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.     

Methods in Primate Nutritional Ecology: A User’s Guide

An important goal of primatology is to identify the ecological factors that affect primate abundance, diversity, demography, and social behavior. Understanding the nutritional needs of primates is central to understanding primate ecology because adequate nutrition is a prerequisite for successful reproduction. Here, we review nutritional methods and provide practical guidelines to measure nutrient intake by primates in field settings. We begin with an assessment of how to estimate food intake by primates using behavioral observations. We then describe how to collect, prepare, and preserve food samples. Finally, we suggest appropriate nutritional assays for estimating diet nutritional quality and point to the merits and limitations of each. We hope this review will inspire primatologists to use nutritional ecology to answer many unresolved questions in primatology.     

Ecological correlates of trophic status and frugivory in neotropical primates

Primates are among the most observable and best studied vertebrate order in tropical forest regions, with widespread attention dedicated to the feeding ecology of wild populations. In particular, primates play a key role as frugivores and seed‐dispersal agents for a myriad of tropical plants. Sampling effort by primatologists, however, has been unequally distributed, hampering quantitative comparisons of primate diets. We provide the first systematic review of primate diets, with an emphasis on frugivory, using a comprehensive compilation of 290 unique primate dietary studies from 164 localities in 17 countries across the entire Neotropical realm. We account for sampling effort (standardised as hours) in comparing the richness of fruiting plants recorded in primate diets, and the relative contribution of frugivory to the overall diet in relation to key life‐history traits, such as body mass. We find strong support for the long‐held hypothesis, based on Kay's Threshold, that body size imposes an upper limit on insectivory and a lower limit on folivory, and therefore that frugivory is most important at intermediate body sizes. However, the upper body mass limit of extant neotropical primates, truncated by the post‐Pleistocene megafaunal overkill, has implications for the extent of the frugivory–folivory continuum in extinct lineages. Contemporary threats faced by the largest primates serve as a further warning that the feeding ecology and diet of all neotropical primates remain severely undersampled with regard to the composition and richness of fruits consumed. Indeed, frugivorous primates expected to have the most species‐rich plant diets are amongst those most poorly sampled, exposing implications for our current understanding of primate–plant interaction networks.     

Successful breeding attempt of a pair of Philippine tarsier (Tarsius syrichta) in a conservation center in Bilar,Bohol, Philippines and recommendations for tarsier husbandry

The Philippine tarsier (Tarsius syrichta) belongs to the least known nocturnal primates. Tarsiers and remaining biodiversity of the Philippines are under tremendous threats from increasing human expansion, with habitat loss and illegal pet trade being the main reasons for tarsier population decline. In addition, even though the attempts were made by western and local facilities, tarsiers have not survived well in captivity. In this paper, I present an example of successful breeding of the Philippine tarsier in captive conditions but in natural climate. As the most important elements of success, I see a large amount of space provided to tarsiers, the climate similar to their natural habitat and the food resembling their natural diet. Our pair of tarsiers were joined during the mating period and held separately outside the mating period, which corresponds with their behavior in the wild and may have played a crucial role in breeding success. Eliminating stress to animals is also important. The study can provide valuable guidelines for other facilities keeping tarsiers in the Philippines and help to improve tarsiers’ welfare and in the future help to establish a viable captive population of the Philippine tarsier that will serve as a backup population and also will decrease demand on tarsiers captured from the wild.     

Primates and parasites: A case for a multidisciplinary approach

Examinations of primate parasitic infections can inform both primatologists and parasitologists about evolutionary and ecological relationships. Interspecific, intraspecific, and interindividual variation in parasitic infections may correlate with environmental, demographic, behavioral, and human variables. Understanding these relationships is particularly important for conservation management issues for endangered species. We describe techniques for the noninvasive collection and preservation of fecal samples from wild primates and the salvaging of parasitological information from primate hosts in the field.     

Primates and parasites: A case for a multidisciplinary approach

Examinations of primate parasitic infections can inform both primatologists and parasitologists about evolutionary and ecological relationships. Interspecific, intraspecific, and interindividual variation in parasitic infections may correlate with environmental, demographic, behavioral, and human variables. Understanding these relationships is particularly important for conservation management issues for endangered species. We describe techniques for the noninvasive collection and preservation of fecal samples from wild primates and the salvaging of parasitological information from primate hosts in the field.     

Conserving social-ecological systems in Indonesia: human-nonhuman primate interconnections in Bali and Sulawesi

An important question asked by primatologists and conservationists alike is: what is the relevance of primates and primate conservation for ecosystem conservation? The goal of this article is to contribute to this dialogue by advocating the use of a research perspective that focuses on the dynamics of human-nonhuman primate sympatry and interaction (i.e., ethnoprimatology) in order to better understand complex social-ecological systems and to inform their conservation management. This perspective/approach is based largely on the recognition that human primates are important components of all ecological systems and that niche construction is a fundamental feature of their adaptive success. To demonstrate the relevance of the human-nonhuman primate interface for ecosystem conservation, we provide examples from our research from two islands in the Indonesian archipelago: Bali and Sulawesi. In Bali, humans and long-tail macaques coexist in a system that creates favorable environments for the macaques. This anthropogenic landscape and the economic and ecological relationships between humans and monkeys on Bali provide insight into sustainable systems of human/nonhuman primate coexistence. In Lore Lindu National Park in Central Sulawesi, villagers and Tonkean macaques overlap in their use of both forest and cultivated resources. The finding that the Arenga pinnata palm is extremely important for both villagers and macaques points to a conservation management recommendation that may help protect the overall ecosystem; the cultivation and propagation of mutually important tree species at forest-agricultural ecotone as a means to curb crop raiding and to alleviate farmer's perceived need to clear additional forest.     

Primates as pets in Mexico City: an assessment of the species involved, source of origin, and general aspects of treatment

The large human populations in cities are an important source of demand for wildlife pets, including primates, and not much is known about the primate species involved in terms of their general origin, the length of time they are kept as pets, and some of the maintenance problems encountered with their use as pets. We report the results of a survey conducted in Mexico City among primate pet owners, which was aimed at providing some of the above information. We used an ethnographic approach, and pet owners were treated as informants to gain their trust so that we could enter their homes and learn about the life of their primate pets. We surveyed 179 owners of primate pets, which included 12 primate species. Of these, three were native species (Ateles geoffroyi, Alouatta pigra, and A. palliata). The rest were other neotropical primate species not native to Mexico, and some paleotropical species. Spider monkeys and two species of howler monkeys native to Mexico accounted for 67% and 15%, respectively, of the primate cases investigated. The most expensive primate pets were those imported from abroad, while the least expensive were the Mexican species. About 45% of the native primate pets were obtained by their owners in a large market in Mexico City, and the rest were obtained in southern Mexico. Although they can provide companionship for children and adults, primate pets are subject to a number of hazards, some of which put their lives at risk. The demand by city dwellers for primate pets, along with habitat destruction and fragmentation, exerts a significant pressure on wild populations in southern Mexico.     

Interspecific Interactions between Primates,Birds, Bats,and Squirrels May Affect Community Composition on Borneo

For several decades, primatologists have been interested in understanding how sympatric primate species are able to coexist. Most of our understanding of primate community ecology derives from the assumption that these animals interact predominantly with other primates. In this study, we investigate to what extent multiple community assembly hypotheses consistent with this assumption are supported when tested with communities of primates in isolation versus with communities of primates, birds, bats, and squirrels together. We focus on vertebrate communities on the island of Borneo, where we examine the determinants of presence or absence of species, and how these communities are structured. We test for checkerboard distributions, guild proportionality, and Fox's assembly rule for favored states, and predict that statistical signals reflecting interactions between ecologically similar species will be stronger when nonprimate taxa are included in analyses. We found strong support for checkerboard distributions in several communities, particularly when taxonomic groups were combined, and after controlling for habitat effects. We found evidence of guild proportionality in some communities, but did not find significant support for Fox's assembly rule in any of the communities examined. These results demonstrate the presence of vertebrate community structure that is ecologically determined rather than randomly generated, which is a finding consistent with the interpretation that interactions within and between these taxonomic groups may have shaped species composition in these communities. This research highlights the importance of considering the broader vertebrate communities with which primates co‐occur, and so we urge primatologists to explicitly consider nonprimate taxa in the study of primate ecology. Am. J. Primatol. 75:170‐185, 2013. © 2012 Wiley Periodicals, Inc.     

Welfare based primate rehabilitation as a potential conservation strategy: does it measure up?

Many primate species are threatened with extinction and are the focus of extensive conservation efforts including re-introduction, captive breeding and habitat conservation. Welfare-based rehabilitation (hereafter also ‘rehabilitation’) is a management strategy commonly used for primates, particularly those species targeted by the pet and bush meat trades. Rehabilitation of rescued primates typically has the dual motivation of welfare and conservation, but has not been assessed as a conservation strategy. As the species involved in rehabilitation are often endangered (e.g. chimpanzees, gorillas, orang-utans), it is important for rehabilitation projects to follow a ‘best practice’ model in order to increase positive outcomes. In this study, we compared the approaches of 28 welfare-based primate rehabilitation projects to the ‘IUCN guidelines for nonhuman primate re-introductions’, in addition to components of the ‘Best practice guidelines for the re-introduction of great apes’ in order to assess where additional work might be needed for released animals to contribute to conservation outcomes. Few projects examined complied with the guidelines for re-introduction, failing to incorporate important factors such as quarantine, long term post-release monitoring and training for predator awareness. Further development of species-specific rehabilitation guidelines may improve the outcomes of future rehabilitation projects. To support this, we recommend that detailed methods and results be published for all rehabilitation efforts, regardless of the outcome.     

Qualitative risk analysis of introducing Batrachochytrium dendrobatidis to the UK through the importation of live amphibians

The international amphibian trade is implicated in the emergence and spread of the amphibian fungal disease chytridiomycosis, which has resulted in amphibian declines and extinctions globally. The establishment of the causal pathogen, Batrachochytrium dendrobatidis (Bd), in the UK could negatively affect the survival of native amphibian populations. In recognition of the ongoing threat that it poses to amphibians, Bd was recently included in the World Organisation for Animal Health Aquatic Animal Health Code, and therefore is in the list of international notifiable diseases. Using standardised risk analysis guidelines, we investigated the likelihood that Bd would be introduced to and become established in wild amphibians in the UK through the importation of live amphibians. We obtained data on the volume and origin of the amphibian trade entering the UK and detected Bd infection in amphibians being imported for the pet and private collection trade and also in amphibians already held in captive pet, laboratory and zoological collections. We found that current systems for recording amphibian trade into the UK underestimate the volume of non-European Union trade by almost 10-fold. We identified high likelihoods of entry, establishment and spread of Bd in the UK and the resulting major overall impact. Despite uncertainties, we determined that the overall risk estimation for the introduction of Bd to the UK through the importation of live amphibians is high and that risk management measures are required, whilst ensuring that negative effects on legal trade are minimised.     

First field record of an introduced pet-feeder cockroach,Blaptica dubia (Serville, 1838) (Blattidae,Blaberinae), in a temperate zone of Japan

The expansion of the worldwide pet trade has increased the invasion risks from not only exotic pet animals, but also live feeder organisms for predatory pet animals. Here, we report the first field record of a tropical live feeder cockroach, Blaptica dubia (Serville, 1838), in the central part of Japan. This widely traded feeder insect may be able to colonize temperate zones because they were estimated to survive through two winters in Japan at temperatures close to the upper limits of their critical thermal minimum. Further field observations are needed to understand the behavior of this species in the wild and predict the risk of invasion in temperate zones.     

Preserving Preuss’s Red Colobus (<Emphasis Type="Italic">Piliocolobus preussi</Emphasis>): an Ethnographic Analysis of Hunting,Conservation, and Changing Perceptions of Primates in Ikenge-Bakoko,Cameroon

The futures of nonhuman primate species and human communities in shared landscapes rely on our ability to engage with and understand the complex histories and multiscalar aspects of human–animal relationships. We use the Critically Endangered Preuss’s red colobus (Piliocolobus preussi) as a case study to examine the important ways in which histories of multiscalar human–primate interactions play out in the village of Ikenge-Bakoko, Korup National Park, Cameroon. We contextualize ethnographic and catchment data from adult men (N?=?32) and women (N?=?31) within long-term diurnal primate monitoring datasets to better understand the relationships among hunting practices, local perceptions of diurnal primates, populations of P. preussi, and conservation management. Our data indicate a disconnect between local cultural definitions of “hunter” and Western assumptions as to the makeup and nature of this and other categories. We show that such contradictions can have negative outcomes for conservationists seeking to turn the science of establishing accurate off-take rates of prey species into practical management solutions. Using a single village as a focal point, we highlight the importance of an ethnoprimatological approach to understanding the intricate entanglements among conservation histories, subsistence strategies, and human and nonhuman primate lives. The application of ethnoprimatology is critical for twenty-first century primatologists who must navigate conservation concerns while also acknowledging and valuing the experiences of the human communities living alongside the primates we study.     

Is 2020 the year when primatologists should cancel fieldwork? A reply

The aim of this article is to explore the impact of coronavirus disease (COVID-19) pandemic on primate-related conservation work. The withdrawal of primatologists and conservation staff from field research can lead to a number of detrimental effects not just on conservation but also on local communities in low- and middle-income countries. Inequalities in access to health and financial insecurities may be drivers for the illegal wildlife trade and the lack of tourism and research activity may allow poachers to work with greater ease. The paper also looks at how conservation organizations and research bodies should modify their field protocols by developing robust occupational health policies that will not only make field work safer but also support local staff as they are likely to face the greatest threats to their physical health, psychological health, and economic loss from COVID-19. By adopting a One Health approach that considers the complex interactions between human and primate health, researchers will be able to find new ways of working not only to protect primates but understand how they adapt to the COVID-19 pandemic.     

The what and where of primate field research may be failing primate conservation

With approximately 30% of nonhuman primate species listed as critically endangered, the window of opportunity to conserve primates is closing fast. In this article, we focus on the degree to which publications in field primatology are biased in favor of particular taxa and field sites. We examined more than 29,000 peer‐reviewed articles and identified 876 field visits to 349 field sites. We found a highly clumped distribution by site and species. We also examined publication ethical statements and the extent to which they acknowledged local human communities (<5%). Due to a lack of consistency across publications, we provide recommendations for improving ethical statements and for evaluating research impact. Given the plight of primate biodiversity, these results suggest broader coverage of primate species and geographies, as well as more attention to the local human communities whose support is necessary if the intent is to have primate species in the wild in the 22nd century.     

What,where and when: spatial foraging decisions in primates

When exploiting the environment, animals have to discriminate, track, and integrate salient spatial cues to navigate and identify goal sites. Actually, they have to know what can be found (e.g. what fruit), where (e.g. on which tree) and when (in what season or moment of the year). This is very relevant for primate species as they often live in seasonal and relatively unpredictable environments such as tropical forests. Here, we review and compare different approaches used to investigate primate spatial foraging strategies: from direct observations of wild primates to predictions from statistical simulations, including experimental approaches on both captive and wild primates, and experiments in captivity using virtual reality technology. Within this framework, most of these studies converge to show that many primate species can (i) remember the location of most of food resources well, and (ii) often seem to have a goal‐oriented path towards spatially permanent resources. Overall, primates likely use mental maps to plan different foraging strategies to enhance their fitness. The majority of studies suggest that they may organise spatial information on food resources into topological maps: they use landmarks to navigate and encode local spatial information with regard to direction and distance. Even though these studies were able to show that primates can remember food quality (what) and its location (where), still very little is known on how they incorporate the temporal knowledge of available food (when). Future studies should attempt to increase our understanding of the potential of primates to learn temporal patterns and how both socio‐ecological differences among species and their cognitive abilities influence such behavioural strategies.     

Detection of TT virus among chimpanzees in the wild using a noninvasive technique

Zoonotic transmission and emergence of pathogens are serious threats to endangered populations of free-ranging primate species. Recent discovery of a nonpathogenic yet highly prevalent virus in human populations, TT virus (TTV), has prompted studies into the presence of this virus among captive individuals of other species of nonhuman primates. In this study, we screened captive primate species for TTV. In addition, we provide the first data on TTV infectionin free-ranging primates by noninvasive screening of three chimpanzee (Pan troglodytes sweinfurthii) commlunities. Phylogenetic relationships between virus isolates and those previously reported from hulman popullations, captive primates, and domesticated species are inferred. Our findings are discussed with respect to potential zoonotic events that may result from increased levels of human encroachlment into wild habitats.     

Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities

Background

Host-associated microbes comprise an integral part of animal digestive systems and these interactions have a long evolutionary history. It has been hypothesized that the gastrointestinal microbiome of humans and other non-human primates may have played significant roles in host evolution by facilitating a range of dietary adaptations. We have undertaken a comparative sequencing survey of the gastrointestinal microbiomes of several non-human primate species, with the goal of better understanding how these microbiomes relate to the evolution of non-human primate diversity. Here we present a comparative analysis of gastrointestinal microbial communities from three different species of Old World wild monkeys.

Methodology/Principal Findings

We analyzed fecal samples from three different wild non-human primate species (black-and-white colobus [Colubus guereza], red colobus [Piliocolobus tephrosceles], and red-tailed guenon [Cercopithecus ascanius]). Three samples from each species were subjected to small subunit rRNA tag pyrosequencing. Firmicutes comprised the vast majority of the phyla in each sample. Other phyla represented were Bacterioidetes, Proteobacteria, Spirochaetes, Actinobacteria, Verrucomicrobia, Lentisphaerae, Tenericutes, Planctomycetes, Fibrobacateres, and TM7. Bray-Curtis similarity analysis of these microbiomes indicated that microbial community composition within the same primate species are more similar to each other than to those of different primate species. Comparison of fecal microbiota from non-human primates with microbiota of human stool samples obtained in previous studies revealed that the gut microbiota of these primates are distinct and reflect host phylogeny.

Conclusion/Significance

Our analysis provides evidence that the fecal microbiomes of wild primates co-vary with their hosts, and that this is manifested in higher intraspecies similarity among wild primate species, perhaps reflecting species specificity of the microbiome in addition to dietary influences. These results contribute to the limited body of primate microbiome studies and provide a framework for comparative microbiome analysis between human and non-human primates as well as a comparative evolutionary understanding of the human microbiome.     

Plant DNA sequences from feces: potential means for assessing diets of wild primates

Analyses of plant DNA in feces provides a promising, yet largely unexplored, means of documenting the diets of elusive primates. Here we demonstrate the promise and pitfalls of this approach using DNA extracted from fecal samples of wild western gorillas (Gorilla gorilla) and black and white colobus monkeys (Colobus guereza). From these DNA extracts we amplified, cloned, and sequenced small segments of chloroplast DNA (part of the rbcL gene) and plant nuclear DNA (ITS-2). The obtained sequences were compared to sequences generated from known plant samples and to those in GenBank to identify plant taxa in the feces. With further optimization, this method could provide a basic evaluation of minimum primate dietary diversity even when knowledge of local flora is limited. This approach may find application in studies characterizing the diets of poorly-known, unhabituated primate species or assaying consumer-resource relationships in an ecosystem.