Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats—mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world’s primates and the costs of their loss to ecosystem health and human society is imperative.

Keywords

Nonhuman primates (primates hereafter) are of central importance to tropical biodiversity and to many ecosystem functions, processes, and services. They are our closest living biological relatives, offering critical insights into human evolution, biology, and behavior and playing important roles in the livelihoods, cultures, and religions of many societies. Unsustainable human activities are now the major force driving primate species to extinction. Here, we combine the most frequently used standard for species conservation status [the International Union for Conservation of Nature (IUCN) Red List] with data from peer-reviewed scientific literature and from the United Nations databases to evaluate human-induced threats to primate survival. We examine trends in forest loss resulting from regional and global economic pressures and discuss the impacts of hunting, illegal trade, and other anthropogenic threats on primate populations. We also model agricultural expansion into the 21st century and identify expected spatial conflict within primate range areas. We assess the current level of scientific knowledge available for individual primate taxa, and we highlight the ecological, social, cultural, economic, and scientific importance of primates, as well as the global consequences of their population declines. We also consider future research needs and advances in technology for monitoring human-induced environmental changes that affect primate populations. Finally, we propose a conceptual model to guide the development of global, regional, and local approaches to promote primate conservation while at the same time attending to human needs. The goal of this review is not to produce a list of threats but rather to urge attention to the multiple global and regional anthropogenic factors that imperil primates worldwide and to encourage the development of sustainable and effective solutions that enhance primate survival in the medium and long term.

Assessment of threat level is according to the IUCN Categories and Criteria VU (Vulnerable), EN (Endangered), and CR (Critically Endangered). Number in parentheses after each family indicates the number of species recognized in the family. Data for each species are indicated in tables S1 to S4. Notably, there are threatened species in all 16 primate families. Ten families have more than 50% of their species threatened (broken line at 50%). Note that the graph is only for the Threatened IUCN categories. Families not showing 100% values may have some species classified as Near Threatened (NT), Least Concern (LC), Data Deficient (DD), and Not Evaluated (NE) (see tables S1 to S3). Upon revision of the taxonomy of Malagasy lemurs, a number of taxa once thought to be widespread are now highly threatened; a similar scenario is envisioned for the galagids, where there appears to be a large number of newly recognized species with limited ranges. Taxonomy is based on previous works ( 1 – 3 ).

Using information from the IUCN and our current assessment, we estimate that ~60% of primate species, from all 16 extant families, are threatened with extinction because of unsustainable human activities ( Figs. 1 and 2 and tables S1 to S4). Threats to primates are widespread: 87% of species in Madagascar are threatened, as are 73% in Asia, 37% in mainland Africa, and 36% in the Neotropics ( Fig. 1 and figs. S2B and S3A). The populations of 75% of primate species are decreasing globally ( Fig. 1 and fig. S3B). Considering the large number of species currently threatened and experiencing population declines, the world will soon be facing a major extinction event if effective action is not implemented immediately.

Geographic distribution of primate species. Numbers in red by each region refer to the number of extant species present. The bars at the bottom show the percent of species threatened with extinction and the percent of species with declining populations in each region. Percentage of threatened species and percentage of species with declining populations in each region from tables S1 to S4. Geographical range data of living, native species from the IUCN Red List (www.iucnredlist.org) are overlaid onto a 0.5° resolution equal-area grid. In cases in which a species’ range was split into multiple subspecies, these were merged to create a range map for the species. Mainland Africa includes small associated islands.

The order Primates is one of the most species-rich groups of mammals, surpassed only by the orders Chiroptera (bats, 1151 species) and Rodentia (rodents, 2256 species) ( 1 , 2 ). The most recent taxonomic compilation (April 2016) lists 701 extant taxa belonging to 504 species from 79 genera and 16 families (tables S1 to S4 and Supplementary Text) ( 2 – 5 ). Primates occur in four regions—the Neotropics (171 species), mainland Africa (111 species), Madagascar (103 species), and Asia (119 species) ( Fig. 1 )—and are present naturally in 90 countries; however, two-thirds of all species occur in just four countries—Brazil, Madagascar, Indonesia, and the Democratic Republic of the Congo (DRC) (figs. S1 and S2A). These countries represent high-priority areas for primate conservation. The large majority of primates inhabit tropical moist lowland forests, but they also occur in tropical dry forests, mangrove vegetation above high-tide levels, moist montane forests, high-elevation (from 1000 to >4000 m) deciduous and broadleaf temperate forests, savannas, grasslands, inland wetlands, rocky areas, and even deserts ( 2 , 4 ). The body mass of living primates ranges from 30 g in Madame Berthe’s mouse lemur (Microcebus berthae) to about 200 kg in male western and eastern gorillas (Gorilla gorilla and Gorilla beringei, respectively) (Supplementary Text) ( 2 , 4 , 5 ).

FACTORS THAT THREATEN PRIMATE POPULATIONS

The IUCN indicates that the main threats to primate species are loss of habitat due to agriculture (76% of species), logging and wood harvesting (60%), and livestock farming and ranching (31%), as well as direct loss due to hunting and trapping (60%) (fig. S4A). Other threats, such as habitat loss due to road and rail construction, oil and gas drilling, and mining, affect 2 to 13% of primate species, and there are also emerging threats, such as pollution and climate change (fig. S4B and table S5). Globally, agriculture is the principal threat, but secondary threats vary by region. For example, livestock farming and ranching negatively affect 59% of primate species in the Neotropics. In contrast, in mainland Africa, Madagascar, and Asia, hunting and trapping affect 54 to 90% of the species. Logging is the third greatest threat to primates in all regions (fig. S4A).

Land-cover changes, global market demands, and industry-driven deforestation Global market demands for nonarboreal (for example, soybeans, sugar cane, and rice) and arboreal crops (for example, oil palm and natural rubber), livestock (particularly cattle), and tropical hardwoods have resulted in a process of rapid and widespread industry-driven deforestation in the Neotropics, mainland Africa, Madagascar, and Asia (Supplementary Text and fig. S5, A to F) (6). For example, between 1990 and 2010, agricultural expansion in primate range regions was estimated at 1.5 million km2 (an area three times that of France) and forest cover loss at 2 million km2 (Fig. 3 and fig. S6, A to C). Increasing global demand for oil palm products is a major driver of recent severe declines in Sumatran and Bornean orangutan (Pongo abelii and Pongo pygmaeus, respectively) numbers and a serious risk for African apes because large segments of existing populations occur outside protected areas (7–10). Moreover, future oil palm development is likely to threaten forested areas in South America and Africa (10), which is projected to result in severe negative consequences for primate populations in those regions (fig. S5C). The expansion of rubber plantations in southwest China has caused the near extinction of the northern white-cheeked crested gibbon (Nomascus leucogenys) and the Hainan gibbon (Nomascus hainanus) (11). Similarly, deforestation due to the establishment of rubber plantations in India is reported to have severely affected the Bengal slow loris (Nycticebus bengalensis), the western hoolock gibbon (Hoolock hoolock), and Phayre’s langur (Trachypithecus phayrei) (11, 12). Modeling the overlap between primate species’ distributions and forecasted future agricultural production for the 21st century indicates that regions predicted to undergo the greatest agricultural expansion over the next decades comprise 68% of the global area currently occupied by primates (Fig. 4). This will result in unprecedented spatial conflict with 75% of primate species worldwide (Supplementary Text). Therefore, the implementation of policies to divert agricultural expansion to areas where it is likely to result in the least environmental impacts is essential to reduce spatial conflicts between primate-rich areas and the expanding agricultural frontier (13). Fig. 3 Agricultural expansion and declines in forest cover for the period 1990–2010 in primate range regions. A rapid expansion of agriculture in primate range regions has been paralleled by a sharp decline in forest cover in the 20-year period considered. Trends for each individual region are shown in fig. S6 (A to C). Data for Africa include Madagascar (source of raw data, FAOSTAT: faostat.fao.org/site/377/DesktopDefault.aspx?PageID=377#ancor. Consulted June 2016). Fig. 4 Global patterns of forecasted agricultural expansion for the 21st century in primate range regions and estimated range contraction. (A) Estimated current global primate distributions. (B) The predicted 21st century expansion of agriculture estimates a spatial overlap with about 75% of primate species habitat worldwide. Red areas indicate higher spatial overlap between agricultural expansion and primate habitat. Blue areas indicate limited spatial conflict. Agricultural expansion represents a synthesis of the expected increase in the location and area devoted to agricultural production, according to the land-cover map produced by the Integrated Model to Assess the Global Environment and potential productivity obtained from the Global Agro-Ecological Zones (Supplementary Text) (13). (C) Estimated range contraction in primate distributions by the end of the 21st century under a worst-case scenario of agricultural expansion. See Supplementary Text for methods.

Logging, mining, and fossil fuel extraction Globalized financial markets and a worldwide commodity boom have led to an ever-growing demand for tropical timber and a concomitant expansion of industrial logging, resulting in deforestation and creating a potent economic impetus for road building in forested areas (Supplementary Text) (14). Countries in primate range regions are responding to global market demands by expanding logging activities to increase economic growth. In 2010, the Neotropics accounted for 48% of the production of industrial hardwood, followed by Southeast Asia (23%), sub-Saharan Africa (16%), and South Asia (13%) (fig. S5E). In Madagascar, the large-scale harvesting of rosewood (Dalbergia) since 2009 has negatively affected several protected areas (15). The immediate and long-term effects of legal and illegal logging are a reduction of canopy cover, the destruction of forest undergrowth, and the decline of large tree species important to primates as sources of food and shelter (16). Mining for minerals and diamonds is also a growing threat to tropical ecosystems and their primates. Although it involves relatively small areas, mining contributes to deforestation, forest degradation, and the pollution and poisoning of streams and soil (17). In central Africa, the population densities of apes in mined forests [75.7 (45.35 to 126.33) nests/km2] are markedly lower than in forested sites where mining is absent [234 (185 to 299) nests/km2] (18). In Madagascar, illicit gold and sapphire mining by itinerant miners has affected many forests, including protected ones (19). Mining of gold, nickel, and copper on Dinagat island, in the Philippines, is endangering the survival of the Philippine tarsier (Carlito syrichta) (20). Bushmeat hunting associated with the mining of coltan, tin, gold, and diamonds in the DRC is the main threat to Grauer’s gorilla (G. beringei graueri) (21); recent surveys indicate a 77% decline in its numbers, from 17,000 in 1995 to just 3800 in 2014/2015 (22). In Perú, the mining of zinc and copper threatens the endemic and Critically Endangered yellow-tailed woolly monkey (Lagothrix flavicauda) (23). Development associated with fossil fuel extractions also jeopardizes primate survival. By 2035, global demand for oil and natural gas is projected to increase by >30 and 53% respectively, and primate-rich areas, such as the western Amazon and the western Pacific Ocean (Malaysia, Borneo) will be adversely affected. It is estimated that oil and gas concessions in the western Amazon, and in remote forested areas of Colombia, Ecuador, Brazil, Perú, and Bolivia, already cover about 733,414 km2 (twice the size of Germany) (24).

Other anthropogenic stressors The expansion of industrialized agriculture, logging, mining, oil/gas extraction, and the building of dams and power-line corridors in tropical forest areas is expected to increase human transportation road networks by some 25 million km by 2050 (Supplementary Text) (25). Consequences of the unrestricted road and rail building include increased forest losses from human population migration, illegal colonization, and logging; increased bushmeat hunting; and the illegal wildlife trade (Supplementary Text) (26). The construction of conventional dams and megadams for generating electricity to attract energy-intensive industry and stimulate local productivity in the world’s most biodiverse river basins—the Amazon, Congo, and Mekong—also poses a severe threat to local primate persistence (27). For example, the development of 12 megadams in the state of Sarawak, Malaysia, is expected to result in the loss of at least 2425 km2 of forest cover, affecting populations of the Endangered Müller’s gibbon (Hylobates muelleri) (28). Currently, primates feeding on crops (commonly termed “crop raiding”) is not considered a major cause of global primate population declines by the IUCN because much of the conflict is local in its occurrence, impact, and the types of crops and primate species affected (9, 29–33). There are areas of the world, such as parts of North Africa and Asia, where humans tolerate primates as crop pests because of religious beliefs, cultural traditions, and economic benefit (29). For example, in the Lindu highlands and Buton island of Sulawesi, humans are tolerant of crop feeding macaques due to the role the macaques hold in the local folklore and because they can help in the harvesting of certain crops, such as cashews, where the monkeys eat only the fruit and let the nut fall to the ground to be collected by farmers (29). In other cases, crop feeding by primates (for example, howler monkeys) is tolerated without any economic reward (30). Where human and nonhuman primates come into more severe conflict due to crop raiding [for example, chimpanzees (Pan troglodytes), gorillas (Gorilla spp.), and baboons (Papio spp.) in Africa and orangutans (Pongo spp.) in Southeast Asia] (9, 31–33), culturally and economically appropriate management interventions can mitigate the impact (9, 33). Human-primate conflict due to primates feeding on crops remains a persistent problem and is likely to increase because primate-suitable habitat is converted into agricultural fields or gardens in response to local and global market demands (Fig. 4). Civil unrest also affects primate populations because of saturation bombing, the use of defoliating chemicals (34, 35), and the increase in bushmeat hunting. Poaching of bonobos (Pan paniscus) and gorillas, for example, markedly increased in the DRC and Rwanda as a result of ongoing civil wars (34). In Cambodia, armed conflicts have severely affected populations of the black-shanked douc (Pygathrix nigripes) (35). Land mines, the legacy of wars in the 1960s and 1970s, continue to endanger apes in Southeast Asia and Africa (34, 36).

Forest fragmentation and degradation and the limited resilience of primates Long-term deforestation has resulted in the fragmentation of 58% of subtropical and 46% of tropical forests (37, 38), forcing primates to live in isolated forest patches, including protected areas. This has led to decreasing numbers, population restructuring, and the loss of genetic diversity, as shown for pied tamarins (Saguinus bicolor), northern muriquis (Brachyteles hypoxanthus), Udzungwa red colobus monkeys (Piliocolobus gordonorum), several species of Chinese colobines (Rhinopithecus and Trachypithecus), Cross River gorillas (G. gorilla diehli), and Bornean orangutans (39–45). Edge effects predominate in many areas of disturbed forests, exacerbating habitat degradation (37). Agricultural expansion as well as legal and illegal logging cause further desiccation of vegetation, and human-induced forest fires devastate large areas in primate range regions yearly, resulting in increased tree mortality and losses of up to one-third of canopy cover (46, 47). Although the effects of habitat loss, fragmentation, and degradation upon primates are mediated by variations in species-specific traits (rarity, trophic levels, dispersal mode, reproductive biology, life history, diet, and ranging behavior), the common response across taxa is population decline (Fig. 1). Some primates are more behaviorally and ecologically resilient than others when faced with habitat loss, fragmentation, and degradation. Bornean orangutans, for example, can survive, at least temporarily, in logged forests, Acacia plantations, and oil palm plantations (48). Baboons (Papio), Hanuman langurs (Semnopithecus), and macaques (Macaca) are particularly adaptable and can survive even in urban areas (49). Chimpanzees appear to evaluate risks when crop-foraging and adjust their foraging patterns in deciding whether to exploit fragmented forests near humans (50). Bonobos tend to avoid areas of high human activity, fragmented forests, or both, and although this may suggest flexibility, the presence of humans appears to significantly reduce their access to potentially available habitat (51). Still, persistence in isolated forest fragments, logged forests, agroecosystems, and urban areas is unlikely to be a sustainable option for most species due to hunting, further habitat reduction and fragmentation, reduced carrying capacity, parasite and disease transmission from humans and domestic animals, dog predation, human-primate conflict due to crop raiding, isolation, and continued changes in land use (52). Primates in degraded forests face nutritional shortfalls and lower gut microbial diversity (53–55). They also show an increased prevalence of parasites and pathogens. For example, the increased exposure of lemurs (Avahi laniger, Eulemur rubriventer, Hapalemur aureus, Microcebus rufus, Propithecus edwardsi, and Prolemur simus) and chimpanzees (P. troglodytes) to human populations has increased their risk of infection by diarrhea-causing enteric pathogens (56, 57). The close phylogenetic relationship between humans and other primates also creates an exceptionally high potential for pathogen exchange (58), as evidenced by disease emergence in humans as an unintentional effect of the hunting and butchering of wild primates (for example, human outbreaks of Ebola and the global HIV/AIDS pandemic) (59). In addition, exponential human population growth (fig. S7, A and B) and associated human-induced forest loss increase opportunities for wild primates to become exposed to human and domesticated animal pathogens (60). Primates escaping or released from the pet trade or sanctuaries can carry pathogens with a potential of transmission to resident populations (61). Moreover, ecotourism and research, despite contributing in positive ways to primate conservation, have the unintended consequence of exposing wild primates to human pathogens (62, 63).

Hunting Human population growth and increasing per capita wealth have led to an increase in commercialized bushmeat hunting relative to subsistence hunting in many parts of the world. This has become a major driving force for primate population decline, especially in Africa and Southeast Asia (45, 64). Although bushmeat hunting is difficult to track, reports indicate that about 150,000 primate carcasses from 16 species were traded annually as bushmeat in urban and rural markets at 89 sites in Nigeria and Cameroon (Supplementary Text) (64). In Borneo, between 1950 and 3100 orangutans are estimated to be killed annually (including 375 to 1550 females), a level that far exceeds the maximum sustainable offtake for population viability (45). Because only a relatively small number of primates live inside protected areas [for example, 21 to 27.5% of all great apes (51, 65)], populations outside protected areas are declining rapidly; the consequent increase in rarity raises the price of primate meat, making it more worthwhile for poachers to risk encroaching into protected areas to hunt (66).

Legal and illegal trade Many primate species are increasingly threatened by legal and illegal unsustainable trade. Primates are traded for consumption, biomedical research, and zoo and wildlife collections; as pets; for the sale of body parts (bodies, skins, hair, and skulls) used in traditional medicine; as talismans and trophies; and for magical purposes (67, 68). The Convention on International Trade in Endangered Species (CITES) database for 2005–2014 reported a global primate trade of some 450,000 live individuals plus an additional 11,000 individuals in the form of body parts. Asian species accounted for 93% of this trade (12 genera), Neotropical species for 4% (13 genera), and African species for 3% (33 genera) (table S6 and fig. S8, A to C). However, these figures are conservative because CITES only reports statistics formally provided by each country. For example, although CITES reported fewer than 400 night monkeys (Aotus) traded internationally between 2005 and 2014 (table S6), in the tri-border area between Perú, Brazil, and Colombia, it was estimated that ~4000 night monkeys (Aotus nancymaae, Aotus vociferans, and Aotus nigriceps) were traded to a single biomedical research facility between 2007 and 2008 alone, for a price of approximately $100,000 (69). The expansion of road networks in frontier forests facilitates the extraction and trade of primates to cities and beyond borders (25). Together with increasing opportunities from e-commerce, this has given suppliers and smugglers unprecedented access to new markets (70, 71). Wildlife laundering (mixing protected species with legal shipments of similar species) also occurs when wild-collected primates are passed off as captive bred (Supplementary Text) (72).

Climate change Although empirical evidence for the impact of climate change on primates is scarce, a recent global assessment suggests that numerous primates will experience changing climatic conditions during the 21st century, with the Amazon, the Atlantic Forest of Brazil, Central America, and East and Southeast Asia being considered hotspots of climate change–induced primate vulnerability (73). Primate taxa with limited geographic distributions and species characterized by slow life history traits (for example, late age at first reproduction and long interbirth intervals) are highly vulnerable to shifting ecological conditions and are likely to be most affected (74, 75). Although some species may cope with these changes either by migrating to more suitable conditions or by adapting in situ, dispersal or range shift is not always possible and may have highly negative consequences (Supplementary Text) (76). Forest fragmentation induced by climate change can affect the availability of dispersal routes (77). Climate change may also force individuals out of protected areas, making them more vulnerable to hunting and other anthropogenic impacts (78), and range shifts among interacting species can affect food supplies and introduce new predators, pathogens, and/or competitors (79). Interactions between climate change and other extinction drivers also need to be considered. For instance, projections of land-cover change show that the Bornean orangutan might lose 15 to 30% of its habitat by 2080, mainly due to deforestation and oil palm agriculture, but when coupled with climate change, even more habitat is likely to become unsuitable (80). Additionally, more frequent and severe climate change can induce floods, droughts, fires, hurricanes, and El Niño–Southern Oscillation events (81) that can affect the food supply available to primate populations, with negative impacts on health, fertility, and mortality (82).