Cooper, William E., Jr. and Jason J. Habegger.  2001.  Responses by juvenile savannah monitor lizards (Varanus exanthematicus) to chemical cues from animal prey, plants palatable to herbivores, and conspecifics.  Journal of Herpetology 35(4):618-624.

ABSTRACT

Varanid lizards often tongue-flick in feeding and social contexts, but little is known regarding their abilities to identify a variety of prey using only chemical cues or to detect pheromones. We studied responses by juvenile Varanus exanthematicus to surface chemical stimuli from several animal taxa, two plant species palatable to herbivorous lizards, and conspecifics, using diluted cologne and deionized water as pungency and odorless controls. In 60-sec trials with stimuli presented on cotton swabs, lizards showed stronger responses to prey stimuli from mouse, cricket, earthworm, and a gekkonid lizard than to control stimuli. These findings suggest that the lizards are able to locate and identify prey from a wide variety of taxa, which would be adaptive for a generalist predator. Only mouse and cricket stimuli induced a greater proportion of individuals to bite swabs than control stimuli. Because these prey were the laboratory diet, biting frequency may depend on familiarity with the prey. Like other tested insectivores and carnivores, V. exanthematicus showed no signs of discriminative responses to plant chemicals. The lizards tongue-flicked in response to conspecific cues at a higher rate than to the odorless control but at a lower rate than to cues from a gekkonid lizard, indicating that conspecific cues were detected and discriminated from prey cues.

Varanid lizards tongue-flick to investigate objects in diverse contexts, but empirical knowledge about their abilities to discriminate among biologically important chemical stimuli is limited. When a moist squamate tongue is protruded, it passes through a volume of air and often contacts a substrate. Molecules that adhere to it are transported into the mouth when the tongue is retracted (Graves and Halpern, 1989; Halpern, 1992); these molecules move through ducts opening into the roof of the mouth to the vomeronasal chemosensory epithelia (Graves and Halpern, 1989; Halpern and Kubie, 1980). Vomerolfaction, the sense mediated by the vomeronasal organs, is distinct from olfaction in being sensitive primarilly to nonvolatile molecules (Cooper and Burghardt, 1990a). Not all lizard tongue-flicking is for vomerolfactory sampling (Cooper, 1994a, Greenberg, 1993; Schwenk, 1985), but lingually mediated chemical discriminations of prey and plant foods require vomerolfaction (Cooper and Alberts, 1991).

Varanid lizards have highly developed lingual-vomeronasal systems. Their tongues are more deeply forked than those of other lizards (Cooper, 1996; Schwenk, 1994), and they have more abundant vomeronasal chemoreceptor cells than all other lizards except teiids (Cooper, 1997a; Gabe and Saint Girons, 1976). In addition, the frequent tongue-flicking exhibited while foraging, engaging in social behavior, and investigating novel situations (Auffenberg, 1981a,b, 1984) suggests that chemicals sampled by tongue-flicking may play important roles in evaluation of environmental stimuli.

Varanids can identify prey and predators using only chemical cues. Varanus exanthematicus tongue-flicked mouse surface chemicals at higher rates than control stimuli (Cooper, 1989a). New hatchlings of V. gouldii that had never eaten exhibited higher tongue-flick rates, and more lizards bit in response to internal chemicals from mashed crickets than to surface chemicals from mouse and gecko (Hemidactylus frenatus) or to odorous and odorless control stimuli (Garrett and Card, 1993). Varanus exanthematicus also exhibits strike-induced chemosensory searching (SICS), an attempt to follow chemical trails to relocate prey that has been bitten and then lost (Cooper, 1989b, 1993).

Much less is known about the use of chemical cues by varanids in other adaptive contexts. Responses to predator chemicals have been studied only in V. albigularis, in which naive hatchlings attacked invertebrate prey covered by skin of nonvenomous sympatric snakes but avoided prey covered by skin of venomous snakes that eat hatchlings (Phillips and Alberts, 1992). Pheromonal communication by varanids has not been studied, but field observations of social behavior in V. komodoensis, V. bengalensis, V. olivaceous, and V. salvator (Auffenberg, 1981a,b, 1988, 1994; Vogel, 1979) indicate that monitors tongue-flick each other frequently during social encounters and suggest that V. komodoensis may have a highly developed scent-trailing ability (Auffenberg, 1981a).

We report three experiments designed to assess aspects of chemosensory abilities of juvenile V. exanthematicus. This species is widespread in central and southern Africa (Hedges, 1983; Rogner, 1997). It consumes a variety of insects, other invertebrates, and vertebrates (Cisse, 1972; Hedges, 1983). We tested the ability to discriminate invertebrate and vertebrate prey chemicals from odorous and odorless control substances, expanding upon a previous study that investigated only mouse chemicals as prey cues (Cooper, 1989a). We also examined responses to chemical stimuli from two plant species, using a sample size large enough to detect any meaningful differences in frequencies of tongue-flicking and biting attack elicited by prey and control stimuli. Our data contribute to the information on carnivorous lizards necessary to ascertain whether responsiveness to plant chemicals evolved with plant diet in herbivores or was retained from carnivorous ancestors. Additionally, we report the first experimental observations of responses to conspecific chemical cues by varanids.

MATERIALS AND METHODS

Animals and Maintenance.--Twenty juvenile V. exanthematicus were obtained from Strictly Reptiles (Chicago, IL). They were held in an animal care facility at Indiana University-Purdue University Fort Wayne (IPFW) accredited by the American Association for Accreditation of Laboratory Animal Care. Each individual was housed singly in a glass terrarium (50 (times) 31 (times) 27 cm) having a substrate of indoor-outdoor carpet, a water bowl and a screen top. A 12:12 h L: D light cycle was maintained by fluorescent lighting. The room temperature was 29(degree)C, and heat lamps adjacent to cages provided the opportunity for thermoregulation. The lizards ate crickets and mice readily under laboratory conditions. To ensure motivation to feed, lizards were not fed for three days prior to each experiment.

Experimental Procedures.--Experiments were conducted to determine the responses of V. exanthematicus to chemical cues from several types of potential animal prey and to ascertain whether they show similar strong chemosensory and feeding responses to chemical stimuli from plants that evoke such response from herbivorous and omnivorous lizards. We also examined responses to skin chemicals of juvenile conspecifics. All chemical stimuli were prepared and presented on cotton swabs using procedures described in Cooper and Burghardt (1990b) and Cooper (1998a,b).

We used randomized blocks designs in which each individual was tested in all stimulus conditions and recorded numbers of tongue-flicks and the occurrence and latency in seconds of bites directed to cotton swabs bearing the stimuli in 60-sec trials. Tongue-flicks reflect chemosensory investigation and bites are predatory attacks. Bites on the swabs were readily distinguished from defensive bites observed in other contexts by the lack of aggressive posturing and by associated tongue-flicking. No defensive bites or associated defensive behavioral displays occurred during the experiments. Although the experimental designs were not blind, the procedures are standardized, and the lizards would have no opportunity to learn any subtle differences in presentation of stimulus types. The frequent occurrence of bites and their frequently exclusive occurrence in trials with prey stimuli in a wide range of studies by many investigators (studies reviewed by Cooper, 1994b) makes it clear that bites in these swab studies represent feeding attempts.

Diluted cologne was used as a pungency control (i.e., a control for responses to an odorous stimulus not relevant trophically or socially). In trials with cologne, lizards sometimes show behavior not seen in trials with water or other stimuli. These may vary across lizard species and include opening of the mouth (which may last several seconds), labial-licks, and tongue-flicks that do not contact the swab. Thus, although the numbers of tongue-flicks and bites directed to swabs typically do not differ from those in response to water (e.g., Cooper, 1998b, 2000a,b), it is clear that lizards detect the cologne.

In experiment 1, the stimuli presented were domestic cricket (Acheta domesticus), romaine lettuce, cologne, and deionized water. Romaine lettuce was selected as a plant stimulus source because chemical stimuli from this species elicit strong tongue-flicking and biting responses by some herbivorous lizards (WEC, unpubl. data) but not by an insectivorous lizard (Cooper and Hartdegen, 1999). In experiment 2, the stimuli were domestic mouse (Mus domesticus), earthworm (Lumbricus terrestris), dandelion flower (Taraxicum officinale), and deionized water. Dandelion flowers evoke strong chemosensory response from omnivorous skinks and agamine lizards (WEC, unpubl. data). In experiment 3, the stimuli tested were from the gekkonid lizard Chondrodactylus angulifer from South Africa, conspecifics, and deionized water. We predicted that the lizards would respond more strongly to chemical stimuli from the gecko as prey than to the water control and would detect conspecific chemical cues as indicated by a difference in tongue-flick rate from water. Trials were conducted from 1230-1800 h CST using a minimum intertrial interval of 60 min.

Statistical analyses.--The variables analyzed statistically were number of tongue-flicks per trial, number of individuals that bit swabs, and the tongue-flick attack score for repeated measures designs TFAS(R); Cooper and Burghardt, 1990b . The sequence of stimulus testing was counterbalanced in all experiments to prevent bias resulting from order of presentation. In experiment 1, four of the 24 possible sequences were eliminated randomly with the proviso that all stimulus types occurred first in one of the sequences removed. In experiment 2, the sequence of trials was partially counterbalanced for the 18 individuals that completed experiment 1 so that one sequence beginning with each stimulus type was eliminated. Experiment 3 was completely counterbalanced for 18 individuals.

Differences among stimuli in tongue-flicks and TFAS(R) were tested for significance primarily by analysis of variance for a single-factor experiment with a randomized blocks design. Nonparametric tests were used only if assumptions for parametric tests could not be met. Appropriate paired comparisons followed if the main effect was significant (Winer, 1962; Zar, 1996). Statistical procedures were as described in Cooper (2000a) and Cooper and Flowers (2001), with the exception that data on number of individuals that bit were analyzed using sign tests with significance levels protected by a sequential Bonferroni adjustment for the number of tests conducted (Wright, 1992). Data are presented as mean (plus or minus) 1.0 SE.

When responses to plant stimuli did not differ significantly from those to control stimuli, statistical power analyses were conducted to estimate the likelihood that real differences would have been detected. We used a procedure described in Zar (1996) to estimate the phi coefficient as 4.31 based on earlier experiments using the same methods (Cooper and Hartdegen, 1999).

RESULTS

Experiment 1.--TFAS(R) was much greater in the cricket condition than in any of the other conditions (Fig. 1). This was primarily a consequence of the much larger number of individuals that bit swabs bearing cricket stimuli than in the other conditions because the mean number of tongue-flicks was similar among all stimuli (Table 1). Two of 20 individuals were dropped from the experiment because they did not tongue-flick, one each with sequences in which cricket and romaine lettuce stimuli were tested first. For tongue-flicks, variances of the raw data were significantly heterogeneous (Fmax = 4.76, k = 4, df = 17, P < 0.05) but were rendered homogeneous by logarithmic transformation (Fmax = 1.74, k = 4, df = 17; P > 0.10). Using the transformed data, numbers of tongue-flicks (Fig. 1) did not differ significantly among conditions (F = 0.52; df = 3, 51; P > 0.10).

Thirteen of 18 individuals bit swabs bearing cricket stimuli, but none bit in the other conditions (Table 1). The number of individuals that bit was significantly greater in the cricket condition than in each of the other conditions (P < 1.2 (times) 10-4 each). Individuals that bit did so only after tongue-flicking. Latency to bite was 13.1 (plus or minus) 3.5, with range 2-40 sec. Another individual that performed the most tongue-flicks of all (76) did not bite but appeared to search visually.

TFAS(R) showed a similar pattern of significance to number of bites. Variances differed significantly among conditions for raw TFAS(R) (Fmax = 18.73, k = 4, df = 17, P < 0.01), but were homogeneous for the logarithmically transformed data (Fmax = 1.70, k = 4, df = 17, P > 0.10). The main condition effect was highly significant (F = 27.46, k = 3, df = 51, P << 0.001). TFAS(R) was significantly greater in the cricket condition than in any of the other conditions (P < 2.0 (times) 10-4 each), but did not differ significantly between any of the other pairs of conditions (P > 0.10 each; power was > 0.99).

Experiment 2.--The lizards responded strongly to chemical stimuli from animals but not to plant or control stimuli (Fig. 2, Table 1). Two individuals, one with worm stimuli and the other with dandelion stimuli in the first trial, were dropped from the experiment because of lack of tongue-flicking, giving a sample size of 16.

There were large differences among conditions in number of tongue-flicks (Table 1). The number of tongue-flicks had significantly heterogeneous variances (Fmax = 7.94, k = 4, df = 15, P < 0.01), but the logarithmically transformed variances were homogeneous (Fmax = 2.69, k = 4, df = 15, P > 0.05). The main effect for the transformed data was significant (F = 12.53; df = 3, 45; P < 5.0 (times) 10-6) because of high numbers of tongue-flicks to mouse and worm stimuli. The number of tongue-flicks in the mouse condition was significantly greater than in the dandelion (P < 3.0 (times) 10-4) and deionized water conditions (P < 5.0 (times) 10-4) but did not differ from that in the worm condition (P > 0.10). Number of tongue-flicks in the worm condition was significantly greater than in the dandelion and deionized water conditions (P < 4.0 (times) 10-4 each). Numbers of tongue-flicks did not differ significantly in the dandelion and deionized water conditions (P > 0.10).

Fewer individuals bit swabs than in experiment one, but biting was again restricted to swabs bearing chemical stimuli from animals (Table 1). Seven lizards bit in the mouse condition and three in the worm condition. Significantly more individuals bit in the mouse condition than in the dandelion and deionized water conditions (P < 0.008 each, one-tailed). No other differences among conditions were significant.

Data for TFAS(R) showed even greater differences among stimuli than the other variables (Fig. 2). Variances among conditions were significantly heterogeneous for both the raw data (Fmax = 14.09, k = 4, df = 15, = P < 0.01) and the logarithmically transformed data (Fmax = 4.74; k = 4, df = 15, P < 0.05). TFAS(R) varied significantly among conditions (x2 = 35.72, df = 3, P < 0.001). Multiple comparisons tests showed that mouse and worm stimuli each elicited significantly greater TFAS(R) than did dandelion stimuli or deionized water (P < 0.001 each). TFAS(R) did not differ significantly between the mouse and worm conditions (0.10 > P > 0.05) or the dandelion and deionized water conditions (P > 0.10; power was > 0.99).

Experiment 3.--Numbers of tongue-flicks varied substantially among conditions, with the highest tongue-flick rate in the gecko condition, an intermediate rate in the conspecific condition, and the lowest in the deionized water condition (Table 1). No lizards bit swabs. Because of the absence of biting, the number of tongue-flicks and TFAS(R) were identical. Variances for number of tongue-flicks were heterogeneous (Fmax = 3.65, k = 3, df = 17, P < 0.5) for the raw data but homogeneous for the logarithmically transformed data (Fmax = 1.49, k = 3, df = 17, P > 0.10). The main condition effect was highly significant (F = 20.96; df = 2, 34; P = 1.0 (times) 10-6). Differences in numbers of tongue-flicks between all stimulus pairs were significant: conspecific versus gecko, P < 0.0068; conspecific versus deionized water, P = 0.0012; gecko versus deionized water, P = 1.2 (times) 10-4).

DISCUSSION

Varanus exanthematicus is capable of discriminating prey chemicals from chemical cues from a variety of nonfood sources. The strong responses to mouse stimuli corroborate the findings of previous work on prey chemical discrimination and strike-induced chemosensory searching by this species (Cooper, 1989a,b, 1993). The stronger responses to chemical stimuli from crickets, mice, earthworms, and geckos than to deionized water show that the lizards detected the prey stimuli. The stronger responses to stimuli from these prey types than to cologne, plant, and conspecific stimuli reveal prey chemical discrimination.

The savannah monitor exhibits strong discriminative responses to chemical stimuli from a range of potential prey including representatives of three phyla and two vertebrate classes. This is as expected for an opportunistic, generalist predator that uses chemical cues to locate and identify food. Although it would have been preferable to use prey species sympatric with V. exanthematicus, animals used as stimulus sources belong to phyla consumed by the lizards in nature. Annelids have not been reported in the diet of V. exanthematicus although insects and vertebrates have (Cisse, 1972). The strong responses to chemical cues of allopatric animals presumably reflect chemical similarities between tested species related sympatric prey species.

Foraging behavior and diet importantly affect responsiveness to chemical stimuli by lizards. There are two major foraging modes among insectivorous and carnivorous lizards, active and ambush foraging. Active foragers, which move through the habitat while searching for prey, can identify and locate prey by chemical cues; ambush foragers, which wait immobile for passing prey, do not tongue-flick to locate and identify prey (Cooper, 1995, 1997b). Although quantitative data are lacking, terrestrial varanid lizards are considered to be active foragers (Cooper, 1994b). Data for V. exanthematicus conform to the prediction that active foragers exhibit prey chemical discrimination.

Diet and chemosensory responsiveness are closely linked in snakes (e. g., Arnold, 1981; Cooper et al., 1990, 2000), but this relationship is poorly understood in lizards, many of which are generalist predators of arthropods and other small prey. If such lizards respond to chemical cues from diverse prey taxa, as does V. exanthematicus, it will be difficult to ascertain any relationships between diet and responses to prey chemical cues.

Familiarity (Burghardt, 1992) and inclusion in the natural diet may account for much of the variation in responsiveness to chemical stimuli from the four potential prey species as observed in V. exanthematicus. These familiar foods were the only ones that elicited significantly greater frequency of biting than plant and other control stimuli. Most of the diet of V. exanthematicus consists of a variety of invertebrates, although it also eats some vertebrates (Cisse, 1972). This may account for biting by several individuals in trials with swabs bearing earthworm stimuli. Because V. exanthematicus eats reptiles (Hedges, 1983), the elevated tongue-flick rate in response to gecko stimuli may represent investigation of potential prey but not necessarily. That no lizards bit in experiment 3 shortly after participating in two similar experiments might be a result of habituation to testing or of the allopatry of C. angulifer and V. exanthematicus.

The plants used as stimulus sources did not elicit strong chemosensory investigation or feeding responses despite the likelihood that they provided complex organic chemical cues. The lack of difference in responses to chemical stimuli from plants, odorous control, and odorless control stimuli is presumably a real phenomenon given the high statistical power of the tests to detect such differences. This suggests either that the plant stimuli were undetectable or that they were detectable but did not elicit increased chemosensory investigation. Chemical stimuli from romaine lettuce and dandelion flowers elicit increases in tongue-flicking and biting by herbivorous lizards (Cooper, 2000a,c; Cooper and Flowers, 2001). Although the families of these herbivores have much lower densities of vomeronasal chemoreceptor cells than varanids (Cooper, 1997a; Gabe and Saint Girons, 1976), suggesting that varanids have greater vomerolfactory sensitivity, it is not clear whether V. exanthematicus has the capacity to detect the plant stimuli. Among monitor lizards, only V. olivaceus consumes substantial amounts of plant matter (Auffenberg, 1988). Even if V. exanthematicus detected plant stimuli, it presumably did not increase chemosensory investigation or attack because plant stimuli do not represent food.

Regardless of the detectability of plant stimuli, V. exanthematicus, like all other insectivorous and carnivorous lizards tested, did not respond strongly to plant chemicals (Cooper and Hartdegen, 1999; Cooper and Steele, 1999; Cooper 2000b; Cooper and Habegger, 2000; this study). In contrast, all species of plant-eating lizards tested, representing independent origins of plant consumption in three families, discriminate plant chemicals from control stimuli (e.g., Cooper and Alberts, 1990; Cooper, 2000a,c-d; Cooper and Flowers, 2001). More comparative data are needed to test the hypothesis that evolution of herbivory is accompanied by acquisition of responsiveness to plant chemicals.

Savannah monitors detected conspecific chemical cues, as shown by the greater number of tongue-flicks to conspecific cues than deionized water. That they also responded differently to conspecific and gecko cues demonstrates differential response to conspecific cues and suggests a capacity for pheromonal communication. Diverse lizards use pheromones for functions including identification of species, sex, reproductive status, kinship, and scent-trailing (Cooper, 1994b, reviewed by Mason, 1992). Several factors in addition to its widespread occurrence in other lizards suggest that pheromonal communication may occur in varanids: the deeply forked, elongated tongue and abundant vomerolfactory receptors, observations of tongue-flicking during social behavior (Auffenberg, 1981a, 1988, 1994), and the present finding of chemosensory discrimination of conspecific chemicals from those from another lizard and an odorless control. Experimental studies are needed to ascertain possible pheromonal functions.

Added material.
WILLIAM E. COOPER JR.1 AND JASON J. HABEGGER.
Department of Biology, Indiana University-Purdue University at Fort Wayne, Fort Wayne, Indiana 46805, USA.

1 Corresponding Author. E-mail: cooperw@ipfw.edu.

ACKNOWLEDGMENTS

This work was partially supported by a Summer Stipend for Undergraduate Research to JJH from Indiana University-Purdue University at Fort Wayne.

TABLE 1. Means, standard errors and ranges of tongue-flicks (TF) in 60 sec by Varanus exanthematicus and numbers of individuals that bit in response to swabs bearing chemical cues. Gecko = Chondrodactylus angulifer.
(TABLE) TF
Number
X SE Range that bit
Experiment 1 (N = 18)
Cricket 9.8 3.7 1-76 13
Romaine lettuce 11.4 2.3 2-34 0
Cologne 13.7 3.9 1-58 0
Deionized water 10.6 1.8 1-27 0
Experiment 2 (N = 16)
Mouse 25.8 4.6 2-52 7
Worm 22.4 3.5 6-51 3
Dandelion 7.4 1.7 1-23 0
Deionized water 7.1 1.6 1-24 0
Experiment 3 (N = 18)
Conspecific 16.5 3.2 1-43 0
Gecko 28.0 5.1 4-63 0
Deionized water 10.0 2.7 1-35 0.

FIG. 1. Tongue-flick attack scores (TFAS(R) for 18 Varanus exanthematicus responding to to cotton swabs bearing chemical stimuli from cricket (CR), romaine lettuce (RL), cologne (COL), and deionized water (WAT). Error bars represent 1.0 SE.

FIG. 2. Mean tongue-flick attack scores (TFAS(R)) for 16 Varanus exanthematicus responding to chemical stimuli from mouse (MO), earthworm (EW), cologne (CL), and deionized water (WA). Error bars represent 1.0 SE.

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