A tool to act blind? Object-assisted eye-covering as a self-handicapping behavior and social play signal in Balinese long-tailed macaques.

Self-handicapping behaviors evolved as honest signals that reliably reflect the quality of their performers. In playful activities, self-handicapping is described as intentionally and unnecessarily putting oneself into disadvantageous positions and situations. Self-handicapping during play may allow individuals to learn to cope with unexpected events by improving sensori-motor coordination, as well as function as a play solicitation signal. One such self-handicapping behavior involves moving about while deliberately covering one's eyes. We conducted a quantitative study of object-assisted eye-covering (OAEC) in a population of free-ranging Balinese macaques. After evaluating the frequency, form, distribution, and context of OAEC, we measured the responses this behavior elicited (1) in the performers with a focus on sensori-motor self-handicapping, and (2) in their conspecifics, with an emphasis on whether, and if so how, OAEC may facilitate social play. Our data provided some support for several hypotheses: OAEC is a sensori-motor self-handicapping behavior, an attention-getting cue, a social play signal, and a socially self-handicapping tactic during social play. We discuss our results from the perspective of tool-assisted self-handicapping behavior, propose a scenario to account for the emergence of this behavioral innovation, and speculate on the cultural nature of OAEC.

Social influence on the expression of robbing and bartering behaviours in Balinese long-tailed macaques.

Animals use social information, available from conspecifics, to learn and express novel and adaptive behaviours. Amongst social learning mechanisms, response facilitation occurs when observing a demonstrator performing a behaviour temporarily increases the probability that the observer will perform the same behaviour shortly after. We studied "robbing and bartering" (RB), two behaviours routinely displayed by free-ranging long-tailed macaques (Macaca fascicularis) at Uluwatu Temple, Bali, Indonesia. When robbing, a monkey steals an inedible object from a visitor and may use this object as a token by exchanging it for food with the temple staff (bartering). We tested whether the expression of RB-related behaviours could be explained by response facilitation and was influenced by model-based biases (i.e. dominance rank, age, experience and success of the demonstrator). We compared video-recorded focal samples of 44 witness individuals (WF) immediately after they observed an RB-related event performed by group members, and matched-control focal samples (MCF) of the same focal subjects, located at similar distance from former demonstrators (N = 43 subjects), but in the absence of any RB-related demonstrations. We found that the synchronized expression of robbing and bartering could be explained by response facilitation. Both behaviours occurred significantly more often during WF than during MCF. Following a contagion-like effect, the rate of robbing behaviour displayed by the witness increased with the cumulative rate of robbing behaviour performed by demonstrators, but this effect was not found for the bartering behaviour. The expression of RB was not influenced by model-based biases. Our results support the cultural nature of the RB practice in the Uluwatu macaques.

The role of anthropic, ecological, and social factors in sleeping site choice by long-tailed macaques (Macaca fascicularis).

When choosing their sleeping sites, primates make adaptive trade-offs between various biotic and abiotic constraints. In human-modified environments, anthropic factors may play a role. We assessed the influence of ecological (predation), social (intergroup competition), and anthropic (proximity to human settlements) factors in sleeping site choice by long-tailed macaques (Macaca fascicularis) occupying a habitat at the interface of natural forests and human-modified zones in Bali Barat National Park, Indonesia. Over the course of 56 nights, we collected data relating to physical features of sleeping trees, patterns of the use of sleeping sites within the home range, pre-sleep behavior, diurnal ranging patterns and availability of natural and human food. Overall, the macaques used 17 sleeping sites with 37 sleeping trees. When the monkeys slept in forest zones, they selected sleeping trees that had larger trunks but were not significantly taller than surrounding trees. Though the macaques rarely re-used sleeping sites on consecutive nights, they frequently re-used four sites over the study period. The group favored sleeping within the core area of its home range, despite the occurrence of frequent agonistic intergroup encounters there. Macaques preferentially selected sleeping trees located within or near human-modified zones, especially when human food was abundant and natural food was scarce. These results partially support the hypothesis that long-tailed macaques choose their sleeping sites to avoid predation; proximity to human settlements appears to be the primary factor influencing sleeping site choice in this primate species. Our results reflect the strong influence that anthropic factors have on primates, which subsist in increasingly human-dominated landscapes.

Human behavior and opportunities for parasite transmission in communities surrounding long-tailed macaque populations in Bali, Indonesia.

Spatial overlap and shared resources between humans and wildlife can exacerbate parasite transmission dynamics. In Bali, Indonesia, an agricultural-religious temple system provides sanctuaries for long-tailed macaques (Macaca fascicularis), concentrating them in areas in close proximity to humans. In this study, we interviewed individuals in communities surrounding 13 macaque populations about their willingness to participate in behaviors that would put them at risk of exposure to gastrointestinal parasites to understand if age, education level, or occupation are significant determinants of exposure behaviors. These exposure risk behaviors and attitudes include fear of macaques, direct contact with macaques, owning pet macaques, hunting and eating macaques, and overlapping water uses. We find that willingness to participate in exposure risk behaviors are correlated with an individual's occupation, age, and/or education level. We also found that because the actual risk of infection varies across populations, activities such as direct macaque contact and pet ownership, could be putting individuals at real risk in certain contexts. Thus, we show that human demographics and social structure can influence willingness to participate in behaviors putting them at increased risk for exposure to parasites.

Healing Hanuman's Army: Veterinary Care as a Core Component of One Health Principles in a Southeast Asian Monkey Forest.

Wildlife that inhabit urban landscapes face the dual challenge of negotiating their positions in their group while navigating obstacles of anthropogenically modified landscapes. The dynamics of urban environments can result in novel injuries and mortalities for these animals. However, these negative impacts can be mitigated through planning, and onsite veterinary care like that provided by the Ubud Monkey Forest in Bali, Indonesia. We examined 275 recorded injuries and mortalities among six social groups of long-tailed macaques (Macaca fascicularis) brought to the veterinary clinic from 2015-2018. We fit the probabilities of injury vs. death among macaques brought to the clinic using a multilevel logistic regression model to infer the relationship between injury vs. death and associated demographic parameters. Males were more likely to sustain injuries and females were more likely to die. The frequency of injuries and mortalities changed over the four-year study period, which was reflected in our model. The odds of mortality were highest among young macaques and the odds of injury vs. mortality varied across the six social groups. We categorized injuries and mortalities as "natural" or "anthropogenic". Most injuries and mortalities were naturally occurring, but powerlines, motorized vehicles, and plastic present ongoing anthropogenic threats to macaque health. Most wounds and injuries were successfully treated, with healthy animals released back to their group. We suggest other sites with high levels of human-alloprimate interplays consider the Ubud Monkey Forest veterinary office as a model of care and potentially adopt their approaches.

Cohort dominance rank and "robbing and bartering" among subadult male long-tailed macaques at Uluwatu, Bali.

Robbing and bartering is a habitual behavior among free-ranging long-tailed macaques (Macaca fascicularis) at a single site in Bali, Indonesia. The behavior consists of three main elements: (1) a macaque takes an item from a human; (2) the macaque maintains possession of the item; then (3) the macaque releases or hands off the item after accepting a food offer from a human. In this paper, we analyze data on individual variation in robbing and bartering among subadult males in relation to dominance rank. Using focal animal sampling we collected 197 observation hours of data on 13 subadult males from two groups (6 from Celagi; 7 from Riting) at the Uluwatu temple site from May 2017 to March 2018, recording 44 exchanges of items for food from 92 total robberies following 176 total attempts. We also measured dominance rank using interaction data from our focal animals. Dominance rank was strongly positively correlated with robbery efficiency in Riting, but not Celagi, meaning that more dominant Riting subadult males exhibited fewer overall robbery attempts per successful robbery. We suggest the observed variation in robbing and bartering practices indicates there are crucial, yet still unexplored, social factors at play for individual robbing and bartering decisions.

Dyadic response facilitation of object play in Balinese long-tailed macaques.

Social influence is at the core of the emergence and maintenance of behavioral traditions in various animal taxa. Response facilitation is a mechanism of social influence whereby observing a demonstrator performing a behavior temporarily increases the probability that the observer will perform the same behavior. We focused on stone handling (SH) behavior, a form of object-directed play routinely displayed by free-ranging long-tailed macaques (Macaca fascicularis) in Ubud, Bali, Indonesia. We tested whether the expression of SH was subject to dyadic response facilitation. We compared video-recorded focal samples of an individual immediately after they had witnessed a SH bout performed by a conspecific, and matched-control focal samples of the same witness in the absence of any surrounding SH bouts. We found converging evidence that SH was facilitated within pairs of individuals. First, SH occurred significantly more often and lasted significantly longer in the post-witnessing condition than in the matched-control condition. Second, a monkey initiated SH more rapidly in the former than in the latter, and this significant facilitation effect mainly occurred during the first two minutes after witnessing SH. By demonstrating that the expression of SH was socially mediated, we provided further support for the cultural nature of this behavior.

First survey on seroprevalence of Japanese encephalitis in long-tailed macaques (Macaca fascicularis) in Bali, Indonesia.

Background and Aim: Japanese encephalitis (JE) is a zoonotic infectious inflammatory brain disease caused by the JE virus (JEV). Considerable research into the seroprevalence of JE in domestic animals has been conducted, but there have been no reports of its occurrence in wild animals, including long-tailed macaques (Macaca fascicularis). This study aimed to estimate the seroprevalence of JEV infection and its determinants in long-tailed macaques in Bali and the prevalence of mosquito vectors. Materials and Methods: Blood samples (3 mL) were collected from a population of M. fascicularis (92 heads) inhabiting a small forest with irrigated rice field nearby (wetland area) in Ubud, Gianyar, and from two populations in dryland areas with no wet rice field (Uluwatu, Badung, and Nusa Penida, Bali Province, Indonesia). The collected sera were tested for antibodies against JEV using a commercially available enzyme-linked immunosorbent assay kit (qualitative monkey JE Immunoglobulin G antibody kit). The seropositivity of the antibodies was then compared based on different variables, namely, habitat type, age, and sex. Results: The seroprevalence of the JEV antibodies in all the samples tested was found to be 41.3%. The seropositivity of the monkey serum samples collected from the wetland area was 46.4%, which was higher than the seropositivity of the sera samples collected from the dried field areas (1.25%). Monkey sera collected from the wetland areas were 6.1 times (odds ratio [OR]: 6.1; 95% confidence interval [CI]: 0.71-51.5, p>0.05) more likely to be seropositive compared to the monkey sera collected from the dried field areas. Meanwhile, female monkeys were 1.79 times (OR: 1.79; 95% CI: 0.76-4.21; p>0.05) more likely to be seropositive to JEV than males. Similarly, juvenile monkeys were 2.38 times (OR: 2.38; 95% CI: 0.98-5.79); p>0.05) more likely to be seropositive against the JEV than adult monkeys. However, none of these differences achieved statistical significance. Regarding the JEV mosquito vector collection, more Culex mosquitoes were found in the samples from the wetland areas than from the dried field areas. Conclusion: The study confirms the existence of JEV infection in long-tailed macaques in Bali. There were patterned seropositivity differences based on habitat, age, and sex of the monkeys, but these were not significant. The possibility of monkeys as a JEV reservoir and the presence of the mosquitoes as the JEV vector are suggested but require more study to confirm.

Acquisition of object-robbing and object/food-bartering behaviours: a culturally maintained token economy in free-ranging long-tailed macaques.

The token exchange paradigm shows that monkeys and great apes are able to use objects as symbolic tools to request specific food rewards. Such studies provide insights into the cognitive underpinnings of economic behaviour in non-human primates. However, the ecological validity of these laboratory-based experimental situations tends to be limited. Our field research aims to address the need for a more ecologically valid primate model of trading systems in humans. Around the Uluwatu Temple in Bali, Indonesia, a large free-ranging population of long-tailed macaques spontaneously and routinely engage in token-mediated bartering interactions with humans. These interactions occur in two phases: after stealing inedible and more or less valuable objects from humans, the macaques appear to use them as tokens, by returning them to humans in exchange for food. Our field observational and experimental data showed (i) age differences in robbing/bartering success, indicative of experiential learning, and (ii) clear behavioural associations between value-based token possession and quantity or quality of food rewards rejected and accepted by subadult and adult monkeys, suggestive of robbing/bartering payoff maximization and economic decision-making. This population-specific, prevalent, cross-generational, learned and socially influenced practice may be the first example of a culturally maintained token economy in free-ranging animals. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Stone affordances as potential for action expression in object play in long-tailed macaques (Macaca fascicularis).

Object affordances play a major role in action expression: (a) providing opportunities to generate potential solutions to instrumental problems and (b) shaping and constraining the motor actions available to an individual. The playful manipulation of objects can facilitate individual acquisition of functional object-assisted actions through affordance learning. We tested the "object affordance" hypothesis in free-ranging long-tailed macaques. This hypothesis holds that the physical properties associated with stone size afford different stone-directed actions, in the context of stone handling (SH) behavior, a form of culturally maintained stone play from which stone tool use can emerge. We predicted that higher SH versatility (i.e., total number of different SH behavioral elements expressed) and higher duration of the SH behavioral element "Pound" would be associated with the manipulation of medium-sized stones, followed by small stones, and then large stones. Our data partly supported these predictions. Both medium-sized and small-sized stones afforded the highest SH versatility, and a higher duration of "Pound" than large stones. As expected, duration of "Pound" was higher with medium than small stones, but the difference was not statistically significant. Our results were consistent with Newell's constraint model, which emphasizes the role of objects' physical properties in limiting and enhancing the expression of actions directed to these objects. The relaxed selective pressures acting on SH behavior may enhance the expression of a range of actions directed toward stones of different sizes that could facilitate the emergence of instrumental solutions and may contribute to explaining the evolution of lithic technology in early humans. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Effect of Infant Presence on Social Networks of Sterilized and Intact Wild Female Balinese Macaques (Macaca fascicularis).

Contraception is increasingly used to control wild animal populations. However, as reproductive condition influences social interactions in primates, the absence of new offspring could influence the females' social integration. We studied two groups of wild macaques (Macaca fascicularis) including females recently sterilized in the Ubud Monkey Forest, Indonesia. We used social network analysis to examine female grooming and proximity networks and investigated the role of infant presence on social centrality and group connectivity, while controlling for the fertility status (sterilized N = 14, intact N = 34). We compared the ego networks of females experiencing different nursing conditions (young infant (YI) vs. old infant (OI) vs. non-nursing (NN) females). YI females were less central in the grooming network than other females while being more central in proximity networks, suggesting they could keep proximity within the group to protect their infant from hazards, while decreasing direct grooming interactions, involving potential risks such as kidnapping. The centrality of sterilized and intact females was similar, except for the proximity network where sterilized females had more partners and a better group connectivity. These results confirm the influence of nursing condition in female macaque social networks and did not show any negative short-term effects of sterilization on social integration.

Inferring functional patterns of tool use behavior from the temporal structure of object play sequences in a non-human primate species.

Inferring functional components of behavioral sequences is a crucial but challenging task. A systematic comparison of their temporal structure is a good starting point, based on the postulate that more functional traits are less structurally variable. We studied stone handling behavior (SH) in Balinese long-tailed macaques, a versatile form of stone-directed play. We tested the hypothesis that stones are used by male monkeys to stimulate their genitals in a sexual context (i.e., "sex toy" hypothesis). Specifically, two SH actions (i.e., "tap-on-groin" (TOG) and "rub-on-groin" (ROG), respectively the repetitive tapping and rubbing of a stone onto the genital area) gained functional properties as self-directed tool-assisted masturbation. Owing to the structural organization of playful activities, we predicted that SH sequences without TOG/ROG would exhibit higher levels of variability, repeatability and exaggeration than SH sequences with TOG/ROG. We also predicted that TOG/ROG would occur more often and last longer in SH sequences in which penile erection - a sexually-motivated physiological response in primates - was observed than in SH sequences in which penile erection was not observed. To identify and compare recurring series of SH patterns otherwise undetectable by using conventional quantitative approaches across SH sequences containing TOG/ROG or not, we used a temporal analysis known as "T-pattern detection and analysis" (TPA). Our predictions about variability, exaggeration and temporal association between TOG/ROG in males and penile erection were supported. As expected, SH sequences without TOG/ROG were, on average, more repeatable than SH sequences with TOG/ROG, but the difference was not statistically significant. Overall, the "sex toy" hypothesis was partly supported, and our results suggested that TOG and ROG are two forms of tool-assisted genital stimulation, possibly derived from the playful handling of stones. These findings are consistent with the view that tool use may evolve in stages from initially non-functional object manipulation, such as object play.

Diverse contexts of zoonotic transmission of simian foamy viruses in Asia.

In Asia, contact between persons and nonhuman primates is widespread in multiple occupational and nonoccupational contexts. Simian foamy viruses (SFVs) are retroviruses that are prevalent in all species of nonhuman primates. To determine SFV prevalence in humans, we tested 305 persons who lived or worked around nonhuman primates in several South and Southeast Asian countries; 8 (2.6%) were confirmed SFV positive by Western blot and, for some, by PCR. The interspecies interactions that likely resulted in virus transmission were diverse; 5 macaque taxa were implicated as a potential source of infection. Phylogenetic analysis showed that SFV from 3 infected persons was similar to that from the nonhuman primate populations with which the infected persons reported contact. Thus, SFV infections are likely to be prevalent among persons who live or work near nonhuman primates in Asia.

Intergroup variation in robbing and bartering by long-tailed macaques at Uluwatu Temple (Bali, Indonesia).

Robbing and bartering (RB) is a behavioral practice anecdotally reported in free-ranging commensal macaques. It usually occurs in two steps: after taking inedible objects (e.g., glasses) from humans, the macaques appear to use them as tokens, returning them to humans in exchange for food. While extensively studied in captivity, our research is the first to investigate the object/food exchange between humans and primates in a natural setting. During a 4-month study in 2010, we used both focal and event sampling to record 201 RB events in a population of long-tailed macaques (Macaca fascicularis), including four neighboring groups ranging freely around Uluwatu Temple, Bali (Indonesia). In each group, we documented the RB frequency, prevalence and outcome, and tested the underpinning anthropogenic and demographic determinants. In line with the environmental opportunity hypothesis, we found a positive qualitative relation at the group level between time spent in tourist zones and RB frequency or prevalence. For two of the four groups, RB events were significantly more frequent when humans were more present in the environment. We also found qualitative partial support for the male-biased sex ratio hypothesis [i.e., RB was more frequent and prevalent in groups with higher ratios of (sub)adult males], whereas the group density hypothesis was not supported. This preliminary study showed that RB is a spontaneous, customary (in some groups), and enduring population-specific practice characterized by intergroup variation in Balinese macaques. As such, RB is a candidate for a new behavioral tradition in this species.