Snake Species Discrimination and the Role of Olfactory Cues in the Snake-Directed Behavior of the California Ground Squirrel

Behaviour ◽  
1978 ◽  
Vol 65 (1-2) ◽  
pp. 115-123 ◽  
Author(s):  
Hennessy David F. ◽  
Owings Donald H.

This experiment had two objectives. One was to seek evidence for greater caution by California ground squirrels (Spermophilus beccheyi) when interacting with venonnous rattlesnakes (Crotalus viridis), their most important snake predator, than when interacting with nonvenomous gopher snakes (Pituophis melanoleucus), their second-most important snake predator. The second was to examine the role of olfaction in mediating snake-directed behavior by these squirrels, since matry squirrel-snake encounters occur in burrows where visual cues are unavailable. In an illuminated room, we videotaped the responses by eight freely moving ground squirrels to the two snake species; the snakes were presented in large, transparent plastic bags that were either sealed (odor unavailable) or perforated (odor available). The results confirmed our predictions that the squirrels should behave more cautiously toward rattlesnakes than toward gopher snakes, and that olfaction is an important mediator of snake-directed behavior. Although the squirrels approached the two snake species equally often, they attended more to the rattlesnake than to the gopher snake, but remained farther away from the rattlesnake. When snake odor was available, the squirrels spent more time attending to the snakes, approached the snakes more frequently, approached the snakes in elongate postures more often and sand kicked more at the snakes. We proposed the following. 1. The antipredator strategy of snake harassment by California ground squirrels is sensitive to risk, exhibiting attenuation where risk is higher. 2. Olfaction is likely to be even more important during squirrel-snake encounters in the dark, especially in burrows. 3. The ability to recognize snakes on the basis of odor may not depend on prior experience with snakes, and may circumvent difficulties associated with visual detection of snakes.

Behaviour ◽  
1978 ◽  
Vol 65 (1-2) ◽  
pp. 115-123 ◽  
Author(s):  
Hennessy David F. ◽  
Owings Donald H.

This experiment had two objectives. One was to seek evidence for greater caution by California ground squirrels (Spermophilus beccheyi) when interacting with venomous rattlesnakes (Crotalus viridis), their most important snake predator, than when interacting with nonvenomous gopher snakes (Pituophis nielanoleucus), their second-most important snake predator. The second was to examine the role of olfaction in mediating snake-directed behavior by these squirrels, since many squirrel-snake encounters occur in burrows where visual cues are unavailable. In an illuminated room, we videotaped the responses by eight freely moving ground squirrels to the two snake species; the snakes were presented in large, transparent plastic bags that were either sealed (odor unavailable) or perforated (odor available). The results confirmed our predictions that the squirrels should behave more cautiously toward rattlesnakes than toward gopher snakes, and that olfaction is an important mediator of snake-directed behavior. Although the squirrels approached the two snake species equally often, they attended more to the rattlesnake than to the gopher snake, but remained farther away from the rattlesnake. When snake odor was available, the squirrels spent more time attending to the snakes, approached the snakes more frequently, approached the snakes in elongate postures more often and sand kicked more at the snakes. We proposed the following. i. The antipredator strategy of snake harassment by California ground squirrels is sensitive to risk, exhibiting attenuation where risk is higher. 2. Olfaction is likely to be even more important during squirrel-snake encounters in the dark, especially in burrows. 3. The ability to recognize snakes on the basis of odor may not depend on prior experience with snakes, and may circumvent difficulties associated with visual detection of snakes.


Behaviour ◽  
1993 ◽  
Vol 124 (1-2) ◽  
pp. 137-162 ◽  
Author(s):  
Richard G. Coss ◽  
Naomie S. Poran ◽  
Kevin L. Gusé ◽  
David G. Smith

AbstractNonvenomous Pacific gopher snakes (Pituophis melanoleucus catenifer) and venomous northern Pacific rattlesnakes (Crotalus viridis oreganus) have coexisted in a predator-prey relationship with California ground squirrels (Spermophilus beecheyi) for many thousands of generations. This long-term relationship has fostered in ground squirrels the evolution of antisnake defenses that consist of physiological resistance to rattlesnake venom and behavioral tactics of probing and harassing that might facilitate snake-species discrimination. Snake harassment by adults might also protect pups by interfering with snake hunting activities. Some ground squirrel populations have colonized habitats where rattlesnakes, but not gopher snakes, are rare or absent. Initial research indicates that squirrels experiencing relaxed selection from rattlesnakes are very aggressive toward their remaining nonvenomous snake predator, the gopher snake. Two experiments investigated the effects of relaxed selection from rattlesnakes by examining: 1) changes in level of venom resistance, 2) the reorganization of antisnake behaviors in lab-born pups and wild-caught adults from different sites, and 3) the role of natural experiences on the development of antisnake behavior in a rattlesnake-adapted population. Level of venom resistance was examined by an in vitro radioimmunoassay of serum-to-venom binding of two populations of Douglas ground squirrels (S. b. douglasii). The ancestors of one population are estimated to have experienced relaxed selection from rattlesnakes for about 9,000 years based on genetic distance and radiocarbon analyses. The antisnake behavior of 60-73 day-old lab-born pups from these two populations was video taped during presentations of a caged rattlesnake or gophcr snake for alternate 5-min trials in a seminatural laboratory setting. Two groups of wild-caught adult Beechey groundsquirrels (S. b. beecheyi) were studied using the same protocol for examining antisnake behavior. One group was obtained from a population that recently colonized a rattlesnake-rare site and exhibits moderate venom resistance. The second group came from a population that exhibits very low venom resistance and inhabits a rattlesnake-free site; relaxed selection from rattlesnakes for this population is estimated to span approximately 60,000 years. Comparisons of Douglas ground squirrels from rattlesnake-abundant and rettlesnakerare sites revealed that venom resistance declined approximately 59% after an estimated 9,000 years of relaxed selection from rattlesnakes. Lab-born Douglas pups from the same rattlesnake-rare site were more aggressive toward the gopher snake than toward the rattlesnake whereas pups from the population experiencing predation from both species of snake treated both snakes as similarly dangerous. Unlike pups, wild-caught adults from the rattesnake-adapted population harassed the rattlesnake more intensely than the gopher snake, a phenomenon that may reflect their experience with snakes in nature and larger body size that reduces their vulnerability to envenomation. Wild-caught Beechey ground squirrels that recently colonized a rattlesnake-rare site did not differentiate the rattlesnake and gopher snake whereas Beechey ground squirrels whose ancestors have experienced prolonged relaxed selection from rattlesnakes were more aggressive toward the gopher snake. Consistent with previous findings, prolonged relaxed selection from rattlesnakes, but not gopher snakes, appears to have reduced the inhibition to harass large gopher snakes. This microevolutionary shift in increased aggressiveness toward the gopher snake could result from the virtual absence of any risk in misidentifying rattlesnakes from gopher snakes.


Behaviour ◽  
2001 ◽  
Vol 138 (5) ◽  
pp. 575-595 ◽  
Author(s):  
Matthew Rowe ◽  
Donald Owings ◽  
Diane McKernon ◽  
Patricia Arrowood ◽  
Richard Coss

AbstractThe purposes of this study were: (1) to describe the snake-directed antipredator behavior of rock squirrels; (2) to assess whether rock squirrels distinguish nonvenomous gopher snakes from venomous rattlesnakes; (3) to compare antisnake behavior in a snake-rare urban site and a snake-abundant wilderness site as a means of assessing whether natural selection or experience has generated population differences in behavior; (4) to assess snake densities in the two study sites; (5) to compare the antisnake behavior of rock squirrels with that of their closest relatives, California ground squirrels (Spermophilus beecheyi), a species that appears to differ from rock squirrels in exhibiting marked sexual-size dimorphism; and (6) to gather additional data on sexual size dimorphism in these two ground squirrel species. We tethered nonvenomous gopher snakes (Pituophis melanoleucus) and venomous western diamondback rattlesnakes (Crotalus atrox) in the field near burrows of marked squirrels and videotaped the ensuing interactions. Rock squirrels from both urban and wilderness populations confronted snakes while waving their fluffed tails from side to side, throwing substrate at the snakes, and even attacking snakes on occasion. Survey data confirmed large differences in snake densities between the two sites. Squirrels from the snake-abundant wilderness site distinguished rattlesnakes from gopher snakes, but squirrels from the snake-rare urban site did not. Since these squirrels show similar evidence of selection from snakes, as revealed by their equivalent physiological resistance to rattlesnake venom, we attributed these behavioral differences to the effects of snake experience. Rock squirrel antisnake behavior was very similar to that of California ground squirrels. Where the two species' behavior was dissimilar, the differences may be due in part to the interspecies variation in sexual size dimorphism confirmed in this study, and to the greater number of rattlesnake species that rock squirrels encounter.


Parasitology ◽  
1910 ◽  
Vol 3 (4) ◽  
pp. 417-422 ◽  
Author(s):  
Creighton Wellman ◽  
Wm. B. Wherry

While examining last year some California ground squirrels, we found among this rodent's endoparasites the following protozoa, worm and mite which appear to be new. Ordinarily the mere recording of new species of the parasites of wild animals is of little interest to physicians, but since the rô1e played by O. beecheyi in the maintenance of plague on our Pacific Coast was definitely established (vide Wherry, Journ. Infect. Dis. 1908, v. 485)1 all medical men are naturally interested in the diseases which affect this rodent. Therefore the following brief descriptions of the parasites we have found are offered.


Behaviour ◽  
1990 ◽  
Vol 112 (3-4) ◽  
pp. 222-244 ◽  
Author(s):  
Naomie S. Poran ◽  
Richard G. Coss

AbstractThe development of antisnake behavioral and immunological defenses was investigated in laboratory born California ground squirrels (Spermophilus beecheyi) from an area in California where Northern Pacific rattlesnakes (Crotalus viridis oreganus) and Pacific gopher snakes (Pituophis melanoleucus catenifer) are abundant. Previous studies have shown that adult ground squirrels from this area possess innate physiological resistance to rattlesnake venom while pups are highly vulnerable to predation from snakes. Pups from other areas are known to exhibit snake recognition and adult-like antisnake behaviors on first encounter, a finding that prompted further study of pups from this area. The present study had four objectives: 1) to determine if inexperienced pups can distinguish rattlesnakes from gopher snakes, 2) to determine what role mothers play in shaping their pups' behavior during their first encounters with snakes, 3) to determine if maturational factors affect the expression of antisnake behaviors, and 4) to determine if maturational factors affect rattlesnake venom resistance, especially during the first weeks of life. Two groups of 63-70 day-old pups were studied during their first encounters with both a rattlesnake and a gopher snake. The snakes were presented separately in a wire-screened compartment positioned in the center of the experiment room containing sand substratum. Pups in this setting were either alone or with their mothers during 5-min encounters with the snakes, which were video taped from an overhead mirror. Two years later, pups which had previously engaged the snakes with their mothers were retested with the same snakes as adults and their behavior was compared to that of the earlier group of pups encountering the snakes alone. In another group of pups, radioimmunoassays of serum-to-venom binding examined changes in venom resistance at 14, 30, 48, and 80 days of age. The results indicated that pups do indeed differentiate rattlesnakes from gopher snakes irrespective of whether the mother is present or absent as inferred from the greater time that they spent near the rattlesnake. When the mothers were present, pups spent much less time investigating the rattlesnake or gopher snake closely as compared with the condition in which pups were alone. Except for displacing pups interacting with the snakes at close range, which could theoretically reduce the probability of pup injury, mothers exhibited very little overt protection of pups. Pups and adults behaved similarly when they engaged the snakes as evinced by their close-range investigative behavior, substrate throwing, and tail-flagging activity with the exception that adults were less vigilant in monitoring the snake's activity from anywhere in the experiment room. Analysis of developmental changes in venom resistance revealed that serum-to-venom binding achieves adult levels at 30 days of age which is about 15 days prior to burrow emergence. Despite adult serum-to-venom binding levels, pups are vulnerable to envenomation due to their reduced body mass and serum volume available to neutralize rattlesnake venom. From an over-all perspective, recently emerged ground squirrel pups from a population in which adults are highly resistant to rattlesnake venom are vulnerable to snake predation. Yet, enigmatically, they exhibit adult-like patterns of antisnake behaviors that are very risky, such as close-range investigation and substrate throwing. Tail flagging at the pup stage of development is more easily interpretable as providing some protection from snakes because it attracts the mother's attention and that of nearby adults who are likely to intervene. We interpret the early appearance in pups of risky adult-like investigative and snake-harassment behaviors as a by-product of epigenetic processes aimed at older, less vulnerable stages of development in which these behaviors are likely to have greater defensive utility.


Behaviour ◽  
1986 ◽  
Vol 99 (1-2) ◽  
pp. 101-116 ◽  
Author(s):  
Donald H. Owings ◽  
A. Beckett Gladney ◽  
David F. Hennessy ◽  
Daniel W. Leger

AbstractThe predator-evoked calling of California ground squirrels (Spermophilus beecheyi) was studied in the field during the reproductive season. Three different sources of data indicated that adults call more after, than before their young have reached the age of first emergence from natal burrows. During exposure to a tethered rattlesnake (Crotalus viridis oreganus) and to a freely-moving dog (Canis familiaris), and in natural encounters with a coyote (Canis latrans) or bobcat (Lynx rufus), calling was more frequent after than before young first emerged. We concluded that California ground squirrels call in order to warn their offspring about predators, like other ground squirrel species do. In order to see the increase in mammalian predator evoked calling after pup emergence, we had to separate calling on the basis of its temporal organization. Nonrepetitive calling involved spacing a few vocalizations irregularly in time. Calls patterned in this way were more common early in an encounter, became more frequent after pup emergence, and more consistently elicited immediate reactions. Such calling was probably used to warn pups. Repetitive calling comprised rhythmic emission of a series of vocalizations. Calls organized repetitively were more common later in an encounter, were not emitted more frequently after pup emergence, and less consistently evoked immediate reactions. These and other differences between the two temporal patterns of vocalizing led us to propose that repetitive calling represented a "tonic" communicatory effort (as in SCHLEIDT, 1973). Repetitive inputs to other squirrels may act "cumulatively" in a longer time scale than nonrepetitive calling, so as to cultivate or maintain vigilance in other squirrels. The repetitive caller could benefit by using the enhanced reactions of these more vigilant squirrels as a source of information about the predator. We propose that predator-prey episodes may be understandable from an "epigenetic" perspective. That is, the first alarm calls during an encounter should shift squirrels from an unwarned to a warned status; subsequent calling must then function in some other way than as a warning.


Author(s):  
Adam F. Werner ◽  
Jamie C. Gorman

Objective This study examines visual, auditory, and the combination of both (bimodal) coupling modes in the performance of a two-person perceptual-motor task, in which one person provides the perceptual inputs and the other the motor inputs. Background Parking a plane or landing a helicopter on a mountain top requires one person to provide motor inputs while another person provides perceptual inputs. Perceptual inputs are communicated either visually, auditorily, or through both cues. Methods One participant drove a remote-controlled car around an obstacle and through a target, while another participant provided auditory, visual, or bimodal cues for steering and acceleration. Difficulty was manipulated using target size. Performance (trial time, path variability), cue rate, and spatial ability were measured. Results Visual coupling outperformed auditory coupling. Bimodal performance was best in the most difficult task condition but also high in the easiest condition. Cue rate predicted performance in all coupling modes. Drivers with lower spatial ability required a faster auditory cue rate, whereas drivers with higher ability performed best with a lower rate. Conclusion Visual cues result in better performance when only one coupling mode is available. As predicted by multiple resource theory, when both cues are available, performance depends more on auditory cueing. In particular, drivers must be able to transform auditory cues into spatial actions. Application Spotters should be trained to provide an appropriate cue rate to match the spatial ability of the driver or pilot. Auditory cues can enhance visual communication when the interpersonal task is visual with spatial outputs.


2011 ◽  
Vol 2011 ◽  
pp. 1-5 ◽  
Author(s):  
Atsushi Hirao

In avian mating systems, male domestic fowls are polygamous and mate with a number of selected members of the opposite sex. The factors that influence mating preference are considered to be visual cues. However, several studies have indicated that chemosensory cues also affect socio-sexual behavior, including mate choice and individual recognition. The female uropygial gland appears to provide odor for mate choice, as uropygial gland secretions are specific to individual body odor. Chicken olfactory bulbs possess efferent projections to the nucleus taeniae that are involved in copulatory behavior. From various reports, it appears that the uropygial gland has the potential to act as the source of social odor cues that dictate mate choice. In this review, evidence for the possible role of the uropygial gland on mate choice in domestic chickens is presented. However, it remains unclear whether a relationship exists between the uropygial gland and major histocompatibility complex-dependent mate choice.


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