Social interactions and activity patterns of old Barbary macaques: Further insights into the foundations of social selectivity

Abstract

Human aging is accompanied by a decrease in social activity and a narrowing in social networks. Studies in nonhuman primates may provide valuable comparative insights in which way aging impacts social life, in the absence of cultural conventions and an awareness of a limited lifetime. For female Barbary macaques at "La Forêt des Singes" in Rocamadour, France, we previously reported an age-associated decrease in active grooming time and network size. Here, we aimed to extend these findings by investigating in which way physical decline, spatial proximity, and aggression vary with age in female Barbary macaques. We analyzed >1,200 hr of focal observations for 46 females aged 5-29 years. As expected, older females engaged less frequently in challenging locomotor activity, such as climbing or running, than younger ones. The previously reported decrease in grooming time was not due to shorter grooming bout duration. Instead, active grooming bouts lasted even longer, which discounts the idea that manual fatigue explains the shift in grooming pattern. We found that older females tended to be spatially reclusive and that they were less frequently the targets of aggression. Although older females showed aggressive behaviors at similar rates as younger females, the proportion of low-level aggression (i.e., threats) increased with age. We suggest that these threats are not simply a signal of dominance, but also function to deter approaches by others. Overall, these findings are in line with the idea that older females aim to avoid potentially negative interactions, specifically if these are costly. In sum, these findings support the idea that shifts in female Barbary macaques' grooming activity, do not simply result from physical deterioration, but are instead due to a higher selectivity in the choice of social partners.

Differential ageing trajectories in motivation, inhibitory control and cognitive flexibility in Barbary macaques (Macaca sylvanus)

“…Changes in activity patterns with increasing age might add to the decrease in motivation to participate and persist. Considering the time spent on highly energetic activities like running, climbing and jumping, a study on Barbary macaques found an age-related decline, suggesting that older monkeys were less physically able or less motivated to engage in such activities [30]. The exploration of the tasks in our study also required physical engagement to obtain the reward.…”

Deficits in Social Behavior Precede Cognitive Decline in Middle-Aged Mice

“…Similarly, behavioral studies in rodents have also shown a decrease in social interactions (Salchner et al, 2004) or social recognition memory with age (Prediger et al, 2005; Markham and Juraska, 2007). In the same line, it has been reported that older female macaques spend less time in close proximity to others and engage in fewer social interactions (Corr, 2003; Almeling et al, 2016, 2017). Together, these observations indicate that animal models can reproduce some of the age-related social cognitive deficits in humans and can help to better understand the neural correlates of such a decline.…”

Shifting sociality during primate ageing

“…This phenomenon has been best-studied among female-philopatric Old World monkeys, where females remain in their natal group and males disperse. For example, older rhesus macaques ( Macaca mulatta ) [25], stump-tailed macaques ( Macaca arctoides ) [26], Japanese macaques ( Macaca fuscata ) [26–30], long-tailed macaques (sometimes called crab-eating macaques; Macaca fascicularis ) [31,32] and Barbary macaques ( Macaca sylvanus ) [18,23] all exhibit reduced social engagement in terms of spatial distance to others, time spent alone, approaching others or total network size. While there has been less work examining psychological mechanisms, older rhesus macaques also show a declining propensity to follow other's gaze [19,20].…”

“…Older rhesus macaques show these changes in giving grooming and aggression even though older individuals continue to receive grooming from others at high rates, and are less likely themselves to be attacked [13,25,42,49]. Similarly, older Barbary macaques [18,23], long-tailed macaques [32], bonnet macaques [38] and Japanese macaques [24,27,29,30] also show declines in grooming given but initiate aggressive behaviours like younger adults. Macaques show similar shifts in their production of and responses to negative emotional signals or contexts: the production of negative emotional signals such as yawning and scratching increases in older adults [32]; production of conspecific threat signals generally stays consistent or increases in adult animals [42,50]; and older macaques can show exacerbated responses to external threats in controlled experiments [47].…”

“…For example, a fair amount of research on macaque species has focused on provisioned populations [e.g. 13,18,19,23–29,48,111,122,124,126,127], which may show different ageing patterns from the wild owing to socioecological effects.…”