Snake Species Discrimination by Wild Bonnet Macaques (<i>Macaca radiata</i>)

Ramakrishnan, Uma; Coss, Richard G.; Schank, Jeffrey C.; Dharawat, Amita; Kim, Susan

doi:10.1111/j.1439-0310.2004.01063.x

Cited by 42 publications

(62 citation statements)

References 44 publications

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“…Infant monkeys with bilateral neurotoxic lesions of the superior colliculus continue to reach for food in the presence of a snake model, whereas shamoperated monkeys avoid the food (21). Evasive movements such as these are typical of animals that are surprised or threatened by others (22,23). The pulvinar is also connected to the amygdala (24).…”

Section: Discussionmentioning

confidence: 99%

Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

Isbell

Matsumoto

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

229

157

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Snakes and their relationships with humans and other primates have attracted broad attention from multiple fields of study, but not, surprisingly, from neuroscience, despite the involvement of the visual system and strong behavioral and physiological evidence that humans and other primates can detect snakes faster than innocuous objects. Here, we report the existence of neurons in the primate medial and dorsolateral pulvinar that respond selectively to visual images of snakes. Compared with three other categories of stimuli (monkey faces, monkey hands, and geometrical shapes), snakes elicited the strongest, fastest responses, and the responses were not reduced by low spatial filtering. These findings integrate neuroscience with evolutionary biology, anthropology, psychology, herpetology, and primatology by identifying a neurobiological basis for primates' heightened visual sensitivity to snakes, and adding a crucial component to the growing evolutionary perspective that snakes have long shaped our primate lineage.evolution | Snake Detection Theory | visual responses | low-pass filtered images S nakes have long been of interest to us above and beyond the attention we give to other wild animals. The attributes of snakes and our relationships with them have been topics of discussion in fields as disparate as religion, philosophy, anthropology, psychology, primatology, and herpetology (1, 2). Ochre and eggshells dated to as early as 75,000 y ago and found with cross-hatched and ladder-shaped lines (3, 4) resemble the dorsal and ventral scale patterns of snakes. As the only natural objects with those characteristics, snakes may have been among the first models used in representational imagery created by modern humans. Our interest in snakes may have originated much further back in time; our primate lineage has had a long and complex evolutionary history with snakes as competitors, predators, and prey (1). The position of primates as prey of snakes has, in fact, been argued to have constituted strong selection favoring the evolution of the ability to detect snakes quickly as a means of avoiding them, beginning with the earliest primates (2, 5). Across primate species, ages, and (human) cultures, snakes are indeed detected visually more quickly than innocuous stimuli, even in cluttered scenes (6-11). Physiological responses reveal that humans are also able to detect snakes visually even before becoming consciously aware of them (12). Although the visual system must be involved in the preferential ability to detect snakes rapidly and preconsciously or automatically, the neurological basis for this ability has not yet been elucidated, perhaps because an evolutionary perspective is rarely incorporated in neuroscientific studies. Our study helps to fill this interdisciplinary gap by investigating the responses of neurons to snakes and other natural stimuli that may have acted as selective pressures on primates in the past.Here, we identify a mechanism for the visual system's involvement in rapid snake detection by measurin...

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Section: Discussionmentioning

confidence: 99%

Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

Isbell

Matsumoto

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

229

157

View full text Add to dashboard Cite

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“…Alarm calling is further evidence that primates evolved in the presence of predators, and is also employed differently from species to species. It was shown that vervet monkeys and bonnet macaques have the ability to define species within classes of predators (Seyfarth et al 1980;Ramakrishnan et al 2005), while Diana monkeys also respond differently based on predator hunting style (Zuberbuhler et al 1997). This is evidence that each species has evolved specific mechanisms that are likely suited to the specific needs of their own environments.…”

Section: Resultsmentioning

confidence: 99%

“…Similarly, Ramakrishnan et al (2005) found bonnet macaques can distinguish between venomous, nonvenomous and predatory snakes. The macaques responded with caution to all snake species, but pythons (Python molurus), the only snakes known to consume bonnet macaques, were the only species that elicited alarm calls (Ramakrishnan et al 2005). This shows that bonnet macaques have the ability to distinguish between snake species, as their main predator prompted the most active response.…”

Section: Alarm Callingmentioning

confidence: 89%

“…By using specific alarm calls, vervet monkeys respond according to the threat and hunting style they believe they were faced with (Seyfarth et al 1980). Similarly, Ramakrishnan et al (2005) found bonnet macaques can distinguish between venomous, nonvenomous and predatory snakes. The macaques responded with caution to all snake species, but pythons (Python molurus), the only snakes known to consume bonnet macaques, were the only species that elicited alarm calls (Ramakrishnan et al 2005).…”

Section: Alarm Callingmentioning

confidence: 97%

“…This behaviour is employed differently across primate species and can be used to signal threats to the group, including predator classification and to deter predators (Seyfarth et al 1980;Zuberbuhler et al 1997;Ramakrishnan et al 2005). It is thought that vigilance and alarm calling have both positive and negative effects on groups and individuals, and are utilised differently across primate species.…”

Section: Introductionmentioning

confidence: 99%

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Dealing with predators: Vigilance and alarm calling in primates

Raff¹

2017

The Human Voyage

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Predation is considered one of the most important selective pressures on animals. Evidence of predation on primates is particularly rare; however, it is thought that it has been a major selective force for many species in the primate order. This can be seen through the occurrence and application of vigilance and alarm calling in many primate species. Studies of vigilance have shown that animals have a tendency to decrease individual vigilance as group size increases. However, it has been found that primates do not fit this model, and either maintain or increase their individual vigilance as group size increases. A likely reason for the maintenance of individual vigilance is that primates utilise this behaviour as both a form of antipredation behaviour and social monitoring; thus it largely depends on the social structure of the species and the environmental conditions of the ecosystem being occupied by a primate group. Another antipredator behaviour that occurs in primates is alarm calling, which may be to deter predators. The studies presented here show that primates have the ability to distinguish between predators, between and within predator classes and also predator hunting styles. It is believed that the development of these behaviours in the primate order shows that these animals have evolved in environments where predation is a threat.

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Development of Snake‐Directed Antipredator Behavior by Wild White‐faced Capuchin Monkeys: I. Snake‐Species Discrimination

Meno

Coss

Perry

2012

American J Primatol

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Young animals are known to direct alarm calls at a wider range of species than adults. Our field study examined age-related differences in the snake-directed antipredator behavior of infant, juvenile, and adult white-faced capuchin monkeys (Cebus capucinus) in terms of alarm calling, looking behavior, and aggressive behavior. In the first experiment, we exposed infant and juvenile white-faced capuchins to realistic-looking inflatable models of their two snake predators, the boa constrictior (Boa constrictor) and neotropical rattlesnake (Crotalus durissus) and a white airplane as a novel control. In the second experiment, infants, juveniles, and adults were presented photographic models of a coiled boa constrictor, rattlesnake, indigo snake (Drymarchon corais), a noncapuchin predator, and a white snake-like model. We found that antipredator behavior changed during the immature stage. Infants as young as 4 months old were able to recognize snakes and display antipredator behavior, but engaged in less snake-model discrimination than juveniles. All age classes exhibited a lower response to the white snake-like model, indicating that the absence of color and snake-scale patterns affected snake recognition. Infants also showed a higher level of vigilance after snake-model detection as exhibited by a higher proportion of time spent looking and head cocking at the models. Aggressive antipredator behavior was found in all age classes, but was more prevalent in juveniles and adults than infants. This study adds to the knowledge of development of antipredator behavior in primates by showing that, although alarm calling behavior and predator recognition appear at a very young age in capuchins, snake-species discrimination does not become apparent until the juvenile stage.

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Snake Species Discrimination by Wild Bonnet Macaques (Macaca radiata)

Cited by 42 publications

References 44 publications

Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

Dealing with predators: Vigilance and alarm calling in primates

Development of Snake‐Directed Antipredator Behavior by Wild White‐faced Capuchin Monkeys: I. Snake‐Species Discrimination

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