PRIMATOLOGY
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Impending extinction crisis of the world’s primates:
Why primates matter
Alejandro Estrada,
1
* Paul A. Garber,
2
* Anthony B. Rylands,
3
Christian Roos,
4
Eduardo Fernandez-Duque,
5
Anthony Di Fiore,
6
K. Anne-Isola Nekaris,
7
Vincent Nijman,
7
Eckhard W. Heymann,
8
Joanna E. Lambert,
9
Francesco Rovero,
10
Claudia Barelli,
10
Joanna M. Setchell,
11
Thomas R. Gillespie,
12
Russell A. Mittermeier,
3
Luis Verde Arregoitia,
13
Miguel de Guinea,
7
Sidney Gouveia,
14
Ricardo Dobrovolski,
15
Sam Shanee,
16,17
Noga Shanee,
16,17
Sarah A. Boyle,
18
Agustin Fuentes,
19
Katherine C. MacKinnon,
20
Katherine R. Amato,
21
Andreas L. S. Meyer,
22
Serge Wich,
23,24
Robert W. Sussman,
25
Ruliang Pan,
26
Inza Kone,
27
Baoguo Li
28
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 de-
clining 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 agri-
culture, 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 re-
gions 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’sprimatesandthe
costs of their loss to ecosystem health and human society is imperative.
INTRODUCTION
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 im-
portant 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 stan-
dard for species conservatio n status [the International Union for Con-
servation 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,weproposeaconceptual
1
Institute of Biology, National Autonomous University of Mexico, CP 04510, Mexico City, Mexico.
2
Department of Anthropology, Program in Ecology, Evolution, and
Conservation Biology, University of Illinois, Urbana, IL 61801, USA.
3
Conservation International, 2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA.
4
Gene Bank of
Primates and Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Göttingen, Germany.
5
Department of
Anthropology, Yale University, New Haven, CT 06511, USA.
6
Department of Anthropology, University of Texas, Austin, TX 78705, USA.
7
Department of Social Sciences,
Oxford Brookes University, Oxford OX3 0BP, U.K.
8
Abteilung Verhaltensökologie und Soziobiologie, Deutsches Primatenzentrum, Leibniz-Institut für Primatenforschung,
Kellnerweg 4, D-37077 Göttingen, Germany.
9
Department of Anthropology, University of Colorado at Boulder, 1350 Pleasant Street UCB 233, Boulder, CO 80309, USA.
10
Tropical Biodiversity Section, MUSE—Museo delle Scienze, Corso del Lavoro e della Scienza 3, 38122 Trento, Italy.
11
Department of Anthropology, and Behaviour,
Ecology and Evolution Research Centre, Durham University, South Road, Durham DH1 3LE, U.K.
12
Departments of Environmental Sciences and Environmental Health, Rollins
School of Public Health, Emory University, 400 Dowman Drive, Math and Science Center, Suite E510, Atlanta, GA 30322, USA.
13
Naturhistorisches Museum Bern, Bernastrasse
15, CH-3005 Bern, Switzerland.
14
Department of Ecology, Federal University of Sergipe, São Cristóvão, SE 49100-000, Brazil.
15
Department of Zoology, Federal University of
Bahia, Salvador, BA 40170-290, Brazil.
16
Neotropical Primate Conservation, 23 Portland Road, Manchester M32 0PH, U.K.
17
Asociación Neotropical Primate Conservation
Perú, 1187 Avenida Belaunde, La Esperanza, Yambrasbamba, Bongará, Amazonas, Peru.
18
Department of Biology, Rhodes College, 2000 North Parkway, Memphis, TN
38112, USA.
19
Department of Anthropology, University of Notre Dame, Notre Dame, IN 46556, USA.
20
Department of Sociology and Anthropology, Saint Louis University,
St. Louis, MO 63108, USA.
21
Department of Anthropology, Northwestern University, 1810 Hinman Avenue, Evanston, IL 60208, USA.
22
Programa de Pós-Graduação em
Zoologia, Departamento de Zoologia, Universidade Federal do Paraná, C.P. 19020, Curitiba, PR 81531-990, Brazil.
23
School of Natural Sciences and Psychology, Liverpool John
Moores University, James Parsons Building, Byrom Street, Liverpool L3 3AF, U.K.
24
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam,
Netherlands.
25
Department of Anthropology, Washington University, St. Louis, MO 63130, USA.
26
School of Anatomy, Physiology and Human Biology, University of Western
Australia (M309), 35 Stirling Highway, Crawley, Western Australia 6009, Australia.
27
Centre Suisse des Recherches Scientifiques, Université de Cocody, Abidjan, Côte d’Ivoire.
28
Xi’an Branch of Chinese Academy of Sciences, College of Life Sciences, Northwest University, No. 229, Taibai North Road, Xi’an 710069, China.
*Corresponding author. Email: aestradaprimates@gmail.com (A.E.); p-garber@illinois.edu (P.A.G.)
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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 anthro-
pogenic 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.
IMPENDING DEFAUNATION OF THE WORLD’S PRIMATES
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 c ountries—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
th ey al so oc cu r in trop i ca l 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’smouselemur(Microcebus
berthae) to about 200 kg in male western and eastern gorillas (Gorilla
gorilla and Gorilla beringei, respectively) (Supplementary Text) (2, 4, 5).
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 dec reasin g glob ally
(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.
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
Fig. 1. Global primate species richness, distributions, and the percentage of species threatened and with declining populations. 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 populationsineachregionfromtablesS1
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.
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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 proce ss o f rapid and widespread industry -driven de-
forestation in the Neotropics, mainland A frica, 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 km
2
(an area three times that of France) and
forest cover loss at 2 million km
2
(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 be-
cause large segments of existing populations occur outside protected
area s (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 gibbo n (Nomascus leucogenys) and the Hainan gibbon
(Nomascus hainanus)(11). Similarly, deforestation due to the establish-
ment 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’slangur(Trachypithecus phayrei)
(11, 12). Modeling the overlap between primate species’ distributions
and forecasted future agricultural production for the 21st century in-
dicates that regions predicted to undergo the greatest agricultural expan -
sion 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 expan-
sion 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).
Logging, mining, and fossil fuel extraction
Globalized financial markets and a worldwide commodity boom have
led to an ever-growing demand for tropical timber andaconcomitant
expansion of industrial logging, resulting in deforestation and creating a
potent economic impetus for road building in forested areas (Supple-
mentary 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/km
2
]
are markedly lower than in forested sites where mining is absent [234
(185 to 299) nests/km
2
](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
miningofcoltan,tin,gold,anddiamonds in the DRC is the main threat
Fig. 2. Percent of species threatened with extinction in each primate family. 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. Dataforeachspeciesare
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),DataDeficient(DD),andNotEvaluated(NE)(seetablesS1toS3).Uponrevision 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).
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to Grauer’sgorilla(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 fossilfuelextractionsalsojeopardizes
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 km
2
(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-li ne 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 km
2
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 popula-
tion 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 ex-
ample, 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 tol-
erated without any economic reward (30). Where human and non-
human 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 tamari ns (Saguinus bicolor), northern
muriquis (Brachyteles hypoxanthus
), Udzungwa red colobus monkeys
(Pili
oco
lobus gordonorum), several species of Chinese colobines
(Rhinopithecus and Trachypithecus),CrossRivergorillas(G. gorilla diehli),
and Bornean orangutans (39–45). Edge effects predominate in many
areas of disturbed forests, exacerbating habitat degradation (37). Agricul-
tural expansion as well as legal and illegal logging cause further desicca-
tion 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
(Ma caca) are particularly adaptable and can survive even in urban areas
(49 ). Chimpanzees appear to evaluate risks when crop-foraging and ad-
just their foraging patterns in deciding whether to exploit fragmented
forestsnearhumans(50). Bonobos tend to avoid areas of high human
activity, fragmented forests, or both, and although this may suggest flex-
ibility, the presence of humans appears to significantly reduce their
access to potentially available habitat (51). Still, persistence in isolated
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).
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Fig. 4. Globalpatterns of forecasted agricultural expansion for the 21st century in primate range regions and estimatedrange 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.
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