Kent M. Scudder

Analysis of the behavioral sequence emitted by rattlesnakes during feeding episodes: I. Striking and chemosensory searching

Rattlesnakes exhibited an elevated rate of tongue flicking after striking a mouse. This chemosensory searching process probably aids the snake in locating its dead or dying prey when movement cues are no longer produced. Seeing, smelling, and detecting thermal cues arising from a live mouse were not sufficient to produce the increase in the tongue-flick rate; the mouse must be struck. After striking a mouse, rattlesnakes also showed some degree of inhibition against striking a second mouse for as long as 20 min. Hence, “switching on” the chemosensory searching process involves “switching off” (at least partially) the striking system.

Strike-Induced Chemosensory Searching by Rattlesnakes: The Role of Envenomation-Related Chemical Cues in the Post-Strike Environment

Rattlesnakes and many other viperids typically strike and release adult rodent prey (Gans, 1966; O’Connell et al., 1982; Radcliffe et al., 1980), allowing the envenomated rodent to wander up to 600 cm before succumbing to the venom (Estep et al., 1981). The snakes then follow the chemical trail left by the envenomated prey. Although this predatory strategy risks losing the prey, it avoids tissue damage that could result from rodent teeth and claws if the snake attempted to hold the struggling prey after the strike. Even some of the deadliest elapids exhibit this strategy when they prey upon rodents (Chiszar et al., under review; Radcliffe et al., 1982; Shine & Covacevich, 1982), indicating that rodents are formidable prey and that the strike-release-trail system probably appeared very early in the evolution of venomous snakes (see Marx & Rabb, 1965, for a discussion of viperid evolution).

Chemosensory Searching by Rattlesnakes During Predatory Episodes

Striking rodent prey is a prerequisite for chemosensory searching (prey trailing using the tongue — Jacobson’s organ system) in rattlesnakes. High tongue flick rates occur after striking prey but not after seeing, smelling or detecting thermal cues arising from a rodent. At least two consequences of striking appear to be involved in the activation of chemosensory searching: (1) proprioception arising from the biomechanical aspects of the strike, and (2) chemical input to the vomeronasal organs concomitant with the strike. These two effects seem to be additive.

Rattlesnake predatory behaviour: mediation of prey discrimination and release of swallowing by cues arising from envenomated mice.

Abstract Responses of rattlesnakes to envenomated mice were examined in five experiments. In experiment 1 rattlesnakes ( Crotalus durissus terrificus and C. viridis viridis ) discriminated mice that they had envenomated, as indexed by number of tongue flicks and accumulated investigation time, when these prey items were paired with control mice killed by the experimenter. Experiment 2 demonstrated that rattlesnakes also exhibited this discrimination when presented with mice envenomated by a conspecific and controls killed by the experimenter. In experiments 1 and 2, we observed that rattlesnakes delivered a large number of tongue flicks to exudates associated with nasal-oral tissues of envenomated mice. It has commonly been noted that rattlesnakes typically swallow envenomated, dead mice head first. In experiment 3 this observation was statistically verified. Evidence obtained in experiment 4 indicated that nasal-oral tissues of envenomated, dead mice were discriminated from anogenital tissues by rattlesnakes. Cues arising from the nasal-oral tissues probably (1) assisted the snakes in locating the head-end of the rodent, and (2) released the swallowing modal-action pattern, the final phase of the predatory sequence. In experiment 5, rattlesnakes exhibited no discrimination between nasal-oral and anogenital tissues of non-envenomated, dead mice, indicating that the results of experiment 4 were probably dependent upon effects of envenomation.

Rate of tongue flicking by garter snakes (Thamnophis radix haydeni) and rattlesnakes (Crotalus v. viridis, Sistrurus catenatus tergeminus, and Sistrurus catenatus edwardsi) during prolonged exposure to food odors.

Garter snakes (Thamnophis radix haydeni) emitted more tongue flicks in environments containing fish or salamander odors than in a control environment. This indicates that appetitive searching (guided by the vomero-nasal system) can be activated by olfactory cues. Specimens of three taxa of rattlesnakes (Crotalus viridis viridis, Sistrurus catenatus tergeminus, and Sistrurus catenatus edwardsi) did not emit more tongue flicks in an environment containing mouse odors than in a control environment. Hence, the vomeronasal systems of these rattlesnakes were not activated by olfactory cues. A hypothesis is offered about the conditions required to stimulate tongue flicking in rattlesnakes.

Investigatory behavior in snakes, II: Cage cleaning and the induction of defecation in snakes

In Experiment 1, boid and colubrid snakes defecated with shorter latencies after their home cages were cleaned than did control snakes that received equivalent handling without cage cleaning. Experiment 2 replicated this finding and also showed that snakes exposed to clean cages emit more tongue flicks after reintroduction to the clean home cage than do control snakes. Experiment 3 demonstrated that cage cleaning has similar effects in two species of crotalid snakes. The increase in tongue flicking after cage cleaning is interpreted as investigatory behavior and reflects the fact that snakes respond to the absence of familiar odors. Experiment 4 showed that a clean cage containing odors derived from snake feces produces less tone-flick exploration and fewer defecation responses in rattlesnakes than does a clean cage without such odors.

Effects of six visual stimulus conditions on defensive and exploratory behavior in two species of rattlesnakes.

Presentation of faces of living animals (dog, human) and nonliving models (coyote, mink) to prairie rattlesnakes, Crotalus viridis viridis, and Western Massasauga rattlesnakes, Sistrurus catenatus tergeminus, for 10-sec. intervals of visual inspection established that movement is the primary component in eliciting defensive and exploratory responses. These snakes probably are not sensitive to any particular static conformational features of the faces of canids or mustelids, indicating the incorrectness of an initial working hypothesis that such features are releasers of defensive behavior. Since small moving objects tend to release predatory attack behavior while large moving objects release defensive behavior, we offer the hypothesis that a movement-size feature detection system mediates these visually guided behaviors.

Simultaneous and successive discriminations between envenomated and nonenvenomated mice by rattlesnakes (Crotalus durissus and C. viridis)

Rattlesnakes of two species (Crotalus durissus and C. viridis) discriminated between envenomated and nonenvenomated mice when the two kinds of mice were presented in simultaneous discrimination tests. The snakes spent more time investigating the former mouse, and they selected it more frequently than the latter. The present study showed that the ability of these rattlesnakes to make this discrimination did not change when the two stimulus items were presented successively (1 week apart). Accordingly, the discrimination is not based on a contrast effect requiring direct comparison of the two stimulus mice. It is proposed that rattlesnakes possess an internal representation of an envenomated mouse which guides searching and choice behavior.

Exploratory Behavior in Prairie Rattlesnakes ( Crotalus Viridis ) and Water Moccasins ( Agkistrodon Piscivorus )

Six prairie rattlesnakes (Crotalus viridis) and six water moccasins (Agkistrodon piscivorus) were observed for 10 min. under each of four conditions: (a) home cage after brief handling, (b) a cage formerly occupied by a hognose snake (Heterodon nasicus; harmless to both rattlesnakes and moccasins), (c) a cage formerly occupied by a kingsnake (Lampropeltis getulus; a predator of both rattlesnakes and moccasins), and (d) a clean open field. The latter three conditions were novel environments for the subjects. The dependent variable was the number of tongue flicks emitted per min. Tongue-flick rates were greatest in the open field and hognose snake cage and lowest in the home cage, indicating that more tongue flicking occurs in the harmless novel environments than can be explained solely on the basis of handling. This difference provides an operational definition of exploratory behavior. The kingsnake cage generated a rate of tongue flicking which was higher than that seen in the home cage but lower than the rates seen in the open field and hognose snake cage, indicating that odors of this predator inhibit exploration by potential prey. The inhibitory effect was stronger in water moccasins than in rattlesnakes.

Paternal urine elicits increased maternal care in grasshopper mice

Southern grasshopper mice, Onychomys torridus, exhibit monogamous pair bonding. Both mother and father display high levels of parental care of their offspring. Based upon earlier work (Schultz, N. J. (1979) . Paternal role and behavior of the southern grasshopper mouse, Onychomys torridus. Doctoral thesis, The Johns Hopkins University), if the male of a pair is removed from the female and their litter, maternal pup licking, an important parental care action, declines. However, if isolated mothers with pups are exposed to urine samples collected from their respective mates, maternal pup licking increases significantly. The effect does not appear for a few days, but then increases rapidly and significantly. Apparently, paternal urine contains a chemical cue that increases levels of adaptive maternal care toward young.