Stress behaviors in captive robust capuchins: Effects of humidity, visitors, management and sex

Abstract

Wild robust capuchins (Sapajus spp.) are omnivorous neotropical primates that live in relatively large groups in extensive home and daily ranges with activity budgets dominated by traveling, foraging, and object manipulation, meaning that enclosed spaces can result in significant deprivation. Space restriction, manipulation by caretakers, and the chronic presence of visitors, can disrupt the animals' welfare, altering their normal activities and inducing stress behaviors. We aimed to study the behavioral repertoire, activity budget, and frequency of stress behaviors (stereotypes and self-directed behaviors) between two captive groups of robust capuchins in a public zoo in Foz do Iguaçu, Brazil, to understand how much their behavioral homeostasis has been affected. More specifically, we assessed the effect of environmental variables (temperature, relative air humidity, number of visitors, and food management) and sex on the frequency of stress behaviors. Capuchins showed a high frequency of stress behaviors, which represented around 10% of their activity budget (though the frequencies were unevenly distributed among the individuals), and traveling was positively correlated with stereotypes. We found that high relative air humidity appears to induce more stereotypes, high numbers of visitors appear to increase self-directed and vigilance behaviors and reduce stereotypes, food management can increase both kinds of stress behaviors, and females demonstrated more frequent stress behaviors than males, but individual variation may play a role. Capuchins in the group with a greater space restriction showed more stereotypes, while those in the group with more individuals showed more selfdirected behaviors. Our study shows that the stress behaviors performed by the capuchins are complex and it is difficult to determine a single cause, because many traits could be involved. Despite that, this study enlightens us to direct some approaches to help these animals to meet their ecological and social needs, mitigating their stress.

Urine washing in urban robust capuchin monkeys (Sapajus sp.): The relation with visitors

“…Interestingly, we found a positive and significant relationship between the daily number of people observed in the fragment and UW—but not between the daily number of human‐monkey interaction and UW, nor between the interaction of these two predictive variables and UW—which indicates people as a direct or at least as an indirect stimulus for our capuchins to display more UW. At first sight, our findings could indicate that the animals use UW behavior to relieve stress caused directly by the presence of people, who are known to be a source of stress for capuchins, even when these animals are used to the presence of visitors (de la Barrera Cardozo et al, 2021; Sherwen et al, 2015). People can also cause stress indirectly, because the food they provide can increase the disputes between the monkeys (Hsu et al, 2009; Ram et al, 2003).…”

“…Social hypotheses propose that monkeys perform UW to communicate about sexual condition (Boinski, 1992; Campos & Fedigan, 2013; Jones, 2003; Miller et al, 2008; Milton, 1985; Phillips et al, 2011; Strier, 2021), to demarcate an area (Campos & Fedigan, 2013; Charles‐Dominique, 1977; Milton, 1975), to communicate an identity or hierarchical status that facilitate the assessment of quality, promoting the possibility of decreasing the likelihood of aggression, appeasing social conflicts (Fragaszy et al, 2004; Heymann, 1995; Jones, 2003; Milton, 1975; Oppenheimer & Oppenheimer, 1973; Ueno, 1994), or to relieve tensions after agonisms, when the victim's anxiety levels typically increase and it could displays UW as a displacement behavior (Jones, 2003; Miller et al, 2008; Milton, 1975, 1985; Strier, 2021). Interestingly, if UW serves to relieve tensions, UW itself could be viewed as a behavioral indicator of disruption in the animals’ welfare ( sensu Berger‐Tal et al, 2011), since frequent displacement behaviors is an indication of animal stress (e.g., de la Barrera Cardoso et al, 2021). However, various studies have refuted the role of UW in sexual function (Carnegie et al, 2005; Carosi et al, 2005; Roeder & Anderson, 1991; Schino et al, 2011), demarcation (Campos & Fedigan, 2013; Carosi et al, 2005; Heymann, 1995; Roeder & Anderson, 1991), hierarchy (Schino et al, 2011), and appeasement (Roeder & Anderson, 1991).…”

“…Robust capuchins can be found in small green urban areas (Aguiar et al, 2014), where they must deal with new stimuli and pressures, including frequent contact with humans (Back et al, 2019; Suzin et al, 2017). People can be considered a potential threat and stress source for different primate species, including capuchins, that may affect their welfare (Bryson‐Morrison et al, 2017; de la Barrera Cardozo et al, 2021; Hosey, 2000; Sherwen et al, 2015). However, people can also be viewed as a food source (Suzin et al, 2017), though food competition can increase due to human provisioning (Hsu et al, 2009; Ram et al, 2003).…”

Automatically detecting stereotyped behaviors from surveillance videos of zoos and animal reserves for captive animal welfare

“…Focal animal sampling was used for descriptive analysis of 70 hours of behavior observation [11]. Wagner et al observed the behavior of capuchin monkeys in the public Zoo of Vers-Duifen, Brazil, for 40 days to determine the frequency of stereotypical behavior and self-orientation and to analyze the effects on behavioral stability [12]. In addition to zoos, the stereotypical behavior of monkeys in research facilities was observed and analyzed [13].…”