Factors influencing terrestriality in primates of the Americas and Madagascar

Author:

Eppley Timothy M.12ORCID,Hoeks Selwyn3,Chapman Colin A.4567ORCID,Ganzhorn Jörg U.8ORCID,Hall Katie9,Owen Megan A.1ORCID,Adams Dara B.1011ORCID,Allgas Néstor12ORCID,Amato Katherine R.13ORCID,Andriamahaihavana McAntonin14,Aristizabal John F.1516ORCID,Baden Andrea L.171819ORCID,Balestri Michela20ORCID,Barnett Adrian A.2122ORCID,Bicca-Marques Júlio César23ORCID,Bowler Mark12425ORCID,Boyle Sarah A.26ORCID,Brown Meredith27,Caillaud Damien28ORCID,Calegaro-Marques Cláudia29,Campbell Christina J.30,Campera Marco20,Campos Fernando A.31ORCID,Cardoso Tatiane S.32ORCID,Carretero-Pinzón Xyomara33ORCID,Champion Jane27,Chaves Óscar M.34ORCID,Chen-Kraus Chloe35ORCID,Colquhoun Ian C.36ORCID,Dean Brittany27,Dubrueil Colin27ORCID,Ellis Kelsey M.37,Erhart Elizabeth M.38ORCID,Evans Kayley J. E.27ORCID,Fedigan Linda M.27ORCID,Felton Annika M.39ORCID,Ferreira Renata G.40ORCID,Fichtel Claudia41ORCID,Fonseca Manuel L.42ORCID,Fontes Isadora P.4344,Fortes Vanessa B.45ORCID,Fumian Ivanyr46,Gibson Dean1,Guzzo Guilherme B.47ORCID,Hartwell Kayla S.2748,Heymann Eckhard W.41ORCID,Hilário Renato R.49ORCID,Holmes Sheila M.50ORCID,Irwin Mitchell T.51ORCID,Johnson Steig E.27,Kappeler Peter M.4152ORCID,Kelley Elizabeth A.53,King Tony545556,Knogge Christoph57ORCID,Koch Flávia41,Kowalewski Martin M.58,Lange Liselot R.5960ORCID,Lauterbur M. Elise6162ORCID,Louis Edward E.63ORCID,Lutz Meredith C.64ORCID,Martínez Jesús6566ORCID,Melin Amanda D.27ORCID,de Melo Fabiano R.6768ORCID,Mihaminekena Tsimisento H.5469ORCID,Mogilewsky Monica S.70,Moreira Leandro S.4668ORCID,Moura Letícia A.6871ORCID,Muhle Carina B.23,Nagy-Reis Mariana B.72,Norconk Marilyn A.73ORCID,Notman Hugh2774ORCID,O’Mara M. Teague757677ORCID,Ostner Julia7879,Patel Erik R.80,Pavelka Mary S. M.27,Pinacho-Guendulain Braulio8182ORCID,Porter Leila M.51,Pozo-Montuy Gilberto8384ORCID,Raboy Becky E.85ORCID,Rahalinarivo Vololonirina86,Raharinoro Njaratiana A.14ORCID,Rakotomalala Zafimahery14,Ramos-Fernández Gabriel8788ORCID,Rasamisoa Delaïd C.1,Ratsimbazafy Jonah69ORCID,Ravaloharimanitra Maholy54,Razafindramanana Josia86,Razanaparany Tojotanjona P.1489,Righini Nicoletta90ORCID,Robson Nicola M.91ORCID,Gonçalves Jonas da Rosa92ORCID,Sanamo Justin93,Santacruz Nicole94,Sato Hiroki95,Sauther Michelle L.96,Scarry Clara J.9798ORCID,Serio-Silva Juan Carlos99ORCID,Shanee Sam100,Lins Poliana G. A. de Souza101ORCID,Smith Andrew C.102ORCID,Smith Aguilar Sandra E.103ORCID,Souza-Alves João Pedro104105ORCID,Stavis Vanessa Katherinne106107ORCID,Steffens Kim J. E.108ORCID,Stone Anita I.109,Strier Karen B.110ORCID,Suarez Scott A.111ORCID,Talebi Maurício112113ORCID,Tecot Stacey R.114ORCID,Tujague M. Paula115116117ORCID,Valenta Kim118ORCID,Van Belle Sarie119,Vasey Natalie270ORCID,Wallace Robert B.6566120ORCID,Welch Gilroy48,Wright Patricia C.121122,Donati Giuseppe20ORCID,Santini Luca123ORCID

Affiliation:

1. Conservation Science and Wildlife Health, San Diego Zoo Wildlife Alliance, Escondido, CA 92027

2. Department of Anthropology, Portland State University, Portland, OR 97201

3. Department of Environmental Science, Radboud Institute for Biological and Environmental Sciences, Radboud University, 6500 GL Nijmegen, The Netherlands

4. Department of Anthropology, Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC 20037

5. Wilson Center, Washington, DC 20004

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

7. Shaanxi Key Laboratory for Animal Conservation, Northwest University, 710069 Xi’an, China

8. Department of Animal Ecology and Conservation, Institute of Zoology, Universität Hamburg, 20146 Hamburg, Germany

9. Sedgwick County Zoo, Wichita, KS 67212

10. Department of Anthropology, The Ohio State University, Columbus, OH 43210

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

12. Asociación Neotropical Primate Conservation Perú, 5N 750 San Martin, Perú

13. Department of Anthropology, Northwestern University, Evanston, IL 60208

14. Mention Zoologie et Biodiversité Animale, Faculté des Sciences, Université d’Antananarivo, 101 Antananarivo, Madagascar

15. Departamento de Ciencias Químico Biológicas, Instituto de Ciencias Biomédicas, Universidad Autónoma de Ciudad Juárez, CP 32310 Ciudad Juárez, México

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

17. Department of Anthropology, Hunter College of City University of New York, New York, NY 10065

18. Department of Anthropology, The Graduate Center of City University of New York, New York, NY 10016

19. The New York Consortium in Evolutionary Primatology, New York, NY 10024

20. Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, United Kingdom

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

22. Department of Zoology, Federal University of Pernambuco, Recife-PE 50670-901, Brazil

23. Laboratório de Primatologia, Escola de Ciências da Saúde e da Vida, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre-RS 90619-900, Brazil

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

25. Suffolk Sustainability Institute, Ipswich IP4 1QJ, United Kingdom

26. Department of Biology, Rhodes College, Memphis, TN 38112

27. Department of Anthropology & Archaeology, University of Calgary, Calgary, AB T2N 1N4, Canada

28. Department of Anthropology, University of California, Davis, CA 95616

29. Departamento de Zoologia, Universidade Federal do Rio Grande do Sul, Porto Alegre-RS 90650-001, Brazil

30. Department of Anthropology, California State University Northridge, Northridge, CA 91325

31. Department of Anthropology, University of Texas at San Antonio, San Antonio, TX 78249

32. Coordenação de Ciências da Terra e Ecologia, Museu Paraense Emílio Goeldi, Belém-PA 66077-830, Brazil

33. Proyecto Zocay, Villavicencio, Colombia

34. Escuela de Biología, Universidad de Costa Rica, San José 11501-2060, Costa Rica

35. Department of Anthropology, Yale University, New Haven, CT 06511

36. Department of Anthropology and The Centre for Environment & Sustainability, University of Western Ontario, London, ON N6A 3K7, Canada

37. Department of Anthropology, Miami University, Oxford, OH 45056

38. Department of Anthropology, Texas State University, San Marcos, TX 78666

39. Southern Swedish Forest Research Centre, Swedish University of Agricultural Sciences, SE-230 53 Alnarp, Sweden

40. Pós-Graduação em Psicobiologia, Universidade Federal do Rio Grande do Norte, Natal-RN 59078-970, Brazil

41. Behavioral Ecology and Sociobiology Unit, German Primate Center, 37077 Göttingen, Germany

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

43. Programa de Pós-graduação em Desenvolvimento e Meio Ambiente, Universidade Federal de Sergipe, São Cristóvão-SE 49100-000, Brazil

44. Secretaria Municipal de Meio Ambiente, Aracaju-SE 49015-190, Brazil

45. Laboratório de Primatologia, Departamento de Zootecnia e Ciências Biológicas, Universidade Federal de Santa Maria, Palmeira das Missões-RS 98300-000, Brazil

46. Fundação de Apoio à Pesquisa, Universidade Federal de Goiás, Goiânia-GO 74690-612, Brazil

47. Museu de Ciências Naturais, Universidade de Caxias do Sul, Caxias do Sul-RS 95070-560, Brazil

48. Foundation for Wildlife Conservation, Bainbridge Island, WA 98110

49. Departamento de Meio Ambiente e Desenvolvimento, Universidade Federal do Amapá, Macapá-AP 68903-419, Brazil

50. Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden

51. Department of Anthropology, Northern Illinois University, DeKalb, IL 60115

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

53. Saint Louis Zoo, Saint Louis, MO 63110

54. The Aspinall Foundation, 101 Antananarivo, Madagascar

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

56. Durrell Institute of Conservation and Ecology, School of Anthropology and Conservation, University of Kent, Canterbury CT2 7NZ, United Kingdom

57. Instituto de Pesquisas Ecológicas, Nazaré Paulista-SP 12960-000, Brazil

58. Estacion Biologica Corrientes (CCT Nordeste), Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina, Corrientes W3401XAL, Argentina

59. Association for Research and Conservation in the Amazon, Puerto Maldonado 17001, Madre de Dios, Peru

60. Junglekeepers Peru, Puerto Maldonado 17001, Madre de Dios, Peru

61. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85719

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

63. Grewcock Center for Conservation and Research, Omaha’s Henry Doorly Zoo and Aquarium, Omaha, NE 68107

64. Animal Behavior Graduate Group, University of California, Davis, CA 95616

65. Wildlife Conservation Society, Casilla 3-35181 SM., La Paz, Bolivia

66. Red Boliviana de Primatología, Bolivia

67. Department of Forestry Engineering, Federal University of Viçosa, Viçosa-MG 36570-900, Brazil

68. Muriqui Instituto de Biodiversidade, Caratinga-MG 35300-037, Brazil

69. Groupe d’Etude et de Recherches sur les Primates de Madagascar, 101 Antananarivo, Madagascar

70. School of the Environment, Portland State University, Portland, OR 97201

71. Pós-Graduação em Ciências Biológicas (Biologia Animal), Universidade Federal do Espírito Santo, Vitória-ES 29075-910, Brazil

72. Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, Canada

73. Department of Anthropology, Kent State University, Kent, OH 44240

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

75. Department of Biological Sciences, Southeastern Louisiana University, Hammond, LA 70402

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

77. Smithsonian Tropical Research Institute, 0843-03092 Panamá, República de Panamá

78. Department of Behavioral Ecology, University of Goettingen, 37077 Goettingen, Germany

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

80. Lemur Conservation Foundation, Myakka City, FL 34251

81. Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana, 52005 Unidad Lerma, México

82. Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Instituto Politécnico Nacional, Unidad Oaxaca, 71230 Oaxaca, México

83. Conservación de la Biodiversidad del Usumacinta A.C., Balancán, 86990 Tabasco, México

84. Facultad Maya de Estudios Agropecuarios, Universidad Autónoma de Chiapas, 29980 Catazajá, México

85. Department of Biology, University of Maryland, College Park, MD 20742

86. Mention Anthropobiologie et Développement Durable, Faculté des Sciences, University of Antananarivo, 101 Antananarivo, Madagascar

87. Department of Mathematical Modelling of Social Systems, Institute for Research on Applied Mathematics and Systems, Universidad Nacional Autónoma de México, 3000 Mexico City, Mexico

88. Center for Complexity Sciences, Universidad Nacional Autónoma de México, 3000 Mexico City, Mexico

89. Graduate School of Asian and African Area Studies, Kyoto University, Kyoto 615-8510, Japan

90. Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, CP 44100 Guadalajara, Mexico

91. Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom

92. Instituto de Desenvolvimento Sustentável Mamirauá, Tefé-AM 69553-225, Brazil

93. Département Sciences de la Nature et de l’Environnement, Facultés des Sciences, Université d’Antsiranana, 201 Antsiranana, Madagascar

94. College of Veterinary Medicine, Cornell University, Ithaca, NY 14853

95. Primate Research Institute, Kyoto University, Aichi 484-8506, Japan

96. Department of Anthropology, University of Colorado-Boulder, Boulder, CO 80302

97. Department of Anthropology, California State University, Sacramento, CA 95819

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

99. Red de Biología y Conservación de Vertebrados, Instituto de Ecología AC, 91070 Xalapa, Mexico

100. Neotropical Primate Conservation, Seaton PL11 3JQ, United Kingdom

101. Pós-Graduação em Ecologia e Conservação da Biodiversidade, Universidade Federal do Mato Grosso, Cuiabá-MT 78060-900, Brazil

102. School of Life Sciences, Anglia Ruskin University, Cambridge CB1 1PT, United Kingdom

103. Instituto de Investigaciones Sociológicas, Universidad Autónoma Benito Juárez de Oaxaca, 68120 Oaxaca, Mexico

104. Departamento de Zoologia, Universidade Federal de Pernambuco, Recife-PE 50670-901, Brazil

105. Laboratório de Ecologia, Comportamento e Conservação, Universidade Federal de Pernambuco, Recife-PE 50670-901, Brazil

106. 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

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

108. Department of Biology, Institute of Zoology, Universität Hamburg, 20146 Hamburg, Germany

109. Biology Department, California Lutheran University, Thousand Oaks, CA 91360

110. Department of Anthropology, University of Wisconsin–Madison, Madison, WI 53706

111. Department of Behavioral Sciences, San Diego Mesa College, San Diego, CA 92111

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

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

114. School of Anthropology, University of Arizona, Tucson, AZ 85719

115. Facultad de Ciencias Forestales, Universidad Nacional de Misiones, CP 3380 Misiones, Argentina

116. Instituto de Biología Subtropical, Consejo Nacional de Investigaciones Científicas y Técnicas, Puerto Iguazú, 3370 Misiones, Argentina

117. Asociación Civil Centro de Investigaciones del Bosque Atlántico, Puerto Iguazú, 3370 Misiones, Argentina

118. Department of Anthropology, University of Florida, Gainesville, FL 32603

119. Department of Anthropology, University of Austin at Texas, Austin, TX 78712

120. Wildlife Conservation Society, Bronx, NY 10460

121. Department of Anthropology, Stony Brook University, Stony Brook, NY 11794

122. Centre ValBio, Ranomafana, Ifanadiana 312, Madagascar

123. Department of Biology and Biotechnology “Charles Darwin”, Sapienza University of Rome, 00185 Rome, Italy

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.

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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