Factors influencing terrestriality in primates of the Americas and Madagascar

Timothy M. Eppley; Selwyn Hoeks; Colin A. Chapman; Jörg U. Ganzhorn; Katie Hall; Megan A. Owen; Dara B. Adams; Néstor Allgas; Katherine R. Amato; McAntonin Andriamahaihavana; John F. Aristizabal; Andrea L. Baden; Michela Balestri; Adrian A. Barnett; Júlio César Bicca-Marques; Mark Bowler; Sarah A. Boyle; Meredith Brown; Damien Caillaud; Cláudia Calegaro-Marques; Christina J. Campbell; Marco Campera; Fernando A. Campos; Tatiane S. Cardoso; Xyomara Carretero-Pinzón; Jane Champion; Óscar M. Chaves; Chloe Chen-Kraus; Ian C. Colquhoun; Brittany Dean; Colin Dubrueil; Kelsey M. Ellis; Elizabeth M. Erhart; Kayley J.E. Evans; Linda M. Fedigan; Annika M. Felton; Renata G. Ferreira; Claudia Fichtel; Manuel L. Fonseca; Isadora P. Fontes; Vanessa B. Fortes; Ivanyr Fumian; Dean Gibson; Guilherme B. Guzzo; Kayla S. Hartwell; Eckhard W. Heymann; Renato R. Hilário; Sheila M. Holmes; Mitchell T. Irwin; Steig E. Johnson; Peter M. Kappeler; Elizabeth A. Kelley; Tony King; Christoph Knogge; Flávia Koch; Martin M. Kowalewski; Liselot R. Lange; Edward E. Louis; Meredith C. Lutz; Jesús Martínez; M. Elise Lauterbur; Amanda D. Melin; Fabiano R. de Melo; Tsimisento H. Mihaminekena; Monica S. Mogilewsky; Leandro S. Moreira; Letícia A. Moura; Mariana B. Nagy-Reis; Marilyn A. Norconk; Hugh Notman; Carina B. Muhle; M. Teague O’Mara; Julia Ostner; Erik R. Patel; Mary S.M. Pavelka; Braulio Pinacho-Guendulain; Leila M. Porter; Gilberto Pozo-Montuy; Becky E. Raboy; Vololonirina Rahalinarivo; Njaratiana A. Raharinoro; Zafimahery Rakotomalala; Gabriel Ramos-Fernández; Delaïd C. Rasamisoa; Jonah Ratsimbazafy; Maholy Ravaloharimanitra; Josia Razafindramanana; Tojotanjona P. Razanaparany; Nicoletta Righini; Nicola M. Robson; Jonas da Rosa Gonçalves; Justin Sanamo; Nicole Santacruz; Hiroki Sato; Michelle L. Sauther; Clara J. Scarry; Juan Carlos Serio-Silva; Sam Shanee; Poliana G.A. de Souza Lins; Andrew C. Smith; Sandra E. Smith Aguilar; João Pedro Souza-Alves; Vanessa Katherinne Stavis; Kim J.E. Steffens; Anita I. Stone; Karen B. Strier; Scott A. Suarez; Maurício Talebi; Stacey R. Tecot; M. Paula Tujague; Kim Valenta; Natalie Vasey; Robert B. Wallace; Sarie Van Belle; Gilroy Welch; Patricia C. Wright; Giuseppe Donati; Luca Santini

doi:10.1073/pnas.2121105119

Factors influencing terrestriality in primates of the Americas and Madagascar

Timothy M. Eppley, Selwyn Hoeks, Colin A. Chapman, Jörg U. Ganzhorn, Katie Hall, Megan A. Owen, Dara B. Adams, Néstor Allgas, Katherine R. Amato, McAntonin Andriamahaihavana, John F. Aristizabal, Andrea L. Baden, Michela Balestri, Adrian A. Barnett, Júlio César Bicca-Marques, Mark Bowler, Sarah A. Boyle, Meredith Brown, Damien Caillaud, Cláudia Calegaro-MarquesChristina J. Campbell, Marco Campera, Fernando A. Campos, Tatiane S. Cardoso, Xyomara Carretero-Pinzón, Jane Champion, Óscar M. Chaves, Chloe Chen-Kraus, Ian C. Colquhoun, Brittany Dean, Colin Dubrueil, Kelsey M. Ellis, Elizabeth M. Erhart, Kayley J.E. Evans, Linda M. Fedigan, Annika M. Felton, Renata G. Ferreira, Claudia Fichtel, Manuel L. Fonseca, Isadora P. Fontes, Vanessa B. Fortes, Ivanyr Fumian, Dean Gibson, Guilherme B. Guzzo, Kayla S. Hartwell, Eckhard W. Heymann, Renato R. Hilário, Sheila M. Holmes, Mitchell T. Irwin, Steig E. Johnson, Peter M. Kappeler, Elizabeth A. Kelley, Tony King, Christoph Knogge, Flávia Koch, Martin M. Kowalewski, Liselot R. Lange, Edward E. Louis, Meredith C. Lutz, Jesús Martínez, M. Elise Lauterbur, Amanda D. Melin, Fabiano R. de Melo, Tsimisento H. Mihaminekena, Monica S. Mogilewsky, Leandro S. Moreira, Letícia A. Moura, Mariana B. Nagy-Reis, Marilyn A. Norconk, Hugh Notman, Carina B. Muhle, M. Teague O’Mara, Julia Ostner, Erik R. Patel, Mary S.M. Pavelka, Braulio Pinacho-Guendulain, Leila M. Porter, Gilberto Pozo-Montuy, Becky E. Raboy, Vololonirina Rahalinarivo, Njaratiana A. Raharinoro, Zafimahery Rakotomalala, Gabriel Ramos-Fernández, Delaïd C. Rasamisoa, Jonah Ratsimbazafy, Maholy Ravaloharimanitra, Josia Razafindramanana, Tojotanjona P. Razanaparany, Nicoletta Righini, Nicola M. Robson, Jonas da Rosa Gonçalves, Justin Sanamo, Nicole Santacruz, Hiroki Sato, Michelle L. Sauther, Clara J. Scarry, Juan Carlos Serio-Silva, Sam Shanee, Poliana G.A. de Souza Lins, Andrew C. Smith, Sandra E. Smith Aguilar, João Pedro Souza-Alves, Vanessa Katherinne Stavis, Kim J.E. Steffens, Anita I. Stone, Karen B. Strier, Scott A. Suarez, Maurício Talebi, Stacey R. Tecot, M. Paula Tujague, Kim Valenta, Natalie Vasey, Robert B. Wallace, Sarie Van Belle, Gilroy Welch, Patricia C. Wright, Giuseppe Donati, Luca Santini

Research output: Contribution to journal › Article › peer-review

9 Scopus citations

Abstract

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.

Original language	English (US)
Article number	e2121105119
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	119
Issue number	42
DOIs	https://doi.org/10.1073/pnas.2121105119
State	Published - Oct 18 2022

Keywords

primate communities j primate evolution j evolutionary transitions j niche shift j climate change

ASJC Scopus subject areas

General

Access to Document

10.1073/pnas.2121105119

Cite this

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., ... Santini, L. (2022). Factors influencing terrestriality in primates of the Americas and Madagascar. Proceedings of the National Academy of Sciences of the United States of America, 119(42), Article e2121105119. https://doi.org/10.1073/pnas.2121105119

Eppley, TM, Hoeks, S, Chapman, CA, Ganzhorn, JU, Hall, K, Owen, MA, Adams, DB, Allgas, N, Amato, KR, Andriamahaihavana, M, Aristizabal, JF, Baden, AL, Balestri, M, Barnett, AA, Bicca-Marques, JC, Bowler, M, Boyle, SA, Brown, M, Caillaud, D, Calegaro-Marques, C, Campbell, CJ, Campera, M, Campos, FA, Cardoso, TS, Carretero-Pinzón, X, Champion, J, Chaves, ÓM, Chen-Kraus, C, Colquhoun, IC, Dean, B, Dubrueil, C, Ellis, KM, Erhart, EM, Evans, KJE, Fedigan, LM, Felton, AM, Ferreira, RG, Fichtel, C, Fonseca, ML, Fontes, IP, Fortes, VB, Fumian, I, Gibson, D, Guzzo, GB, Hartwell, KS, Heymann, EW, Hilário, RR, Holmes, SM, Irwin, MT, Johnson, SE, Kappeler, PM, Kelley, EA, King, T, Knogge, C, Koch, F, Kowalewski, MM, Lange, LR, Louis, EE, Lutz, MC, Martínez, J, Lauterbur, ME, Melin, AD, de Melo, FR, Mihaminekena, TH, Mogilewsky, MS, Moreira, LS, Moura, LA, Nagy-Reis, MB, Norconk, MA, Notman, H, Muhle, CB, O’Mara, MT, Ostner, J, Patel, ER, Pavelka, MSM, Pinacho-Guendulain, B, Porter, LM, Pozo-Montuy, G, Raboy, BE, Rahalinarivo, V, Raharinoro, NA, Rakotomalala, Z, Ramos-Fernández, G, Rasamisoa, DC, Ratsimbazafy, J, Ravaloharimanitra, M, Razafindramanana, J, Razanaparany, TP, Righini, N, Robson, NM, da Rosa Gonçalves, J, Sanamo, J, Santacruz, N, Sato, H, Sauther, ML, Scarry, CJ, Serio-Silva, JC, Shanee, S, de Souza Lins, PGA, Smith, AC, Smith Aguilar, SE, Souza-Alves, JP, Stavis, VK, Steffens, KJE, Stone, AI, Strier, KB, Suarez, SA, Talebi, M, Tecot, SR, Tujague, MP, Valenta, K, Vasey, N, Wallace, RB, Van Belle, S, Welch, G, Wright, PC, Donati, G & Santini, L 2022, 'Factors influencing terrestriality in primates of the Americas and Madagascar', Proceedings of the National Academy of Sciences of the United States of America, vol. 119, no. 42, e2121105119. https://doi.org/10.1073/pnas.2121105119

@article{2d956cc61951422c8a404d570940dbcb,

title = "Factors influencing terrestriality in primates of the Americas and Madagascar",

abstract = "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.",

keywords = "primate communities j primate evolution j evolutionary transitions j niche shift j climate change",

author = "Eppley, {Timothy M.} and Selwyn Hoeks and Chapman, {Colin A.} and Ganzhorn, {J{\"o}rg U.} and Katie Hall and Owen, {Megan A.} and Adams, {Dara B.} and N{\'e}stor Allgas and Amato, {Katherine R.} and McAntonin Andriamahaihavana and Aristizabal, {John F.} and Baden, {Andrea L.} and Michela Balestri and Barnett, {Adrian A.} and Bicca-Marques, {J{\'u}lio C{\'e}sar} and Mark Bowler and Boyle, {Sarah A.} and Meredith Brown and Damien Caillaud and Cl{\'a}udia Calegaro-Marques and Campbell, {Christina J.} and Marco Campera and Campos, {Fernando A.} and Cardoso, {Tatiane S.} and Xyomara Carretero-Pinz{\'o}n and Jane Champion and Chaves, {{\'O}scar M.} and Chloe Chen-Kraus and Colquhoun, {Ian C.} and Brittany Dean and Colin Dubrueil and Ellis, {Kelsey M.} and Erhart, {Elizabeth M.} and Evans, {Kayley J.E.} and Fedigan, {Linda M.} and Felton, {Annika M.} and Ferreira, {Renata G.} and Claudia Fichtel and Fonseca, {Manuel L.} and Fontes, {Isadora P.} and Fortes, {Vanessa B.} and Ivanyr Fumian and Dean Gibson and Guzzo, {Guilherme B.} and Hartwell, {Kayla S.} and Heymann, {Eckhard W.} and Hil{\'a}rio, {Renato R.} and Holmes, {Sheila M.} and Irwin, {Mitchell T.} and Johnson, {Steig E.} and Kappeler, {Peter M.} and Kelley, {Elizabeth A.} and Tony King and Christoph Knogge and Fl{\'a}via Koch and Kowalewski, {Martin M.} and Lange, {Liselot R.} and Louis, {Edward E.} and Lutz, {Meredith C.} and Jes{\'u}s Mart{\'i}nez and Lauterbur, {M. Elise} and Melin, {Amanda D.} and {de Melo}, {Fabiano R.} and Mihaminekena, {Tsimisento H.} and Mogilewsky, {Monica S.} and Moreira, {Leandro S.} and Moura, {Let{\'i}cia A.} and Nagy-Reis, {Mariana B.} and Norconk, {Marilyn A.} and Hugh Notman and Muhle, {Carina B.} and O{\textquoteright}Mara, {M. Teague} and Julia Ostner and Patel, {Erik R.} and Pavelka, {Mary S.M.} and Braulio Pinacho-Guendulain and Porter, {Leila M.} and Gilberto Pozo-Montuy and Raboy, {Becky E.} and Vololonirina Rahalinarivo and Raharinoro, {Njaratiana A.} and Zafimahery Rakotomalala and Gabriel Ramos-Fern{\'a}ndez and Rasamisoa, {Dela{\"i}d C.} and Jonah Ratsimbazafy and Maholy Ravaloharimanitra and Josia Razafindramanana and Razanaparany, {Tojotanjona P.} and Nicoletta Righini and Robson, {Nicola M.} and {da Rosa Gon{\c c}alves}, Jonas and Justin Sanamo and Nicole Santacruz and Hiroki Sato and Sauther, {Michelle L.} and Scarry, {Clara J.} and Serio-Silva, {Juan Carlos} and Sam Shanee and {de Souza Lins}, {Poliana G.A.} and Smith, {Andrew C.} and {Smith Aguilar}, {Sandra E.} and Souza-Alves, {Jo{\~a}o Pedro} and Stavis, {Vanessa Katherinne} and Steffens, {Kim J.E.} and Stone, {Anita I.} and Strier, {Karen B.} and Suarez, {Scott A.} and Maur{\'i}cio Talebi and Tecot, {Stacey R.} and Tujague, {M. Paula} and Kim Valenta and Natalie Vasey and Wallace, {Robert B.} and {Van Belle}, Sarie and Gilroy Welch and Wright, {Patricia C.} and Giuseppe Donati and Luca Santini",

note = "Funding Information: ACKNOWLEDGMENTS. T.M.E. was supported by funding from the American Society of Primatologists, Conservation International{\textquoteright}s Primate Action Fund, IDEA-Wild, the Margot Marsh Biodiversity Fund, the Mohamed bin Zayed Species Conservation Fund (Project 11253008), Primate Conservation Inc., and the Primate Society of Great Britain/Knowsley Safari Park. D.B.A. was supported by the National Science Foundation Doctoral Dissertation Improvement Grants (NSF-DDIG) (BCS 1341174), the Animal Behavior Society, the Society for Integrative and Comparative Biology, the Tinker Foundation, and the Mansfield and Columbus campuses at The Ohio State University. N.A. was supported by Neotropical Primate Conservation through various grants. K.R.A. is supported as a fellow in the Canadian Institute for Advanced Research{\textquoteright}s “Humans and the microbiome” program. J.C.B.-M. was supported by funding by the World Wildlife Fund-US (#6573), the Brazilian National Council for Scientific and Technological Development/Conselho Nacional de Desenvolvimento Cietifico e Tecnol{\'o}gico (CNPq) (PQ 1C #304475/2018-1), and Programa Nacional de P{\'o}s-Doutorado of the Coordenac¸{\~a}o de Aperfeic¸oamento de Pessoal de {\'N}ıvel Superior–Brazil (Brazilian Higher Education Authority)/Comissao de Aperfeic¸oamento de Pessoal de Nival Superior (CAPES) (Finance Code 001; PNPD Grant 2755/2010). S.A.B. received financial support from the Biological Dynamics of Forest Fragments Project, the Smithsonian Tropical Research Institute, Arizona State University, Fulbright/Institute of International Education, the Margot Marsh Biodiversity Foundation, Providing Educational Opportunities, Primate Conservation Inc., the Organization for Tropical Studies, and the American Society of Primatologists. T.S.C. was supported by a scholarship from Fundac¸{\~a}o de Amparo {\`a} Pesquisa (FUNAPE) and would like to thank the Minerac¸{\~a}o Rio do Norte (MRN) for their support. {\'O}.M.C. was supported by Programa Nacional de P{\'o}s-Doutorado of the Coordenac¸{\~a}o de Aperfeic¸oamento de Pessoal de {\'N}ıvel Superior–Brazil (Brazilian Higher Education Authority)/CAPES (Finance Code 001; PNPD Grant 2755/2010). C.C.-K. received financial support from The NSF (NSF-BSC-1745371), Yale University MacMillan Center for International Studies, the National Geographic Society (EC-420R-18), The Explorers Club, Yale Institute for Biospheric Studies, Yale University Department of Anthropology, The International Primatological Society, and Primate Conservation Inc. Madagascar Ministry of the Environment and Madagascar National Parks permitted this research. I.C.C. received research support from the NSF (Dissertation Improvement Award Grant BNS-9101520), the National Geographic Society (Grant 4496-91), the Boise Fund of the University of Oxford, a Grant-in-Aid of Research from Sigma Xi–The Scientific Research Society, a Washington University Graduate Fellowship, the St. Louis Rainforest Alliance, and the St. Louis Zoo. L.M.F. was supported by Natural Sciences & Engineering Research Council of Canada, and the Canada Research Chairs Programme. A.M.F. was funded by the Wildlife Conservation Society, Conservation International, the Ruf-ford Foundation, and the Primate Society of Great Britain. R.G.F. was supported by the Fundac¸{\~a}o Grupo Boticario (0973-2013-8) and CNPq. I.F. was supported by a scholarship from FUNAPE and would like to thank the MRN for their support. K.S.H. was supported by the Foundation for Wildlife Conservation, the Zoological Society of Milwaukee, Birds Without Borders, the University of Calgary, Athabasca University, and the Natural Sciences and Engineering Research Council of Canada. E.W.H. was supported by Deutsche Forschungsgemeinschaft, Deutscher Akademischer Austauschdienst (DAAD), Universit€atsbund G€ottingen. S.M.H. was supported by the Natural Sciences and Engineering Research Council of Canada, the Philanthropic Educational Organization, Conservation International, and Primate Conservation Inc. S.E.J. was supported by the Natural Sciences and Engineering Research Council of Canada, Conservation International, and Primate Conservation Inc. M.C.L. received funding from the National Science Foundation Graduate Research Fellowship (Award 1650042), University of California, Davis, Bucknell University, a Greenville Zoo Conservation grant, the Pittsburgh Zoo Conservation and Sustainability Fund, Primate Conservation Inc., an International Primatological Society Research Grant, and IDEAWild. F.R.d.M. was support by a scholarship from FUNAPE and would like to thank the MRN for their support. T.H.M. was funded primarily by The Aspinall Foundation through the “Saving Prolemur simus” project, with additional support from Beauval Nature and International Union for Conservation of Nature-“Save Our Species.” L.S.M. was supported by a scholarship from FUNAPE and would like to thank the MRN for their support. M.T.O. was supported in part by the NSF-DDIG (BCS 0851761), the J. William Fulbright Foundation, Sigma Xi, and the School of Human Evolution and Social Change at Arizona State University. B.P.-G. was supported by grants from the Comisi{\'o}n Nacional para el Conocimiento y Uso de la Bioversidad (HK009) and Consejo Nacional de Ciencia y Technolog{\'i}a (CONACYT) (J51278), as well as graduate scholarships from CONACYT (2008–2010 and 2018–2021). G.P.-M. was supported by a doctorate and master{\textquoteright}s degree scholarship from CONACYT (2007–2010) and by the Academic Division of Biological Sciences of the Universidad Ju{\'a}rez Aut{\'o}noma de Tabasco. G.P.-M. also thanks the local people from Balanc{\'a}n for their guidance. B.E.R. was supported by funding provided by the Durrell Wildlife Conservation Trust, the Lion Tamarins of Brazil Fund, Margot Marsh Biodiversity Foundation, the Tulsa Zoo, Sigma Xi, and an NSF Research and Training grant to University of Maryland. G.R.-F. was supported by CONACYT Grants J51278, 157656, and CF263958 and by National Geographic Society Grant WW-R008-17. C.J.S. was supported by the Leakey Foundation, NSF-DDIG (BCS-0752683 to C. H. Janson), the National Geographic Society, and the Wenner-Gren Foundation. S.S. was supported by Neotropical Primate Conservation through various grants. P.G.A.d.S.L. received research support from the Fundac¸{\~a}o Grupo Boticario (0973-2013-8) and CNPq. A.C.S. was supported by Biotechnology and Biological Sciences Research Council Grant 98/S11498. S.E.S.A. was supported by CONACYT through student Grant 207883. Data were collected with the assistance of Augusto Canul, Eulogio Canul, Juan Canul, and Macedonio Canul. J.P.S.-A. was supported by DAAD, CAPES, and International Primatological Society Conservation grants, and currently supported by Fundac¸{\~a}o de Amparo a Ci{\^e}ncia e Tecnologia (BFP-0149-2.05/19). V.K.S. was supported by the Coordination of Improvement of Higher Level Personnel (CAPES). K.J.E.S. was supported by Evangelisches Studienwerk Villigst, Uni-versit€at Hamburg, and Kompetenzzentrum Nachhaltige Universit€at, Primate Conservation Inc. (PCI #1542), and the German Academic Exchange Service DAAD. M.P.T. was supported by the American Society of Mammalogists, the Consejo Nacional de Investigaciones Cient{\'i}ficas y T{\'e}cnicas, and IDEAWild. S.V.B. was supported by the National Autonomous University of Mexico (PAPIIT-Project IN200216). Funding Information: T.M.E. was supported by funding from the American Society of Primatologists, Conservation International{\textquoteright}s Primate Action Fund, IDEAWild, the Margot Marsh Biodiversity Fund, the Mohamed bin Zayed Species Conservation Fund (Project 11253008), Primate Conservation Inc., and the Primate Society of Great Britain/Knowsley Safari Park. D.B.A. was supported by the National Science Foundation Doctoral Dissertation Improvement Grants (NSF-DDIG) (BCS 1341174), the Animal Behavior Society, the Society for Integrative and Comparative Biology, the Tinker Foundation, and the Mansfield and Columbus campuses at The Ohio State University. N.A. was supported by Neotropical Primate Conservation through various grants. K.R.A. is supported as a fellow in the Canadian Institute for Advanced Research{\textquoteright}s “Humans and the microbiome” program. J.C.B.-M. was supported by funding by the World Wildlife Fund-US (#6573), the Brazilian National Council for Scientific and Technological Development/Conselho Nacional de Desenvolvimento Cietifico e Tecnol{\'o}gico (CNPq) (PQ 1C #304475/2018-1), and Programa Nacional de P{\'o}s-Doutorado of the Coordena{\c c}{\~a}o de Aperfei{\c c}oamento de Pessoal de N{\'i}vel Superior–Brazil (Brazilian Higher Education Authority)/Comissao de Aperfei{\c c}oamento de Pessoal de Nival Superior (CAPES) (Finance Code 001; PNPD Grant 2755/2010). S.A.B. received financial support from the Biological Dynamics of Forest Fragments Project, the Smithsonian Tropical Research Institute, Arizona State University, Fulbright/Institute of International Education, the Margot Marsh Biodiversity Foundation, Providing Educational Opportunities, Primate Conservation Inc., the Organization for Tropical Studies, and the American Society of Primatologists. T.S.C. was supported by a scholarship from Funda{\c c}{\~a}o de Amparo {\`a} Pesquisa (FUNAPE) and would like to thank the Minera{\c c}{\~a}o Rio do Norte (MRN) for their support. {\'O}.M.C. was supported by Programa Nacional de P{\'o}s-Doutorado of the Coordena{\c c}{\~a}o de Aperfei{\c c}oamento de Pessoal de N{\'i}vel Superior–Brazil (Brazilian Higher Education Authority)/CAPES (Finance Code 001; PNPD Grant 2755/2010). C.C.-K. received financial support from The NSF (NSF-BSC-1745371), Yale University MacMillan Center for International Studies, the National Geographic Society (EC-420R-18), The Explorers Club, Yale Institute for Biospheric Studies, Yale University Department of Anthropology, The International Primatological Society, and Primate Conservation Inc. Madagascar Ministry of the Environment and Madagascar National Parks permitted this research. I.C.C. received research support from the NSF (Dissertation Improvement Award Grant BNS-9101520), the National Geographic Society (Grant 4496-91), the Boise Fund of the University of Oxford, a Grant-in-Aid of Research from Sigma Xi–The Scientific Research Society, a Washington University Graduate Fellowship, the St. Louis Rainforest Alliance, and the St. Louis Zoo. L.M.F. was supported by Natural Sciences & Engineering Research Council of Canada, and the Canada Research Chairs Programme. A.M.F. was funded by the Wildlife Conservation Society, Conservation International, the Rufford Foundation, and the Primate Society of Great Britain. R.G.F. was supported by the Funda{\c c}{\~a}o Grupo Boticario (0973-2013-8) and CNPq. I.F. was supported by a scholarship from FUNAPE and would like to thank the MRN for their support. K.S.H. was supported by the Foundation for Wildlife Conservation, the Zoological Society of Milwaukee, Birds Without Borders, the University of Calgary, Athabasca University, and the Natural Sciences and Engineering Research Council of Canada. E.W.H. was supported by Deutsche Forschungsgemeinschaft, Deutscher Akademischer Austauschdienst (DAAD), Universit{\"a}tsbund G{\"o}ttingen. S.M.H. was supported by the Natural Sciences and Engineering Research Council of Canada, the Philanthropic Educational Organization, Conservation International, and Primate Conservation Inc. S.E.J. was supported by the Natural Sciences and Engineering Research Council of Canada, Conservation International, and Primate Conservation Inc. M.C.L. received funding from the National Science Foundation Graduate Research Fellowship (Award 1650042), University of California, Davis, Bucknell University, a Greenville Zoo Conservation grant, the Pittsburgh Zoo Conservation and Sustainability Fund, Primate Conservation Inc., an International Primatological Society Research Grant, and IDEAWild. F.R.d.M. was support by a scholarship from FUNAPE and would like to thank the MRN for their support. T.H.M. was funded primarily by The Aspinall Foundation through the “Saving Prolemur simus” project, with additional support from Beauval Nature and International Union for Conservation of Nature-“Save Our Species.” L.S.M. was supported by a scholarship from FUNAPE and would like to thank the MRN for their support. M.T.O. was supported in part by the NSF-DDIG (BCS 0851761), the J. William Fulbright Foundation, Sigma Xi, and the School of Human Evolution and Social Change at Arizona State University. B.P.-G. was supported by grants from the Comisi{\'o}n Nacional para el Conocimiento y Uso de la Bioversidad (HK009) and Consejo Nacional de Ciencia y Technolog{\'i}a (CONACYT) (J51278), as well as graduate scholarships from CONACYT (2008–2010 and 2018–2021). G.P.-M. was supported by a doctorate and master{\textquoteright}s degree scholarship from CONACYT (2007–2010) and by the Academic Division of Biological Sciences of the Universidad Ju{\'a}rez Aut{\'o}noma de Tabasco. G.P.-M. also thanks the local people from Balanc{\'a}n for their guidance. B.E.R. was supported by funding provided by the Durrell Wildlife Conservation Trust, the Lion Tamarins of Brazil Fund, Margot Marsh Biodiversity Foundation, the Tulsa Zoo, Sigma Xi, and an NSF Research and Training grant to University of Maryland. G.R.-F. was supported by CONACYT Grants J51278, 157656, and CF263958 and by National Geographic Society Grant WW-R008-17. C.J.S. was supported by the Leakey Foundation, NSF-DDIG (BCS-0752683 to C. H. Janson), the National Geographic Society, and the Wenner-Gren Foundation. S.S. was supported by Neotropical Primate Conservation through various grants. P.G.A.d.S.L. received research support from the Funda{\c c}{\~a}o Grupo Boticario (0973-2013-8) and CNPq. A.C.S. was supported by Biotechnology and Biological Sciences Research Council Grant 98/S11498. S.E.S.A. was supported by CONACYT through student Grant 207883. Data were collected with the assistance of Augusto Canul, Eulogio Canul, Juan Canul, and Macedonio Canul. J.P.S.-A. was supported by DAAD, CAPES, and International Primatological Society Conservation grants, and currently supported by Funda{\c c}{\~a}o de Amparo a Ci{\^e}ncia e Tecnologia (BFP-0149-2.05/19). V.K.S. was supported by the Coordination of Improvement of Higher Level Personnel (CAPES). K.J.E.S. was supported by Evangelisches Studienwerk Villigst, Universit{\"a}t Hamburg, and Kompetenzzentrum Nachhaltige Universit{\"a}t, Primate Conservation Inc. (PCI #1542), and the German Academic Exchange Service DAAD. M.P.T. was supported by the American Society of Mammalogists, the Consejo Nacional de Investigaciones Cient{\'i}ficas y T{\'e}cnicas, and IDEAWild. S.V.B. was supported by the National Autonomous University of Mexico (PAPIIT-Project IN200216). Publisher Copyright: Copyright {\textcopyright} 2022 the Author(s).",

year = "2022",

month = oct,

day = "18",

doi = "10.1073/pnas.2121105119",

language = "English (US)",

volume = "119",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

number = "42",

}

TY - JOUR

T1 - Factors influencing terrestriality in primates of the Americas and Madagascar

AU - Eppley, Timothy M.

AU - Hoeks, Selwyn

AU - Chapman, Colin A.

AU - Ganzhorn, Jörg U.

AU - Hall, Katie

AU - Owen, Megan A.

AU - Adams, Dara B.

AU - Allgas, Néstor

AU - Amato, Katherine R.

AU - Andriamahaihavana, McAntonin

AU - Aristizabal, John F.

AU - Baden, Andrea L.

AU - Balestri, Michela

AU - Barnett, Adrian A.

AU - Bicca-Marques, Júlio César

AU - Bowler, Mark

AU - Boyle, Sarah A.

AU - Brown, Meredith

AU - Caillaud, Damien

AU - Calegaro-Marques, Cláudia

AU - Campbell, Christina J.

AU - Campera, Marco

AU - Campos, Fernando A.

AU - Cardoso, Tatiane S.

AU - Carretero-Pinzón, Xyomara

AU - Champion, Jane

AU - Chaves, Óscar M.

AU - Chen-Kraus, Chloe

AU - Colquhoun, Ian C.

AU - Dean, Brittany

AU - Dubrueil, Colin

AU - Ellis, Kelsey M.

AU - Erhart, Elizabeth M.

AU - Evans, Kayley J.E.

AU - Fedigan, Linda M.

AU - Felton, Annika M.

AU - Ferreira, Renata G.

AU - Fichtel, Claudia

AU - Fonseca, Manuel L.

AU - Fontes, Isadora P.

AU - Fortes, Vanessa B.

AU - Fumian, Ivanyr

AU - Gibson, Dean

AU - Guzzo, Guilherme B.

AU - Hartwell, Kayla S.

AU - Heymann, Eckhard W.

AU - Hilário, Renato R.

AU - Holmes, Sheila M.

AU - Irwin, Mitchell T.

AU - Johnson, Steig E.

AU - Kappeler, Peter M.

AU - Kelley, Elizabeth A.

AU - King, Tony

AU - Knogge, Christoph

AU - Koch, Flávia

AU - Kowalewski, Martin M.

AU - Lange, Liselot R.

AU - Louis, Edward E.

AU - Lutz, Meredith C.

AU - Martínez, Jesús

AU - Lauterbur, M. Elise

AU - Melin, Amanda D.

AU - de Melo, Fabiano R.

AU - Mihaminekena, Tsimisento H.

AU - Mogilewsky, Monica S.

AU - Moreira, Leandro S.

AU - Moura, Letícia A.

AU - Nagy-Reis, Mariana B.

AU - Norconk, Marilyn A.

AU - Notman, Hugh

AU - Muhle, Carina B.

AU - O’Mara, M. Teague

AU - Ostner, Julia

AU - Patel, Erik R.

AU - Pavelka, Mary S.M.

AU - Pinacho-Guendulain, Braulio

AU - Porter, Leila M.

AU - Pozo-Montuy, Gilberto

AU - Raboy, Becky E.

AU - Rahalinarivo, Vololonirina

AU - Raharinoro, Njaratiana A.

AU - Rakotomalala, Zafimahery

AU - Ramos-Fernández, Gabriel

AU - Rasamisoa, Delaïd C.

AU - Ratsimbazafy, Jonah

AU - Ravaloharimanitra, Maholy

AU - Razafindramanana, Josia

AU - Razanaparany, Tojotanjona P.

AU - Righini, Nicoletta

AU - Robson, Nicola M.

AU - da Rosa Gonçalves, Jonas

AU - Sanamo, Justin

AU - Santacruz, Nicole

AU - Sato, Hiroki

AU - Sauther, Michelle L.

AU - Scarry, Clara J.

AU - Serio-Silva, Juan Carlos

AU - Shanee, Sam

AU - de Souza Lins, Poliana G.A.

AU - Smith, Andrew C.

AU - Smith Aguilar, Sandra E.

AU - Souza-Alves, João Pedro

AU - Stavis, Vanessa Katherinne

AU - Steffens, Kim J.E.

AU - Stone, Anita I.

AU - Strier, Karen B.

AU - Suarez, Scott A.

AU - Talebi, Maurício

AU - Tecot, Stacey R.

AU - Tujague, M. Paula

AU - Valenta, Kim

AU - Vasey, Natalie

AU - Wallace, Robert B.

AU - Van Belle, Sarie

AU - Welch, Gilroy

AU - Wright, Patricia C.

AU - Donati, Giuseppe

AU - Santini, Luca

N1 - Funding Information: ACKNOWLEDGMENTS. T.M.E. was supported by funding from the American Society of Primatologists, Conservation International’s Primate Action Fund, IDEA-Wild, the Margot Marsh Biodiversity Fund, the Mohamed bin Zayed Species Conservation Fund (Project 11253008), Primate Conservation Inc., and the Primate Society of Great Britain/Knowsley Safari Park. D.B.A. was supported by the National Science Foundation Doctoral Dissertation Improvement Grants (NSF-DDIG) (BCS 1341174), the Animal Behavior Society, the Society for Integrative and Comparative Biology, the Tinker Foundation, and the Mansfield and Columbus campuses at The Ohio State University. N.A. was supported by Neotropical Primate Conservation through various grants. K.R.A. is supported as a fellow in the Canadian Institute for Advanced Research’s “Humans and the microbiome” program. J.C.B.-M. was supported by funding by the World Wildlife Fund-US (#6573), the Brazilian National Council for Scientific and Technological Development/Conselho Nacional de Desenvolvimento Cietifico e Tecnológico (CNPq) (PQ 1C #304475/2018-1), and Programa Nacional de Pós-Doutorado of the Coordenac¸ão de Aperfeic¸oamento de Pessoal de Ńıvel Superior–Brazil (Brazilian Higher Education Authority)/Comissao de Aperfeic¸oamento de Pessoal de Nival Superior (CAPES) (Finance Code 001; PNPD Grant 2755/2010). S.A.B. received financial support from the Biological Dynamics of Forest Fragments Project, the Smithsonian Tropical Research Institute, Arizona State University, Fulbright/Institute of International Education, the Margot Marsh Biodiversity Foundation, Providing Educational Opportunities, Primate Conservation Inc., the Organization for Tropical Studies, and the American Society of Primatologists. T.S.C. was supported by a scholarship from Fundac¸ão de Amparo à Pesquisa (FUNAPE) and would like to thank the Minerac¸ão Rio do Norte (MRN) for their support. Ó.M.C. was supported by Programa Nacional de Pós-Doutorado of the Coordenac¸ão de Aperfeic¸oamento de Pessoal de Ńıvel Superior–Brazil (Brazilian Higher Education Authority)/CAPES (Finance Code 001; PNPD Grant 2755/2010). C.C.-K. received financial support from The NSF (NSF-BSC-1745371), Yale University MacMillan Center for International Studies, the National Geographic Society (EC-420R-18), The Explorers Club, Yale Institute for Biospheric Studies, Yale University Department of Anthropology, The International Primatological Society, and Primate Conservation Inc. Madagascar Ministry of the Environment and Madagascar National Parks permitted this research. I.C.C. received research support from the NSF (Dissertation Improvement Award Grant BNS-9101520), the National Geographic Society (Grant 4496-91), the Boise Fund of the University of Oxford, a Grant-in-Aid of Research from Sigma Xi–The Scientific Research Society, a Washington University Graduate Fellowship, the St. Louis Rainforest Alliance, and the St. Louis Zoo. L.M.F. was supported by Natural Sciences & Engineering Research Council of Canada, and the Canada Research Chairs Programme. A.M.F. was funded by the Wildlife Conservation Society, Conservation International, the Ruf-ford Foundation, and the Primate Society of Great Britain. R.G.F. was supported by the Fundac¸ão Grupo Boticario (0973-2013-8) and CNPq. I.F. was supported by a scholarship from FUNAPE and would like to thank the MRN for their support. K.S.H. was supported by the Foundation for Wildlife Conservation, the Zoological Society of Milwaukee, Birds Without Borders, the University of Calgary, Athabasca University, and the Natural Sciences and Engineering Research Council of Canada. E.W.H. was supported by Deutsche Forschungsgemeinschaft, Deutscher Akademischer Austauschdienst (DAAD), Universit€atsbund G€ottingen. S.M.H. was supported by the Natural Sciences and Engineering Research Council of Canada, the Philanthropic Educational Organization, Conservation International, and Primate Conservation Inc. S.E.J. was supported by the Natural Sciences and Engineering Research Council of Canada, Conservation International, and Primate Conservation Inc. M.C.L. received funding from the National Science Foundation Graduate Research Fellowship (Award 1650042), University of California, Davis, Bucknell University, a Greenville Zoo Conservation grant, the Pittsburgh Zoo Conservation and Sustainability Fund, Primate Conservation Inc., an International Primatological Society Research Grant, and IDEAWild. F.R.d.M. was support by a scholarship from FUNAPE and would like to thank the MRN for their support. T.H.M. was funded primarily by The Aspinall Foundation through the “Saving Prolemur simus” project, with additional support from Beauval Nature and International Union for Conservation of Nature-“Save Our Species.” L.S.M. was supported by a scholarship from FUNAPE and would like to thank the MRN for their support. M.T.O. was supported in part by the NSF-DDIG (BCS 0851761), the J. William Fulbright Foundation, Sigma Xi, and the School of Human Evolution and Social Change at Arizona State University. B.P.-G. was supported by grants from the Comisión Nacional para el Conocimiento y Uso de la Bioversidad (HK009) and Consejo Nacional de Ciencia y Technología (CONACYT) (J51278), as well as graduate scholarships from CONACYT (2008–2010 and 2018–2021). G.P.-M. was supported by a doctorate and master’s degree scholarship from CONACYT (2007–2010) and by the Academic Division of Biological Sciences of the Universidad Juárez Autónoma de Tabasco. G.P.-M. also thanks the local people from Balancán for their guidance. B.E.R. was supported by funding provided by the Durrell Wildlife Conservation Trust, the Lion Tamarins of Brazil Fund, Margot Marsh Biodiversity Foundation, the Tulsa Zoo, Sigma Xi, and an NSF Research and Training grant to University of Maryland. G.R.-F. was supported by CONACYT Grants J51278, 157656, and CF263958 and by National Geographic Society Grant WW-R008-17. C.J.S. was supported by the Leakey Foundation, NSF-DDIG (BCS-0752683 to C. H. Janson), the National Geographic Society, and the Wenner-Gren Foundation. S.S. was supported by Neotropical Primate Conservation through various grants. P.G.A.d.S.L. received research support from the Fundac¸ão Grupo Boticario (0973-2013-8) and CNPq. A.C.S. was supported by Biotechnology and Biological Sciences Research Council Grant 98/S11498. S.E.S.A. was supported by CONACYT through student Grant 207883. Data were collected with the assistance of Augusto Canul, Eulogio Canul, Juan Canul, and Macedonio Canul. J.P.S.-A. was supported by DAAD, CAPES, and International Primatological Society Conservation grants, and currently supported by Fundac¸ão de Amparo a Ciência e Tecnologia (BFP-0149-2.05/19). V.K.S. was supported by the Coordination of Improvement of Higher Level Personnel (CAPES). K.J.E.S. was supported by Evangelisches Studienwerk Villigst, Uni-versit€at Hamburg, and Kompetenzzentrum Nachhaltige Universit€at, Primate Conservation Inc. (PCI #1542), and the German Academic Exchange Service DAAD. M.P.T. was supported by the American Society of Mammalogists, the Consejo Nacional de Investigaciones Científicas y Técnicas, and IDEAWild. S.V.B. was supported by the National Autonomous University of Mexico (PAPIIT-Project IN200216). Funding Information: T.M.E. was supported by funding from the American Society of Primatologists, Conservation International’s Primate Action Fund, IDEAWild, the Margot Marsh Biodiversity Fund, the Mohamed bin Zayed Species Conservation Fund (Project 11253008), Primate Conservation Inc., and the Primate Society of Great Britain/Knowsley Safari Park. D.B.A. was supported by the National Science Foundation Doctoral Dissertation Improvement Grants (NSF-DDIG) (BCS 1341174), the Animal Behavior Society, the Society for Integrative and Comparative Biology, the Tinker Foundation, and the Mansfield and Columbus campuses at The Ohio State University. N.A. was supported by Neotropical Primate Conservation through various grants. K.R.A. is supported as a fellow in the Canadian Institute for Advanced Research’s “Humans and the microbiome” program. J.C.B.-M. was supported by funding by the World Wildlife Fund-US (#6573), the Brazilian National Council for Scientific and Technological Development/Conselho Nacional de Desenvolvimento Cietifico e Tecnológico (CNPq) (PQ 1C #304475/2018-1), and Programa Nacional de Pós-Doutorado of the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–Brazil (Brazilian Higher Education Authority)/Comissao de Aperfeiçoamento de Pessoal de Nival Superior (CAPES) (Finance Code 001; PNPD Grant 2755/2010). S.A.B. received financial support from the Biological Dynamics of Forest Fragments Project, the Smithsonian Tropical Research Institute, Arizona State University, Fulbright/Institute of International Education, the Margot Marsh Biodiversity Foundation, Providing Educational Opportunities, Primate Conservation Inc., the Organization for Tropical Studies, and the American Society of Primatologists. T.S.C. was supported by a scholarship from Fundação de Amparo à Pesquisa (FUNAPE) and would like to thank the Mineração Rio do Norte (MRN) for their support. Ó.M.C. was supported by Programa Nacional de Pós-Doutorado of the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–Brazil (Brazilian Higher Education Authority)/CAPES (Finance Code 001; PNPD Grant 2755/2010). C.C.-K. received financial support from The NSF (NSF-BSC-1745371), Yale University MacMillan Center for International Studies, the National Geographic Society (EC-420R-18), The Explorers Club, Yale Institute for Biospheric Studies, Yale University Department of Anthropology, The International Primatological Society, and Primate Conservation Inc. Madagascar Ministry of the Environment and Madagascar National Parks permitted this research. I.C.C. received research support from the NSF (Dissertation Improvement Award Grant BNS-9101520), the National Geographic Society (Grant 4496-91), the Boise Fund of the University of Oxford, a Grant-in-Aid of Research from Sigma Xi–The Scientific Research Society, a Washington University Graduate Fellowship, the St. Louis Rainforest Alliance, and the St. Louis Zoo. L.M.F. was supported by Natural Sciences & Engineering Research Council of Canada, and the Canada Research Chairs Programme. A.M.F. was funded by the Wildlife Conservation Society, Conservation International, the Rufford Foundation, and the Primate Society of Great Britain. R.G.F. was supported by the Fundação Grupo Boticario (0973-2013-8) and CNPq. I.F. was supported by a scholarship from FUNAPE and would like to thank the MRN for their support. K.S.H. was supported by the Foundation for Wildlife Conservation, the Zoological Society of Milwaukee, Birds Without Borders, the University of Calgary, Athabasca University, and the Natural Sciences and Engineering Research Council of Canada. E.W.H. was supported by Deutsche Forschungsgemeinschaft, Deutscher Akademischer Austauschdienst (DAAD), Universitätsbund Göttingen. S.M.H. was supported by the Natural Sciences and Engineering Research Council of Canada, the Philanthropic Educational Organization, Conservation International, and Primate Conservation Inc. S.E.J. was supported by the Natural Sciences and Engineering Research Council of Canada, Conservation International, and Primate Conservation Inc. M.C.L. received funding from the National Science Foundation Graduate Research Fellowship (Award 1650042), University of California, Davis, Bucknell University, a Greenville Zoo Conservation grant, the Pittsburgh Zoo Conservation and Sustainability Fund, Primate Conservation Inc., an International Primatological Society Research Grant, and IDEAWild. F.R.d.M. was support by a scholarship from FUNAPE and would like to thank the MRN for their support. T.H.M. was funded primarily by The Aspinall Foundation through the “Saving Prolemur simus” project, with additional support from Beauval Nature and International Union for Conservation of Nature-“Save Our Species.” L.S.M. was supported by a scholarship from FUNAPE and would like to thank the MRN for their support. M.T.O. was supported in part by the NSF-DDIG (BCS 0851761), the J. William Fulbright Foundation, Sigma Xi, and the School of Human Evolution and Social Change at Arizona State University. B.P.-G. was supported by grants from the Comisión Nacional para el Conocimiento y Uso de la Bioversidad (HK009) and Consejo Nacional de Ciencia y Technología (CONACYT) (J51278), as well as graduate scholarships from CONACYT (2008–2010 and 2018–2021). G.P.-M. was supported by a doctorate and master’s degree scholarship from CONACYT (2007–2010) and by the Academic Division of Biological Sciences of the Universidad Juárez Autónoma de Tabasco. G.P.-M. also thanks the local people from Balancán for their guidance. B.E.R. was supported by funding provided by the Durrell Wildlife Conservation Trust, the Lion Tamarins of Brazil Fund, Margot Marsh Biodiversity Foundation, the Tulsa Zoo, Sigma Xi, and an NSF Research and Training grant to University of Maryland. G.R.-F. was supported by CONACYT Grants J51278, 157656, and CF263958 and by National Geographic Society Grant WW-R008-17. C.J.S. was supported by the Leakey Foundation, NSF-DDIG (BCS-0752683 to C. H. Janson), the National Geographic Society, and the Wenner-Gren Foundation. S.S. was supported by Neotropical Primate Conservation through various grants. P.G.A.d.S.L. received research support from the Fundação Grupo Boticario (0973-2013-8) and CNPq. A.C.S. was supported by Biotechnology and Biological Sciences Research Council Grant 98/S11498. S.E.S.A. was supported by CONACYT through student Grant 207883. Data were collected with the assistance of Augusto Canul, Eulogio Canul, Juan Canul, and Macedonio Canul. J.P.S.-A. was supported by DAAD, CAPES, and International Primatological Society Conservation grants, and currently supported by Fundação de Amparo a Ciência e Tecnologia (BFP-0149-2.05/19). V.K.S. was supported by the Coordination of Improvement of Higher Level Personnel (CAPES). K.J.E.S. was supported by Evangelisches Studienwerk Villigst, Universität Hamburg, and Kompetenzzentrum Nachhaltige Universität, Primate Conservation Inc. (PCI #1542), and the German Academic Exchange Service DAAD. M.P.T. was supported by the American Society of Mammalogists, the Consejo Nacional de Investigaciones Científicas y Técnicas, and IDEAWild. S.V.B. was supported by the National Autonomous University of Mexico (PAPIIT-Project IN200216). Publisher Copyright: Copyright © 2022 the Author(s).

PY - 2022/10/18

Y1 - 2022/10/18

N2 - 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.

AB - 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.

KW - primate communities j primate evolution j evolutionary transitions j niche shift j climate change

UR - http://www.scopus.com/inward/record.url?scp=85139464241&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85139464241&partnerID=8YFLogxK

U2 - 10.1073/pnas.2121105119

DO - 10.1073/pnas.2121105119

M3 - Article

C2 - 36215474

AN - SCOPUS:85139464241

SN - 0027-8424

VL - 119

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 42

M1 - e2121105119

ER -

Factors influencing terrestriality in primates of the Americas and Madagascar

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