Donald H. Owings

Snake Mobbing By California Ground Squirrels: Adaptive Variation and Ontogeny

California ground squirrels (Spermophilus beecheyi) commonly live in association with and are the prey of snakes. Field observations indicate that encounters between the two may often include mobbing by the squirrel and defensive behavior by the snake. Our research had three goals : 1) to systematically observe and describe these mobbing interactions in both field and laboratory situations; 2) to compare in the laboratory the intensity of mobbing gopher, garter, and rattlesnakes by squirrels from two populations which encounter rattlesnakes (rattlesnake adapted), and one which does not (rattlesnake nonadapted) ; 3) to record and describe reactions to a garter snake by young snake-naive squirrels from rattlesnake adapted and nonadapted populations. We found the following. 1. Squirrels approached snakes, investigated them in elongate postures, bobbed their heads, flagged their tails, and sniffed snakes. Aggressively motivated squirrels kicked sand at the snakes, displayed lateral postures, pounced on, and bit them. 2. The stressful impact of this behavior upon the snake is documented by positive correlations between indices of mobbing intensity by squirrels and indices of defensive behavior by the snake. 3. Squirrels from both rattlesnake adapted populations mobbed snakes less intensely than the rattlesnake nonadapted squirrels. 4. The adult-like response of young snake-naive squirrels to a garter snake was significantly stronger than to a moving novel object, thus demonstrating that their response to the snake was based upon stimulus parameters other than novelty. 5. Snake-naive young from a rattlesnake adapted population mobbed less intensely than snake-naive young from a rattlesnake nonadapted population. 6. Snake-naive young mobbed more intensely than wild-caught adults. We proposed the following. 1. Snake mobbing may benefit ground squirrels by reducing the snakes hunting efforts in the area in which mobbing occurred. 2. The presence of venomous snakes increases the risk to the mobber, thereby favoring an adaptive attenuation in mobbing intensity. 3. Because young squirrels are often left at the burrow by foraging mothers, it is likely that first encounters with snakes often occur in the absence of adults. Under these conditions natural selection might favor predetermined epigenesis of the ability to recognize and respond appropriately to snakes. 4. Young snake-naive squirrels may not be as capable as adults of recognizing immobile snakes. Their enhanced response, relative to adults, to moving snakes may be an adaptive mechanism which permits the young to learn to recognize static snake form.

Moon-related surface activity of bannertail (Dipodomys spectabilis) and fresno (D. Nitratoides) kangaroo rats

Abstract Temporal aspects of nocturnal activity of bannertail kangaroo rats were measured in the field. Maximum activity was about twenty minutes aftyer sunset, thereafter declining throughout the night. Activity was about three times greater when the moon was down than when it was up. Activity shifted somewhat from the open to vegetation cover when the moon was up. Laboratory measures of activity from captive bannertails were also obtained. The activity of bannertails kept in small pens resambled corresponding aspects of the field data. Activity in wheels was unlike activity in the field, and the effects of a laboratory ‘moon’ were opposite to those of the real moon upon bannertails in the field.

Ground squirrels use an infrared signal to deter rattlesnake predation

The evolution of communicative signals involves a major hurdle; signals need to effectively stimulate the sensory systems of their targets. Therefore, sensory specializations of target animals are important sources of selection on signal structure. Here we report the discovery of an animal signal that uses a previously unknown communicative modality, infrared radiation or “radiant heat,” which capitalizes on the infrared sensory capabilities of the signals target. California ground squirrels (Spermophilus beecheyi) add an infrared component to their snake-directed tail-flagging signals when confronting infrared-sensitive rattlesnakes (Crotalus oreganus), but tail flag without augmenting infrared emission when confronting infrared-insensitive gopher snakes (Pituophis melanoleucus). Experimental playbacks with a biorobotic squirrel model reveal this signals communicative function. When the infrared component was added to the tail flagging display of the robotic models, rattlesnakes exhibited a greater shift from predatory to defensive behavior than during control trials in which tail flagging included no infrared component. These findings provide exceptionally strong support for the hypothesis that the sensory systems of signal targets should, in general, channel the evolution of signal structure. Furthermore, the discovery of previously undescribed signaling modalities such as infrared radiation should encourage us to overcome our own human-centered sensory biases and more fully examine the form and diversity of signals in the repertoires of many animal species.

The importance of mate behavioural compatibility in parenting and reproductive success by cockatiels, Nymphicus hollandicus

In species with long-term pair relationships, behavioural compatibility between mates could be a significant source of selection among pairs. We explored the relation between behavioural compatibility and reproductive success in cockatiels, a socially monogamous species with biparental care and variable compatibility. The mate behavioural compatibility measure, derived from our previous work with these birds, was based on five pair-level variables: proximity, behavioural synchrony, copulation, allopreening responsiveness and total aggression. We operationally defined mates as more compatible when they showed greater proximity, synchrony, allopreening responsiveness and copulation frequencies and lower frequencies of aggression. Using a captive, seminatural population, we tested the following three interrelated hypotheses: (1) pairs with greater behavioural compatibility before breeding should have greater reproductive success; (2) among pairs that laid fertile eggs, pairs with greater behavioural compatibility should show better incubation coordination and (3) pairs with better incubation coordination should hatch more fertile eggs. Our results were consistent with these hypotheses. Pairs that laid eggs had significantly higher behavioural compatibility scores than did those that laid no eggs. Pairs with higher behavioural compatibility scores reared significantly more chicks to independence even after controlling for the effects of pair bond duration and parental age. Among pairs that laid fertile eggs, mates with higher behavioural compatibility scores had greater incubation coordination, measured by periods during which only one parent at a time attended the eggs, and greater hatching success of fertile eggs. Behavioural compatibility between mates in socially monogamous species may have reproductive consequences, and emergent behavioural features of pair relationships may have evolutionary significance.

Responses to alarm calls by California ground squirrels: Effects of call structure and maternal status

Summary1.The purposes of this study were to assess the response eliciting properties of five structural variants of the California ground squirrel alarm call system, and to compare the responsiveness of females with and without young to the vocalizations. Tape recordings of alarm calls and control sounds were played back in the field to adult female ground squirrels. The squirrels responded very little to control sounds. Following alarm calls, however, posture height and running increased; feeding, walking and non-locomotion movements decreased. None of the playbacks elicited vocalizations from the squirrels.2.The four chatter-chat calls evoked patterns of response that were distinctly different from reactions to the whistle. The immediate running response to chatter-chats was followed quickly by upright posturing, which subsequently declined throughout the 3-min period following the call. Feeding was suppressed throughout the 3-min post-chatter-chat interval, but movement increased after initial inhibition. After the initial running response to whistles, walking was common and upright posturing was delayed until the second post-call minute. Feeding and nonlocomotion movement were initially suppressed but increased monotonically over time. We proposed that these differences were adaptively related to the fact that chatter-chats typically follow detection of terrestrial predators, whereas whistles usually signal flying raptors.3.The responses to the four chatter-chat calls were graded in intensity, reaching higher levels in response to calls with more notes and lower noise content. The chat, a one-note call with high noise content, evoked the weakest reaction. We proposed that these two dimensions of calling (number of notes and noise content), in conjunction with several other semi-independent parameters, provide a sufficient diversity of signals to permit specification of the referent of the call (conspecific or predator) as well as the arousal level of the caller.4.We hypothesized that kin selection was responsible for the greater responsiveness of parous than of nonparous females to the alarm calls, and we discussed some implications of this difference.

Reproductive behaviour and multiple paternity of California ground squirrels

Abstract Abstract. The mating system of the California ground squirrel, Spermophilus beecheyi , was examined to determine the incidence of multiple paternity of litters and the circumstances under which it occurs. The population studied has a promiscuous mating system. All receptive females solicited and mated with multiple males, which resulted in 88·9% (eight of nine) of litters sampled in 1988 being multiply sired, the highest frequency of multiple paternity yet reported for a natural population of any species. Five proteins in blood samples of adults and litters were tested by polyacrylamide gel electrophoresis and isoelectric focusing for the analysis. Males defended territories that partially overlapped home ranges of females, but did not achieve exclusive access to those females. Females travelled from their home burrows to mate both with males whose home ranges partially overlapped their own and with males whose home ranges did not overlap with their own. Females mated with an average of 6·7 males during receptive periods that averaged (±SD) 6·67 ± 3±18 h in duration.

The behaviour of California ground squirrels

Abstract This report describes the general behaviour patterns, spacing patterns and alarm vocalizations of California ground squirrels ( Spermophilus beecheyi ) as observed in three successive springs of research. Functions are suggested for most behaviour patterns. Males maintain home ranges relatively exclusive of other males via site-specific aggression. Female home ranges overlap extensively with those of other females, and defence is confined to the immediate vicinity of the burrow. Both sexes respond to avian and mammalian predators with relatively predator-specific vocalizations.

Home range, population structure, and spatial organization of California ground Squirrels

Home-range size and spatial organization were described for a population of California ground squirrels ( Spermophilus beecheyi ) in which maternal relationships and residence time were known for individuals. Home-range sizes as determined by harmonic-mean transformation for female California ground squirrels were similar to those reported for females of some populations of sciurids, but the home ranges of males were smaller than those reported for other spermophile males. Home-range sizes of females were larger than those of males. No significant difference in size of home ranges of males was detected between breeding and postbreeding seasons. Neither females nor males had exclusive use of their home ranges. More female yearlings established burrow systems near their natal burrows than did males. Each young female that was retrapped as a yearling had established a home range adjacent to or overlapping that of her mother. After establishing burrow systems as yearlings, adults typically exhibited multiyear site fidelity. Both females and males probably lived near descendent kin.

Evolutionary dissipation of an antisnake system : differential behavior by California and Arctic ground squirrels in above- and below-ground contexts

Arctic ground squirrels (Spermophilus parryii ablusus) have been free from snake predation for about 3 million years. To evaluate the effects of this prolonged relaxation of natural selection, lab-born Arctic ground squirrels were compared to snake-inexperienced California ground squirrels (Spermophilus beecheyi fisheri) from a habitat where rattlesnake and gopher snake predation is intense. Their behavior was video taped during 10-min encounters with a Pacific gopher snake (Pituophis melanoleucus catenifer) in a seminatural above-ground setting and in an artificial burrow. In separate trials, a domesticated Norway rat was used as a control for the effects of encountering a novel animate object; this rat was enclosed in a slowly moving opaque nylon bag above ground but was allowed to move freely below ground. No evidence was found that, after prolonged relaxed selection from snakes, Arctic ground squirrels retained the specialized behavioral antisnake defenses evident in California ground squirrels. Although we originally hypothesized that the more constrained burrow context might limit the evolutionary dissipation of behavioral antisnake defenses, we found no evidence of a more intact system in Arctic squirrels below than above ground. Arctic squirrels used many of the same general kinds of motor patterns as California squirrels, but in ways that failed to differentiate the gopher snake from the rat in either above- or below-ground contexts. In contrast, the California squirrels tail flagged only in the presence of the snake above ground and differentially applied substrate-throwing at the snake and rat burrow intruders, harassing the snake more than twice as much as the rat. Above ground, California ground squirrels were more conservative toward both adversaries than Arctic ground squirrels were, keeping their distance and therefore experiencing fewer noxious consequences, such as snake strikes. However, this result was context dependent. Below ground, California ground squirrels were more willing than Arctic ground squirrels to approach and harass both burrow intruders. Although repeated striking evoked occasional snake-directed substrate throwing above ground, Arctic ground squirrels never threw substrate at the snake in the burrow. In comparison with California ground squirrels, Arctic ground squirrels appear to enter their first gopher snake encounter with both a much lower assessment of the risk involved and less clearly defined knowledge about how to deal with these risks. We conclude that 3 million years of genetic drift has altered the cognitive system structuring the meaning of snakes to Arctic ground squirrels in various settings.

The Role of Information in Communication: An Assessment/Management Approach

The assumption that communication involves the transfer or withholding of information underlies most current research and interpretation of animal communication. This assumption implies that information plays a causal role in communication. Here we suggest that information, when accorded a central causal role, has limited our understanding of communication.