Tongue-flick Rates Research Articles

Guatemalan beaded lizards (Helodermatidae: Heloderma charlesbogerti) navigate and follow a scent trail in maze tasks.

Maze studies have provided substantial information about nonhuman cognition, such as insights on navigational strategies, spatial memory, and choice discriminations. This knowledge can aid in how we understand the foraging strategies of many animals, particularly understudied and endangered species, such as the Guatemalan beaded lizard (Heloderma charlesbogerti). These actively foraging lizards rely on chemoreception to locate prey, but it is unknown to what extent they engage in olfaction and vomerolfaction to hunt and navigate their environment. We investigated how Guatemalan beaded lizards moved through a physical maze. When navigating an eight-arm radial maze with all arms baited, lizards tended to turn into the immediately adjacent arm in a single direction, similar to other reptiles that have been tested in radial arm mazes. In a T-maze, the lizards had to discriminate between arms that contained scent and no-scent from a distance. They were generally unable to choose the baited (correct) arm at levels greater than chance, indicating an inability for this discrimination. With the addition of a scent trail, however, all lizards chose the baited arm at levels significantly above chance, and this increased accuracy was correlated with increased latency to make the arm choice. The lizards also demonstrated a decreased rate of tongue flicking as proximity to reward increased. Guatemalan beaded lizards can efficiently navigate a radial arm maze and can successfully use vomerolfaction with substrate-borne cues to locate prey, but they appear to have minimal olfaction abilities when sensing from a distance. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Heterospecific eavesdropping on disturbance cues of a treefrog.

Alarm signals and cues are crucial to animal survival and vary greatly across species. Eavesdropping on heterospecific alarm signals and cues can provide eavesdroppers with information about potential threats. In addition to acoustic alarm signals, evidence has accumulated that chemical alarm cues and disturbance cues can also play a role in alerting conspecifics to potential danger in adult anurans (frogs and toads). However, there is very little known about whether disturbance cues are exploited by heterospecifics. In the present study, we conducted a binary choice experiment and a prey chemical discrimination experiment, respectively, to test the responses of a sympatric anuran species (red webbed treefrogs, Rhacophorus rhodopus) and a sympatric predator species (Chinese green tree vipers, Trimeresurus stejnegeri) to disturbance odors emitted by serrate-legged small treefrogs (Kurixalus odontotarsus). In the binary choice experiment, we found that the presence of disturbance odors did not significantly trigger the avoidance behavior of R. rhodopus. In the prey chemical discrimination experiment, compared with odors from undisturbed K. odontotarsus (control odors) and odorless control, T. stejnegeri showed a significantly higher tongue-flick rate in response to disturbance odors. This result implies that disturbance odor cues of K. odontotarsus can be exploited by eavesdropping predators to detect prey. Our study provides partial evidence for heterospecific eavesdropping on disturbance cues and has an important implication for understanding heterospecific eavesdropping on chemical cues of adult anurans.

Behavioral patterns in the early-stage antipredator response change after tail autotomy in adult wall lizards.

Autotomy is a drastic antipredator defense consisting of the voluntary shedding of a body part to escape from the predators. The loss of a body part may impair locomotion, feeding or mating, so animals may face a higher predation risk shortly after autotomy. Thus, until regeneration is completed, prey may adjust their behavior to reduce predation risk, and this could involve secondary costs. We assessed the effect of tail loss on the antipredator behavior of wall lizards (Podarcis muralis), comparing the behavior of tailed and tailless individuals exposed to a predatory snake (Coronella austriaca) scent, under controlled experimental conditions. Tailless lizards spent significantly more time performing behaviors with antipredatory significance (e.g., moving slowly), whereas tailed individuals performed exploratory walking for significantly more time. Moreover, tailless lizards spent more time basking, which probably increases the effectiveness of their cryptic design and decreases detection by predators. Lizards intensified the tongue flick rates when exposed to a pungent control or snake scents, as compared to their response to a neutral control. Besides, both tailed and tailless lizards intensified some aspects of their antipredator behavior (walking slowly and avoiding refuge use) when exposed to snake scent, which indicates discrimination of the smell of predatory snakes. Lizards decreased refuge use when exposed to predator scents, probably because the refuges are evaluated as unsafe due to a high concentration of snake scents. To conclude, our experiments showed that, after losing their tails, wall lizards modify their behavior in a way that likely minimizes predation risk.

Chemical cues may allow a fossorial amphisbaenian reptile to avoid extremely saline soils when selecting microhabitats

When selecting optimal habitats, animals should rely on detecting environmental cues that indicate the suitability of a given site. In fossorial animals, restrictions of the underground environment might limit the opportunities for habitat selection. However, field observations of some fossorial amphisbaenian reptiles indicate that microhabitat occupancy is not random. This might simply result from the low survival of individuals in suboptimal habitats, but it may reflect active behavioral selection. We suggest that, in the fossorial environment, chemical cues may be very important for actively selecting or avoiding specific microhabitats. Here, we tested the ability of Trogonophis wiegmanni amphisbaenians to discriminate and select different types of substrates by using chemical cues alone. In laboratory preference tests, amphisbaenians selected soils with low salinity levels (natural or experimentally manipulated), mimicking the microhabitat selection patterns observed in the wild. Moreover, chemosensory tests measuring tongue-flick rates showed that amphisbaenians discriminated using chemical cues alone between soil types according to natural salinity levels, and also between manipulated chemical stimuli with different salinity levels. These results suggest that the microgeographic patterns of distribution of these amphisbaenians are due to their ability to use substrate chemical cues to actively avoid extremely saline soils. and select optimal microhabitats.

How to maintain underground social relationships? Chemosensory sex, partner and self recognition in a fossorial amphisbaenian.

Maintaining social relationships depends on the ability to recognize partners or group members against other individuals. This is especially important in animals with relatively stable social groups. The amphisbaenian Trogonophis wiegmanni is a semi blind fossorial reptile that spends its entire life underground where it interacts with mates and social partners. In this environment, visual cues are limited. Chemosensory cues may rather allow conspecific social and partner recognition. We recorded the number of tongue-flick (TF) rates of T. wiegmanni amphisbaenians to scents of both sexes with different pairing social bonds (familiar vs. unfamiliar) presented on cotton swabs to test discrimination of social groups. As seen from a rise in the number of TFs, males discriminated unfamiliar females from unfamiliar males. This suggests that chemical cues may be used by males to locate new mates. In contrast, females detected scent of unfamiliar conspecifics, but did not show sex discrimination. Both males and females discriminated the scent of an individual with which they had formed a pair bond from an unfamiliar individual of the same sex as the partner. Also, males, but not females, were capable of self-recognition, suggesting that scent marks of males in home ranges may provide individual information in intrasexual relationships. We conclude that conspecific discrimination based on chemical cues may allow the maintenance of social relationships and relatively stable pairs in fossorial reptiles inhabiting visually restricted environments.

Conspecific chemical cues facilitate mate trailing by invasive Argentine black and white tegus.

Squamate reptiles (snakes and lizards) rely on chemical cues from conspecifics to search the environment for potential mates. How such cues are used by invasive species to facilitate reproduction, especially seasonally, is a key question that can inform management practices. The Argentine black and white tegu (Salvator merianae) is an invasive reptile species in south Florida threatening native fauna in biodiverse regions such as Everglades National Park. While some information exists on the reproductive ecology of this species in its native range in South America, the chemical ecology of S. merianae is unclear especially in its invasive range. By testing both male (n = 7) and female (n = 7) tegus in a Y-maze apparatus, we assessed if either sex follows chemical trails left by conspecifics and if behaviors were sex- or season-specific. We conducted three types of trials where conspecifics created odor trails: Male-only (male scent only in base and one arm of Y), Female-only, and Male vs. female. Males did not preferentially follow scent trails from either sex, but they did differentially investigate conspecific scent from both sexes. Seasonally, males showed increased rates of chemosensory sampling (rates of tongue-flicking) during the spring (breeding season; March-May) compared to fall (non-breeding season; September-November). Males also had reduced turning and pausing behavior while trailing in the spring. Female tegus exhibited stronger conspecific trailing abilities than males, following both male and female scent trails, and they explored the maze less before making an arm choice. Females also investigated the scent trails intensely compared to males (more passes in scented arms, more time with scent trails). Our results demonstrate for the first time that females of an invasive reptile species can follow conspecific scent trails. Given the strong female responses to odor, sex-specific targeting of tegus via application of a conspecific chemical cue in traps could enhance removal rates of females during the breeding season.

Response behaviour of native lizards and invading wall lizard to interspecific scent: implications for invasion success

The human-assisted movement of species beyond their native range facilitates novel interactions between invaders and native species that can determine whether an introduced species becomes invasive and the nature of any consequences for native communities. Avoiding costly interactions through recognition and avoidance can be compromised by the naivety of native species to novel invaders and vice versa. We tested this hypothesis using the common wall lizard, Podarcis muralis, and the native lizard species with which it may now interact in Britain (common lizard, Zootoca vivipara, sand lizard, Lacerta agilis) and on Vancouver Island (northern alligator lizard, Elgaria coerulea) by exploring species' responses (tongue flicks, avoidance behaviour) to heterospecific scent cues in controlled experiments. The tongue flick response of P. muralis depended on the different species’ scent, with significantly more tongue flicks directed to E. coerulea scent than the other species and the control. This recognition did not result in any other behavioural response in P. muralis (i.e. attraction, aggression, avoidance). Lacerta agilis showed a strong recognition response to P. muralis scent, with more tongue flicks occurring close to the treatment stimuli than the control and aggressive behaviour directed towards the scent source. Conversely, Z. vivipara spent less time near P. muralis scent cues than the control but its tongue flick rate was higher towards this scent in this reduced time, consistent with an avoidance response. There was no evidence of E. coerulea recognition of P. muralis scent in terms of tongue flicks or time spent near the stimuli, although the native species did show a preference for P. muralis-scented refuges. Our results suggest a variable response of native species to the scent of P. muralis, from an avoidance response by Z. vivipara that mirrors patterns of exclusion observed in the field to direct aggression observed in L. agilis and an ambiguous reaction from E. coerulea which may reflect a diminished response to a cue with a low associated cost. These results have significant implications for the invasive success and potential impacts of introduced P. muralis populations on native lizards.

Chemosensory deficiency may render island-dwelling lizards more vulnerable to invasive predators

AbstractNewly introduced predators constitute a major threat to prey populations worldwide. Insular prey animals in particular often do not succeed in overcoming their naivety towards alien predators, making them specifically vulnerable. Why this is the case remains incompletely understood. Here, we investigate how the ability to detect and respond to predator chemical cues varies among populations of the Dalmatian wall lizard, Podarcis melisellensis. Lizards were sampled from five locations in south-eastern Croatia (one mainland location and four islands) that varied in the composition of their predator community. We observed the lizards’ behaviour in response to chemical cues of native saurophagous snakes (the Balkan whip snake, Hierophis gemonensis, and eastern Montpellier snake, Malpolon insignitus) and an introduced mammalian predator (the small Indian mongoose, Herpestes auropunctatus – a species held responsible for the loss of numerous insular reptile populations worldwide). Mainland lizards showed elevated tongue-flick rates (indicative of scent detection) as well as behaviours associated with distress in response to scents of both native and introduced predators. In sharp contrast, island lizards did not alter their behaviour when confronted with any of the predator cues. Alarmingly, even lizards from islands with native predators (both snakes and mammals) and from an island on which mongooses were introduced during the 1920s were non-responsive. This suggests that insular populations are chemosensorily deprived. As failure at the predator-detection level is often seen as the most damaging form of naivety, these results provide further insight into the mechanisms that render insular-living animals vulnerable to invasive species.

Male Burmese pythons follow female scent trails and show sex-specific behaviors.

Animals communicate with potential mates using species-specific signals, and pheromones are powerful sexual signals that modify conspecific behavior to facilitate mate location. Among the vertebrates, snakes are especially adept in mate searching via chemical trailing, which is particularly relevant given that many snake species are invasive outside their native ranges. Chemical signals used in mate choice are, thus, potentially valuable tools for management of invasive snake species. The Burmese python (Python bivittatus) is an invasive snake in the Florida Everglades where it is negatively impacting native fauna. In this study, we sought to: (i) determine if males can follow conspecific chemical trails in a Y-maze; and (ii) describe the mate searching behaviors exhibited by males while trailing. All males consistently followed a single female scent trail in the maze, but when only a male scent trail was present they did not discriminate between the male and blank arms. Rate of tongue-flicking, a proxy for chemosensory sampling, was also marginally higher when males were following female versus male scent trails. However, when both female and male scent trails were simultaneously present in the Y-maze, males did not show a preference for the female arm, although the tongue-flick rate was higher in the female-only trial compared to female versus male. Analyses of multiple male behaviors individually and using an ethogram revealed that behaviors were more frequent and complex in the female-only trials compared to male-only trials. Additional behavioral trials are needed to determine if an effective pheromonal approach to Burmese python management is possible.

Integrating behaviour into the pace-of-life continuum: Divergent levels of activity and information gathering in fast- and slow-living snakes

An animal’s life history, physiology, and behaviour can be shaped by selection in a manner that favours strong associations among these aspects of an integrated phenotype. Recent work combining animal personality and life-history theory proposes that animals with faster life-history strategies (i.e., fast growth, high annual reproductive rate, short lifespan) should exhibit higher general activity levels relative to those with slower life-history strategies, but empirical tests of within-species variation in these traits are lacking. In garter snakes from ecotypes which are known to differ in ecology, life-history strategy, and physiology, we tested for differences in tongue-flick rate as a measure of information gathering and movement patterns as a measure of general activity. Tongue flicks and movement were strongly positively correlated and both behaviours were repeatable across trials. Snakes from the fast-living ecotype were more active and showed evidence of habituation. The slow-living ecotype maintained low levels of activity throughout the trials. We propose that environmental factors, such as high predation, experienced by the fast-living ecotype select for both increased information-gathering and activity levels to facilitate efficient responses to repeated challenges. Thus, we offer evidence that behaviour is an important component of co-evolved suites of traits forming a general pace-of-life continuum in this system.

How phylogeny and foraging ecology drive the level of chemosensory exploration in lizards and snakes.

The chemical senses are crucial for squamates (lizards and snakes). The extent to which squamates utilize their chemosensory system, however, varies greatly among taxa and species' foraging strategies, and played an influential role in squamate evolution. In lizards, 'Scleroglossa' evolved a state where species use chemical cues to search for food (active foragers), whereas 'Iguania' retained the use of vision to hunt prey (ambush foragers). However, such strict dichotomy is flawed as shifts in foraging modes have occurred in all clades. Here, we attempted to disentangle effects of foraging ecology from phylogenetic trait conservatism as leading cause of the disparity in chemosensory investment among squamates. To do so, we used species' tongue-flick rate (TFR) in the absence of ecological relevant chemical stimuli as a proxy for its fundamental level of chemosensory investigation, that is baseline TFR. Based on literature data of nearly 100 species and using phylogenetic comparative methods, we tested whether and how foraging mode and diet affect baseline TFR. Our results show that baseline TFR is higher in active than ambush foragers. Although baseline TFRs appear phylogenetically stable in some lizard taxa, that is a consequence of concordant stability of foraging mode: when foraging mode shifts within taxa, so does baseline TFR. Also, baseline TFR is a good predictor of prey chemical discriminatory ability, as we established a strong positive relationship between baseline TFR and TFR in response to prey. Baseline TFR is unrelated to diet. Essentially, foraging mode, not phylogenetic relatedness, drives convergent evolution of similar levels of squamate chemosensory investigation.

Intersexual chemo-sensation in a "visually-oriented" lizard, Anolis sagrei.

While the conspicuous visual displays of anoles have been studied in great depth, the possibility that these lizards may also interact through chemical signalling has received hardly any consideration. In this study, we observed the behaviour of male brown anoles (Anolis sagrei) when introduced into an environment previously inhabited by female conspecifics, and compared it to when they were introduced into an untreated environment. The males in our tests exhibited significantly more elaborate display behaviour (i.e., greater number of dewlap extensions and head-nods) and a significantly greater number of tongue extrusions while in the cage formerly occupied by females than when placed in the untreated, control cage. The absolute numbers of tongue extrusions, however, were relatively low in comparison to average tongue-flick rates of ‘true’ chemically-oriented lizards. Our results strongly suggest that the males were capable of detecting chemical cues left behind by the females. These observations provide the first evidence of intersexual chemo-sensation in an anole lizard.

Predators as mediators: Differential antipredator behavior in competitive lizard species in a multi-predator environment

Prey response to different predators is complex and can include diverse antipredatory strategies. In syntopic populations of competing species common predators can play a mediator role thus influence the interaction out-come of prey-species in an indirect way. We studied differences in antipredator response in two competing lizards in syntopy in a multi-predator environment. Studied prey species, Iberolacerta horvathi and Podarcis muralis, are likely to compete in syntopic populations limited in size and have similar morphology and ecology but exhibit fine-scale ecophysiological differences. Taking into account interspecific differences in ecophysiology we expected that I. horvathi as a more precise thermoregulator would be less prone to use refuges that represent a thermal cost (are colder than outside). The pattern we found was the opposite of our expectations; I. horvathi escaped at greater distances and remained in the refuge for longer before re-emerging than P. muralis. Second part of the study revealed that both species were able to recognize chemical cues of predator snakes (represented as higher tongue flick rates in the presence of scents of predator snakes in comparison to control). Behavioral responses, which are linked with stressful situations connected to saurophagous snakes, were more frequent and variable in I. horvathi. Overall, antipredator responses seem to be more pronounced in I. horvathi than in P. muralis. While this “more cautious” attitude of I. horvathi should provide higher short-term benefits (higher survival rates), this would hold true only in populations where predation pressure is high. Otherwise it carries substantial time and thermoregulatory costs. For I. horvathi, costs of refuge use should be even higher due to narrower dimensions of their ecophysiological fundamental niche. Such divergences in antipredator behavior are expected to shape the relationships between both species in syntopic populations modulated by common predation pressure and habitat structure.

Behavioral variation in prey odor responses in northern pine snake neonates and adults

Squamate reptiles (snakes, lizards, amphisbaenians) rely heavily on chemosensory cues to identify, locate and choose between suitable prey items, but comparatively little research has focused on the chemical ecology of threatened squamate species. Such knowledge highlights ecologically important aspects of their survival. Due to gape limitations, squamates often demonstrate ontogenetic shifts in their diet where they consume larger prey as they grow older and their gape size increases. This shift enables squamates—especially snakes—to exploit new resources in their environments, usually mammalian prey. To test for ontogenetic variation in prey odor responses of a threatened snake species, the Northern pine snake (Pituophis melanoleucus melanoleucus), we presented food-naive neonates and food-experienced adults with potential prey and non-prey animal scents and quantified their behavioral responses. Our data indicate a strong response to rodent scents from both neonates and adults. Further, neonates showed more frequent investigative probing and retreating behaviors from scented swabs and a higher rate of tongue-flicking than adults. We also developed a new metric for measuring snake responses to prey odor, a tongue-flick reaction score (TFRS), that incorporates investigative behaviors that may be unique to constrictor-type snakes. The TFRS did not differ between age classes and was highest when rodent odors were tested. A canonical discriminant analysis confirmed the relationship between TFRS behavioral components and tested chemical signal reactions. Based on our data, P. melanoleucus may fall into a category of snakes that exhibit an ontogenetic telescope rather than a general ontogenetic shift in their prey odor responses.

Chemosensory Prey Detection by the AmphisbaenianTrogonophis wiegmanni

Foraging underground poses a number of important challenges for fossorial animals, such as amphisbaenians. For instance, visual detection and identification of prey is often hampered by low light conditions and poor eye sight. In response, many fossorial animals have switched to other sensory systems, such as chemoreception. We tested the ability of the amphisbaenian Trogonophis wiegmanni to detect and discriminate between different prey types based on chemical cues alone. Results of a laboratory experiment showed that amphisbaenians were able to detect prey using chemoreception, as indicated by an increase in chemosensory tongue-flick responses to swabs bearing chemicals from prey in comparison with blank controls. Also, differential tongue-flick rates to chemicals from different prey types indicated that at least some prey types may be discriminated from others based on chemosensory cues. These results suggest that T. wiegmanni amphisbaenians use chemoreception when foraging.

Chemical recognition in a snake–lizard predator–prey system

In a predator–prey interaction, the fitnesses of the predator and the prey depend on their abilities to recognize each other, a process that may involve different sensory modalities. Squamate reptiles are highly dependent on chemical senses for such recognition, and here we explored the ability of a generalist saurophagous snake, Philodryas chamissonis, to discriminate scents of two congeneric and sympatric lizard prey species, Liolaemus nitidus and L. chiliensis. A generalist saurophagous snake might just be sensitive to lizard scents in general, and if so, no discrimination between prey species is expected. However, these lizards use different substrates; L. nitidus basks on rocks, whereas L. chiliensis mainly basks on bushes and rarely on ground. The snake P. chamissonis basks on ground and rocks, and rarely on bushes. Therefore, if the rate of encounter affects the ability to recognize prey, we predict that P. chamissonis would show prey discrimination because scents of L. chiliensis may be encountered less frequently in its habitat. Results showed that the snake had a refined discrimination of lizard prey, reducing tongue flick rate and movements in response to scents from the common prey scents, L. nitidus. We also studied the ability of L. chiliensis to detect the snake and found that snake scents triggered a reduction in activity. The potential infrequent encounter between predator and prey may explain the asymmetric predator–prey recognition, as can be predicted from the “life-dinner” principle.

Prey Chemical Discrimination by the Desert Nightsnake (Hypsiglena chlorophaea): A Comparison of Invertebrate and Vertebrate Prey

We investigated responses of adult and juvenile Desert Nightsnakes (Hypsiglena chlorophaea) to odor extracts of potential invertebrate and vertebrate prey. Snakes were collected during 2009 from three localities in Washington state. We obtained odor from three potential invertebrate prey—spider (Tegenaria spp.), scorpion (Paruroctonus boreus), and field cricket (Gryllus spp.)—and compared responses with a vertebrate prey item, a Western Terrestrial Gartersnake (Thamnophis elegans). All potential prey items were collected at the same site as H. chlorophaea. We presented odors on 15-cm cotton swabs held 2.5 cm in front of the snake's snout. For each trial we recorded the number of tongue flicks in 60 sec, the latency to first tongue flick, and whether the stimulus elicited an attack. We observed no significant difference in latency of responses between spider, scorpion, cricket, or snake odors. However, both adult and juvenile H. chlorophaea responded with higher tongue-flick rates to snake odor. Juveniles showed an increase in tongue-flick rate toward crickets. Attacks were made against snake odor with no difference between adult and juvenile responses. Our results indicate that adults and juveniles of H. chlorophaea do not feed on invertebrates, and in some cases invertebrates may pose a threat to small snakes such as H. chlorophaea. However, the diet of H. chlorophaea may vary geographically, and populations of H. chlorophaea with a more southerly distribution may feed on invertebrates. Whether such differences in diet exist between populations will remain unresolved until additional studies of the diet of southern populations of H. chlorophaea are compared with those of northern populations.

Chemosensory age discrimination in the snake <i>Boa constrictor</i> (Serpentes: Boidae)

Many snakes are able to use their chemosensory system to detect scent of conspecifics, which is important in many social contexts. Age discrimination based on chemical cues may be especially important to ensure access to sexually mature potential partners. In this study, we used 24 individual Boa constrictor snakes (12 adults mature and 12 non-mature individuals) that had been captured in different areas of Ecuador, and were maintained in captivity at the Vivarium of Quito. We used tongue-flick experiments to examine whether these snakes were able to discriminate between scents from mature and non-mature individuals. Results showed that B. constrictor snakes used chemical cues to recognize conspecifics and that the scent of individuals of different ages elicited chemosensory responses of different magnitudes. The scents from adult conspecifics elicited the quickest and highest chemosensory responses (i.e., short latency times and high tongue-flick rates), although we did not find differential responses to scent of males and females. The magnitude of the responses was lower to scent of sub adult individuals, and then even lower to scent of juvenile snakes, but in all cases the scent of snakes was discriminated from a blank control. We discuss the potential chemical mechanisms that may allow age recognition and its implications for social and sexual behavior of this snake species.

The Function of Oscillatory Tongue-Flicks in Snakes: Insights from Kinematics of Tongue-Flicking in the Banded Water Snake (Nerodia fasciata)

Tongue-flicking is an important sensory behavior unique to squamate reptiles in which chemical stimuli gathered by the tongue are delivered the vomeronasal organ situated in the roof of the mouth. Because tongue-flick numbers can easily be quantified, this behavior has been widely used as a measure of vomeronasal sampling in snakes using related variables such as tongue-flick rate or tongue-flick/attack score. Surprisingly, the behavior itself and especially the function of the oscillatory tongue-flicks remains poorly understood. To describe the overall kinematics of tongue-flicking in the colubrid snake Nerodia fasciata and to test predictions on the function of oscillatory tongue-flicks, we filmed the tongue-flicks of 8 adult Nerodia fasciata using 4 synchronized high-speed cameras. Three-dimensional kinematic and performance variables were extracted from the videos in order to quantify tongue movements. Based on the kinematic analysis, we demonstrate the existence of 2 functional and behavioral tongue-flick categories. Tongue-flicks with oscillations meet all the criteria for being adapted to the collection of odorants; simple downward extensions appear better suited for the rapid pick up of nonvolatile chemical stimuli from the substrate or a food item. External stimuli such as tactile and/or vomeronasal stimulation can induce a shift between these categories.

Ontogenetic shift in response to prey-derived chemical cues in prairie rattlesnakes Crotalus viridis viridis

Abstract Snakes often have specialized diets that undergo a shift from one prey type to another depending on the life stage of the snake. Crotalus viridis viridis (prairie rattlesnake) takes different prey at different life stages, and neonates typically prey on ectotherms, while adults feed almost entirely on small endotherms. We hypothesized that elevated rates of tongue flicking to chemical stimuli should correlate with particular prey consumed, and that this response shifts from one prey type to another as individuals age. To examine if an ontogenetic shift in response to chemical cues occurred, we recorded the rate of tongue flicking for 25 neonate, 20 subadult, and 20 adult (average SVL = 280.9, 552, 789.5 mm, respectively) wild-caught C. v. viridis to chemical stimuli presented on a cotton-tipped applicator; water-soluble cues from two ectotherms (prairie lizard, Sceloporus undulatus, and house gecko, Hemidactylus frenatus), two endotherms (deer mouse, Peromyscus maniculatus and lab mouse, Mus musculus), and water controls were used. Neonates tongue flicked significantly more to chemical cues of their common prey, S. undulatus, than to all other chemical cues; however, the response to this lizard’s chemical cues decreased in adult rattlesnakes. Subadults tongue flicked with a higher rate of tongue flicking to both S. undulatus and P. maniculatus than to all other treatments, and adults tongue flicked significantly more to P. maniculatus than to all other chemical cues. In addition, all three sub-classes demonstrated a greater response for natural prey chemical cues over chemical stimuli of prey not encountered in the wild (M. musculus and H. frenatus). This shift in chemosensory response correlated with the previously described ontogenetic shifts in C. v. viridis diet. Because many vipers show a similar ontogenetic shift in diet and venom composition, we suggest that this shift in prey cue discrimination is likely a general phenomenon among viperid snakes.