Tongue-flick Rates Research Articles

Responses by amphisbaenianBlanus cinereus to chemicals from prey or potentially harmful ant species

We tested the ability of amphisbaenians (Blanus cinereus) to discriminate between odors of ant species selected as prey (Pheidole pallidula) and odors of potentially harmful ant species (Messor barbarus) that are avoided. Tongue-flick rate to swabs impregnated with ant odors, cologne, or deionized water differed among treatments, showing that amphisbaenians were able to discriminate ant species odors. Amphisbaenians showed an aggressive response and bit applicators bearing the odor of harmful ants, while the odor of prey ants did not elicit bites to swabs. The possible evolutionary advantage of identifying and avoiding harmful ants is discussed in relation to the fossoriality of amphisbaenians.

Strike-induced chemosensory searching is absent in the cordylid lizard,Cordylus cordylus, a scleroglossan ambush forager

Strike-induced chemosensory searching (SICS) was not detected experimentally in the cordylid lizard,Cordylus cordylus. Both components of SICS, a post-strike elevation in tongue-flick rate (PETF) and searching movements for attacked and released prey, were absent. The findings are consistent with previous data showing that PETF and/or SICS are lacking in all lizard families yet studied that forage primarily by ambush, but are present in actively foraging scleroglossan families and the herbivorous iguanian family Iguanidae. It is suggested that foraging behavior is a primary determinant of the presence or absence of SICS in lizards. Nevertheless, in most families in the two major clades, Iguania and Scleroglossa, the plesiomorphic foraging mode is retained. The findings agree with the prediction that SICS is absent in families lacking lingually mediated prey chemical discrimination (PCD), presumably due to selection against movement by ambush foragers that avoid being detected by either prey or predators because they remain motionless. Although PETF and SICS were absent, labial-licking and lingual movements similar to those observed after swallowing increased after biting prey, suggesting that the functions of these lingual movements may have been related to grooming. Locomotory movements did not increase following biting and appeared to represent avoidance of the experimenter.

Postbite elevation in tongue-flicking rate by an iguanian lizard,Dipsosaurus dorsalis

The herbivorous iguanid lizardDipsosaurus dorsalis exhibited PETF (postbite elevation in tongue-flicking rate), an increase in tongue-flicking rate after experimental removal from the mouth of food that had been bitten. This was demonstrated by a significantly higher tongue-flick rate after having bitten food than in three experimental conditions controlling for responses to the experimental setting, sight of food, and mechanical disturbance caused by the experimental removal of food from a lizard's mouth. As in most other families of lizards, PETF was brief, occurring only during the first minute. Lizards are divided into two major suprafamilial taxa, Iguania and Scleroglossa, consisting of carnivorous species characterized by two major foraging modes, ambush and active, and of herbivores and omnivores. PETF is absent in the two families of carnivorous iguanian lizards studied that are ambush foragers but present in three families of scleroglossan lizards that are active foragers. However, PETF is absent in the two species studied in a scleroglossan family, Gekkonidae, which forages by ambush, and present in an iguanian herbivore, as reported herein. We propose that the presence or absence of PETF, in addition to its phylogenetic determinants, is adaptively adjusted to foraging mode.

Feeding behavior and an oropharyngeal component of satiety in a two-headed snake

We studied the feeding behavior of a dicephalous Black Rat Snake ( Elaphe o. obsoleta) whose heads attack and ingest prey independently. Both heads were given satiation feedings with mouse prey at either 5-day intervals (1989, n = 16 feedings) or 9–11 day intervals (1990, n = 4 feedings). In 1989, a meal pattern was manifested as a negative correlation between total (left + right) meal size (g) and total size of the last meal. Meal sizes of the heads were consistently different (L > R) despite their apparently identical genotypes. We confirmed tongue-flicking rate and swallowing time as indices of satiety/hunger in each head. In order to test whether oropharyngeal stimulation is involved in satiation, we analyzed three measures: willingness to feed, and intrameal changes in swallowing, and tongue-flicking rates. Data for these tests were taken from experimental feedings in which one head was fed to satiation (first head) before the other head (second head) was fed. The second head generally did eat (8 of 10 experimental feedings) after the first head had become satiated. In addition, while the time to swallow a mouse generally increased as the snake neared satiety, swallowing time decreased significantly ( p = 0.04) from the first head's last mouse to the second head's first mouse. Finally, in two of three feedings, the first head's tongue-flicking rate decreased before the second head's. These results, which take advantage of this unique animal, indicate that oropharyngeal stimulation is involved in meal termination.

Strike-induced chemosensory searching by a teiid lizard, the golden tegu (Tupinambis nigropunctatus)

Strike-induced chemosensory searching (SICS) is experimentally demonstrated in a teiid lizard,Tupinambis nigropunctatus. SICS consists of a concurrent post-strike elevation in tongue-flick rate (PETF) and searching movements after voluntary release or escape of bitten prey or removal of prey from the predator's mouth. The results are consistent with previous data showing that PETF and/or SICS occur in all families of scleroglossan lizards and snakes and all families of actively foraging lizards yet studied. The relatively short duration of SICS (2 min) in a lizard having lingual and vomeronasal structure highly specialized for chemosensory sampling and analysis suggests that phylogenetic and ecological factors may be more important than morphology in determining the duration. The greatest known durations occur only in the presumably monophyletic clade containing varanoid lizards and snakes, all of which have highly developed chemical sampling and chemoreceptor apparatus, but in addition feed on prey that has a high probability of being relocated by prolonged scent-trailing. Because only active foragers move through the habitat while tongue-flicking and exhibit lingually mediated prey chemical discrimination, only active foragers may be expected to use SICS. SICS would appear to be useless to an ambush forager and might disrupt its defensive crypticity, rendering it more detectable to predators and prey. Therefore, it may be predicted that SICS is adaptively adjusted to foraging mode.

Prey chemical discrimination and strike-induced chemosensory searching in the lizardLiolaemus zapallarensis

Experimental tests were conducted to determine whether the ambush foraging iguanian lizard,Liolaemus zapallarensis, was capable of discriminating prey chemicals from control substances and whether this lizard exhibits strike-induced chemosensory searching (SICS) or its components after biting prey. The two components of SICS are a poststrike elevation in tongue-flicking rate (PETF) and apparent searching movements for relocation of prey that has been bitten, but released or escaped.Liolaemus zapallarensis failed to discriminate prey chemicals from control substances, but exhibited significant PETF lasting one minute. SICS was absent inL. zapallarensis because no post-strike movements were observed. The absence of both prey chemical discrimination and SICS exhibited byL. zapallarensis is common to all the insectivorous iguanians and ambush foraging lizards studied to date. However,L. zapallarensis is the first insectivorous iguanian species shown to exhibit PETF. The results suggest thatL. zapallarensis does not use the tongue for detection, identification, or relocation of prey while foraging. The possibility does remain thatL. zapallarensis may be capable of chemically identifying prey once the prey stimuli reach the oral cavity.

MAO-A and -B inhibitors selectivity alter Xenopus mucus-induced behaviors of snakes

Skin mucus of the frog Xenopus laevis, contacted orally by snakes, induces dyskinetic oral movements and climbing behavior that promote escape. The mucus contains peptides and indoleamines known to produce drug-induced movement disorders in other species. We hypothesized that inhibition of monoamine oxidase-A (MAO-A) by N-methyl- N-propargyl-3-(2,4-dichlorophenoxy)-propylamine [clorgyline (CLG)] and MAO-B by R(-)-N,a- Dimethyl-N-2- propynyl-benzeneethanam ine [ L-deprenyl (LDL) ] would selectively modify mucus-induced behaviors by elevating norepinephrine and serotonin (with CLG), phenylethylamine (with LDL), or dopamine (with both drugs). In Experiment 1 (EXP1), adult snakes received mucus and/or 20 μg/g (IP) of both drugs. In EXP2, juveniles received mucus and/or 5, 10, and 20 μg CLG or LDL. CLG given alone had no effect on tongue flicking, activity, and climbing (EXP1,2). LDL alone decreased tongue flicking in EXP2 and increased climbing (EXP1,2). Given with mucus, both drugs further lowered the tongue flicking rates attenuated by mucus (EXP1,2); only LDL potentiated mucus-induced climbing. Yawning was the only mucus-induced dyskinesia attenuated (20 μg CLG, adults; 20 μg LDL, juveniles). We suggest that dopamine and/or phenylethylamine, the substrates for MAO-B, may promote mucus-induced climbing and tongue flicking but may have some protective role against mucus-induced yawning in water snakes.

Response of brown tree snakes (Boiga irregularis) to human blood

Ten specimens ofBoiga irregularis were presented with clean or bloody tampons. The latter were used by women during menses. Trial duration was 60 sec, intertrial interval was 24 hr, and the dependent variable was rate of tongue flicking (a measure of chemosensory investigation). Bloody tampons elicited significantly more tongue flicking than did control tampons. An additional snake is shown attacking and ingesting a soiled tampon, confirming that chemosensory interest was associated with predatory behavior.

Stimuli Influencing the Release and Aim of Predatory Strikes of the Northern Pacific Rattlesnake (Crotalus viridis oreganus)

This study examined the relative importance of visual, chemical and thermal stimuli for releasing predatory strikes of the northern Pacific rattlesnake (Crotalus viridis oreganus). In experiment 1, adult snakes deprived of food for 30 days or longer were randomly presented four stimulus conditions (1 /day) combining visual, visual-chemical, visual-thermal and visual-chemical-thermal stimuli in moving models resembling mice. Experiment 2 replicated experiment 1 except that snakes were deprived of food 9 days and a fifth condition, live mice, was added. The number of strikes elicited by each condition suggested that visual cues alone were ineffective releasers of the strike, the addition of thermal cues dramatically increased the likelihood of attack, and the presence of chemical cues was not essential for striking. However, differences between the two experiments suggested that the contribution of chemoreception to prestrike behavior increased with prolonged food deprivation. The most effective strike-releasing conditions were struck more quickly and after fewer tongue flicks than less effective conditions, but tongue flick rates (recorded only in experiment 2) did not differ between conditions. Increased length of food deprivation appeared to decrease the latency to strike. Most models were struck in anterior regions, which suggested that directional movement contributed to the strike aim. The proportion of models envenomated during the strike differed between two model conditions, implying that rattlesnakes possess control over the mechanics of venom in-

Odorized air current trailing by garter snakes, Thamnophis sirtalis.

The response of adult red-sided garter snakes, Thamnophis sirtalis parietalis, to airborne odor trails was studied. An airtight T-maze was used, through which a constant airflow was drawn by a vacuum pump. The arms of the 'T' provided a choice between earthworm extract and distilled water. Experiment 1 tested the snake's responses to varying concentrations of earthworm extract. Snakes accurately trailed the extract at tested concentrations (0.0, 0.01, 0.1, 1, 10, 100%). At ten percent concentration, tongue-flick rate and speed along the maze increased significantly above lower levels, suggesting the existence of a threshold concentration. A correlation between mean tongue-flick rate and mean speed was demonstrated. Experiment 2 tested the effect of differentially blocked vomeronasal ducts on a snake's ability to trail. When both ducts were blocked, no trailing was observed, suggesting that vomeronasal stimulation is required. Blocking a single duct resulted in a significant number of snakes turning to the side of the functioning duct, suggesting that the tongue-vomeronasal system may function as a chemotaxic system.

Prairie Rattlesnakes <i>(Crotalus viridis) </i>Respond to Rodent Blood with Chemosensory Searching

In Experiment I, homogenized rodent tissue was applied to the lips of prairie rattlesnakes (Crotalus viridis). This treatment produced elevated rates of tongue flicking compared to controls that received water, but the elevations seen following stimulation with homogenate were not as large as those seen after snakes struck prey. In Experiment II, water, rodent blood, and integumentary cues were applied to the lips of rattlesnakes, and only blood resulted in elevated rates of tongue flicking. We conclude that blood is a critical component of the homogenate. It is hypothesized that detection of blood during predatory strikes may be a causal element in the triggering of strike-induced chemosensory searching, a typical component of rattlesnake predatory behavior.

Elevation in tongue-flick rate after biting prey in the broad-headed skink,Eumeces laticeps

A postbite elevation in tongue-flicking (PETF) rate occurs in adult male broad-headed skinks,Eumeces laticeps. Males having bitten neonatal mice showed significantly higher tongue-flicking rates in the 2 min following experimental removal of the prey than did males in several control conditions. In a second experiment designed to separate the effects of tactile and chemical stimulation of the oral cavity during biting, males tongue-flicked at significantly higher rates in response to swabs bearing surface chemicals from neonatal mice than to identical swabs lacking the surface chemicals. These findings agree with previous data showing that PETF and searching movements occur in those families of lizards that can detect prey chemicals and use the tongue to do so during active foraging. The occurrence of PETF and putative searching movements supports the interpretation that PETF represents an attempt to relocate lost prey by chemosensory means. PETF was much briefer inE. laticeps than in many snakes and in a representative species from another lizard family and was not detectable after the first minute. This brevity is consistent with the prediction that PETF should be brief in squamates that feed on prey not likely to be located by scent-trailing.

The role of chemosensory cues in discrimination of prey odors by the amphisbaenianBlanus cinereus

Responses of amphisbaenians (Blanus cinereus) to deionized water, a control for pungency (cologne), and integumental prey odors (coleopteran larvae and adult ants) on cotton swabs were studied in experiments with a randomized blocks design to discover whether amphisbaenians use chemical cues to detect and identify prey. No individual bit the applicators. Amphisbaenians tongue-flicked at lower rates than epigean saurians, which are active foragers. Tongue-flick rate differed among treatments, but responses to prey odors were not significantly different from those to cologne. The number of directed tongue-flicks emitted during the 60-sec trials was, however, lower in response to deionized water than in response to cologne or prey odors. Response details, the low rate of tongue-flick, and absence of biting are discussed in relation to the foraging behavior and fossoriality of amphisbaenians. Evidence from this study indicates that the vomeronasal sense is used by amphisbaenians to identify odors, but our experiments failed to demonstrate that amphisbaenians discriminate between prey and nonprey odors.

Discrimination of integumentary prey chemicals and strike-induced chemosensory searching in the ball python,Python regius

Experimental tests show that the ball python (Python regius) has the ability to discriminate prey chemicals from control substances by tongue-flicking and exhibits a poststrike elevation in tongue-flicking rate (PETF). Prey chemical discrimination was revealed by significantly higher number of tongue-flicks and tongue-flick attack score in response to integumental chemicals from mice than to cologne or distilled water and by a higher frequency of biting in response to prey than control chemicals. PETF was indicated by higher tongue-flicking rates after biting than in several control conditions. Concurrent movements of the body suggest the operation of strike-induced chemosensory searching (SICS). Ecological factors affecting responses to prey chemicals, including defensive behaviors and characteristics of foraging behavior related to reliance on different sensory modalities, are discussed. The presence of PETF and SICS in a henophidian snake and in scleroglossan lizards suggests that these behaviors are plesiomorphic in snakes.

Responses to prey chemicals by a lacertid lizard,Podarcis muralis: Prey chemical discrimination and poststrike elevation in tongue-flick rate

The ability to discriminate prey chemicals from control substances and the presence of a poststrike elevation in tongue-flicking (PETF) rate are experimentally demonstrated in the lacertid lizard,Podarcis muralis, The tongue-flick attack score, a composite index of response strength, was significantly higher in response to integumental chemicals from cricket than to cologne or distilled water. The cricket chemicals additionally elicited a significantly greater rate of tongue-flicking and higher proportion of attacks by the lizards than did control stimuli. PETF combined with apparent searching movements strongly suggest the presence of strike-induced chemosensory searching (SICS). Experimental evidence indicates that both PETF and SICS occur in insectivorous representatives of three families of actively foraging autarchoglossan lizards, suggesting their widespread occurrence in such lizards. The adaptive roles of chemosensory behavior in the foraging behavior of P.Muralis are discussed. It is proposed that these lizards may form chemical search images and that PETF and SICS may have been present in the lacertilian ancestors of snakes.

Strike-induced chemosensory searching in venomoid pit vipers at Hogle Zoo

Six pit vipers with ligated and severed venom ducts were each observed twice. In the no-strike trial a rodent was presented for 3 sec but held (on tongs) out of striking range. The strike trial began with a 3 sec presentation, but the prey item was then moved into striking range, and all snakes immediately struck and released the rodents. Prey were removed after no-strike and strike presentations and the rate of tongue flicking was recorded for 30 min. Only strike presentations were followed by high rates of tongue flicking, which were indistinguishable from those seen in pit vipers with functioning venom apparatus. We conclude that venom injection is irrelevant for the causation of strike-induced chemosensory searching.

Responses of the lizard Lacerta vivipara to predator chemical cues: the effects of temperature

The thermal dependence of chemoreceptive and behavioural responses of the lizard Lacerta vivipara to chemical cues of the predatory snake Vipera berus were studied. The lizards were observed in cages that had previously been inhabited by a viper and their behaviour was compared with that of lizards in unfamiliar, but clean cages. The lizards' body temperatures were controlled by placing the cages in environmental chambers. Although tongue-flick rates were clearly temperature-dependent, snake chemicals elicited increased tongue-flick rates at all temperatures (20–35°C). Body temperature therefore seems to influence the intensity of chemosensory examination, but does not seem to affect its function within the temperature range considered. Snake chemical cues also induced a shift in general behaviour of the lizards. When confronted with the stimuli, they changed their normal behaviour (an alternation of activity bouts and basking) towards long periods of immobility, interrupted by jerky, hesitant walks. The effects of temperature on this reaction primarily concerned thermoregulatory behaviour: in the control experiments, basking was prolonged at low temperatures whereas in the viper experiments, it lasted longer at high temperatures.

Roles of vomeronasal organ chemoreception in tongue flicking, exploratory and feeding behaviour of the lizard, Chalcides ocellatus

A correlation between elevated tongue flick rate and vomeronasal organ use has frequently formed the basis for studies of lizard chemosensory behaviour, although this hypothesis has not been tested directly. The relationship between vomeronasal organ use and tongue flick rate was investigated by testing ocellated skinks, Chalcides ocellatus, with normal or sealed vomeronasal ducts (which prevents chemical access to the vomeronasal organ) in a novel environment, and in their home boxes. Lizards with normal vomeronasal organs exhibited higher tongue flick rates in novel environments than in their home boxes. Lizards with sealed vomeronasal ducts exhibited significantly lower tongue flick rates than did lizards with normal vomeronasal organs, and did not demonstrate elevated tongue flick rates relative to home box levels in response to the novel environment. Therefore, elevation of tongue flick rates in response to environmental stimuli appears to be dependent on a functional vomeronasal organ. However, sealing the vomeronasal ducts did not prevent an increase in movement in novel environments relative to home boxes indicating that detection of novel stimuli and resulting exploratory behaviour do not require a functional vomeronasal organ. Prey consumption, but not prey attack, was severely impaired in lizards with sealed vomeronasal ducts, suggesting that vomeronasal system identification of objects that are attacked is important for completion of predatory sequences.

A comparative analysis of scoring methods for chemical discrimination of prey by squamate reptiles

In studies of squamate responses to prey chemicals presented on cotton-tipped applicators, investigators typically record several responses, each of which gives only part of the overall picture. The tongue-flick/attack score (TFAS) is a widely used composite measure of response strength that accounts for attack, its latency, and number of tongue-flicks. We present data and analyses on these variables and investigate the utility of several other possible response variables. It is concluded, for both practical and theoretical reasons, that TFAS and two modifications of it are the best measures of response strength. Uses and statistical analyses of TFAS and variables derived from it are discussed. It is recommended that information on tongue-flick rate, number of individuals attacking, and latency to attack be presented.

Bushmaster (Lachesis muta) predatory behavior at Dallas Zoo and San Diego Zoo

Bushmasters (Lachesis muta) that were observed during feeding episodes occasionally released rodents after the predatory strike. For one such episode, we report the presence of a sustained, high rate of tongue-flicking that lasted 136 min. In this paper, we also present photographs showing skin folds that cover the snake’s pits and eyes when a rodent prey was being held following the predatory strike. We suggest that L. muta may occasionally exhibit strike-induced chemosensory searching and trail-following when large (but ingestible) prey are encountered.