Age‐specific functions of Stone Handling, a solitary‐object play behavior, in Japanese Macaques (Macaca fuscata)

Abstract

Stone handling (SH) in Japanese macaques, a form of solitary-object play, is newly acquired only by young individuals, and is the first example of a directly nonadaptive behavior that is maintained as a behavioral tradition within free-ranging provisioned social troops. We report here the first systematic investigation of this behavior in a stable captive social troop, the Takahama troop, which is housed in an outdoor enclosure of the Primate Research Institute (PRI), Kyoto University, Japan. This study was conducted to evaluate relevant competing hypotheses regarding the function of object play (e.g., misdirected foraging behavior and motor training) to explain the proximal causes and ultimate function(s) of SH. The "misdirected foraging behavior" hypothesis can be ruled out because of the lack of a clear temporal relationship between feeding and the occurrence of SH in any age class. Age-related differences in SH performance and behavioral patterns were observed, suggesting possible differences in the immediate cause and ultimate function between young and adults. Young individuals engaged in frequent bouts of short duration, involving locomotion and vigorous body actions throughout the day, which is typical for play by young in general. This pattern of behavior is consistent with the motor training hypothesis, which states that play occurs during the development of motor and perceptual skills and is thus potentially critical for neural and cognitive development. This practice is continued by those who acquire it at an early age, with adults engaging in significantly fewer but longer bouts that involve more stationary, complex manipulative patterns, almost exclusively in the late afternoon. We propose that for adults, at the proximate level SH is psychologically relaxing, but ultimately functions to maintain and regenerate neural pathways, and potentially helps to slow down the deterioration of cognitive function associated with advanced age in long-lived provisioned and captive macaques.

Behavior Systems Approach to Object Play: Stone Handling Repertoire as a Measure of Propensity for Complex Foraging and Percussive Tool Use in the Genus Macaca

“…In line with the "surplus energy" hypothesis, proposing that play behavior enables the adaptive expenditure of excess metabolic energy, SH bouts in juveniles (often not limited in energy) were more frequent, versatile, and vigorous, but shorter, than in adults (Leca et al, 2007). Consistent with the "motor training" hypothesis, SH could have beneficial consequences both in immature individuals by allowing a faster development of manipulative skills (Nahallage & Huffman, 2007a) and in senescent individuals by maintaining neural pathways through the daily practice of fined-tuned manual activity, and potentially slowing down the deterioration of sensorimotor and cognitive abilities associated with advanced age . Additionally, even though the "misdirected foraging" hypothesis was not supported in a captive group of Japanese macaques (Nahallage & Huffman, 2007a), it was supported in all free-ranging provisioned groups of this species, where there was a clear temporal connection between SH occurrence and the post-provisioning period (Leca et al, 2008a).…”

“…Consistent with the "motor training" hypothesis, SH could have beneficial consequences both in immature individuals by allowing a faster development of manipulative skills (Nahallage & Huffman, 2007a) and in senescent individuals by maintaining neural pathways through the daily practice of fined-tuned manual activity, and potentially slowing down the deterioration of sensorimotor and cognitive abilities associated with advanced age . Additionally, even though the "misdirected foraging" hypothesis was not supported in a captive group of Japanese macaques (Nahallage & Huffman, 2007a), it was supported in all free-ranging provisioned groups of this species, where there was a clear temporal connection between SH occurrence and the post-provisioning period (Leca et al, 2008a). Despite sometimes conflicting results, these alternative hypotheses are not mutually exclusive; they suggest that SH could be underlain by various motivational, cognitive, and maturational processes depending on the age class and the context in which this activity occurs.…”

“…Understanding the motivations underlying object play behavioral patterns, specifically SH actions that are performed throughout the lifespan, can offer insight into the fitness consequences of playful activities. Because SH is routinely performed by both young individuals and adults, health-related and welfare benefits of this behavior have been suggested (see Nahallage & Huffman, 2007a;Nahallage et al, 2016).…”

Sex differences in the stone tool‐use behavior of a wild population of burmese long‐tailed macaques (Macaca fascicularis aurea)

“…Research on individual variation in stone handling across Japan has not shown any stable sex differences across ten groups in stone use patterns [Leca et al, 2007a]. However, in a different study on a single group, adult females handled stones less frequently and performed fewer types of patterns [Nahallage & Huffman, 2007a]. Developmental changes do occur in stone use [Leca et al, 2007b], and learning the behavioral acts appears to be socially mediated [Huffman, 1984[Huffman, , 1996Huffman et al, 2008;Nahallage & Huffman, 2007b].…”

Brincar na perspectiva psicoetológica: implicações para pesquisa e prática

“…The second example was extracted from a set of articles by Michael Huffman (Huffman, 1984;Huffman & Quiatt, 1986;Nahallage & Huffman, 2007 about play with stones in four groups of Macaca fuscata in captivity and in 11 groups in the wild. This form of play consists of repetitive handling of stones: scattering and gathering, rolling from one hand to another, hitting one stone against another with a clacking noise, crashing them into the substrate, rubbing, throwing, dropping them in the water, washing, wrapping with leaves, using a stone as grooming tool, running and throwing.…”