William E. Cooper

Foraging mode, prey chemical discrimination, and phylogeny in lizards

The long-held hypothesis that active foragers should use chemical senses to detect food more than do ambush foragers is verified for lizards. In actively foraging and herbivorous families, tongue-flicking permits sampling of chemicals for detection and identification of prey, but in ambush-foraging families the tongue does not participate even in detection of prey. Because foraging mode and prey chemical discrimination are stable within most families and in some higher taxa, their states are often historically determined. Possible influences of foraging ecology and phylogeny on prey chemical discrimination were analysed by studying correlated changes in the two variables. For several alternative phylogenetic reconstructions, shifts in foraging mode are coincident with shifts in prey chemical discrimination. These results suggest adaptive adjustment of prey chemical discrimination to foraging mode. Other possible interpretations are discussed. Evolution of lingual morphology and behaviour and of the vomeronasal system for enhanced efficiency of active foraging suggest that foraging behaviour may have driven much of the diversification of squamate reptiles.

TRADEOFFS BETWEEN ESCAPE BEHAVIOR AND FORAGING OPPORTUNITY BY THE BALEARIC LIZARD (PODARCIS LILFORDI)

Optimal escape theory predicts that prey permit closer approach by predators when fleeing is more costly, but does not predict other aspects of escape such as distance fled or the likelihood of returning to the initial site in the presence or absence of a resource such as food. Because a lizard preparing to feed may lose the feeding opportunity, optimal escape theory predicts that the lizard should allow a predator to approach closer before fleeing when a stationary food source is present than in its absence. In addition, we predicted that when a predator was nearby, lizards would flee a shorter distance and return more often when food was present than absent. We presented adult males of the omnivorous Balearic lizard, Podarcis lilfordi, with a tethered piece of pear or a pebble of similar size and shape. One of us approached a lizard in a standardized manner, stopping and remaining still when the lizard fled. The other investigator recorded escape and return behaviors. Lizards in the presence of food permitted closer approach before fleeing, fled a substantially shorter distance, and were far more likely to return to the site of stimulus presentation than when a pebble was presented. These findings suggest that prey may alter several aspects of escape behavior to reduce costs due to lost opportunities, and present a likelihood that interspecific variation exists in the combination of aspects of antipredatory behavior that are modified.

Multiple functions of extraoral lingual behaviour in iguanian lizards: prey capture, grooming and swallowing, but not prey detection

Abstract Abstract. Lingual chemosensory sampling allows many lizards to detect and later relocate prey after failed capture attempts. Although several families in the iguanian radiation do not discriminate prey chemicals prior to attack on prey, little is known about their responses to oral contact with prey chemicals during successful or failed predation attempts. Experimental tests of responses to swabs bearing surface chemicals from prey revealed no evidence of prey chemical discrimination in two species from different iguanian families. Neither of these nor a third species exhibited strike-induced chemosensory searching in experiments that readily elicit this behaviour in many other lizard taxa. None of the three species performed searching movements after ingesting prey. The form of lingual protrusion observed differed from that used by other lizards to detect prey. Instead of being directed to environmental substrates, the tongue was used to capture prey or lick the labial scales, or was protruded in a manner suggesting postural adjustments or cleaning subsequent to swallowing. Comparison of present and previous results suggests that use of lingually mediated prey chemical discrimination prior to attack and strike-induced chemosensory searching after attack may be coupled in carnivorous lizards, both being present or both absent. Available data suggest that lingual sampling to detect prey in pre- and post-attack settings occurs in actively foraging lizards, but not in ambush foragers, and that it typically occurs in both settings in scleroglossans, but not iguanians. Although iguanians do not use the tongue to detect prey chemicals before attack, lingual prehension of prey or labial-licking may have provided the contact with chemicals on environmental substrates that led to selection for tongue-flicking to detect prey chemicals or pheromones.

Pursuit deterrence varies with predation risks affecting escape behaviour in the lizard Callisaurus draconoides.

A growing body of evidence suggests that many prey attempt to prevent attack by signalling that they have detected a predator and are able to escape. Much of the evidence for pursuit deterrence is indirect in that signalling is not shown to reduce probability of attack. Indirect evidence is obtained by eliminating alternative hypotheses and demonstrating that signals are directed to predators. Other studies have shown that signalling is related to single predation risk factors. Because prey need not signal at low risk and should attempt to escape immediately when at high risk, pursuit–deterrent signals should occur most frequently at intermediate risk. Tests of escape theory have demonstrated that flight initiation distance (predator–prey distance when prey flees) increases as risk associated with various risk factors increases. I show that in the lizard Callisaurus draconoides , which signals by waving its tail, probability and timing of signalling are affected by degree of risk for several factors that strongly affect flight initiation distance, specifically distance to refuge, speed and directness of approach, and predator persistence. Flight initiation distance increased with risk for all factors, but for all but one factor, relationships to risk differed between signalling and escape, and differences were readily predicted from functional differences between these behaviours.

RELATIONSHIPS AMONG FORAGING VARIABLES, PHYLOGENY, AND FORAGING MODES, WITH NEW DATA FOR NINE NORTH AMERICAN LIZARD SPECIES

Complete characterization of lizard foraging behaviors may require information about aspects rarely measured. Most studies record only number of movements per minute (MPM) and/or percent of time moving (PTM), but lizards differ markedly in average speed (AS) and speed while moving (MS) during foraging and in proportion of attacks initiated after detecting prey while the lizard is moving (PAM). We present data on these variables for nine lizard species and on foraging speed for several others, permitting first assessments of relationships between speed, PAM, and both phylogeny and foraging mode; examination of the effect of body length on foraging speed; and correlative analyses of relationships between foraging variables. Although sprint speed may increase with body size, foraging speed did not, presumably for two reasons. Because search speed is much lower than sprint speed, as is speed of movement between ambush sites, searching efficiency and stamina may be more important determinants of foraging speed than is sprint speed. Second, the body size range was small, allowing the possibility that foraging speed may vary with body length over the much larger size range between the smallest and largest species worldwide. Nevertheless, a large majority of lizard species are in the size range tested, suggesting that body length may not strongly affect foraging speed except when extremely short or long species are included in comparative analyses. High PAM, high AS, and low MS were characteristic of autarchoglossans and active foragers, whereas low PAM, low AS and high MS were exhibited by iguanians and ambush foragers. In independent species analyses, significant correlations were observed between several pairs of foraging variables. In analyses using phylogenetically independent contrasts, the only significant finding was a strong positive correlation between PAM and PTM. Although these findings suggest that foraging speed, MPM, and either PTM or PAM may provide independent measures of foraging activity needed to adequately describe interspecific variation, this conclusion is tentative due to the small sample size of limited taxonomic breadth.

Age, sex and escape behaviour in the Striped Plateau Lizard (Sceloporus virgatus) and the Mountain Spiny Lizard (S. jarrovii), with a review of age and sex effects on escape by lizards

Escape behaviour often differs between sexes, reproductive states and ages. Escape theory predicts that flight initiation distance (FID = predator–prey distance when escape begins) increases as predation risk and fitness increase, and decreases as cost of escaping increases. Similar predictions hold for distance fled and refuge entry, suggesting that age and sex differences in escape behaviour may occur when risk, fitness, and opportunity costs differ. I studied such differences in two lizard species and reviewed relevant literature on escape by lizards. In Sceloporus virgatus no difference occurred between sexes or female reproductive states in FID, distance fled, distance from refuge, or probability of entering refuge. In S. jarrovii juveniles had shorter FID and distance fled than adults; juveniles were closer than females to refuge, but this did not affect FID or distance fled. Juveniles were more likely than adults to be on rocks and use them as refuges. The literature review showed that sexual dimorphism in FID occurs in about 1/5 of species (male FID usually > female FID), but distance fled differed between sexes in only 1 of 21 species. Juveniles had shorter FID than adults in all of five species; the relationship between age and distance fled was highly variable. Reasons for patterns of age/sex differences are discussed. Because age and sex differences in these factors and escape strategy can alter multiple components affecting optimality, sometimes in opposite ways, these factors and escape strategy must be known to predict effects of age, sex and reproductive state on escape.

Thermal Cost of Refuge Use Affects Refuge Entry and Hiding Time by Striped Plateau Lizards Sceloporus virgatus

Abstract Escaping prey decide whether to enter and how long to stay in refuges. According to refuge-use theory, hiding time increases as costs of emerging increase and costs of staying in refuge decrease. We studied effects of air temperature on probability of entering refuges and the effects of thermal cost on hiding time (duration in refuge). Few striped plateau lizards (Sceloporus virgatus) used refuges at intermediate air temperatures, but most readily entered cool refuges at the lowest air temperatures and relatively warm refuges at higher temperatures. Because running speed in lizards decreases as body temperature decreases, S. virgatus that are cool upon morning emergence presumably reduced their probability of being captured by entering refuges. As air and presumably body temperatures increase, refuges are initially cooler than outside, contributing to infrequent use. At higher, but not thermally stressful, temperatures, a greater probability of using refuges may reflect lower thermal costs in refuges that have warmed. Hiding time decreased as temperatures became cooler in refuges than outside. Our results confirm previous work on actively foraging lacertid lizards showing that hiding time decreases as thermal costs of refuge use increases, and extend this finding to a very distantly related phrynosomatid species that is an ambush forager. Thus, the thermal cost of refuge use affects hiding time even in lizards that do not require high body temperature for prolonged foraging movements. A growing body of knowledge supports the hypothesis that tradeoffs between costs of emerging and remaining in refuges guide decisions about hiding time.

Effects of estrogen and male head coloration on chemosensory investigation of female cloacal pheromones by male broad-headed skinks (Eumeces laticeps).

Indirect experimental evidence suggests that pheromone production and responsiveness to pheromones in a lizard, the broad-headed skink (Eumeces laticeps), are regulated by sex steroid hormones. For study of estrogenic effects on female pheromone levels, tongue flicking by males was recorded in response to chemical samples from the female cloaca, the secretion site of the female sex pheromone. Cloacal chemicals from estrogen-treated females elicited higher tongue flick rates by all males than samples from sham-injected females. Male head coloration is bright orange in the breeding season, but fades to tan outside the breeding season. The availability of males having the full range of head coloration due to asynchronous onset of breeding condition in a laboratory population made it possible to examine the relationship between head coloration and responsiveness to female pheromones. Males with brightly colored heads, presumably reflecting higher underlying androgen levels, performed more tongue flicks in response to cloacal chemicals from estrogen-treated females than did males with tan heads. Male head coloration did not affect responsiveness to cloacal chemicals from sham-injected females.

DURATION OF MOVEMENT AS A LIZARD FORAGING MOVEMENT VARIABLE

Studies of lizard foraging modes and their correlates have led to major advances in our understanding of the evolution of lizard taxonomic, morphological, physiological, ecological and behavioral diversity. Although two basic foraging modes, ambush and active foraging, have been recognized, variability in foraging movements among species has led to controversies about their existence and the complexity and continuity of foraging behaviors. The variables central to the controversies are number of movements per minute and percent time moving. A third variable, the average duration per bout of movement, has been neglected. For 80 species I show that average duration, like the other variables, is continuous, unimodal, and lognormally distributed. Average duration is highly correlated with percent time moving, but only weakly with number of movements per minute. In discriminant function analysis and cluster analyses, average duration performed slightly worse at separating species by mode than percent time moving as a single variable and in combination with movements per minute. Because it is so highly correlated with percent time moving, average duration cannot be used as a third axis of a multivariable foraging space, but a variable indicating the variability of movement duration might provide new insights. Species for which modes were misclassified had percent time moving close to 10%. Average duration data support earlier reports that some gekkonids have unusually long-lasting movements for ambush foragers, yet remain immobile for long intervals between movements.

Sexual Dimorphism in Distance from Cover but Not Escape Behavior by the Keeled Earless Lizard Holbrookia propinqua

Abstract Potential sexual dimorphism of several aspects of antipredatory behavior by the Keeled Earless Lizard (Holbrookia propinqua) was studied by simulating approach by a predator. Females stayed closer to cover suitable for use as refuges than males, but no sex differences were detected in the distance between predator and prey when escape was initiated, the distance fled, or the tendency to enter refuges. Despite the sex difference in distance to cover, the regressions of flight initiation distance and distance fled on distance to cover were monomorphic. The sexes fled similar mean distances even though females were closer to refuges because some lizards stopped short of refuges and others fled past them. No differences in antipredatory behavior were noted between bright and plain female color phases.