Primates and pandemics: A biocultural approach to understanding disease transmission in human and nonhuman primates.

Investigations into zoonotic disease outbreaks have been largely epidemiological and microbiological, with the primary focus being one of disease control and management. Increasingly though, the human-animal interface has proven to be an important driver for the acquisition and transmission of pathogens in humans, and this requires syncretic bio-socio-cultural enquiries into the origins of disease emergence, for more efficacious interventions. A biocultural lens is imperative for the examination of primate-related zoonoses, for the human-primate interface is broad and multitudinous, involving both physical and indirect interactions that occur due to shared spaces and ecologies. I use the case example of a viral zoonotic epidemic that is currently endemic to India, the Kysanaur Forest Disease, to show how biocultural anthropology provides a broad and integrative perspective into infectious disease ecology and presents new insights into the determinants of disease outbreaks. Drawing on insights from epidemiology, political ecology, primate behavioral ecology and ethnoprimatology, this paper demonstrates how human-primate interactions and shared ecologies impact infectious disease spread between human and nonhuman primate groups.

Collective movement decision-making in primates in crop-raiding contexts.

Crop-raiding by wildlife species often involves collective group movement and animal decision-making in this context is an important area of investigation as the risks and rewards associated with crop-raiding are greater than those that are likely to occur in wild food foraging situations. Yet, the form of consensus decision-making involved in wildlife crop-raiding has not been evaluated. In the current study, we assessed the decision-making process exhibited by rhesus macaques, a generalist primate species, in the context of crop-raiding. We predicted that rhesus macaques would display unshared consensus decision-making during the higher risk-entailed crop-raiding collective movements. We followed two groups of rhesus macaques and collected data on their movement and foraging behavior during crop-raiding events. The results from our study showed that collective movements in the context of crop-raiding were largely led by single individuals. However, individuals of all age-sex categories successfully led crop-raiding collective movements. Although adult individuals joined adult-initiated raid movements most often, they also joined raids initiated by other age classes. Contrary to our predictions, in crop-raiding contexts, rhesus macaques demonstrated a tendency towards equally shared decision-making for group movements.

Why do people visit primate tourism sites? Investigating macaque tourism in Japan and Indonesia.

Primates are popular species in wildlife tourism contexts and provide economic benefits to habitat countries where primate-based tourism activities are a part of the country's tourism economy. Primate tourism runs a broad gamut from safari-like expeditions within remote primate habitats to designated monkey parks and incidental primate tourism. In most forms of primate tourism, primate ecology and behaviour are directly influenced by humans, making these interfaces particularly relevant for examination using the lens of ethnoprimatology. While several studies have assessed the impact of tourism on primates, little is known about people's motivations for observing monkeys for recreational purposes. Here we present two case studies-the Jigokudani Monkey Park, Japan, and the Telaga Warna Nature Recreational Park, Indonesia-where we provide quantitative assessments of people's motivations for visiting managed (monkey parks) and unmanaged (incidental) monkey tourism sites. We further show that management regimes, socio-demographic attributes, previous experience of interactions with macaques, and feeding them play a role in people's desire to visit macaque tourism sites. In Japan, those who had interacted with macaques before were more likely to visit the park to observe macaques clearly and at close quarters. In contrast, respondents in Indonesia were more interested in the recreational opportunities offered by the nature reserve rather than in macaques. However, here too, people who had interacted with macaques earlier were more likely to visit incidental macaque tourist sites for the sole purpose of viewing or interacting with macaques. Almost 50% of the Japanese respondents visited the monkey park due to personal inclinations, while less than 14% of people in Indonesia visited the park of their own volition. Also, over 57% of the Japanese respondents said that visiting monkey parks helped them gain a better understanding of macaque behaviour, whereas only about 26% respondents said likewise in Indonesia. Unlike the Japanese respondents, most of the Indonesian respondents engaged in feeding macaques. These findings suggest that management regimes as well as socio-demographic attributes may influence people's motivations to visit macaque tourism sites.

The costs and benefits of coexistence: What determines people's willingness to live near nonhuman primates?

Living near primate species has positive and negative outcomes for human communities. While most studies focus on understanding people's perceptions regarding the adverse consequences of interacting with primates, less is known about people's willingness to coexist with primates or reasons that may promote human-primate coexistence. We surveyed 794 people co-living with four different primate species-rhesus macaque Macaca mulatta, bonnet macaque Macaca radiata, lion-tailed macaque Macaca silenus, and Hanuman langur Semnopithecus dussumieri-in southern and western India to understand how people perceived the costs and benefits of coexistence. The results of our semi-structured interview study revealed that although tangible costs (i.e., financial losses from primate depredation) primarily drive people's stated tolerance for primate presence, intangible benefits from primates (i.e., their ecological, existence, sentience, and religious values) also critically affect attitudes towards coexistence. Amongst the four species, people associated rhesus macaques with the greatest costs and fewest benefits, lion-tailed macaques with the lowest costs, and bonnet macaques with the highest benefits. People preferred lion-tailed macaques and Hanuman langurs more than bonnet and rhesus macaques, and affection for a species shaped how people viewed costs accruing from the species. People's preferences for species were influenced by their existence, ecological, and sentience values more than their religious value. We suggest that intangible benefits influence people's fondness for a primate species and this, in turn, shapes how people perceive costs resulting from the species. Hence strengthening people's perceptions of the intangible benefits they receive from primate species will improve human tolerance for living near primates. We argue that there is a need to understand the context of human-primate conflicts beyond the cost aspects and focus on the benefits to improve human-primate coexistence.

The human-primate interface in the New Normal: Challenges and opportunities for primatologists in the COVID-19 era and beyond.

The emergence of SARS-CoV-2 in late 2019 and human responses to the resulting COVID-19 pandemic in early 2020 have rapidly changed many aspects of human behavior, including our interactions with wildlife. In this commentary, we identify challenges and opportunities at human-primate interfaces in light of COVID-19, focusing on examples from Asia, and make recommendations for researchers working with wild primates to reduce zoonosis risk and leverage research opportunities. First, we briefly review the evidence for zoonotic origins of SARS-CoV-2 and discuss risks of zoonosis at the human-primate interface. We then identify challenges that the pandemic has caused for primates, including reduced nutrition, increased intraspecific competition, and increased poaching risk, as well as challenges facing primatologists, including lost research opportunities. Subsequently, we highlight opportunities arising from pandemic-related lockdowns and public health messaging, including opportunities to reduce the intensity of problematic human-primate interfaces, opportunities to reduce the risk of zoonosis between humans and primates, opportunities to reduce legal and illegal trade in primates, new opportunities for research on human-primate interfaces, and opportunities for community education. Finally, we recommend specific actions that primatologists should take to reduce contact and aggression between humans and primates, to reduce demand for primates as pets, to reduce risks of zoonosis in the context of field research, and to improve understanding of human-primate interfaces. Reducing the risk of zoonosis and promoting the well-being of humans and primates at our interfaces will require substantial changes from "business as usual." We encourage primatologists to help lead the way.

Is human-rhesus macaque (Macaca mulatta) conflict in India a case of human-human conflict?

The perceptions of wildlife managers regarding human-wildlife conflict (HWC) scenarios are likely to affect the outcomes of conflict mitigation measures. We studied the attitudes and perceptions of forest department personnel regarding the management of human-rhesus macaque conflict (HRMC) in Himachal Pradesh, northern India. We collected data through a questionnaire survey and used frameworks from organizational psychology to draw insights from our results. Forest department personnel belonging to different organizational levels varied with respect to their views on conflict mitigation measures. While the views of upper level management personnel aligned closely with the publicly-stated position of the forest department, the opinions of lower level management personnel were aligned with the opinions of farmers. Overall, wildlife managers differed from farmers in their opinions regarding causes and mitigation of HRMC. Our results indicate the presence of human-human conflict in the context of HRMC and we discuss the implications of this for the management of HRMC.

Reliability of macaques as seed dispersers.

Seed dispersal is an ecological process crucial for forest regeneration and recruitment. To date, most studies on frugivore seed dispersal have used the seed dispersal effectiveness framework and have documented seed-handling mechanisms, dispersal distances and the effect of seed handling on germination. In contrast, there has been no exploration of "disperser reliability" which is essential to determine if a frugivore is an effective disperser only in particular regions/years/seasons or across a range of spatio-temporal scales. In this paper, we propose a practical framework to assess the spatial reliability of frugivores as seed dispersers. We suggest that a frugivore genus would be a reliable disperser of certain plant families/genera if: (a) fruits of these plant families/genera are represented in the diets of most of the species of that frugivore, (b) these are consumed by the frugivore genus across different kinds of habitats, and (c) these fruits feature among the yearly staples and preferred fruits in the diets of the frugivore genus. Using this framework, we reviewed frugivory by the genus Macaca across Asia to assess its spatial reliability as seed dispersers. We found that the macaques dispersed the seeds of 11 plant families and five plant genera including at least 82 species across habitats. Differences in fruit consumption/preference between different groups of macaques were driven by variation in plant community composition across habitats. We posit that it is essential to maintain viable populations of macaques across their range and keep human interventions at a minimum to ensure that they continue to reliably disperse the seeds of a broad range of plant species in the Anthropocene. We further suggest that this framework be used for assessing the spatial reliability of other taxonomic groups as seed dispersers.

The monkey is not always a God: Attitudinal differences toward crop-raiding macaques and why it matters for conflict mitigation.

Attitudinal differences toward wildlife have important implications for conflict management and when the species in question have strong cultural and religious associations, conflict mitigation becomes a challenging endeavor. We investigated farmers' attitudes toward two different crop-raiding macaque species, the rhesus macaque in northern India, and the bonnet macaque in southern India. Apart from regional differences in attitudes, we also assessed temporal changes in attitude toward the rhesus macaque. We carried out household surveys using a semistructured questionnaire to collect data. Our findings reveal that respondents in southern and northern India differ significantly in their views regarding species sanctity and preference for mitigation options. Although people's perceptions of the rhesus macaques had changed over time in northern India, farmers were still unwilling to cause harm to the macaques. We discuss the underlying causes of these observed differences in attitude and their impact on the management of human-macaque conflict.

Distribution of the Grey Slender Loris (Loris lyddekerianus Cabrera, 1908) in Tamil Nadu, Southern India.

The grey slender loris Loris lydekkerianus, one of only two nocturnal primates of India, is found in the southern part of the country. Our understanding of its geographical distribution is largely based on historical records and short surveys, and little is known of its occurrence in southern India today. We sought to establish the relative abundance of this species in 26 districts in the state of Tamil Nadu and the union territory of Pondicherry in southern India. We sighted lorises in 19 districts, and their relative abundance ranged from 0.01 to 2.21/km. The south-central districts of Tamil Nadu showed the highest densities of lorises, while the western districts showed the lowest. Based on these results, we recommend increased protection measures for the forest patches of the Eastern Ghats mountains in order to ensure the long-term survival of the grey slender loris.

Primates, Provisioning and Plants: Impacts of Human Cultural Behaviours on Primate Ecological Functions.

Human provisioning of wildlife with food is a widespread global practice that occurs in multiple socio-cultural circumstances. Provisioning may indirectly alter ecosystem functioning through changes in the eco-ethology of animals, but few studies have quantified this aspect. Provisioning of primates by humans is known to impact their activity budgets, diets and ranging patterns. Primates are also keystone species in tropical forests through their role as seed dispersers; yet there is no information on how provisioning might affect primate ecological functions. The rhesus macaque is a major human-commensal species but is also an important seed disperser in the wild. In this study, we investigated the potential impacts of provisioning on the role of rhesus macaques as seed dispersers in the Buxa Tiger Reserve, India. We studied a troop of macaques which were provisioned for a part of the year and were dependent on natural resources for the rest. We observed feeding behaviour, seed handling techniques and ranging patterns of the macaques and monitored availability of wild fruits. Irrespective of fruit availability, frugivory and seed dispersal activities decreased when the macaques were provisioned. Provisioned macaques also had shortened daily ranges implying shorter dispersal distances. Finally, during provisioning periods, seeds were deposited on tarmac roads that were unconducive for germination. Provisioning promotes human-primate conflict, as commensal primates are often involved in aggressive encounters with humans over resources, leading to negative consequences for both parties involved. Preventing or curbing provisioning is not an easy task as feeding wild animals is a socio-cultural tradition across much of South and South-East Asia, including India. We recommend the initiation of literacy programmes that educate lay citizens about the ill-effects of provisioning and strongly caution them against the practice.

Seed dispersal by rhesus macaques Macaca mulatta in Northern India.

Frugivorous primates are important seed dispersers and their absence from forest patches is predicted to be detrimental to tropical forest regeneration and recruitment. With the reduction of primate populations globally, ecologically resilient primate species, characterized by dietary flexibility and the ability to thrive in a variety of habitats, assume new importance as seed dispersers. The most widely distributed non-human primate, the rhesus macaque Macaca mulatta has been intensively studied but little is known about its role in maintaining ecosystem structure and functions. Due to their frugivorous diet, large group sizes, large home ranges and tolerance to disturbance, rhesus macaques may be effective seed dispersers. We studied seed dispersal by rhesus macaques at the Buxa Tiger Reserve, India, through a combination of behavioural observations and germination experiments. Rhesus macaques dispersed 84% of the 49 species they fed on either through spitting or defecation. Nearly 96% of the handled seeds were undamaged and 61% of the species for which germination tests were performed had enhanced germination. Almost 50% of the monitored seeds among those deposited in situ germinated and 22% established seedlings, suggesting that rhesus macaques are important seed dispersers in tropical forests. Due to their widespread distribution and large populations, rhesus macaques are perceived as common and are categorized as Least Concern on the IUCN Red List, effectively excluding them from any conservation plans. Based on the results of our study, we argue that rhesus macaques fulfill critical ecological functions in their habitat and that this parameter must be taken into consideration when they are reviewed for conservation priorities.

Comparative demography of two commensal macaques in India: implications for population status and conservation.

Rhesus and bonnet macaques are among the most common primates found in India and have been categorised as being of Least Concern by the IUCN. Despite the wealth of information on their ecology and behaviour, little attention has been paid to their demography or population status. We studied the demographic status of the two species along their common distribution zone in western, central and south-eastern India. Bonnet macaques were largely found in forest areas whereas rhesus macaques were observed more often in human-dominated habitats. The troop sizes of the two species also tended to be largest in different habitats, bonnet macaques in forested areas and rhesus macaques in urban areas. We suggest that the presence of large numbers of rhesus macaques in anthropogenic areas in south-eastern India is not a natural phenomenon but has been caused by human intervention. The bonnet macaque population has decreased in number in the common distribution zone, and as this species, unlike the rhesus macaque, is endemic to India, we strongly recommend the need to reassess its conservation status.

Exudativory in the Bengal slow loris (Nycticebus bengalensis) in Trishna Wildlife Sanctuary, Tripura, northeast India.

In this study we estimated the extent of exudativory in Nycticebus bengalensis and examined whether exudates can be considered as fallback foods. This study was carried out in Trishna Wildlife Sanctuary, northeastern India, in winter (December-February) and summer (March and April). We estimated time-activity budget using instantaneous sampling and used continuous focal animal sampling to record all instances and durations of feeding, over a total of 177 hr. Feeding accounted for 22.3+/-2.2% of the activity budget, with no seasonal difference. Bengal slow lorises fed on exudates, nectar, fruit, bark, invertebrates and avian eggs. In addition to scraping they also obtained exudates by gouging holes into the bark of trees. In winter, lorises almost exclusively fed on exudates (94.3% of winter feeding time). In summer, exudates (67.3%) and nectar from one species (22.3%) dominated the diet. This study identifies the Bengal slow loris as the most exudativorous loris. Exudates rather than being a staple fallback food, seem to be a preferred, patchily distributed and common food in the diet of the Bengal slow loris. Exudativory in this species is characterized by high selectivity among species and seasonal variation, which may be related to variations in productivity of exudates and their chemical composition. An understanding of these factors is necessary for predicting the response of this species to human disturbance such as logging. This study also underscores the importance of protecting some of the common species such as Terminalia belerica on which the loris feeds during periods of scarcity.

Reproductive biology of the slender loris (Loris lydekkerianus lydekkerianus).

The slender loris (Loris lydekkerianus lydekkerianus), a nocturnal prosimian, was studied for 21 months in its natural habitat of scrub jungle in Dindigul, south India. Here we report on its reproductive biology. Identified and unidentified lorises were observed for a total of 2,656 h. Reproductive seasonality was seen, with births and oestrus observed to be highest in April-June and October-December. The mating system was promiscuous with 1 female mating successively with 3-4 males. A gestation period of 5.5 months and an inter-birth interval of 7 months were recorded. Adult females had a reproductive potential of 4 infants per year. The findings presented in this paper constitute the first information on the life history parameters of wild slender lorises.

Home range and ranging pattern in the slender loris(Loris tardigradus lydekkerianus).

The home range and ranging pattern of the slender loris (Loris tardigradus lydekkerianus) was studied for 21 months in a scrub jungle in Dindigul, Tamil Nadu, south India. Sixteen individuals were observed for a total of 2261 hours. Home ranges were measured for eight adult individuals and eight juvenile and subadult individuals. Males had significantly larger home ranges than the females, and home range size increased post-weaning. The ranging patterns involved minimal female intrasexual overlap, large male intrasexual overlap and large intersexual range overlap.