Development of antipredator responses in snakes: II. Effects of recent feeding on defensive behaviors of juvenile garter snakes (Thamnophis sirtalis).

The effect of having eaten a large meal (50% of body weight) on the defensive behavior of juvenile garter snakes (Thamnophis sirtalis) was investigated. Twenty-five 10-wk-old snakes were tested for antipredator responses (strikes) directed toward a threatening stimulus (moving and nonmoving human hand) before and after having eaten a large worm segment. Snakes directed significantly (p?     

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 airbome 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 airbome 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 airbome odorants are detected by the main MO system and that such detection does not require a functional VN system. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Roles of the vomeronasal and olfactory systems in courtship behavior of male garter snakes.

Studied whether male garter snakes required intact vomeronasal or olfactory systems to detect the pheromone that triggers the chin-pressing behavior of courtship. Male garter snakes with testosterone propionate pellets implanted sc were tested for courtship displays with estradiol-benzoate-treated females. Three groups of 10 males were formed from snakes exhibiting strong courtship responses. Bilateral olfactory nerve cuts were attempted on 1 group, vomeronasal nerve cuts on a 2nd, and control surgeries on a 3rd. All snakes in the olfactory nerve cut and control groups courted after surgery, and 3 snakes in each group copulated. More than half of the snakes in the olfactory nerve cut group had complete nerve cuts. Nine of the 10 snakes in the vomeronasal nerve cut group exhibited no courtship responses after surgery. The 1 snake in this group that courted was the only snake in which intact vomeronasal nerve fascicles were observed. Data indicate that male garter snakes without functional olfactory systems do court and mate normally, but that male garter snakes without functional vomeronasal systems exhibit no courtship responses. (38 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Temperature activation of courtship behavior in the male red-sided garter snake (Thamnophis sirtalis parietalis): Role of the anterior hypothalamus-preoptic area.

Adult male red-sided garter snakes (Thamnophis sirtalis parietalis) received radio-frequency lesions prior to 17 weeks of low-temperature hibernation. Animals found to have bilateral lesions of the anterior hypothalamus-preoptic area ({ah-poa}) failed to exhibit courtship behavior on emergence from hibernation. Those individuals in which the major portion of the destruction was centered in the anterior POA also exhibited deficits in thermoregulatory behavior. Animals that received unilateral lesions of the {ah-poa} initiated courtship behavior after controls and had an abbreviated period of courtship; these animals exhibited normal responses to thermal stimuli. Male snakes with lesions outside the {ah-poa} courted normally and demonstrated no differences in thermoregulatory behavior compared with the surgical controls. These results indicate that in male red-sided garter snakes, an intact {ah-poa} is critical for the integration of thermal stimuli that activate seasonal courtship behavior. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Signal processing in the vomeronasal system: modulation of sexual behavior in the female rat

Chemosensory cues detected by the vomeronasal (VN) organ modulate a variety of social interactions in many species. In particular, activation of the VN system by pheromones regulates sexual behavior in the rodent. Although the exact nature of stimulus access to the organ is not clearly defined, the neuroanatomical pathway connecting the VN organ to hypothalamic centers controlling reproductive function is well established and relatively straightforward. Electrophysiological techniques have provided insight into the signal transduction process throughout the VN system. Combining behavioral studies with immunocytochemical detection of immediate early genes and neuropeptides reveals that gonadotropin hormone releasing hormone (GnRH)-containing neurons are specifically activated by stimulation of the VN organ. Furthermore, some of the activated GnRH neurons project to the ventromedial hypothalamus where they are hypothesized to induce sexual responsiveness. Early anecdotal evidence of an influence of the VN organ on human reproductive events has been substantiated by more recent anatomical, behavioral, and electrophysiological studies. Thus, further deciphering of the signal transduction process within the VN system of the rodent may yield unique insights into behaviors associated with human reproduction.     

Role of the anterior hypothalamus–preoptic area in the regulation of courtship behavior in the male Canadian red-sided garter snake (Thamnophis sirtalis parietalis): Lesion experiments.

Lesions of the medial preoptic area and/or the ventromedial hypothalamus resulted in an abrupt and immediate decline in courtship behavior in 28 male Canadian red-sided garter snakes. Lesions of the more anterior portions of the preoptic area resulted in a more gradual, delayed decline in courtship behavior. Ss sustaining lesions dorsal, ventral, or caudal to the anterior hypothalamus–preoptic area (AH–POA) exhibited no change in courtship behavior relative to controls. Measurements of testis size, spermatogenic stage, and circulation levels of androgens revealed no differences between any of the groups. There were marked differences in the change in hematocrit over time between the groups. Results indicate that the AH–POA is involved in the control of courtship behavior in the adult male red-sided garter snake. Moreover, it is suggested that the stimulus affecting the AH–POA to activate courtship is temperature-related. (32 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Stimulus control of lingual predatory luring and related foraging tactics of mangrove saltmarsh snakes (nerodia clarkii compressicauda).

Knowledge of the various cues that elicit natural behavior is important to our understanding of why and when animals behave as they do. In order to gain insight into the behavior and ecology of Nerodia clarkii compressicauda, a piscivorous snake that uses a unique form of predatory luring as a foraging tactic, we observed 22 juvenile subjects in the presence of visual and chemical prey stimuli in a repeated-measures design. The use of video playback as a visual stimulus in this experiment permitted complete isolation from tactile and chemical cues. Snakes were more sedentary and used lingual luring more when both cue types were present than when none or only one of the cues was available. Subjects also attacked more often in the presence of both stimuli. Predatory attacks by prey-na?ve subjects directed to video cues when only visual prey stimuli were available demonstrated that snakes can identify prey visually without prior experience. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Species and sex differences in substrate preference and tongue flick rate in three sympatric species of water snakes (Nerodia).

Tested isolation-reared sympatric water snakes (Nerodia r. rhombifera, N. c. cyclopion, and N. fasciata confluens) in a balanced 2-choice design to determine preference between clean and same-sex conspecific-soiled gravel substrates. Ss included 8 snakes (4 of each sex) of each species. Time spent on each substrate, types of tongue flicking behavior, tail vibration, defecation, and head rubbing were recorded. Species and sex differences were found in the relative time spent on the 2 substrates. Both sexes of N. rhombifera preferred the clean substrate, whereas both sexes of N. cyclopion preferred the soiled substrate, although the difference in time spent on the substrates was small for males. N. fasciata sexes differed in their preference, with the females preferring the soiled substrate and the males preferring, but not so strongly, the clean substrate. The frequencies of the 4 types of tongue extensions differed across species and sexes, with "air" tongue flicks accounting for the most variance. A lower total rate of tongue flicking occurred when the snakes were on the preferred substrate. These species and sex differences may help minimize competition due to dietary overlap between N. rhombifera and N. cyclopion, and between male and female N. fasciata. (33 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Strike-induced chemosensory searching by ingestively naive garter snakes (Thamnophis sirtalis).

Neonatal, previously unfed garter snakes exposed to aqueous chemical cues from earthworms tongue flicked at higher rates during the 5 min after withdrawal of the stimulus than after aqueous control trials. If snakes struck at but did not touch the worm stimulus, they showed a much greater increase over control trials in postexposure tongue flicking than when they did not strike, and the increased rate persisted longer. These results demonstrate strike-induced chemosensory searching (SICS) by ingestively naive snakes. It is highly probable that other squamate reptiles show a similar well-integrated suite of sequential foraging behaviors at birth or hatching. Differences among species in SICS may be related to details of sequential prey capture tactics in reconstruction of phylogenetic patterns. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Garter snake trailing behavior: Effects of varying prey-extract concentration and mode of prey-extract presentation.

In a multiple-choice maze, garter snakes were trained to follow earthworm-extract trails for worm bit rewards. Ss were juvenile and adult garter snakes of both sexes of the species Thamnophis sirtalis sirtalis and Thamnophis radix. In Exp I, Ss were tested for their abilities to follow extract trails that had been dried or extract trails that were removed from direct lingual access by a perforated floor. Ss were able to follow the dry trails and unable to follow removed trails. In Exp II, Ss were tested for their behavioral responses to different concentrations of extract trails. Ss trailed more accurately, moved more slowly, and exhibited much higher tongue flick rates on the intense concentration trails. Results are interpreted in terms of the assumption that effective trails are perceived by the tongue flick delivery of odorants to the vomeronasal organs. (37 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Plasticity of foraging behavior in garter snakes (Thamnophis sirtalis) reared on different diets.

The ontogeny of foraging was studied in 107 neonatal garter snakes (Thamnophis sirtalis) reared on 3 different diets: fish, leafworms, or mixed. Times to approach, capture, handle, and swallow prey were measured during each snake's first feeding and again after 11 to 12 meals. Overall times to consume prey decreased between the first and last tests for the 3 groups, but both prey type and the relative amounts of prey consumed differentially affected the various feeding phases. Approach latencies significantly decreased for snakes fed worms or fish exclusively but not for the mixed-diet snakes. The degrees to which capturing and swallowing latencies decreased differed among diet groups. Diet had little effect on prey handling duration. Sex and litter effects were reduced after feeding experience. These results reveal flexibility in feeding behavior as well as the costs and benefits of experience with multiple prey classes. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Death feigning by grass snakes (Natrix natrix) in response to handling by human "predators."

Death feigning, a variant of tonic immobility, is usually interpreted as a last-resort antipredator measure. The authors describe death feigning in grass snakes (Natrix natrix) and test some of its potential correlates. Death feigning was seen in 66% of wild-caught snakes but was not seen in hatchlings from laboratory-incubated eggs. Minimal indication of death feigning was mouth gaping, often with the tongue hanging free, but more dramatic cases involved voluntary supination and/or lack of muscle tone. Aside from hatchlings, which did not feign death, there was little variation in frequency or intensity of death feigning with body size. There was no effect of body temperature on death feigning nor were snakes that were moving when caught less likely to feign death than those that were not moving. Interpretation of the adaptive value of death feigning in grass snakes or in other animals is hampered by lack of evidence of this behavior in the field in response to natural predators. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Laboratory observations of aggregative behavior of garter snakes, Thamnophis sirtalis: Roles of the visual, olfactory, and vomeronasal senses.

Two experiments determined (a) whether male garter snakes require a functional vomeronasal or olfactory system to return to previously preferred shelter locations and (b) the sensory modalities used to aggregate in the absence of previously deposited chemical cues. In Exp I, 22 male garter snakes with vomeronasal nerve lesions did not return to previously preferred shelter locations when tested individually. However, when tested with a group that included 9 control Ss, they returned to previously preferred shelters. The shelter-selection behavior of Ss with olfactory nerve lesions improved postoperatively, whereas the behavior of Ss with sham lesions was unchanged. In Exp II, 32 Ss were tested for aggregation in aquaria in which the substrate and other contents were cleaned between trials. After blindfolding or olfactory nerve cuts, Ss aggregated at normal levels. When Ss' vomeronasal ducts were sutured closed, aggregation scores were significantly depressed, although 2 of the 3 groups with vomeronasal duct sutures did aggregate just above change levels. Results from both studies indicate that use of chemical signals by garter snakes in shelter selection and aggregation is mediated by the vomeronasal system and that neither the olfactory nor the visual system is critical for these behaviors. (30 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The forked tongue and edge detection in snakes (Crotalus oreganus): An experimental test.

Many stimulus-detection systems are lateralized to allow for simultaneous comparison of paired stimuli. It has been hypothesized that the deeply forked tongue of snakes and some derived lizards functions as a chemical edge detector where cues gathered by each tine are kept separate to provide two points of lateral odor assessment by the central nervous system via vomeronasal input. While following a chemical trail, one time can be on the trail, the other off, and such differential information prompts the snake to turn back to the trail. The authors tested this hypothesis in rattlesnakes within a predatory context by unilaterally severing the vomeronasal nerves. If edge detection is used by snakes during prey trailing, then unilateral denervation should disrupt trailing ability. The authors found no change in the seven separate trailing parameters measured. Therefore, they found no support for the edge detection hypothesis as it applies to prey trailing behavior. Instead, the deeply forked tongue may represent a chemosensory specialization to increase odor-sampling area, with snakes and derived lizards detecting only the concentration of chemical trails. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

A brief commentary on the usefulness of studying fears of snakes.

Used therapy analogue studies with Ss who feared snakes or rats to evaluate types of behavior therapy. In a small pilot study Es were able to desensitize 4 Ss to fears of snakes or laboratory rats. However, the 2 control Ss also overcame their fears of snakes. They had been instructed to hold the snake when it was presented to them and to act unafraid. They were also told that they would overcome their fears in this manner. It is suggested that any "technique" that helps a person confront the fear of snakes may "cure" him, that studying the treatment of snake fears may be irrelevant to the understanding of treating clinical neuroses. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Tongue flicking in agamid lizards: morphology, kinematics, and muscle activity patterns

We wanted to examine whether a relation between foraging strategy, morphology, the mechanics of tongue protrusion, and prey chemical detection and discrimination exists in agamid lizards. Tongue-flick behavior was observed in two species of this family: Uromastix acanthinurus and Plocederma stellio. Potential prey chemical discrimination by means of tongue flicking was examined by using applicator tests. Tongue flicks were subsequently recorded by high-speed video in combination with the electrical activity of a number of jaw and hyolingual muscles. The kinematics of jaws and tongue and the muscle activity patterns were quantified. To investigate if the observed differences in tongue-flick behavior (mainly in the frequency of use) are translated into corresponding differences in tongue morphology, the tongues of both species were examined by light and scanning electron microscopy. The species differed mainly in the surface morphology of the foretongue and in the abundance and distribution of taste buds on the tongue and oral cavity. These differences can be related to behavioural observations; whereas U. acanthinurus readily uses tongue flicks to detect and discriminate between food items, P. stellio does not. However, differences in tongue-flick mechanics (kinematics, electromyograms) between both species were minor. Based on the data gathered in this study and from previously published data, an evolutionary transformation series leading to the complex tongue-flick cycles as observed in snakes is proposed. The required morphological and mechanical changes that accompany such an evolutionary sequence are discussed.     

Development of antipredator responses in snakes: I. Defensive and open-field behaviors in newborns and adults of three species of garter snakes (Thamnophis melanogaster, T. sirtalis, T. butleri).

A comparative study of defensive behavior in multiple litters of newborn garter snakes and adult female garter snakes from 3 species was conducted in the laboratory. In Exp I, 241 1-day-old Ss, roughly equally divided among the 3 species, were tested for defensive behaviors directed toward a moving or nonmoving stimulus. T. melanogaster babies were the most reactive in terms of strikes, bites, and defensive tongue flicks. T. sirtalis and T. butleri were less reactive and not significantly different from each other. In Exp II, 32 adult females reacted in ways similar to the neonates, except that the T. sirtalis females were more reactive toward the moving stimulus than were the T. butleri females. Exp III showed large and significant differences in open-field behavior among the newborn of the 3 species but few significant correlations between open-field measures and antipredator responses. (19 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Stimulus control of defensive behaviors of garter snakes (Thamnophis sirtalis): Effects of eye spots and movement.

The purpose of these experiments was to examine the effects of eye spots and stimulus movement as mediators of antipredator responses in garter snakes. In Experiment 1, 13 Eastern garter snakes (Thamnophis sirtalis) at 6–8 weeks of age were confronted with a series of threatening models that varied in the configuration of the eyes (artificial glass eyes, circular black spots, elongated black bars, or no eyespots). There were significant differences in the number of strikes elicited by the models, and the model with realistic glass eyes elicited the most strikes. In Experiment 2, we examined the effects of erratic and consistent stimulus movement on defensive behavior in 12 garter snakes at 12–26 weeks of age. The snakes delivered significantly more strikes to an erratically moving model than to a model oscillated at a regular rate. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Trailing behavior in banded rock rattlesnakes (Crotalus lepidus klauberi) and prairie rattlesnakes (C. viridis viridis).

Two rattlesnake taxa were compared in a task requiring 12 banded rock rattlesnakes to follow rodent trails. All Ss were wild-caught adults and had been in captivity feeding exclusively on rodents for 2 yrs prior to the present study. Banded rock rattlesnakes are primarily lizard eaters in nature but readily accept rodent prey in captivity. Prairie rattlesnakes are rodent specialists. Snakes of both taxa strike from ambush and typically hold lizards following envenomation, whereas rodents are released and allowed to wander freely while venom takes effect. Rodent carcasses are then located through chemoreception. Results show that the taxa exhibited some similar responses in the rodent trailing task, but C. l. klauberi had scores significantly inferior to those of C. v. viridis on several dependent variables (percent of tongue flicks and time on trail). It is suggested that greater dependence of C. v. viridis on rodents has brought about more effective trailing behavior than is seen in C. l. klauberi. Although it is possible that genetic differences are responsible for these behavioral differences, an alternative argument on the basis of differential early ontogeny cannot be eliminated. (23 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Manipulation of avoidance behavior as a function of increased or decreased demand on repeated behavioral tests.

5 groups of 15 female undergraduates reporting fear of snakes participated in 2 behavioral avoidance tests employing a snake as the target object. 4 groups were first tested under low demand for approach and then under the same conditions or under 1 of 3 conditions of demand increase, mediated by instructions, mode of administration, or both. The 5th group was tested under high, then low demand. Ss first tested under low demand showed significantly more fear than those first tested under high demand. In addition, Ss in the demand-increase groups showed significant increases in approach at the 2nd behavior avoidance test, while Ss in the demand-decrease group showed a significant reduction in approach. Ss in the repeated-measure control group showed no significant changes. (16 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)