Tongue-flick Rates Research Articles

Lingual and Biting Responses to Food Chemicals by Some Eublepharid and Gekkonid Geckos

Lingual and Biting Responses to Food Chemicals by Some Eublepharid and Gekkonid Geckos

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.

Prey chemical discrimination in ambush foragers: absence in representatives of two additional iguanian lizard families and probable olfactory mediation in a gekkonine gecko

Lingually mediated prey chemical discrimination in lizards has evolved in active foragers, been lost in taxa that have reverted to ambush foraging, and has not evolved in taxa that have retained the ancestral ambushing. Previous studies have shown that all families of insectivorous ambushers lack prey chemical discrimination, including most families of iguanian lizards and two gekkonid species. I conducted experimental studies of prey chemical discrimination in representatives of two additional iguanian families and a third gekkonid lizard. An oplurid species, Oplurus cuvieri and a corytophanid, Corytophanes cristatus, did not discriminate among prey chemicals and control substances. Prey chemical discrimination is now known to be absent in insectivorous ambush foragers in all but one of the families in Iguania, one of the two major lizard radiations. Hoplocercidae remains unstudied. Like other ambushing gekkonid lizards, Pachydactylus turneri did not exhibit elevated tongue-flick rates in response to prey chemicals. However, after tongue-flicking or being touched on the labial scales by cotton swabs, these lizards bit swabs bearing prey chemicals more frequently than control stimuli. They also exhibited buccal pulsing more frequently in response to prey chemicals than deionized water, suggesting olfactory sampling. The unusually highly developed olfactory organs of gekkonid lizards and their nocturnal habits suggest that olfaction may be more important to foraging than in other lizards. Further studies are needed to determine relative roles of olfaction and vomerolfaction in selective response to prey chemicals and to ascertain whether and to what extent the tongue may be used to locate and identify prey.

Olfactory discrimination in scat-piling lizards

Several lizard species in the Australian scincid genus Egernia have been reported to deposit scats in piles. We show that E. striolata, which does produce scat piles, and E. inornata, which does not, can both discriminate their own secretions, on paper substrates, from those of unfamiliar conspecifics. This was indicated by elevated tongue flick rates and more time in contact with the unfamiliar stimulus. This was not just a response to a novel stimulus because the secretions from another species (E. stokesii) elicited lower responses. When scats were presented, only striolata demonstrated discrimination between their own scats and those of unfamiliar conspecifics. This suggests that scats could be used to produce individual signals, perhaps indicating residence status, in scat-piling species. For striolata the signal from scats became less effective as the scats became older, suggesting the need to pile scats to renew the signal. Key words: communication, Egernia, lizards, recognition, scats, skinks. [Behav Ecol 10:136‐140 (1999)]

Intraspecific Chemical Recognition in the Lizard Liolaemus tenuis

Experimental tests were conducted to determine whether females and males of the tree-dwelling lizard Liolaemus tenuis (Tropiduridae) show intraspecific chemical recognition during breeding and postreproductive seasons. Animals were individually maintained in plastic enclosures for one week. Thereafter, the number of tongue-flicks that a lizard performed in the enclosure of a male, a female, its own home enclosure, and a control (unused) enclosure were recorded. In both seasons, males and females made fewer tongue-flicks in their home enclosures than in any other one, indicating a recognition of a familiar place, probably a chemical self-recognition. Conspecific chemical recognition was season dependent. During the post-reproductive season, lizards tongue-flicked at similar rates in conspecific and control enclosures, while during the breeding season enclosures of females elicited more tongue-flicks by both sexes, and the overall tongue-flick rates were higher than in the postreproductive season. Results are discussed within the context of the social system of the species.

Discriminative Response to Animal, But Not Plant, Chemicals by an Insectivorous, Actively Foraging Lizard, Scincella lateralis , and Differential Response to Surface and Internal Prey Cues

Responses by the insectivorous, actively foraging scincid lizard, Scincella lateralis, to chemical cues from a plant food favored by herbivorous lizards, its ability to discriminate prey chemicals from control substances, and its relative response to internal and surface prey chemicals were studied experimentally. We presented chemical cues to the lizards on cotton swabs and recorded their tongue-flicks and biting attacks on the swabs. The lizards exhibited significantly greater tongue-flick rates and biting frequencies to prey surface cues than to plant surface chemicals from romaine lettuce, diluted cologne (pungency control), and deionized water. Responses to the plant stimuli did not differ from those to the two control stimuli, in contrast with strong responses to the same plant cues by herbivores. This finding provides the first information suggesting that chemosensory response may be adapted to diet, with responsiveness to plant stimuli evolving de novo in herbivores. Biting and tongue-flicking responses were significantly greater to cricket chemicals than to all other stimuli, among which there were no differences. Thus, the lizards are capable of prey chemical discrimination, which may be ubiquitous among actively foraging lizards. The lizards exhibited more frequent biting and higher tongue-flick rates to internal than surface prey chemicals. Although different methods of stimulus preparation are appropriate for different purposes, we conclude that prey surface chemicals available to foraging lizards are most desirable for studies bearing on location and identification of prey.

Discrimination between self-produced pheromones and those produced by individuals of the same sex in the lizard Cordylus cordylus

Male and female Cordylus cordylus can discriminate between tiles labeled by their own pheromones and tiles labeled by individuals of the same sex, as shown by elevated tongue-flick rates in which the tongue contacts only air above the tiles labeled by other individuals and tongue-flicks in which the tongue contacts the tiles themselves. Potential pheromone sources for these discriminations are the femoral glands, cloacal glands, generation glands, ventral skin, and excretory products. Although studied in few species, pheromonal discriminations between self and other individuals, familiar and unfamiliar individuals, and kin and unrelated individuals appear to be broadly distributed in lizards, occurring in Iguania and in both Gekkonoidea and Scincomorpha within Scleroglossa. Both sexes of C. cordylus defend territories against both sexes. An ability to distinguish pheromones of other individuals of the same sex from self-produced pheromones would allow detection of intruders, but pheromonal discriminations among individuals would be more useful. Adaptive functions of pheromonal discriminations for residents and nonresidents and discriminatory abilities required are discussed. Tongue-flicks touching labeled tiles differed between experimental conditions, suggesting vomerolfactory discrimination, but the interpretation of a similar difference for tongue-flicks that contacted no substrate is problematical. Such air tongue-flicks might indicate sampling of volatile molecules for delivery to the vomeronasal organs. Experiments are needed to conclusively determine the sensory bases of the discriminations and the role of air tongue-flicks.

Iberian Rock Lizards (Lacerta monticola cyreni) Assess Conspecific Information Using Composite Signals from Faecal Pellets

AbstractA field and laboratory study was performed to analyse the role of excrement deposited on the substrate in intraspecific communication of the Iberian rock‐lizard (Lacerta monticola cyreni). In the field, lizards selected specific sites on rocks to deposit faecal pellets, probably in order to facilitate visual location of pellets by conspecifics. Differential tongue flick rates to chemicals presented on cotton swabs demonstrated that male lizards can detect and discriminate between self‐produced scents from faecal pellets and those of other conspecific males. In a subsequent experiment, male lizards were tested in a chamber with two platforms containing a faecal pellet of other male on one side and a control artificial pellet on the opposite side. Males spent significantly less time on the side containing the faecal pellet, suggesting that the decision of where to stay may depend on the presence of faecal pellets. Smaller males moved less than larger males on the experimental side whereas on the control side body size did not influence the proportion of time moving. The ability to discriminate chemicals from faeces, and the effects of faecal pellets on lizard behaviour, suggests that faeces might act as composite signals (visual and chemical) in the intraspecific communication of this lizard.

Pheromonal Discrimination of Sex by Male and Female Leopard Geckos (Eublepharis macularius)

The ability of male and female Eublepharis macularius to discriminate among pheromones of males and females and a blank control was investigated. Stimuli were presented on ceramic tiles in the animal's home cages. Males tongue-flicked at significantly lower rates in response to male stimuli than to female and control stimuli. Males also performed aggressive behaviors toward male, but not female or control, stimuli, and tail vibrations toward female, but not male or control, stimuli. Mean tongue-flick rates by females did not differ significantly among conditions. Discrimination of male pheromones by females was demonstrated by greater performance of labial-licking and chin-rubbing in response to male stimuli than to either female or control stimuli.

Response to Rodent Saliva by Two Species of Rodentiophagous Snakes

Brown tree snakes (Boiga irregularis) and prairie rattlesnakes (Crotalus viridis) responded with higher rates of tongue flicking to rodent saliva than to water. Both materials were presented on cotton-tipped applicators touched gently to the snakes' lips. Rattlesnakes also struck more frequently at applicators bearing saliva than at control applicators. Since rodents frequently lick themselves during bouts of grooming behavior, saliva is certainly a component of the chemicals associated with rodent integuments. It is concluded that this association has given rise in rodentiophagous predators to a sensitivity to saliva or to salivary components.

The role of nasal chemical senses in garter snake response to airborne odor cues from prey.

Garter snakes increase tongue-flick rates in the presence of airborne odorants (amyl acetate, limonene, earthworm wash vapor, fish water vapor, earthworms, goldfish) but not water vapor. Main olfactory (MO) nerve lesions result in loss of this tongue-flick rate elevation in the presence of airborne odorants. Vomeronasal (VN) nerve lesions result in a diminution of tongue-flick rate elevation. Garter snakes discriminate between the 2 arms of a maze containing airborne earthworm odor as compared with a blank control. Following MO nerve lesions, snakes fail to make this discrimination. Following VN nerve lesions or VN duct suture, snakes are initially able to make the discrimination but may eventually cease to prefer the prey-odor side of the maze and may stop eating prey rewards. These results support the idea that airborne odorants are detected by the main MO system and that such detection does not require a functional VN system.

Effects of movement and eating on chemosensory tongue-flicking and on labial-licking in the leopard gecko (Eublepharis macularius)

Two forms of lingual protrusion, tongueflicking and labial-licking, were differentially affected by combinations of movement and eating conditions in a eublepharid gecko (Eublepharis macularius). Tongue-flicking, in which the tongue contacts substrates beyond the lizard's body, occurred at increased rates during locomotion and during locomotion was significantly more frequent after eating than in a baseline condition. Labial-licking, in which a protruded portion of the tongue touches the labial, mental or rostral scales that surround the mouth, increased after eating. Unlike tongue-flick rates, by far the highest labial-lick rates were observed in stationary lizards after eating. The elevated tongue-flicking rates during movement after eating may be a manifestation of a postingestive chemosensory search for prey. In addition to grooming, several possible chemosensory functions of labial-licking are discussed, including gustatory sampling, sampling prey chemicals on the labials for transfer to the vomeronasal system, and redistribution of chemicals on the tongue to enhance transfer. It is suggested that labial-licking might help motionless lizards maintain vigilance for visual prey stimuli associated with the specific chemical prey cues. Another possible explanation for the increased labial-lick rate while motionless after eating is that prey chemicals induce tongue-flicking, but that the distance protruded is lessened and the tongue does not contact environmental substrates. Tongue-flicking while stationary is unlikely to lead to detection of additional prey and might incur detection by the lizard's predators or prey.

Post-prandial chemosensory searching in black rat snakes

In a laboratory experiment, black rat snakes, Elaphe o. obsoleta, increased rates of tongue flicking following ingestion of prey. This post-prandial tongue-flick increase, in combination with searching behaviour, represented post-prandial chemosensory searching (PPCS). Such chemosensory searching enabled rat snakes to locate subsequent prey more quickly than initial prey, which may prove beneficial in the wild. Single snakes of five other colubrid species also showed post-prandial tongue flick increases in similar experiments. Field observations are described that support inferences drawn from experimental results. Strike-induced chemosensory searching (SICS) is well known in venomous snakes, and was thought to have evolved as an adaptation for chemically trailing envenomated prey after voluntary release. This study adds to a growing list of non-venomous squamates that appear to show SICS, suggesting that the trait may instead be widespread and ancestral. The data are consistent with the view that SICS arose in a snake–lizard ancestor and may now serve different functions in different lineages. The emerging scenario for the evolution of chemosensory searching is a complex mix of adaptation and exaptation, underscoring the need to distinguish historical origin from current utility in the study of behavioural traits.

Do lingual behaviors and locomotion by two gekkotan lizards after experimental loss of bitten prey indicate chemosensory search?

Abstract Poststrike elevation in tongue-flicking rate (PETF) and strike-induced chemosensory searching (SICS) were assessed experimentally in two species of gekkonoid lizards belonging to families differing in foraging mode. PETF is an increase in rate of lingual protrusions after a prey item has been bitten and escapes or is removed from the mouth of a squamate reptile, whereas SICS is PETF combined with locomotory searching behavior. Eublepharis mucularius, the leopard gecko, is an actively, albeit slowly, foraging eublepharid. This species exhibited PETF for a duration of about five minutes based on total lingual protrusions. Labial-licks were initially much more frequent than tongue-flicks. A substantial increase in movement occurred during minutes 5-8, hinting that SICS might be present, but was not quite significant. SICS is likely present, as in other actively foraging lizards, but was not conclusively demonstrated. Handling the lizards induced increased locomotion in both the experimental condition and a control condition, presumably accounting for the apparent delay in onset of increased movement. The tokay gecko, Gekko gecko, a gekkonid ambush forager, performed no tongue-flicks, but exhibited PETF based on labial-licks during the first minute. SICS was absent. These findings support the hypothesis that SICS is absent in ambush foraging lizards, which do not use the lingual-vomeronasal system to search for prey. They are suggestive, but equivocal regarding the hypothesis that SICS is present in actively foraging lizards that exhibit lingually mediated prey chemical discrimination. The finding of PETF in G. gecko suggests that this species and several iguanians previously found to increase rates of labial-licking after biting prey may be able to detect prey chemicals.

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.

Strike-Induced Chemosensory Searching in the Gila Monster

Strike-induced chemosensory searching (SICS), consisting of a poststrike elevation in tongue-flick rate (PETF) and searching movements following voluntary release or removal of prey from the predator's mouth, is experimentally verified in a helodermatid lizard, the gila monster (Heloderma suspectum). This finding agrees with previous results showing that PETF and SICS are present in all families of autarchoglossan lizards and snakes studied and in families of active foragers. Since SICS was found to last at least 10 min, longer than in any squamate reptiles except snakes and varanid lizards, the duration of SICS is greatest in the clade consisting of Varanoidea (Helodermatidae + Varanidae) and Serpentes. Long-lasting SICS in this clade is consistent with the hypothesis that morphological specialization of the tongue and vomeronasal system enhancing chemosensory detection and identification of prey may be important for the evolution of long duration. However, the short duration of SICS in teiids suggests the additional importance of phylogenetic constraints. Although the gila monster is venomous, SICS in this species has not led to evolution of a strikerelease-trail strategy as employed by highly venomous sankes, presumably because the gila monster does not eat large, dangerous prey and does not use its venom to subdue prey.

Prey Chemical Discrimination and Foraging Mode in Gekkonoid Lizards

Relationships among phylogeny, foraging mode, and prey chemical discrimination by tongue-flicking were investigated by experimentally testing for the presence of lingually mediated prey chemical discrimination in representatives of two families of gekkonoid lizards having different foraging modes. In the experiments, the tongue-flicking and biting responses of each lizard were recorded in response to cotton swabs bearing three classes of stimuli: prey surface chemicals, cologne as a pungency control, and deionized water as an odorless control. In a eublepharid species, Eublepharis macularius, the tongue-flick rate, the proportion of individuals attacking the swab, and a composite measure combining effects of tongue-flicking and attack (TFAS(R)) were significantly higher and the latency to attack significantly shorter in the prey stimulus condition than in the other conditions, which did not themselves differ. In contrast, no tongue-flicking or attacks were observed in any of the conditions for two gekkonid species, Thecadactylus rapicauda and Gekko gecko. Because eublepharids are active foragers whereas gekkonids are ambush foragers, prey chemical discrimination was associated with active foraging, as predicted. Prior to this report, all families of ambush-foraging lizards known to lack prey chemical discrimination belonged to a single clade, Iguania. Actively foraging carnivorous lizards identify prey by chemical cues and belong to Scleroglossa, which includes the families studied here. It is argued that adoption of active foraging may have induced selection for gain of prey chemical discrimination involving tongueflicking in eublepharids. Phylogeny and the presence or absence of prey chemical discrimination are closely related in lizard families because foraging mode is conservative in the major clades Iguania and Scleroglossa.

Strike-induced chemosensory searching by the anguid lizard Elgaria coerulea

AbstractStrike-induced chemosensory searching (SICS), including a post-strike elevation in tongue-flick rate (PETF) and searching movements following experimental removal of prey from the predator's mouth, is demonstrated to occur in an anguid lizard, Elgaria coerulea. This finding confirms predictions based on the previously established widespread occurrence of SICS in scleroglossan (especially autarchoglossan) lizard families and on a strong association between SICS and active foraging. Reasons why SICS should be favored by natural selection in active foragers are discussed, but the presence of SICS in anguids is attributed to phylogenetic inertia rather than adaptation. SICS was statistically significant only during the first two minutes in E. coerulea. Its limited duration in an anguid and much greater duration in helodermatids, varanids, and snakes suggest that prolonged SICS may have had a single origin in the common ancestor of Varanoidea or, much less likely, of (Varanoidea + Xenosauridae). Uncertainties about origins due to missing data on certain taxa and to unresolved phylogenetic relationships within Seleroglossa are discussed.

Prolonged poststrike elevation in tongue-flicking rate with rapid onset in gila monster,Heloderma suspectum: Relation to diet and foraging and implications for evolution of chemosensory searching

Experimental tests showed that poststrike elevation in tongue-flicking rate (PETF) and strike-induced chemosensory searching (SICS) in the gila monster last longer than reported for any other lizard. Based on analysis of numbers of tongue-flicks emitted in 5-min intervals, significant PETF was detected in all intervals up to and including minutes 41-45. Using 10-min intervals, PETF lasted though minutes 46-55. Two of eight individuals continued tongue-flicking throughout the 60 min after biting prey, whereas all individuals ceased tongue-flicking in a control condition after minute 35. The apparent presence of PETF lasting at least an hour in some individuals suggests that there may be important individual differences in duration of PETF. PETF and/or SICS are present in all families of autarchoglossan lizards studied except Cordylidae, the only family lacking linguallly mediated prey chemical discrimination. However, its duration is known to be greater than 2-min only in Helodermatidae and Varanidae, the living representatives of Varanoidea. That prolonged PETF and SICS are typical of snakes provides another character supporting a possible a varanoid ancestry for Serpentes. Analysis of 1-min intervals showed that PETF occurred in the first minute. A review of the literature suggests that a pause in tongue-flicking and delay of searching movements are absent in lizards and the few nonvenomous colubrid snakes tested. The delayed onset of SICS may be a specific adaptation of some viperid snakes to allow potentially dangerous prey to be rendered harmless by venom following voluntary release after envenomation and preceding further physical contact with the prey.

Pheromone detection by an amphisbaenı́an

Abstract. Detection of conspecific chemical stimuli and their use to discriminate males from females is demonstrated in an amphisbaenian, Blanus cinereus. In two experiments using randomized blocks designs, males were presented cotton swabs bearing male stimuli, female stimuli, and deionized water in counterbalanced sequence. Detection of conspecific stimuli was evident by the significantly higher tongue-flick rates by male subjects in response to chemical stimuli from precloacal pores and trunk skin of both sexes than from a control stimulus. Differential response was indicated by a significantly greater tongue-flick rate in response to female than to male precloacal pore stimuli. That more males bit applicators bearing conspecific male precloacal pore stimuli than the other stimuli also suggests functional recognition of males. That tongue-flick rates for male and female trunk skin stimuli were indistinguishable suggests that tongue-flicking the trunk skin does not allow sex recognition and that sex pheromones are not present in that region. Latency to the first tongue-flick was shorter in response to precloacal pore stimuli of females than that of males, suggesting that volatile pheromonal components most likely detected by olfaction elicit tongue-flicking. Because the sensory basis for discriminations based on tongue-flicking is presumably vomerolfaction, the possibility must be considered that olfaction contributes to the tongue-flicking rate for pheromonal responses involving analysis of lingually sampled pheromones by the vomeronasal system to both initial and later responses. Because pheromonal responses by B. cinereus are similar to those in scleroglossan lizards and snakes, the closest relatives of amphisbaenians, pheromonal communication may be plesiomorphic in this taxon. It may be selectively important in amphisbaenians due to fossoriality and reduced vision.