Preferential snake detection in a simulated ecological experiment.

OBJECTIVES: According to Isbell's snake detection theory (SDT), the need to rapidly detect and thus avoid snakes had a major impact on the evolution of the primate visual system, and thus the origin and evolution of the primate lineage, as expansion of the visual sense is a key characteristic of primates. The SDT rests on the assumption that there are both cortical (conscious) and subcortical (unconscious) brain structures and pathways that are responsible for rapid visual detection of and quick avoidance reactions to snakes. Behavioral evidence for the SDT primarily comes from visual search tasks and presentations of images on a computer screen; our aim was to evaluate the SDT under more ecologically valid circumstances. MATERIALS AND METHODS: We asked participants to take a virtual hike in which a realistic model of a snake, rabbit, or bottle had been placed on the trail. Subjects were instructed simply to imagine themselves as the hiker while watching the video. We measured heart rate and skin conductance reactions while the participants viewed the video. After the video, the participants were shown pictures of the three stimuli and asked if they had seen any of them. RESULTS: We found that snakes were detected more often than rabbits or bottles, and that participants showed greater changes in heart rate and greater skin conductance responses in the snake condition than in the other two conditions, even when the participant did not report having seen the snake. DISCUSSION: A critical component of the SDT is that primates must be able to quickly detect snakes even when their attention is directed elsewhere. Using a novel experimental context-a simulated hike-we assessed arousal and detection without directing participants to attend to any particular stimulus or event. Our data support the SDT by providing evidence of enhanced detection and autonomic arousal even in the absence of detection. Replication of these results using additional controls and experimental contexts will help refine our understanding of snake avoidance by primates.

Scratching under positive and negative arousal in common marmosets (Callithrix jacchus).

Scratching has been widely used as an indicator of anxiety in many primate species. However, a handful of studies have shown no change in scratching under anxiety-provoking circumstances. In addition, the existing literature has investigated scratching only in relation to negative arousal (i.e., anxiety), even though anxiety and excitement (positive arousal) share important physiological and behavioral correlates, including increased heart rate, blood pressure, and locomotion. In the current study, we scored all instances of scratching in 11 outdoor-housed captive common marmosets (Callithrix jacchus) during three contexts that were intended to be negatively arousing and three contexts that were intended to be positively arousing during a baseline, manipulation, and post-induction period. Summed across the three negative arousal contexts, the results showed that subjects exhibited significantly lower scratching rates during the manipulation than during either the baseline or post-induction periods, and the pattern of means was the same for all three of those contexts. Under the three contexts of positive arousal, subjects exhibited different patterns of scratching rates during the manipulation periods (play = increases, foraging = decreases, food anticipation = no change). Data from the current study, and a close examination of data from studies showing no change in scratching under anxiety-provoking circumstances, suggest that the anxiety-scratching relationship may be more complex than has been reported previously. Our results raise a potential concern about the unchallenged use of scratching as a behavioral indicator of anxiety in captive non-human primates, with important implications for welfare and management of these species.

Patterns on serpentine shapes elicit visual attention in marmosets (Callithrix jacchus).

Given the prevalence of threatening snakes in the evolutionary history, and modern-day environments of human and nonhuman primates, sensory, and perceptual abilities that allow for quick detection of, and appropriate response to snakes are likely to have evolved. Many studies have demonstrated that primates recognize snakes faster than other stimuli, and it is suggested that the unique serpentine shape is responsible for its quick detection. However, there are many nonthreatening serpentine shapes in the environment (e.g., vines) that are not threatening; therefore, other cues must be used to distinguish threatening from benign serpentine objects. In two experiments, we systematically evaluated how common marmosets (Callithrix jacchus) visually attend to specific snake-like features. In the first experiment, we examined if skin pattern is a cue that elicits increased visual inspection of serpentine shapes by measuring the amount of time the marmosets looked into a blind before, during, and after presentation of clay models with and without patterns. The marmosets spent the most time looking at the objects, both serpentine and triangle, that were etched with scales, suggesting that something may be uniquely salient about scales in evoking attention. In contrast, they showed relatively little interest in the unpatterned serpentine and control (a triangle) stimuli. In experiment 2, we replicated and extended the results of experiment 1 by adding additional stimulus conditions. We found that patterns on a serpentine shape generated more inspection than those same patterns on a triangle shape. We were unable to confirm that a scaled pattern is unique in its ability to elicit visual interest; the scaled models elicited similar looking times as line and star patterns. Our data provide a foundation for future research to examine how snakes are detected and identified by primates. Am. J. Primatol. 78:928-936, 2016. © 2016 Wiley Periodicals, Inc.

Social learning in captive African elephants (Loxodonta africana africana).

Social learning is a more efficient method of information acquisition and application than trial and error learning and is prevalent across a variety of animal taxa. Social learning is assumed to be important for elephants, but evidence in support of that claim is mostly anecdotal. Using a herd of six adult female African bush elephants (Loxodonta africana africana) at the San Diego Zoo's Safari Park, we evaluated whether viewing a conspecific's interactions facilitated learning of a novel task. The tasks used feeding apparatus that could be solved in one of two distinct ways. Contrary to our hypothesis, the method the demonstrating animal used did not predict the method used by the observer. However, we did find evidence of social learning: After watching the model, subjects spent a greater percentage of their time interacting with the apparatus than they did in unmodeled trials. These results suggest that the demonstrations of a model may increase the motivation of elephants to explore novel foraging tasks.

A foraging advantage for dichromatic marmosets (Callithrix geoffroyi) at low light intensity.

Most New World monkey species have both dichromatic and trichromatic individuals present in the same population. The selective forces acting to maintain the variation are hotly debated and are relevant to the evolution of the 'routine' trichromatic colour vision found in catarrhine primates. While trichromats have a foraging advantage for red food compared with dichromats, visual tasks which dichromats perform better have received less attention. Here we examine the effects of light intensity on foraging success among marmosets. We find that dichromats outperform trichomats when foraging in shade, but not in sun. The simplest explanation is that dichromats pay more attention to achromatic cues than trichromats. However, dichromats did not show a preference for foraging in shade compared with trichromats. Our results reveal several interesting parallels with a recent study in capuchin monkeys (Cebus capucinus), and suggest that dichromat advantage for certain tasks contributes to maintenance of the colour vision polymorphism.

Does Rattling Deter? The Case of Domestic Dogs.

Although the rattling of rattlesnakes (Crotalus and Sistrurus) is widely accepted as being aposematic, the hypothesis that rattling deters approach from the snake's potentially dangerous adversaries has not been well tested. In a controlled study using rattling recorded from captive rattlesnakes (C. oreganus helleri) and a variety of comparison sounds or no-sound controls, domestic dogs (Canis familiaris) showed no hesitation to approach camouflaged speakers projecting the recorded rattles. The dogs were equally likely to approach speakers projecting rattling as they were to approach speakers playing control sounds, or speakers that were silent. Furthermore, the dogs spent no less time in front of the speakers projecting the rattles than they did in front of speakers projecting control sounds or no sound. The dogs' reactions may not be representative of other species with whom rattlesnakes come into contact, but the data suggest a need for some circumspection about the role of rattling in the rattlesnake's defensive repertoire. Our results also suggest that dogs may be vulnerable to envenomation because they fail to react to the sound of rattling with avoidance.

Hand preference predicts reactions to novel foods and predators in marmosets (Callithrix geoffroyi).

In chimpanzees (Pan troglodytes) and common marmosets (Callithrix jacchus), left-handed individuals are less likely than right-handed individuals to explore new objects and situations, suggesting a relationship between the hemispheric specialization of emotional states and motor function. To further explore this relationship and to test the hypothesis that fearfulness is related to hand preference, we assessed willingness to approach, sniff, and taste novel foods, and the duration of freeze reactions in response to hawk calls, in 18 Geoffroy's marmosets (Callithrix geoffroyi). In accordance with these hypotheses, left-handed marmosets were slower to explore novel foods and slower to emerge from a freeze response than right-handed marmosets. Hand preference and at least some features of temperament seem to be related in this and other species of primates.

Vigilance, vocalizations, and cryptic behavior at retirement in captive groups of red-bellied tamarins (Saguinus labiatus).

Frequent references are made to presumed antipredator adaptations exhibited by callitrichids, but there are very few systematic investigations of these behaviors. One set of untested presumptions stems from observations that callitrichids become especially vigilant and cryptic prior to retirement each evening. This hypothesis was tested in the current study by quantifying the rates of vocalizations and extragroup behavior at various times of the day. Using two groups of captive red-bellied tamarins, it was demonstrated that these primates do become relatively more quiet and more attentive to the nonsocial environment prior to retirement each evening, culminating in virtual silence once the nest box has been entered. While the adaptive significance of these phenomena has not yet been tested, it is likely that the behaviors reduce vulnerability to predation.

Visual monitoring of threatening objects by captive tamarins (Saguinus labiatus).

Captive social groups of red-bellied tamarins (Saguinus labiatus) were observed in the presence of threatening, inanimate objects. The tamarins monitored the stimuli over the course of the 20-minute trials by conducting brief, periodic visual checks of the objects. The average number of checks per subject per trial was stable both across trials and between groups, and individual differences in rates varied relatively little around the group means. These data generate the hypothesis that there is a species-typical execution of vigilance in the presence of mildly threatening objects. This execution takes the form of brief visual inspections of the stimulus, usually by one tamarin at a time, at a fairly consistent rate. The discussion of the data takes place in the context of the behavioral ecology of callitrichid species.

Evidence for a "monitoring call" in red-bellied tamarins.

In addition to a variety of calls whose functions are to increase or decrease space among individuals, many species of primates use one or more vocalizations that are emitted in no one particular context and elicit no one particular response. Although investigators have given this type of vocalization a number of different names (e.g., contact call, cohesion call), what these calls seem to have in common is that 1) they allow individuals to monitor the general whereabouts of groupmates and 2) they somehow contribute to group cohesion. Neither of these assumptions has been tested, however. In the red-bellied tamarin (Saguinus labiatus), a vocalization we call the "slide" appears to be a monitoring call. In the current study we tested three hypotheses about the slide call: 1) If slide calls are not direct requests for action, there should be no reliable correlation between slide calls and movement toward or away from the slide caller; 2) if slide calls are emitted to monitor groupmates' whereabouts, they should occur at comparatively low rates when the presence of groupmates can easily be affirmed by visual means (e.g., when the animals are confined in a small space); 3) if slide calls contribute to intragroup cohesion, they should be produced at comparatively high rates during activity that requires coordinated behavior. Each of these predictions was supported. Although variants of the call and/or additional functions of the call(s) may emerge from further testing, social monitoring appears to be at least one important function of the slide calls of red-bellied tamarins, especially in circumstances where coordinated and/or cohesive behavior is required of the group.

Personality traits of adolescent pig-tailed monkeys (Macaca nemestrina): An analysis of social rank and early separation experience.

Personality ratings of ten adolescent pig-tailed macaques (Macaca nemestrina) were carried out by three experienced observers who used a simple three-point rating system. A modification of Stevenson-Hinde & Zunz's [1978] procedure, the agreement between raters on each of 21 traits was evaluated. When correlated with social rank, it was shown that dominant animals were rated as being, for example, confident, effective, and opportunistic. Subordinant monkeys were rated as insecure and dependent. Rank correlated negatively, however, with observers' impressions of popularity. Subjects who had undergone a brief maternal separation were rated as less sociable than their nonseparated counterparts. Furthermore, rank-related traits corresponded well with the three personality components that were derived by Stevenson-Hind & Zunz [1978]; this suggested that clusters of traits reliably accompanied and/or contributed to the attainment of social rank.

Following the rules: why small groups of tamarins do not reconcile conflicts.

Reconciliation is the post-conflict friendly reunion between opponents. A series of conditions and rules in order for reconciliation to take place has been recently proposed. One critical condition is that the relationship between opponents must be disrupted. We tested this condition using post-conflict and matched-control observations on 4 small groups of tamarins (Saguinus labiatus). Our previous lack of evidence for reconciliation was confirmed. No post-conflict relationship damage was therefore expected. We found evidence that relationships were disturbed following conflicts over food but, as in other primates, no evidence for reconciliation following such conflicts was found. For non-food-related conflicts there was no evidence that relationships were disturbed, as opponents were in close proximity to each other and resumed the exact same activity as frequently in the post-conflict observations as they did in the matched-control observations. We conclude that 'everyday' aggression may not disrupt the relationships among individuals from the same family group and therefore reconciliation is not needed.

Pre-retirement predator encounters alter the morning behavior of captive marmosets (Callithrix geoffroyi).

Limited data are available on the long-term effect an encounter with a predator has on its potential prey. Anecdotal reports from field research indicate that even unsuccessful attacks by predators on callitrichids have long-lasting effects. The subjects for this study were two groups of Geoffroy's marmosets (Callithrix geoffroyi) housed outside, off exhibit, at the Center for Reproduction of Endangered Species at the San Diego Wild Animal Park. Before they retired in the evening, the marmosets were observed under one of three conditions: snake model, cloth control, and no-stimulus control. Data were collected the following morning for 1 hr after the animals emerged from the sleeping box. Compared to control conditions, exposure to the snake model before retirement the previous evening was associated with significantly more vigilance checks (i.e., inspecting the area where the stimulus was last seen), and a delay in beginning to forage on the ground. These results suggest that callitrichids use recent threatening experiences to guide their vigilance behavior 12 hr after the threat is detected, and that they adjust their early morning behavior in response to potential predatory threats.

Hawk calls elicit alarm and defensive reactions in captive Geoffroy's marmosets (Callithrix geoffroyi).

Most descriptions of callitrichid antipredator behavior have come from observations of visual encounters with predators, but there is also anecdotal evidence suggesting that callitrichids may use auditory cues associated with raptors for the early detection of potential danger. In the present study, Geoffroy's marmosets consistently reacted to the tape-recorded calls of a red-tailed hawk (Buteo jamaicensis) with high-intensity antipredator behaviors. Compared to the taped calls of a raven (Corvus corax) and the taped sound of a power drill, the hawk calls elicited more startle reactions, more alarm calls, longer freeze times, increased use of safe areas of their enclosure and greater disruption in ongoing behavior. Once in a relatively safe location in the enclosure, the marmosets visually monitored the site of origin of the calls for 10 min and minimized locomotion for 30 min, but resumed baseline levels of other activities that had been disrupted by the hawk calls. Marmosets may use the auditory cues associated with predators for early detection, and subsequent avoidance, of a potential predator in the vicinity.