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Main Manuscript for
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Factors influencing terrestriality in primates of the Americas and Madagascar
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Timothy M. Eppley a,b,1, Selwyn Hoeks c, Colin A. Chapman d,e,f,g, Jörg U. Ganzhorn h, Katie
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Hall i, Megan A. Owen a, Dara B. Adams j,k, Néstor Allgas l, Katherine R. Amato m, McAntonin
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Andriamahaihavana n, John F. Aristizabal o,p, Andrea L. Baden q,r,s, Michela Balestri t, Adrian A.
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Barnett u,v, Júlio César Bicca-Marques w, Mark Bowler a,x,y, Sarah A. Boyle z, Meredith Brown aa,
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Damien Caillaud bb, Cláudia Calegaro-Marques cc, Christina J. Campbell dd, Marco Campera t,
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Fernando A. Campos ee, Tatiane S. Cardoso ff, Xyomara Carretero-Pinzón gg, Jane Champion aa,
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Óscar M. Chaves hh, Chloe Chen-Kraus ii, Ian C. Colquhoun jj, Brittany Dean aa, Colin Dubrueil
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aa, Kelsey M. Ellis kk, Elizabeth M. Erhart ll, Kayley J. E. Evans aa, Linda M. Fedigan aa, Annika
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M. Felton mm, Renata G. Ferreira nn, Claudia Fichtel oo, Manuel L. Fonseca pp, Isadora P. Fontes
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qq,rr, Vanessa B. Fortes ss, Ivanyr Fumian tt, Dean Gibson a, Guilherme B. Guzzo uu, Kayla S.
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Hartwell aa,vv, Eckhard W. Heymann oo, Renato R. Hilário ww, Sheila M. Holmes xx, Mitchell T.
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Irwin yy, Steig E. Johnson aa, Peter M. Kappeler oo,zz, Elizabeth A. Kelley ab, Tony King ac,ad,ae,
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Christoph Knogge af, Flávia Koch oo, Martin M. Kowalewski ag, Liselot R. Lange ah,ai, M. Elise
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Lauterbur aj,ak, Edward E. Louis, Jr. al, Meredith C. Lutz am, Jesús Martínez an,ao, Amanda D.
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Melin aa, Fabiano R. de Melo ap,aq, Tsimisento H. Mihaminekena ac,ar, Monica S. Mogilewsky as,
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Leandro S. Moreira tt,aq, Letícia A. Moura aq,at, Carina B. Muhle w, Mariana B. Nagy-Reis au,
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Marilyn A. Norconk av, Hugh Notman aa,aw, M. Teague O’Mara ax,ay,az, Julia Ostner ba,bc, Erik R.
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Patel bd, Mary S. M. Pavelka aa, Braulio Pinacho-Guendulain be,bf, Leila M. Porter yy, Gilberto
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Pozo-Montuy bg,cw, Becky E. Raboy bh, Vololonirina Rahalinarivo bi, Njaratiana A. Raharinoro n,
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Zafimahery Rakotomalala n, Gabriel Ramos-Fernández bj,bk, Delaïd C. Rasamisoa a, Jonah
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Ratsimbazafy ar, Maholy Ravaloharimanitra ac, Josia Razafindramanana bi, Tojotanjona P.
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Razanaparany bl,n, Nicoletta Righini bm, Nicola M. Robson bn, Jonas da Rosa Gonçalves bp, Justin
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Sanamo bq, Nicole Santacruz br, Hiroki Sato bs, Michelle L. Sauther bt, Clara J. Scarry bu,bv, Juan
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Carlos Serio-Silva bw, Sam Shanee bx, Poliana G. A. de Souza Lins by, Andrew C. Smith bz,
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Sandra E. Smith Aguilar ca, João Pedro Souza-Alves cb,cd, Vanessa Katherinne Stavis ce,cf, Kim J.
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E. Steffens cg, Anita I. Stone ch, Karen B. Strier ci, Scott A. Suarez cj, Maurício Talebi ck,cl, Stacey
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R. Tecot cm, M. Paula Tujague cn,co,cp, Kim Valenta cq, Sarie Van Belle cr, Natalie Vasey b,vv,
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Robert B. Wallace an,cs,ao, Gilroy Welch vv, Patricia C. Wright ct,cu, Giuseppe Donati t,2, Luca
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Santini cv,2
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a Conservation Science and Wildlife Health, San Diego Zoo Wildlife Alliance, Escondido, CA
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92027
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b Department of Anthropology, Portland State University, Portland, OR 97201
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c Department of Environmental Science, Radboud Institute for Biological and Environmental
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Sciences (RIBES), Radboud University, 6500 GL Nijmegen, The Netherlands
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d Department of Anthropology, Center for the Advanced Study of Human Paleobiology, The
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George Washington University, Washington D.C. 20037
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e Wilson Center, 1300 Pennsylvania Avenue NW, Washington, D.C. 20004
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f School of Life Sciences, University of KwaZulu-Natal, Scottsville, Pietermaritzburg, South
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Africa
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g Shaanxi Key Laboratory for Animal Conservation, Northwest University, Xi’an 710069, China
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h Department of Animal Ecology and Conservation, Institute of Zoology, Universität Hamburg,
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20146 Hamburg, Germany
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i Sedgwick County Zoo, Wichita, KS 67212
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j Department of Anthropology, The Ohio State University, Columbus, OH 43210
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k Department of Anthropology, Humboldt State University, Arcata, CA 95521
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l Asociación Neotropical Primate Conservation Perú, Moyobamba, San Martin, Perú
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m Department of Anthropology, Northwestern University, Evanston 60208
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n Mention Zoologie et Biodiversité Animale, Faculté des Sciences, Université d’Antananarivo,
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101 Antananarivo, Madagascar
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o Departamento de Ciencias Químico Biológicas, Instituto de Ciencias Biomédicas, Universidad
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Autónoma de Ciudad Juárez, Ciudad Juárez, México
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p Laboratorio de Ecología de Bosques Tropicales y Primatología, Departamento de Ciencias
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Biológicas, Universidad de Los Andes, Bogotá, 111711, Colombia
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q Department of Anthropology, Hunter College of City University of New York, NY 10065
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r Department of Anthropology, The Graduate Center of City University of New York, NY 10016
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s The New York Consortium in Evolutionary Primatology (NYCEP), New York, NY
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t Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, UK
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u Centre for Research in Evolutionary and Environmental Anthropology, Roehampton
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University, London SW15 5PJ, UK
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v Department of Zoology, Federal University of Pernambuco, Recife-PE, 50670-901, Brazil
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w Laboratório de Primatologia, Escola de Ciências da Saúde e da Vida, Pontifícia Universidade
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Católica do Rio Grande do Sul, PUCRS, Porto Alegre-RS, 90619-900, Brazil
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x Department of Engineering, Arts, Science and Technology, University of Suffolk, Ipswich IP4
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1QJ, UK
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y Suffolk Sustainability Institute, Ipswich IP4 1QJ, UK
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z Department of Biology, Rhodes College, Memphis, TN 38112
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aa Department of Anthropology & Archaeology, University of Calgary, Calgary, Alberta, T2N
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1N4, Canada
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bb Department of Anthropology, University of California, Davis, CA, 95616
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cc Departamento de Zoologia, Universidade Federal do Rio Grande do Sul, Porto Alegre-RS,
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90650-001, Brazil.
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dd Department of Anthropology, California State University Northridge, Northridge, CA 91325
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ee Department of Anthropology, University of Texas at San Antonio, San Antonio, TX 78249
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ff Coordenação de Ciências da Terra e Ecologia, Museu Paraense Emílio Goeldi, Belém-PA,
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66077-830, Brazil
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gg Proyecto Zocay, Colombia
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hh Escuela de Biología, Universidad de Costa Rica, San José, 11501-2060, Costa Rica
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ii Department of Anthropology, Yale University, New Haven, CT 06511
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jj Department of Anthropology and The Centre for Environment & Sustainability, University of
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Western Ontario, London, Ontario, N6A 3K7, Canada
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kk Department of Anthropology, Miami University, Oxford, OH 45056
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ll Department of Anthropology, Texas State University, San Marcos, TX 78666
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mm Southern Swedish Forest Research Centre, Swedish University of Agricultural Sciences
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(SLU), Alnarp, Sweden
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nn Pós-Graduação em Psicobiologia, Universidade Federal do Rio Grande do Norte, Natal-RN,
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59078-970, Brazil
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oo Behavioral Ecology and Sociobiology Unit, German Primate Center, 37077 Göttingen,
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Germany
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pp Laboratorio de Ecología de Bosques Tropicales y Primatología, Departamento de Ciencias
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Biológicas, Universidad de los Andes, Bogotá, 111711, Colombia
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qq Programa de Pós-graduação em Desenvolvimento e Meio Ambiente, Universidade Federal de
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Sergipe, São Cristóvão-SE, 49100-000, Brazil
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rr Secretaria Municipal de Meio Ambiente, Aracaju-SE, 49015-190, Brazil
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ss Laboratório de Primatologia, Departamento de Zootecnia e Ciências Biológicas, Universidade
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Federal de Santa Maria, Palmeira das Missões-RS, 98300-000, Brazil
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tt Fundação de Apoio à Pesquisa (FUNAPE), Universidade Federal de Goiás, Goiânia-GO,
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74690-612, Brazil
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uu Museu de Ciências Naturais, Universidade de Caxias do Sul, Caxias do Sul-RS, 95070-560,
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Brazil
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vv Foundation for Wildlife Conservation, Belize
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ww Departamento de Meio Ambiente e Desenvolvimento, Universidade Federal do Amapá,
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Macapá-AP, 68903-419, Brazil
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xx Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural
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Sciences, Umeå, Sweden
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yy Department of Anthropology, Northern Illinois University, DeKalb, IL 60115
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zz Department of Sociobiology and Anthropology, University of Göttingen, 37077 Göttingen,
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Germany
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ab Saint Louis Zoo, Saint Louis, MO 63110
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ac The Aspinall Foundation, 101 Antananarivo, Madagascar
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ad The Aspinall Foundation, Port Lympne Reserve, Hythe CT21-4LR, UK
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ae Durrell Institute of Conservation and Ecology, School of Anthropology and Conservation,
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University of Kent, Canterbury CT2 7NZ, UK
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af Instituto de Pesquisas Ecológicas (IPÊ), Nazaré Paulista-SP, 12960-000, Brazil
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ag Estacion Biologica Corrientes (CCT Nordeste) – CONICET, Corrientes, W3401XAL,
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Argentina
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ah Association for Research and Conservation in the Amazon (ARCAmazon), Puerto Maldonado,
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Madre de Dios, Peru
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ai Junglekeepers Peru, Puerto Maldonado, Madre de Dios, Peru
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aj Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85719
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ak Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY 11790
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al Omaha’s Henry Doorly Zoo and Aquarium, Omaha, NE 68107
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am Animal Behavior Graduate Group, University of California, Davis, CA 95616
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an Wildlife Conservation Society, La Paz, Bolivia
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ao Red Boliviana de Primatología (RedBolPrim), Bolivia
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ap Department of Forestry Engineering, Federal University of Viçosa, Viçosa-MG, 36570-900,
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Brazil
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aq Muriqui Instituto de Biodiversidade (MIB), Caratinga-MG, 35300-037, Brazil
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ar Groupe d’Etude et de Recherches sur les Primates de Madagascar (GERP), 101 Antananarivo,
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Madagascar
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as School of the Environment, Portland State University, Portland, OR 97201
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at Universidade Federal do Espírito Santo (UFES), Vitória-ES, 29075-910, Brazil
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au Biological Sciences, University of Alberta, Edmonton, Alberta, T6G 2E9, Canada
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av Department of Anthropology, Kent State University, Kent, OH 44240
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aw Centre for Social Sciences (Anthropology), Athabasca University, Athabasca, Alberta, T9S
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3A3, Canada
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ax Department of Biological Sciences, Southeastern Louisiana University, Hammond, LA 70402
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ay Department of Migration, Max Planck Institute of Animal Behavior, 78315 Radolfzell,
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Germany
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az Smithsonian Tropical Research Institute, Panamá, 0843-03092, República de Panamá
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ba Department of Behavioral Ecology, University of Goettingen, 37077 Goettingen, Germany
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bc Research Group Primate Social Evolution, German Primate Center, Leibniz Institute for
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Primate Research, 37077 Goettingen, Germany
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bd Lemur Conservation Foundation, Myakka City, FL 34251
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be Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana (UAM), Unidad
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Lerma, México
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bf Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR),
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Unidad Oaxaca, Instituto Politécnico Nacional, Oaxaca, México
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bg Conservación de la Biodiversidad del Usumacinta A.C., Balancán, Tabasco, México
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bh Department of Biology, University of Maryland, College Park, MD 20742
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bi Mention Anthropobiologie et Développement Durable, Faculté des Sciences, University of
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Antananarivo, 101 Antananarivo, Madagascar
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bj Department of Mathematical Modelling of Social Systems, Institute for Research on Applied
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Mathematics and Systems, Universidad Nacional Autónoma de México, Mexico City, México
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bk Center for Complexity Sciences, Universidad Nacional Autónoma de México, Mexico City,
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México
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bl Graduate School of Asian and African Area Studies, Kyoto University, Kyoto, 615-8510,
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Japan
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bm Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de
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Guadalajara, México
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bn Department of Life Sciences, Imperial College London, London SW7 2AZ, UK
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bp Instituto de Desenvolvimento Sustentável Mamirauá, Tefé-AM, 69553-225, Brazil
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bq Département Sciences de la Nature et de l’Environnement, Facultés des Sciences, Université
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d’Antsiranana, 201 Antsiranana, Madagascar
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br College of Veterinary Medicine, Cornell University, Ithaca, NY 14853
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bs Primate Research Institute, Kyoto University, Aichi 484-8506, Japan
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bt Department of Anthropology, University of Colorado-Boulder, Boulder, CO 80302
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bu Department of Anthropology, California State University, Sacramento, Sacramento, CA 95819
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bv Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University,
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Stony Brook, NY, 11794
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bw Red de Biología y Conservación de Vertebrados, Instituto de Ecología AC, Xalapa, Veracruz,
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México
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bx Neotropical Primate Conservation, Seaton, Cornwall PL11 3JQ, UK
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by Pós-Graduação em Ecologia e Conservação da Biodiversidade, Universidade Federal do Mato
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Grosso, Cuiabá-MT, 78060-900, Brazil
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bz School of Life Sciences, Anglia Ruskin University, Cambridge CB1 1PT, UK
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ca Instituto de Investigaciones Sociológicas de la Universidad Autónoma Benito Juárez de
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Oaxaca, Oaxaca, México
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cb Departamento de Zoologia, Universidade Federal de Pernambuco, Recife-PE, 50670-901,
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Brazil
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cd Laboratório de Ecologia, Comportamento e Conservação (LECC), Universidade Federal de
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Pernambuco, Recife-PE, 50670-901, Brazil
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ce Laboratório de Produtos Naturais e Espectrometria de Massas (LaPNEM), Faculdade de
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Ciências Farmacêuticas, Alimentos e Nutrição (FACFAN), Universidade Federal de Mato
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Grosso do Sul (UFMS), Campo Grande-MS, 79070-900, Brazil
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cf Universidade Federal de Mato Grosso do Sul (UFMS), Campo Grande-MS, 79070-900, Brazil
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cg Department of Biology, Institute of Zoology, Universität Hamburg, 20146 Hamburg, Germany
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ch Biology Department, California Lutheran University, Thousand Oaks, CA 91360
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ci Department of Anthropology, University of Wisconsin-Madison, 1180 Observatory Drive,
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Madison, WI 53706
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cj Department of Behavioral Sciences, San Diego Mesa College, San Diego, CA 92111
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ck Departamento de Cíências Ambientais, Lab Ecologia e Conservação da Natureza and the
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Programa Análise Ambiental Integrada, Universidade Federal de São Paulo, São Paulo-
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SP, 04040-003, Brazil
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cl Instituto Pró-Muriqui, São Paulo-SP, Brazil
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cm School of Anthropology, University of Arizona, Tucson, AZ 85719
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cn Facultad de Ciencias Forestales (FCF), Universidad Nacional de Misiones (UNaM), Eldorado,
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Misiones, Argentina
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co Instituto de Biología Subtropical (IBS), Consejo Nacional de Investigaciones Científicas y
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Técnicas (CONICET), Puerto Iguazú, Misiones, Argentina
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cp Asociación Civil Centro de Investigaciones del Bosque Atlántico (CeIBA), Puerto Iguazú
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(3370), Misiones, Argentina
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cq Department of Anthropology, University of Florida, Gainesville, FL 32603
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cr Department of Anthropology, University of Austin at Texas, Austin, TX 78712
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cs Wildlife Conservation Society, Bronx, NY 10460
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ct Department of Anthropology, Stony Brook University, Stony Brook, NY 11794
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cu Centre ValBio, Ranomafana, Madagascar
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cv Department of Biology and Biotechnology “Charles Darwin”, Sapienza University of Rome,
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00185 Rome, Italy
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cw Facultad Maya de Estudios Agropecuarios, Universidad Autónoma de Chiapas, Catazajá,
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Chiapas, México
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1 To whom correspondence may be addressed. Email: teppley@sdzwa.org
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2 Contributed equally to this work
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Author Contributions: T.M.E., K.H., A.A.B., P.C.W., G.D., and L.S. designed research. T.M.E.,
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C.A.C., J.U.G., M.A.O., D.B.A., N.A., K.R.A., M.A.A., J.F.A., A.L.B., M.B., J.C.B.M., M.B.,
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S.A.B., M.B., D.C., C.C.M., C.J.C., M.C., F.A.C., T.S.C., X.C.P., J.C., O.M.C., C.C.K., I.C.C.,
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B.D., C.D., K.M.E., E.M.E., K.J.E.E., L.M.F., A.M.F., R.G.F., C.F., M.L.F., I.P.F., V.B.F., I.F.,
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D.G., G.B.G., K.S.H., E.W.H., R.R.H., S.M.H., M.T.I., S.E.J., P.M.K., E.A.K., T.K., C.K., F.K.,
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M.M.K., L.R.L., M.E.L., E.E.L., M.C.L., J.M., A.D.M., F.R.M., T.H.M., M.S.M., L.S.M.,
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L.A.M., C.B.M., M.B.N.R., M.A.N., H.N., M.T.O., J.O., E.R.P., M.S.M.P., B.P.G., L.M.P.,
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G.P.M., B.E.R., V.R., N.A.R., Z.R., G.R.F., D.C.R., J.R., M.R., J.R., T.P.R., N.R., N.M.R.,
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J.R.G., J.S., N.S., H.S., M.L.S., C.J.S., J.C.S.S., S.S., P.G.A.S.L., A.C.S., S.E.S.A., J.P.S.A.,
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V.K.S., K.J.E.S., A.I.S., K.B.S., S.A.S., M.T., S.R.T., M.P.T., K.V., S.V.B., N.V., R.B.W.,
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G.W., P.C.W., and G.D. contributed datasets. T.M.E., S.H., G.D., and L.S. analyzed data.
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T.M.E., S.H., G.D., and L.S. wrote the paper. All authors read and edited this manuscript.
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Competing Interest Statement: The authors declare no competing interest.
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Classification: Biological Sciences: Anthropology
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Keywords: primate communities; primate evolution; evolutionary transitions; niche shift;
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climate change
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This PDF file includes:
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Main Text
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Figures 1 and 2
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Table 1
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Abstract
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Among mammals, the order Primates is exceptional in having a high taxonomic richness where
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the taxa are arboreal, semi-terrestrial, or terrestrial. Though habitual terrestriality is pervasive
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among the apes and African and Asian monkeys (catarrhines), it is largely absent among
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monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines),
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which are mostly arboreal. Numerous ecological drivers and species-specific factors are
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suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and
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current environmental conditions may provide analogous scenarios to those transitional periods.
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Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas
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and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat
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canopy cover, predation risk, maximum temperature, precipitation, primate species richness,
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human population density, and distance to roads) or species-specific traits (body mass, group
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size, and degree of frugivory) associate with increased terrestriality. We collated 150,961
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observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in
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the Americas. Multiple factors were associated with ground use in these otherwise arboreal
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species, including increased temperatures, a decrease in canopy cover, a dietary shift away from
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frugivory, and larger group size. These factors mostly explain intra-specific differences in
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terrestriality. As humanity modifies habitats and causes climate change, our results suggest that
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species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are
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more likely to shift towards greater ground use.
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Significance Statement
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Primates from the Americas and Madagascar are predominantly arboreal but occasionally
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descend to the ground. This increased ground use was associated with multiple ecological
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drivers, including increased temperatures and a decrease in canopy cover, as well as species-
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specific traits, including a dietary shift away from fruits and larger group size. As anthropogenic
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impacts to habitats and climate worsen, our results suggest that diurnal species already inhabiting
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hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift
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towards greater ground use.
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Main Text
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Introduction
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Eutherian mammal radiations are characterized by multiple evolutionary transitions
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between terrestrial, arboreal, fossorial, and aquatic lifestyles (1, 2). In primates, arboreality is
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hypothesized to be the ancestral condition (2-5). The evolutionary shift in some primate lineages
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to terrestrial niches is associated with various morphological/skeletal adaptations (6-10).
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Terrestriality is the prevalent strategy among some lineages of Catarrhini primates (i.e., African
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and Asian monkeys and great apes; 9, 11). Conversely, adaptations for predominantly terrestrial
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lifestyles are notably absent among living Platyrrhini of the Americas and Strepsirrhini of Africa
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(including Madagascar) and Asia (7, 12-14). However, some of these arboreal, diurnal primates
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periodically use the ground (15-21).
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The evolutionary transition from arboreality to terrestriality is complex and carries
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debated costs and benefits (22, 23), of which three main areas are discussed. First, descending to
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the ground may come at the cost of greater predation risk (24, 25). Yet, it is unclear whether
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arboreal or terrestrial lifestyles are characterized by greater predation risks (22, 23, 26-28).
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Regardless, ground use by arboreal primates exposes them to novel predators and predation
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patterns. Recent natural and anthropogenically driven ecological changes, however, negatively
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impact native carnivore occupancy (29, 30), and may reduce terrestrial predation risk and, thus,
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facilitating ground use in primates (17, 20, 31-33). It should be noted, however, that native
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carnivores are often supplanted by non-native carnivores, including dogs, which can have a
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negative impact on primate populations (29, 34, 35). Second, species occurring in naturally open
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canopy habitats have been shown to use the ground frequently (36). To such a degree,
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environmental changes and increasing anthropogenic encroachment on tropical forests may act
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as catalysts for species to adopt terrestrial habits as canopy cover becomes patchy and forest
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fragments provide fewer or lower quality resources. As a result, species may descend to the
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ground to cross open areas more frequently to fulfil their energetic requirements, access
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reproductive opportunities, or to disperse (17, 32, 37, 38). Therefore, plasticity in use of
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additional ecological niches (e.g., terrestrial stratum) may enhance resilience to disturbance and
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persistence in some fragmented landscapes (39, 40, 41). Third, extreme temperatures limit
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species’ biological functions (42, 43). As the understory and terrestrial environments are cooler
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than the upper canopy (43, 44), intense seasonal heat in previously dense tropical forest
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environments may drive arboreal species to seek thermoregulatory relief on the ground (45, 46).
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Arboreal primates during hot periods regularly descend to the ground to access terrestrial water
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sources for drinking or immersive cooling (18, 38, 47-51), and this behavior may become
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increasingly common given the cascading impacts of climate change (e.g., extreme heatwaves
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and droughts; 52, 53).
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Primate community structure may also play an important role leading to terrestriality.
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Typically, sympatric species maintain separate niches to reduce ecological competition (54, 55).
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Therefore, in sites with high primate species richness (i.e., number of species) and greater
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potential for interspecific competition, species that can expand into terrestrial niches may
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experience reduced competition. As sympatric competitors, including other primate species, are
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potentially crowded into smaller ranges due to habitat losses, interspecific competition may
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increase until a new state is reached (56).
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Species-specific factors have also been suggested to facilitate niche transition. Limited
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resource availability in the canopy may lead to shifts in foraging strategies (57), including
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increased terrestriality (11, 16, 38). For instance, arboreal species reliant on seasonal resources
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may be more inclined to expand their dietary niche to include ground-based resources during
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periods of food scarcity (33). Furthermore, fully or semi-terrestrial primates tend to be larger
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than strictly arboreal primates and tend to live in larger groups (22, 58, 59). Both characteristics
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are likely adaptations to high predation pressure and resource availability (59-63) and may have
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facilitated the shift to terrestriality. Additionally, quadrupedal locomotion along the forest
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canopy, which mainly includes largely horizontal substrates, may have selected for hind- and
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forelimbs of similar length (7). This is in contrast to species using vertical clinging and leaping
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locomotion from vertical substrates, which is associated with much longer hindlimbs (7). Species
326
in the former category are predicted from a biomechanical perspective to have more effective
327
cursorial quadrupedalism in a terrestrial environment (8, 64). Such species-specific factors may
328
have facilitated the evolutionary transition of some primates to terrestrial lifestyles (9, 11, 65).
329
13
We focus on diurnal primates of the Americas and Madagascar to explore anthropogenic
330
and ecological factors, and species-specific traits that are associated with greater use of the
331
ground in two independent radiations. We did not include monkeys and apes from Africa and
332
Asia as many of these species regularly exhibit semi-terrestrial and/or terrestrial lifestyles (9,
333
11), and thus they experienced their niche transition presumably millions of years ago.
334
Specifically, we are not interested in testing adaptations to terrestriality, but rather in the
335
ecological, anatomical, and behavioral traits that make terrestriality a possible option for an
336
arboreal primate. Regarding ecological and anthropogenic factors, we predict that terrestriality
337
will be greater in species at sites 1) where fewer native terrestrial predators pose a risk; 2) with
338
more open, degraded, or fragmented forest areas, (i.e., less canopy cover); 3) with higher
339
maximum temperatures favoring behavioral thermoregulation; 4) with high primate species
340
richness, and 5) in greater distance from both roads and areas of higher human population
341
densities (Fig. 1). Considering species-specific traits that may promote ground use, we predict
342
that terrestriality will be greater in species 1) that rely less on a diet of fruit as folivores tend to
343
have gut adaptations more suitable for terrestrial resources; 2) with larger bodies; 3) that form
344
larger groups; and 4) that exhibit anatomical adaptations for arboreal quadrupedalism (Fig. 1).
345
346
Results
347
The 47 arboreal diurnal primate species we studied spent little time on the ground (2.5 ±
348
0.1% of the activity budget, monthly mean ± SE; N = 2,227 months), and for over half of the
349
species (61.7%) terrestrial behavior comprised less than 1% of their total monthly activity.
350
Lemurs spent 4.8 ± 0.3% (monthly mean ± SE; N = 1,002 months) of their time on the ground,
351
whereas platyrrhine monkeys spent 2.4 ± 0.2% (monthly mean ± SE; N = 1,225 months) of their
352
14
time on the ground. Lemurs were on average more terrestrial than platyrrhine monkeys (Table 1;
353
SI Appendix, Table S2).
354
In the complete model, which accounts for both intra- and interspecific variability, the
355
most important ecological pressure positively associated with terrestriality was maximum
356
temperature, while habitat canopy cover was negatively associated with time spent on the ground
357
(SI Appendix, Table S2 and Fig. S8). Considering anthropogenic factors, distance to roads was
358
positively associated with ground use (SI Appendix, Table S2 and Fig. S8). For species-specific
359
factors, a species’ degree of frugivory was negatively associated with terrestriality, whereas
360
larger group size was positively associated with terrestriality (SI Appendix, Table S2 and Fig.
361
S8). Furthermore, post-habituation time was negatively associated with ground use, meaning that
362
species studied across a greater number of months were less likely to exhibit terrestriality (SI
363
Appendix, Table S2 and Fig. S8).
364
For the within-species model, which evaluates the variability among conspecific
365
populations (Table 1; SI Appendix, Fig. S9), multiple ecological pressures influenced primate
366
ground use. Similar to the complete model, maximum temperature and distance to roads were
367
positively associated with terrestriality, while habitat canopy cover was negatively associated
368
with terrestriality. Unlike the complete model, however, terrestriality decreased with increasing
369
terrestrial predation risk, and increased with primate species richness. We also found a positive
370
interaction between primate-rich habitats and habitat canopy cover, indicating an amplified effect
371
of canopy cover on terrestriality in areas with higher primate species richness. Like the complete
372
model, the three species-specific factors related to terrestriality were degree of frugivory
373
(negative), group size (positive), and post-habituation (negative).
374
15
In the between-species model, which measures variability across species (Table 1; SI
375
Appendix, Fig. S10), none of the factors were strongly related to terrestriality. The only
376
ecological factor that exhibited a clear association was primate species richness (negative).
377
Species in habitats with denser canopy cover and with fewer sympatric primate species spent a
378
greater proportion of time on the ground. Terrestriality was positively related with body mass
379
and negatively with group size, indicating smaller species and larger groups, respectively,
380
spending more time on the ground.
381
382
Discussion
383
We found more terrestrial activity in hotter environments with more mammalian
384
predators, larger groups, and taxa with less frugivorous diets. However, the degree of
385
terrestriality varies both within and between species, and when this variation is analyzed
386
separately it reveals a more complex picture. Our within-species comparison shows that groups
387
living in more open habitats with more potential predators and richer primate communities
388
exhibit greater degrees of terrestriality. Species at more remote sites, i.e., greater distances from
389
roads, also spent more time on the ground. By comparison, our between-species analysis reveals
390
that species that descend more often to the ground tend to be smaller and live in larger groups.
391
Contrary to previous single-species studies that showed an observer effect (15, 39, 66, but see
392
33), shorter study duration (the number of post-habituation months) was strongly associated with
393
ground use.
394
395
Ecological correlates to terrestriality
396
16
Maximum temperatures showed a positive relationship with the time spent on the ground
397
on both the complete and intraspecific models, while our proxy for seasonality (i.e., monthly
398
precipitation) was not influential within any of the models. Gradual and rapid temperature
399
increases correlates with behavioral shifts (cf. 67, 68). A possible explanation is that lemurs and
400
platyrrhine monkeys increase their use of the ground as an adaptive thermoregulation strategy
401
(69, 70). For example, we found that primate species like Eulemur fulvus and E. rufifrons spent
402
considerably more time on the ground in relatively hotter tropical deciduous forest habitats of
403
Madagascar compared to their conspecifics inhabiting the cooler humid forest habitats, likely to
404
access terrestrial water sources (50). This finding supports the idea that shifting between
405
arboreality and terrestriality is an effective thermoregulatory response, with important
406
implications considering current global warming trends (52, 71, 72).
407
Canopy cover has long been considered a factor in many evolutionary shifts (73).
408
However, the degree to which this may result in a more terrestrial primate lifestyle is unclear
409
(11). Denser canopy cover was associated with spending less active time on the ground within-
410
species, but was not associated with ground use in the between-species model. The former is in
411
line with our expectation that terrestrial activity tends to be higher in habitats with sparser
412
canopies, such as those disturbed by anthropogenic activities (19, 38). Arboreal species in more
413
open habitats (i.e., sparser canopies) may need to descend to the ground to forage and drink (19,
414
34, 38, 74, 75), though their ability to do so may be guided by species-specific characteristics
415
acting as a predisposition, i.e., behavioral and anatomical exaptations (76, 77).
416
Primate species richness had contrasting results, with a negative effect on terrestriality in
417
the interspecific model and positive effect in the intraspecific model. As all primates within the
418
communities examined are arboreal, greater numbers of species at a site may lead to higher
419
17
competition for canopy resources, including both food and space. Under specific circumstances,
420
descending to a rarely exploited niche (the forest floor) may be critical for coping with periods of
421
limited resources (78). The positive interaction effect between canopy cover and primate species
422
richness in the intraspecific model supports our hypothesis. Essentially, the negative effect of
423
canopy cover on terrestriality was weaker as sympatric taxa richness increased. In other words,
424
when canopy cover increases, the decrease in terrestriality is less pronounced in habitats with
425
high primate diversity where we would expect higher competition. However, it is possible that at
426
sites where a species may have recently become locally extirpated, this loss may result in
427
competitive release, allowing one or more of the remaining species to partially, or fully, exploit
428
newly available resources (79-81). Compared to many mammal taxa, primates tend to exhibit a
429
high degree of behavioral flexibility (82-83), and interindividual variation may be the
430
mechanism underlying niche expansion (84).
431
Predation pressure is difficult to quantify and evaluate. The number of potential predator
432
species provides a proxy with which to measure this risk (85, 86), and some site-/species-focused
433
studies have noted that relaxation of predation pressure led to more ground-based activity (20,
434
32, 39). Interestingly, terrestrial predator species richness was associated with more terrestrial
435
activity in our within-species model. Though we were unable to account for predator population
436
abundance or the potential ecological and co-occurrence factors affecting these taxa (87), it
437
appears that anthropogenic factors may play a role. Human population density and distance to
438
roads may be considered as general proxies for various aspects of human encroachment,
439
including feral dogs (Canis familiaris) which are known to prey upon wildlife (34, 35, 74). Of
440
the two anthropogenic factors, conspecifics were more terrestrial at sites further away from
441
roads.
442
18
443
Species-specific factors as potential facilitators of terrestriality
444
Frugivory was associated with decreased ground use in both the complete and
445
intraspecific models, supporting previous assertions that diet is a driving force of terrestriality
446
(38, 88). This link may be associated with folivores or species with a broad dietary spectrum
447
using the ground more often to forage on different preferred foods (17, 89), and/or because they
448
have gastrointestinal and dental adaptations allowing them to more efficiently use terrestrial
449
resources (90). Despite the general reduced ground use by frugivores, periods of reduced fruit
450
availability may lead facultative frugivores to search the ground for novel food resources to meet
451
their seasonal nutritional needs (21, 91, 92). Many primates with broad dietary niches come to
452
the ground to engage in geophagy and to access mineral licks (93, 94) and potentially fermented
453
foods (95). However, given the supplementary nature of this feeding habit (96) that often
454
involves short terrestrial travel, it has not been considered a key causative factor in any major
455
shift in strata use. Primates may also descend to the ground to forage for arthropod prey (19, 21).
456
Group size had an effect in both the complete and within-species models. Large groups
457
can facilitate terrestriality as they can potentially reduce predation risk. Folivores are in principle
458
less constrained by group size compared to frugivores due to the less clumped spatiotemporal
459
availability of preferred resources, though this is not always the case (97, 98). However, though
460
it is conceivable that large groups foster terrestrial activity, it is also possible that groups that use
461
the ground more often tend to form larger groups to reduce predation risk, leaving the causal
462
relationship unclear. In both Brachyteles hypoxanthus in Caratinga (Brazil) and Hapalemur
463
meridionalis in Mandena (Madagascar), it was the case that the largest group was considerably
464
more terrestrial than smaller groups (17, 39).
465
19
Biomechanical, e.g., size-related and anatomical, challenges may impose various
466
biological, ecological, and physiological constraints within both the arboreal and terrestrial strata
467
(8). Such morphological factors could be species-specific consequences that evolve after, or in
468
parallel with, the initial niche expansion into terrestrial activity. However, contrary to our
469
hypothesis, we found a negative effect of body mass between species (i.e., smaller species
470
showed increased terrestriality). Original hypotheses about the relationship between body size
471
and terrestriality proposed by Fleagle (7, 59) were developed to explain the range of niche use in
472
the entire Primate Order, including the larger-bodied catarrhines. The primates included in this
473
study, platyrrhines and lemuriformes, represent a more restricted range of body mass variation,
474
and therefore it is possible that a different relationship between terrestriality and body mass is
475
present for the entire Order. We cannot evaluate the role that the relatively recent extinction of
476
the larger and more terrestrial lemur species (99) may have had in releasing the competition for
477
terrestrial resources with the extant smaller lemur species.
478
Though post-habituation months was used to control for a possible positive observer
479
effect, our complete and within-species model showed that primates studied for shorter periods
480
more strongly associated with ground use. While this contrasts from some single-species studies
481
(15, 39, 66), we believe our negative effect is more likely the result of the non-random
482
distribution of study periods with respect to seasons and/or the non-random distribution of
483
species with respect to their average level of arboreality within our dataset.
484
485
Conclusion
486
We have shown that there are multiple factors that may lead arboreal primates to use the
487
ground and that this transition is influenced by site-specific ecological pressures. Specifically,
488
20
habitats with sparser canopies may be responsible for the evolutionary transition of non-human
489
primates to terrestrial lifestyles (11, 19), whereas the more proximate causes of strata shift appear
490
to be hotter environmental conditions (72) and dietary shifts away from frugivory. Considering
491
species-specific traits, larger groups and smaller body mass facilitated ground use.
492
Although significant climate changes in both the Americas (100) and Madagascar (101) likely
493
facilitated faunal turnover and speciation, it is not clear why terrestriality did not evolve there to
494
the same extent as it is seen in catarrhines. Fossil records are sparse and the real extent of niche
495
diversification that occurred in lemurs and platyrrhines over their evolutionary history is far from
496
being understood (7). Examining primate behavioral and ecological flexibility alongside current
497
environmental conditions, however, provides insight into evolutionary transitional periods that
498
resulted in shifts to novel ecological niches. As human activity drives climate change, degrades
499
primate habitats, and shifts plant phenological patterns, primate populations are facing
500
unprecedented challenges that threaten their persistence (52, 71, 102-105). We expect that an
501
increased use of the ground strata by species inhabiting hot, sparsely canopied sites and that
502
exhibit a more generalized diet, can buffer species against extinction. Productive future lines of
503
research that will further clarify factors driving the evolution of terrestriality include comparing
504
behavioral repertoires in terrestrial versus arboreal environments, evaluating potential ecological
505
and life history drivers of annual variation in terrestrial behaviors, and if habitat structure
506
explains variation in population-level terrestriality. All non-human primates, however, will be
507
faced with challenges created by anthropogenic changes and for species less inclined to
508
terrestrial activity, fast and effective conservation strategies will need to be implemented to
509
ensure their survival.
510
511
21
Materials and Methods
512
Co-authors contributed raw monthly behavioral ecology data from 47 primate taxa,
513
specifically 15 lemur species representing two families (Lemuridae and Indriidae), and 32
514
platyrrhine species representing four families (Atelidae, Callitrichidae, Cebidae, and Pitheciidae)
515
(Dataset S1). This collated dataset includes 150,961 observation hours across 2,227 months from
516
species at 68 research sites, specifically 20 sites in Madagascar and 48 sites throughout the
517
Americas (Fig. 2; SI Appendix, Table S1). Our dataset includes 16 primate species (specifically
518
10 lemur and six platyrrhine monkey species) for which we have data from multiple sites.
519
For each species, we provide monthly proportional data to account for different data
520
collection methods used in each study. Since nocturnal species are exposed to different
521
ecological pressures compared to diurnal primates, we only focused on diurnal primates.
522
Datasets included had a minimum of 12 hours/month to increase the chances that rare events, in
523
our case terrestriality by arboreal species, would be recorded (106). We considered the monthly
524
proportion of time spent terrestrially as our dependent variable.
525
526
Ecological drivers
527
We extracted site- and time-specific climate and habitat values in Google Earth Engine
528
(earthengine.google.com) using the spatial coordinates and the year and month of the
529
observations (107). We extracted monthly maximum temperatures and monthly total
530
precipitation from the ERA5 Monthly Aggregates dataset (108). The latter is used as a
531
conservative proxy for seasonality (109), incorporating the rainfall variation at research sites for
532
the months included in our dataset. We obtained the relative canopy cover using a circular buffer
533
around the coordinates of each study site from the Landsat Tree Cover Continuous Fields
534
22
(GLCF) dataset (110; SI Appendix, Fig. S1). Specifically, the buffer area was equal to twice the
535
size of each study species reported mean home range area.
536
We estimated the number of potential terrestrial mammalian predators per species per site
537
from the number of carnivore species per location using IUCN range maps (111). For each
538
species per location, we only considered predators with a mean body mass greater than or equal
539
to ¼ of the mean body mass of the focal primate. This ratio was based on the minimum predator-
540
prey ratio observed in terrestrial mammals (Appendix S1 in 112). The body mass threshold is
541
very conservative and may lead to the inclusion of species that do not typically prey on adult
542
primates; however, considering primates’ slow life histories and the additive risks to
543
juveniles/infants, smaller predators can potentially trigger a fear reaction (113, 114). This
544
approach is also limited by the nature of IUCN range maps and the consideration of predator-
545
prey body mass ratios, which likely overestimates the presence of predators as large predators
546
may have been extirpated by local hunting and habitat loss. However, this approach allows us to
547
estimate the spatial gradients of predator species richness at this scale of analysis for all sites and
548
species, thereby avoiding potential author or publication reporting biases (cf. 115). Although
549
primates may also be preyed upon by birds of prey, snakes, and other primates, carnivores are
550
considered their main terrestrial predators (116, 117).
551
Using IUCN range maps (111), we also estimated the number of sympatric primate
552
species per site, i.e., species richness (SI Appendix, Figs. S2 and S3). Given the potential
553
increased effect of interspecific competition in sites with less canopy cover (potentially more
554
fragmented), we examined the interaction between these two factors.
555
Finally, we considered two proxies of anthropogenic disturbance: human population
556
density and distance to roads. The former accounts for the number presence of humans, whereas
557
23
the latter is a proxy of inverse of remoteness (i.e., inverse of accessibility to humans). We
558
obtained the human population density data from the Socioeconomic Data and Applications
559
Center (http://sedac.ciesin.columbia.edu/). We used the Gridded Population of the World (GPW)
560
dataset, v.4 dataset (118) for 2000, 2005, 2010, 2015, and 2020 at 30 arc-second resolution
561
(~1km) (SI Appendix, Figs. S4 and S5). We matched the terrestriality data with the values of
562
human population density using the closest layer in time. Road data for the countries of interest
563
were extracted from the OpenStreetMap database (openstreetmap.org). From the vector files we
564
only retained primary, secondary, and tertiary roads, motorways, trunks, all related "links", and
565
residential roads. Instead, we excluded all unclassified roads, paths, footways, and similar. We
566
then rasterized the vector layer at 1km resolution and calculated the distance from the nearest
567
road for the entire study area (SI Appendix, Figs. S6 and S7). All raster data processing was
568
conducted in R version 3.6.3 (119) using ‘raster’ package (120).
569
570
Species-specific factors
571
For each species’ specific site, co-author(s) contributed the monthly proportion of time
572
spent feeding on fruit, the mean body mass and the mean group size measured in the field. In the
573
absence of mean body mass, we used data from the ‘All the World's Primates’ database (121).
574
We inferred locomotion type via the Inter-Membral Index (IMI; 64), which is calculated as
575
((length of humerus + length of radius) / (length of femur + length of tibia)) * 100. Quadrupedal
576
primates typically have an IMI between 67 and 104; of the arboreal quadrupeds, those falling
577
below the lower threshold typically exhibit vertical clinging and leaping (VCL), and those above
578
the upper threshold are typically categorized as exhibiting brachiation, but also suspensory
579
locomotion (7, 8, 64). Given potential for error when collecting field measurements, and the
580
24
relative stability of the IMI within genera, we assigned each species to a category based on the
581
IMI averaged at the genus level.
582
583
Statistical analyses
584
We tested our hypotheses by fitting a zero-inflated model with a beta family and logit
585
link-function and using Bayesian inference. The use of a zero-inflation and beta family allowed
586
accommodating for the highly skewed and zero-inflated distribution of terrestriality values
587
bounded between 0 and 1. We added a group level to study site and one to species to control for
588
multiple estimates in the same locations and multiple estimates per species, respectively.
589
Considering climatic variation and its effect on resource phenology (122), we controlled for
590
seasonality using monthly temperature and total precipitation at each site. We used study
591
duration (i.e., the number of months post-habituation) to control for observer effect within the
592
models. We controlled for phylogenetic effects by using a variance-covariance matrix derived
593
from the phylogeny in Upham et al. (123). An additional observation level random effect was
594
added to control for overdispersion. All fixed factors were scaled to a mean of zero and standard
595
deviation of 1 to ensure comparability of the effect sizes, as well as improving numerical
596
stability in their estimation. We used weakly informative priors using a normal distribution with
597
a standard deviation of 10 for the intercept, and a standard deviation of 1.5 for all slope
598
coefficients, thereby limiting the range to a plausible gradient of variation considering the logit
599
link-function and scaled coefficients (124). All predictors were tested for multi-collinearity prior
600
to the modelling but none showed a correlation coefficient >0.7, so all variables were retained in
601
the final model (125).
602
25
The complete model accounted for both intra- and interspecific variability in
603
terrestriality, thus, we ran two additional models to disentangle the variability within- and
604
between-species. To assess whether the detected effects could also explain the different degrees
605
of terrestriality among conspecific populations (within-species model), we included only
606
anthropogenic and ecological drivers, as well as site-specific species’ factors for which we had
607
data (% frugivory and group size). Prior to fitting this second model, we first subtracted the
608
species’ mean from each observation value (species mean deviation) (126). Then, we fitted a
609
model including both ecological drivers and species-specific traits to estimate the variability
610
across species (between-species model), from which we subtracted the species mean deviation
611
from each observation value. For both the within- and between-species model, we rescaled the
612
variable to a mean of zero and standard deviation of 1 prior to model fitting and used the same
613
weakly informative priors used for the complete model.
614
We ran 6,000 iterations over 10 Markov Chain Monte Carlo chains for each model, with
615
a ‘burn in’ period of 2,000 iterations per chain leading to a total of 40,000 usable posteriors. We
616
also checked models for chain convergence and parameter identifiability. We summarized the
617
posterior distributions of coefficient estimates using 95% credible intervals. We considered
618
credible intervals that did not overlap with zero as strong evidence of directionality. We also
619
reported the probability of direction, a threshold-independent measure of evidence that varies
620
from 50% to 100% and that indicates the probability of a coefficient being different from zero
621
(127). We fitted the models in R version 3.6.3 (119) using the ‘brms’ package (128), for model
622
fitting, ‘bayestestR’ (127) for Bayesian summary statistics, and ‘ape’ (129) and ‘phytools’ (130)
623
for handling the phylogenetic data. All statistical codes used in the analyses are available via
624
Figshare (https://doi.org/10.6084/m9.figshare.19344992.v1).
625
26
626
Acknowledgments
627
TME was supported by funding from the American Society of Primatologists, Conservation
628
International’s Primate Action Fund, IDEAWILD, Margot Marsh Biodiversity Fund, Mohamed
629
bin Zayed Species Conservation Fund (Project Number: 11253008), Primate Conservation Inc.,
630
and the Primate Society of Great Britain/Knowsley Safari Park. DBA was supported by the
631
National Science Foundation DDIG (BCS 1341174), Animal Behavior Society, Society for
632
Integrative and Comparative Biology, the Tinker Foundation, and the Mansfield and Columbus
633
campuses at Ohio State University. NA was supported by Neotropical Primate Conservation
634
through various grants. KRA is supported as a fellow in CIFAR’s ‘Humans and the microbiome’
635
program. JCBM was supported by funding by the World Wildlife Fund-U.S. (# 6573), Brazilian
636
National Council for Scientific and Technological Development/CNPq (PQ 1C #304475/2018-
637
1), Programa Nacional de Pós-Doutorado of the Coordenação de Aperfeiçoamento de Pessoal de
638
Nível Superior – Brazil (Brazilian Higher Education Authority)/CAPES (Finance Code 001;
639
PNPD grant # 2755/2010). SAB received financial support from the Biological Dynamics of
640
Forest Fragments Project (BDFFP), Smithsonian Tropical Research Institute, Arizona State
641
University, Fulbright/Institute of International Education, Margot Marsh Biodiversity
642
Foundation, Providing Educational Opportunities (PEO), Primate Conservation, Inc.,
643
Organization for Tropical Studies, and American Society of Primatologists. TSC was supported
644
by a scholarship from FUNAPE (Fundação de Amparo à Pesquisa) and would like to thank the
645
Mineração Rio do Norte (MRN) for their support. OMC was supported by Programa Nacional de
646
Pós-Doutorado of the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil
647
(Brazilian Higher Education Authority)/CAPES (Finance Code 001; PNPD grant # 2755/2010).
648
27
CCK received financial support from The National Science Foundation (NSF-BSC-1745371),
649
Yale University MacMillan Center for International Studies, National Geographic Society (EC-
650
420R-18), The Explorers Club, Yale Institute for Biospheric Studies, Yale University
651
Department of Anthropology, The International Primatological Society, and Primate
652
Conservation Inc. Madagascar Ministry of the Environment and Madagascar National Parks
653
permitted this research. ICC received research support from the National Science Foundation
654
(Dissertation Improvement Award Grant No. BNS-9101520), the National Geographic Society
655
(Grant No. 4496-91), the Boise Fund of the University of Oxford, a Grant-in-Aid of Research
656
from Sigma Xi - The Scientific Research Society, a Washington University Graduate Fellowship,
657
the St. Louis Rainforest Alliance, and the St. Louis Zoo. LMF was supported by NSERCC
658
(Natural Sciences & Engineering Research Council of Canada, & CRC (Canada Research Chairs
659
Programme. AMF was funded by the Wildlife Conservation Society, Conservation International,
660
the Rufford Foundation and Primate Society of Great Britain. RGF was supported by the
661
Fundação Grupo Boticario (0973-2013-8) and CNPQ. IF was supported by a scholarship from
662
FUNAPE (Fundação de Amparo à Pesquisa) and would like to thank the Mineração Rio do
663
Norte (MRN) for their support. KSH was supported by the Foundation for Wildlife
664
Conservation, the Zoological Society of Milwaukee, Birds Without Borders/Aves Sin Fronteras,
665
the University of Calgary, Athabasca University, and the Natural Sciences and Engineering
666
Research Council of Canada. EWH was supported by Deutsche Forschungsgemeinschaft (DFG),
667
Deutscher Akademischer Austauschdienst (DAAD), Universitätsbund Göttingen. SMH was
668
supported by the Natural Sciences and Engineering Research Council of Canada, the
669
Philanthropic Educational Organization, Conservation International, and Primate Conservation,
670
Inc. SEJ was supported by the Natural Sciences and Engineering Research Council of Canada,
671
28
Conservation International, and Primate Conservation, Inc. MCL received funding from the
672
National Science Foundation Graduate Research Fellowship (Award Number 1650042),
673
University of California - Davis, Bucknell University, Greenville Zoo Conservation Grant,
674
Pittsburgh Zoo Conservation and Sustainability Fund, Primate Conservation Inc., International
675
Primatological Society Research Grant, and IDEAWild. FRM was support by a scholarship from
676
FUNAPE (Fundação de Amparo à Pesquisa) and would like to thank the Mineração Rio do
677
Norte (MRN) for their support. THM was funded primarily by The Aspinall Foundation through
678
the "Saving Prolemur simus" project, with additional support from Beauval Nature and IUCN-
679
SOS "Save Our Species". LSM was support by a scholarship from FUNAPE (Fundação de
680
Amparo à Pesquisa) and would like to thank the Mineração Rio do Norte (MRN) for their
681
support. MTO was supported in part by the National Science Foundation DDIG (BCS 0851761),
682
the J. William Fulbright Foundation, Sigma Xi, and the School of Human Evolution and Social
683
Change at Arizona State University. BPG was supported by grants from CONABIO (HK009)
684
and CONACYT (J51278), as well as graduate scholarships from CONACYT (2008-2010 and
685
2018-2021). GPM was supported by a doctorate and master’s degree scholarship from
686
CONACYT (2007-2010) and by the Academic Division of Biological Sciences of the
687
Universidad Juárez Autónoma de Tabasco. I also thank the local people from Balancán for their
688
guidance. BER was supported by funding provided by the Durrell Wildlife Conservation Trust,
689
the Lion Tamarins of Brazil Fund, Margot Marsh Biodiversity Foundation, the Tulsa Zoo, Sigma
690
Xi, an NSF Research and Training Grant to University of Maryland. GRF was supported by
691
grants J51278, 157656 and CF263958 from the National Council for Science and Technology
692
(CONACYT) and by grant WW-R008-17 by the National Geographic Society. CJS was
693
supported by Leakey Foundation, NSF-DDIG (BCS-0752683 to C.H. Janson), National
694
29
Geographic Society, and the Wenner-Gren Foundation. SS was supported by Neotropical
695
Primate Conservation through various grants. PGASL received research support from the
696
Fundação Grupo Boticario (0973-2013-8) and CNPQ. ACS was supported by a Biotechnology
697
and Biological Sciences Research Council grant (98/S11498). SESA was supported by the
698
Mexican National Council for Science and Technology (CONACYT) through student grant
699
207883. Data were collected with the assitance of Augusto Canul, Eulogio Canul, Juan Canul
700
and Macedonio Canul. JPSA was supported by DAAD, CAPES and IPS Conservation Grants,
701
and currently supported by FACEPE (BFP-0149-2.05/19). VKS was supported by the
702
Coordination of Improvement of Higher Level Personnel (CAPES). KJES was supported by
703
Evangelisches Studienwerk Villigst, Universität Hamburg and Kompetenzzentrum Nachhaltige
704
Universität, Primate Conservation, Inc. (PCI #1542), and the German Academic Exchange
705
Service DAAD. MPT was supported by the American Society of Mammalogists, the Consejo
706
Nacional de Investigaciones Científicas y Técnicas (CONICET), Idea Wild. SVB was supported
707
by the National Autonomous University of Mexico (PAPIIT-Project IN200216).
708
709
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Figure legends
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Fig. 1. Hypothesized relationships between species-specific traits, and ecological and
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anthropogenic factors and ground use by monkeys in the Americas and lemurs in Madagascar,
1155
and not any specific transition in one species or another. For species-specific traits, taxa
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exhibiting quadrupedal locomotion (inferred from their inter-membral index), have a larger
1157
group size, and have greater body mass are hypothesized to use the ground more. Taxa with diets
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consisting of more fruit, and exhibiting vertical clinging and leaping (VCL) and brachiator
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locomotion (inferred from their inter-membral index) are hypothesized to spend less time on the
1160
ground. Regarding ecological factors, taxa inhabiting sites with higher maximum temperatures
1161
and greater primate species richness are hypothesized to use the ground more. Taxa inhabiting
1162
sites with a greater number of terrestrial predators and greater continuous canopy coverage are
1163
hypothesized to spend less time on the ground. Regarding anthropogenic factors, taxa inhabiting
1164
sites that are further distances from roads are hypothesized to use the ground more, whereas taxa
1165
inhabiting sites that are closer to larger human population densities are hypothesized to spend
1166
less time on the ground.
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Fig. 2. Spatial distribution of primate genera included in our behavioral ecology dataset.
1170