Monkey Forest Research Articles

Investigating Potential Effects of the Contraceptive Implanon on the Behavior of Free-Ranging Adult Female Barbary Macaques

In recent years, the use of hormonal contraception in captive, free-ranging, and wild mammal populations has increased, but the effects on these nonhuman animals' behavior and the associated welfare impacts remain poorly understood. This study of free-ranging adult female Barbary macaques (Macaca sylvanus) at Trentham Monkey Forest compared females implanted with the progestin-only contraceptive Implanon to those not receiving contraception. Females with contraceptive implants had higher rates of self-scratching and spent more time self-grooming (2 behavioral indexes of anxiety) than those without implants. They also directed more aggression at others, spent more time receiving grooming and traveling, and spent less time giving grooming and resting. No significant differences between the 2 groups of females were seen for time spent foraging. These results suggest that Implanon had a number of effects on Barbary macaques, although these need to be considered in light of the significant benefits afforded by the use of this contraceptive. The findings of this study provide important information to those evaluating the relative welfare costs and benefits of alternative methods of population control in this and other species.

The functions of non-reproductive mounts among male Barbary macaques (Macaca sylvanus).

Same-sex, non-reproductive mounts have been observed in a number of primate species and in various social contexts. However, the function of non-reproductive mounts is still largely unknown. We aimed to test whether non-reproductive mounts function to assert dominance and as appeasement behavior in male Barbary macaques. We analyzed post-mount behavior in 54 macaques belonging to two captive groups at Trentham Monkey Forest in Staffordshire, using 10 min post-mount/matched-control focal sessions collected either on the mounter or the mountee. In support of the dominance assertion hypothesis, the higher-ranking male within a mounting pair was more likely to be the mounter than the mountee, and to mock bite the lower-ranking male. In support of the appeasement hypothesis, the former mounting partners were more likely to exchange grooming and to have a lower frequency of self-scratching (a measure of social tension) after a non-reproductive mount than in control sessions. Our study indicates that non-reproductive mounts have different and not mutually exclusive functions and can modulate the quality of social interactions among group members. We discuss the possible factors that can affect the occurrence of non-reproductive mounts within and between species.

Grooming and Anxiety in Barbary Macaques

AbstractGrooming is a fundamental component of sociality in many gregarious animal species, and elucidating the costs and benefits of this behaviour is crucial for understanding its function. There is evidence that animals giving grooming pay a cost in terms of the time and energy they invest, while recipients benefit not just from the removal of dirt and parasites, but also from the relaxing effects of being groomed. Recently, however, studies of primates have indicated that giving grooming may also provide such hedonic benefits, reducing levels of stress or anxiety in the groomer. In this study of free‐ranging adult female Barbary macaques at Trentham Monkey Forest (Stoke‐on‐Trent, UK), we tested the hypothesis that grooming reduces anxiety in the donor and/or the recipient. During focal follows, we quantified females' rates of self‐scratching as a behavioural index of their anxiety levels. Self‐scratching rates in the 2‐min periods after bouts of grooming (given, received and reciprocated) were compared to overall mean self‐scratching rates; we predicted that if grooming reduces anxiety, self‐scratching rates would be significantly lower after grooming bouts than mean levels. We first analysed all grooming bouts and then analysed separately grooming bouts with adult males, with all adult females, with subordinate adult females and with dominant adult females. Contrary to our prediction, self‐scratching rates were never seen to be lower after grooming than mean levels. In fact, for the majority of grooming partner–direction combinations, we found significantly higher rates of self‐scratching after grooming compared to mean levels. The hypothesis that grooming reduces anxiety was therefore not supported. Grooming seems in some cases to increase, not alleviate, anxiety. We explore possible explanations for these unexpected results.

Associations between social behaviour and adrenal activity in female Barbary macaques: Consequences of study design

Faecal glucocorticoid metabolite (fGCM) concentrations have been used to evaluate adrenal activity in a variety of species; including as an indicator of the physiological response to social stress. However, across studies, the relationships between dominance rank, social behaviours and adrenal responses can be inconsistent. Differences in the relationship between rank and glucocorticoids may be due to the relative costs of social status, and the relative frequencies of social stressors and potential coping mechanisms. However, the differences in observed relationships between specific social behaviours and glucocorticoids may be partly explained by sampling frequency, as studies often use average fGCM concentrations collected over a period of weeks or months, rather than fGCM concentrations that are temporally-matched with behavioural data. In this study, we directly compared long-term average and temporally-matched data to determine whether particular social behaviours were related to adrenal activity in female Barbary macaques (Macaca sylvanus) at Trentham Monkey Forest, UK; and whether observed relationships were consistent using these two approaches. Average rates of autogrooming were positively correlated with average fGCM; however, this relationship was not robust in temporally-matched samples. Instead, specific social behaviours associated with agonism were associated with fGCM in temporally-matched samples within individuals. These results indicate that analyses of relationships using long-term average fGCM and temporally-matched samples do not necessarily provide comparable results, highlighting that study design is critical in determining associations between an individual’s social behaviour and the relative physiological costs involved.

An experimental study of behavioural coping strategies in free-ranging female Barbary macaques (Macaca sylvanus)

A fundamental goal of stress research is to understand how individuals cope with challenges. Studies on a range of vertebrate species suggest that three groups of behaviour—affiliative, aggressive and self-directed behaviours—serve as coping strategies. To date, experimental studies of coping behaviour have tended to be conducted in captive conditions; the limited number of studies in free-ranging or wild settings have been observational in nature. We investigated coping behaviours in free-ranging female Barbary macaques (Macaca sylvanus) at Trentham Monkey Forest, UK, using an experimental playback approach to quantify subjects' responses to mildly aversive threat-grunts. Compared to silent control trials, playbacks of threat-grunts increased aggressive behaviours and one of the two self-directed behaviours examined (self-scratching). No such differences were seen for self-grooming, or for any affiliative behaviour. Elevations in the rate of one measure of aggression, lunging, were positively related to an average measure of adrenocortical activity (median faecal glucocorticoid metabolite levels over the study period). Evidence from females in a variety of Old World monkey species, including Barbary macaques, indicates that affiliative behaviours have an important role in coping with stressful events in the medium to longer term. Our results suggest that, in the short term, female Barbary macaques may use aggressive rather than affiliative behaviours in response to mild stress. These findings highlight the importance of considering how coping mechanisms may vary over time after a stressor, and how coping mechanisms relate to adrenocortical activity. Playback approaches like ours provide a powerful, flexible tool to explore issues such as this in free-ranging and wild animal populations.

Reciprocation and interchange of grooming, agonistic support, feeding tolerance, and aggression in semi‐free‐ranging Barbary macaques

Evidence from a range of primate species indicates that grooming can be exchanged either for itself or for other rank-related "commodities," such as agonistic support, feeding tolerance, or reduced aggression. Patterns of exchange behavior have been found to vary considerably between species, and understanding the causes of this variation is central to the study of the evolution of primate social systems. It is, therefore, essential that exchange behavior is examined in a wide range of species and settings. This article is the first to explore the reciprocation and interchange of grooming in the Barbary macaque (Macaca sylvanus). We collected focal data on semi-free-ranging adult female Barbary macaques at Trentham Monkey Forest, England, and analyzed dyadic data using Generalized Linear Mixed Models. We found evidence for the reciprocal exchange of grooming and for the interchange of grooming for agonistic support and tolerance while feeding. There was no evidence that grooming was traded for a reduction in aggression; indeed, we found a positive relationship between aggression given and grooming received. This may reflect the "extortion" of grooming from subordinates by dominant animals. These results will facilitate comparative analyses of exchange behavior by adding to the current database a new species, characterized by a different social style from those macaque species previously investigated.

Human culture and monkey behavior: assessing the contexts of potential pathogen transmission between macaques and humans

An in-depth understanding of the contexts and patterns of human-macaque interactions can play an important role in assessing and managing the potential for pathogen transmission. The Padangtegal Monkey Forest in Bali, Indonesia, and the Upper Rock Nature Reserve in Gibraltar are two sites that have been relatively well studied in regard to human-macaque interactions. This article presents an overview of interaction patterns between humans and macaques at these sites along with a description of the cultural, demographic, and contextual differences between local and nonlocal humans at the sites. Differences in these two sites' interaction patterns included bite rates, the role of food in aggressive interactions, and the context in which the interactions took place. Similarities included overrepresentation by adult male macaques in interactions and a substantial impact by local cultural and demographic factors. These similarities and differences are interpreted as resulting from differences in macaque species and behaviors, and human demography, culture, and behavioral patterns.

Disproportionate participation by age/sex classes in aggressive interactions between long‐tailed macaques (Macaca fascicularis) and human tourists at Padangtegal monkey forest, Bali, Indonesia

We observed 420 aggressive interactions between tourists and Macaca fascicularis at the Padangtegal Wanara Wana Temple forest site in Bali, Indonesia, during the months of June and July 2001. The data collected included patterns of aggression, presence or absence of food, and demographic information on resident macaques and human visitors. Analyses of the interactions suggest that macaques respond differentially to humans according to the age/sex classes involved. Additionally, adult and subadult male macaques participated in more aggressive behaviors than expected, while adult female macaques and immatures participated in such behaviors less than expected. These variations in interaction patterns between macaques and tourists may have substantial implications for management issues and the potential for pathogen transmission.

Human exposure to herpesvirus B-seropositive macaques, Bali, Indonesia.

Herpesvirus B (Cercopithecine herpesvirus 1) has been implicated as the cause of approximately 40 cases of meningoencephalitis affecting persons in direct or indirect contact with laboratory macaques. However, the threat of herpesvirus B in nonlaboratory settings worldwide remains to be addressed. We investigated the potential for exposure to herpesvirus B in workers at a “monkey forest” (a temple that has become a tourist attraction because of its monkeys) in Bali, Indonesia. In July 2000, 105 workers at the Sangeh Monkey Forest in Central Bali were surveyed about contact with macaques (Macaca fascicularis). Nearly half of those interviewed had either been bitten or scratched by a macaque. Prevalence of injury was higher in those who fed macaques. Serum from 31 of 38 Sangeh macaques contained antibodies to herpesvirus B. We conclude that workers coming into contact with macaques at the Sangeh Monkey Forest are at risk for exposure to herpesvirus B.

The effects of tourism on conservation at the monkey forest in Ubud, Bali

Les macaques à longue queue (Macaca fascicularis) sont depuis longtemps commensaux de l’homme et profitent depuis des milliers d’années de l’association avec l’homme. Toutefois dans la dernière décennie, les populations de cette espèce déclinent avec l’accroissement continu des activités économiques en Asie du Sud-Est. L’expansion de l’agriculture, l’exploitation forestière et d’autres formes de destruction de l’habitat conjuguées à la croissance de la population humaines sont largement responsables du déclin mondial des populations de primates non-humains. Cet article décrit une exception notable caractérisée par l’accroissement de la population locale de macaques dans la Forêt des Singes de Ubud à Bali (Indonésie). Les communautés locales protègent la flore et la faune de la forêt de Ubud en favorisant les valeurs hindouistes traditionnelles et le tourisme. Un comité directorial de la Forêt des Singes s’est constitué au sein des structures religieuses et coutumières traditionnelles. Ce comité a proposé et mis en œuvre de nombreuses opérations de conservation dont le contrôle de l’érosion, la plantation d’arbres, et l’accroissement de la surface de forêt. Nous avons travaillé en contact étroit avec les communautés locales pendant 7 ans et nous insistons sur l’importance de cette action au sein des formes traditionnelles de gouvernement local. Nos premiers résultats scientifiques ont été présentés au comité et nous avons fourni notre avis sur les problèmes rencontrés, par exemple, entre touristes et singes. Les scientifiques peuvent ainsi jouer un rôle efficace de conservation en travaillant en accord avec les populations locales dans leur contexte culturel.

Positioning Eco-Tourism for Improving Destination Image of Bali Indonesia

Ecotourism attractions in this study include: (1) Bali Marine Park, (2) Bali Elephant Safari Park, (3) Bali Barat (West Bali) National Park, (4) Bali Butterfly Park, (5) Bali Reptile Park, (6) Sangeh Monkey Forest, (7) Ubud Botanic Garden, and (8) Bali Botanic Garden based on the attributes of “facility, attractiveness, accessibility, and service”. This study utilized quantitative method, specifically exploratory research method and conclusive research method based on previous research and existing theories, in order to achieve the research objectvies with the goal to generate new findings. Based on multidimensional scaling analysis, the perception of Bali Botanic Garden is similar to that of Sangeh Monkey Forest and Bali Barat National Park. While not in the same category as Bali Botanic Garden, the similarity coordinate of Ubud Botanic Garden is so close that it is a considerable competitor to Bali Botanic Garden. The ecotourism attractions perceived to have similarities are Bali Butterfly Park and Ubud Botanic Garden. Another grouping based on similarity are Bali Marine Park and Bali Elephant Safari Park, whose similarity coordinates are quite distant from the other ecotourism attractions.