Plant Chemical Discrimination Research Articles

Prey chemical discrimination by a diploglossine lizard, the giant Hispaniolan galliwasp (Celestus warreni)

AbstractPrey chemical discrimination, the ability to respond differentially to prey chemicals and control stimuli, enables many squamate reptiles to locate and identify prey using chemical cues sampled by tongue-flicking and analyzed by vomerolfaction. Among lizards this ability is limited to species that are active foragers having insectivorous/carnivorous diets and to omnivores and herbivores, even those derived from ancestral ambush foragers. We experimentally studied responses by hatchlings of giant Hispaniolan galliwasps, Celestus warreni, which appear to have a strict animal diet and are putatively active foragers, to prey chemicals and control substances. More individuals tongue-flicked in the cricket condition than the water condition. Response strength indicated by the tongue-flick attack score, a composite index of response strength based on number of tongue-flicks, biting (one lizard) and latency to bite, was greater in response to cricket stimuli than plant (lettuce) stimuli, cologne or distilled water. Thus, the galliwasps exhibited prey chemical discrimination. Celestus warreni, the first representative of Diploglossinae to be tested, exhibits chemosensory behavior similar to that of other anguids. Although no quantitative data on foraging mode are available, another diploglossine, Diploglossus vittatus, is an active forager. The limitation of prey chemical discrimination to active foragers among lizards with animal diets lend further support to the likelihood that C. warreni is an active forager. The galliwasps did not exhibit plant chemical discrimination.

Phylogenetic Constraints Do Not Block Food Chemical Discrimination in the Omnivorous Phrynosomatid Lizard Uma Exsul

In lizards identification of food using chemical cues allows active foragers to locate hidden prey and omnivores and herbivores to identify palatable plant food, but ambush foragers identify food visually rather than chemically. Omnivores and herbivores derived from ambushing ancestors discriminate food chemicals from control substances. The only known exception is the omnivorous phrynosomatid lizard Sceloporus poinsettii, which lacks food chemical discrimination and which might have been constrained from evolving it by scarcity of chemoreceptors. We studied food chemical discrimination by the phrynosomatid Uma exsul, an omnivore whose diet is 25% plant by volume. In 60 s trials in which chemical cues from mealworms, romaine lettuce, cologne, and water were presented on cotton swabs, lizards responded more strongly to plant and animal chemicals than control stimuli. Food chemical discrimination by Uma exsul strengthens evidence that plant chemical discrimination evolves in tandem with plant diet and prey chemical discrimination also appears in omnivores or herbivores derived from ambush foragers. Confirmation of food chemical discrimination in U. exsul vitiates the evolutionary constraint hypothesis for S. poinsettii. That lizards tongue-flicked and bit infrequently, yet discriminated, is unusual, suggesting that lingually mediated plant chemical discrimination may have evolved recently, few tongue-flicks are needed to evaluate nutritive properties of plant foods, or plant chemical discrimination is an adaptively unimportant epiphenomenon of plant consumption. Because they do not search actively for prey or tongue-flick before attacking, phrynosomatids presumably evolve prey chemical discrimination by genetic correlation with plant chemical discrimination.

Tasty figs and tasteless flies: plant chemical discrimination but no prey chemical discrimination in the cordylid lizard Platysaurus broadleyi

Lizards use visual and/or chemical cues to locate and identify food. The ability to discriminate prey chemical cues is affected by phylogeny, diet, and foraging mode. Augrabies flat lizards (Platysaurus broadleyi) are omnivorous members of the lizard clade Scleroglossa. Within Scleroglossa, all previously tested omnivores are capable of both prey and plant chemical discrimination. At Augrabies Falls National Park, P. broadleyi feed on both insects (black flies) and plant material (figs), and as scleroglossans, are predicted to discriminate both plant and prey chemicals. However, Platysaurus broadleyi use visual, not chemical cues, to detect and capture black flies, which occur in large concentrations in the study area. We tested free-ranging individuals for the ability to discriminate insect and plant chemicals from controls. There was a significant stimulus effect such that lizards tongue-flicked fig-labelled tiles significantly more than the remaining stimuli, spent more time at the fig-labelled tile, and attempted to eat fig-labelled tiles more often than tiles labelled with control or insect stimuli. Platysaurus broadleyi is exceptional in being the first lizard shown to possess plant chemical discrimination but to lack prey chemical discrimination. We suggest that an absence of prey chemical discrimination may be a consequence of foraging behaviour and environmental effects. Because insect prey are highly clumped, abundant, and aerial, profitable ambushing using visual cues may have relaxed any selective pressure favouring insect prey chemical discrimination. However, a more likely alternative is that responses to figs are gustatory, whereas as prey chemical discrimination and plant chemical discrimination are usually mediated by vomerolfaction.

Correlated evolution of herbivory and food chemical discrimination in iguanian and ambush foraging lizards

To efficiently locate and assess foods, animal sensory capacities and behavioral discriminations based on them must be appropriate for the diet and method of hunting. In lizards, actively foraging insectivores identify animal prey using lingually sampled chemical cues, but ambush foragers do not. Among plant eaters derived from active foragers, plant chemical discrimination is added to prey chemical discrimination, resulting in correlated evolution of plant diet and plant chemical discrimination. Here I present comparative evidence on the relationships between plant diet and food chemical discrimination in Iguania, which consists primarily of ambush foragers and is one of two major lizard clades, and for ambushing lizards in general. Comparative analyses conducted using phylogenetic methods show that (1) all but one species of omnivore studied exhibited both prey and plant chemical discrimination, whereas ambush foragers exhibited neither; (2) significant correlated evolution occurred between plant diet and plant chemical discrimination in Iguania and in omnivores and herbivores derived from ambush foragers; and (3) correlated evolution has occurred between prey and plant chemical discrimination in Iguania and, more generally, in taxa derived from ambush foragers. These results are explained by selection on plant eaters to assess the nutritional value and possible toxicity of plants and by continued consumption of some animal prey even in herbivores combined with freedom from factors that select against prey chemical discrimination in ambush foragers. Copyright 2003.

Food Chemical Discrimination by the Omnivorous Lizard Leiolepis belliana

The omnivorous acrodont lizard Leiolepis belliana was shown experimentally to respond more strongly to chemical cues from prey and plant food than from control stimuli, as indicated by tongue-flicking and biting responses. These results extend previous findings that prey and plant chemical discrimination is widespread among omnivorous iguanians.

Convergent evolution of plant chemical discrimination by omnivorous and herbivorous scleroglossan lizards

AbstractBecause sensory capacities and responsiveness must correspond to adaptively important environmental cues, they may require evolutionary modification to match shifts in the adaptive milieu. Many lizards identify prey by tongue‐flicking, especially actively foraging species of Scleroglossa, the speciose lizard taxon that includes snakes. Correspondence between diet and chemosensory responsiveness, although known in two genera of colubrid snakes, has not been established in lizards because most species are generalist predators. Omnivory and herbivory are uncommon among scleroglossans, but have evolved frequently enough to permit tests of the hypothesis that shifts to plant consumption have been accompanied by acquisition of responsiveness to plant food chemicals. Based on literature surveys I traced the evolution of scleroglossan lizard diet and food chemical discrimination. Three tests taking phylogenetic relationships into account (concentrated changes tests, Pagel's tests, and a modification of Ridley's test) showed that correlated evolution has occurred, with strong responses to plant chemicals having evolved convergently in at least five taxa that underwent shifts from insectivory to omnivory or herbivory. In all four origins of omnivory and herbivory in taxa derived from ancestral active foragers, lizards retained prey chemical discrimination. In the single origin of omnivory in an ancestrally ambush foraging taxon, both plant and prey chemical discrimination evolved de novo. These findings show that one aspect of chemosensory identification of food has been evolutionarily adjusted to diet in a major group of vertebrates.

Food-chemical discrimination and correlated evolution between plant diet and plant-chemical discrimination in lacertiform lizards

Lizards use chemical cues to locate and identify prey and plant food, assess the nutritional quality of food, and detect plant toxins. Among insectivorous lizards, all actively foraging species studied respond strongly to prey chemicals sampled lingually, but ambush foragers do not. Much recent research has been devoted to assessing differential responses to food and nonfood chemicals (i.e., food-chemical discrimination) by omnivorous and herbivorous species and determining whether correlated evolution has occurred between plant diet and plant-chemical discrimination. We conducted experimental studies of food-chemical discrimination by two species of teiid lizards, the omnivorous Cnemidophorus murinus and the actively foraging insectivorous Ameiva ameiva. The omnivore distinguished both prey and plant chemicals from control substances. The insectivore exhibited prey-chemical, but not plant-chemical, discrimination, as indicated by tongue-flicking and biting. A comparative analysis using concentrated-changes tests showed that correlated evolution has occurred between plant consumption and plant-chemical discrimination in a major lizard taxon, Lacertiformes. These results extend and strengthen previous findings of similar correlated evolution to a new group and add to a growing database indicating that omnivorous lizards use chemical cues to assess both prey and plant foods.

RESPONSES TO FOOD CHEMICALS BY TWO INSECTIVOROUS AND ONE OMNIVOROUS SPECIES OF LACERTID LIZARDS

In snakes, many of which have fairly specialized diets, there is a correspondence between diet and chemosensory responsiveness to food cues not yet demonstrated in lizards, most of which are generalist insectivores. If such a correspondence exists for plants consumed by omnivorous species, we can make two predictions. Actively foraging insectivorous lizards such as most lacertids should exhibit prey chemical discrimination, but be unresponsive to chemicals from palatable plants. Omnivorous species derived from insectivores should discriminate both prey and plant chemicals from control substances. We show in experiments testing lingual and biting responses to food cues and control stimuli that the lacertid insectivores Podarcis hispanica and Lacerta perspicillata exhibit prey, but not plant, chemical discrimination and the omnivore P.sicula discriminates both prey and plant chemicals from control substances. The findings are consistent with the hypothesis that correlated evolution has occurred between plant consumption and plant chemical discrimination in lacertids, but data are needed for several more lineages of independently derived omnivores and for additional insectivores to test the hypothesis statistically.

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

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.

Responses to Animal and Plant Chemicals by Several Iguanian Insectivores and the Tuatara, Sphenodon punctatus

We conducted experimental tests of the responses to food chemicals presented on cotton swabs or ceramic tiles by tuataras and insectivorous species from several families of iguanian lizards. Tu- ataras, which are primarily carnivorous, never tongue flicked but frequently bit cotton balls bearing prey surface chemicals, suggesting that they may be able to detect airborne prey chemicals via olfaction. None of the lizards tested, the agamids Chamaeleo pardalis and Acanthosaura crucigera, the polychrotids Anolis smallwoodi and Chamaeleolis chamaeleonides, the phrynosomatids Sceloporus variabilis and Uta stansburi- ana, and the crotaphytid Crotaphytus collaris, exhibited any differential responses among prey chemicals, chemicals from palatable plants, and pungency control or odorless control stimuli. The findings buttress previous work that has shown a lack of prey chemical discrimination in ambush foragers, including all sampled iguanian insectivores. Given that all tested omnivores and herbivores respond strongly to plant chemicals, they are also consistent with the hypothesis that discriminatory lingual and biting responses to plant chemicals occur only in species having diets with a large plant component. Correlated evolution between herbivory and plant chemical discrimination remains to be established. For unknown reasons, Sceloporus variabilis tongue flicked less frequently in tile tests with romaine lettuce stimuli than with cricket and banana stimuli.

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.

Plant chemical discriminations by an herbivorous iguanid lizard, Sauromalus ater

AbstractWe experimentally studied the ability of the iguanid lizard Sauromalus ater to discriminate between plant and animal foods and control stimuli using only chemical cues. When chemicals were presented on cotton swabs, the lizards exhibited stronger responses, as indicated by tongue-flicking and biting, to chemical stimuli from romaine lettuce than from crickets and control substances. Responses to plant and animal food did not differ significantly in S. ater, which eats animal prey only occasionally in natural populations. Although there were no significant differences between responses to cricket chemicals and other stimuli for the entire data set, those individuals that ate or attacked crickets tongue-flicked at high rates in response to cricket chemicals. Based on the presence of herbivory and plant chemical discrimination in three iguanid genera, it is likely that plant chemical discrimination is ubiquitous in iguanids. Given the uncertainty of iguanian phylogeny, the evolution of herbivory and response to plant chemicals cannot be traced with confidence. However, it appears very likely that lingually mediated plant chemical discriminations evolved in the common ancestor of Iguanidae or earlier in iguanian history in response to a shift to an herbivorous diet.

Responses to prey and plant chemicals by three iguanian lizards: relationship to plants in the diet

AbstractWe examined responses of three iguanian lizards, the phrynosomatid Sceloporus poinsettii and the tropidurids Tropidurus hispidus and Phymaturus punae, to prey chemicals and plant chemicals. When chemical stimuli were presented on cotton swabs or on ceramic tiles, neither S. poinsettii nor T. hispidus discriminated among prey, plant, and control stimuli. In contrast, an individual of P. punae discriminated both prey and plant chemicals from control stimuli in swab tests, typically biting swabs bearing prey or plant cues. These findings are consistent with the hypothesis that plant chemical discrimination evolves in herbivorous iguanians such as P. punae. Sceloporus poinsettii, which appears to be entirely insectivorous at some times, but eats substantial quantities of flowers at others, did not discriminate among the stimuli. Because all previously tested herbivores and omnivores responded strongly to prey and plant chemicals, the absence of such discriminations by S. poinsettii raises questions about the degree and regularity of herbivory that may be required for plant chemical discrimination to evolve. The results extend the absence of prey chemical discrimination in ambush foragers to T. hispidus.

Elevated tongue-flicking and biting by the insectivorous lygosomine skink Mabuya macularia to prey, but not plant, chemicals

The ability of an insectivorous scincid lizard, Mabuya macularia to discriminate among prey chemicals and control substances and its responses to chemical cues from several plant species eaten by herbivorous and omnivorous lizards were examined experimentally using the swab method. We presented cotton swabs bearing chemical cues to the lizards and recorded the numbers of tongue-flicks directed to swabs in 60 sec and whether or not they bit the swab. The lizards exhibited much stronger responses to prey chemicals (cricket) than to stimuli from romaine lettuce, diluted cologne (pungency control), and deionized water (odorless control). Responses to romaine lettuce stimuli did not differ from those to the two control stimuli. In further observations, there were no significant differences in response strength between deionized water and chemical stimuli from strawberry, red grape, and dandelion flower. These findings support the hypothesis that insectivorous lizards do not exhibit strong chemosensory investigation of plants that are palatable and do induce high rates of tongue-flicking and/or biting in herbivorous lizards. Although insufficient comparative data are available to test the hypothesis that plant chemical discrimination evolves in response to dietary shifts from insectivory to omnivory or herbivory, the present data and all published data are consistent with the hypothesis. The data for M. macularia suggest that plant chemical discriminations may have been absent in basal lygosomine skinks and derived in the herbivorous lygosomine Corucia zebrata.

Responses to chemical cues from animal and plant foods by actively foraging insectivorous and omnivorous scincine lizards

If tongue-flicking is important to lizards to sample chemical cues permitting identification of foods, tongue-flicking and subsequent feeding responses should be adjusted to match diet. This hypothesis can be examined for plant foods because most lizards are insectivores, but herbivory/omnivory has evolved independently in many lizard taxa. Here we present experimental data on chemosensory responses to chemical cues from animal prey and palatable plants by three species of the scincine lizards. When tested with chemical stimuli presented on cotton swabs, the insectivorous Eumeces fasciatus responded strongly to prey chemicals but not to chemicals from plants palatable to omnivorous lizards or to pungent or odorless control stimuli. Two omnivorous species, E. schneideri and Scincus mitranus, responded more strongly to chemical cues from both prey and food plants than to the control chemicals. All available data for actively foraging lizards, including these skinks, show that they are capable of prey chemical discrimination, and insectivores do not exhibit elevated tongue-flicking or biting responses to chemical cues from palatable plants. In all of the several species of herbivores/omnivores tested, the lizards show elevated responses to both animal and plant chemicals. We suggest two independent origins of both omnivory and plant chemical discrimination that may account for the evolution of diet and food chemical discriminations in the eight species of skinks studied, five of which are omnivores. All data are consistent with the hypothesis that acquisition of omnivory is accompanied by acquisition of plant chemical discrimination, but data on a broad diversity of taxa are needed for a definitive comparative test of the evolutionary hypothesis. J. Exp. Zool. 287:327-339, 2000.