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Cited by 1,466Primate Behavior and EcologyWildlife Ecology and ConservationConservation, Ecology, Wildlife Education

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Impending extinction crisis of the world’s primates: Why primates matter

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Estrada, Alejandro, Garber, Paul A., Rylands, Anthony B., Roos, Christian, Fernandez-Duque, Eduardo, Di Fiore, Anthony, Nekaris, K. Anne-Isola, Nijman, Vincent, Heymann, Eckhard W., Lambert, Joanna E., Rovero, Francesco, Barelli, Claudia, Setchell, Joanna M., Gillespie, Thomas R., Mittermeier, Russell A., Arregoitia, Luis Verde, de Guinea, Miguel, Gouveia, Sidney, Dobrovolski, Ricardo, Shanee, Sam, Shanee, Noga, Boyle, Sarah A., Fuentes, Agustin, MacKinnon, Katherine C., Amato, Katherine R., Meyer, Andreas L. S., Wich, Serge, Sussman, Robert W., Pan, Ruliang, Kone, Inza, Li, Baoguo·2017·Science Advances
DOI 10.1126/sciadv.1600946PMC PMC5242557
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Abstract

Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend.

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Figures

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 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.
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 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.CC BY-NC · PubMed Central
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. 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).
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. 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).CC BY-NC · PubMed Central
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. 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).CC BY-NC · PubMed Central
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.
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.CC BY-NC · PubMed Central
Fig. 5 Phylogenetic signal as a predictor of extinction risk in the world’s primates. Distribution of threat values (IUCN Red List categories) for 340 primate species. Representative genera labeled. After taxonomic updates, our working phylogeny included 350 of the 367 species considered in the molecular supertree (73), of which 340 are not Data Deficient. Closely related species are more likely to have the same threat status than species taken randomly from the phylogeny [D = 0.31; P (D < 1) < 0.001], supporting a strong phylogenetic signal (see Supplementary Text for details of methodology). Data for Africa include Madagascar. IUCN Red List Categories: CR (Critically Endangered), EN (Endangered), VU (Vulnerable), NT (Near Threatened), and LC (Least Concern).
Fig. 5 Phylogenetic signal as a predictor of extinction risk in the world’s primates. Distribution of threat values (IUCN Red List categories) for 340 primate species. Representative genera labeled. After taxonomic updates, our working phylogeny included 350 of the 367 species considered in the molecular supertree (73), of which 340 are not Data Deficient. Closely related species are more likely to have the same threat status than species taken randomly from the phylogeny [D = 0.31; P (D < 1) < 0.001], supporting a strong phylogenetic signal (see Supplementary Text for details of methodology). Data for Africa include Madagascar. IUCN Red List Categories: CR (Critically Endangered), EN (Endangered), VU (Vulnerable), NT (Near Threatened), and LC (Least Concern).CC BY-NC · PubMed Central
Fig. 6 Factors driving primate population declines and possible mitigating approaches. Four broad social and economic processes drive the proximate causes of threat to primates and human actions that directly affect primate habitats and populations. Mitigating approaches aim at lowering the impact of proximate causes of primate declines. Infrastructure development also includes road and rail expansion.
Fig. 6 Factors driving primate population declines and possible mitigating approaches. Four broad social and economic processes drive the proximate causes of threat to primates and human actions that directly affect primate habitats and populations. Mitigating approaches aim at lowering the impact of proximate causes of primate declines. Infrastructure development also includes road and rail expansion.CC BY-NC · PubMed Central
Fig. 7 Photos of selected primates from each major world region. Conservation status and photo credits include the following: (A) Golden snub-nosed monkey (Rhinopithecus roxellana), Endangered, P. A. Garber. (B) Ring-tailed lemur (Lemur catta), Endangered, R. A. Mittermeier. (C) Udzungwa red colobus (P. gordonorum), Endangered (Photo Credit: Thomas Struhsaker, Duke University). (D) Javan slow loris (Nycticebus javanicus), Critically Endangered (Photo Credit: Andrew Walmsley, Andrew Walmsley Photography). (E) Sumatran orangutan (P. abelii), Critically Endangered (Photo Credit: Perry van Duijnhoven). (F) Azara’s night monkey (Aotus azarae), Least Concern [Photo Credit: Claudia Valeggia (Yale University)/Owl Monkey Project, Formosa-Argentina].
Fig. 7 Photos of selected primates from each major world region. Conservation status and photo credits include the following: (A) Golden snub-nosed monkey (Rhinopithecus roxellana), Endangered, P. A. Garber. (B) Ring-tailed lemur (Lemur catta), Endangered, R. A. Mittermeier. (C) Udzungwa red colobus (P. gordonorum), Endangered (Photo Credit: Thomas Struhsaker, Duke University). (D) Javan slow loris (Nycticebus javanicus), Critically Endangered (Photo Credit: Andrew Walmsley, Andrew Walmsley Photography). (E) Sumatran orangutan (P. abelii), Critically Endangered (Photo Credit: Perry van Duijnhoven). (F) Azara’s night monkey (Aotus azarae), Least Concern [Photo Credit: Claudia Valeggia (Yale University)/Owl Monkey Project, Formosa-Argentina].CC BY-NC · PubMed Central

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Citations

Cites

Research works printed but not linked: 14

  1. C. Campbell A. Fuentes K. MacKinnon S. Bearder R. Stumpf Eds. Primates in Perspective (Oxford Univ. Press ed. 2 2010).
  2. A. Lanjouw H. Rainer A. White Apes overview in State of the Apes: Industrial Agriculture and Ape Conservation H. Rainer A. White A. Lanjouw Eds. (Arcus/Cambridge Univ. Press 2015) pp. 164–192.
  3. A. Lanjouw in State of the Apes: Extractive Industries and Ape Conservation H Rainer A. White A. Lanjouw Eds. (Arcus/Cambridge Univ. Press 2014) pp. 127–161.
  4. B. Mercer Tropical Forests: A Review (The Prince’s Charities’ International Sustainability Unit 2015).
  5. E. Efiom thesis Consequences of bushmeat hunting in tropical forests Lund University (2013).
  6. Millennium Ecosystem Assessment Ecosystems and Human Well-Being: Synthesis (Island Press 2005).
  7. W. Liu, C. Huang, C. Roos, Q. Zhou, Y. Li, F. Wei, Identification of the species, origin and sex of smuggled douc langur (Pygathrix sp.) remains. Vietnamese J. Primatol. 1–2, 63–69 (2008).
  8. M. L. Gore, J. Ratsimbazafy, A. Rajaonson, A. Lewis, J. S. Kahler, Public perceptions of poaching risks in a biodiversity hotspot: Implications for wildlife trafficking interventions. J. Trafficking Organ. Crime Secur. 2, 1–20 (2016).
  9. C. P. Groves Primate Taxonomy (Smithsonian Institution Press 2001).
  10. C. P. Groves Order Primates in Mammal Species of the World: A Taxonomic and Geographic Reference D. E. Wilson D. M. Reeder Eds. (Johns Hopkins Univ. Press ed. 3 2005) pp. 111–184.
  11. A. Casson Oil Palm Soybeans and Critical Habitat Loss: A Review (WWF Forest Conversion Initiative 2003).
  12. J. M. Linder, African primate diversity threatened by “new wave” of industrial oil palm expansion. Afr. Primates 8, 25–38 (2013).
  13. I. Koné, K. Ouattara, A. D. Koffi, A top priority site for primate conservation in Côte d’Ivoire soon designated as a protected area? Afr. Primates 10, 59–60 (2015).
  14. K. Kakaes F. Greenword M. Lippincott S. Dosemagen P. Meier S. A. Wich Drones and Aerial Observation: New Technologies for Property Rights Human Rights and Global Development: A Primer (New America 2015); http://drones.newamerica.org/primer/DronesAndAerialObservation.pdf

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Authors
Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., Di Fiore, A., Nekaris, K. A.-I., Nijman, V., Heymann, E. W., Lambert, J. E., Rovero, F., Barelli, C., Setchell, J. M., Gillespie, T. R., Mittermeier, R. A., Arregoitia, L. V., de Guinea, M., Gouveia, S., Dobrovolski, R., Shanee, S., Shanee, N., Boyle, S. A., Fuentes, A., MacKinnon, K. C., Amato, K. R., Meyer, A. L. S., Wich, S., Sussman, R. W., Pan, R., Kone, I., & Li, B.
Affiliations
  • Universidad Nacional Autónoma de México (MX)
  • University of Illinois Urbana-Champaign (US)
  • Conservation International (US)
  • German Primate Center (DE)
  • Department of Anthropology, Yale University, New Haven, CT 06511, USA.
  • Department of Anthropology, University of Texas, Austin, TX 78705, USA.
  • Oxford Brookes University (GB)
  • University of Colorado Boulder (US)
  • Museo delle Scienze (IT)
  • Durham University (GB)
  • Emory University (US)
  • Naturhistorisches Museum Bern, Bernastrasse 15, CH-3005 Bern, Switzerland.
  • Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, U.K.
  • Universidade Federal de Sergipe (BR)
  • Universidade Federal da Bahia (BR)
  • Neotropical Primate Conservation, 23 Portland Road, Manchester M32 0PH, U.K.
  • Rhodes College (US)
  • Department of Anthropology, University of Notre Dame, Notre Dame, IN 46556, USA.
  • Saint Louis University (US)
  • Northwestern University (US)
  • Universidade Federal do Paraná (BR)
  • Liverpool John Moores University (GB)
  • Washington University in St. Louis (US)
  • The University of Western Australia (AU)
  • Centre Suisse des Recherches Scientifiques, Université de Cocody, Abidjan, Côte d’Ivoire.
  • Chinese Academy of Sciences (CN)
Corresponding author
  • Estrada, Alejandro
  • Garber, Paul A.
ORCID
Venue
Science Advances
Publisher
American Association for the Advancement of Science (AAAS)
Published
2017-01-06
Volume
3
Issue
1
Pages
e1600946-e1600946
ISSN
2375-2548 (ISSN-L)
DOI
10.1126/sciadv.1600946
PMC
PMC5242557
OpenAlex
W2581828022
Cited by
1,466
References
190
Citations by year
2026: 103 · 2025: 130 · 2024: 150 · 2023: 224 · 2022: 195 · 2021: 157 · 2020: 204 · 2019: 142 · 2018: 109 · 2017: 50
FWCI
21.39
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • Science Advances (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Liverpool John Moores University (acceptedVersion)
  • Durham Research Online (Durham University) (acceptedVersion, other-oa)
  • UvA-DARE (University of Amsterdam) (submittedVersion, cc-by-nc)
  • Durham Research Online (Durham University) (submittedVersion, cc-by)
  • UWA Profiles and Research Repository (UWA) (submittedVersion, cc-by-nc)
  • Florence Research (University of Florence) (submittedVersion)
  • Radar (Oxford Brookes University) (submittedVersion, cc-by-nc)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders
  • CNPq (ID0EGCFM13839, 476528/2013-5)
  • CAPES, FAPESB, CNPq (ID0EHIFM13840, 461665/2014-0)
  • PRODOC/UFBA (ID0E2MFM13841, 5849/2013)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
  • Physical Sciences › Environmental Science › Ecology › Wildlife Ecology and Conservation
  • Physical Sciences › Environmental Science › Management, Monitoring, Policy and Law › Conservation, Ecology, Wildlife Education
Keywords
primate extinction, primate conservation, habitat loss, bushmeat hunting, illegal wildlife trade, climate change, emerging infectious diseases, human evolution, tropical biodiversity, forest regeneration, anthropogenic pressure, Neotropical region, Madagascar, Africa, Asia
MeSH terms
Animals, Cercopithecidae, Ecosystem, Extinction, Biological

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