Primate Conservation: Unmet Challenges and the Role of the International Primatological Society

In the last 40 years, threats to the survival of wild primate populations have greatly increased. Primatologists have long been aware of these threats, and since 1978 have formulated plans to safeguard threatened species. Yet an increasing number of primate species face a high to extremely high risk of extinction. I asked 14 experienced field primatologists for their views on the most serious challenges to more effective primate conservation. They listed habitat loss and hunting as the major direct threats to primate survival, and noted that these activities are driven predominantly by the growth of human populations and the tendency of people to consume resources beyond their immediate survival needs. Two factors identified as most hindering effective action were a lack of political will and insufficient funding, while the main actions recommended to mitigate threats were to undertake more awareness-raising and make protected areas more effective. Such actions have long been recommended, so why have they not worked better? Perhaps the pressures on the natural world are too great to be countered, but I suggest also that too many of the various actors involved in conservation are overly driven by materialism and self-interest. I recommend more attention to the common good and a greater emphasis on the ethical and spiritual reasons for conservation. The International Primatological Society itself could have more vigorous debates on conservation policy at its congresses, and should consider the creation of regional chapters with the aim of promoting primatology in habitat countries.     

Distribution Survey and Threat Assessment of the Yellow-tailed Woolly Monkey (<Emphasis Type="BoldItalic">Oreonax flavicauda;</Emphasis> Humboldt 1812), Northeastern Peru

Peruvian yellow-tailed woolly monkeys (Oreonax flavicauda) are considered Critically Endangered (IUCN Categories A4c). The International Primatological Society also considers them one of the world’s 25 most endangered primate species and therefore a conservation priority. However, there is little concerted conservation action, and the existing protected area network may be inadequate to protect this species from extinction. Until recently this species has been the focus of few studies and its distributional limits remain unknown. I present results of a range-wide survey of Oreonax flavicauda in northeastern Peru. I conducted 53 presence/absence field surveys at 43 sites between March 2007 and March 2010, with data collected for an additional 7 sites from other researchers. I chose sites where the species was previously reported or following suggestions from predictive GIS modeling. Oreonax flavicauda was present at 35 sites, all presence records were in Ficus spp.–dominated cloud forests between 1500 and 2650 m above sea level. I give the geographical limits of this species distribution throughout the north, east, and west of its range; the exact extent of its range to the south requires further investigation. Oreonax flavicauda continues to be threatened throughout its range. The major threats I identified at the survey locations were the continued conversion of forests to cattle pasture, opening of new access routes into virgin areas, and both commercial and subsistence hunting. My results suggest that existing conservation measures may be inadequate at protecting this species but that substantial opportunities do exist. Further surveys need to be made in the southern distribution of this species to determine more accurately extant habitat.     

The neglected sense-olfaction in primate behavior, ecology, and evolution

This special issue emerged from a symposium held during the 20th Congress of the International Primatological Society in Torino, Italy, in August 2004. The symposium brought together scientists studying several different aspects of olfaction in primates. The topics addressed ranged from the morphology and physiology of the sensory apparatus, the genetics and chemistry of olfactory signals and the use of such signals in primate communication, to a comparative analysis of the role of olfaction in neural evolution. The papers in this issue reflect a surge of interest in diverse aspects of olfaction-an interest that has been stimulated by the more rigorous theoretical approaches and new techniques that have recently become available. This introduction briefly reviews past research on primate olfaction, summarizes the scope of this special issue, and provides a somewhat speculative glimpse of the future.     

我国灵长类的现状与保护

近些年来,国际上愈来愈认识到灵长类动物资源保护的重要性,在自然保护和拯救濒危物种方面作了种种努力。由于长期以来,人类对灵长类动物滥加捕杀和不合理的开发自然,特别是对于森林的毁坏,导致了栖息地的急剧改变,已使许多种类处于濒临灭绝的境地(Thorington,1974a,1974b,1978a,1978b)。国际自然与自然资源保护联盟编汇的红皮书（Red Data Book）录列了41种（亚种）属不同程度濒危种。濒危动植物种国际贸易公约（CITES）甚至已将全部灵长类分别列入国际间严禁或控制进出口贸易的名录之中。     

Is 2020 the year when primatologists should cancel fieldwork?

Year 2020 has brought the greatest global pandemic to hit the world since the end of the First World War. The severe acute respiratory syndrome coronavirus 2 and the resulting disease named coronavirus disease 2019 has brought the world to its knees both financially and medically. The American Society of Primatologists has postponed their annual meetings from the end of May 2020 until the end of September 2020, while the International Primatological Society have postponed their biennial congress from August 2020 to August 2021, which has also resulted in their 2022 meetings in Malaysia being pushed back until 2023. Here, I explore the potential dangers of pursuing any primate fieldwork during this pandemic on our study species, their ecosystems, and local peoples. I believe that the risk of bringing this virus into our study ecosystems is too great and that primatologists should cancel all field research until the pandemic ends or a vaccine/reliable treatment is widely available. This is the year we all must become One Health practitioners!     

Socioeconomic Contexts of Primate Conservation: Population,Poverty, Global Economic Demands,and Sustainable Land Use

Recent assessments by the International Union for Conservation of Nature (IUCN) indicate the existence of about 612 recognized primate species and subspecies (IUCN RedList, 2012), but close to 50% of these taxa are at risk of extinction as a result of human action. In this article, I call attention to underlying regional and global socioeconomic contexts of primate conservation. Using information from FAO and UN databases and other sources, I examine, for the Neotropics, sub‐Saharan Africa, and Southeast Asia, trends in forest loss and human demographics and social condition, discuss the impact of global market pressures upon primate habitats, and examine land‐use patterns that may favor primate conservation. Between 1990 and 2010, an estimated 149 million ha of forest were lost in the three regions and additional losses are expected in the future. Global human population will increase from 7 billion in 2012 to 9 billion in 2050. Currently, 2 billion people live in the three primate range regions under high levels of poverty. Large‐scale deforestation is related to global market demands, especially from developed and developing nations, for food (e.g., cattle), domestic animal feed (e.g., soybeans), biofuel‐based crops (e.g., oil palm), and industrial round wood. The growth of protected areas in the three regions has been steady for several decades, but it is not enough to ensure long‐term conservation of many primate taxa. Other conservations tools involving sustainable land use and biodiversity conservation corridors are required at the landscape level. The above assessment can easily be applied at the local level by primatologists, giving more precision to conservation initiatives. Am. J. Primatol. 75:30‐45, 2013. © 2012 Wiley Periodicals, Inc.     

New World primates,new frontiers: Insights from the woolly spider monkey,or muriqui (Brachyteles arachnoides)

Despite over 25 years of intensive research, much of our knowledge of primate behavior has been limited to a small number of Old World, semiterrestrial species. With the exception of chimpanzees, these species share consistent patterns of behavior, including aggressive competition between males, male dominance over females, male dispersal and female kin groups, that have come to characterize the Order Primates. However, as research has expanded to include a number of newly studied species, such generalizations about primate behavior are no longer appropriate. Data presented on the wooly spider monkey, or muriqui (Brachyteles arachnoides), provide examples of the ways in which traditional views of primate behavior are being reconsidered. In muriquis, and in several other New World monkeys, female kin groups do not occur because females disperse from their natal groups. In addition, aggressive competition between males is virtually absent; and, female muriquis appear to be codominant with males. Constraints on sexual dimorphism may help to explain why muriquis (and other New World primates) differ so fundamentally from the better known semi-terrestrial Old World monkeys.Logo of the 1988 International Primatological Society.     

Reducing the primate pet trade: Actions for primatologists

This commentary emerged from a panel presentation at the International Primatological Society Congress in Nairobi, Kenya, 2018. The goal was to provide regional updates on the status of primate removal from habitat countries, especially for the pet trade, and develop guidelines that could help primatologists address this critical problem. The trade in live primates includes those used as pets, in entertainment, and as subjects of biomedical experimentation, but here we focus on those primates destined for the pet trade. Such transactions are a hugely lucrative business, impacting hundreds of thousands of individuals annually and affecting the survival of wild populations. Being intimately familiar with primate social behavior, life history and biology, primatologists, whether they work with captive or wild primates, are in a unique position to understand the nature of the trade and attempt to counter its effects. In addition to updating the status of the primate pet trade, we provide recommendations that may help primatologists formulate a plan to deal, locally and regionally, with illegal trafficking in live primates. General guidelines include increasing awareness of local customs, policies and laws; developing collaborative research opportunities for local people; engaging in training/informational opportunities; and instructing on how to take action when encountering illegally-trafficked primates.     

Working from the Inside Out: Fostering Intrinsic Motivation and Expanding Our Criteria for Conservation Success

Primatological research is often associated with understanding animals and their habitats, yet practical conservation depends entirely on human actions. This encompasses the activities of Indigenous and local people, conservationists, and NGOs working on the ground, as well as more remote funders and policymakers. In this paper we explore what it means to be a conservationist in the 2020s. While many primatologists accept the benefits of more socially inclusive dimensions of research and conservation practice, in reality there remain many challenges. We discuss the role primatologists can play to enhance interdisciplinary working and their relationships with communities living in and around their study sites, and examine how increased reflexivity and consideration of one’s positionality can improve primatological practice. Emphasis on education and stakeholder consultation may still echo colonial, top-down dialogues, and the need for greater emphasis on genuine knowledge-sharing among all stakeholders should be recognised. If we are sincere about this approach, we might need to redefine how we see, consider, and define conservation success. We may also have to embrace more compromises. By evaluating success in conservation we explore how reflexive engagements with our positionality and equitable knowledge-sharing contribute to fostering intrinsic motivation and building resilience.

     

Reaching a Consensus: Terminology and Concepts Used in Coordination and Decision-Making Research

Research on coordination and decision-making in humans and nonhuman primates has increased considerably throughout the last decade. However, terminology has been used inconsistently, hampering the broader integration of results from different studies. In this short article, we provide a glossary containing the central terms of coordination and decision-making research. The glossary is based on previous definitions that have been critically revised and annotated by the participants of the symposium “Where next? Coordination and decision-making in primate groups” at the XXIIIth Congress of the International Primatological Society (IPS) in Kyoto, Japan. We discuss a number of conceptual and methodological issues and highlight consequences for their implementation. In summary, we recommend that future studies on coordination and decision-making in animal groups do not use the terms “combined decision” and “democratic/despotic decision-making.” This will avoid ambiguity as well as anthropocentric connotations. Further, we demonstrate the importance of 1) taxon-specific definitions of coordination parameters (initiation, leadership, followership, termination), 2) differentiation between coordination research on individual-level process and group-level outcome, 3) analyses of collective action processes including initiation and termination, and 4) operationalization of successful group movements in the field to collect meaningful and comparable data across different species.     

The primate palette: The evolution of primate coloration

Flip through The Pictorial Guide to the Living Primates¹ and you will notice a striking yet generally underappreciated aspect of primate biology: primates are extremely colorful. Primate skin and pelage coloration were highlighted examples in Darwin's² original discussions of sexual selection but, surprisingly, the topic has received little research attention since. Here we summarize the patterns of color variation observed across the primate order and examine the selective forces that might drive and maintain this aspect of primate phenotypic diversity. We discuss how primate color patterns might be adaptive for physiological function, crypsis, and communication. We also briefly summarize what is known about the genetic basis of primate pigmentation and argue that understanding the proximate mechanisms of primate coloration will be essential, not only for understanding the evolutionary forces shaping phenotypic variation, but also for clarifying primate taxonomies and conservation priorities.     

Dominance-seeking strategies in primates: an evolutionary perspective

The thesis advanced in this paper is that there are basic social influence strategies and attendant principles that are characteristic of social primates. A model for analyzing and comparing social influence strategies in primates, with particular attention to dominance-seeking strategies, is advanced. The utility of the model is illustrated by reference to studies of social influence strategies in baboons, chimpanzees, and humans. Emphasis is placed on the role of communication as the vehicle for social competence. Speculation is offered about the importance of the evolution of symbolic communication in expanding the repertoire of dominance-seeking strategies in human primates. Paper presented at the XII Congress of the International Primatological Society, Brasilia, Brasil 24–29, July, 1988.     

An overview of international wildlife trade from Southeast Asia

Wildlife trade is the very heart of biodiversity conservation and sustainable development providing an income for some of the least economically affluent people and it generates considerable revenue nationally. In Asia the unsustainable trade in wildlife has been identified as one of the main conservation challenges. Internationally, wildlife trade is regulated through the Convention on International Trade in Endangered Species of wild fauna and flora (CITES) to which all Southeast Asian nations are signatory. I obtained data on international trade in CITES-listed animals in the period 1998–2007. In all >35 million animals (0.3 million butterflies; 16.0 million seahorses; 0.1 million other fish; 17.4 million reptiles; 0.4 million mammals; 1.0 million birds) were exported in this period, 30 million (~300 species) of them being wild-caught. In addition 18 million pieces and 2 million kg of live corals were exported. Malaysia, Vietnam, Indonesia and China are the major exporters of wild-caught animals and the European Union and Japan are the most significant importers. Over this period exports in birds significantly decreased, trade in the other taxa either increased or remained stable. For all taxa but butterflies the vast majority of individuals represent wild-caught individuals. Records of illegal or undeclared international trade are scant but can be significantly larger than levels of official exports. It is concluded that there is an urgent need for better assessments of what levels of exploitation are sustainable (including exploring appropriate proxies for Non Detriment Findings), for initiatives to make regulatory mechanisms more effective (including the introduction of minimum mandatory standards and monitoring selected wildlife trade hubs), and for better licensing and registration. Funding for at least some of these initiatives can be obtained by imposing small levies on exports of CITES-listed wildlife.     

Recent advances in color vision research

The remarkable variation in color vision both among and within primate species is receiving increasing attention from geneticists, psychophysicists, physiologists, and behavioral ecologists. It is known that color vision ability affects foraging behavior. Color vision is also likely to have implications for predation avoidance, social behavior, mate choice, and group dynamics, and should also influence the choice of stimuli for cognitive experiments. Therefore, understanding the color vision of a study species is important and of particular significance to scientists studying species with polymorphic color vision (most platyrrhines and some strepsirrhines). The papers in this issue were inspired by a symposium held during the 20th Congress of the International Primatological Society at Turin, Italy, in August 2004. The aim of the symposium was to bring together research from a range of disciplines, using recent methodological advances in molecular, modeling, and experimental techniques, to help elucidate the evolution, ecological importance, and distribution of color vision genotypes and phenotypes. The symposium achieved its aim, and as with most research in expanding disciplines, there are surprises and many questions still to be answered. Further advances will be made using a combination of different approaches involving analyses at the level of molecu1es, types of cell and neural networks, detailed and long-term field work, modeling, and carefully controlled experimentation.     

The social, economic, and environmental contributions of Pan African Sanctuary Alliance primate sanctuaries in Africa

Over the last few decades, primate sanctuaries have become more numerous, particularly in Africa. Sanctuaries play an obvious and vital role in the battle against the illegal trade in wildlife and provide opportunities for local people to learn about the importance of protecting habitat and laws governing wildlife trade. Given the multi-disciplinary role of sanctuaries, the Pan African Sanctuary Alliance provides mechanisms to exchange best practices and establishes links to other conservation partners. In April 2011, the managers of the 22 Pan African Sanctuary Alliance members were surveyed in order to collect detailed information on the conservation activities of each sanctuary. The majority of the 22 sanctuaries conducted both on- and off-site education activities, engaging more than 429,000 people in education activities per year. Sanctuaries reported that they provided employment for over 550 local community members across Africa, as well as resources for community education and infrastructure, with an economic impact over $3 million per year. Sanctuaries were also involved in activities that promote law enforcement and believed that the activities they supported have led to better protection of primate habitats. The results of the survey demonstrate that sanctuaries have moved towards supporting and implementing community development activities aimed at poverty reduction, while conducting conservation activities. While Pan African Sanctuary Alliance sanctuaries were initially established to provide care and housing for orphaned, confiscated and displaced primates, this paper demonstrates how sanctuaries have combined ex-situ with in-situ initiatives to support social, economic, and environmental progress in primate range countries in Africa.     

Ethnoprimatology without Conservation: The Political Ecology of Farmer–Green Monkey (<Emphasis Type="Italic">Chlorocebus sabaeus</Emphasis>) Relations in St. Kitts,West Indies

The driving force behind the mixed-methods ethnoprimatological endeavor is to effectively conserve nonhuman primates. In this article, I argue that ethnoprimatological research can meet this goal only by discarding the purely science views of conservation that dominate the current literature. By considering more than local ecological perceptions, their ideological agendas, and their levels of power via a political ecology framework, ethnoprimatologists can simultaneously socialize the ecosystems we study and contribute our ethological skills to advance traditionally humanist disciplines’ increased attention to a wider field of agents and structures that matter. I support these arguments through an examination of farmer–green monkey (Chlorocebus sabaeus) relations in St. Kitts. Kittitian farmers’ narrative revealed three scales that collectively construct what is locally known as “the monkey problem:” increased rates of local contact between farmers and monkeys on farms, contestations over the future of St. Kitts’ land, and global debates over appropriate strategies to manage the monkey population. I show that although “the monkey problem” in St. Kitts does not involve an endangered or threatened species, my analysis of this construct has implications for primate populations that are threatened. This is because the root cause of this “problem”—the globalized discourse of nature conservation overpowering and problematizing local views about people–animal interactions—characterizes so many of the locales home to primates of conservation concern.     

Molecular systematics and conservation of the langurs and leaf monkeys of South Asia

Numerous morphology-based classification schemes have been proposed for langurs and leaf monkeys of South Asia but there is very little agreement between them. An incorrect classification scheme when used as a basis for biogeographic studies can support erroneous hypotheses. Further, lack of taxonomic resolution will also confound conservation efforts, given that conservation biologists use traditional morphology-based-classification schemes to prioritize species for conservation. Here, I have revisited recent molecular phylogenetic studies done on langurs and leaf monkeys of South Asia. Results from these studies are in turn used to derive a rational and scientific basis for prioritizing species for conservation. Molecular data support the classification of langurs of the Indian subcontinent—Hanuman, Nilgiri and purple-faced langurs—in the genus Semnopithecus, whereas Phayre’s leaf monkey along with other Southeast Asian leaf monkeys form another distinct clade (Trachypithecus). The phylogenetic position of capped and golden langurs remains unresolved. Molecular data suggest that they are closely related to each other but this group might have evolved through past hybridization between Semnopithecus and Trachypithecus. Additionally, genetic data also support the splitting of the so-called Hanuman langurs into at least three species. The scores for taxonomic uniqueness of langurs and leaf monkeys of South Asia were revised using this molecular phylogeny-based classification. According to the revised scores, Phayres leaf monkey and golden langur are priority species for conservation followed by capped and Nilgiri langurs.     

Sleep and nesting behavior in primates: A review

Sleep is a universal behavior in vertebrate and invertebrate animals, suggesting it originated in the very first life forms. Given the vital function of sleep, sleeping patterns and sleep architecture follow dynamic and adaptive processes reflecting trade-offs to different selective pressures. Here, we review responses in sleep and sleep-related behavior to environmental constraints across primate species, focusing on the role of great ape nest building in hominid evolution. We summarize and synthesize major hypotheses explaining the proximate and ultimate functions of great ape nest building across all species and subspecies; we draw on 46 original studies published between 2000 and 2017. In addition, we integrate the most recent data brought together by researchers from a complementary range of disciplines in the frame of the symposium “Burning the midnight oil” held at the 26th Congress of the International Primatological Society, Chicago, August 2016, as well as some additional contributors, each of which is included as a “stand-alone” article in this “Primate Sleep” symposium set. In doing so, we present crucial factors to be considered in describing scenarios of human sleep evolution: (a) the implications of nest construction for sleep quality and cognition; (b) the tree-to-ground transition in early hominids; (c) the peculiarities of human sleep. We propose bridging disciplines such as neurobiology, endocrinology, medicine, and evolutionary ecology, so that future research may disentangle the major functions of sleep in human and nonhuman primates, namely its role in energy allocation, health, and cognition.     

Thirty Years of Research in Kibale National Park,Uganda, Reveals a Complex Picture for Conservation

Kibale National Park, Uganda, has a rich and abundant primate community and a complicated history of anthropogenic disturbance. Moreover, it has been the focus of over 30 yr of research and has received considerable attention from nongovernmental and governmental conservation organizations. As a result, Kibale serves as a valuable case study with which to evaluate the factors that regulate primate population density and the challenges of deriving generalizations for conservation. We review the impact of logging and forest fragmentation on primate population density and trace the efficacy of various conservation strategies. A 28-yr comparison of primate abundance in logged and unlogged forests and a 10-yr study of forest dynamics showed that primate recovery in logged areas is generally slow or not occurring at all for some species, which is likely driven by the fact that the forest is not recovering as expected. No primate species characteristic predicted their ability to live in forest fragments around Kibale. While a nutritional model was useful to predict the abundance of colobus in forest fragments outside of Kibale, a 5-yr study revealed that human land-use practices are more fundamentally shaping population dynamics. We evaluate data on primate abundance in light of Milton’s protein/fiber model to predict colobine biomass. We demonstrate that while the model can predict colobus biomass in pristine habitats, the 2 colobus species respond differently to disturbance. We offer suggestions for future conservation research and consider strategies to conserve forested national parks based on experiences gained over 30 yr.     

Primate Seed Dispersal and Forest Restoration: An African Perspective for a Brighter Future

Primate seed dispersal is a vital, but complex, ecological process that involves many interacting agents and plays important roles in the maintenance of old-growth forest, as well as in the development of regenerating forest. Focusing primarily on African examples, in this article we briefly review the ecological process of primate seed dispersal, highlighting understudied and contentious topics, and then we discuss how our knowledge on primate seed dispersal can promote both forest restoration and primate conservation. Though it is frequently claimed that primates are critically important for the maintenance of diverse tropical forest ecosystems, we believe that more empirical evidence is needed to support this claim. Confounding factors can often be difficult to rule out and long-term studies extending beyond the seedling or sapling stage are very rare. In addition, though primates are critical for initial seed dispersal of many tree species, spatial and temporal variation in post-deposition processes, such as secondary seed dispersal and predation by rodents, can dramatically alter the initial patterns generated by primates. However, given the need for immediate conservation action to prevent further primate extinctions, we advocate that the knowledge about primate seed dispersal be used in formulating informed conservation plans. One prominent area where this knowledge will prove extremely valuable is in forest restoration efforts. To aid in the development of such efforts, we pose five questions, the answers to which will help facilitate forest restoration becoming a useful tool in strategies designed to conserve primates.