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27. Snake.Scent Application Behavior in the Siberian Chipmunk Eutamias Sibiricus Asiaticus

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27. Snake.Scent Application Behavior in the Siberian Chipmunk Eutamias Sibiricus Asiaticus No. 5] Proc. Japan Acad., 57, Ser. B (1981) 141 27. Snake.Scent Application Behavior in the Siberian Chipmunk Eutamias sibiricus asiaticus By Tomomichi KOBAYASHI*) and Munetaka WATANABE** (Communicated by Kiyoshi TAKEWAKI,M. J. A., May 12, 1981) Snakes are important predators for many rodents (Fitch and Twining, 1946; Owings and Coss, 1977; Robinson, 1980). Some rodents are known to direct a mobbing to snakes (Richardson, 1942; Owings and Coss, 1977), which is a type of antipredator response observed in many vertebrates (Altmann, 1956; Kruuk, 1964, 1972; Curio, 1966). Recently we found the antipredator behavior of another type than the mobbing in Siberian chipmunks, which is performed in the encounter with the carcass of snakes, in contrast to the mobbing that is usually directed to live snakes. When the chipmunk has found a snake carcass, it approaches the carcass very cautiously with an appearance of fear, then nibbles the surface of the carcass (usually that of the head or tail region) (Fig. la), mumbles it in the mouth and applies the nibbled bit on the body fur (Fig. 1b). This applica- tion behavior is performed almost in the same manner as the self- grooming (Steiner, 1973) seen often in the rodents ; the chipmunk Fig. 1. Snake-scent application behavior to the carcass of a snake by a chipmunk. A chipmunk nibbles the surface of the carcass (a) and mumbles and applies the nibbled bit on the fur of its own body (b). *' Dept . of Biol., Fac. of Sci., Okayama University. **' Dept . of Biol., College of Liberal Arts and Sciences, Okayama Univer- sity, Tsushima, Okayama 700. 142 T. KOBAYASHI and M. WATANABE [Val. 57(B), chews and licks repeatedly the fur of the lower half of the body and the back of the trunk. During the application the fur gets so wet that the black basal portion of the fur (Kawamichi and Kawamichi, 1978) comes into sight. The anti-snake behavior, which we will name snake-scent application (SSA) behavior, is directed also to the urine of snakes. The chipmunk applies the half-solid urine on its fur in the same manner as the SSA to the carcass. This study analysed the repertory of objects to which the SSA was directed, the sign stimuli and the adaptive significance of the SSA behavior. The experiments were carried out using three of six Siberian chipmunks Eutamias sibiricus asiaticus which all performed the SSA behavior. The three chipmunks tested were individually identified and named Benn (ci, 2.5 years old), Horn (~ , 2 years) and Rott ( S~ 2.5 years) respectively. They were reared in an outdoor enclosure (10 x 10x2 m high) which simulated their natural habitat. Objects for testing the SSA were put on some places in the enclosure. In the first experiment the repertory of objects inducing the SSA behavior in the chipmunks was examined by presenting the carcass, urine and feces of snakes, the carcass of lizards, birds and a mammal, and the urine of birds, as shown in Table I. The chipmunks performed the SSA only to the carcass and urine of the snakes so far as we tested. This result suggests that the SSA is limitedly directed to the carcass and urine of snakes. The second experiment was planned to determine sign stimuli Table I. Mean duration of snake-scent application behavior to the carcass, urine and feces of various animals by three individuals of the chipmunk Eutamias sibiricus asiaticus No. 5] Snake-Scent Application in Chipmunk 143 for inducing the SSA. The surface of the carcass of Ela,phe clim,aco phora, excepting that of its cloacal region, was artificially scratched and the injured surface was rubbed on some spots on the ground in the enclosure. The chipmunks nibbled the grass on the spots and applied it on their fur. They responded in the same manner also to the spots soaked with a solution (almost transparent) prepared by dissolving snake urine in water at 1/10 concentration (Table II). These facts show that the sign stimulus for the SSA is of olfactory nature. In the third experiment the anatomical source of the SSA-releas- ing odor substances was investigated. The body of Elaphe climaco- phora was separated into five parts as follows; (1) skin, (2) vertebra and skeletal muscle, (3) entrails and vein, (4) rectum and (5) anal gland-a pair of sac-like organs in the tail of snakes, secreting active odor substances (Oldak, 1976)-and muscles surrounding it. The occurrence and duration of the SSA behavior by chipmunks in the presentation of each of the above five parts were recorded. Table II clearly shows that the parts (1) and (5) release the SSA. Consider- ing the result of this experiment together with that of the second experiment, it is possible that the odor substance responsible for the SSA to the carcass is contained in the snake skin, and that the odor substance for the SSA to the urine is the secretion from the anal gland which is supposed to soak into urine during urination. The latter possibility appears to be strongly supported by strikingly long SSA behavior in the presentation of anal gland secretion. In the fourth experiment our working hypothesis concerning the adaptive significance of the SSA behavior was examined; that is, the scent of snake skin or urine applied on the fur during the SSA by chipmunks could suppress the predation of the latter by snakes which Table II. Mean duration of snake-scent application behavior by chipmunks 144 T. KOBAYASHIand M. WATANABE [Vol. 57(B), use olfaction as the main sensory cue in their predation (Burghardt and Hess, 1968; Burghardt and Abeshaheen, 1971; Burghardt, 1975). Three individuals of Elaphe climaco phora A (~, 134 cm), B (5', 128 cm) and C (~, 112 cm) were separately reared in serpentaria (2 x 2 x 0.5 m high). A pair of mice Mus musculus or voles Apodemus speciosus was killed by choking off. To the fur of the experimentals the snake urine was applied. To some of the controls none were applied, and to the others, either turbid water, swallow urine or domestic fowl urine was applied. Both the experimental and control carcasses were put in a close arrangement in the serpentaria after drying their fur, and whether the snake predated the carcasses or not was inspected two to twenty-three hours after presentation. The results of this experiment are summarized in Table III. In six out of total twelve trials the controls were predated and the experimentals were not. In two trials both the experimental and the control were predated. It is noticeable that there were no trials where only the experimental was predated. This fact seems to confirm our hypothesis. In Trials 6 and 7 for the snake A the carcasses of the experimentals Table III. Predation by Elaphe climacophora in the presentation of mice or voles No. 5] Snake-Scent Application in Chipmunk 145 were presented 24 and 30 hrs after applying snake urine respectively. The result that the experimentals were not predated in both trials suggests that the predation-suppressing effect of the scent of snake urine might be retained for at least 30 hrs after the SSA by Siberian chipmunks in the field. In Trials 3 and 7 for the snake A, swallow-urine applied in- dividuals (controls) were predated, although snake-urine applied ones (experimentals) were not. This fact shows that possible predation- suppressing odor substance in snake urine might not be uric acid which is the main component of reptilian and avian urine. The sup- pression of predation in snake-urine applied individuals is possibly due to the active volatile secretion of anal glands, which was guessed to be a substance releasing the SSA behavior from the third ex- periment. Acknowledgement. The authors wish to thank Dr. M. Toriba of the Japan Snake Institute, Gunma Prefecture, for his valuable advice. References Altmann, S. A. (1956) : Avian mobbing behavior and predator recognition. Condor, 58, 241-253. Burghardt, G. M. (1975) : Chemical prey preference polymorphism in newborn garter snakes T hamnophis sirtalis. Behaviour, 52, 202-225. Burghardt, G. M., and J. P. Abeshaheen (1971) : Responses to chemical stimuli of prey in newly hatched snakes of Genus Elaphe. Anim. Behav., 19, 486-489. Burghardt, G. M., and E. H. Hess (1968) : Factors influencing the chemicall release of prey attack in newborn snakes. J. Comp. Physiol. Phychol., 66, 289- 295. Curio, E. (1966) : How finches react to predators. Animals, 142-143. Fitch, H. S., and H. Twining (1946) : Feeding habits of the Pacific rattlesnake. Copeia, 64-71. Kawamichi, T., and M. Kawamichi (1978) : Hair clipping patterns for marking tree shrew and chipmunk. Japan. J. Ecol., 28, 65-67. Kruuk, H. (1964) : Predators and antipredator behavior of the black-headed gull (Larus ridibundus). Behaviour, suppl. II, 129. (1972) : The spotted hyena. Univ. Chicago Press, Chicago. Oldak, P. D. (1976) : Comparison of the scent gland secretion lipids of twenty- five snakes: Implications for biochemical systematics. Copeia, 320-326. Owings, D. H., and R. G. Coss (1977) : Snake mobbing by California ground squirrels: Adaptive variation and ontogeny. Behaviour, 62, 50-69. Richardson, W. B. (1942) : Reaction toward snakes as shown by wood rat Neotoma albigula. J. Comp. Psychol., 34, 1-10. Robinson, S. R. (1980) : Antipredator behaviour . and predator recognition in Belding's ground squirrels. Anim. Behav., 28, 840-852. Steiner, A. L. (1973) : Self- and allo-grooming behavior in some ground squirrels (Sciuridae), a descriptive study. Can. J. Zool., 51, 150-162..
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