: Feeding Ecology of Erycine Boas J. Zool., Lond. (1999) 248,49±58 # 1999 The Zoological Society of London Printed in the United Kingdom Gape size and evolution of diet in snakes: feeding ecology of erycine boas Javier A. RodrõÂ guez-Robles*, Christopher J. Bell{ and Harry W. Greene{ Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, CA 94720-3160, U.S.A. (Accepted 5 August 1998) Abstract The Macrostomata accounts for more than 85% of extant snakes and is characterized by increased mobility of the jaws and increased gape size. We used stomach contents of museum specimens and speci®c literature records to describe the food habits of a basal clade of macrostomatan snakes ± the erycine boas (Erycinae) ± with an emphasis on the North American Charina bottae. Mammals, lizards, birds, and squamate eggs composed 66%, 17%, 7%, and 5%, respectively, of the prey of C. bottae. Smaller C. bottae fed on squamate eggs and lizards, whereas larger snakes added mammals and birds to their diet, and ceased to take squamate eggs. Ten of 12 snakes with multiple prey had eaten nestling birds or mammals, and snakes that ate multiple prey were not signi®cantly larger than those that had single prey. Charina trivirgata and C. reinhardtii also prey on mammals, whereas species of Eryx feed mainly on mammalian prey, but also eat lizards and occasionally birds. Evolutionarily more basal groups of snakes primarily feed on elongate prey, which suggests that innovations of the feeding apparatus of macrostomatans allowed these snakes to eat heavier and bulkier prey, particularly mammals. Erycines appeared and diversi®ed at approximately the same geological time as rodents, suggesting that rodents perhaps constituted an abundant prey resource that favoured the diversi®cation of early macrostomatans. Key words: Boidae, Charina, Eryx, feeding ecology, fossil record, gape size INTRODUCTION history of the group. With that broader goal, we used stomach contents of museum specimens and a survey For gape-limited predators such as snakes that swallow of literature records to describe the feeding ecology their prey whole, foraging success (i.e. mass eaten per of erycine boas, a basal clade of macrostomatan unit time) likely increases with maximum ingestible prey snakes. size, other factors being equal (Forsman & Lindell, Extant snakes are divided into two major clades: 1993). Consequently, selection on traits in¯uencing Scolecophidia (blindsnakes of three families) and swallowing performance has probably been strong Alethinophidia (all other snakes; Fig. 1). Macrostomata throughout the evolutionary history of snakes, as accounts for approx. 95% of Alethinophidia and com- implied by the various morphological adaptations prises boas and sand boas (Boidae), pythons facilitating the ingestion of larger prey by more recently (Pythonidae), Round Island boas (Bolyeriidae), dwarf evolved ophidian clades (Greene, 1983a; Pough & boas (Tropidophiidae), Australasian ®lesnakes (Acro- Groves, 1983; Cundall, 1987; Rieppel, 1988; Cundall & chordidae), vipers and pitvipers (Viperidae), stiletto Greene, in press). Studying the feeding biology of a snakes (Atractaspididae), racers, ratsnakes, water- particular group of snakes in a phylogenetic context and snakes, etc. (Colubridae), and cobras, mambas, with an adequate fossil record should help elucidate coralsnakes, seasnakes, etc. (Elapidae). The clade is factors that signi®cantly in¯uenced the evolutionary characterized by, among other traits, morphological synapomorphies correlated with increased mobility of the jaws and increased gape size (Rieppel, 1988; Cundall *All correspondence to: Javier A. RodrõÂ guez, Museum of Vertebrate & Greene, in press), hence the name Macrostomata Zoology, University of California, Berkeley, CA 94720-3160, U.S.A. E-mail: [email protected] (`big mouth'). { Present address: Department of Geological Sciences, University of Species of Erycinae, currently classi®ed within Boidae Texas at Austin, Austin, TX 78712-1101, U.S.A. (Fig. 1), are found in North America, Europe, Asia, and { Present address: Section of Ecology and Systematics, Division of Biological Sciences, Cornell University, Ithaca, N.Y. 14853-2701, Africa. Traditional taxonomic treatments recognized U.S.A. two monotypic genera (Charina, Lichanura) in North 50 J. A. RodrIÂ guez-Robles, C. J. Bell and H. W. Greene Scolecophidia Serpentes Leptotyphlopidae Anomalepididae Typhlopidae Anomochilus Uropeltidae Cylindrophis Anilius scytale Xenopeltis Alethinophidia Loxocemus bicolor Boinae Charina reinhardtii Charina bottae Charina trivirgata Eryx Pythonidae Bolyeriidae Tropidophiidae Macrostomata Acrochordidae Boidae Viperidae Atractaspididae Erycinae Colubridae Elapidae Fig. 1. Phylogenetic relationships among extant snakes, emphasizing those of erycine boas, Charina and Eryx (after Cadle, 1988; Cundall, Wallach & Rossman, 1993; Kluge, 1993). America, with Old World species placed in one or two southern California to the tip of Baja California, and genera (an all-encompassing Eryx or a restricted Eryx eastward to western Arizona and the state of Sonora in with Gongylophis to accommodate the species conicus, northwestern Mexico (Yingling, 1982). Rosy boas occur colubrinus, muelleri,andwhitakeri; Das, 1991; Tokar, in deserts and rocky shrubland and can be active at 1995, 1996). Kluge (1993) documented 16 synapomor- night, dusk, or in the daytime (Klauber, 1931; H. W. phies placing the Calabar burrowing `python' Greene, pers. obs.). Charina reinhardtii inhabits forested (traditionally placed in the monotypic Calabaria) within habitats of equatorial west and central Africa (Kluge, the Erycinae, and argued for the recognition of two 1993). Fourteen species of Eryx (sand boas) occupy named clades of erycines: Eryx to include the Old primarily deserts and steppes (although E. conicus also World sand boas (see also Szyndlar & Schleich, 1994); occurs in luxuriant forests) from northern and western and Charina to include the North American forms plus Africa, northward to the Balkan peninsula and northern C. reinhardtii (Calabar burrowing boa), a taxonomic coasts of the Caspian Sea in eastern Europe, and east- arrangement we follow herein (Fig. 1). ward throughout India, Sri Lanka, western China and The two species of New World erycines, Charina Mongolia (Wall, 1911; Sorensen, 1988; Kluge, 1993). bottae and C. trivirgata, are allopatric in western North Adult erycines are typically < 1 m in total length, America. Charina bottae (rubber boa) occurs from although the maximum size for the extant species is south-western Canada to southern California in the approximately 1.3 m and 1.14 kg (for E. johnii; Chari, United States, and eastward from western California to 1950). northern Wyoming and Colorado (Stewart, 1977). Our goals here are to evaluate variation in taxonomic Rubber boas occur in grassland, chaparral, and wood- composition of diets and erycine foraging tactics, with land (Nussbaum, Brodie & Storm, 1983). They are good an emphasis on C. bottae. We also rely on the excellent swimmers, burrowers, and climbers, and are largely fossil record of erycines and of rodents to gain a crepuscular and nocturnal, but can also be active during historical perspective on how prey characteristics may the daytime (Ross, 1931; Stebbins, 1954; Peterson & have in¯uenced evolutionary innovations in the trophic Dorcas, 1992). Charina trivirgata (rosy boa) ranges from apparatus of macrostomatans. Feeding ecology of erycine boas 51 Table 1. Prey eaten by Charina bottae.`Perognathus (sensu lato) sp.' refers to Chaetodipus or Perognathus (sensu stricto). `Frequency' refers to the number of times each prey taxon was found in the entire sample; numbers in parentheses indicate the number of snakes that ate that particular prey Percentage of total Prey taxon Frequency no. of prey Source Gastropoda Stylommatophora Arionidae Ariolimax columbianus 1 (1) 1.1 G. Anderson, pers. comm. Aves Passeriformes Paridae Parus rufescens 6 (1) 6.7 Copper, Ohmart & Dahlsten, 1978 Mammalia Insectivora Talpidae Scapanus latimanus 3 (1) 3.4 This study cf. Scapanus latimanus 3 (1) 3.4 This study Unidenti®ed talpid 2 (1) 2.2 This study Soricidae Sorex sp. 2 (2) 2.2 This study; Koch & Peterson, 1995 Rodentia Dipodidae Zapus princeps 1 (1) 1.1 Stebbins, 1954 Geomyidae Thomomys talpoides 5 (1) 5.6 Bartholomew & Lleyson, 1993 Heteromyidae Perognathus (sensu lato) sp. 1 (1) 1.1 This study Muridae Microtus californicus 1 (1) 1.1 This study Microtus longicaudus 1 (1) 1.1 Brunson & Demaree, 1951 cf. Microtus montanus 1 (1) 1.1 Fitch, 1936 Peromyscus maniculatus 6 (1) 6.7 This study Peromyscus cf. P. maniculatus 4 (1) 4.5 This study Peromyscus sp. 1 (1) 1.1 This study Unidenti®ed rodent 13 (5) 14.6 This study; Van Denburgh, 1922; Agerter, 1932; Logier, 1932; Tanner & Tanner, 1939 Unidenti®ed mammal 15 (5) 16.9 This study; Cope, 1900 Reptilia Squamata Anguidae Elgaria coerulea 1 (1) 1.1 P. Gregory, pers. comm. Elgaria sp. 6 (6) 6.7 This study; Stebbins, 1954 Phrynosomatidae Sceloporus occidentalis 4 (2) 4.5 This study; Van Denburgh, 1922 Sceloporus sp. 3 (3) 3.4 This study; Cope, 1900 Unidenti®ed lizard 1 (1) 1.1 This study Squamate eggs 1 1 (1) 1.1 This study 2 1 (1) 1.1 This study 4 1 (1) 1.1 This study 6 cf. Sceloporus graciosus eggs 1 (1) 1.1 R. Staub, pers. comm. Unidenti®ed animal 4 (4) 4.5 This study Total 89 METHODS avoiding only type specimens and fragile individuals. Whenever possible, for each snake with prey we We examined 249 and 84 specimens of Charina bottae recorded
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