Tongue-flick Rates Research Articles

Thermal dependence of chemical assessment of predation risk affects the ability of wall lizards, Podarcis muralis, to avoid unsafe refuges

Prey often respond to predators by increasing refuge use, but some refuges may expose prey to other types of predators. Because predators are not always visible inside refuges, their chemical stimuli may provide early warning of their presence. However, in ectotherms, chemosensory detection of predators may be thermally dependent. Lizards often hide in cold refuges, where their body temperature (Tb) may decrease, and this might affect their ability to detect chemicals of saurophagous snakes that ambush inside refuges. We examined the effects of Tb of wall lizards, Podarcis muralis, on their ability to detect chemicals of smooth snakes, Coronella austriaca. Differential tongue flick (TF) rates and behavioral patterns of lizards in response to scent of smooth snakes showed that lizards with optimal Tb discriminated and avoided the snake's scent, whereas lizards with suboptimal Tb did not. We also examined the importance of this effect on movement patterns and refuge use by lizards in terraria with safe (odorless) or unsafe refuges (snake-scented). While results of this experiment were variable, there was evidence of snake avoidance in that lizards at optimal Tb spent less time in snake-scented refuges relative to odorless refuges. Therefore, this study provides evidence that chemosensory discrimination of snake chemicals is thermally dependent, and, thus, suboptimal Tb impedes a lizard's ability to avoid snake-scented refuges.

Chemosensory Recognition and Behavioral Responses of Wall Lizards, Podarcis muralis, to Scents of Snakes that Pose Different Risks of Predation

Many animals use chemical cues to detect predators. However, according to the threat sensitivity hypothesis, natural selection should favor individuals able to respond differentially to the chemical cues of predators that pose different levels of risk rather than responding to chemical cues of all predators in a similar way. The behavioral responses of prey to chemical cues of predators might depend, for example, on the degree to which predators include prey in their diets. The Wall Lizard (Podarcis muralis) is under high predation pressure by saurophagous-specialist Smooth Snakes (Coronella austriaca). Wall Lizards are also an important part of the diet of the Montpellier Snake (Malpolon monspessulanus) and occasional prey of the Ladder Snake (Elaphe scalaris). Also, Wall Lizards are sympatric with the non-saurophagous Viperine Snake (Natrix maura). In the laboratory, we compared the tongue-flick rates and behavioral patterns of Wall Lizards in response to exposure to chemical signals of these four snake species that pose different risks of predation. Results suggested that Wall Lizards were able to discriminate the chemical cues of the predatory snakes from the non-saurophagous snake. However, lizards did not respond differentially to chemical cues of different predatory snakes. We suggest that other additional cues are probably needed to elicit an adequate, specific defensive response.

Chemosensory predator recognition induces defensive behavior in the slow-worm (Anguis fragilis)

Many antipredator adaptations are induced or mediated by the ability of the prey to recognize chemical cues from the predator. This ability is particularly advantageous for organisms whose environment precludes the effective use of other sensory systems, such as fossorial lizards. We tested the ability of the slow-worm, Anguis fragilis Linnaeus, 1758, a semifossorial legless lizard, to detect and discriminate chemical stimuli arising from potential predators. We compared rates of tongue-flicks to swabs impregnated with scents from the smooth snake (Coronella austriaca Laurenti, 1768), a sympatric predator, the grass snake (Natrix natrix (Linnaeus, 1758)), a sympatric but non-saurophagous predator, and the three-toed skink (Chalcides striatus (Cuvier, 1829)), a sympatric insectivorous, and thus innocuous, skink. Differential tongue-flick rates suggest that scents of smooth snakes were recognized by slow-worms. Moreover, scents of smooth snakes were quickly avoided and elicited defensive behaviors much more often than any other scent, suggesting that chemical cues are a reliable means of assessing the snake's presence. These chemosensory capacities would be evolutionarily advantageous to avoid predation by snakes and are likely to represent a component of the suite of adaptations associated with low-visibility habitats.

Infrared imaging in vipers: differential responses of crotaline and viperine snakes to paired thermal targets

Pit vipers use infrared-sensitive pit organs to accurately target homeothermic prey even in the absence of visual cues. It has been suggested that other vipers, including large ambush predators of the genus Bitis, also may use radiant infrared information for predatory targeting. We compared behavioral responses of pit vipers and snakes of the viperine genus Bitis to paired targets of different temperatures (i.e. cool and warm balloons), some scented with rodent odors. The rates of tongue flicking, head turning and approaches by pit vipers ( Agkistrodon contortrix and Crotalus atrox) were significantly higher toward warm targets than toward cool ones. Moreover, they all were significantly higher in pit vipers than in the vipers Bitis arietans, Bitis gabonica, and Bitis nasicornis. Bitis sp. exhibited no significant differences in their behaviors toward warm versus cool targets. Pit vipers often struck at targets (always the warm target even when paired with a prey-scented cool target), but Bitis sp. never struck at either warm or cool targets. These results show that the behavioral correlates of infrared-based predatory and/or defensive targeting differ significantly between these two groups of viperid snakes, and suggest that the neural substrates of infrared imaging in crotaline snakes are either absent or functionally distinct in viperine snakes of the genus Bitis.

Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges

The threat sensitivity hypothesis assumes that multiple cues from a predator should contribute in an additive way to determine the degree of risk-sensitive behaviour. The ability to use multiple cues in assessing the current level of predation risk should be especially important to prey exposed to multiple predators. Wall lizards, Podarcis muralis, respond to predatory attacks from birds or mammals by hiding inside rock crevices, where they may encounter another predator, the smooth snake, Coronella austriaca. We investigated in the laboratory whether chemical cues may be important to wall lizards for detection of snakes. The greater tongue-flick rate and shorter latency to first tongue-flick in response to predator scents indicated that lizards were able to detect the snakes' chemical cues. We also investigated the use of different predatory cues by lizards when detecting the presence of snakes within refuges. We simulated successive predator attacks and compared the propensity of lizards to enter the refuge and time spent within it for predator-free refuges, refuges containing either only visual or chemical cues of a snake, or a combination of these. The antipredatory response of lizards was greater when they were exposed to both visual and chemical cues than when only one cue was presented, supporting the threat sensitivity hypothesis. This ability may improve the accuracy of assessments of the current level of predation risk inside the refuge. It could be especially important in allowing lizards to cope with threats posed by two types of predators requiring conflicting prey defences.

Foraging Behavior in the Arboreal Boid Corallus grenadensis

Corallus grenadensis is an arboreal boa endemic to the Grenada Bank. Thirty-five encounters with boas resulted in 17.65 hours of observations, including 6.3 hours of video-tape (which included two acts of predation). Boas under 100 cm are largely active foragers that move slowly through bushes and trees and tongue-flick leaf and branch surfaces apparently seeking chemosensory evidence of nocturnally quiescent lizard (Anolis) prey. Significantly more search time was directed to branches below the snake rather than to either the branches supporting the snake or to those above the snake, and tongue-flick rates were significantly higher for moving snakes than for those that were stationary. Smaller snakes prey on nocturnally quiescent lizards and they spent more time moving than did large snakes that feed on nocturnally active rodents and often employ an ambush foraging strategy. Once visual and, presumably, thermal information was received from a sleeping anole, C. grenadensis adopted a lengthy stalking process devoid of tongue-flicks. Snakes approached inactive lizards from adjacent branches with great stealth, moving at a rate of about 1 cm/min. The strike was made from close range (within 3 cm), and the prey was never released once contact was made. We conclude that, if chemosensory cues successfully lead a treeboa to a visual encounter with a sleeping lizard, subsequent behavior ensures a high rate of predation success.

Differential Avoidance Responses to Chemical Cues from Familiar and Unfamiliar Conspecifics by Male Iberian Rock Lizards (Lacerta monticola)

We conducted a field study to analyze spatial relationships among male Iberian Rock Lizards, Lacerta monticola. We then used the same individuals in a laboratory experiment to test whether avoidance responses of a male lizard in a previously unknown area is affected by presence of scents of familiar and unfamiliar resident males. Time spent attempting to escape in presence of unfamiliar odors was significantly higher than in presence of familiar odors suggesting avoidance of unfamiliar scent marks, which may lower the costs of aggressive interactions. Our results are concordant with previous studies in which differential tongue-flick rates showed discrimination between odors of familiar and unfamiliar males of L. monticola.

Cologne as a pungency control in tests of chemical discrimination: effects of concentration, brand, and simultaneous and sequential presentation

Cologne has been used extensively as a pungency control in experiments on chemosensory behavior to assess responses to an odorous, readily detectable stimulus that is irrelevant to the adaptive response being studied. However, undiluted cologne may be aversive, its effects might differ among brands, it might suppress responses to simultaneously presented chemical stimuli, and might affect subsequent responsiveness to other stimuli. We present experimental data showing that undiluted cologne can be aversive, but that aversion can be eliminated by dilution. We also show that the utility of cologne as a pungency control varies among brands, that cologne does not suppress responses to food chemicals in some species, but does in others, and that prior exposure to cologne does not affect later response to food chemicals. In 60 s swab trials with the Balearic lizard (Podarcis lilfordi), the main chemosensory responses were unaffected by cologne concentration. However, one-fourth of lizards exhibited slight to moderate aversion to undiluted cologne and 3:1 water:cologne, but not to a readily detected lower concentration (9:1). Two cologne brands did not affect responses, but a third brand induced increased tongue-flick rates. Colognes that stimulate increased tongue-flicking might mask real experimental effects. Cologne presented simultaneously with cricket chemicals did not affect tongue-flicking and biting responses in two species, but caused increased tongue-flicking in a third species and weaker response to cricket chemicals in a fourth. Prior testing with cologne did not affect responsiveness to cricket chemicals in a subsequent trial. Although cologne is a useful pungency control, pilot tests are needed to verify its utility for unstudied cologne types and animal species.

Differential effects of lesions of the vomeronasal and olfactory nerves on garter snake (Thamnophis sirtalis) responses to airborne chemical stimuli.

The roles of the main (MOS) and accessory (AOS) olfactory systems of garter snakes in response to airborne chemicals were investigated. Preoperatively, all snakes responded to airborne odors with increased tongue-flick rate and duration. Postoperatively, sham-operated snakes responded to airborne odors with increased tongue-flick rates, but snakes with main olfactory nerve cuts failed to respond to the odors, and snakes with vomeronasal nerve cuts responded to nonprey odors only. Preoperatively, exposure to earthworm odor produced more frequent and shorter duration tongue-flicks during locomotion compared with exposure to water. Postoperatively, only sham-lesioned snakes exhibited differential responding to earthworm odors. This study demonstrates that the MOS is critical for the initiation of tongue-flick behavior in response to airborne odors and that discrimination of odors with biological significance requires a functional AOS.

Foraging mode and evolution of strike-induced chemosensory searching in lizards.

Strike-induced chemosensory searching (SICS) in lizards and snakes is a means of relocating prey by scent-trailing. The two main components of SICS are an elevated tongue-flick rate for vomerolfactory sampling after biting prey (PETF) and searching movements. In combination, these behaviors permit scent-trailing. Prey chemical discrimination, which is a prerequisite for SICS, is present in active foragers, but not in ambush foragers. Using comparative data. I show that searching movements and SICS have undergone correlated evolution with foraging mode and with prey chemical discrimination in lizards. This suggests that active foraging selects for prey chemical discrimination, which is then employed to search for escaped prey using the typical movements and tongue-flicking behaviors of active foragers. SICS in lizards is simply heightened active foraging after biting prey. In nonvenomous snakes, SICS is similar to that in lizards but is not restricted to active foragers. Only highly venomous snakes voluntarily release dangerous prey upon envenomation, pause to let the venom incapacitate the prey, and then relocate the prey by scent-trailing. PETF was observed in two ambush foragers and is not evolutionarily correlated with foraging mode or searching movements. Because it occurs in species lacking prey chemical discrimination, such PETF may be a response to gustatory cues or to internal chemicals not encountered on surfaces or trails of uninjured prey.

Ambient Temperature Activity of Horned Adders, Bitis caudalis: How Cold Is Too Cold?

Most physiological processes are greatly affected by temperature; therefore animals thermoregulate to maintain a body temperature (Tb) that approximates that which is optimal for physiological performance (reviews by Avery, 1982; Huey, 1982; but see Webb and Shine, 1998). As an ectotherm, a snake relies on external heat sources to maintain its preferred Tb. Although heat sources are readily available during the day, the nocturnal environment has few, if any, heat sources. Even though the nocturnal environment poses a significant thermal handicap, numerous snakes species are nocturnal (Greene, 1997). Because of the lack of heat sources, activity of nocturnal species should be sensitive to ambient temperature (Ta). The physiological and behavioral means by which snakes adapt to thermal challenges associated with nocturnality has not received extensive study. Many performance measures including locomotion, digestion rate, tongue flick, and strike velocity are maximized at relatively high Tb (e.g., Stevenson et al., 1985; Ayers and Shine, 1997; Dorcas et al., 1997; Webb and Shine, 1998). These body functions are near maximum levels during the day but are significantly reduced at night (Stevenson et al., 1985). Activity at night would not only require a snake to use physiological processes associated with foraging (e.g., locomotion, tongueflick rate, strike velocity) when they are suboptimal but could also negatively impact temperature-sensitive physiological processes, which are not associated with activity (e.g., digestion). Nocturnal activity of rubber boas, Charina bottae, led to a Tb below that which would occur if the snake remained in a nighttime refugium (an inverted Tb pattern; Dorcas and Peterson, 1998). A nocturnally active snake typically has a Tb that approximates Ta (Dorcas and Peterson, 1998); therefore, Ta may be more critical to performance of nocturnal species than of diurnal species, where radiation and conductance can lead to a Tb much greater than Ta (Peterson, 1987). Because of the thermosensitivity of processes critical to foraging, thermal factors might constrain the timing, place, and duration of predatory bouts (Ayers and Shine, 1997). Such constraints can lead to seasonal differences in activity period. For example, copperheads, Agkistrodon contortrix, are diurnal during cool seasons (spring and fall) but are nocturnal during the warm summer months (Sanders and Jacob, 1981). Thermal constraints can also lead to ontogenetic differences in activity period. Adult diamond pythons, Morelia spilota spilota, forage nocturnally, whereas juveniles are diurnal (Ayers and Shine, 1997). We used a controlled laboratory environment to test the

Behavioral responses to plant toxins by two omnivorous lizard species

An ability to detect plant toxins and thereby avoid eating chemically defended plants would be very beneficial for omnivorous and herbivorous lizards. We studied the ability of the omnivorous Podarcis lilfordi to detect compounds belonging to three classes of common plant toxins, as well as responses indicating aversion. Solutions of the alkaloid quinine, saponin, and the phenolic coumarin, as well as distilled water (odorless control), were presented to lizards on cotton swabs. The lizards detected all three toxins as indicated by significantly decreased tongue-flick rates and tongue-flick attack scores in comparison with distilled water. Several other variables revealed aversion to saponin, including a low number of individuals that bit swabs, avoidance of swabs after tongue-flicking, performance after tongue-flicking the swab of repeated short-excursion tongue-flicks that were directed away from the swab and did not contact any substrate, failure to respond at all in the next trial, and wiping the snout on the floor of the terrarium. Reasons for apparent differences in tongue-flicking behavior between P. lilfordi and two other omnivorous lizard species are discussed. We also showed experimentally that saponin depresses the tongue-flick rate in the omnivorous Bonaire whiptail lizard, Cnemidophorus murinus. Tongue-flicking enables at least one lizard species to detect specific chemicals representing three major classes of plant toxins. It is hypothesized that this ability is a widespread adaptation to reduce ingestion of plant toxins.

Absence of Discriminatory Tongue-Flicking Responses to Plant Chemicals by Helodermatid Lizards

criminate between palatable plant food and control stimuli by tongue-flicking (Cooper and Alberts, 1990; Cooper, 2000a, 2000b, 2000c; Cooper and Flowers, 2000). Because tongueflicking serves to sample chemicals from environmental substrates for delivery to the vomeronasal organs, and because prey chemical discrimination in lizards requires vomerolfaction (Cooper and Alberts, 1991), plant chemical discriminations presumably are vomerolfactory. In snakes there is a close correspondence between diet and strength of chemosensory responses to potential foods (Burghardt, 1970; Arnold, 1981; Cooper et al., 2000a), but no such correspondence has been established in lizards. Because the large majority of lizards consume little or no plant matter (Iverson, 1982), herbivory may afford an opportunity to examine a similar correspondence between diet and chemosensory responsiveness in lizards. To assess whether such correspondence occurs, WEC has undertaken comparative studies to assess responses by herbivorous and omnivorous lizards to plant chemicals and prey chemicals. Responses to plant chemicals by species that do not eat plants must be determined to learn whether plant chemical discriminations are acquired in association with plant consumption. Actively foraging insectivorous and carnivorous lizards respond to chemical cues from animal prey by tongue-flicking and biting the stimulus sources, discriminating between them and control substances (Cooper, 1995, 1997, 1999). The ability to identify prey using chemical cues may be adaptive for location and recognition of prey (Cooper, 1994). If the ability to recognize prey is specific, actively foraging carnivores should not respond strongly to chemical cues from plants palatable to herbivorous lizar s. This prediction has been substantiated for scincine (Cooper et al., 2000b) and lygosomine skinks (Cooper and Hartdegen, 1999), a lacertid and a teiid (Cooper et al., 2000c); a eublepharid gecko (Cooper and Habegger, 2000), and a varanid (Cooper and Habegger, in press). For a phylogenetically based examination of correlated evolution between herbivory and plant chemical discrimination, information is needed on responses to plant chemicals for a wide taxonomic range of herbivores and insectivores. In this study we present data showing no indication of strong response to plant chemicals by the 2 extant helodermatid lizards, the gila monster, Heloderma suspectum, and the Mexican beaded lizard, H. horridum. The gila monster discriminates prey chemicals from control substances by tongue-flicking (Cooper, 1989) and exhibits prolonged strike-induced chemosensory searching, an increase in tongue-flick rate and scent-trailing to locate lost prey (Cooper et al., 1994; Cooper and Arnett, 1995; Garrett et al., 1996). Chemosensory behavior has not been studied in Mexican

Chemosensory predator recognition induces specific defensive behaviours in a fossorial amphisbaenian

We tested the ability of amphisbaenians, Blanus cinereus, a fossorial and almost blind reptile, to detect and discriminate odours from potential predators and to show the corresponding defensive response. Amphisbaenian behaviour was observed in tubes, where we recorded the tongue-flick rate to swabs impregnated with odours of (1) a southern smooth snake, Coronella girondica, which feeds on amphisbaenians, (2) a scolopendromorph centipede (Scolopendra sp.), which are aggressive prey species that can seriously damage amphisbaenians, and (3) Bedriaga's skink, Chalcides bedriagai, a semifossorial reptile innocuous to amphisbaenians. Cologne odour and deionized water were used as pungent and nonodoriferous controls. The amphisbaenians responded to the chemical cues by increased tongue-flick rates, with the highest rates being given in response to the snake and centipede, showing that they were able to detect and discriminate the odours arising from potentially harmful species. The chemical exploration of these odours also induced defensive responses. The amphisbaenians bit or retreated from the applicators bearing snake and centipede odours, whereas skink odour did not elicit defensive responses. In addition, they showed more stress and antipredator behaviours, fled rapidly and later became less mobile during trials with the snake or centipede odours, but produced different complexes of defensive responses to each one. These results indicate that chemical cues of a predator may elicit specific defensive antipredator behaviours in amphisbaenians. We discuss the possible evolutionary advantage of identifying and avoiding potential predators in relation to fossoriality.

Food chemical cues elicit general and population‐specific effects on lingual and biting behaviors in the lacertid lizard Podarcis lilfordi

Actively foraging lizards are capable of identifying prey using only chemical cues sampled by tongue-flicking, and the relatively few omnivorous and herbivorous lizards tested similarly can identify both animal and plant foods from chemical cues. Whether lizards that eat plants respond to cues specific to preferred plant types and whether there is geographic variability in responses to cues from various plants correlated with the importance of those plants in local diets is unknown. In three populations of an omnivorous lacertid, the Balearic lizard Podarcis lilfordi, we studied chemosensory sampling and feeding responses to chemical cues from plant and animal foods presented on cotton swabs. Each lizard population is endemic to one islet off the coast of Menorca, Balearic Islands, Spain. Lizards in all three populations discriminated chemical cues from plant and animal foods from control substances. Our results extend findings of prey chemical discrimination and plant chemical discrimination in omnivores, increasing confidence that correlated evolution has occurred between plant diet and chemosensory response to palatable plants. There were no consistent differences among populations in tongue-flicking and biting responses to stimuli from flowers of syntopic and allopatric plant species. The lizards may respond to cues indicative of palatability in a wide range of plant species rather than exhibiting strong responses only to locally available plant species. Nevertheless, tongue-flicking and biting frequencies varied among plant species, perhaps indicating food preferences. In addition, there were differences among populations in tongue-flick rates, latency to bite, and licking behavior. Licking was observed in only one lizard population as a response to floral chemicals from only one of the plants species tested, raising the possibility of a population-specific linkage between identification of a particular plant species and performance of an appropriate feeding response.

Chemosensory discrimination of familiar and unfamiliar conspecifics by lizards: implications of field spatial relationships between males

The ability of territorial lizards to discriminate between scents of neighbors and non-neighbors might contribute to decreasing the costs of aggressive interactions. To test this hypothesis, we conducted a field study to analyze the spatial relationships between male Iberian rock-lizards, Lacerta monticola. We then used the same individuals in a laboratory experiment to test whether male lizards can use chemical cues to discriminate between familiar conspecific males (those whose home ranges overlapped) and unfamiliar conspecific males (those whose home ranges did not overlap, and whose home range centers were at least 50 m apart). Differences in tongue-flick rates in the presence of chemical cues suggested that male L. monticola discriminated between odors of familiar and unfamiliar males. The behavioral responses were also dependent on relative differences in body size between the responding male and the unfamiliar male that donated the scent: There was a significant negative correlation between tongue-flick rates emitted in cages of unfamiliar males and the body size differences between males. In contrast, when the donor of the scent was a familiar male, the tongue-flick rate was not dependent on body size differences. These results are compatible with individual discrimination through chemical cues in male L. monticola.

Omnivorous lacertid lizards (Gallotia) from El Hierro, Canary Islands, can identify prey and plant food using only chemical cues

We studied lingual and biting responses to food chemicals by two species of omnivorous lacertid lizards, the Canary Island endemics Gallotia simonyi (the giant lizard of El Hierro) and Gallotia caesaris (Boettger's lizard), to ascertain their ability to discriminate between prey and plant food chemicals on the one hand and control stimuli on the other. We recorded frequencies of tongue-flicking and latency to bite in 60-s trials in which chemical stimuli on cotton-tipped applicators were presented to the lizards. Both species exhibited prey-chemical discrimination, as indicated by elevated tongue-flick rates and higher proportions of individuals biting in response to surface chemicals from crickets. Both species exhibited plant-chemical discrimination, as indicated by significantly greater tongue-flick rates and biting frequency in response to chemicals from tomato fruit than to the control stimuli. Juvenile G. simonyi responded much more strongly to chemical stimuli from tomato fruit than from leaves of Psoralea bituminosa, which is not a preferred food for juveniles. The findings are consistent with the hypothesis that chemosensory discrimination evolves in omnivorous lizards to permit evaluation of food quality, resulting in correspondence between plant diet and plant-chemical discrimination, both being absent in insectivores. The results are also consistent with the hypothesis that prey-chemical discrimination is retained and plant-chemical discrimination evolves in the omnivorous lizards derived from actively foraging insectivores.

Use of Predator Chemical Cues by Three Species of Lacertid Lizards (Lacerta bedriagae, Podarcis tiliguerta, and Podarcis sicula)

Three species of lacertid lizards (Lacerta bedriagae, Podarcis tiliguerta, and Podarcis sicula) are able to detect the former presence of the saurophagous snake Coluber viridiflavus by tongue flicking. Lizards tongue flicked more in cages previously inhabited by the predatory snake than in clean cages or in cages treated with eau-de-cologne. They also exhibited behavioral acts typically associated with stressful situations (foot shakes, tail vibrations, starts) more frequently when predator chemicals are present Individ- uals from the two Podarcis species that came from populations syntopic with C. viridiflavus were also able to distinguish between chemical cues from this saurophagous predator and a nonsaurophagous snake (Natrix maura). In these lizards, the former presence of N. maura did not elicit higher tongue-flick rates or stress- indicating behaviors. In contrast, individuals of Lacerta bedriagae collected from a snake-free area increased tongue-flick rate and frequency of stress-related behavior in response to chemicals of both snakes, suggesting that prior contact is not required for chemosensory recognition of snakes in this species but may facilitate the distinction between different species of snakes. The presence of predator (C. viridiflavus) chemical cues induces a shift in the microhabitat use of the lizard species studied. In a large terrarium containing various substrates, lizards chose different types of microhabitats when chemical cues of C. viridiflavus were present than when absent and avoided the side of the terrarium labeled with the chemicals.

Geographic variation in antisnake tactics: the evolution of scent-mediated behavior in a lizard.

We used modern comparative methods to examine the evolution of scent-mediated antisnake behavior in the rock-dwelling velvet gecko (Oedura lesueurii). The selective agent is a snake species (broad-headed snake, Hoplocephalius bungaroides) that feeds primarily on velvet geckos by remaining sedentary in rock crevices for days or weeks, waiting to ambush lizards. The past and present distribution of this predator is well documented because of its threatened conservation status. We used this information to sample lizards from three populations distributed with snakes (sympatric) and three populations that appear never to have been distributed with snakes (allopatric) in each of two widespread but geographically distinct genetic groups of velvet gecko (as determined using allozyme electrophoresis). Wild-caught immature geckos from sympatric populations showed higher tongue-flick rates and stronger shifts in locomotion (increased duration of crawling and remaining stationary while pressed against the rock) toward snake-scented rocks than did lizards from allopatric populations. However, predation environment did not significantly affect a lizard's tendency to display other typical antisnake tactics such as tail waving or fleeing. These results were highly repeatable across the two sampled genetic groups of velvet gecko, despite demonstrable genetic divergence between groups. Experiments with hatchling lizards that had no experience with predators indicate that qualitative components of antisnake behaviors are probably inherited. The method of phylogenetically independent contrasts strongly suggests that the presence or absence of snakes has driven the evolution of behavior in velvet geckos. Collectively, these results provide support for an often suggested but speculative expectation that prey can adapt to predation pressure on a local scale.

Responses to Chemical Cues from Plant and Animal Food by an Omnivorous Lizard, Gerrhosaurus validus

Many lizards use lingually sampled chemical cues to locate, identify, and perhaps assess the quality of foods (Cooper, 1995, 1997). Responses to prey chemicals have been studied in species representing all of the major lizard taxa. Primarily because most lizards are insectivorous/ carnivorous, far less is known about response to chemical cues from plant foods by omnivorous or herbivorous lizards. It seems probable that in species derived from insectivores that now exhibit prey chemical discrimination, adding plant food to the ancestrally animal diet set up the potential for natural selection to increase the sensitivity or responsiveness to plant food chemicals. This hypothesis must be tested comparatively; it cannot be tested using a single species. Among scleroglossan lizards, actively foraging insectivores can discriminate between prey and control stimuli using only chemical cues sampled by tongueflicking (Cooper, 1995, 1997, 1999, 2000a). This generalization applies to all species yet tested, but few species have been studied in most families. One of the most thoroughly studied groups is the Scincidae, one of three families in the Scincoidea. Prey chemical discrimination has been demonstrated in several actively foraging species of skinks (Loop and Scoville, 1972; Burghardt, 1973; Nicoletto, 1985; Cooper and Vitt, 1989; Cooper and Hartdegen, 1999; Cooper, 2000a) and was found to be absent in a single ambush forager (Cooper, 2000a). In the primarily herbivorous lygosomine skink Corucia zebrata (Cooper, 2000b), chemical cues from both plant and animal cues induced increased tongue-flick rates and higher frequency of biting than did control chemicals. Much less is known about chemosensory responses to food in the remaining families of Scincoidea. Gerrhosauridae and Cordylidae are the two families of the Cordyliformes, the sister taxon of the Scincidae. In the Cordylidae, prey and plant chemical discriminations are absent in an ambushing, insectivorous species, HAO, E.-M., AND K. ADLER. 1993. Herpetology of hina. Soc. Stud. Amph. Rept. Contrib. Herpetol. Cordylus cordylus (Cooper and Van Wyk, 1994; Cooper and Steele, 1999). The sole gerrhosaurid studied, Gerrhosaurus nigrolineatus, an insectivore (Branch, 1998) which is believed to be an active forager, exhibited prey chemical discrimination (Cooper, 1992). In this paper I present the first test of the hypothesis that an omnivorous species (Rogner, 1997) of gerrhosaurid lizard, Gerrhosaurus validus, discriminates plant food chemical cues from control chemicals. This species appears to be an active forager on the basis of limited field data (Cooper et al., 1997). In addition to providing a test of the specific prediction, the results add to the data base needed to test the hypothesis that correlated evolution has occurred between plant diet and chemosensory responsiveness to plant chemicals. Tests of responses to animal prey chemicals provide an additional test of the established evolutionary relationship between prey chemical discrimination and foraging mode in lizards (Cooper, 1995, 1997). Nine adult Gerrhosaurus validus were obtained from a commercial dealer and were housed in an accredited