The perceptual determinants of gaze aversion by humans were examined in psychotic children with autistic symptoms, who persistently avoid eye-contact, and in normal children. Previous studies of normal adults have indicated that two concentric discoid elements, schematically resembling two facing eyes, are arousing stimuli. It was of interest to determine if similar eyelike schemata, as compared with less eyelike schemata of greater or lesser complexity, would elicit the least visual inspection as an arousal-reducing cut-off act. To clarify discrepancies in the literature as to whether normal and psychotic children differ in their sensitivity to prolonged eye-contact and concomitant readiness to gaze avert, these groups were compared for differential responsiveness to the same stimuli. Measurement of different inspection of eyelike schemata was accomplished using a special model-viewing apparatus in which two models were presented side-by-side in paired comparisons. The duration of each glance directed at a particular model was recorded on video tape and later measured with a stopwatch. Three experiments were performed. The first examined 10 normal and 10 psychotic children during presentations of 5 models comprising a blank model and models with I through 4 concentric discoid elements separated by the same interpupillary distance as are real human eyes. The second experiment examined 15 psychotic children using models presenting two concentric discoid elements in vertical, diagonal, and horizontal orientations. The third experiment examined 10 normal and 10 psychotic children using 5 models comprising two schematic facing eyes as represented by concentric discoid elements, more realistic eyes with staring and adverted irises, and closed eyes. The following results were obtained: I. A model won a particular comparison bout if it was looked at longer than its comparison model. In all experiments and in both groups of children, the model presenting two horizontally placed concentric discoid elements won the fewest number of paired comparison bouts against the field of other models. The only exception occurred for normals in the first experiment in which the blank model won fewer comparison bouts than the model presenting two concentric discoid elements. 2. For the over-all duration of model inspection in the first experiment, the psychotics looked longer at the models than did the normals. However, these groups did not differ as much for the model with two concentric discoid elements. Both groups, particularly the psychotics, looked less at the model presenting two concentric discoid elements than at models presenting other arrangements of concentric discoid elements in the first experiment. Similarly in the third experiment, both groups looked less at the model with two concentric discoid elements than at models with staring and averted irises, albeit these differences were not significant. Normals and psychotics did not differ appreciably in their over-all looking at the more realistic eyelike schemata in the third experiment. With respect to the spatial orientation of two concentric discoid elements in the second experiment, the psychotics looked the least at the model presenting two discoid elements in the horizontal plane. In light of the clinical observations that normals and psychotics differ in gaze behavior, the findings that normal adults are aroused by two concentric discoid elements, and the theoretical aspects of the cut-off hypothesis, the results suggest the following: I. Two horizontally placed concentric discoid elements, schematically resembling two facing eyes, are provocative stimuli eliciting less visual inspection in accordance with the cut-off hypothesis. 2. The lack of differential gazing by normals and psychotics during presentations of models with two schematic facing eyes seems to indicate that, in the absence of supporting features of a human face, two schematic facing eyes were equally provocative to both groups of children.
Captive lesser mouse lemurs (Microcebus murinus) were observed to avert their heads during face-to-face encounters. Based on evidence obtained from other vertebrate species, predominantly among the Primates, it was assumed that the facing orientation and direction of gaze of an adversary was the provocative agent eliciting gaze aversion by mouse lemurs. A more precise examination of the perceptual determinants of gaze aversion employed models presenting various combinations of eyelike concentric circles. Presented side-by-side in paired comparisons, it was predicted that a model presenting two horizontally placed concentric circles, which schematically resemble two facing eyes, would elicit less visual inspection, i.e., more visual avoidance, than models presenting less physiognomic arrangements of concentric circles. Using a special model-viewing apparatus, Experiment I examined the gaze behavior of 28 mouse lemurs in their peak activity period to determine the response-eliciting effectiveness of 5 models varying in the number of concentric circles. Experiment 2 examined 50 lemurs, some of which were in seasonally and artificially induced torpor. Three models differing in the spatial orientation of two concentric circles were investigated in an attempt to control for contour complexity. Both the bout frequency and duration of model fixation were measured using head orientation as the response criterion. The following results were obtained: 1. For the over-all paired comparisons in both experiments, the model presenting two horizontally positioned concentric circles was the only model which elicited significantly fewer bouts of longer fixation. 2. Because of a lack of homogeneity in model fixation, due to intense fear in some lemurs, the lemurs were separated into homogeneous subgroups using statistical criteria in the first experiment and behavioral criteria in the second. Only the largest subgroups comprising relatively calm mouse lemurs exhibited differential model fixation at a significant level. In both experiments, these particular subgroups looked significantly less at the critical model exhibiting two schematic facing eyes than at any of the other models. In conjunction with observations of dyadic interactions among mouse lemurs, the experimental findings suggest the following: 1. Two schematic facing eyes viewed out of context with a predator or conspecific are a provocative source of stimulation eliciting less visual inspection which could be considered analogous to bouts of gaze aversion observed among interacting lemurs. 2. In concordance with laboratory observations of attenuated gaze aversion by frightened mouse lemurs, the more fear-motivated lemurs in the present experiments exhibited reduced differential model inspection. The affinity between these findings implies, perhaps, that fear-motivation increases the tendency to engage in less selective investigative gazing as the animal shifts into a protective behavior mode. This as well as any other functional interpretation of the role of gaze behavior during agonistic encounters, however, awaits further experimental support.
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.
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.
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.
In this paper we report the results of our first efforts to evaluate the functional significance to signaler and perceiver of variation in tail flagging (Fig. 1 and Fig. 2A-C) by California ground squirrels (Spermophilus beecheyi). We first report a series of anecdotes in which we describe the circumstances of a variety of tail movements by California ground squirrels, including the different kinds of tail flagging. Secondly and primarily we identify the information afforded by snake-elicited tail flagging. Tail flagging is a signal used by California ground squirrels primarily when they are harassing a potential snake predator (Fig. 4). It attracts other squirrels who may also begin harassing the snake. The risk to squirrels in encounters with snakes continuously varies, and the squirrels adjust their behavior accordingly. Consequently in this situation we expected to find shifts in the information afforded by different tail-flagging variants. We view the information afforded by tail movement and other signals as a consequence, not of selection for making that information available, but of the correlations resulting from situational constraints on the signaler's behavior, e.g., correlations between tail movement variation and variation in significant events. We used two complementary approaches to help determine the information afforded by tail flagging. In one, we asked whether information important to percipients is afforded by tail flagging. In the second, we searched for situational correlates of tail-flagging variants. We applied the second approach to each individual separately and to the group comprising these individuals. This allowed us to look for idiosyncrasies in signaler behavior. Although a relatively simple signal, tail flagging varies along several structural and temporal parameters. From video recordings we quantified a structural parameter- number of movement cycles in a bout of tail flagging - and two temporal parameters- rate and temporal clustering of tail flagging. Our results show that squirrels adjust their tail-flagging behavior in the following ways. 1. When a rattlesnake rattles, harassing squirrels increase the number of cycles per bout of tail flagging. 2. Lone snake-directed squirrels temporally clump their flagging bouts more than snake-directed squirrels accompanied by other snake-directed individuals. 3. The structure of flagging varied with the squirrel's behavior vis-a-vis the snake. While dealing directly with a snake, squirrels emitted relatively few 1-cycle bouts of flagging. While in the vicinity and monitoring snake-related events, but engaged primarily in other activities such as feeding or grooming, squirrels emitted relatively greater numbers of 1-cycle bouts. As one would predict from this difference, individuals were farther from the snake on the average while emitting 1-cycle bouts than while emitting 2-cycle bouts. Adults used far more 2-cycle bouts than 1, and 3 or higher. In the field, bouts of 4-cycles or greater were very rare. We found that the information afforded by a bout of tail flagging was much greater when we considered structural variation, than when we did not. For example, flaggers were more likely on the average to "pause" before than after tail flagging. However, although the same difference held for 1-cycle bouts, just the reverse was true for 3-cycle bouts, and there was little difference in the probability of pausing for 2-cycle bouts. We found similar differences for other behavioral correlates of tail flagging. A percipient could much more precisely predict a tail flagger's behavior by considering signal variation. Our results indicate a percipient can infer from a high proportion of 3-cycle bouts that the flagger is beginning an episode of snake-directed activity, whereas 1-cycle bouts indicate a temporary cessation of snake-directed behavior. We expect to find even greater situational specificity of tail flagging when we simultaneously consider multiple structural dimensions, such as axis of movement and number of cycles. When we looked at the information afforded by a bout of tail flagging separately for individual squirrels, it was clear that the specific behavioral profiles associated with different variants of tail flagging were somewhat idiosyncratic. Thus, a percipient squirrel should be able to infer more from the tail flags of a familiar squirrel than an unfamiliar squirrel. We propose that signals are used to elicit a particular kind of performance from the target(s). The effectiveness of such action depends upon a knowledge of the current status of the individual's target(s). We conclude that variation in tail flagging is constrained in at least three ways: 1) by the number and quality of targets of tail flagging (e.g., snakes, squirrels); 2) by the signaler's certainty about the status of the target(s) (by eliciting behavior in targets, tail flagging may be used in part to extract information about the target's state); and 3) by the quality and availability of feedback (the success of tail flagging is continually assessed on the basis of feedback). The understanding of the functional significance of tail flag variability therefore becomes the problem of understanding how the flagger uses signal adjustments to deal with changes in its circumstances in terms of these three general constraints.