Correlated evolution of thermal characteristics and foraging strategy in lacertid lizards

Abstract

• We investigated the association between field body temperatures (T_b), field air temperatures (T_a), and their differences (Δ) with measurements of foraging activity (percentage of time moving (PTM), number of movements per minute (MPM) and proportion of prey attacked while moving (PAM)) for 25 species of lacertid lizards.

• Lizards active at relatively high field body temperatures tended to have higher PTM and PAM values. We found no association between temperatures and MPM. The difference Δ did not co-vary with PTM and MPM, but showed a positive trend with PAM.

• Our results seem robust with regard to the assumptions of different models of evolution and to the phylogenetic trees used.

Introduction

In many animals, acquiring food is a risky, time-consuming and energetically demanding activity. At the same time, it is a prerequisite for survival and reproduction. In consequence, foraging efficiency can be expected to be under strong selective pressure. Since food gathering is typically a whole-animal function, it seems likely that this selection pressure will affect the whole of an animal's morphology, physiology, behaviour and life history (McLaughlin, 1989).

Lizards have proved to be excellent model organisms in studies on the correlates of foraging styles (Reilly et al., 2006). Pianka (1966) recognised two modes of foraging in lizards: sit-and-wait foraging (SW) and active foraging (AF). SW foragers remain sedentary for most of their activity period, waiting in ambush for suitable prey. Movements are limited to short, fast launches towards prey and the occasional change of lookout site. In contrast, AF foragers move frequently and explore the environment, actively searching for prey. The apparent dichotomy in foraging modes seems to be associated with a parallel disparity in various morphological, physiological, ecological and behavioural characteristics (see Huey and Pianka, 1981; Anderson and Karasov, 1981; Magnusson et al., 1985; Perry et al., 1990; Huey et al., 1984; Cooper, 1994a, Cooper, 1994b).

Although still under debate (e.g. Cooper, 2005; Huey and Pianka, 2007), publication of foraging behavioural data from a wider range of lizard taxa, and the application of phylogenetically informed statistics, has led many students to abandon the dichotomous view of foraging styles for a more continuous picture, with examples of “real” SW and AF foragers at the extremes, but also with intermediate styles (Perry, 1999; Cooper, 2005). This urges a re-evaluation of the associations between foraging style and other aspects of the animals’ biology. In this paper, we concentrate on the possible interactions between foraging style and thermal ecology.

Body temperature affects the rate of all biochemical and physiological processes and thus has a profound effect on a lizard's whole-animal performance and, ultimately, its fitness (Huey and Stevenson, 1979; Huey, 1982). In environments with sub-optimal or fluctuating thermal conditions, selection will therefore favour a certain degree of thermoregulation. For instance, lizards that maintain body temperatures near the physiological optimum will maximize the efficiency of muscular contraction and neuromuscular coordination (Putnam and Bennett, 1982; Marsh and Bennett, 1985), resulting in higher sprint speeds (e.g. Bennett, 1980) and an improved capacity to capture prey or to escape predation (Christian and Tracy, 1981; Avery et al., 1982; Van Damme et al., 1991; Díaz, 1994). Most often, lizards regulate their body temperatures behaviourally. However, like foraging, behavioural thermoregulation can also be costly in terms of time, energy and increased risk, and the balance between costs and benefits is reflected in thermoregulatory precision (Huey and Slatkin, 1976). The central role of temperature regulation in lizard biology has prompted a large body of research (reviews in Huey, 1982; Angiletta et al., 2002).

Although nobody will doubt that foraging and thermoregulation play central roles in lizard biology, surprisingly few studies have explored possible interactions between both functions quantitatively. There are two ways in which such interactions may arise: (1) body temperature can affect foraging style directly and (2) thermoregulatory behaviour, needed to maintain a certain body temperature, may interfere with foraging activity. However, it is not a priori clear in which direction these interactions will work. In the scant literature on the issue, assertions in both directions can be found.

Some authors claim that AF foragers require high body temperatures to maintain their high level of movement (e.g. Magnusson et al., 1985; Bergallo and Rocha, 1993). This seems plausible, given the thermal dependence of locomotor capacity (e.g. Bennett, 1980; Van Berkum, 1986; Van Damme et al., 1989) and tongue flick rates (e.g. Van Damme et al., 1991). The maximal performance of organisms with high optimal temperatures may be greater than that of organisms with low optimal temperatures (the “hotter is better” hypothesis, see Huey and Kingsolver, 1989). Among lizard species, high endurance capacity, characteristic for AF (Garland, 1999), correlated with high body temperatures (Garland, 1994). SW predators may not need elevated body temperatures for prolonged foraging bouts or chemoreception, but they do require the ability to strike explosively and precisely, often at more agile prey. Acceleration is an understudied function in lizards, but is likely to be highly temperature dependent (see e.g. Greenwald, 1974). In the other direction, maintaining high body temperatures will increase metabolic expenditure and hence food intake requirements. Body temperature therefore plays a role in foraging economics and, depending on other factors (such as food availability), may promote a more active or passive foraging style (Karasov and Anderson, 1984).

Several authors have hinted at possible interactions between thermoregulatory behaviour and foraging behaviour. With a limited time budget, time spent in one type of activity (e.g. thermoregulating) may be at the expense of the other activity (foraging), unless both activities can be combined. In this respect, one might expect SW predators to be better off, because they can more easily combine thermoregulatory behaviour with prey seeking, e.g. basking at their foraging post. Following similar reasoning, Regal (1983) suggested that because thermoregulation requires complex behaviours (e.g. postural adjustments, selection of thermally favourable sites), precise thermoregulation is incompatible with frequent movements and hence AF. In contrast, Magnusson et al. (1985) argued that an AF style would allow predators to exploit the thermal patchiness of their environment better and hence increase their thermoregulatory precision. Secor and Nagy (1994) noted that the prolonged immobility needed for ambushing prey precludes shuttling thermoregulation, forcing SW predators to accept sub-optimal and variable body temperatures.

In this paper, we explore relationships between foraging style and thermal ecology within lacertid lizards. With a distribution covering large parts of Eurasia and all of Africa, members of the Lacertidae can be found in a wide variety of climates, habitats and microhabitats. Although most species are typical heliothermic diurnal lizards, attained field body temperatures vary considerably among species (Castilla et al., 1999). Most species primarily feed on arthropods, but some also eat substantial amounts of plant material (Van Damme, 1999). Foraging strategies vary from SW to active hunting (Pianka et al., 1979; Huey and Pianka, 1981; Perry et al., 1990; Cooper and Whiting, 1999; Verwaijen and Van Damme, submitted for publication).