Abstract

Tropical forests are known for their high diversity. Yet, forest patches do occur in the tropics where a single tree species is dominant. Such “monodominant” forests are known from all of the main tropical regions. For Amazonia, we sampled the occurrence of monodominance in a massive, basin-wide database of forest-inventory plots from the Amazon Tree Diversity Network (ATDN). Utilizing a simple defining metric of at least half of the trees ≥ 10 cm diameter belonging to one species, we found only a few occurrences of monodominance in Amazonia, and the phenomenon was not significantly linked to previously hypothesized life history traits such wood density, seed mass, ectomycorrhizal associations, or Rhizobium nodulation. In our analysis, coppicing (the formation of sprouts at the base of the tree or on roots) was the only trait significantly linked to monodominance. While at specific locales coppicing or ectomycorrhizal associations may confer a considerable advantage to a tree species and lead to its monodominance, very few species have these traits. Mining of the ATDN dataset suggests that monodominance is quite rare in Amazonia, and may be linked primarily to edaphic factors.

Details

Title
Rarity of monodominance in hyperdiverse Amazonian forests
Author
Hans ter Steege 1   VIAFID ORCID Logo  ; Henkel, Terry W 2 ; Helal, Nora 3 ; Marimon, Beatriz S 4 ; Ben Hur Marimon-Junior 4 ; Huth, Andreas 5 ; Groeneveld, Jürgen 6 ; Sabatier, Daniel 7 ; de Souza Coelho, Luiz 8 ; Diogenes de Andrade Lima Filho 8 ; Salomão, Rafael P 9 ; Iêda Leão Amaral 8 ; Francisca Dionízia de Almeida Matos 8 ; Castilho, Carolina V 10 ; Phillips, Oliver L 11 ; Guevara, Juan Ernesto 12 ; Marcelo de Jesus Veiga Carim 13 ; Dairon Cárdenas López 14 ; Magnusson, William E 15 ; Wittmann, Florian 16 ; Irume, Mariana Victória 8 ; Maria Pires Martins 8 ; José Renan da Silva Guimarães 13 ; Molino, Jean-François 7 ; Bánki, Olaf S 17 ; Fernandez Piedade, Maria Teresa 18 ; Pitman, Nigel C A 19 ; Abel Monteagudo Mendoza 20 ; José Ferreira Ramos 8 ; Bruno Garcia Luize 21 ; Evlyn Márcia Moraes de Leão Novo 22 ; Percy Núñez Vargas 23 ; Thiago Sanna Freire Silva 24 ; Eduardo Martins Venticinque 25 ; Manzatto, Angelo Gilberto 26 ; Neidiane Farias Costa Reis 27 ; Terborgh, John 28 ; Casula, Katia Regina 27 ; Euridice N Honorio Coronado 29 ; Montero, Juan Carlos 30 ; Feldpausch, Ted R 31 ; Duque, Alvaro 32 ; Costa, Flávia R C 8 ; Castaño Arboleda, Nicolás 14 ; Schöngart, Jochen 18 ; Killeen, Timothy J 33 ; Vasquez, Rodolfo 20 ; Bonifacio Mostacedo 34 ; Demarchi, Layon O 18 ; Assis, Rafael L 35 ; Baraloto, Chris 36 ; Engel, Julien 37 ; Petronelli, Pascal 38 ; Castellanos, Hernán 39 ; Marcelo Brilhante de Medeiros 40 ; Quaresma, Adriano 18 ; Marcelo Fragomeni Simon 40 ; Andrade, Ana 41 ; Camargo, José Luís 41 ; Laurance, Susan G W 42 ; Laurance, William F 42 ; Rincón, Lorena M 8 ; Schietti, Juliana 8 ; Sousa, Thaiane R 8 ; Emanuelle de Sousa Farias 43 ; Maria Aparecida Lopes 44 ; Lima Magalhães, José Leonardo 45 ; Henrique Eduardo Mendonça Nascimento 8 ; Helder Lima de Queiroz 46 ; Aymard, Gerardo A, C 47 ; Brienen, Roel 11 ; Cardenas Revilla, Juan David 8 ; Ima Célia Guimarães Vieira 48 ; Bruno Barçante Ladvocat Cintra 49 ; Stevenson, Pablo R 50 ; Yuri Oliveira Feitosa 51 ; Duivenvoorden, Joost F 52 ; Mogollón, Hugo F 53 ; Araujo-Murakami, Alejandro 54 ; Leandro Valle Ferreira 48 ; Lozada, José Rafael 55 ; Comiskey, James A 56 ; de Toledo, José Julio 57 ; Damasco, Gabriel 58 ; Dávila, Nállarett 59 ; Draper, Freddie 60 ; García-Villacorta, Roosevelt 61 ; Lopes, Aline 62 ; Vicentini, Alberto 15 ; Alonso, Alfonso 63 ; Dallmeier, Francisco 63 ; Gomes, Vitor H F 64 ; Lloyd, Jon 65 ; Neill, David 66 ; Daniel Praia Portela de Aguiar 18 ; Arroyo, Luzmila 54 ; Fernanda Antunes Carvalho 67 ; Fernanda Coelho de Souza 68 ; Dário Dantas do Amaral 48 ; Feeley, Kenneth J 69 ; Gribel, Rogerio 70 ; Pansonato, Marcelo Petratti 71 ; Barlow, Jos 72 ; Berenguer, Erika 73 ; Ferreira, Joice 74 ; Fine, Paul V A 58 ; Marcelino Carneiro Guedes 75 ; Jimenez, Eliana M 76 ; Licona, Juan Carlos 77 ; Peñuela Mora, Maria Cristina 78 ; Villa, Boris 18 ; Cerón, Carlos 79 ; Maas, Paul 80 ; Silveira, Marcos 81 ; Stropp, Juliana 82 ; Thomas, Raquel 83 ; Baker, Tim R 11 ; Daly, Doug 84 ; Dexter, Kyle G 85 ; Huamantupa-Chuquimaco, Isau 23 ; Milliken, William 86 ; Pennington, Toby 87 ; Marcos Ríos Paredes 88 ; Fuentes, Alfredo 89 ; Klitgaard, Bente 90 ; Pena, José Luis Marcelo 91 ; Peres, Carlos A 92 ; Silman, Miles R 93 ; J Sebastián Tello 94 ; Chave, Jerome 95 ; Fernando Cornejo Valverde 96 ; Anthony Di Fiore 97 ; Renato Richard Hilário 57 ; Phillips, Juan Fernando 98 ; Rivas-Torres, Gonzalo 99 ; van Andel, Tinde R 3 ; Patricio von Hildebrand 100 ; Janaína Costa Noronha 101 ; Edelcilio Marques Barbosa 8 ; Flávia Rodrigues Barbosa 101 ; Luiz Carlos de Matos Bonates 8 ; Rainiellen de Sá Carpanedo 101 ; Hilda Paulette Dávila Doza 88 ; Fonty, Émile 102 ; Ricardo, GómeZárate z 103 ; Gonzales, Therany 104 ; George Pepe Gallardo Gonzales 88 ; Hoffman, Bruce 105 ; André Braga Junqueira 106 ; Malhi, Yadvinder 107 ; Ires Paula de Andrade Miranda 8 ; Linder Felipe Mozombite Pinto 88 ; Prieto, Adriana 108 ; Domingos de Jesus Rodrigues 101 ; Rudas, Agustín 108 ; Ruschel, Ademir R 74 ; Silva, Natalino 109 ; Vela, César I A 110 ; Vos, Vincent Antoine 111 ; Zent, Egleé L 112 ; Zent, Stanford 112 ; Bianca Weiss Albuquerque 18 ; Cano, Angela 113 ; Yrma Andreina Carrero Márquez 55 ; Correa, Diego F 114 ; Janaina Barbosa Pedrosa Costa 75 ; Bernardo Monteiro Flores 115 ; Galbraith, David 11 ; Holmgren, Milena 116 ; Kalamandeen, Michelle 11 ; Marcelo Trindade Nascimento 117 ; Oliveira, Alexandre A 118 ; Ramirez-Angulo, Hirma 119 ; Rocha, Maira 18 ; Veridiana Vizoni Scudeller 120 ; Sierra, Rodrigo 121 ; Tirado, Milton 121 ; Maria Natalia Umaña Medina 122 ; Geertje van der Heijden 123 ; Emilio Vilanova Torre 124 ; Vriesendorp, Corine 19 ; Wang, Ophelia 125 ; Young, Kenneth R 126 ; Manuel Augusto Ahuite Reategui 127 ; Baider, Cláudia 128 ; Balslev, Henrik 129 ; Cárdenas, Sasha 50 ; Casas, Luisa Fernanda 50 ; Farfan-Rios, William 93 ; Ferreira, Cid 8 ; Linares-Palomino, Reynaldo 63 ; Mendoza, Casimiro 130 ; Mesones, Italo 58 ; Torres-Lezama, Armando 119 ; Ligia Estela Urrego Giraldo 32 ; Villarroel, Daniel 54 ; Zagt, Roderick 131 ; Alexiades, Miguel N 132 ; Edmar Almeida de Oliveira 4 ; Garcia-Cabrera, Karina 93 ; Hernandez, Lionel 39 ; Walter Palacios Cuenca 133 ; Pansini, Susamar 27 ; Pauletto, Daniela 134 ; Freddy Ramirez Arevalo 135 ; Adeilza Felipe Sampaio 27 ; Valderrama Sandoval, Elvis H 136 ; Luis Valenzuela Gamarra 20 ; Levesley, Aurora 11 ; Pickavance, Georgia 11 ; Melgaço, Karina 11 

1  Biodiversity Dynamics, Naturalis Biodiversity Center, Leiden, RA, The Netherlands; Systems Ecology, Free University, Amsterdam, HV, The Netherlands 
2  Department of Biological Sciences, Humboldt State University, Arcata, CA, USA 
3  Biodiversity Dynamics, Naturalis Biodiversity Center, Leiden, RA, The Netherlands 
4  Programa de Pós-Graduação em Ecologia e Conservação, Universidade do Estado de Mato Grosso, Nova Xavantina, MT, Brazil 
5  Department of Ecological Modelling, Helmholtz Centre for Environmental Research - UFZ, Leipzig, Germany 
6  Department of Ecological Modelling, Helmholtz Centre for Environmental Research - UFZ, Leipzig, Germany; Institute of Forest Growth and Computer Sciences, Technische Universitaet Dresden, Tharandt, Germany 
7  AMAP, IRD, CIRAD, CNRS, INRA, Université de Montpellier, Montpellier, France 
8  Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, AM, Brazil 
9  Programa Professor Visitante Nacional Sênior na Amazônia - CAPES, Universidade Federal Rural da Amazônia, Belém, PA, Brazil; Coordenação de Botânica, Museu Paraense Emílio Goeldi, Belém, PA, Brazil 
10  EMBRAPA – Centro de Pesquisa Agroflorestal de Roraima, Boa Vista, RR, Brazil 
11  School of Geography, University of Leeds, Leeds, UK 
12  Grupo de Investigación en Biodiversidad, Medio Ambiente y Salud-BIOMAS, Universidad de las Américas, Quito, Ecuador; Keller Science Action Center, The Field Museum, Chicago, IL, USA 
13  Departamento de Botânica, Instituto de Pesquisas Científicas e Tecnológicas do Amapá - IEPA, Amapá, Brazil 
14  Herbario Amazónico Colombiano, Instituto SINCHI, Bogotá, DC, Colombia 
15  Coordenação de Pesquisas em Ecologia, Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, AM, Brazil 
16  Dep. of Wetland Ecology, Institute of Geography and Geoecology, Karlsruhe Institute of Technology - KIT, Rastatt, Germany; Biogeochemistry, Max Planck Institute for Chemistry, Mainz, Germany 
17  Naturalis Biodiversity Center, Leiden, RA, The Netherlands 
18  Coordenação de Dinâmica Ambiental, Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, AM, Brazil 
19  Science and Education, The Field Museum, Chicago, IL, USA 
20  Jardín Botánico de Missouri, Oxapampa, Pasco, Peru 
21  Departamento de Ecologia, Universidade Estadual Paulista - UNESP – Instituto de Biociências – IB, Rio Claro, SP, Brazil 
22  Divisao de Sensoriamento Remoto – DSR, Instituto Nacional de Pesquisas Espaciais – INPE, São José dos Campos, SP, Brazil 
23  Herbario Vargas, Universidad Nacional de San Antonio Abad del Cusco, Cusco, Cuzco, Peru 
24  Departamento de Geografia, Universidade Estadual Paulista -UNESP – Instituto de Geociências e Ciências Extas – IGCE, Bela Vista, Rio Claro, SP, Brazil 
25  Centro de Biociências, Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil 
26  Departamento de Biologia, Universidade Federal de Rondônia, Porto Velho, RO, Brazil 
27  Programa de Pós- Graduação em Biodiversidade e Biotecnologia PPG- Bionorte, Universidade Federal de Rondônia, Porto Velho, RO, Brazil 
28  Department of Biology and Florida Museum of Natural History, University of Florida, Gainesville, FL, USA; Centre for Tropical Environmental and Sustainability Science and College of Science and Engineering, James Cook University, Cairns, Queensland, Australia 
29  Instituto de Investigaciones de la Amazonía Peruana (IIAP), Iquitos, Loreto, Peru; School of Geography, University of Leeds, Leeds, UK 
30  Instituto Boliviano de Investigacion Forestal, Santa Cruz, Santa Cruz, Bolivia; Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, AM, Brazil 
31  Geography, College of Life and Environmental Sciences, University of Exeter, Exeter, UK; School of Geography, University of Leeds, Leeds, UK 
32  Departamento de Ciencias Forestales, Universidad Nacional de Colombia, Medellín, Antioquia, Colombia 
33  Agteca-Amazonica, Santa Cruz, Bolivia 
34  Facultad de Ciencias Agrícolas, Universidad Autónoma Gabriel René Moreno, Santa Cruz, Santa Cruz, Bolivia 
35  Natural History Museum, University of Oslo, Oslo, Norway 
36  International Center for Tropical Botany (ICTB) Department of Biological Sciences, Florida International University, Miami, FL, USA 
37  AMAP, IRD, CIRAD, CNRS, INRA, Université de Montpellier, Montpellier, France; International Center for Tropical Botany (ICTB) Department of Biological Sciences, Florida International University, Miami, FL, USA 
38  Cirad UMR Ecofog, AgrosParisTech, CNRS, INRA, Univ Guyane, Kourou Cedex, France 
39  Centro de Investigaciones Ecológicas de Guayana, Universidad Nacional Experimental de Guayana, Puerto Ordaz, Bolivar, Venezuela 
40  Prédio da Botânica e Ecologia, Embrapa Recursos Genéticos e Biotecnologia, Parque Estação Biológica, Brasilia, DF, Brazil 
41  Projeto Dinâmica Biológica de Fragmentos Florestais, Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, AM, Brazil 
42  Centre for Tropical Environmental and Sustainability Science and College of Science and Engineering, James Cook University, Cairns, Queensland, Australia 
43  Laboratório de Ecologia de Doenças Transmissíveis da Amazônia (EDTA), Instituto Leônidas e Maria Deane, Fiocruz, Manaus, AM, Brazil; Programa de Pós-graduação em Biodiversidade e Saúde, Instituto Oswaldo Cruz - IOC/FIOCRUZ, Pav. Arthur Neiva – Térreo, Rio de Janeiro, RJ, Brazil 
44  Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, PA, Brazil 
45  Programa de Pós-Graduação em Ecologia, Universidade Federal do Pará, Belém, PA, Brazil; Embrapa Amazônia Oriental, Belém, PA, Brazil 
46  Diretoria Técnico-Científica, Instituto de Desenvolvimento Sustentável Mamirauá, Tefé, AM, Brazil 
47  Programa de Ciencias del Agro y el Mar, Herbario Universitario (PORT), UNELLEZ-Guanare, Guanare, Portuguesa, Venezuela 
48  Coordenação de Botânica, Museu Paraense Emílio Goeldi, Belém, PA, Brazil 
49  Coordenação de Dinâmica Ambiental, Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, AM, Brazil; School of Geography, University of Leeds, Leeds, UK 
50  Laboratorio de Ecología de Bosques Tropicales y Primatología, Universidad de los Andes, Bogotá, DC, Colombia 
51  Programa de Pós-Graduação em Biologia (Botânica), Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, AM, Brazil 
52  Institute of Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, XH, The Netherlands 
53  Endangered Species Coalition, Silver Spring, MD, USA 
54  Museo de Historia Natural Noel Kempff Mercado, Universidad Autónoma Gabriel Rene Moreno, Santa Cruz, Santa Cruz, Bolivia 
55  Facultad de Ciencias Forestales y Ambientales, Instituto de Investigaciones para el Desarrollo Forestal, Universidad de los Andes, Mérida, Mérida, Venezuela 
56  Inventory and Monitoring Program, Fredericksburg, VA, USA; Center for Conservation and Sustainability, Smithsonian Conservation Biology Institute, Washington, DC, USA 
57  Universidade Federal do Amapá, Ciências Ambientais, Macapá, AP, Brazil 
58  Department of Integrative Biology, University of California, Berkeley, CA, USA 
59  Biologia Vegetal, Universidade Estadual de Campinas, Campinas, SP, Brazil 
60  Department of Global Ecology, Carnegie Institution for Science, Stanford, CA, USA; International Center for Tropical Botany (ICTB) Department of Biological Sciences, Florida International University, Miami, FL, USA 
61  Institute of Molecular Plant Sciences, University of Edinburgh, Edinburgh, UK; Tropical Diversity Section, Royal Botanic Garden Edinburgh, Edinburgh, Scotland, UK 
62  Coordenação de Dinâmica Ambiental, Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, AM, Brazil; Department of Ecology, University of Brasilia, Brasilia, DF, Brazil 
63  Center for Conservation and Sustainability, Smithsonian Conservation Biology Institute, Washington, DC, USA 
64  Coordenação de Botânica, Museu Paraense Emílio Goeldi, Belém, PA, Brazil; Programa de Pós-Graduação em Ciência Ambientais, Universidade Federal do Pará, Belém, PA, Brazil 
65  Faculty of Natural Sciences, Department of Life Sciences, Imperial College London, London, UK 
66  Ecosistemas, Biodiversidad y Conservación de Especies, Universidad Estatal Amazónica, Puyo, Pastaza, Ecuador 
67  Coordenação de Pesquisas em Ecologia, Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, AM, Brazil; Universidade Federal de Minas Gerais, Instituto de Ciências Biológicas, Departamento de Genética, Ecologia e Evolução, Belo Horizonte, MG, Brazil 
68  Coordenação de Pesquisas em Ecologia, Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, AM, Brazil; School of Geography, University of Leeds, Leeds, UK 
69  Department of Biology, University of Miami, Coral Gables, FL, USA; Fairchild Tropical Botanic Garden, Coral Gables, FL, USA 
70  Diretoria de Pesquisas Científicas, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro, RJ, Brazil 
71  Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, AM, Brazil; Instituto de Biociências - Dept. Ecologia, Universidade de Sao Paulo - USP, Rua do Matão, São Paulo, SP, Brazil 
72  Lancaster Environment Centre, Lancaster University, Lancaster, Lancashire, UK 
73  Environmental Change Institute, University of Oxford, Oxford, Oxfordshire, UK 
74  Embrapa Amazônia Oriental, Belém, PA, Brazil 
75  Empresa Brasileira de Pesquisa Agropecuária, Embrapa Amapá, Macapá, Amapá, Brazil 
76  Grupo de Investigación en Tecnologías de la Información y Medio Ambiente, Instituto Tecnológico de Antioquia - Institución Universitaria, Medellín, Colombia 
77  Instituto Boliviano de Investigacion Forestal, Santa Cruz, Santa Cruz, Bolivia 
78  Universidad Regional Amazónica IKIAM, Tena, Napo, Ecuador 
79  Escuela de Biología Herbario Alfredo Paredes, Universidad Central, Quito, Pichincha, Ecuador 
80  Taxonomy and Systematics, Naturalis Biodiversity Center, Leiden, RA, The Netherlands 
81  Museu Universitário/Centro de Ciências Biológicas e da Natureza/Laboratório de Botânica e Ecologia Vegetal, Universidade Federal do Acre, Rio Branco, AC, Brazil 
82  Institute of Biological and Health Sciences, Federal University of Alagoas, Maceio, AL, Brazil 
83  Iwokrama International Centre for Rainforest Conservation, Georgetown, Guyana 
84  New York Botanical Garden, New York, NY, USA 
85  School of Geosciences, University of Edinburgh, Edinburgh, UK; Tropical Diversity Section, Royal Botanic Garden Edinburgh, Edinburgh, Scotland, UK 
86  Natural Capital and Plant Health, Royal Botanic Gardens, Kew, Richmond, Surrey, UK 
87  Geography, College of Life and Environmental Sciences, University of Exeter, Exeter, UK; Tropical Diversity Section, Royal Botanic Garden Edinburgh, Edinburgh, Scotland, UK 
88  Servicios de Biodiversidad EIRL, Iquitos, Loreto, Peru 
89  Herbario Nacional de Bolivia, Universitario UMSA, La Paz, La Paz, Bolivia; Center for Conservation and Sustainable Development, Missouri Botanical Garden, St. Louis, MO, USA 
90  Department for Identification & Naming, Royal Botanic Gardens, Kew, Richmond, Surrey, UK 
91  Department of Forestry Management, Universidad Nacional Agraria La Molina, Lima, Peru 
92  School of Environmental Sciences, University of East Anglia, Norwich, UK 
93  Biology Department and Center for Energy, Environment and Sustainability, Wake Forest University, Winston Salem, NC, USA 
94  Center for Conservation and Sustainable Development, Missouri Botanical Garden, St. Louis, MO, USA 
95  Laboratoire Evolution et Diversité Biologique, CNRS and Université Paul Sabatier, UMR 5174 EDB, Toulouse, France 
96  Andes to Amazon Biodiversity Program, Madre de Dios, Madre de Dios, Peru 
97  Department of Anthropology, University of Texas at Austin, Austin, TX, USA 
98  Fundación Puerto Rastrojo, Bogotá, DC, Colombia 
99  Colegio de Ciencias Biológicas y Ambientales-COCIBA & Galapagos Institute for the Arts and Sciences-GAIAS, Universidad San Francisco de Quito-USFQ, Quito, Pichincha, Ecuador; Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL, USA 
100  Fundación Estación de Biología, Bogotá, DC, Colombia 
101  ICNHS, Federal University of Mato Grosso, Sinop, MT, Brazil 
102  Direction régionale de la Guyane, ONF, Cayenne, French Guiana; AMAP, IRD, CIRAD, CNRS, INRA, Université de Montpellier, Montpellier, France 
103  PROTERRA, Instituto de Investigaciones de la Amazonía Peruana (IIAP), Iquitos, Loreto, Peru 
104  ACEER Foundation, Puerto Maldonado, Madre de Dios, Peru 
105  Amazon Conservation Team, Paramaribo, Suriname 
106  Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona, Bellaterra, Barcelona, Spain 
107  Environmental Change Institute, Oxford University Centre for the Environment, Dyson Perrins Building, Oxford, England, UK 
108  Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá, DC, Colombia 
109  Instituto de Ciência Agrárias, Universidade Federal Rural da Amazônia, Belém, PA, Brazil 
110  Escuela Profesional de Ingeniería Forestal, Universidad Nacional de San Antonio Abad del Cusco, Puerto Maldonado, Madre de Dios, Peru 
111  Universidad Autónoma del Beni José Ballivián, Riberalta, Beni, Bolivia 
112  Laboratory of Human Ecology, Instituto Venezolano de Investigaciones Científicas - IVIC, Caracas, Caracas, Venezuela 
113  Laboratorio de Ecología de Bosques Tropicales y Primatología, Universidad de los Andes, Bogotá, DC, Colombia; Cambridge University Botanic Garden, 1 Brookside., Cambridge, UK 
114  Laboratorio de Ecología de Bosques Tropicales y Primatología, Universidad de los Andes, Bogotá, DC, Colombia; School of Agriculture and Food Sciences - ARC Centre of Excellence for Environmental Decisions CEED, The University of Queensland, St. Lucia, QLD, Australia 
115  University of Campinas, Plant Biology Department, São Paulo, CEP, Brazil 
116  Resource Ecology Group, Wageningen University & Research, Wageningen, Gelderland, The Netherlands 
117  Laboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense, Campos dos Goyatacazes, RJ, Brazil 
118  Instituto de Biociências - Dept. Ecologia, Universidade de Sao Paulo - USP, Rua do Matão, São Paulo, SP, Brazil 
119  Instituto de Investigaciones para el Desarrollo Forestal (INDEFOR), Universidad de los Andes, Conjunto Forestal, Mérida, Mérida, Venezuela 
120  Departamento de Biologia, Universidade Federal do Amazonas - UFAM – Instituto de Ciências Biológicas – ICB1, Manaus, AM, Brazil 
121  GeoIS, El Día 369y El Telégrafo, 3° Piso, Quito, Pichincha, Ecuador 
122  Laboratorio de Ecología de Bosques Tropicales y Primatología, Universidad de los Andes, Bogotá, DC, Colombia; Department of Biology, University of Maryland, College Park, MD, USA 
123  University of Nottingham, University Park, Nottingham, UK 
124  Instituto de Investigaciones para el Desarrollo Forestal (INDEFOR), Universidad de los Andes, Conjunto Forestal, Mérida, Mérida, Venezuela; School of Environmental and Forest Sciences, University of Washington, Seattle, WA, USA 
125  Environmental Science and Policy, Northern Arizona University, Flagstaff, AZ, USA 
126  Geography and the Environment, University of Texas at Austin, Austin, TX, USA 
127  Medio Ambiente, PLUSPRETOL, Iquitos, Loreto, Peru 
128  The Mauritius Herbarium, Agricultural Services, Ministry of Agro-Industry and Food Security, Reduit, Mauritius; Instituto de Biociências - Dept. Ecologia, Universidade de Sao Paulo - USP, Rua do Matão, São Paulo, SP, Brazil 
129  Department of Bioscience, Aarhus University, Aarhus, Denmark 
130  FOMABO, Manejo Forestal en las Tierras Tropicales de Bolivia, Sacta, Cochabamba, Bolivia; Escuela de Ciencias Forestales (ESFOR), Universidad Mayor de San Simon (UMSS), Sacta, Cochabamba, Bolivia 
131  Tropenbos International, Wageningen, The Netherlands 
132  School of Anthropology and Conservation, University of Kent, Canterbury, Kent, UK 
133  Herbario Nacional del Ecuador, Universidad Técnica del Norte, Quito, Pichincha, Ecuador 
134  Instituto de Biodiversidade e Floresta, Universidade Federal do Oeste do Pará, Santarém, PA, Brazil 
135  Facultad de Biologia, Universidad Nacional de la Amazonia Peruana, Iquitos, Loreto, Peru 
136  Department of Biology, University of Missouri, St. Louis, MO, USA; Facultad de Biologia, Universidad Nacional de la Amazonia Peruana, Iquitos, Loreto, Peru 
Pages
1-15
Publication year
2019
Publication date
Sep 2019
Publisher
Nature Publishing Group
e-ISSN
20452322
Source type
Scholarly Journal
Language of publication
English
DOI
https://doi.org/10.1038/s41598-019-50323-9
ProQuest document ID
2297118321
Copyright
© 2019. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.