Reassessing the Effects of Prey Size and Status on Prey Restraint Behaviour of Macrostomate Snakes Rita S

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Reassessing the Effects of Prey Size and Status on Prey Restraint Behaviour of Macrostomate Snakes Rita S Ethology Contextual Flexibility: Reassessing the Effects of Prey Size and Status on Prey Restraint Behaviour of Macrostomate Snakes Rita S. Mehta* & Gordon M. Burghardt * Department of Psychology, University of Tennessee, Knoxville, TN, USA Department of Psychology and Department of Evolution and Ecology, University of Tennessee, Knoxville, TN, USA Correspondence Abstract Rita S. Mehta, Section of Evolution and Ecology, University of California, Storer Hall, Contextual flexibility in prey restraint behaviour has been documented One Shields Ave, Davis, CA 95616, USA. in advanced snakes (Colubroidea), but the degree of flexibility for earlier E-mail: [email protected] snake lineages has been largely unstudied. We document the prey restraint behaviour of five snake species belonging to three early mac- Received: May 29, 2007 rostomate lineages: Loxocemidae, Erycinae and Boidae. Species from Initial acceptance: August 4, 2007 these lineages were chosen for this study because they utilize similar Final acceptance: September 7, 2007 (S. A. Foster) prey resources but exhibit different ecological habits that may have important consequences on prey restraint behaviour. Snakes (n = 27) doi: 10.1111/j.1439-0310.2007.01437.x were studied in a systematic experimental design assessing the effects of mouse size (small and large) and status (live and dead) across a total of 216 feeding trials. Loxocemus and Erycine snakes were highly flexible in their prey restraint behaviour patterns and these varied across prey cate- gory. Individuals of Boa constrictor exhibited very little contextual flexi- bility in feeding behaviour, confirming earlier reports. Flexibility in prey restraint behaviour corresponded with loop application pattern, whether the snake bent laterally or ventrally when forming a loop around prey. Our study is the first to show that early macrostomate snakes exhibit flexible prey restraint behaviours. Thus, our results suggest that flexibil- ity in predatory behaviour may be more widespread across snake taxa than previously thought and we offer hypotheses for the observed inter- specific differences in snake feeding behaviour. tions such as under what conditions behavioural Introduction flexibility evolves (Gordon 1991). Animals interact with their environment in diverse Many predatory organisms have the ability to shift ways. Behavioural flexibility, the ability to vary the among different behaviours or modes while feeding deployment of behavioural patterns in response to (Helfman 1990). Flexibility in various aspects of the different situations, is an important aspect of the predatory cycle has been shown to be dependent phenotype of many organisms (Caro & Bateson upon proximate characteristics of the prey as well as 1986; Helfman 1990; Gordon 1991; Kieffer & Colgan ecological conditions that may affect the density of 1993; Mercier & Lenoir 1999). The aggregate set of the prey or where prey can be found (Jaeger & Bar- available behaviours, commonly known as a nard 1981; Formanowicz et al. 1982; Brown 1986). behavioural repertoire, represents the variety of Within the predatory cycle, prey handling is one ways in which an organism can respond to a partic- common axis of behavioural diversification that may ular situation. Understanding when and why specific reveal interspecific divergence between predators behaviours are employed as well as their flexibility utilizing similar resources. Prey vary in size, shape, has the potential to shed light on more general ques- elusiveness, antipredator adaptations and location. Ethology 114 (2008) 133–145 ª 2008 The Authors Journal compilation ª 2008 Blackwell Verlag, Berlin 133 Contextual Flexibility R. S. Mehta & G. M. Burghardt Any number of combinations of these prey charac- extent of flexibility in prey restraint behaviour, how- teristics can influence the types of prey acquisition ever, has not been determined for most snake lin- behaviours employed and, in turn, shape the eages, and it is premature to evaluate whether the behavioural flexibility of predators (Helfman & Clark present observations are due to shared descent or 1986; Helfman & Winkelman 1991; Burghardt & other factors such as physiology or ecology. Our goal Krause 1999; Souza et al. 2007). Determining how here was to empirically evaluate the contextual natural variation in prey characteristics affects prey flexibility of prey restraint behaviour for representa- acquisition by predators is an important step to tives of three early macrostomate lineages: Loxocemus understanding the development of predatory reper- bicolor, New and Old World Erycines (Charina toires and ultimately the evolution of novel feeding trivirgata, Charina bottae and Eryx muelleri) and Boa strategies. constrictor. These five taxa were chosen for this study Snakes comprise a monophyletic clade of obligate because they exhibit different ecological habits and predators that exhibit tremendous ecological and molecular and morphological phylogenies indicate evolutionary diversity. The vast majority of the 3000 that two of these lineages, L. bicolor and ‘Erycines’ or so species of snakes are able to consume large and (sensu latu), may be potentially interesting for future potentially dangerous prey (Cundall & Greene comparative studies attempting to polarize behavio- 2000). The widespread presence of constriction, a ural characters in snakes (Tchernov et al. 2000; specialized prey restraint behaviour in snake lineages Scanlon 2006). Recent molecular studies suggest that that are known to consume relatively bulky prey, L. bicolor is the sister taxon to pythons (Vidal & suggests that large prey species, capable of retaliating David 2004; Vidal & Hedges 2004; Vidal et al. 2007) against the predator, necessitate specialized restraint while Old World and New World Erycines are boid tactics. snakes but are not each others closest relatives (Vidal During constriction a snake restrains prey by et al. 2007). Loxocemus bicolor and Erycines exhibit applying two or more body loops around the prey both semi-fossorial and terrestrial habits, while while exerting pressure (Greene & Burghardt 1978; B. constrictor is semi-arboreal and terrestrial. Despite Greene 1983a, 1994). Constriction serves as an ideal these ecological differences, dietary data reveals con- topic for comparative evolutionary studies as it con- siderable dietary overlap across these five species. sists of a readily defined sequential modal action pat- Both L. bicolor and Erycines consume lizards, squa- tern (Burghardt 1973; Barlow 1977), varies across mate eggs and small mammals (Mora & Robinson species, and occurs in lineages that are ecologically 1984; Mora 1987, 1991; Rodriguez-Robles et al. and morphologically diverse (Greene 1977; Greene 1999; Rodriguez-Robles 2003), while larger Erycine & Burghardt 1978; Moon & Mehta 2007). Much of snakes also tend to add larger mammals and birds in the work on prey restraint repertoires in snakes has their diet (Rodriguez-Robles et al. 1999). Boa constric- focused on members of a large and diverse radiation, tor consumes mostly lizards, birds and mammals the Colubroidea, containing over 80% of all snake (Greene 1983a,b; Smith 1994; Sironi et al. 2000; species. Many members of the Colubroidea, have a Greene et al. 2003; Boback 2004). Therefore, any relatively large prey restraint repertoire and are interspecific differences in the prey restraint reper- known to vary their restraint behaviours in response toire of these boid predators, may suggest that other to prey size, type and activity level (Greene & Burg- factors may shape the evolution of feeding behav- hardt 1978; Greenwald 1978; De Queiroz 1984; iour in early macrostomate snakes. Milostan 1989; Gregory et al. 1980; Mori 1991, Although Greene & Burghardt (1978) examined 1994, 1995; Rodriguez-Robles & Leal 1993; Mehta the constriction postures of boas and pythons on 2003). Based on observations of a small number of various substrates and with various prey items, a species, it has been suggested that other snake lin- systematic stimulus control design was not used. eages, such as boas and pythons, are less capable of A stimulus control study not only allows for close varying their prey restraint behaviour in response to examination of any variability in behaviour, but this proximate characteristics of the prey (Greene 1977; standard experimental design is ideal for comparative Milostan 1989). studies. This study is the first to systematically The observation that prey restraint behaviour address the contextual flexibility, or lack thereof, in exhibits some degree of flexibility and that this flexi- prey restraint behaviour for non-colubroid snakes. bility varies interspecifically in colubrid snakes, sug- To examine the effects of prey characteristics on the gests that factors such as phylogenetic history may predatory cycle, we varied two aspects of mamma- shape the prey restraint repertoire of snakes. The lian prey (Mus musculus) previously shown to affect Ethology 114 (2008) 133–145 ª 2008 The Authors 134 Journal compilation ª 2008 Blackwell Verlag, Berlin R. S. Mehta & G. M. Burghardt Contextual Flexibility prey restraint behaviour in snakes: size (Mehta used a 2 · 2 factorial design (small prey vs. large 2003) and status (De Queiroz 1984). prey · live vs. dead) in which prey were adminis- tered using an 8 · 8 Latin square cyclic matrix. Snakes were tested twice in each of the four prey Materials and Methods categories. Twelve adult sunbeam snakes, L. bicolor, six subadult Experiments were initiated by placing live prey or
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