David Chiszar

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.

HABITAT SELECTION AND PREY ODOR IN THE FORAGING BEHAVIOR OF WESTERN RATTLESNAKES (CROTALUS VIRIDIS)

We tested the roles of prey odor and other habitat cues in the pre-strike movement patterns of two, ecologically distinct sub-species of the western rattlesnake in naturalistic arenas. In the first experiment, rattlesnakes preferred habitat containing prey odor and cover comprised of rocks, sticks and plants. While searching, rattlesnakes methodically investigated the edges and crevices within rock, areas rodents might frequent in nature. In the second experiment, rattlesnakes investigated sticks more than rocks arranged topographically similar to sticks. In the third experiment, rattlesnakes preferred habitat that included brush foliage and used chemical prey trails in pre-strike behavior via (i) trail-following, (ii) casting search patterns and (iii) scanning search patterns. Several snakes coiled in stereotyped ambush postures that allowed them to face chemical trails while resting against rocks and foliage. These results suggest that rattlesnake foraging exhibits qualities advantageous for hunting rodent prey in addition to providing protection from predators and perhaps promoting thermoregulation. Sub-species did not exhibit geographic variation in foraging behavior despite differences in natural history and morphology. Hence, the microevolutionary pattern suggests that generalized foraging repertoires are successful in numerous environments when coupled with locally specialized body patterns.

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.

Effects of Chemical and Visual Stimuli Upon Chemosensory Searching by Garter Snakes and Rattlesnakes

Many studies indicate that chemical cues activate garter snake feeding behavior whereas visual and/or thermal stimuli do so for rattlesnakes. However, no experiments have factorially combined chemical and visual cues for either of these taxa. The present work explored possible interactive effects of these stimuli on rate of tongue flicking (RTF) in garter snakes (Thamnophis radix haydeni) and rattlesnakes (Crotalus e. enyo, C. v. viridis, and Sistrurus catenatus tergeminus). In Experiments 1 and 2 snakes were exposed to four conditions represent- ing an orthogonal combination of presence vs. absence of visual and chemical stimuli arising from prey. RTF was recorded for 5 min under each condition. Garter snakes exhibited a significant elevation in RTF in the presence of chemical cues whether or not visual cues were present. There was also an effect of visual cues but no interaction between visual and chemical cues. Rattlesnakes did not respond to chemical cues; these snakes showed only an effect of visual cues. In Experiment 3, rattlesnakes were again observed as above, with the exception that test sessions were of 10 min duration. Behavior during the first 5 min was identical to that seen in Experiment 2, but during min 6-10 the snakes responded more in the condition containing visual plus chemical cues than in any other condition. Visual stimuli alerted rattlesnakes to the presence of potential prey and gave rise to elevated RTF which subsequently allowed these predators to utilize chemical cues that happened to be available. Hence, garter snakes and rattlesnakes use both chemical and visual information but differ in the sequence in which these stimuli are used.

Trailing Behavior in Prairie Rattlesnakes (Crotalus viridis)

Six rattlesnakes (Crotalus v. viridis) were observed in four experimental conditions designed to assess ability to follow odoriferous mouse trails. If snakes had not struck mice just prior to being exposed to the trails, then no trailing behavior was observed, whereas trails were followed with precision if the snakes struck mice prior to the tests. Striking led to pronounced elevations in rate of tongue flicking, and the magnitude of this effect did not depend upon presence vs absence of mouse trails in the post-strike environment. However, when a trail was present, the high rate of tongue flicking facilitated locating the trail and following it to the mouse carcass positioned at its end. Once a trail was located, the snake confined its head to within 2 cm of the odoriferous cues, and 75% of the tongue flicks were directed to the trail.

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.

Chemical cues used by prairie rattlesnakes (Crotalus viridis) to follow trails of rodent prey

Each of 10 prairie rattlesnakes (Crotalus viridis) was exposed to three types of trails after striking rodent prey (Mus musculus). One trail was made with mouse urine, another was made with tap water, and the third consisted of materials from mouse integument. The snakes exhibited trailing behavior only when integumentary trails were available. It was concluded that prairie rattlesnakes do not utilize urinary cues; instead they attend to materials associated with rodent skin and fur.

Investigatory behavior inthe plains garter snake (Thamnophis radix) and several additional species

Garter snakes (Thamnophis radix), hognose snakes (Heterodon platyrhinos), and rattlesnakes (Crotalus species) flick their tongues and crawl about in an open field containing no food or sexual (i.e., reproductive) odors. As Experiment I shows, the taxa differ reliably in both rate of tongue flicking and rate of locomotion. In Experiment II, garter snakes (Thamnophis radix) placed into an open field for 5 min showed more tongue flicking than snakes that were handled and placed directly back into their home cages, indicating that the first group was exploring the apparatus rather than responding only to handling. During Minutes 3 through 5 (Experiment III) in the open field, garter snakes emitted fewer tongue flicks than they did during the first minute, and after 20 min, the rate of tongue flicking was virtually zero. However, snakes were capable of responding to presentation of new objects and/or odors, indicating that the previous response decrement was not derived from effector fatigue but rather from some habituatory process. Experiment IV revealed that satiated snakes habituated more rapidly than hungry snakes during exploration of the open field. Hence, exploratory behavior in these snakes is at least partially under the control of the same factors which mediate food-related appetitive activities.

Analysis of aggressive behaviour in the bluegill sunfish Lepomis macrochirus rafinesque: Effects of sex and size

Abstract Two experiments explored the effects of resident and intruder sex (experiment 1) and size (experiment 2) upon aggressive behaviour exhibited by sunfish during 30-min observation sessions. Bluegill sunfish ( Lepomis macrpchirus Rafinesque) in non-reproductive condition were subjects in both experiments. Residents occupied 95-litre aquaria for 7 days prior to the introduction of an intruder at the start of an observation session. This paradigm allows independent assessment of the effects of both resident-aggressor sex (or size) and intruder-aggressee sex (or size). The first experiment revealed that neither resident sex nor intruder sex exerted significant effects on resident aggressiveness. Experiment 2 showed that large residents exhibited more aggressive responses to both large and small intruders than did small residents. Implications of these findings for perceptual mechanisms underlying the release of bluegill aggression are discussed.