Rarity of monodominance in hyperdiverse Amazonian forests

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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.

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Most cited references 81

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Diversity in tropical rain forests and coral reefs.

J. H. Connell (1978)

The commonly observed high diversity of trees in tropical rain forests and corals on tropical reefs is a nonequilibrium state which, if not disturbed further, will progress toward a low-diversity equilibrium community. This may not happen if gradual changes in climate favor different species. If equilibrium is reached, a lesser degree of diversity may be sustained by niche diversification or by a compensatory mortality that favors inferior competitors. However, tropical forests and reefs are subject to severe disturbances often enough that equilibrium may never be attained.

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Hyperdominance in the Amazonian tree flora.

Hans ter Steege, Nigel C A Pitman, Daniel Sabatier … (2014)

The vast extent of the Amazon Basin has historically restricted the study of its tree communities to the local and regional scales. Here, we provide empirical data on the commonness, rarity, and richness of lowland tree species across the entire Amazon Basin and Guiana Shield (Amazonia), collected in 1170 tree plots in all major forest types. Extrapolations suggest that Amazonia harbors roughly 16,000 tree species, of which just 227 (1.4%) account for half of all trees. Most of these are habitat specialists and only dominant in one or two regions of the basin. We discuss some implications of the finding that a small group of species--less diverse than the North American tree flora--accounts for half of the world's most diverse tree community.

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The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests.

Richard P Phillips, Edward Brzostek, Meghan G Midgley (2013)

Understanding the context dependence of ecosystem responses to global changes requires the development of new conceptual frameworks. Here we propose a framework for considering how tree species and their mycorrhizal associates differentially couple carbon (C) and nutrient cycles in temperate forests. Given that tree species predominantly associate with a single type of mycorrhizal fungi (arbuscular mycorrhizal (AM) fungi or ectomycorrhizal (ECM) fungi), and that the two types of fungi differ in their modes of nutrient acquisition, we hypothesize that the abundance of AM and ECM trees in a plot, stand, or region may provide an integrated index of biogeochemical transformations relevant to C cycling and nutrient retention. First, we describe how forest plots dominated by AM tree species have nutrient economies that differ in their C-nutrient couplings from those in plots dominated by ECM trees. Secondly, we demonstrate how the relative abundance of AM and ECM trees can be used to estimate nutrient dynamics across the landscape. Finally, we describe how our framework can be used to generate testable hypotheses about forest responses to global change factors, and how these dynamics can be used to develop better representations of plant-soil feedbacks and nutrient constraints on productivity in ecosystem and earth system models. © 2013 The Authors. New Phytologist © 2013 New Phytologist Trust.

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Author and article information

Contributors

Hans ter Steege:

ORCID: http://orcid.org/0000-0002-8738-2659

hans.tersteege@naturalis.nl

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2045-2322

Publication date (Electronic): 25 September 2019

Publication date PMC-release: 25 September 2019

Publication date Collection: 2019

Volume: 9

Electronic Location Identifier: 13822

Affiliations

[1 ]ISNI 0000 0001 2159 802X, GRID grid.425948.6, Biodiversity Dynamics, Naturalis Biodiversity Center, ; PO Box 9517, Leiden, 2300 RA The Netherlands

[2 ]ISNI 0000 0004 1754 9227, GRID grid.12380.38, Systems Ecology, Free University, ; De Boelelaan 1087, Amsterdam, 1081 HV The Netherlands

[3 ]ISNI 0000 0001 2288 5055, GRID grid.257157.3, Department of Biological Sciences, , Humboldt State University, ; 1 Harpst Street, Arcata, CA 95521 USA

[4 ]GRID grid.442109.a, Programa de Pós-Graduação em Ecologia e Conservação, , Universidade do Estado de Mato Grosso, ; Nova Xavantina, MT Brazil

[5 ]ISNI 0000 0004 0492 3830, GRID grid.7492.8, Department of Ecological Modelling, , Helmholtz Centre for Environmental Research - UFZ, ; Permoserstr. 15, Leipzig, 4318 Germany

[6 ]ISNI 0000 0001 2111 7257, GRID grid.4488.0, Institute of Forest Growth and Computer Sciences, Technische Universitaet Dresden, ; Postfach 1117, Tharandt, 1735 Germany

[7 ]ISNI 0000 0001 2160 870X, GRID grid.503016.1, AMAP, IRD, CIRAD, CNRS, INRA, Université de Montpellier, ; TA A-51/PS2, Bd. de la Lironde, A comprehensive, Montpellier, F-34398 France

[8 ]ISNI 0000 0004 0427 0577, GRID grid.419220.c, Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia - INPA, ; Av. André Araújo, 2936, Petrópolis, Manaus, AM 69067-375 Brazil

[9 ]GRID grid.440587.a, Programa Professor Visitante Nacional Sênior na Amazônia - CAPES, Universidade Federal Rural da Amazônia, ; Av. Perimetral, s/n, Belém, PA Brazil

[10 ]ISNI 0000 0001 2175 1274, GRID grid.452671.3, Coordenação de Botânica, Museu Paraense Emílio Goeldi, ; Av. Magalhães Barata 376, C.P. 399, Belém, PA 66040-170 Brazil

[11 ]EMBRAPA – Centro de Pesquisa Agroflorestal de Roraima, BR 174, km 8 – Distrito Industrial, Boa Vista, RR 69301-970 Brazil

[12 ]ISNI 0000 0004 1936 8403, GRID grid.9909.9, School of Geography, University of Leeds, ; Woodhouse Lane, Leeds, LS2 9JT UK

[13 ]GRID grid.442184.f, Grupo de Investigación en Biodiversidad, Medio Ambiente y Salud-BIOMAS, Universidad de las Américas, ; Campus Queri, Quito, Ecuador

[14 ]ISNI 0000 0001 0476 8496, GRID grid.299784.9, Keller Science Action Center, The Field Museum, ; 1400S. Lake Shore Drive, Chicago, IL 60605-2496 USA

[15 ]Departamento de Botânica, Instituto de Pesquisas Científicas e Tecnológicas do Amapá - IEPA, Rodovia JK, Km 10, Campus do IEPA da Fazendinha, Amapá, 68901-025 Brazil

[16 ]ISNI 0000 0001 2104 9506, GRID grid.493190.6, Herbario Amazónico Colombiano, Instituto SINCHI, ; Calle 20 No 5-44, Bogotá, DC Colombia

[17 ]ISNI 0000 0004 0427 0577, GRID grid.419220.c, Coordenação de Pesquisas em Ecologia, Instituto Nacional de Pesquisas da Amazônia - INPA, ; Av. André Araújo, 2936, Petrópolis, Manaus, AM 69067-375 Brazil

[18 ]ISNI 0000 0001 0075 5874, GRID grid.7892.4, Dep. of Wetland Ecology, , Institute of Geography and Geoecology, Karlsruhe Institute of Technology - KIT, ; Josefstr.1, Rastatt, D-76437 Germany

[19 ]ISNI 0000 0004 0491 8257, GRID grid.419509.0, Biogeochemistry, Max Planck Institute for Chemistry, ; Hahn-Meitner Weg 1, Mainz, 55128 Germany

[20 ]ISNI 0000 0001 2159 802X, GRID grid.425948.6, Naturalis Biodiversity Center, ; PO Box 9517, Leiden, 2300 RA The Netherlands

[21 ]ISNI 0000 0004 0427 0577, GRID grid.419220.c, Coordenação de Dinâmica Ambiental, Instituto Nacional de Pesquisas da Amazônia - INPA, ; Av. André Araújo, 2936, Petrópolis, Manaus, AM 69067-375 Brazil

[22 ]ISNI 0000 0001 0476 8496, GRID grid.299784.9, Science and Education, The Field Museum, ; 1400S. Lake Shore Drive, Chicago, IL 60605-2496 USA

[23 ]Jardín Botánico de Missouri, Oxapampa, Pasco Peru

[24 ]ISNI 0000 0001 2188 478X, GRID grid.410543.7, Departamento de Ecologia, , Universidade Estadual Paulista - UNESP – Instituto de Biociências – IB, ; Av. 24A, 1515, Bela Vista, Rio Claro, SP 13506-900 Brazil

[25 ]ISNI 0000 0001 2116 4512, GRID grid.419222.e, Divisao de Sensoriamento Remoto – DSR, Instituto Nacional de Pesquisas Espaciais – INPE, ; Av. dos Astronautas, 1758, Jardim da Granja, São José dos Campos, SP 12227-010 Brazil

[26 ]ISNI 0000 0001 2198 6786, GRID grid.449379.4, Herbario Vargas, Universidad Nacional de San Antonio Abad del Cusco, ; Avenida de la Cultura, Nro 733, Cusco, Cuzco Peru

[27 ]Departamento de Geografia, Universidade Estadual Paulista -UNESP – Instituto de Geociências e Ciências Extas – IGCE, Bela Vista, Rio Claro, SP 13506-900 Brazil

[28 ]ISNI 0000 0000 9687 399X, GRID grid.411233.6, Centro de Biociências, Departamento de Ecologia, , Universidade Federal do Rio Grande do Norte, ; Av. Senador Salgado Filho, 3000, Natal, RN 59072-970 Brazil

[29 ]GRID grid.440563.0, Departamento de Biologia, , Universidade Federal de Rondônia, ; Rodovia BR 364s/n Km 9,5 - Sentido Acre, Unir, Porto Velho, RO 76.824-027 Brazil

[30 ]GRID grid.440563.0, Programa de Pós- Graduação em Biodiversidade e Biotecnologia PPG- Bionorte, Universidade Federal de Rondônia, ; Campus Porto Velho Km 9,5 bairro Rural, Porto Velho, RO 76.824-027 Brazil

[31 ]ISNI 0000 0004 1936 8091, GRID grid.15276.37, Department of Biology and Florida Museum of Natural History, , University of Florida, ; Gainesville, FL 32611 USA

[32 ]ISNI 0000 0004 0474 1797, GRID grid.1011.1, Centre for Tropical Environmental and Sustainability Science and College of Science and Engineering, James Cook University, ; Cairns, Queensland 4870 Australia

[33 ]ISNI 0000 0001 2177 4732, GRID grid.493484.6, Instituto de Investigaciones de la Amazonía Peruana (IIAP), ; Av. A. Quiñones km 2,5, Iquitos, Loreto 784 Peru

[34 ]ISNI 0000 0001 2217 2493, GRID grid.493404.e, Instituto Boliviano de Investigacion Forestal, ; Av. 6 de agosto #28, Km. 14, Doble via La Guardia, Casilla 6204, Santa Cruz, Santa Cruz Bolivia

[35 ]ISNI 0000 0004 1936 8024, GRID grid.8391.3, Geography, College of Life and Environmental Sciences, University of Exeter, ; Rennes Drive, Exeter, EX4 4RJ UK

[36 ]ISNI 0000 0001 0286 3748, GRID grid.10689.36, Departamento de Ciencias Forestales, , Universidad Nacional de Colombia, ; Calle 64 x Cra 65, Medellín, Antioquia 1027 Colombia

[37 ]Agteca-Amazonica, Santa Cruz, Bolivia

[38 ]GRID grid.440538.e, Facultad de Ciencias Agrícolas, Universidad Autónoma Gabriel René Moreno, ; Santa Cruz, Santa Cruz Bolivia

[39 ]ISNI 0000 0004 1936 8921, GRID grid.5510.1, Natural History Museum, University of Oslo, ; Postboks 1172, Oslo, 318 Norway

[40 ]ISNI 0000 0001 2110 1845, GRID grid.65456.34, International Center for Tropical Botany (ICTB) Department of Biological Sciences, Florida International University, ; 11200 SW 8th Street, OE 243, Miami, FL 33199 USA

[41 ]ISNI 0000 0001 2112 9282, GRID grid.4444.0, Cirad UMR Ecofog, AgrosParisTech, CNRS, INRA, Univ Guyane, ; Campus agronomique, Kourou Cedex, 97379 France

[42 ]GRID grid.440751.3, Centro de Investigaciones Ecológicas de Guayana, Universidad Nacional Experimental de Guayana, ; Calle Chile, urbaniz Chilemex, Puerto Ordaz, Bolivar Venezuela

[43 ]ISNI 0000 0004 0541 873X, GRID grid.460200.0, Prédio da Botânica e Ecologia, Embrapa Recursos Genéticos e Biotecnologia, Parque Estação Biológica, ; Av. W5 Norte, Brasilia, DF 70770-917 Brazil

[44 ]ISNI 0000 0004 0427 0577, GRID grid.419220.c, Projeto Dinâmica Biológica de Fragmentos Florestais, Instituto Nacional de Pesquisas da Amazônia - INPA, ; Av. André Araújo, 2936, Petrópolis, Manaus, AM 69067-375 Brazil

[45 ]ISNI 0000 0001 0723 0931, GRID grid.418068.3, Laboratório de Ecologia de Doenças Transmissíveis da Amazônia (EDTA), Instituto Leônidas e Maria Deane, Fiocruz, ; Rua Terezina, 476, Adrianópolis, Manaus, AM 69060-001 Brazil

[46 ]ISNI 0000 0001 0723 0931, GRID grid.418068.3, Programa de Pós-graduação em Biodiversidade e Saúde, Instituto Oswaldo Cruz - IOC/FIOCRUZ, Pav. Arthur Neiva – Térreo, ; Av. Brasil, 4365 – Manguinhos, Rio de Janeiro, RJ 21040-360 Brazil

[47 ]ISNI 0000 0001 2171 5249, GRID grid.271300.7, Instituto de Ciências Biológicas, Universidade Federal do Pará, ; Av. Augusto Corrêa 01, Belém, PA 66075-110 Brazil

[48 ]ISNI 0000 0001 2171 5249, GRID grid.271300.7, Programa de Pós-Graduação em Ecologia, Universidade Federal do Pará, ; Av. Augusto Corrêa 01, Belém, PA 66075-110 Brazil

[49 ]ISNI 0000 0004 0541 873X, GRID grid.460200.0, Embrapa Amazônia Oriental, ; Trav. Dr. Enéas Pinheiro s/no., Belém, PA 66095-100 Brazil

[50 ]ISNI 0000 0004 5899 1409, GRID grid.469355.8, Diretoria Técnico-Científica, Instituto de Desenvolvimento Sustentável Mamirauá, ; Estrada do Bexiga, 2584, Tefé, AM 69470-000 Brazil

[51 ]Programa de Ciencias del Agro y el Mar, Herbario Universitario (PORT), UNELLEZ-Guanare, Guanare, Portuguesa 3350 Venezuela

[52 ]ISNI 0000000419370714, GRID grid.7247.6, Laboratorio de Ecología de Bosques Tropicales y Primatología, Universidad de los Andes, ; Carrera 1 # 18a- 10, Bogotá, DC 111711 Colombia

[53 ]ISNI 0000 0004 0427 0577, GRID grid.419220.c, Programa de Pós-Graduação em Biologia (Botânica), Instituto Nacional de Pesquisas da Amazônia - INPA, ; Av. André Araújo, 2936, Petrópolis, Manaus, AM 69067-375 Brazil

[54 ]ISNI 0000000084992262, GRID grid.7177.6, Institute of Biodiversity and Ecosystem Dynamics, University of Amsterdam, ; Sciencepark 904, Amsterdam, 1098 XH The Netherlands

[55 ]Endangered Species Coalition, 8530 Geren Rd., Silver Spring, MD 20901 USA

[56 ]Museo de Historia Natural Noel Kempff Mercado, Universidad Autónoma Gabriel Rene Moreno, Avenida Irala 565 Casilla Post al 2489, Santa Cruz, Santa Cruz Bolivia

[57 ]ISNI 0000 0004 1937 0853, GRID grid.267525.1, Facultad de Ciencias Forestales y Ambientales, Instituto de Investigaciones para el Desarrollo Forestal, Universidad de los Andes, ; Via Chorros de Milla, 5101 Mérida, Mérida Venezuela

[58 ]Inventory and Monitoring Program, National Park Service, 120 Chatham Lane, Fredericksburg, VA 22405 USA

[59 ]GRID grid.419531.b, Center for Conservation and Sustainability, Smithsonian Conservation Biology Institute, ; 1100 Jefferson Dr. SW, Suite 3123, Washington, DC 20560-0705 USA

[60 ]ISNI 0000 0004 0643 9014, GRID grid.440559.9, Universidade Federal do Amapá, Ciências Ambientais, ; Rod. Juscelino Kubitschek km2, Macapá, AP 68902-280 Brazil

[61 ]ISNI 0000 0001 2181 7878, GRID grid.47840.3f, Department of Integrative Biology, , University of California, ; Berkeley, CA 94720-3140 USA

[62 ]ISNI 0000 0001 0723 2494, GRID grid.411087.b, Biologia Vegetal, Universidade Estadual de Campinas, ; Caixa Postal 6109, Campinas, SP 13.083-970 Brazil

[63 ]ISNI 0000 0004 0618 5819, GRID grid.418000.d, Department of Global Ecology, , Carnegie Institution for Science, ; 260 Panama St., Stanford, CA 94305 USA

[64 ]ISNI 0000 0004 1936 7988, GRID grid.4305.2, Institute of Molecular Plant Sciences, University of Edinburgh, ; Mayfield Rd, Edinburgh, EH3 5LR UK

[65 ]ISNI 0000 0004 0598 2103, GRID grid.426106.7, Tropical Diversity Section, Royal Botanic Garden Edinburgh, ; 20a Inverleith Row, Edinburgh, Scotland EH3 5LR UK

[66 ]ISNI 0000 0001 2238 5157, GRID grid.7632.0, Department of Ecology, , University of Brasilia, ; Brasilia, DF 70904-970 Brazil

[67 ]ISNI 0000 0001 2171 5249, GRID grid.271300.7, Programa de Pós-Graduação em Ciência Ambientais, Universidade Federal do Pará, ; Rua Augusto Corrêa 01, Belém, PA 66075-110 Brazil

[68 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, Faculty of Natural Sciences, Department of Life Sciences, Imperial College London, ; Silwood Park, South Kensington Campus, London, SW7 2AZ UK

[69 ]GRID grid.440858.5, Ecosistemas, Biodiversidad y Conservación de Especies, Universidad Estatal Amazónica, ; Km. 2 1/2 vía a Tena (Paso Lateral), Puyo, Pastaza Ecuador

[70 ]ISNI 0000 0001 2181 4888, GRID grid.8430.f, Universidade Federal de Minas Gerais, Instituto de Ciências Biológicas, Departamento de Genética, Ecologia e Evolução, ; Av. Antônio Carlos, 6627 Pampulha, Belo Horizonte, MG 31270-901 Brazil

[71 ]ISNI 0000 0004 1936 8606, GRID grid.26790.3a, Department of Biology, , University of Miami, ; Coral Gables, FL 33146 USA

[72 ]ISNI 0000 0001 1091 1201, GRID grid.421473.7, Fairchild Tropical Botanic Garden, ; Coral Gables, FL 33156 USA

[73 ]ISNI 0000 0004 0616 3978, GRID grid.452542.0, Diretoria de Pesquisas Científicas, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, ; Rio de Janeiro, RJ Brazil

[74 ]ISNI 0000 0004 1937 0722, GRID grid.11899.38, Instituto de Biociências - Dept. Ecologia, Universidade de Sao Paulo - USP, Rua do Matão, ; Trav. 14, no. 321, Cidade Universitária, São Paulo, SP 05508-090 Brazil

[75 ]ISNI 0000 0000 8190 6402, GRID grid.9835.7, Lancaster Environment Centre, Lancaster University, ; Lancaster, Lancashire LA1 4YQ UK

[76 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, Environmental Change Institute, University of Oxford, ; Oxford, Oxfordshire OX1 3QY UK

[77 ]ISNI 0000 0004 0541 873X, GRID grid.460200.0, Empresa Brasileira de Pesquisa Agropecuária, Embrapa Amapá, ; Rod. Juscelino Kubitschek km 5, Macapá, Amapá 68903-419 Brazil

[78 ]GRID grid.441890.0, Grupo de Investigación en Tecnologías de la Información y Medio Ambiente, Instituto Tecnológico de Antioquia - Institución Universitaria, ; Calle 78B No. 72A-220, Medellín, Colombia

[79 ]ISNI 0000 0004 4909 487X, GRID grid.499611.2, Universidad Regional Amazónica IKIAM, ; Km 7 via Muyuna, Tena, Napo Ecuador

[80 ]Escuela de Biología Herbario Alfredo Paredes, Universidad Central, Ap. Postal 17.01.2177, Quito, Pichincha Ecuador

[81 ]ISNI 0000 0001 2159 802X, GRID grid.425948.6, Taxonomy and Systematics, Naturalis Biodiversity Center, ; PO Box 9517, Leiden, 2300 RA The Netherlands

[82 ]GRID grid.412369.b, Museu Universitário/Centro de Ciências Biológicas e da Natureza/Laboratório de Botânica e Ecologia Vegetal, Universidade Federal do Acre, ; Rio Branco, AC 69915-559 Brazil

[83 ]ISNI 0000 0001 2154 120X, GRID grid.411179.b, Institute of Biological and Health Sciences, Federal University of Alagoas, ; Av. Lourival Melo Mota, s/n, Tabuleiro do Martins, Maceio, AL 57072-970 Brazil

[84 ]Iwokrama International Centre for Rainforest Conservation, Georgetown, Guyana

[85 ]ISNI 0000 0004 1936 762X, GRID grid.288223.1, New York Botanical Garden, ; 2900 Southern Blvd, Bronx, New York, NY 10458-5126 USA

[86 ]ISNI 0000 0004 1936 7988, GRID grid.4305.2, School of Geosciences, University of Edinburgh, ; 201 Crew Building, King’s Buildings, Edinburgh, EH9 3JN UK

[87 ]ISNI 0000 0001 2097 4353, GRID grid.4903.e, Natural Capital and Plant Health, Royal Botanic Gardens, Kew, ; Richmond, Surrey TW9 3AB UK

[88 ]Servicios de Biodiversidad EIRL, Jr. Independencia 405, Iquitos, Loreto 784 Peru

[89 ]ISNI 0000 0001 1955 7325, GRID grid.10421.36, Herbario Nacional de Bolivia, Universitario UMSA, ; Casilla 10077 Correo Central, La Paz, La Paz Bolivia

[90 ]ISNI 0000 0004 0466 5325, GRID grid.190697.0, Center for Conservation and Sustainable Development, Missouri Botanical Garden, ; P.O. Box 299, St. Louis, MO 63166-0299 USA

[91 ]ISNI 0000 0001 2097 4353, GRID grid.4903.e, Department for Identification & Naming, , Royal Botanic Gardens, Kew, ; Richmond, Surrey TW9 3AB UK

[92 ]ISNI 0000 0001 2168 6564, GRID grid.10599.34, Department of Forestry Management, , Universidad Nacional Agraria La Molina, ; Avenido La Molina, Apdo. 456, La Molina, Lima, Peru

[93 ]ISNI 0000 0001 1092 7967, GRID grid.8273.e, School of Environmental Sciences, University of East Anglia, ; Norwich, NR4 7TJ UK

[94 ]ISNI 0000 0001 2185 3318, GRID grid.241167.7, Biology Department and Center for Energy, Environment and Sustainability, Wake Forest University, ; 1834 Wake Forest Rd, Winston Salem, NC 27106 USA

[95 ]ISNI 0000 0004 0383 1272, GRID grid.462594.8, Laboratoire Evolution et Diversité Biologique, CNRS and Université Paul Sabatier, UMR 5174 EDB, ; Toulouse, 31000 France

[96 ]Andes to Amazon Biodiversity Program, Madre de Dios, Madre de Dios Peru

[97 ]ISNI 0000 0004 1936 9924, GRID grid.89336.37, Department of Anthropology, , University of Texas at Austin, ; SAC 5.150, 2201 Speedway Stop C3200, Austin, TX 78712 USA

[98 ]Fundación Puerto Rastrojo, Cra 10 No. 24-76 Oficina 1201, 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

[100 ]ISNI 0000 0004 1936 8091, GRID grid.15276.37, Department of Wildlife Ecology and Conservation, , University of Florida, ; 110 Newins-Ziegler Hall, Gainesville, FL 32611 USA

[101 ]Fundación Estación de Biología, Cra 10 No. 24-76 Oficina 1201, Bogotá, DC Colombia

[102 ]ICNHS, Federal University of Mato Grosso, Av. Alexandre Ferronato 1200, Setor Industrial, Sinop, MT 78.557-267 Brazil

[103 ]Direction régionale de la Guyane, ONF, Cayenne, F-97300 French Guiana

[104 ]ISNI 0000 0001 2177 4732, GRID grid.493484.6, PROTERRA, Instituto de Investigaciones de la Amazonía Peruana (IIAP), ; Av. A. Quiñones km 2,5, Iquitos, Loreto 784 Peru

[105 ]ACEER Foundation, Jirón Cusco No. 370, Puerto Maldonado, Madre de Dios Peru

[106 ]Amazon Conservation Team, Doekhieweg Oost #24, Paramaribo, Suriname

[107 ]GRID grid.7080.f, Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona, ; 08193 Bellaterra, Barcelona Spain

[108 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, Environmental Change Institute, Oxford University Centre for the Environment, Dyson Perrins Building, ; South Parks Road, Oxford, England OX1 3QY UK

[109 ]ISNI 0000 0001 0286 3748, GRID grid.10689.36, Instituto de Ciencias Naturales, Universidad Nacional de Colombia, ; Apartado 7945, Bogotá, DC Colombia

[110 ]GRID grid.440587.a, Instituto de Ciência Agrárias, Universidade Federal Rural da Amazônia, ; Av. Presidente Tancredo Neves 2501, Belém, PA 66.077-830 Brazil

[111 ]ISNI 0000 0001 2198 6786, GRID grid.449379.4, Escuela Profesional de Ingeniería Forestal, Universidad Nacional de San Antonio Abad del Cusco, ; Jirón San Martín 451, Puerto Maldonado, Madre de Dios Peru

[112 ]GRID grid.440545.4, Universidad Autónoma del Beni José Ballivián, ; Campus Universitario Final, Av. Ejercito, Riberalta, Beni Bolivia

[113 ]ISNI 0000 0001 2181 3287, GRID grid.418243.8, Laboratory of Human Ecology, Instituto Venezolano de Investigaciones Científicas - IVIC, ; Ado 20632, Caracas, Caracas 1020 A Venezuela

[114 ]ISNI 0000000121885934, GRID grid.5335.0, Cambridge University Botanic Garden, 1 Brookside., ; Cambridge, CB2 1JE UK

[115 ]ISNI 0000 0000 9320 7537, GRID grid.1003.2, School of Agriculture and Food Sciences - ARC Centre of Excellence for Environmental Decisions CEED, The University of Queensland, ; St. Lucia, QLD 4072 Australia

[116 ]ISNI 0000 0001 0723 2494, GRID grid.411087.b, University of Campinas, Plant Biology Department, ; Rua Monteiro Lobato, 255, Cidade Universitária Zeferino Vaz, Barão Geraldo, Campinas, São Paulo, CEP 13083-862 Brazil

[117 ]ISNI 0000 0001 0791 5666, GRID grid.4818.5, Resource Ecology Group, Wageningen University & Research, ; Droevendaalsesteeg 3a, Lumen, building number 100, Wageningen, Gelderland 6708 PB The Netherlands

[118 ]ISNI 0000 0000 9087 6639, GRID grid.412331.6, Laboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense, ; Av. Alberto Lamego 2000, Campos dos Goyatacazes, RJ 28013-620 Brazil

[119 ]ISNI 0000 0004 1937 0853, GRID grid.267525.1, Instituto de Investigaciones para el Desarrollo Forestal (INDEFOR), Universidad de los Andes, Conjunto Forestal, ; 5101 Mérida, Mérida Venezuela

[120 ]ISNI 0000 0001 2221 0517, GRID grid.411181.c, Departamento de Biologia, , Universidade Federal do Amazonas - UFAM – Instituto de Ciências Biológicas – ICB1, ; Av General Rodrigo Octavio 6200, Manaus, AM 69080-900 Brazil

[121 ]GeoIS, El Día 369y El Telégrafo, 3° Piso, Quito, Pichincha Ecuador

[122 ]ISNI 0000 0001 0941 7177, GRID grid.164295.d, Department of Biology, , University of Maryland, ; College Park, MD 20742 USA

[123 ]ISNI 0000 0004 1936 8868, GRID grid.4563.4, University of Nottingham, University Park, ; Nottingham, NG7 2RD UK

[124 ]ISNI 0000000122986657, GRID grid.34477.33, School of Environmental and Forest Sciences, University of Washington, ; Seattle, WA 98195-2100 USA

[125 ]ISNI 0000 0004 1936 8040, GRID grid.261120.6, Environmental Science and Policy, Northern Arizona University, ; Flagstaff, AZ 86011 USA

[126 ]ISNI 0000 0004 1936 9924, GRID grid.89336.37, Geography and the Environment, University of Texas at Austin, ; 305 E. 23rd Street, CLA building, Austin, TX 78712 USA

[127 ]Medio Ambiente, PLUSPRETOL, Iquitos, Loreto Peru

[128 ]GRID grid.473375.1, The Mauritius Herbarium, Agricultural Services, Ministry of Agro-Industry and Food Security, ; Reduit, 80835 Mauritius

[129 ]ISNI 0000 0001 1956 2722, GRID grid.7048.b, Department of Bioscience, , Aarhus University, ; Building 1540 Ny Munkegade, Aarhus C, Aarhus, DK-8000 Denmark

[130 ]FOMABO, Manejo Forestal en las Tierras Tropicales de Bolivia, Sacta, Cochabamba Bolivia

[131 ]ISNI 0000 0001 2176 4059, GRID grid.10491.3d, Escuela de Ciencias Forestales (ESFOR), Universidad Mayor de San Simon (UMSS), ; Sacta, Cochabamba Bolivia

[132 ]Tropenbos International, Lawickse Allee 11 PO Box 232, Wageningen, 6700 AE The Netherlands

[133 ]ISNI 0000 0001 2232 2818, GRID grid.9759.2, School of Anthropology and Conservation, University of Kent, ; Marlowe Building, Canterbury, Kent CT2 7NR UK

[134 ]GRID grid.440859.4, Herbario Nacional del Ecuador, Universidad Técnica del Norte, ; Quito, Pichincha Ecuador

[135 ]ISNI 0000 0004 0509 0076, GRID grid.448725.8, Instituto de Biodiversidade e Floresta, Universidade Federal do Oeste do Pará, ; Rua Vera Paz, Campus Tapajós, Santarém, PA 68015-110 Brazil

[136 ]GRID grid.440594.8, Facultad de Biologia, Universidad Nacional de la Amazonia Peruana, ; Pevas 5ta cdra, Iquitos, Loreto Peru

[137 ]ISNI 0000 0001 2162 3504, GRID grid.134936.a, Department of Biology, , University of Missouri, ; St. Louis, MO 63121 USA

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Hans ter Steege http://orcid.org/0000-0002-8738-2659

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Publisher ID: 50323

DOI: 10.1038/s41598-019-50323-9

PMC ID: 6761143

PubMed ID: 31554920

SO-VID: 1b2b7b87-c113-4b11-a0a7-9b37816133d5

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Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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Date received : 14 May 2019

Date accepted : 2 September 2019

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Keywords: biodiversity,forest ecology

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ScienceOpen disciplines: Uncategorized

Keywords: biodiversity, forest ecology

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