Public awareness of animal welfare in institutions such as zoos and care centers have grown1, many researchers have studied the effects of a captive environment on animal behaviors2,3. Animal welfare in a captive condition is affected by not only individual-level factors, such as personality, genetics, and species characteristics, but also environment-level factors, such as physical environment, social grouping, and enclosure type, which can control the visitor effect4. The visitor effect, which is the influence of the presence and behavior of human visitors on captive animals, has been investigated. Although many studies have shown a negative visitor effect on captive animals5,6,7, there have been some controversial results showing neutral or positive effects8,9,10.
An increase in the number of visitors (visitor density) is associated with a higher rate of visitor-directed vigilance and stress-related behaviors, including visitor- or conspecific-directed aggression, such as among cotton-top tamarins, lemurs, and Diana monkeys (Cercopithecus diana diana) and Western lowland gorillas (Gorilla gorilla gorilla) 8,11. A Previous studies showed that higher visitor density also modifies the activity budget of captive primates. For example, chimpanzees (Pan troglodytes) spend less time on foraging, grooming, and playing12 and Diana monkeys (C. diana diana) on grooming and resting13 if the visitor density in the viewing area increases. Furthermore, a higher visitor density or increased visual contact with visitors may increase stress levels in captive animals. For example, the urinary cortisol levels of captive Colombian spider monkeys (Ateles geoffroyii rufiventris) elevated with increasing visitors14. In contrast, a decrease in the probability of visual contact between animals and visitors reduced glucocorticoid metabolite levels in black-capped capuchins (Cebus apella)15.
However, focusing solely on the visitor density cannot quantify the visitor effect16,17. Visitor behaviors, including talking, shouting, striking the glass partition, and feeding animals, are called visitor attention–getting behaviors (AGBs), which can attract captive animals12. One study on 12 captive primate species reported their consistent locomotion responses toward more active visitors who tried to interact with them18; however, visitor density had no effect. Previous studies have shown that the visitor behavior intensity (effect of visitor behavior on captive animals’ behavior) is as influential as visitor density19,20. Although previous studies have coded the effect of visitor behavior intensity only dichotomously (e.g., passive [none of visitors attracted captive animals’ attention] vs. active [some visitors attracted captive animals’ attention]) 8, research is now considering various visitor behaviors in more detail. For example, specific visitor behaviors, such as shouting, talking, and throwing food, negatively affect the behavior of captive greater rhea (Rhea americana) 21. Aggression in capped langurs (Presbytis pileatus), pigtailed macaques (Macaca numestrina), and olive baboons (Papio anubis) increases when visitors tease them and throw stones or sticks at them22. Considering these negative reactions of captive animals toward visitor behaviors, such as hitting and shouting, it is necessary to investigate the effect of specific visitor behaviors on captive animals in order to improve animal welfare23.
The social setting is one of the prominent variables that can alleviate negative visitor effects that affect animal welfare24,25. Captive animals are often housed in socially isolated conditions for easy management and/or avoiding aggression between individuals26. Therefore, captive animals often experience early social deprivation from their parents or peers, which sometimes results in depression, a lack of social behaviors, self-directed behaviors, and neuroendocrinological issues27,28. As social isolation decreases opportunities for social interaction, it may limit the captive primates’ ability to handle visitor-induced stress through social interactions with conspecifics. Therefore, it is critical to consider the effect of social setting when housing captive animals.
Primates who live together with conspecific individuals (social buffering) show stress alleviation29,30. Rhesus macaques (Macaca mulatta) exhibit less stress-related behavior when socially housed compared to those housed alone31,32. Social buffering can also alleviate stress caused by previous social isolation33. The frequency of stress behaviors is negatively correlated with social behaviors when conspecifics or other captive members are present in the same enclosure, such as cotton-topped tamarins (Saguinus oedipus oedipus) 34 and mangabeys (Cercocebus galeritus chrysogaster) 35.
Gibbons have pair-living social system, and they strengthen their social bonds through social grooming, playing, and duetting36,37. Gibbons also have a high level of social tolerance toward conspecifics, which facilitates strong social bond formation between pair members38. In gibbons, social isolation might limit social interaction with conspecifics, which might affect their capabilities of stress control39. Therefore, we can expect a significant effect of social isolation, along with the visitor effect, on gibbons. Moreover, gibbons are sensitive to exposure to humans, showing increased self-directed behaviors and visitor-directed vigilance40. White-cheeked gibbons (Nomascus leucogenys) show self-directed behaviors more often with a high large number of visitors40, and male white-handed gibbons (Hylobates lar) show territorial behavior with teeth bearing more often with a large number of noisy visitors41. Family units of both siamangs (Symphalangus syndactylus) and white-cheeked gibbons (N. leucogenys) spend more time in an area far away from the visitors’ viewing zone during days of large number of visitors42. In addition, early maternal separation and decrease in social contact with conspecifics increase sexual behaviors, such as masturbation, in eight Hylobates subspecies43. Given these negative reactions to visitors and social isolation of captive gibbons, providing practical solutions and guidelines by examining the visitor effect in relation to the gibbons’ social environment in captivity will contribute to their welfare.
In this study, we investigated the visitor effect in relation to a captive mixed-species gibbon pair comprising a yellow-cheek gibbon (Nomascus gabriellae) and a white-handed gibbon (Hylobates lar). We investigated the effect of visitor behaviors, visitor density, and visitor behavior intensity; the effect of social isolation; and the combined effect of the visitor effect and social isolation on the captive gibbons’ behaviors. We hypothesized that the visitor density and behavior intensity negatively affect the behavior of captive gibbons5,44. We predicted that (1) the visitor effect would affect social interactions by decreasing the spatial distance between the two gibbons to alleviate visitor-induced stress; (2) if the visitor density increases, the frequency of stress-related behaviors would increase and social playing would decrease; and (3) if visitors become more active (e.g., by shouting and striking the glass partition), the gibbons’ visitor-directed vigilance would increase. We also hypothesized that social isolation is negatively related to captive gibbons’ behaviors and will strengthen the negative visitor effect, as it also affects the social setting. We predicted that the two gibbons would exhibit increased stress-related behaviors and visitor-directed vigilance after social isolation. Our findings will contribute to suggesting pragmatic guidelines for managing visitors and social conditions that can reduce negative effects on captive gibbons.