Factors influencing terrestriality in primates of the Americas and Madagascar


Por: Eppley T.M., Hoeks S., Chapman C.A., Ganzhorn J.U., Hall K., Owen M.A., Adams D.B., Allgas N., Amato K.R., Andriamahaihavana M., Aristizabal J.F., Baden A.L., Balestri M., Barnett A.A., Bicca-Marques J.C., Bowler M., Boyle S.A., Brown M., Caillaud D., Calegaro-Marques C., Campbell C.J., Campera M., Campos F.A., Cardoso T.S., Carretero-Pinzón X., Champion J., Chaves ÓM., Chen-Kraus C., Colquhoun I.C., Dean B., Dubrueil C., Ellis K.M., Erhart E.M., Evans K.J.E., Fedigan L.M., Felton A.M., Ferreira R.G., Fichtel C., Fonseca M.L., Fontes I.P., Fortes V.B., Fumian I., Gibson D., Guzzo G.B., Hartwell K.S., Heymann E.W., Hilário R.R., Holmes S.M., Irwin M.T., Johnson S.E., Kappeler P.M., Kelley E.A., King T., Knogge C., Koch F., Kowalewski M.M., Lange L.R., Lauterbur M.E., Louis E.E., Jr, Lutz M.C., Martínez J., Melin A.D., de Melo F.R., Mihaminekena T.H., Mogilewsky M.S., Moreira L.S., Moura L.A., Muhle C.B., Nagy-Reis M.B., Norconk M.A., Notman H., O'Mara M.T., Ostner J., Patel E.R., Pavelka M.S.M., Pinacho-Guendulain B., Porter L.M., Pozo-Montuy G., Raboy B.E., Rahalinarivo V., Raharinoro N.A., Rakotomalala Z., Ramos-Fernández G., Rasamisoa D.C., Ratsimbazafy J., Ravaloharimanitra M., Razafindramanana J., Razanaparany T.P., Righini N., Robson N.M., Gonçalves J.D.R., Sanamo J., Santacruz N., Sato H., Sauther M.L., Scarry C.J., Serio-Silva J.C., Shanee S., Lins P.G.A.S., Smith A.C., Smith Aguilar S.E., Souza-Alves J.P., Stavis V.K., Steffens K.J.E., Stone A.I., Strier K.B., Suarez S.A., Talebi M., Tecot S.R., Tujague M.P., Valenta K., Van Belle S., Vasey N., Wallace R.B., Welch G., Wright P.C., Donati G., Santini L.

Publicada: 1 ene 2022
Categoría: Multidisciplinary

Resumen:
Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

Filiaciones:
Eppley T.M.:
 Conservation Science and Wildlife Health, San Diego Zoo Wildlife Alliance, Escondido, CA 92027

 Department of Anthropology, Portland State UniversityPortland OR 97201, Jamaica

Hoeks S.:
 Department of Environmental Science, Radboud Institute for Biological and Environmental Sciences, Radboud University, GL Nijmegen, 6500, Netherlands

Chapman C.A.:
 Department of Anthropology, Center for the Advanced Study of Human Paleobiology, George Washington UniversityWA, United States

 Wilson CenterWA, United States

 School of Life Sciences, University of KwaZulu-Natal, Scottsville, 3209, South Africa

 Shaanxi Key Laboratory for Animal Conservation, Northwest University, Xi'an, 710069, China

Ganzhorn J.U.:
 Department of Animal Ecology and Conservation, Institute of Zoology, Universität HamburgHamburg 20146, Germany

Hall K.:
 Sedgwick County Zoo, Wichita, United States

Owen M.A.:
 Conservation Science and Wildlife Health, San Diego Zoo Wildlife Alliance, Escondido, CA 92027

Adams D.B.:
 Department of Anthropology, Ohio State University, Columbus, OH 43210, United States

 Department of Anthropology, Humboldt State University, Arcata, CA 95521

Allgas N.:
 Asociación Neotropical Primate Conservation Perú5N 750 San Martin, Peru

Amato K.R.:
 Department of Anthropology, Northwestern University, Evanston, IL 60208, United States

Andriamahaihavana M.:
 Mention Zoologie et Biodiversité Animale, Faculté des Sciences, Université d'Antananarivo, Antananarivo, 101, Madagascar

Aristizabal J.F.:
 Departamento de Ciencias Químico Biológicas, Instituto de Ciencias Biomédicas, Universidad Autónoma de Ciudad Juárez, CP 32310 Ciudad Juárez, Mexico

 Laboratorio de Ecología de Bosques Tropicales y Primatología, Departamento de Ciencias Biológicas, Universidad de Los Andes, 111711 Bogotá, Colombia

Baden A.L.:
 Department of Anthropology, Hunter College of City University of New York, NY, NY 10065, United States

 Department of Anthropology, Graduate Center of City University of New York, NY, NY 10016, United States

 New York Consortium in Evolutionary Primatology, NY, NY 10024, United States

Balestri M.:
 Department of Social Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom

Barnett A.A.:
 Centre for Research in Evolutionary and Environmental Anthropology, Roehampton University, London, SW15 5PJ, United Kingdom

 Department of Zoology, Federal University of Pernambuco, Brazil

Bicca-Marques J.C.:
 Laboratório de Primatologia, Escola de Ciências da Saúde e da Vida, Pontifícia Universidade Católica do Rio Grande do Sul, Brazil

Bowler M.:
 Conservation Science and Wildlife Health, San Diego Zoo Wildlife Alliance, Escondido, CA 92027

 Department of Engineering, Arts, Science, Technology, University of Suffolk, Ipswich, IP4 1QJ, United Kingdom

 Ipswich, IP4 1QJ, United Kingdom

Boyle S.A.:
 Department of Biology, Rhodes College, Memphis, United States

Brown M.:
 Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

Caillaud D.:
 Department of Anthropology, University of California, Davis, CA 95616

Calegaro-Marques C.:
 Departamento de Zoologia, Universidade Federal do Rio Grande do Sul, Brazil

Campbell C.J.:
 Department of Anthropology, California State University Northridge, Northridge, CA 91325

Campera M.:
 Department of Social Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom

Campos F.A.:
 Department of Anthropology, University of Texas at San Antonio, San Antonio, TX 78249, Mexico

Cardoso T.S.:
 Coordenação de Ciências da Terra e Ecologia, Museu Paraense Emílio Goeldi, Brazil

Carretero-Pinzón X.:
 Villavicencio, Colombia

Champion J.:
 Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

Chaves ÓM.:
 Escuela de Biología, Universidad de Costa RicaSan José 11501-2060, Costa Rica

Chen-Kraus C.:
 Department of Anthropology, Yale University, New Haven, CT 06511, United States

Colquhoun I.C.:
 Department of Anthropology and The Centre for Environment & Sustainability, University of Western Ontario, London, Canada

Dean B.:
 Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

Dubrueil C.:
 Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

Ellis K.M.:
 Department of Anthropology, Miami University, Oxford, United Kingdom

Erhart E.M.:
 Department of Anthropology, Texas State UniversitySan Marcos, Guatemala

Evans K.J.E.:
 Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

Fedigan L.M.:
 Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

Felton A.M.:
 Southern Swedish Forest Research Centre, Swedish University of Agricultural Sciences, Sweden

Ferreira R.G.:
 Universidade Federal do Rio Grande do Norte, Brazil

Fichtel C.:
 Behavioral Ecology and Sociobiology Unit, German Primate Center, 37077 Göttingen, Germany

Fonseca M.L.:
 Laboratorio de Ecología de Bosques Tropicales y Primatología, Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá 111711, Colombia

Fontes I.P.:
 Programa de Pós-graduação em Desenvolvimento e Meio Ambiente, Universidade Federal de Sergipe, Brazil

 Secretaria Municipal de Meio Ambiente, Brazil

Fortes V.B.:
 Laboratório de Primatologia, Departamento de Zootecnia e Ciências Biológicas, Universidade Federal de Santa Maria, Brazil

Fumian I.:
 Fundação de Apoio à Pesquisa, Universidade Federal de Goiás, Brazil

Gibson D.:
 Conservation Science and Wildlife Health, San Diego Zoo Wildlife Alliance, Escondido, CA 92027

Guzzo G.B.:
 Museu de Ciências Naturais, Universidade de Caxias do Sul ,Caxias do Sul-RS 95070-560, Brazil

Hartwell K.S.:
 Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

 Foundation for Wildlife Conservation, Bainbridge Island, WA, 98110, Ghana

Heymann E.W.:
 Behavioral Ecology and Sociobiology Unit, German Primate Center, 37077 Göttingen, Germany

Hilário R.R.:
 Departamento de Meio Ambiente e Desenvolvimento, Universidade Federal do Amapá, Brazil

Holmes S.M.:
 Department of Wildlife, Fish, Environmental Studies, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden

Irwin M.T.:
 Department of Anthropology, Northern Illinois University, DeKalb, IL 60115, United States

Johnson S.E.:
 Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

Kappeler P.M.:
 Behavioral Ecology and Sociobiology Unit, German Primate Center, 37077 Göttingen, Germany

 Department of Sociobiology and Anthropology, University of Göttingen, 37077 Göttingen, Germany

Kelley E.A.:
 Saint Louis ZooSaint Louis MO 63110, Seychelles

King T.:
 Aspinall Foundation, Antananarivo, 101, Madagascar

 Aspinall Foundation, Port Lympne Reserve, Hythe CT21-4LR, United Kingdom

 Durrell Institute of Conservation and Ecology, School of Anthropology and Conservation, University of KentCanterbury CT2 7NZ, United Kingdom

Knogge C.:
 Instituto de Pesquisas Ecológicas, Brazil

Koch F.:
 Behavioral Ecology and Sociobiology Unit, German Primate Center, 37077 Göttingen, Germany

Kowalewski M.M.:
 Estacion Biologica Corrientes (CCT Nordeste), Consejo Nacional de Investigaciones Científicas y Técnicas de ArgentinaCorrientes W3401XAL, Argentina

Lange L.R.:
 Association for Research and Conservation in the Amazon, Puerto Maldonado, Madre de Dios 17001, Peru

 Puerto Maldonado, Madre de Dios 17001, Peru

Lauterbur M.E.:
 Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85719, United States

 Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY, 11790

Louis E.E.:
 Grewcock Center for Conservation and Research, Omaha's Henry Doorly Zoo and Aquarium, Omaha, NE 68107

Jr:
 Grewcock Center for Conservation and Research, Omaha's Henry Doorly Zoo and Aquarium, Omaha, NE 68107

Lutz M.C.:
 Animal Behavior Graduate Group, University of California, Davis, CA 95616

Martínez J.:
 Wildlife Conservation Society, Casilla 3-35181 SM.La Paz, Bolivia

 Red Boliviana de Primatología, Bolivia

Melin A.D.:
 Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

de Melo F.R.:
 Department of Forestry Engineering, Federal University of Viçosa, Brazil

 Muriqui Instituto de Biodiversidade, Brazil

Mihaminekena T.H.:
 Aspinall Foundation, Antananarivo, 101, Madagascar

 Groupe d'Etude et de Recherches sur les Primates de Madagascar, Antananarivo, 101, Madagascar

Mogilewsky M.S.:
 School of the Environment, Portland State UniversityPortland OR 97201, Jamaica

Moreira L.S.:
 Fundação de Apoio à Pesquisa, Universidade Federal de Goiás, Brazil

 Muriqui Instituto de Biodiversidade, Brazil

Moura L.A.:
 Muriqui Instituto de Biodiversidade, Brazil

 Pós-Graduação em Ciências Biológicas (Biologia Animal), Universidade Federal do Espírito Santo, Brazil

Muhle C.B.:
 Laboratório de Primatologia, Escola de Ciências da Saúde e da Vida, Pontifícia Universidade Católica do Rio Grande do Sul, Brazil

Nagy-Reis M.B.:
 Biological Sciences, University of Alberta, AB T6G 2E9, Edmonton, Canada

Norconk M.A.:
 Department of Anthropology, Kent State University, Kent, United Kingdom

Notman H.:
 Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

 Centre for Social Sciences (Anthropology), Athabasca University, Athabasca, AB T9S 3A3, Canada

O'Mara M.T.:
 Department of Biological Sciences, Southeastern Louisiana University, Hammond, United States

 Department of Migration, Max Planck Institute of Animal Behavior, 78315 Radolfzell, Germany

 Smithsonian Tropical Research Institute, República de Panamá

Ostner J.:
 Department of Behavioral Ecology, University of Goettingen, Goettingen, 37077, Germany

 Research Group Primate Social Evolution, German Primate Center, Leibniz Institute for Primate Research, Goettingen, 37077, Germany

Patel E.R.:
 Lemur Conservation Foundation, FL 34251

Pavelka M.S.M.:
 Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

Pinacho-Guendulain B.:
 Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana, 52005 Unidad Lerma, Mexico

 Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Instituto Politécnico Nacional, Unidad OaxacaOaxaca 71230, Mexico

Porter L.M.:
 Department of Anthropology, Northern Illinois University, DeKalb, IL 60115, United States

Pozo-Montuy G.:
 Conservación de la Biodiversidad del Usumacinta A.C., Balancán, 86990 Tabasco, Mexico

 Facultad Maya de Estudios Agropecuarios, Universidad Autónoma de Chiapas, 29980 Catazajá, Mexico

Raboy B.E.:
 Department of Biology, University of Maryland, College ParkMD 20742

Rahalinarivo V.:
 Mention Anthropobiologie et Développement Durable, Faculté des Sciences, University of Antananarivo, Antananarivo, 101, Madagascar

Raharinoro N.A.:
 Mention Zoologie et Biodiversité Animale, Faculté des Sciences, Université d'Antananarivo, Antananarivo, 101, Madagascar

Rakotomalala Z.:
 Mention Zoologie et Biodiversité Animale, Faculté des Sciences, Université d'Antananarivo, Antananarivo, 101, Madagascar

Ramos-Fernández G.:
 Department of Mathematical Modelling of Social Systems, Institute for Research on Applied Mathematics and Systems, Universidad Nacional Autónoma de MéxicoMexico City 3000, Mexico

 Center for Complexity Sciences, Universidad Nacional Autónoma de MéxicoMexico City 3000, Mexico

Rasamisoa D.C.:
 Conservation Science and Wildlife Health, San Diego Zoo Wildlife Alliance, Escondido, CA 92027

Ratsimbazafy J.:
 Groupe d'Etude et de Recherches sur les Primates de Madagascar, Antananarivo, 101, Madagascar

Ravaloharimanitra M.:
 Aspinall Foundation, Antananarivo, 101, Madagascar

Razafindramanana J.:
 Mention Anthropobiologie et Développement Durable, Faculté des Sciences, University of Antananarivo, Antananarivo, 101, Madagascar

Razanaparany T.P.:
 Mention Zoologie et Biodiversité Animale, Faculté des Sciences, Université d'Antananarivo, Antananarivo, 101, Madagascar

 Graduate School of Asian and African Area Studies, Kyoto UniversityKyoto 615-8510, Japan

Righini N.:
 Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, CP 44100 Guadalajara, Mexico

Robson N.M.:
 Department of Life Sciences, Imperial College London, London, SW7 2AZ, United Kingdom

Gonçalves J.D.R.:
 Instituto de Desenvolvimento Sustentável Mamirauá, Brazil

Sanamo J.:
 Département Sciences de la Nature et de l'Environnement, Facultés des Sciences, Université d'Antsiranana, Antsiranana, 201, Madagascar

Santacruz N.:
 College of Veterinary Medicine, Cornell University, Ithaca, NY 14853

Sato H.:
 Primate Research Institute, Kyoto UniversityAichi 484-8506, Japan

Sauther M.L.:
 Department of Anthropology, University of Colorado-Boulder, CO 80302, Boulder, United States

Scarry C.J.:
 Department of Anthropology, California State University, Sacramento, CA 95819

 Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, NY, 11794

Serio-Silva J.C.:
 Red de Biología y Conservación de Vertebrados, Instituto de Ecología AC, Mexico

Shanee S.:
 Neotropical Primate Conservation, Seaton PL11 3JQ, United Kingdom

Lins P.G.A.S.:
 Pós-Graduação em Ecologia e Conservação da Biodiversidade, Universidade Federal do Mato Grosso, Brazil

Smith A.C.:
 School of Life Sciences, Anglia Ruskin University, Cambridge, CB1 1PT, United Kingdom

Smith Aguilar S.E.:
 Instituto de Investigaciones Sociológicas, Universidad Autónoma Benito Juárez de OaxacaOaxaca 68120, Mexico

Souza-Alves J.P.:
 Departamento de Zoologia, Universidade Federal de Pernambuco, Brazil

 Laboratório de Ecologia, Comportamento e Conservação, Universidade Federal de Pernambuco, Brazil

Stavis V.K.:
 Laboratório de Produtos Naturais e Espectrometria de Massas, Faculdade de Ciências Farmacêuticas, Alimentos e Nutrição, Universidade Federal de Mato Grosso do Sul, Campo Grande-MS 79070-900, Brazil

 Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Campo Grande-MS 79070-900, Brazil

Steffens K.J.E.:
 Department of Biology, Institute of Zoology, Universität HamburgHamburg 20146, Germany

Stone A.I.:
 Biology Department, California Lutheran University, Thousand Oaks, CA, 91360, Italy

Strier K.B.:
 Department of Anthropology, University of Wisconsin-Madison, Madison, WI 53706, United States

Suarez S.A.:
 Department of Behavioral Sciences, San Diego Mesa College, San Diego, CA 92111

Talebi M.:
 Departamento de Cíências Ambientais, Lab Ecologia e Conservação da Natureza and the Programa Análise Ambiental Integrada, Universidade Federal de São PauloSão Paulo 04040-003, Brazil

 Instituto Pró-Muriqui, São Paulo-SP 18230-0000, Brazil, Brazil

Tecot S.R.:
 School of Anthropology, University of Arizona, Tucson, AZ 85719, United States

Tujague M.P.:
 Facultad de Ciencias Forestales, Universidad Nacional de MisionesCP 3380 Misiones, Argentina

 Instituto de Biología Subtropical, Consejo Nacional de Investigaciones Científicas y Técnicas, Puerto IguazúMisiones 3370, Argentina

 Asociación Civil Centro de Investigaciones del Bosque Atlántico, Puerto IguazúMisiones 3370, Argentina

Valenta K.:
 Department of Anthropology, University of Florida, FL 32603, Gainesville, United States

Van Belle S.:
 Department of Anthropology, University of Austin at Texas, Austin, TX 78712, United States

Vasey N.:
 Department of Anthropology, Portland State UniversityPortland OR 97201, Jamaica

 School of the Environment, Portland State UniversityPortland OR 97201, Jamaica

Wallace R.B.:
 Wildlife Conservation Society, Casilla 3-35181 SM.La Paz, Bolivia

 Red Boliviana de Primatología, Bolivia

 Wildlife Conservation Society, Bronx, NY 10460

Welch G.:
 Foundation for Wildlife Conservation, Bainbridge Island, WA, 98110, Ghana

Wright P.C.:
 Department of Anthropology, Stony Brook University, Stony Brook, NY, 11794

 Centre ValBio, Ranomafana, Ifanadiana, 312, Madagascar

Donati G.:
 Department of Social Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom

Santini L.:
 Department of Biology and Biotechnology "Charles Darwin", Sapienza University of Rome, Rome, 00185, Italy
ISSN: 00278424
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NATL ACAD SCIENCES, 2101 CONSTITUTION AVE NW, WASHINGTON, DC 20418 USA, Estados Unidos America
Tipo de documento: Article
Volumen: 119 Número: 42
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WOS Id: 000898705000002
ID de PubMed: 36215474
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