Le SIDA en Afrique subsaharienne (serveur d'exploration)

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

Identifieur interne : 002F17 ( Pmc/Corpus ); précédent : 002F16; suivant : 002F18

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

Auteurs : Alejandro Estrada ; Paul A. Garber ; Anthony B. Rylands ; Christian Roos ; Eduardo Fernandez-Duque ; Anthony Di Fiore ; K. Anne-Isola Nekaris ; Vincent Nijman ; Eckhard W. Heymann ; Joanna E. Lambert ; Francesco Rovero ; Claudia Barelli ; Joanna M. Setchell ; Thomas R. Gillespie ; Russell A. Mittermeier ; Luis Verde Arregoitia ; Miguel De Guinea ; Sidney Gouveia ; Ricardo Dobrovolski ; Sam Shanee ; Noga Shanee ; Sarah A. Boyle ; Agustin Fuentes ; Katherine C. Mackinnon ; Katherine R. Amato ; Andreas L. S. Meyer ; Serge Wich ; Robert W. Sussman ; Ruliang Pan ; Inza Kone ; Baoguo Li

Source :

RBID : PMC:5242557

Abstract

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


Url:
DOI: 10.1126/sciadv.1600946
PubMed: 28116351
PubMed Central: 5242557

Links to Exploration step

PMC:5242557

Le document en format XML

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<nlm:aff id="aff15">Department of Zoology, Federal University of Bahia, Salvador, BA 40170-290, Brazil.</nlm:aff>
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<name sortKey="Boyle, Sarah A" sort="Boyle, Sarah A" uniqKey="Boyle S" first="Sarah A." last="Boyle">Sarah A. Boyle</name>
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<nlm:aff id="aff18">Department of Biology, Rhodes College, 2000 North Parkway, Memphis, TN 38112, USA.</nlm:aff>
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<name sortKey="Fuentes, Agustin" sort="Fuentes, Agustin" uniqKey="Fuentes A" first="Agustin" last="Fuentes">Agustin Fuentes</name>
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<name sortKey="Mackinnon, Katherine C" sort="Mackinnon, Katherine C" uniqKey="Mackinnon K" first="Katherine C." last="Mackinnon">Katherine C. Mackinnon</name>
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<nlm:aff id="aff20">Department of Sociology and Anthropology, Saint Louis University, St. Louis, MO 63108, USA.</nlm:aff>
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<name sortKey="Amato, Katherine R" sort="Amato, Katherine R" uniqKey="Amato K" first="Katherine R." last="Amato">Katherine R. Amato</name>
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<nlm:aff id="aff21">Department of Anthropology, Northwestern University, 1810 Hinman Avenue, Evanston, IL 60208, USA.</nlm:aff>
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<name sortKey="Meyer, Andreas L S" sort="Meyer, Andreas L S" uniqKey="Meyer A" first="Andreas L. S." last="Meyer">Andreas L. S. Meyer</name>
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<nlm:aff id="aff22">Programa de Pós-Graduação em Zoologia, Departamento de Zoologia, Universidade Federal do Paraná, C.P. 19020, Curitiba, PR 81531-990, Brazil.</nlm:aff>
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<name sortKey="Wich, Serge" sort="Wich, Serge" uniqKey="Wich S" first="Serge" last="Wich">Serge Wich</name>
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<nlm:aff id="aff23">School of Natural Sciences and Psychology, Liverpool John Moores University, James Parsons Building, Byrom Street, Liverpool L3 3AF, U.K.</nlm:aff>
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<nlm:aff id="aff24">Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands.</nlm:aff>
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<name sortKey="Sussman, Robert W" sort="Sussman, Robert W" uniqKey="Sussman R" first="Robert W." last="Sussman">Robert W. Sussman</name>
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<nlm:aff id="aff25">Department of Anthropology, Washington University, St. Louis, MO 63130, USA.</nlm:aff>
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<name sortKey="Pan, Ruliang" sort="Pan, Ruliang" uniqKey="Pan R" first="Ruliang" last="Pan">Ruliang Pan</name>
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<name sortKey="Kone, Inza" sort="Kone, Inza" uniqKey="Kone I" first="Inza" last="Kone">Inza Kone</name>
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<nlm:aff id="aff27">Centre Suisse des Recherches Scientifiques, Université de Cocody, Abidjan, Côte d’Ivoire.</nlm:aff>
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<name sortKey="Li, Baoguo" sort="Li, Baoguo" uniqKey="Li B" first="Baoguo" last="Li">Baoguo Li</name>
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<nlm:aff id="aff28">Xi’an Branch of Chinese Academy of Sciences, College of Life Sciences, Northwest University, No. 229, Taibai North Road, Xi’an 710069, China.</nlm:aff>
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<title xml:lang="en" level="a" type="main">Impending extinction crisis of the world’s primates: Why primates matter</title>
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<name sortKey="Estrada, Alejandro" sort="Estrada, Alejandro" uniqKey="Estrada A" first="Alejandro" last="Estrada">Alejandro Estrada</name>
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<nlm:aff id="aff1">Institute of Biology, National Autonomous University of Mexico, CP 04510, Mexico City, Mexico.</nlm:aff>
</affiliation>
</author>
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<name sortKey="Garber, Paul A" sort="Garber, Paul A" uniqKey="Garber P" first="Paul A." last="Garber">Paul A. Garber</name>
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<nlm:aff id="aff2">Department of Anthropology, Program in Ecology, Evolution, and Conservation Biology, University of Illinois, Urbana, IL 61801, USA.</nlm:aff>
</affiliation>
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<name sortKey="Rylands, Anthony B" sort="Rylands, Anthony B" uniqKey="Rylands A" first="Anthony B." last="Rylands">Anthony B. Rylands</name>
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<nlm:aff id="aff3">Conservation International, 2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA.</nlm:aff>
</affiliation>
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<name sortKey="Roos, Christian" sort="Roos, Christian" uniqKey="Roos C" first="Christian" last="Roos">Christian Roos</name>
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<nlm:aff id="aff4">Gene Bank of Primates and Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Göttingen, Germany.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Fernandez Duque, Eduardo" sort="Fernandez Duque, Eduardo" uniqKey="Fernandez Duque E" first="Eduardo" last="Fernandez-Duque">Eduardo Fernandez-Duque</name>
<affiliation>
<nlm:aff id="aff5">Department of Anthropology, Yale University, New Haven, CT 06511, USA.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Di Fiore, Anthony" sort="Di Fiore, Anthony" uniqKey="Di Fiore A" first="Anthony" last="Di Fiore">Anthony Di Fiore</name>
<affiliation>
<nlm:aff id="aff6">Department of Anthropology, University of Texas, Austin, TX 78705, USA.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Nekaris, K Anne Isola" sort="Nekaris, K Anne Isola" uniqKey="Nekaris K" first="K. Anne-Isola" last="Nekaris">K. Anne-Isola Nekaris</name>
<affiliation>
<nlm:aff id="aff7">Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, U.K.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Nijman, Vincent" sort="Nijman, Vincent" uniqKey="Nijman V" first="Vincent" last="Nijman">Vincent Nijman</name>
<affiliation>
<nlm:aff id="aff7">Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, U.K.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Heymann, Eckhard W" sort="Heymann, Eckhard W" uniqKey="Heymann E" first="Eckhard W." last="Heymann">Eckhard W. Heymann</name>
<affiliation>
<nlm:aff id="aff8">Abteilung Verhaltensökologie und Soziobiologie, Deutsches Primatenzentrum, Leibniz-Institut für Primatenforschung, Kellnerweg 4, D-37077 Göttingen, Germany.</nlm:aff>
</affiliation>
</author>
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<name sortKey="Lambert, Joanna E" sort="Lambert, Joanna E" uniqKey="Lambert J" first="Joanna E." last="Lambert">Joanna E. Lambert</name>
<affiliation>
<nlm:aff id="aff9">Department of Anthropology, University of Colorado at Boulder, 1350 Pleasant Street UCB 233, Boulder, CO 80309, USA.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Rovero, Francesco" sort="Rovero, Francesco" uniqKey="Rovero F" first="Francesco" last="Rovero">Francesco Rovero</name>
<affiliation>
<nlm:aff id="aff10">Tropical Biodiversity Section, MUSE—Museo delle Scienze, Corso del Lavoro e della Scienza 3, 38122 Trento, Italy.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Barelli, Claudia" sort="Barelli, Claudia" uniqKey="Barelli C" first="Claudia" last="Barelli">Claudia Barelli</name>
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<nlm:aff id="aff10">Tropical Biodiversity Section, MUSE—Museo delle Scienze, Corso del Lavoro e della Scienza 3, 38122 Trento, Italy.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Setchell, Joanna M" sort="Setchell, Joanna M" uniqKey="Setchell J" first="Joanna M." last="Setchell">Joanna M. Setchell</name>
<affiliation>
<nlm:aff id="aff11">Department of Anthropology, and Behaviour, Ecology and Evolution Research Centre, Durham University, South Road, Durham DH1 3LE, U.K.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Gillespie, Thomas R" sort="Gillespie, Thomas R" uniqKey="Gillespie T" first="Thomas R." last="Gillespie">Thomas R. Gillespie</name>
<affiliation>
<nlm:aff id="aff12">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.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Mittermeier, Russell A" sort="Mittermeier, Russell A" uniqKey="Mittermeier R" first="Russell A." last="Mittermeier">Russell A. Mittermeier</name>
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<nlm:aff id="aff3">Conservation International, 2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA.</nlm:aff>
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</author>
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<name sortKey="Arregoitia, Luis Verde" sort="Arregoitia, Luis Verde" uniqKey="Arregoitia L" first="Luis Verde" last="Arregoitia">Luis Verde Arregoitia</name>
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<nlm:aff id="aff13">Naturhistorisches Museum Bern, Bernastrasse 15, CH-3005 Bern, Switzerland.</nlm:aff>
</affiliation>
</author>
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<name sortKey="De Guinea, Miguel" sort="De Guinea, Miguel" uniqKey="De Guinea M" first="Miguel" last="De Guinea">Miguel De Guinea</name>
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<nlm:aff id="aff7">Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, U.K.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Gouveia, Sidney" sort="Gouveia, Sidney" uniqKey="Gouveia S" first="Sidney" last="Gouveia">Sidney Gouveia</name>
<affiliation>
<nlm:aff id="aff14">Department of Ecology, Federal University of Sergipe, São Cristóvão, SE 49100-000, Brazil.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Dobrovolski, Ricardo" sort="Dobrovolski, Ricardo" uniqKey="Dobrovolski R" first="Ricardo" last="Dobrovolski">Ricardo Dobrovolski</name>
<affiliation>
<nlm:aff id="aff15">Department of Zoology, Federal University of Bahia, Salvador, BA 40170-290, Brazil.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Shanee, Sam" sort="Shanee, Sam" uniqKey="Shanee S" first="Sam" last="Shanee">Sam Shanee</name>
<affiliation>
<nlm:aff id="aff16">Neotropical Primate Conservation, 23 Portland Road, Manchester M32 0PH, U.K.</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff17">Asociación Neotropical Primate Conservation Perú, 1187 Avenida Belaunde, La Esperanza, Yambrasbamba, Bongará, Amazonas, Peru.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Shanee, Noga" sort="Shanee, Noga" uniqKey="Shanee N" first="Noga" last="Shanee">Noga Shanee</name>
<affiliation>
<nlm:aff id="aff16">Neotropical Primate Conservation, 23 Portland Road, Manchester M32 0PH, U.K.</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff17">Asociación Neotropical Primate Conservation Perú, 1187 Avenida Belaunde, La Esperanza, Yambrasbamba, Bongará, Amazonas, Peru.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Boyle, Sarah A" sort="Boyle, Sarah A" uniqKey="Boyle S" first="Sarah A." last="Boyle">Sarah A. Boyle</name>
<affiliation>
<nlm:aff id="aff18">Department of Biology, Rhodes College, 2000 North Parkway, Memphis, TN 38112, USA.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Fuentes, Agustin" sort="Fuentes, Agustin" uniqKey="Fuentes A" first="Agustin" last="Fuentes">Agustin Fuentes</name>
<affiliation>
<nlm:aff id="aff19">Department of Anthropology, University of Notre Dame, Notre Dame, IN 46556, USA.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Mackinnon, Katherine C" sort="Mackinnon, Katherine C" uniqKey="Mackinnon K" first="Katherine C." last="Mackinnon">Katherine C. Mackinnon</name>
<affiliation>
<nlm:aff id="aff20">Department of Sociology and Anthropology, Saint Louis University, St. Louis, MO 63108, USA.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Amato, Katherine R" sort="Amato, Katherine R" uniqKey="Amato K" first="Katherine R." last="Amato">Katherine R. Amato</name>
<affiliation>
<nlm:aff id="aff21">Department of Anthropology, Northwestern University, 1810 Hinman Avenue, Evanston, IL 60208, USA.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Meyer, Andreas L S" sort="Meyer, Andreas L S" uniqKey="Meyer A" first="Andreas L. S." last="Meyer">Andreas L. S. Meyer</name>
<affiliation>
<nlm:aff id="aff22">Programa de Pós-Graduação em Zoologia, Departamento de Zoologia, Universidade Federal do Paraná, C.P. 19020, Curitiba, PR 81531-990, Brazil.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wich, Serge" sort="Wich, Serge" uniqKey="Wich S" first="Serge" last="Wich">Serge Wich</name>
<affiliation>
<nlm:aff id="aff23">School of Natural Sciences and Psychology, Liverpool John Moores University, James Parsons Building, Byrom Street, Liverpool L3 3AF, U.K.</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff24">Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands.</nlm:aff>
</affiliation>
</author>
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<name sortKey="Sussman, Robert W" sort="Sussman, Robert W" uniqKey="Sussman R" first="Robert W." last="Sussman">Robert W. Sussman</name>
<affiliation>
<nlm:aff id="aff25">Department of Anthropology, Washington University, St. Louis, MO 63130, USA.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Pan, Ruliang" sort="Pan, Ruliang" uniqKey="Pan R" first="Ruliang" last="Pan">Ruliang Pan</name>
<affiliation>
<nlm:aff id="aff26">School of Anatomy, Physiology and Human Biology, University of Western Australia (M309), 35 Stirling Highway, Crawley, Western Australia 6009, Australia.</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Kone, Inza" sort="Kone, Inza" uniqKey="Kone I" first="Inza" last="Kone">Inza Kone</name>
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<nlm:aff id="aff27">Centre Suisse des Recherches Scientifiques, Université de Cocody, Abidjan, Côte d’Ivoire.</nlm:aff>
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<author>
<name sortKey="Li, Baoguo" sort="Li, Baoguo" uniqKey="Li B" first="Baoguo" last="Li">Baoguo Li</name>
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<nlm:aff id="aff28">Xi’an Branch of Chinese Academy of Sciences, College of Life Sciences, Northwest University, No. 229, Taibai North Road, Xi’an 710069, China.</nlm:aff>
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<front>
<div type="abstract" xml:lang="en">
<p>Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend.</p>
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<pmc article-type="review-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Sci Adv</journal-id>
<journal-id journal-id-type="iso-abbrev">Sci Adv</journal-id>
<journal-id journal-id-type="publisher-id">SciAdv</journal-id>
<journal-id journal-id-type="hwp">advances</journal-id>
<journal-title-group>
<journal-title>Science Advances</journal-title>
</journal-title-group>
<issn pub-type="epub">2375-2548</issn>
<publisher>
<publisher-name>American Association for the Advancement of Science</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">28116351</article-id>
<article-id pub-id-type="pmc">5242557</article-id>
<article-id pub-id-type="publisher-id">1600946</article-id>
<article-id pub-id-type="doi">10.1126/sciadv.1600946</article-id>
<article-categories>
<subj-group subj-group-type="article-type">
<subject>Review</subject>
</subj-group>
<subj-group subj-group-type="heading">
<subject>Reviews</subject>
</subj-group>
<subj-group subj-group-type="legacy-article-type">
<subject>SciAdv reviews</subject>
</subj-group>
<subj-group subj-group-type="overline">
<subject>Primatology</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Impending extinction crisis of the world’s primates: Why primates matter</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Estrada</surname>
<given-names>Alejandro</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-6107-9109</contrib-id>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor1">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Garber</surname>
<given-names>Paul A.</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-6107-9109</contrib-id>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="corresp" rid="cor1">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rylands</surname>
<given-names>Anthony B.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
</contrib>
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<name>
<surname>Roos</surname>
<given-names>Christian</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0003-0190-4266</contrib-id>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Fernandez-Duque</surname>
<given-names>Eduardo</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-3993-7912</contrib-id>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Di Fiore</surname>
<given-names>Anthony</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0001-8893-9052</contrib-id>
<xref ref-type="aff" rid="aff6">
<sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nekaris</surname>
<given-names>K. Anne-Isola</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0001-5523-7353</contrib-id>
<xref ref-type="aff" rid="aff7">
<sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nijman</surname>
<given-names>Vincent</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-5600-4276</contrib-id>
<xref ref-type="aff" rid="aff7">
<sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Heymann</surname>
<given-names>Eckhard W.</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-4259-8018</contrib-id>
<xref ref-type="aff" rid="aff8">
<sup>8</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lambert</surname>
<given-names>Joanna E.</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-2849-3930</contrib-id>
<xref ref-type="aff" rid="aff9">
<sup>9</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rovero</surname>
<given-names>Francesco</given-names>
</name>
<xref ref-type="aff" rid="aff10">
<sup>10</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Barelli</surname>
<given-names>Claudia</given-names>
</name>
<xref ref-type="aff" rid="aff10">
<sup>10</sup>
</xref>
</contrib>
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<name>
<surname>Setchell</surname>
<given-names>Joanna M.</given-names>
</name>
<xref ref-type="aff" rid="aff11">
<sup>11</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gillespie</surname>
<given-names>Thomas R.</given-names>
</name>
<xref ref-type="aff" rid="aff12">
<sup>12</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Mittermeier</surname>
<given-names>Russell A.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Arregoitia</surname>
<given-names>Luis Verde</given-names>
</name>
<xref ref-type="aff" rid="aff13">
<sup>13</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>de Guinea</surname>
<given-names>Miguel</given-names>
</name>
<xref ref-type="aff" rid="aff7">
<sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gouveia</surname>
<given-names>Sidney</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0003-4941-7440</contrib-id>
<xref ref-type="aff" rid="aff14">
<sup>14</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Dobrovolski</surname>
<given-names>Ricardo</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-8775-5486</contrib-id>
<xref ref-type="aff" rid="aff15">
<sup>15</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Shanee</surname>
<given-names>Sam</given-names>
</name>
<xref ref-type="aff" rid="aff16">
<sup>16</sup>
</xref>
<xref ref-type="aff" rid="aff17">
<sup>17</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Shanee</surname>
<given-names>Noga</given-names>
</name>
<xref ref-type="aff" rid="aff16">
<sup>16</sup>
</xref>
<xref ref-type="aff" rid="aff17">
<sup>17</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Boyle</surname>
<given-names>Sarah A.</given-names>
</name>
<xref ref-type="aff" rid="aff18">
<sup>18</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Fuentes</surname>
<given-names>Agustin</given-names>
</name>
<xref ref-type="aff" rid="aff19">
<sup>19</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>MacKinnon</surname>
<given-names>Katherine C.</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0003-2586-9418</contrib-id>
<xref ref-type="aff" rid="aff20">
<sup>20</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Amato</surname>
<given-names>Katherine R.</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0003-2722-9414</contrib-id>
<xref ref-type="aff" rid="aff21">
<sup>21</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Meyer</surname>
<given-names>Andreas L. S.</given-names>
</name>
<xref ref-type="aff" rid="aff22">
<sup>22</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wich</surname>
<given-names>Serge</given-names>
</name>
<xref ref-type="aff" rid="aff23">
<sup>23</sup>
</xref>
<xref ref-type="aff" rid="aff24">
<sup>24</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sussman</surname>
<given-names>Robert W.</given-names>
</name>
<xref ref-type="aff" rid="aff25">
<sup>25</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pan</surname>
<given-names>Ruliang</given-names>
</name>
<xref ref-type="aff" rid="aff26">
<sup>26</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kone</surname>
<given-names>Inza</given-names>
</name>
<xref ref-type="aff" rid="aff27">
<sup>27</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Li</surname>
<given-names>Baoguo</given-names>
</name>
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0003-2506-7597</contrib-id>
<xref ref-type="aff" rid="aff28">
<sup>28</sup>
</xref>
</contrib>
<aff id="aff1">
<label>1</label>
Institute of Biology, National Autonomous University of Mexico, CP 04510, Mexico City, Mexico.</aff>
<aff id="aff2">
<label>2</label>
Department of Anthropology, Program in Ecology, Evolution, and Conservation Biology, University of Illinois, Urbana, IL 61801, USA.</aff>
<aff id="aff3">
<label>3</label>
Conservation International, 2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA.</aff>
<aff id="aff4">
<label>4</label>
Gene Bank of Primates and Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Göttingen, Germany.</aff>
<aff id="aff5">
<label>5</label>
Department of Anthropology, Yale University, New Haven, CT 06511, USA.</aff>
<aff id="aff6">
<label>6</label>
Department of Anthropology, University of Texas, Austin, TX 78705, USA.</aff>
<aff id="aff7">
<label>7</label>
Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, U.K.</aff>
<aff id="aff8">
<label>8</label>
Abteilung Verhaltensökologie und Soziobiologie, Deutsches Primatenzentrum, Leibniz-Institut für Primatenforschung, Kellnerweg 4, D-37077 Göttingen, Germany.</aff>
<aff id="aff9">
<label>9</label>
Department of Anthropology, University of Colorado at Boulder, 1350 Pleasant Street UCB 233, Boulder, CO 80309, USA.</aff>
<aff id="aff10">
<label>10</label>
Tropical Biodiversity Section, MUSE—Museo delle Scienze, Corso del Lavoro e della Scienza 3, 38122 Trento, Italy.</aff>
<aff id="aff11">
<label>11</label>
Department of Anthropology, and Behaviour, Ecology and Evolution Research Centre, Durham University, South Road, Durham DH1 3LE, U.K.</aff>
<aff id="aff12">
<label>12</label>
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.</aff>
<aff id="aff13">
<label>13</label>
Naturhistorisches Museum Bern, Bernastrasse 15, CH-3005 Bern, Switzerland.</aff>
<aff id="aff14">
<label>14</label>
Department of Ecology, Federal University of Sergipe, São Cristóvão, SE 49100-000, Brazil.</aff>
<aff id="aff15">
<label>15</label>
Department of Zoology, Federal University of Bahia, Salvador, BA 40170-290, Brazil.</aff>
<aff id="aff16">
<label>16</label>
Neotropical Primate Conservation, 23 Portland Road, Manchester M32 0PH, U.K.</aff>
<aff id="aff17">
<label>17</label>
Asociación Neotropical Primate Conservation Perú, 1187 Avenida Belaunde, La Esperanza, Yambrasbamba, Bongará, Amazonas, Peru.</aff>
<aff id="aff18">
<label>18</label>
Department of Biology, Rhodes College, 2000 North Parkway, Memphis, TN 38112, USA.</aff>
<aff id="aff19">
<label>19</label>
Department of Anthropology, University of Notre Dame, Notre Dame, IN 46556, USA.</aff>
<aff id="aff20">
<label>20</label>
Department of Sociology and Anthropology, Saint Louis University, St. Louis, MO 63108, USA.</aff>
<aff id="aff21">
<label>21</label>
Department of Anthropology, Northwestern University, 1810 Hinman Avenue, Evanston, IL 60208, USA.</aff>
<aff id="aff22">
<label>22</label>
Programa de Pós-Graduação em Zoologia, Departamento de Zoologia, Universidade Federal do Paraná, C.P. 19020, Curitiba, PR 81531-990, Brazil.</aff>
<aff id="aff23">
<label>23</label>
School of Natural Sciences and Psychology, Liverpool John Moores University, James Parsons Building, Byrom Street, Liverpool L3 3AF, U.K.</aff>
<aff id="aff24">
<label>24</label>
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands.</aff>
<aff id="aff25">
<label>25</label>
Department of Anthropology, Washington University, St. Louis, MO 63130, USA.</aff>
<aff id="aff26">
<label>26</label>
School of Anatomy, Physiology and Human Biology, University of Western Australia (M309), 35 Stirling Highway, Crawley, Western Australia 6009, Australia.</aff>
<aff id="aff27">
<label>27</label>
Centre Suisse des Recherches Scientifiques, Université de Cocody, Abidjan, Côte d’Ivoire.</aff>
<aff id="aff28">
<label>28</label>
Xi’an Branch of Chinese Academy of Sciences, College of Life Sciences, Northwest University, No. 229, Taibai North Road, Xi’an 710069, China.</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<label>*</label>
Corresponding author. Email:
<email xlink:href="aestradaprimates@gmail.com">aestradaprimates@gmail.com</email>
(A.E.);
<email xlink:href="p-garber@illinois.edu">p-garber@illinois.edu</email>
(P.A.G.)</corresp>
</author-notes>
<pub-date pub-type="collection">
<month>1</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="epub">
<day>18</day>
<month>1</month>
<year>2017</year>
</pub-date>
<volume>3</volume>
<issue>1</issue>
<elocation-id>e1600946</elocation-id>
<history>
<date date-type="received">
<day>30</day>
<month>4</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>22</day>
<month>11</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2017, The Authors</copyright-statement>
<copyright-year>2017</copyright-year>
<copyright-holder>The Authors</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc/4.0/" id="p-2">
<license-p>This is an open-access article distributed under the terms of the
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/4.0/">Creative Commons Attribution-NonCommercial license</ext-link>
, which permits use, distribution, and reproduction in any medium, so long as the resultant use is
<bold>not</bold>
for commercial advantage and provided the original work is properly cited.</license-p>
</license>
</permissions>
<abstract abstract-type="teaser">
<p>Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend.</p>
</abstract>
<abstract>
<p>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.</p>
</abstract>
<kwd-group>
<title>Keywords</title>
<kwd>nonhuman primates</kwd>
<kwd>tropical forests</kwd>
<kwd>deforestation</kwd>
<kwd>hunting</kwd>
<kwd>illegal trade</kwd>
<kwd>primate conservation</kwd>
<kwd>sustainable land use</kwd>
<kwd>industrial agriculture</kwd>
<kwd>ecosystem health</kwd>
<kwd>rural livelihoods</kwd>
</kwd-group>
<funding-group>
<award-group>
<funding-source>
<institution-wrap>
<institution>CNPq</institution>
</institution-wrap>
</funding-source>
<award-id>ID0EGCFM13839</award-id>
<award-id>476528/2013-5</award-id>
<principal-award-recipient>
<name>
<surname>Gouveia</surname>
<given-names>Sidney</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group>
<funding-source>
<institution-wrap>
<institution>CAPES, FAPESB, CNPq </institution>
</institution-wrap>
</funding-source>
<award-id>ID0EHIFM13840</award-id>
<award-id>461665/2014-0</award-id>
<principal-award-recipient>
<name>
<surname>Dobrovolski</surname>
<given-names>Ricardo</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group>
<funding-source>
<institution-wrap>
<institution>PRODOC/UFBA </institution>
</institution-wrap>
</funding-source>
<award-id>ID0E2MFM13841</award-id>
<award-id>5849/2013</award-id>
<principal-award-recipient>
<name>
<surname>Dobrovolski</surname>
<given-names>Ricardo</given-names>
</name>
</principal-award-recipient>
</award-group>
</funding-group>
<custom-meta-group>
<custom-meta>
<meta-name>Copyeditor</meta-name>
<meta-value>Mikee Bernabe</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
<body>
<sec sec-type="introduction" disp-level="1">
<title>INTRODUCTION</title>
<p>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.</p>
</sec>
<sec disp-level="1">
<title>IMPENDING DEFAUNATION OF THE WORLD’S PRIMATES</title>
<p>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) (
<xref rid="R1" ref-type="bibr">
<italic>1</italic>
</xref>
,
<xref rid="R2" ref-type="bibr">
<italic>2</italic>
</xref>
). 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) (
<xref rid="R2" ref-type="bibr">
<italic>2</italic>
</xref>
<xref rid="R5" ref-type="bibr">
<italic>5</italic>
</xref>
). Primates occur in four regions—the Neotropics (171 species), mainland Africa (111 species), Madagascar (103 species), and Asia (119 species) (
<xref ref-type="fig" rid="F1">Fig. 1</xref>
)—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 (
<xref rid="R2" ref-type="bibr">
<italic>2</italic>
</xref>
,
<xref rid="R4" ref-type="bibr">
<italic>4</italic>
</xref>
). The body mass of living primates ranges from 30 g in Madame Berthe’s mouse lemur (
<italic>Microcebus berthae</italic>
) to about 200 kg in male western and eastern gorillas (
<italic>Gorilla gorilla</italic>
and
<italic>Gorilla beringei</italic>
, respectively) (Supplementary Text) (
<xref rid="R2" ref-type="bibr">
<italic>2</italic>
</xref>
,
<xref rid="R4" ref-type="bibr">
<italic>4</italic>
</xref>
,
<xref rid="R5" ref-type="bibr">
<italic>5</italic>
</xref>
).</p>
<fig id="F1" fig-type="figure" orientation="portrait" position="float">
<label>Fig. 1</label>
<caption>
<title>Global primate species richness, distributions, and the percentage of species threatened and with declining populations.</title>
<p>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.</p>
</caption>
<graphic xlink:href="1600946-F1"></graphic>
</fig>
<p>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 (
<xref ref-type="fig" rid="F1">Figs. 1</xref>
and
<xref ref-type="fig" rid="F2">2</xref>
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 (
<xref ref-type="fig" rid="F1">Fig. 1</xref>
and figs. S2B and S3A). The populations of 75% of primate species are decreasing globally (
<xref ref-type="fig" rid="F1">Fig. 1</xref>
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.</p>
<fig id="F2" fig-type="figure" orientation="portrait" position="float">
<label>Fig. 2</label>
<caption>
<title>Percent of species threatened with extinction in each primate family.</title>
<p>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 (
<xref rid="R1" ref-type="bibr">
<italic>1</italic>
</xref>
<xref rid="R3" ref-type="bibr">
<italic>3</italic>
</xref>
).</p>
</caption>
<graphic xlink:href="1600946-F2"></graphic>
</fig>
</sec>
<sec disp-level="1">
<title>FACTORS THAT THREATEN PRIMATE POPULATIONS</title>
<p>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).</p>
<sec disp-level="2">
<title>Land-cover changes, global market demands, and industry-driven deforestation</title>
<p>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) (
<xref rid="R6" ref-type="bibr">
<italic>6</italic>
</xref>
). For example, between 1990 and 2010, agricultural expansion in primate range regions was estimated at 1.5 million km
<sup>2</sup>
(an area three times that of France) and forest cover loss at 2 million km
<sup>2</sup>
(
<xref ref-type="fig" rid="F3">Fig. 3</xref>
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 (
<italic>Pongo abelii</italic>
and
<italic>Pongo pygmaeus</italic>
, respectively) numbers and a serious risk for African apes because large segments of existing populations occur outside protected areas (
<xref rid="R7" ref-type="bibr">
<italic>7</italic>
</xref>
<xref rid="R10" ref-type="bibr">
<italic>10</italic>
</xref>
). Moreover, future oil palm development is likely to threaten forested areas in South America and Africa (
<xref rid="R10" ref-type="bibr">
<italic>10</italic>
</xref>
), 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 (
<italic>Nomascus leucogenys</italic>
) and the Hainan gibbon (
<italic>Nomascus hainanus</italic>
) (
<xref rid="R11" ref-type="bibr">
<italic>11</italic>
</xref>
). Similarly, deforestation due to the establishment of rubber plantations in India is reported to have severely affected the Bengal slow loris (
<italic>Nycticebus bengalensis</italic>
), the western hoolock gibbon (
<italic>Hoolock hoolock</italic>
), and Phayre’s langur (
<italic>Trachypithecus phayrei</italic>
) (
<xref rid="R11" ref-type="bibr">
<italic>11</italic>
</xref>
,
<xref rid="R12" ref-type="bibr">
<italic>12</italic>
</xref>
). 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 (
<xref ref-type="fig" rid="F4">Fig. 4</xref>
). 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 (
<xref rid="R13" ref-type="bibr">
<italic>13</italic>
</xref>
).</p>
<fig id="F3" fig-type="figure" orientation="portrait" position="float">
<label>Fig. 3</label>
<caption>
<title>Agricultural expansion and declines in forest cover for the period 1990–2010 in primate range regions.</title>
<p>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).</p>
</caption>
<graphic xlink:href="1600946-F3"></graphic>
</fig>
<fig id="F4" fig-type="figure" orientation="portrait" position="float">
<label>Fig. 4</label>
<caption>
<title>Global patterns of forecasted agricultural expansion for the 21st century in primate range regions and estimated range contraction.</title>
<p>(
<bold>A</bold>
) Estimated current global primate distributions. (
<bold>B</bold>
) 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) (
<xref rid="R13" ref-type="bibr">
<italic>13</italic>
</xref>
). (
<bold>C</bold>
) 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.</p>
</caption>
<graphic xlink:href="1600946-F4"></graphic>
</fig>
</sec>
<sec disp-level="2">
<title>Logging, mining, and fossil fuel extraction</title>
<p>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) (
<xref rid="R14" ref-type="bibr">
<italic>14</italic>
</xref>
). 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 (
<italic>Dalbergia</italic>
) since 2009 has negatively affected several protected areas (
<xref rid="R15" ref-type="bibr">
<italic>15</italic>
</xref>
). 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 (
<xref rid="R16" ref-type="bibr">
<italic>16</italic>
</xref>
).</p>
<p>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 (
<xref rid="R17" ref-type="bibr">
<italic>17</italic>
</xref>
). In central Africa, the population densities of apes in mined forests [75.7 (45.35 to 126.33) nests/km
<sup>2</sup>
] are markedly lower than in forested sites where mining is absent [234 (185 to 299) nests/km
<sup>2</sup>
] (
<xref rid="R18" ref-type="bibr">
<italic>18</italic>
</xref>
). In Madagascar, illicit gold and sapphire mining by itinerant miners has affected many forests, including protected ones (
<xref rid="R19" ref-type="bibr">
<italic>19</italic>
</xref>
). Mining of gold, nickel, and copper on Dinagat island, in the Philippines, is endangering the survival of the Philippine tarsier (
<italic>Carlito syrichta</italic>
) (
<xref rid="R20" ref-type="bibr">
<italic>20</italic>
</xref>
). Bushmeat hunting associated with the mining of coltan, tin, gold, and diamonds in the DRC is the main threat to Grauer’s gorilla (
<italic>G. beringei graueri</italic>
) (
<xref rid="R21" ref-type="bibr">
<italic>21</italic>
</xref>
); recent surveys indicate a 77% decline in its numbers, from 17,000 in 1995 to just 3800 in 2014/2015 (
<xref rid="R22" ref-type="bibr">
<italic>22</italic>
</xref>
). In Perú, the mining of zinc and copper threatens the endemic and Critically Endangered yellow-tailed woolly monkey (
<italic>Lagothrix flavicauda</italic>
) (
<xref rid="R23" ref-type="bibr">
<italic>23</italic>
</xref>
). 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 km
<sup>2</sup>
(twice the size of Germany) (
<xref rid="R24" ref-type="bibr">
<italic>24</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Other anthropogenic stressors</title>
<p>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) (
<xref rid="R25" ref-type="bibr">
<italic>25</italic>
</xref>
). 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) (
<xref rid="R26" ref-type="bibr">
<italic>26</italic>
</xref>
). 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 (
<xref rid="R27" ref-type="bibr">
<italic>27</italic>
</xref>
). 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
<sup>2</sup>
of forest cover, affecting populations of the Endangered Müller’s gibbon (
<italic>Hylobates muelleri</italic>
) (
<xref rid="R28" ref-type="bibr">
<italic>28</italic>
</xref>
).</p>
<p>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 (
<xref rid="R9" ref-type="bibr">
<italic>9</italic>
</xref>
,
<xref rid="R29" ref-type="bibr">
<italic>29</italic>
</xref>
<xref rid="R33" ref-type="bibr">
<italic>33</italic>
</xref>
). 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 (
<xref rid="R29" ref-type="bibr">
<italic>29</italic>
</xref>
). 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 (
<xref rid="R29" ref-type="bibr">
<italic>29</italic>
</xref>
). In other cases, crop feeding by primates (for example, howler monkeys) is tolerated without any economic reward (
<xref rid="R30" ref-type="bibr">
<italic>30</italic>
</xref>
). Where human and nonhuman primates come into more severe conflict due to crop raiding [for example, chimpanzees (
<italic>Pan troglodytes</italic>
), gorillas (
<italic>Gorilla</italic>
spp.), and baboons (
<italic>Papio</italic>
spp.) in Africa and orangutans (
<italic>Pongo</italic>
spp.) in Southeast Asia] (
<xref rid="R9" ref-type="bibr">
<italic>9</italic>
</xref>
,
<xref rid="R31" ref-type="bibr">
<italic>31</italic>
</xref>
<xref rid="R33" ref-type="bibr">
<italic>33</italic>
</xref>
), culturally and economically appropriate management interventions can mitigate the impact (
<xref rid="R9" ref-type="bibr">
<italic>9</italic>
</xref>
,
<xref rid="R33" ref-type="bibr">
<italic>33</italic>
</xref>
). 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 (
<xref ref-type="fig" rid="F4">Fig. 4</xref>
).</p>
<p>Civil unrest also affects primate populations because of saturation bombing, the use of defoliating chemicals (
<xref rid="R34" ref-type="bibr">
<italic>34</italic>
</xref>
,
<xref rid="R35" ref-type="bibr">
<italic>35</italic>
</xref>
), and the increase in bushmeat hunting. Poaching of bonobos (
<italic>Pan paniscus</italic>
) and gorillas, for example, markedly increased in the DRC and Rwanda as a result of ongoing civil wars (
<xref rid="R34" ref-type="bibr">
<italic>34</italic>
</xref>
). In Cambodia, armed conflicts have severely affected populations of the black-shanked douc (
<italic>Pygathrix nigripes</italic>
) (
<xref rid="R35" ref-type="bibr">
<italic>35</italic>
</xref>
). Land mines, the legacy of wars in the 1960s and 1970s, continue to endanger apes in Southeast Asia and Africa (
<xref rid="R34" ref-type="bibr">
<italic>34</italic>
</xref>
,
<xref rid="R36" ref-type="bibr">
<italic>36</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Forest fragmentation and degradation and the limited resilience of primates</title>
<p>Long-term deforestation has resulted in the fragmentation of 58% of subtropical and 46% of tropical forests (
<xref rid="R37" ref-type="bibr">
<italic>37</italic>
</xref>
,
<xref rid="R38" ref-type="bibr">
<italic>38</italic>
</xref>
), 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 (
<italic>Saguinus bicolor</italic>
), northern muriquis (
<italic>Brachyteles hypoxanthus</italic>
), Udzungwa red colobus monkeys (
<italic>Piliocolobus gordonorum</italic>
), several species of Chinese colobines (
<italic>Rhinopithecus</italic>
and
<italic>Trachypithecus</italic>
), Cross River gorillas (
<italic>G. gorilla diehli</italic>
), and Bornean orangutans (
<xref rid="R39" ref-type="bibr">
<italic>39</italic>
</xref>
<xref rid="R45" ref-type="bibr">
<italic>45</italic>
</xref>
). Edge effects predominate in many areas of disturbed forests, exacerbating habitat degradation (
<xref rid="R37" ref-type="bibr">
<italic>37</italic>
</xref>
). 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 (
<xref rid="R46" ref-type="bibr">
<italic>46</italic>
</xref>
,
<xref rid="R47" ref-type="bibr">
<italic>47</italic>
</xref>
). 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 (
<xref ref-type="fig" rid="F1">Fig. 1</xref>
).</p>
<p>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,
<italic>Acacia</italic>
plantations, and oil palm plantations (
<xref rid="R48" ref-type="bibr">
<italic>48</italic>
</xref>
). Baboons (
<italic>Papio</italic>
), Hanuman langurs (
<italic>Semnopithecus</italic>
), and macaques (
<italic>Macaca</italic>
) are particularly adaptable and can survive even in urban areas (
<xref rid="R49" ref-type="bibr">
<italic>49</italic>
</xref>
). Chimpanzees appear to evaluate risks when crop-foraging and adjust their foraging patterns in deciding whether to exploit fragmented forests near humans (
<xref rid="R50" ref-type="bibr">
<italic>50</italic>
</xref>
). 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 (
<xref rid="R51" ref-type="bibr">
<italic>51</italic>
</xref>
). 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 (
<xref rid="R52" ref-type="bibr">
<italic>52</italic>
</xref>
).</p>
<p>Primates in degraded forests face nutritional shortfalls and lower gut microbial diversity (
<xref rid="R53" ref-type="bibr">
<italic>53</italic>
</xref>
<xref rid="R55" ref-type="bibr">
<italic>55</italic>
</xref>
). They also show an increased prevalence of parasites and pathogens. For example, the increased exposure of lemurs (
<italic>Avahi laniger</italic>
,
<italic>Eulemur rubriventer</italic>
,
<italic>Hapalemur aureus</italic>
,
<italic>Microcebus rufus</italic>
,
<italic>Propithecus edwardsi</italic>
, and
<italic>Prolemur simus</italic>
) and chimpanzees (
<italic>P. troglodytes</italic>
) to human populations has increased their risk of infection by diarrhea-causing enteric pathogens (
<xref rid="R56" ref-type="bibr">
<italic>56</italic>
</xref>
,
<xref rid="R57" ref-type="bibr">
<italic>57</italic>
</xref>
). The close phylogenetic relationship between humans and other primates also creates an exceptionally high potential for pathogen exchange (
<xref rid="R58" ref-type="bibr">
<italic>58</italic>
</xref>
), 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) (
<xref rid="R59" ref-type="bibr">
<italic>59</italic>
</xref>
). 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 (
<xref rid="R60" ref-type="bibr">
<italic>60</italic>
</xref>
). Primates escaping or released from the pet trade or sanctuaries can carry pathogens with a potential of transmission to resident populations (
<xref rid="R61" ref-type="bibr">
<italic>61</italic>
</xref>
). Moreover, ecotourism and research, despite contributing in positive ways to primate conservation, have the unintended consequence of exposing wild primates to human pathogens (
<xref rid="R62" ref-type="bibr">
<italic>62</italic>
</xref>
,
<xref rid="R63" ref-type="bibr">
<italic>63</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Hunting</title>
<p>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 (
<xref rid="R45" ref-type="bibr">
<italic>45</italic>
</xref>
,
<xref rid="R64" ref-type="bibr">
<italic>64</italic>
</xref>
). 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) (
<xref rid="R64" ref-type="bibr">
<italic>64</italic>
</xref>
). 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 (
<xref rid="R45" ref-type="bibr">
<italic>45</italic>
</xref>
). Because only a relatively small number of primates live inside protected areas [for example, 21 to 27.5% of all great apes (
<xref rid="R51" ref-type="bibr">
<italic>51</italic>
</xref>
,
<xref rid="R65" ref-type="bibr">
<italic>65</italic>
</xref>
)], 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 (
<xref rid="R66" ref-type="bibr">
<italic>66</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Legal and illegal trade</title>
<p>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 (
<xref rid="R67" ref-type="bibr">
<italic>67</italic>
</xref>
,
<xref rid="R68" ref-type="bibr">
<italic>68</italic>
</xref>
). 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 (
<italic>Aotus</italic>
) 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 (
<italic>Aotus nancymaae</italic>
,
<italic>Aotus vociferans</italic>
, and
<italic>Aotus nigriceps</italic>
) were traded to a single biomedical research facility between 2007 and 2008 alone, for a price of approximately $100,000 (
<xref rid="R69" ref-type="bibr">
<italic>69</italic>
</xref>
). The expansion of road networks in frontier forests facilitates the extraction and trade of primates to cities and beyond borders (
<xref rid="R25" ref-type="bibr">
<italic>25</italic>
</xref>
). Together with increasing opportunities from e-commerce, this has given suppliers and smugglers unprecedented access to new markets (
<xref rid="R70" ref-type="bibr">
<italic>70</italic>
</xref>
,
<xref rid="R71" ref-type="bibr">
<italic>71</italic>
</xref>
). 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) (
<xref rid="R72" ref-type="bibr">
<italic>72</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Climate change</title>
<p>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 (
<xref rid="R73" ref-type="bibr">
<italic>73</italic>
</xref>
). 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 (
<xref rid="R74" ref-type="bibr">
<italic>74</italic>
</xref>
,
<xref rid="R75" ref-type="bibr">
<italic>75</italic>
</xref>
). 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) (
<xref rid="R76" ref-type="bibr">
<italic>76</italic>
</xref>
). Forest fragmentation induced by climate change can affect the availability of dispersal routes (
<xref rid="R77" ref-type="bibr">
<italic>77</italic>
</xref>
). Climate change may also force individuals out of protected areas, making them more vulnerable to hunting and other anthropogenic impacts (
<xref rid="R78" ref-type="bibr">
<italic>78</italic>
</xref>
), and range shifts among interacting species can affect food supplies and introduce new predators, pathogens, and/or competitors (
<xref rid="R79" ref-type="bibr">
<italic>79</italic>
</xref>
). 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 (
<xref rid="R80" ref-type="bibr">
<italic>80</italic>
</xref>
). Additionally, more frequent and severe climate change can induce floods, droughts, fires, hurricanes, and El Niño–Southern Oscillation events (
<xref rid="R81" ref-type="bibr">
<italic>81</italic>
</xref>
) that can affect the food supply available to primate populations, with negative impacts on health, fertility, and mortality (
<xref rid="R82" ref-type="bibr">
<italic>82</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Extinction risk and phylogenetic signal</title>
<p>The effect of anthropogenic threats on primates may be compounded by phylogenetic relatedness. Multispecies analyses have shown that extinction risk is not spread randomly across mammalian taxa. Rather, the prevalence of threatened taxa in some clades but not in others implies a strong phylogenetic pattern in susceptibility (
<xref rid="R83" ref-type="bibr">
<italic>83</italic>
</xref>
,
<xref rid="R84" ref-type="bibr">
<italic>84</italic>
</xref>
). Our own comparative analysis of 340 primate species suggests that closely related species are more likely to face the same threat status relative to species selected randomly from the phylogeny (
<xref ref-type="fig" rid="F5">Fig. 5</xref>
, fig. S9, A to C, and Supplementary Text). This result is likely due to the fact that related taxa share intrinsic aspects of their biology, such as body mass, life history, reproductive physiology, geographical distribution, dietary requirements, and behaviors (
<xref rid="R85" ref-type="bibr">
<italic>85</italic>
</xref>
<xref rid="R87" ref-type="bibr">
<italic>87</italic>
</xref>
). For example, several colobines (
<italic>Trachypithecus</italic>
,
<italic>Presbytis</italic>
, and
<italic>Simias</italic>
) in Southeast Asia are highly threatened island endemics and share biological traits known to increase their exposure and vulnerability to threats and extinction risks, such as relatively large body mass, diurnal behavior, and restricted geographic ranges.</p>
<fig id="F5" fig-type="figure" orientation="portrait" position="float">
<label>Fig. 5</label>
<caption>
<title>Phylogenetic signal as a predictor of extinction risk in the world’s primates.</title>
<p>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 (
<xref rid="R73" ref-type="bibr">
<italic>73</italic>
</xref>
), 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 [
<italic>D</italic>
= 0.31;
<italic>P</italic>
(
<italic>D</italic>
< 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).</p>
</caption>
<graphic xlink:href="1600946-F5"></graphic>
</fig>
</sec>
</sec>
<sec disp-level="1">
<title>WHY PRIMATES MATTER</title>
<sec disp-level="2">
<title>Social and cultural importance</title>
<p>Beyond sharing a close evolutionary history with humans, primates contribute importantly to the biological and cultural richness and the natural heritage of the countries in which they occur. Many primates play key roles in ecosystem dynamics and sustainability and are central figures in local and regional traditional knowledge, folklore, history, and even economies (
<xref rid="R88" ref-type="bibr">
<italic>88</italic>
</xref>
). For example, throughout South and Southeast Asia, monkeys figure strongly in Hindu and Buddhist mythology (for example, the Hanuman langur is the monkey god Hanuman in the Ramayana) and have centuries-old sympatric relationships with humans at temples and holy shrines. Today, many of these “monkey temples” are tourist sites, where the monkeys are protected, and provide an important source of income for local populations (
<xref rid="R88" ref-type="bibr">
<italic>88</italic>
</xref>
). Many traditional societies protect or tolerate primates and have integrated them into their historical narratives as sacred cultural figures and persons, as pets, and as food. For example, the Amazonian Guajá people integrate monkeys into their kinship and religious systems while also relying on primates as a sustainable food source (
<xref rid="R89" ref-type="bibr">
<italic>89</italic>
</xref>
). As primates become locally rare or extinct, we risk losing complex ecological, social, and cultural relationships that have developed between humans and primates over millennia (Supplementary Text) (
<xref rid="R88" ref-type="bibr">
<italic>88</italic>
</xref>
,
<xref rid="R90" ref-type="bibr">
<italic>90</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Ecological importance</title>
<p>Primates are prey, predator, and mutualist species in food webs and thereby influence ecosystem structure, function, and resilience. Their evolution, feeding ecology, and geographic distribution are closely linked to the diversification of angiosperms, a principal source of food (pollen, nectar, fruits, and seeds) (
<xref rid="R91" ref-type="bibr">
<italic>91</italic>
</xref>
) for many animals and humans (
<xref rid="R92" ref-type="bibr">
<italic>92</italic>
</xref>
<xref rid="R94" ref-type="bibr">
<italic>94</italic>
</xref>
). Many primates have been identified or suspected as important pollinators due to their opportunistic nondestructive feeding on flowers and nectar (
<xref rid="R94" ref-type="bibr">
<italic>94</italic>
</xref>
,
<xref rid="R95" ref-type="bibr">
<italic>95</italic>
</xref>
). As consumers of different plant parts (for example, fruits, flowers, seeds, gums, and leaves), primates can affect plant propagule dissemination, cause tree mortality, and may negatively affect the reproductive investment of some plants (
<xref rid="R95" ref-type="bibr">
<italic>95</italic>
</xref>
). However, numerous primates are highly frugivorous, and their relatively large size enables them to disperse small and large seeds over long distances, enhancing forest regeneration (
<xref rid="R95" ref-type="bibr">
<italic>95</italic>
</xref>
). In the absence of zoochorous seed dispersal by primates, plant populations can experience decreased genetic heterozygosity and increased genetic subpopulation differentiation, increased negative density dependence, and decreased recruitment (
<xref rid="R96" ref-type="bibr">
<italic>96</italic>
</xref>
<xref rid="R99" ref-type="bibr">
<italic>99</italic>
</xref>
). For example, Madagascar’s lemurs display complex relationships with large seed–producing trees, and lemur extinction may be facilitating a decline in the viability of certain Malagasy tree species (
<xref rid="R100" ref-type="bibr">
<italic>100</italic>
</xref>
). The population collapse of large atelids and cebids in heavily hunted forests of Amazonia has severely degraded long-term forest dynamics and the sustainability of many hardwood tree species with implications for the carbon-storing potential of forests (
<xref rid="R101" ref-type="bibr">
<italic>101</italic>
</xref>
,
<xref rid="R102" ref-type="bibr">
<italic>102</italic>
</xref>
). Similarly, the hunting of gibbons in northern Thailand has had a negative effect on the demography of the lapsi tree (
<italic>Choerospondias axillaris</italic>
), which depends on gibbons to disperse its seeds into light gaps (
<xref rid="R103" ref-type="bibr">
<italic>103</italic>
</xref>
). The loss of primate seed dispersers has demonstrable impacts on human populations in the same ecosystems. For example, 48% of the plants whose seeds are dispersed by primates in the western regions of Côte d’Ivoire and 42% in Uganda have economic or cultural utility to local human inhabitants (
<xref rid="R92" ref-type="bibr">
<italic>92</italic>
</xref>
). In southern Nigeria, rural people rely on gathering primate-dispersed fruit and seed species (
<xref rid="R104" ref-type="bibr">
<italic>104</italic>
</xref>
), suggesting the considerable importance of primate conservation to local human food security.</p>
</sec>
<sec disp-level="2">
<title>Primates as model animals</title>
<p>Primates are highly valued model animals, advancing our understanding of the evolutionary history of our species and providing insight into human behavior, cognition, parenting, cooperation, adult social bonds, forms of social conflict and resolution, learning and memory, and the evolution of tool use and language (
<xref rid="R105" ref-type="bibr">
<italic>105</italic>
</xref>
<xref rid="R108" ref-type="bibr">
<italic>108</italic>
</xref>
). Although there exist important ethical issues that need to be considered when using primates in medical research (
<xref rid="R109" ref-type="bibr">
<italic>109</italic>
</xref>
), primate models have furthered our understanding of atherosclerosis, respiratory diseases, HIV/AIDS, treatment responses to psychoactive drugs, psychopathologies, sociality, mental health disorders, communication, immunology, brain functioning, pharmacology, endocrine regulation of reproduction, genetics and genomics, and disease risk and parasite dynamics, among many other subjects (
<xref rid="R109" ref-type="bibr">
<italic>109</italic>
</xref>
). Wild primate populations may hold valuable clues to the origins and evolution of important pathogens and processes of natural disease transmission by serving as sentinels for early disease detection, identification, and surveillance, thus benefiting humans. Because emerging infectious diseases also pose serious threats to both endangered and nonendangered primate species, studies of these diseases in one primate population may benefit conservation efforts for others (
<xref rid="R59" ref-type="bibr">
<italic>59</italic>
</xref>
).</p>
</sec>
</sec>
<sec disp-level="1">
<title>ADDRESSING CONSERVATION NEEDS</title>
<p>Deforestation, hunting, illegal trade, and wood extraction are leading to a worldwide impoverishment of primate fauna. Drivers of primate loss are dynamic and interact with each other at local, regional, and global scales, leading to a trajectory of biosimplification that is most keenly felt as marked reductions in population sizes and, all too soon, extinctions (
<xref ref-type="fig" rid="F6">Fig. 6</xref>
). The global scale of primate population declines and the predicted increase in the intensity of major anthropogenic threats (
<xref ref-type="fig" rid="F1">Fig. 1</xref>
) suggest that conserving wild primates is an immediate but daunting challenge. Without widespread systemic changes in human behavior, populations will continue to decline over the next few decades, with species currently listed by the IUCN as Threatened becoming extinct and species now classified as Near Threatened or Least Concern facing increased extinction risk. Many primates are iconic (for example, gorillas, chimpanzees, orangutans, spider monkeys, and lemurs;
<xref ref-type="fig" rid="F7">Fig. 7</xref>
), but given the scale of their decline, it is clear that neither their charisma nor their flagship status is sufficient to safeguard them from the threat of human-induced extirpation throughout their native ranges. Extinction rarely results from deficient scientific knowledge of the steps required to protect the species. Instead, it is embedded in political uncertainty, socioeconomic instability, organized criminality, corruption, and policies that favor short-term profits over long-term sustainability (
<xref rid="R110" ref-type="bibr">
<italic>110</italic>
</xref>
). Meaningful primate conservation will require a major revolution in commitment and policy. Alleviating pressures upon primate habitats requires decreasing the per capita demand of industrialized nations for tropical hardwoods, beef, palm oil, soy, rubber, minerals, and fossil fuels, among other goods, while simultaneously promoting sustainable resource-use practices (
<xref ref-type="fig" rid="F6">Fig. 6</xref>
) (
<xref rid="R111" ref-type="bibr">
<italic>111</italic>
</xref>
).</p>
<fig id="F6" fig-type="figure" orientation="portrait" position="float">
<label>Fig. 6</label>
<caption>
<title>Factors driving primate population declines and possible mitigating approaches.</title>
<p>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.</p>
</caption>
<graphic xlink:href="1600946-F6"></graphic>
</fig>
<fig id="F7" fig-type="figure" orientation="portrait" position="float">
<label>Fig. 7</label>
<caption>
<title>Photos of selected primates from each major world region.</title>
<p>Conservation status and photo credits include the following: (
<bold>A</bold>
) Golden snub-nosed monkey (
<italic>Rhinopithecus roxellana</italic>
), Endangered, P. A. Garber. (
<bold>B</bold>
) Ring-tailed lemur (
<italic>Lemur catta</italic>
), Endangered, R. A. Mittermeier. (
<bold>C</bold>
) Udzungwa red colobus (
<italic>P. gordonorum</italic>
), Endangered (Photo Credit: Thomas Struhsaker, Duke University). (
<bold>D</bold>
) Javan slow loris (
<italic>Nycticebus javanicus</italic>
), Critically Endangered (Photo Credit: Andrew Walmsley, Andrew Walmsley Photography). (
<bold>E</bold>
) Sumatran orangutan (
<italic>P. abelii</italic>
), Critically Endangered (Photo Credit: Perry van Duijnhoven). (
<bold>F</bold>
) Azara’s night monkey (
<italic>Aotus azarae</italic>
), Least Concern [Photo Credit: Claudia Valeggia (Yale University)/Owl Monkey Project, Formosa-Argentina].</p>
</caption>
<graphic xlink:href="1600946-F7"></graphic>
</fig>
<sec disp-level="2">
<title>Improving the human condition</title>
<p>The human capital in primate range localities is of utmost importance to primate conservation. High rates of human population growth (5.1 billion people in 2010 to 7.3 billion in 2050 in primate range countries), high levels of poverty and inequality, the loss of natural capital due to extensive and rapid land-cover changes driven by global market demands, poor governance, and the need for food security, health, and literacy are key factors to consider (Supplementary Text and fig. S7, A to C). Solutions to the challenge of primate conservation must include reducing human birth rates and population growth, improving health, reducing poverty and gender biases in education, developing sustainable land-use initiatives, and preserving traditional livelihoods (
<xref ref-type="fig" rid="F6">Fig. 6</xref>
) (
<xref rid="R112" ref-type="bibr">
<italic>112</italic>
</xref>
). Locally, people and governments need to become stakeholders in this effort and perceive that they can benefit from protecting primate populations and their forests while at the same time satisfying their basic needs. This will require education, rethinking, and investment from government, nongovernmental organizations (NGOs), and the private sector. There is no single solution to this global problem. Primate ecotourism may be an effective approach in some localities (for example, gorilla ecotourism in Rwanda, DRC, and Uganda) (
<xref rid="R113" ref-type="bibr">
<italic>113</italic>
</xref>
). In others, mini-livestock breeding may be a productive route to improve food security (
<xref rid="R114" ref-type="bibr">
<italic>114</italic>
</xref>
). Because bushmeat is an important source of food and income for inhabitants from poverty-ridden primate range countries, as well as an important aspect of indigenous culture, in some countries, nonprimate game ranching and game farming may contribute to food security and indirectly to primate conservation (
<xref rid="R115" ref-type="bibr">
<italic>115</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Expansion of protected areas</title>
<p>Although the percentage of the land surface devoted to protected areas has steadily increased in primate range countries (fig. S7D), highlighting protected areas as the only plausible conservation tool may contribute to local poverty by denying poor people power over and access to the natural resources that support their livelihoods (
<xref rid="R116" ref-type="bibr">
<italic>116</italic>
</xref>
). Protected areas must be sufficiently large and provide suitable primate habitats, and species of concern must be present in sufficient numbers within those areas (
<xref rid="R117" ref-type="bibr">
<italic>117</italic>
</xref>
). Unfortunately, countries in the Neotropics, Africa, and Asia are currently downgrading, downsizing, and degazetting protected areas due to growing industrial-scale natural resource extraction, and a significant number of protected areas are experiencing substantial deforestation (
<xref rid="R118" ref-type="bibr">
<italic>118</italic>
</xref>
,
<xref rid="R119" ref-type="bibr">
<italic>119</italic>
</xref>
). Despite these trends, protected areas can and do provide long-term sanctuary for wildlife. For example, a study in the Udzungwa mountains of Tanzania showed that colobine primate populations were stable in the protected areas but declined severely in the unprotected forests (
<xref rid="R120" ref-type="bibr">
<italic>120</italic>
</xref>
). An 8-year study (2007–2014) using camera traps to annually monitor terrestrial mammals and birds in 15 protected areas in the Neotropics, Africa, and Southeast Asia showed strong evidence of stability and even increases in populations, including those of 23 primate species (19 cercopithecines in Africa and Asia, 3 African apes, and 1 lemur) (
<xref rid="R121" ref-type="bibr">
<italic>121</italic>
</xref>
). A complementary conservation approach is the REDD+ program, where payments are made to tropical countries to reduce emissions from deforestation and forest degradation (
<xref rid="R122" ref-type="bibr">
<italic>122</italic>
</xref>
). REDD+ could be a productive approach to increasing primate habitat and connectivity via reforestation and to providing important economic and ecological value for local populations. However, as of yet, no examples of implemented programs and their success on primate conservation are available (
<xref rid="R123" ref-type="bibr">
<italic>123</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Land-sharing and land-sparing</title>
<p>Because forests are among the few economic assets available to the rural poor in the tropics, securing their ownership and sustainable commercial use can help poor families cope with and move out of poverty (
<xref rid="R124" ref-type="bibr">
<italic>124</italic>
</xref>
). In a land-sharing approach (mixing protection and production in an agroecological matrix), community-managed forests are one option to integrate forest management into national poverty reduction programs in rural areas, favoring primate species with small area requirements. These forests also have lower and less variable annual deforestation rates than protected ones (
<xref rid="R124" ref-type="bibr">
<italic>124</italic>
</xref>
). In both land-sparing (favoring species with large area requirements) and land-sharing approaches, promoting biodiversity and the use of lattice-work corridors to connect landscapes along latitudinal and elevational gradients may promote a diversity of habitats for the long-term persistence of primate species that differ in their ecological requirements and may mitigate some of the deleterious effects of climate change (
<xref rid="R125" ref-type="bibr">
<italic>125</italic>
</xref>
,
<xref rid="R126" ref-type="bibr">
<italic>126</italic>
</xref>
). A recent study of the fauna, including lemurs, of a 90-km-long biodiversity corridor connecting two national parks in Madagascar showed the need to differentiate among passive dispersers (species that settle randomly around the source population), active dispersers (species that settle only in favorable habitats), and gap-avoiding dispersers (species that avoid dispersing across nonhabitat areas). Thus, a better understanding of the natural history of different primates is critical to identify which taxa might be sustained within forested corridors and those for which no substitute or alternative habitat exists (
<xref rid="R127" ref-type="bibr">
<italic>127</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Use of new and traditional technology to monitor primate population vulnerability</title>
<p>A new science of monitoring primate habitats, population status, and anthropogenic threats is currently emerging. It includes taking advantage of global telecommunication systems and wireless Internet, satellite- and airborne-based imagery, drone technology, ever more powerful handheld devices (for example, smart phones and tablets), and camera traps (Supplementary Text) (
<xref rid="R120" ref-type="bibr">
<italic>120</italic>
</xref>
,
<xref rid="R128" ref-type="bibr">
<italic>128</italic>
</xref>
). Combined with geographic information system and ground surveys, some of this technology has been used in evaluating sustainable land-use spatial planning and human-primate conflicts [for example, Javan gibbons (
<italic>Hylobates</italic>
<italic>moloch</italic>
)] (
<xref rid="R129" ref-type="bibr">
<italic>129</italic>
</xref>
) and in providing case-by-case assessments of species vulnerability to climate change, as shown for Borneo’s orangutans (Supplementary Text) (
<xref rid="R80" ref-type="bibr">
<italic>80</italic>
</xref>
). These same technologies can also be used by local citizen scientists for species and habitat monitoring, thus enhancing the effectiveness of mitigation measures (
<xref rid="R128" ref-type="bibr">
<italic>128</italic>
</xref>
). Recent technological advances in molecular biology—particularly high-throughput sequencing of DNA extracted from noninvasive samples (for example, feces, urine, and hair)—can accelerate assessments of population size and structure, genetic diversity and evidence of outbreeding, diet (plant, vertebrate, and invertebrate DNA consumption), and parasite and gut microbial diversity for wild primates (
<xref rid="R130" ref-type="bibr">
<italic>130</italic>
</xref>
<xref rid="R134" ref-type="bibr">
<italic>134</italic>
</xref>
). These advances have allowed researchers to identify species and origins of primate parts confiscated in the illegal bushmeat or pet trade (
<xref rid="R135" ref-type="bibr">
<italic>135</italic>
</xref>
) and are helpful in the genetic assessment and management of captive populations designed to establish viable, hybrid-free, “backup” populations to refresh the genetic pool of wild populations via reintroduction (
<xref rid="R136" ref-type="bibr">
<italic>136</italic>
</xref>
,
<xref rid="R137" ref-type="bibr">
<italic>137</italic>
</xref>
).</p>
<p>Although these innovations open new avenues for primate study, successful, long-term programs that monitor primate population abundance also rely on simpler and less expensive methods that engage students and local research assistants, such as traditional census methods. There are relatively few multigeneration studies of primate population dynamics, largely because primates are long-living animals and population changes occur over time periods longer than the duration of most studies and research grants. However, a recent study from the Udzungwa Mountains of Tanzania combined locally based monitoring routines and advanced statistical approaches to investigate population abundance, even when information was missing for some monitoring periods (
<xref rid="R120" ref-type="bibr">
<italic>120</italic>
</xref>
). Another study showed the value of basic field procedures (transect surveys) in monitoring Sumatran orangutan populations, with results that doubled the estimated population from 6600 to 14,613, even though the population was still assessed as declining rapidly due to deforestation (
<xref rid="R138" ref-type="bibr">
<italic>138</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Mitigating illegal trade</title>
<p>It has been noted that to mitigate wildlife poaching, interventions need to go beyond regulation by encouraging capacity building in local communities to conserve wildlife, reexamining sustainable offtake mechanisms, such as regulated trade, ranching, and wildlife farming (
<xref rid="R139" ref-type="bibr">
<italic>139</italic>
</xref>
), and to use social media and the Internet to reduce demand and, ultimately, to curb trade (Supplementary Text and
<xref ref-type="fig" rid="F6">Fig. 6</xref>
) (
<xref rid="R71" ref-type="bibr">
<italic>71</italic>
</xref>
,
<xref rid="R140" ref-type="bibr">
<italic>140</italic>
</xref>
). Although the use of social media to raise local, regional, and global awareness of the plight of the world’s primate fauna and of the ecological, social, cultural, and economic importance of primates is, no doubt, essential, it is just as important to develop local, action-oriented conservation education programs, especially those targeting young people and community decision makers. These are powerful conservation tools, combining knowledge and action acquired from successful ongoing programs in Madagascar (
<xref rid="R141" ref-type="bibr">
<italic>141</italic>
</xref>
), West Java, Indonesia (
<xref rid="R142" ref-type="bibr">
<italic>142</italic>
</xref>
), and Colombia (
<xref rid="R143" ref-type="bibr">
<italic>143</italic>
</xref>
) (see details in Supplementary Text). Criminological investigation that focuses on bushmeat trade and the trafficking of primates for pets, body parts, and trophies is also important for tracing the supply chains and criminal networks involved in illegal trade (see the “Focus of future research efforts” section).</p>
</sec>
<sec disp-level="2">
<title>Reintroductions and long-term forest protection as conservation tools</title>
<p>Where primate species are locally extinct, reintroductions are an option but can be expensive, and long-term protection of forests is arguably a more cost-effective means of preserving primates than reintroduction (
<xref rid="R144" ref-type="bibr">
<italic>144</italic>
</xref>
). Nonetheless, reintroductions raise public and political awareness and provide placement solutions for rescued animals in line with welfare concerns. The use of wild-born, rescued, and rehabilitated primates instead of captive-bred animals in reintroduction programs reduces costs and can increase success (
<xref rid="R145" ref-type="bibr">
<italic>145</italic>
</xref>
). A range of primate species have been successfully introduced in some places, including orangutans, lar gibbons (
<italic>Hylobates lar</italic>
), southern yellow-cheeked gibbons (
<italic>Nomascus gabriellae</italic>
), Indonesian slow lorises (
<italic>Nycticebus</italic>
), Delacour’s langurs (
<italic>Trachypithecus delacouri</italic>
), western gorillas, woolly monkeys (
<italic>Lagothrix lagotricha</italic>
), golden lion tamarins (
<italic>Leontopithecus</italic>
<italic>rosalia</italic>
), and pygmy marmosets (
<italic>Cebuella pygmaea</italic>
) (
<xref rid="R146" ref-type="bibr">
<italic>146</italic>
</xref>
<xref rid="R150" ref-type="bibr">
<italic>150</italic>
</xref>
). Still, evidence of outbreeding and introgression in, for example, Bornean orangutan populations due to the reintroduction of rescued animals of different species and subspecies into wild populations highlights the care that must be taken using these kinds of conservation interventions (
<xref rid="R151" ref-type="bibr">
<italic>151</italic>
</xref>
).</p>
</sec>
<sec disp-level="2">
<title>Reducing the urban footprint on primate habitats</title>
<p>Worldwide, urban policies need to be targeted at reducing people’s ecological footprints in primate range regions. For instance, promoting the recycling of cell phones, laptops, and other electronic devices could diminish the demand for coltan mining from the Congo Basin in Central Africa, which threatens primates in the region, including gorillas and chimpanzees (
<xref rid="R22" ref-type="bibr">
<italic>22</italic>
</xref>
,
<xref rid="R152" ref-type="bibr">
<italic>152</italic>
</xref>
). Decreasing the world’s per capita demand for tropical hardwoods, food and nonfood products, minerals, and fossil fuels, among other goods, from primate range regions would help alleviate pressures on primate habitats (
<xref rid="R112" ref-type="bibr">
<italic>112</italic>
</xref>
).</p>
</sec>
</sec>
<sec disp-level="1">
<title>FOCUS OF FUTURE RESEARCH EFFORTS</title>
<p>The scientific research effort on primates, as measured by the number of published articles on individual primate species on the Web of Science from January 1965 to March 2016, yielded ~47,000 records pertaining to both wild and captive primates. Overall, 16% involve studies of Neotropical monkeys, 36% of African primates, and 48% of Asian primates. Sixty-six percent of the publication records focused on a single family, the Cercopithecidae, principally
<italic>Macaca</italic>
in Asia and
<italic>Papio</italic>
in Africa (fig. S10). These results reflect the important role of some taxa in this family (for example,
<italic>Macaca mulatta</italic>
and
<italic>Papio anubis</italic>
) as models for studies of human health, behavior, and physiology. Studies of primates in the African Hominidae (chimpanzees, bonobos, and gorillas) constituted another 10% of the total records, and species in the Neotropical families Callitrichidae, Cebidae, and Atelidae combined constituted 13%. Species in the remaining 11 primate families accounted for only 11% of the total records (fig. S10). Thus, despite considerable research efforts over the past 40 years, scientific data for a great majority of primate species are still limited. Moreover, decade-long studies have been conducted on very few species, and studies spanning several generations are even fewer. Such paucity of knowledge suggests that there is an urgent need to generate species- and habitat-specific knowledge about population size, life history and ecology, habitat loss, forest fragmentation, climate change, potential for disease transmission, and human-primate interactions, including detailed population/species recovery plans.</p>
<p>Cultural mapping and the fostering of mutually beneficial partnerships with government and people in local communities, coupled with ethnoprimatological field work, are effective tools to identify specific problems and workable in situ solutions for primate conservation (
<xref rid="R153" ref-type="bibr">
<italic>153</italic>
</xref>
). For example, a decade-long study in the Central African Republic revealed that traditional forest uses (for example, hunting and gathering) have been replaced by new activities, such as logging, bushmeat hunting, and even conservation programs, and that local human populations are both materially and culturally impoverished by animal declines (
<xref rid="R153" ref-type="bibr">
<italic>153</italic>
</xref>
). Another study showed that the use of lorises (
<italic>Nycticebus</italic>
and
<italic>Loris</italic>
) in traditional medicine and the pet trade in Sri Lanka, Cambodia, and Indonesia followed culturally specific patterns (
<xref rid="R154" ref-type="bibr">
<italic>154</italic>
</xref>
), and therefore, a deep understanding of local customs is required to develop effective conservation policies.</p>
<p>Because the unprecedented market globalization of the illegal wildlife, bushmeat, and amulet trade is rapidly depleting natural primate populations (
<xref rid="R110" ref-type="bibr">
<italic>110</italic>
</xref>
), criminological intelligence network analyses, within and outside range states, is critically needed. To be effective, this effort needs to integrate local and global attitudes about environmental insecurity and biodiversity exploitation. For example, local people’s perceptions of the risk associated with illegal lemur hunting in Madagascar do not reflect the perception of policy makers (
<xref rid="R155" ref-type="bibr">
<italic>155</italic>
</xref>
). Attention to poaching as a serious conservation crime will yield a better understanding of whether local people engage in such activities to ensure food security and/or to generate income and may illuminate how best to incentivize sustainable alternatives, such as food subsidies or employment as rangers and conservation guards (
<xref rid="R156" ref-type="bibr">
<italic>156</italic>
</xref>
). Given the severity of this problem, the social and organized crime contexts of primate bushmeat and live trade need to be included in an integrated model (
<xref rid="R157" ref-type="bibr">
<italic>157</italic>
</xref>
) that also addresses corruption in supervising government entities in charge of monitoring and prosecuting illegal trade (
<xref ref-type="fig" rid="F6">Fig. 6</xref>
) (
<xref rid="R110" ref-type="bibr">
<italic>110</italic>
</xref>
).</p>
<p>Finally, studies that document the interactions of anthropogenic drivers of environmental change with species-specific biological and behavioral traits (for example, body mass, reproductive rate, dietary flexibility, and nutritional needs) within a phylogenetic comparative framework are needed to further our understanding of the imminent threats faced by individual taxa, especially for species that have few close taxonomic relatives. Over the past two decades, a resynthesis and reorganization of new and previously collected data have increased the number of recognized primate species from 180 to 376 in 2005 and from 376 to 504 in 2016 (
<xref rid="R158" ref-type="bibr">
<italic>158</italic>
</xref>
<xref rid="R161" ref-type="bibr">
<italic>161</italic>
</xref>
). The recognition of the urgent need to understand the diversity of threatened primates inspired a workshop in 2000 in Orlando, Florida, sponsored by Disney’s Animal Kingdom. This workshop gave rise to landmark conservation assessments and action plans for each of the major primate regions (
<xref rid="R162" ref-type="bibr">
<italic>162</italic>
</xref>
<xref rid="R166" ref-type="bibr">
<italic>166</italic>
</xref>
).</p>
</sec>
<sec disp-level="1">
<title>CONCLUDING COMMENTS</title>
<p>Despite the impending extinction facing many of the world’s primates, we remain adamant that primate conservation is not yet a lost cause, and we are optimistic that the environmental and anthropogenic pressures leading to population declines can still be reversed. However, this is contingent on implementing effective scientific, political, and management decisions immediately. Unless we act, human-induced environmental threats in primate range regions will result in a continued and accelerated reduction in primate biodiversity. Primate taxa will be lost through a combination of habitat loss and degradation, population isolation in fragmented landscapes, population extirpation by hunting and trapping, and rapid population decline due to human and domestic animal-borne diseases, increasing human encroachment, and climate change. Perhaps the starkest conclusion of this review is that collectively—as researchers, educators, administrators, and politicians—we are failing to preserve primate species and their habitats. We face a formidable challenge moving forward, as success requires that sustainable solutions address the social, cultural, economic, and ecological interdependencies that are the basis of primate conservation. Our review suggests that by refocusing and publicizing our efforts to academics, government agencies, NGOs, businesses, and the public at large, we can build a comprehensive understanding of the consequences of primate population declines and encourage urgent and effective conservation policies. These policies will differ among countries, regions, habitats, and primate species based on the site-specific nature of each problem. We have one last opportunity to greatly reduce or even eliminate the human threats to primates and their habitats, to guide conservation efforts, and to raise worldwide awareness of their predicament. Primates are critically important to humanity. After all, they are our closest living biological relatives.</p>
</sec>
</body>
<back>
<ack>
<title>Acknowledgments</title>
<p>P.A.G. wishes to thank J. A. Garber for inspiring him to devote more of his time, energy, and thoughts to protecting the world’s endangered primate populations. We also would like to honor the memory of our esteemed coauthor, colleague, friend, and outstanding primatologist (R.W.S.), who passed away in June 2016. We dedicate this paper to him.
<bold>Funding:</bold>
No funding was used to support the writing of this review paper. However, S.G. and R.D. acknowledge the support of CNPq and of CAPES, FAPESB, CNPq (process 461665/2014-0), and PRODOC/UFBA (process 5849/2013), respectively.
<bold>Author contributions:</bold>
A.E. and P.A.G. conceived and designed the review. A.B.R. and C.R. updated and verified the taxonomy of species listed in tables S1 to S3. L.V.A. did the phylogenetic signal analysis and built the phylogenetic trees shown in
<xref ref-type="fig" rid="F5">Fig. 5</xref>
and fig. S4. M.d.G. assisted in compiling the species lists and retrieved the data from the Web of Science. M.d.G., K.A.-I.N., and V.N. compiled the CITES data on primate trade. S.G. and R.D. produced
<xref ref-type="fig" rid="F1">Figs. 1</xref>
and
<xref ref-type="fig" rid="F4">4</xref>
and fig. S2 and did the analysis on agricultural expansion and primate distributions. All of the other authors contributed data, discussed further analyses, and commented on various versions of the manuscript. S.S. is a project director of the UK Neotropical Primate Conservation and the Asociación Neotropical Primate Conservation, Perú.
<bold>Competing interests:</bold>
The authors declare that they have no competing interests. No institutional review board or institutional animal and welfare committee approval was needed for this study.
<bold>Data and materials availability:</bold>
All data are reported as estimates and used for assessments in the paper. This information is presented in the paper and/or in the Supplementary Materials. Additional data related to this paper may be requested from the authors.</p>
</ack>
<app-group>
<app>
<title>SUPPLEMENTARY MATERIALS</title>
<supplementary-material content-type="local-data">
<p>Supplementary material for this article is available at
<ext-link ext-link-type="uri" xlink:href="http://advances.sciencemag.org/cgi/content/full/3/1/e1600946/DC1">http://advances.sciencemag.org/cgi/content/full/3/1/e1600946/DC1</ext-link>
</p>
<p>fig. S1. Primate habitat countries ranked by the number of species present.</p>
<p>fig. S2. Countries with primate species in the Neotropics, Africa (including Madagascar), and Asia and percent of countries with threatened species.</p>
<p>fig. S3. IUCN threat categories and population status of primate species.</p>
<p>fig. S4. Percent of primate species listed under each proximate threat, according to the IUCN.</p>
<p>fig. S5. Growth trends in cattle stock, agricultural activity, and deforestation in primate range regions.</p>
<p>fig. S6. Agricultural expansion and declines in forest cover for the period 1990–2010 in the Neotropics, Africa, and Asia.</p>
<p>fig. S7. Human population growth in primate range regions.</p>
<p>fig. S8. Global primate trade for the period 2005–2014, as reported by parties to the CITES Secretariat.</p>
<p>fig. S9. Phylogenetic patterns associated with extinction risk for primate species in the Neotropics, Africa, and Asia.</p>
<p>fig. S10. Number of published articles found in the Web of Science for primate species in each family.</p>
<p>table S1. Primate species in the Neotropics grouped by family.</p>
<p>table S2. Primate species in mainland Africa grouped by family.</p>
<p>table S3. Primate species in Madagascar grouped by family.</p>
<p>table S4. Primate species in Asia grouped by family.</p>
<p>table S5. Summary of sources of threat and the number of primate species affected, according to the IUCN Red List.</p>
<p>table S6. Global international trade in primates for the period 2005–2014, as reported by parties to the CITES Secretariat.</p>
<p>Supplementary Text</p>
<p>References (
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</app>
</app-group>
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