Correlated evolution of thermal characteristics and foraging strategy in lacertid lizards
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).
Section snippets
Data sources
Foraging data on the following species were taken from the literature (see Table 1 for sources): Acanthodactylus boskianus, A. schreiberi, A. scutellatus, Heliobolus lugubris, Ichnotropis squamulosa, Lacerta agilis, Meroles suborbitalis, Nucras intertexta, N. tesselata, Ophisops elegans, Pedioplanis lineoocellata, and P. namaquensis. For an additional set of species (Acanthodactylus erythrurus, Lacerta monticola, L. oxycephala, L. schreiberi, L. vivipara, Podarcis hispanica, P. melisellensis,
Results
The outcome of our analyses of the relationships among foraging indices and between foraging indices and thermal characteristics was largely independent of the method used. The correlation coefficients and regression parameters obtained were consistent in size and direction, although different methods yielded slightly disparate significance levels (Table 2, Table 3).
Although all three indices of foraging behaviour (PTM, MPM and PAM) correlated positively, the association between PTM and PAM was
Discussion
Our results strongly indicate that lacertid lizards that maintain high body temperatures in the field tend to have a more AF style than lizards active at lower body temperatures, which seems to contest Regal's (1983) idea of a conflict between thermoregulatory and feeding behaviours. Bauwens et al. (1995) demonstrated that the morphology (body size, relative hind limb length), thermal physiology (optimal body temperatures, thermal performance breadth) and thermoregulatory behaviour (preferred
References (66)
- et al.
Contrasts in energy intake and expenditure in sit-and-wait and widely foraging lizards
Oecologia
(1981) - et al.
The evolution of thermal physiology in ectotherms
J. Therm. Biol.
(2002) - Avery, R.A., 1976. Thermoregulation, metabolism and social behaviour in Lacertidae. In: Bellairs, A.d’A., Cox, C.B....
- et al.
The role of thermoregulation in lizard biology: predatory efficiency in a temperate diurnal basker
Behav. Ecol. Sociobiol.
(1982) - et al.
Evolution of sprint speed in lacertid lizards: morphological, physiological, and behavioral covariation
Evolution
(1995) The thermal dependence of lizard behaviour
Anim. Behav.
(1980)- et al.
Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil
Amphibia–Reptilia
(1993) Summer activity patterns and thermoregulation in the wall lizard, Podarcis muralis
Herpetol. J.
(1991)- et al.
Thermal ecology and spatio-temporal distribution of the Mediterranean lizard Psammodromus algirus
Holarctic Ecol.
(1989) - et al.
Thermal and temporal patterns of two Mediterranean Lacertidae
Sci. Herpetol.
(1995)
Field body temperatures, mechanisms of thermoregulation and evolution of thermal characteristics in lacertid lizards
Nat. Croat.
The effect of the thermal environment on the ability of hatchling Galapagos land iguanas to avoid predation during dispersal
Oecologia
Prey chemical discrimination, foraging mode, and phylogeny
Chemical discrimination by tongue-flicking in lizards: a review with hypotheses on its origin and its ecological and phylogenetic relationships
J. Chem. Ecol.
The foraging mode controversy: both continuous variation and clustering of foraging movements occur
J. Zool. (Lond.)
Absence of prey chemical discrimination by tongue-flicking in an ambush-foraging lizard having actively foraging ancestors
Ethology
Foraging modes in lacertid lizards from southern Africa
Amphibia–Reptilia
Oxygen consumption in the lizard genus Lacerta in relation to dial variation, maximum activity and body weight
J. Exp. Biol.
Effects of body temperature on the predatory behaviour of the lizard Psammodromus algirus hunting winged and wingless prey
Herpetol. J.
Mean body temperature and heat absorption in four species of Acanthodactylus lizards (Lacertidae)
Herpetologica
Phylogenies and the comparative method
Am. Nat.
Toward the phylogeny of the family Lacertidae—why 4708 base pairs of mtDNA sequences cannot draw the picture
Biol. J. Linn. Soc.
Phylogenetic analyses of lizard endurance capacity in relation to body size and body temperature
Laboratory endurance capacity predicts variation in field locomotor behaviour among lizard species
Anim. Behav.
Procedures for the analysis of comparative data using phylogenetically independent contrasts
Syst. Biol.
Thermal dependence of striking and prey capture by gopher snakes
Copeia
Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question
Am. Nat.
Temperature, physiology, and the ecology of reptiles
Evolution of thermal sensitivity of ectotherm performance
Trends Ecol. Evol.
Seasonal variation in thermoregulatory behavior and body temperature of diurnal Kalahari lizards
Ecology
Ecological consequences of foraging mode
Ecology
Preface: on widely foraging for Kalahari lizards. Feeding ecology in the natural world.
Cost and benefits of lizard thermoregulation
Quart. Rev. Biol.
Cited by (20)
Thermal biology of two sympatric Lacertid lizards (Lacerta diplochondrodes and Parvilacerta parva) from Western Anatolia
2021, Journal of Thermal BiologyCitation Excerpt :Sympatric squamate species that live in the same environments might differ in their use of thermal micro-habitats (Angilletta, 2009; Gómez Alés et al., 2017). Microhabitat selection (Castilla and Bauwens, 1991; Ortega et al., 2016b), reproduction (Ibargüengoytía et al., 2008; Luo et al., 2010; Meiri et al., 2012), foraging rates (Kearney et al., 2020; Verwaijen and Van Damme, 2007) and growth patterns (Angilletta et al., 2002; Van der Have and De Jong, 1996; Refsnider et al., 2019) are partly determined by thermal factors in ectotherms' environments. The spatial heterogeneity of the thermal environment has an important role in thermoregulation, providing more opportunities for activities for lizards (Logan et al., 2019; Ortega and Martín-Vallejo, 2019; Sears et al., 2011).
An integrative analysis of the short-term effects of tail autotomy on thermoregulation and dehydration rates in wall lizards
2021, Journal of Thermal BiologyCitation Excerpt :Shuttling heliotherms, such as many lizards, do so by adjusting the frequency and duration of basking events and selecting thermally optimal microhabitats (Huey 1982; Angilletta 2009). However, thermoregulatory behaviour may be costly in terms of predation exposure and time budgets (Verwaijen and Van Damme 2007; Herczeg et al., 2006). Thermoregulation is constrained by climate and the physical environment (Carrascal et al., 1992; Aguado and Braña 2014; Sannolo et al., 2019), but also depends on organismal traits such as reproductive condition (Braña 1993; Rodríguez-Díaz et al., 2010), feeding state (Brown and Griffin 2003; Gilbert and Miles 2016), colour (Clusella-Trullas et al., 2009), metabolic and cardiovascular rates (Seebacher and Franklin 2005; Brown and Au 2009), body size (Stevenson 1985; Carrascal et al., 1992), or hydration state (Sannolo and Carretero 2019; Rozen-Rechels et al., 2020).
Observation resolution critically influences movement-based foraging indices
2019, Scientific ReportsEvolution of animal chemical communication: Insights from non-model species and phylogenetic comparative methods
2019, Belgian Journal of Zoology