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The 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.

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Nonvenomous 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.