18.1: Current Conservation of Nonhuman Primates

We are field primatologists interested in understanding primates in their natural environments and in contributing to their conservation. Our research focuses on a diversity of primate species that occur in a wide range of habitats throughout the tropics; however, these species and their habitats are subject to many similar threats. As human populations continue to grow (Figure 18.1.1), primates are being pushed out of their natural home ranges and are being forced to occupy increasingly smaller and more isolated patches of land. Humans and primates are sharing more spaces with one another, making it easier for primates to be hunted or captured and for diseases to spread from humans to primates (and vice versa). Even when primates are not directly threatened by human activities, human-induced climate change is altering local ecosystems at an alarming rate. Local political instability exacerbates all of these problems. Our research causes us to think about these issues on a daily basis. Understanding how these threats affect the primates we study is a very important part of what we do. Ultimately, the research of field primatologists like us is important for documenting the status of wild primate populations, as well as for understanding how they respond to these threats and for gaining insights into the kinds of efforts that can help to improve their chances of survival in an uncertain future.

This appendix begins with a review of the current status of primates and the criteria used in these assessments. We then describe the major threats to primates, explain why primates are important, and consider what can be done to improve their chances. We conclude with a brief consideration of the future for primates.

Figure \(\PageIndex{1}\): World population growth by region. Global populations are projected to exceed 11 billion people by 2100 (UN Population Division 2017).

Diversity of Primates

The order Primates is one of the most diverse groups of mammals on the planet, with 504 species in 79 different genera currently recognized (Figure 18.1.2; Estrada et al. 2017). Recently new genera, species, and subspecies of nonhuman primates (henceforth, simply “primates” ) have been recognized, in some cases as a result of new discoveries and new data, but also because of revisions to taxonomic classification systems based on different species concepts (Groves 2014; Lynch Alfaro et al. 2012; Rylands and Mittermeier 2014).

Figure \(\PageIndex{2}\): The global distribution and species richness of primates and the percentage of those threatened with extinction and declining populations. The numbers next to each geographic area indicate the current species present in that location. The bars below show the percentage of species threatened with extinction (in green) and the percentage of species with declining populations in each region (in red).

Figure \(\PageIndex{3}\): Mountain gorilla (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Mountain gorillas are classified as endangered and are only found in the Virungas area of Rwanda and the Democratic Republic of Congo and the Bwindi forest of Uganda (Hickey et al. 2018; Kalpers et al. 2003). This species has suffered tremendously due to habitat destruction, poaching, political unrest, and war (Kalpers et al. 2003).

Figure \(\PageIndex{4}\): A female northern muriqui (Brachyteles hypoxanthus) with infant at the Feliciano Miguel Abdala Private Natural Heritage Reserve outside of Caratinga, Brazil. Muriquis are found exclusively in the Atlantic Forest of southeastern Brazil. The destruction and fragmentation of these forests have caused this species to be listed as Critically Endangered (Strier et al. 2017). Although still threatened, the continued efforts of the Muriqui Project of Caratinga have brought this species back from the brink of extinction.

Wild primates occur in 90 countries around the world, but two-thirds of all species are found in only four countries: Brazil, Madagascar, Democratic Republic of Congo, and Indonesia (Estrada et al. 2017; Estrada et al. 2018). An estimated 60% of primate species are threatened with extinction and 75% are experiencing population declines (Estrada et al. 2017, see Figure 18.1.2). Yet despite these discouraging statistics, there are a growing number of populations recovering as a result of research and conservation efforts. For example, the population of mountain gorillas (Figure 18.1.3) initially studied by Dian Fossey in Rwanda in 1967 has increased from 250 gorillas in 1981 to 339 in 2008 as a result of ongoing research and conservation efforts that include highly controlled ecotourism (Robbins et al. 2011). Similarly, one population of northern muriqui monkeys (Figure 18.1.4) inhabiting a small privately owned forest fragment in southeastern Brazil’s Atlantic Forest increased from about 50 individuals to nearly 350 individuals as a result of increased habitat protection over the course of the Muriqui Project of Caratinga, a long-term field study initiated more than 35 years ago by one of the authors of this appendix (Strier and Mendes 2012).

International Union for the Conservation of Nature (IUCN)

In conservation, it is crucial to have a global standard to assess and recognize the conservation status of species. The International Union for the Conservation of Nature (IUCN) formed the Red List for Threatened Species in 1994 to determine species extinction risks (IUCN 2017). Scientists submit assessments of species to the IUCN, which are subsequently categorized based on the size and distribution of species’ numbers and available habitat. The categories range from “data deficient,” when not enough is known, to “least concern,” “near threatened,” “vulnerable,” “endangered,” “critically endangered,” “extinct in the wild,” and “extinct.” Threatened species are classified as “vulnerable,” “endangered,” or “critically endangered,” with the most critically endangered species being those whose numbers are fewer than 250 mature individuals and continuing to decline or whose habitats are severely fragmented ( IUCN 2017).

Table 18.1.1: International Union for Conservation of Nature (IUCN) Criteria for Threatened Taxa. Updated from Strier 2011a. Source: Simplified and condensed from IUCN Species Survival Commission, 2012.

Critically Endangered (CR): Facing an extremely high risk of extinction in the wild due to any of the following: A. Reduction in population size of 80%–90% over the last ten years or three generations, depending on the causes and reversibility of the reductions; B. Extent of occurrence <100 km2 or area of occupancy <10 km2 or both; C. Population size estimated to number fewer than 250 mature individuals and to be declining or unevenly distributed; D. Population size estimated to number fewer than 50 mature individuals; E. Probability of extinction within ten years or three generations is at least 50%. Endangered (EN): Facing a very high risk of extinction in the wild due to any of the following: A. Reduction in population size of 50%–70% over the last ten years or three generations, depending on the causes and reversibility of the reductions; B. Extent of occurrence <5000 km2 or area of occupancy <500 km2 or both; C. Population size estimated to number fewer than 2,500 mature individuals and to be declining or unevenly distributed; D. Population size estimated to number fewer than 250 mature individuals; E. Probability of extinction within 20 years or five generations is at least 20%. Vulnerable (VU): Facing a high risk of extinction in the wild due to any of the following: A. Reduction in population size of 30%–50% over the last ten years or three generations, depending on the causes and reversibility of the reductions; B. Extent of occurrence <20,000 km2 or area of occupancy <2000 km2 or both; C. Population size estimated to number fewer than 10,000 mature individuals and to be declining or unevenly distributed; D. Population size estimated to number fewer than 1,000 mature individuals; E. Probability of extinction within 100 years is at least 10%.

The IUCN has a committee specifically dedicated to primates, the IUCN Species Survival Commission (SSC) Primate Specialist Group. This group collaborates with the International Primatological Society (IPS), Conservation International (CI), and the Bristol Zoological Society (BZS) every two years to publish “Primates in Peril: The World’s 25 Most Endangered Primates.” These lists are created at IPS open meetings and are intended to focus attention on all endangered primates by highlighting the plights of some of the most critically endangered (Schwitzer et al. 2017).

Identifying Priorities in Primate Conservation

It is important to consider extinction risk in making conservation decisions, thus the IUCN Red list and the “Primates in Peril” reports are factors in deciding how to allocate resources and funding. Some primate species are found only in biodiversity hot spots, or areas that contain high levels of species diversity and include primates that are endemic to the area and genetically unique (Sechrest et al. 2002). Hot spots are often considered conservation priorities because protecting these areas can result in the protection of large numbers of species. In addition, some conservation organizations focus on highly charismatic primate species (e.g., primates that are large, closely related to humans, or well-known from zoos, such as the golden lion tamarin) to garner attention and resources for conservation. However, dramatic declines of charismatic species indicate that charisma is not enough (Estrada et al. 2017). For example, it is estimated that the population of Bornean orangutans (Pongo pygmaeus) decreased by 100,000 individuals between 1999 and 2015, despite being very popular with the general public (Voigt et al. 2018). In making conservation decisions, primatologists may also consider the importance of genetically unique primates, such as the aye-aye (Daubentonia madagascariensis), the last remaining species within its genus in order to preserve evolutionary history (Strier 2011a).

PRIMATE SIGNIFICANCE

Ecological Significance of Primates

Primates play a key role within their ecosystems, often acting as important contributors to forest community structure by aiding in seed dispersal and pollination of angiosperms and other plant species. Variability in traits such as diet, gut anatomy, and movement patterns influence the spatial landscape of dispersed seeds (Russo and Chapman 2011). Frugivorous primates that range widely are considered the greatest contributors to the dispersal of seeds, as they often either swallow seeds whole, as is common for most Neotropical frugivorous primates (Figure 18.1.5), or spit seeds out, as is common for primates with cheek pouches in Africa and Asia. These primates can contribute greatly to the diversification and regeneration of forest communities by traveling long distances after consumption and depositing seeds away from the parent plant within heterogeneous landscapes (Strier 2017; Terborgh 1983). Frugivory and seed dispersal are critical plant-animal relationships (Russo 2017). Bach Thanh Hai and colleagues (2018) found that yellow-cheeked crested gibbons (Nomascus gabriellae) in Southeast Asia were the most effective seed disperser for the Pacific walnut tree. Gibbons dispersed seeds via consumption anywhere from 4 m  to 425 m from the parent tree. Seeds defecated by gibbons had higher germination and success rates than those spit by macaques in the same forest.

Some species of primate may also act as pollinators for local plant species. These primates are attracted to the nectar and flowers of the plant, which often leave pollen on their faces and fur, subsequently spreading pollen to conspecifics when the primate moves to a new location. Jeremy Hogan and colleagues (2016) suggest that white-faced capuchins (Cebus capucinus imitator) may have a beneficial effect on certain plant species in Costa Rica. Other primates may have co-evolved a plant-pollinator relationship. Data indicate that the black and white ruffed lemur (Varecia variegata) is reliant on the nectar of the traveler’s palm (Ravenala madagascariensis) during specific times of the year, allowing pollen to stick to the ruff of their necks.  This, along with the notion that no other species visit the travel’s palm during certain times of the year, indicate that this plant species may be dependent on nonflying mammals for pollination (Kress et al. 1994).

By acting as seed dispersers and pollinators, primates can aid in the reproductive success, regeneration, and diversification of plants within their ecosystems. The significance of these relationships is only becoming more apparent as habitats continue to be fragmented and destroyed.  As habitats dwindle, the ability to regenerate healthy forest systems is crucial to the health and survival of tropical forest systems worldwide (Stier 2017).

Bioanthropological Significance of Primates

Figure \(\PageIndex{5}\): Fecal matter with seeds from the large-bodied northern muriqui (Brachyteles hypoxanthus). When primates consume fruit, they often swallow seeds whole. This photo shows several intact seeds within feces, after ingestion. Primates are often effective seed dispersers because of the long distances they travel and the fertilizing properties of their dung.

The study of non-human primates has been an integral component of anthropology for many decades. Even before Sherwood Washburn advocated in The New Physical Anthropology (1951) that primates could be studied as living reference for hominin behaviors, anthropologists like Margaret Mead recognized that studies of wild primates could contribute to biological and sociocultural anthropology in many ways (Strier 2011b). Primatology in Japan, the U.S., and Europe grew out of a desire to better understand ourselves. Thus, research in the 1960s and 1970s largely focused on species such as chimpanzees (Pan spp.) or baboons (Papio spp.) that are closely related to humans phylogenetically or live in environments similar to those occupied by early hominins (Haraway 1991; Strum and Fedigan 1999; Washburn 1973). Since those early days, biological anthropological primatology has broadened to include primates from around the world (Strier 2003, 2018a). The inclusion of diverse taxa from what were then-understudied regions challenged notions of “typical” primate behavior, such as the idea that aggression was the main mechanism for maintaining hierarchical social relationships (Strier 1994).

Anthropologists draw broadly from primate studies to explore the many facets of human behavior and evolution. For example, studies demonstrating the tool-using capabilities of wild chimpanzees (Pan troglodytes) and capuchin monkeys (Sapajus spp., formerly Cebus spp.) show that similar ecological pressures and intelligence contribute to tool-using behaviors, rather than just phylogenetic relatedness to humans (Fragaszy et al. 2004; Inoue-Nakamura and Matsuzawa 1997). Similarly, studies of modern primate morphology are frequently used to assess how locomotor style or behaviors (such as foraging) are related to anatomy, and this knowledge can then be used to assess the skeletal and dental anatomy of fossil hominins. Studies of microscopic wear patterns, for example, use living primates as analogues to understand wear patterns generated by different food items as well as the rapidity with which changes to these patterns can occur (Teaford and Oyen 1989; Ungar and Sponheimer 2011). Living nonhuman primates provide a comparative sample with which we deepen our understanding of the evolutionary mechanisms that shaped human evolution.

Cultural Significance of Primates

For as long as our species has existed, groups of people have lived alongside nonhuman primates and engaged with them in varying ways (Fuentes 2012). The development and expansion of the field of ethnoprimatology, the study of the human–nonhuman primate interface, has encouraged researchers from sociocultural anthropology and primatology to investigate these points where primates and humans interact and influence each other in surprising ways (Fuentes 2012; Sponsel 1997). Primates are viewed by many as exceptional animals for the ways in which they reflect elements of humanness, stimulating many thousands of people to observe their exhibits at zoos and sanctuaries throughout the world. However, the significance of these animals to diverse cultures goes beyond anthropocentrism and touches on aspects of ecology, religion, and social systems. Primates are common figures in religion and myth, appearing sometimes as gods or deities themselves (e.g., the Hindu deity Hanuman) and sometimes as mediators between the human and spirit realms (Alves et al. 2017; Peterson 2017; Wheatley 1999). Primates have additional cultural significance as figures in folklore and legend, and they are often ascribed human-like characteristics in many of these narratives (Cormier 2017). These stories often inform local taboos that may discourage the consumption of particular species or deforestation of particular areas (Osei-Tutu 2017; Roncal et al. 2018; Sicotte 2017).

The role that primates play in human cultures is complex and varies significantly with local history, religious practice, and economies. Among the Awa Guajá of eastern Amazonia, for example, primates are considered a part of the humans’ extended kin network and are protected as such, yet they also constitute an important source of dietary protein and are hunted regularly (Cormier 2003). In other primate habitat countries, such as Bali, primates play a significant role in religious practice. Long-tailed macaques (Macaca fascicularis) in Bali are frequently found in the forests surrounding Hindu temples and will consume offerings left by residents and tourists once festivals or rituals are concluded (Fuentes 2010; Wheatley 1999). These macaques are seen by some as mediators between the natural world and the spiritual world that transports offerings from one realm to another (Wheatley 1999). Investigating how local residents view primates—for example, whether species are considered sacred or not—is a vital component of conservation programs in these areas (Peterson and Riley 2017). Studying the interface between human and nonhuman primates, and what factors (e.g., local religious practices, taboos, etc.) influence these interactions can lead to more holistic conservation planning and implementation.

Economic Significance of Primates

One of the most promising ways that primates can benefit people is through the potential to stimulate local economies from ecotourism. Ecotourism differs from traditional tourism in three main ways: it focuses on nature-based attractions, it provides learning opportunities, and its tourism management practices adhere to economic and ecological sustainability (Fennell and Weaver 2005). Primates are charismatic megafauna, meaning that they are large animals (oftentimes mammals) that elicit mass appeal. They have the possibility to draw tourists, which can in turn bring revenue to lower-income communities found near primate habitats. This attraction from tourists, along with revenue-sharing, can then stimulate local populations to have more positive attitudes toward protected areas and become more invested in the well-being and protection of primates and their habitats (Archabald and Naughton-Treves 2001).

Figure \(\PageIndex{6}\): Bonnet macaques (Macaca radiata) being fed by tourists. Food sharing and other forms of direct contact between humans and primates provide opportunities for disease transmission. Despite most ecotourists understanding the dangers of human-primate contact, according to a recent survey over half would still opt to touch or feed primates if possible (Muehlenbein 2017). Though nature-based tourism may have benefits for local communities (Spencely et al. 2010), a better understanding of what drives tourists to engage with primates is necessary to minimize direct human-primate interactions.

Perhaps one of the greatest success stories of nature-based tourism revolves around the mountain gorillas (Gorilla beringei beringei) of Rwanda. After internal conflict plagued Rwanda during the 1990s, the Virungas area developed gorilla-based tourism as a means to aid in socioeconomic development and to bring stability to the region. This process not only helped to increase mountain gorilla populations but was also able to generate enough income to cover the operation costs of three national parks (Maekawa et al. 2013). Research indicated that low-income individuals living around Parc National des Volcans in Rwanda could garner direct income as well as nonfinancial benefits (such as the development of schools and hospitals) from gorilla tourism in the region (Spencely et al. 2010). Although ecotourism has the potential to alleviate poverty situations for local populations and aid in the overall sustainability of natural habitats, it can also bring a suite of new problems to areas.  It can overcrowd national parks and over-habituate primates (Figure 18.1.6), increase potential disease transfer between humans and primates, and exacerbate corruption, which often pulls money away from local communities (Hvenegaard 2014; Muehlenbein et al. 2010).