Evolutionary diversity is associated with wood productivity in Amazonian forests.


Journal

Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577

Informations de publication

Date de publication:
12 2019
Historique:
received: 03 09 2018
accepted: 16 09 2019
pubmed: 13 11 2019
medline: 18 12 2019
entrez: 13 11 2019
Statut: ppublish

Résumé

Higher levels of taxonomic and evolutionary diversity are expected to maximize ecosystem function, yet their relative importance in driving variation in ecosystem function at large scales in diverse forests is unknown. Using 90 inventory plots across intact, lowland, terra firme, Amazonian forests and a new phylogeny including 526 angiosperm genera, we investigated the association between taxonomic and evolutionary metrics of diversity and two key measures of ecosystem function: aboveground wood productivity and biomass storage. While taxonomic and phylogenetic diversity were not important predictors of variation in biomass, both emerged as independent predictors of wood productivity. Amazon forests that contain greater evolutionary diversity and a higher proportion of rare species have higher productivity. While climatic and edaphic variables are together the strongest predictors of productivity, our results show that the evolutionary diversity of tree species in diverse forest stands also influences productivity. As our models accounted for wood density and tree size, they also suggest that additional, unstudied, evolutionarily correlated traits have significant effects on ecosystem function in tropical forests. Overall, our pan-Amazonian analysis shows that greater phylogenetic diversity translates into higher levels of ecosystem function: tropical forest communities with more distantly related taxa have greater wood productivity.

Identifiants

pubmed: 31712699
doi: 10.1038/s41559-019-1007-y
pii: 10.1038/s41559-019-1007-y
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1754-1761

Références

Maherali, H. & Klironomos, J. N. Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316, 1746–1749 (2007).
pubmed: 17588930
Cadotte, M. W. Experimental evidence that evolutionarily diverse assemblages result in higher productivity. Proc. Natl Acad. Sci. USA 110, 8996–9000 (2013).
pubmed: 23674676
Cadotte, M. W., Cavender-Bares, J., Tilman, D. & Oakley, T. H. Using phylogenetic, functional and trait diversity to understand patterns of plant community productivity. PLoS ONE 4, e5695 (2009).
pubmed: 19479086 pmcid: 2682649
Cadotte, M. W., Cardinale, B. J. & Oakley, T. H. Evolutionary history and the effect of biodiversity on plant productivity. Proc. Natl Acad. Sci. USA 105, 17012–17017 (2008).
pubmed: 18971334
Srivastava, D. S., Cadotte, M. W., Macdonald, A. A. M., Marushia, R. G. & Mirotchnick, N. Phylogenetic diversity and the functioning of ecosystems. Ecol. Lett. 15, 637–648 (2012).
pubmed: 22583836
Cadotte, M. W. Phylogenetic diversity and productivity: gauging interpretations from experiments that do not manipulate phylogenetic diversity. Funct. Ecol. 29, 1603–1606 (2015).
Cadotte, M. W. Phylogenetic diversity–ecosystem function relationships are insensitive to phylogenetic edge lengths. Funct. Ecol. 29, 718–723 (2015).
Davies, T. J., Urban, M. C., Rayfield, B., Cadotte, M. W. & Peres-Neto, P. R. Deconstructing the relationships between phylogenetic diversity and ecology: a case study on ecosystem functioning. Ecology 97, 2212–2222 (2016).
pubmed: 27859062
Venail, P. et al. Species richness, but not phylogenetic diversity, influences community biomass production and temporal stability in a re-examination of 16 grassland biodiversity studies. Funct. Ecol. 29, 615–626 (2015).
Coelho de Souza, F. et al. Evolutionary heritage influences Amazon tree ecology. Proc. R. Soc. B Biol. Sci. 283, 20161587 (2016).
Webb, C. O., Ackerly, D. D., Mcpeek, M. A. & Donoghue, M. J. Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33, 475–505 (2002).
Webb, C. O. & Losos, A. E. J. B. Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am. Nat. 156, 145–155 (2000).
pubmed: 10856198
Chave, J. et al. Regional and phylogenetic variation of wood density across 2456 neotropical tree species. Ecol. Appl. 16, 2356–2367 (2006).
pubmed: 17205910
Baraloto, C. et al. Decoupled leaf and stem economics in rain forest trees. Ecol. Lett. 13, 1338–1347 (2010).
pubmed: 20807232
Fauset, S. et al. Hyperdominance in Amazonian forest carbon cycling. Nat. Commun. 6, 6857 (2015).
pubmed: 25919449 pmcid: 4423203
Faith, D. P. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10 (1992).
Tucker, C. M. et al. A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol. Rev. 92, 698–715 (2016).
pubmed: 26785932
Cadotte, M., Albert, C. H. & Walker, S. C. The ecology of differences: assessing community assembly with trait and evolutionary distances. Ecol. Lett. 16, 1234–1244 (2013).
pubmed: 23910526
Swenson, N. G. Phylogenetic resolution and quantifying the phylogenetic diversity and dispersion of communities. PLoS ONE 4, e4390 (2009).
pubmed: 19194509 pmcid: 2633039
Honorio Coronado, E. N. et al. Phylogenetic diversity of Amazonian tree communities. Divers. Distrib. 21, 1295–1307 (2015).
Ter Steege, H. et al. Hyperdominance in the Amazonian tree flora. Science 342, 1243092 (2013).
pubmed: 24136971
Beer, C. et al. Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329, 834–838 (2010).
pubmed: 20603496
Malhi, Y. et al. The regional variation of aboveground live biomass in old-growth Amazonian forests. Glob. Change Biol. 12, 1107–1138 (2006).
Forest, F. et al. Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445, 757–760 (2007).
pubmed: 17301791
Quesada, C. A. et al. Basin-wide variations in Amazon forest structure and function are mediated by both soils and climate. Biogeosciences 9, 2203–2246 (2012).
Sullivan, M. J. P. et al. Diversity and carbon storage across the tropical forest biome. Sci. Rep. 7, 39102 (2017).
pubmed: 28094794 pmcid: 5240619
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).
Quesada, C. A. et al. Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences 7, 1515–1541 (2010).
Chave, J. et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009).
pubmed: 19243406
Voskamp, A., Baker, D. J., Stephens, P. A., Valdes, P. J. & Willis, S. G. Global patterns in the divergence between phylogenetic diversity and species richness in terrestrial birds. J. Biogeogr. 44, 709–721 (2017).
Dexter, K. & Chave, J. Evolutionary patterns of range size, abundance and species richness in Amazonian angiosperm trees. PeerJ 4, e2402 (2016).
pubmed: 27651991 pmcid: 5018673
Baraloto, C. et al. Using functional traits and phylogenetic trees to examine the assembly of tropical tree communities. J. Ecol. 100, 690–701 (2012).
Magurran, A. E. Measuring Biological Diversity (Blackwell Science, 2004).
Reich, P. B. Key canopy traits drive forest productivity. Proc. R. Soc. B Biol. Sci. 279, 2128–2134 (2012).
Williams, L. J., Paquette, A., Cavender-Bares, J., Messier, C. & Reich, P. B. Spatial complementarity in tree crowns explains overyielding in species mixtures. Nat. Ecol. Evol. 1, 0063 (2017).
Jucker, T., Bouriaud, O. & Coomes, D. A. Crown plasticity enables trees to optimize canopy packing in mixed-species forests. Funct. Ecol. 29, 1078–1086 (2015).
Pretzsch, H. Canopy space filling and tree crown morphology in mixed-species stands compared with monocultures. For. Ecol. Manage. 327, 251–264 (2014).
Goodman, R. C., Phillips, O. L. & Baker, T. R. The importance of crown dimensions to improve tropical tree biomass estimates. Ecol. Appl. 24, 680–698 (2014).
pubmed: 24988768
Goodman, R. C., Phillips, O. L. & Baker, T. R. Dryad Data from: The importance of crown dimensions to improve tropical tree biomass estimates. Dryad Digital Repository https://doi.org/10.5061/dryad.p281g (2013).
Parker, I. M. et al. Phylogenetic structure and host abundance drive disease pressure in communities. Nature 520, 542–544 (2015).
pubmed: 25903634
Gilbert, G. S. & Parker, I. M. The evolutionary ecology of plant disease: a phylogenetic perspective. Annu. Rev. Phytopathol. 54, 549–578 (2016).
pubmed: 27359365
Fine, P. V., Mesones, I. & Coley, P. D. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305, 663–665 (2004).
pubmed: 15286371
Forrister, D. L., Endara, M.-J., Younkin, G. C., Coley, P. D. & Kursar, T. A. Herbivores as drivers of negative density dependence in tropical forest saplings. Science 363, 1213–1216 (2019).
pubmed: 30872524
Eichenberg, D. et al. Impacts of species richness on productivity in a large-scale subtropical forest experiment. Science 362, 80–83 (2018).
pubmed: 30287660
Satdichanh, M. et al. Phylogenetic diversity correlated with above-ground biomass production during forest succession: evidence from tropical forests in Southeast Asia. J. Ecol. 107, 1419–1432 (2018).
Cavanaugh, K. C. et al. Carbon storage in tropical forests correlates with taxonomic diversity and functional dominance on a global scale. Glob. Ecol. Biogeogr. 23, 563–573 (2014).
Poorter, L. et al. Diversity enhances carbon storage in tropical forests. Glob. Ecol. Biogeogr. 24, 1314–1328 (2015).
Sande, M. T. et al. Biodiversity in species, traits, and structure determines carbon stocks and uptake in tropical forests. Biotropica 49, 593–603 (2017).
Johnson, M. O. et al. Variation in stem mortality rates determines patterns of above-ground biomass in Amazonian forests: implications for dynamic global vegetation models. Glob. Change Biol. 22, 3996–4013 (2016).
Chao, K. J. et al. Growth and wood density predict tree mortality in Amazon forests. J. Ecol. 96, 281–292 (2008).
Lopez-Gonzalez, G., Lewis, S. L., Burkitt, M. & Phillips, O. L. ForestPlots.net: a web application and research tool to manage and analyse tropical forest plot data. J. Veg. Sci. 22, 610–613 (2011).
Lopez-Gonzalez G., Simon L. L., Mark B., Baker P. J. & Oliver L. P. ForestPlots.net (2009); www.forestplots.net
Forrestel, E. J. et al. Different clades and traits yield similar grassland functional responses. Proc. Natl Acad. Sci. USA 114, 705–710 (2017).
pubmed: 28074042
Dexter, K. G. et al. Dispersal assembly of rain forest tree communities across the Amazon basin. Proc. Natl Acad. Sci. USA 114, 2645–2650 (2017).
pubmed: 28213498
Boyle, B. et al. The taxonomic name resolution service: an online tool for automated standardization of plant names. BMC Bioinformatics 14, 16 (2013).
pubmed: 23324024 pmcid: 3554605
Gonzalez, M. A. et al. Identification of Amazonian trees with DNA barcodes. PLoS ONE 4, e7483 (2009).
pubmed: 19834612 pmcid: 2759516
Lewis, S. L. et al. Tropical forest tree mortality, recruitment and turnover rates: calculation, interpretation and comparison when census intervals vary. J. Ecol. 92, 929–944 (2004).
Talbot, J. et al. Methods to estimate aboveground wood productivity from long-term forest inventory plots. For. Ecol. Manage. 320, 30–38 (2014).
Lewis, S. L. et al. Increasing carbon storage in intact African tropical forests. Nature 457, 1003–1006 (2009).
pubmed: 19225523
Chave, J. et al. Improved allometric models to estimate the aboveground biomass of tropical trees. Glob. Change Biol. 20, 3177–3190 (2014).
Zanne, A. E. et al. Dryad Data from: Towards a worldwide wood economics spectrum. Dryad Digital Repository https://doi.org/10.5061/dryad.234 (2009).
Feldpausch, T. R. et al. Height–diameter allometry of tropical forest trees. Biogeosciences 8, 1081–1106 (2011).
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289–300 (1995).
Ter Steege, H. et al. Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443, 444–447 (2006).
pubmed: 17006512
Kutner, M., Nachtsheim, C., Neter, J. & Li, W. Applied Linear Statistical Models (McGraw-Hill/Irwin, 2004).
Kim, S. ppcor: An R package for a fast calculation to semi-partial correlation coefficients. Commun. Stat. Appl. Methods 22, 665–674 (2015).
pubmed: 26688802 pmcid: 4681537
R. Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014).
Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2009).
Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).
pubmed: 20395285
Lopez-Gonzalez, G., Sullivan, M. & Baker, T. BiomasaFP: tools for analysing data downloaded from ForestPlots.net. R package version 1.1 https://rdrr.io/github/ForestPlots/BiomasaFP/ (2015).
Pinheiro, J. et al. nlme: linear and nonlinear mixed effects models. R package version 3.1-128 https://cran.r-project.org/web/packages/nlme/index.html (2016).
Eva, H. D. et al. The land cover map for South America in the year 2000. GLC2000 Database (European Commission, Joint Research Centre, 2003); https://forobs.jrc.ec.europa.eu/products/glc2000/glc2000.php

Auteurs

Fernanda Coelho de Souza (F)

School of Geography, University of Leeds, Leeds, UK. fecoelhos@gmail.com.

Kyle G Dexter (KG)

School of Geosciences, University of Edinburgh, Edinburgh, UK.
Royal Botanic Garden Edinburgh, Edinburgh, UK.

Oliver L Phillips (OL)

School of Geography, University of Leeds, Leeds, UK.

R Toby Pennington (RT)

Royal Botanic Garden Edinburgh, Edinburgh, UK.
Geography Department, College of Life and Environmental Sciences, University of Exeter, Exeter, UK.

Danilo Neves (D)

Department of Botany, Federal University of Minas Gerais, Belo Horizonte, Brazil.

Martin J P Sullivan (MJP)

School of Geography, University of Leeds, Leeds, UK.

Esteban Alvarez-Davila (E)

Escuela de Ciencias Agropecuarias y Ambientales, Universidad Nacional Abierta y a Distancia, Sede José Celestino Mutis, Bogotá, Colombia.

Átila Alves (Á)

Projeto TEAM-Manaus, Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil.

Ieda Amaral (I)

Projeto TEAM-Manaus, Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil.

Ana Andrade (A)

Biological Dynamics of Forest Fragment Project, INPA and STRI, Manaus, Brazil.

Luis E O C Aragao (LEOC)

Geography Department, College of Life and Environmental Sciences, University of Exeter, Exeter, UK.
National Institute for Space Research, São José dos Campos, Brazil.

Alejandro Araujo-Murakami (A)

Museo de Historia Natural Noel Kempff Mercado, Universidad Autonoma Gabriel Rene Moreno, Santa Cruz, Bolivia.

Eric J M M Arets (EJMM)

Wageningen Environmental Research, Wageningen University and Research, Wageningen, the Netherlands.

Luzmilla Arroyo (L)

Museo de Historia Natural Noel Kempff Mercado, Universidad Autonoma Gabriel Rene Moreno, Santa Cruz, Bolivia.

Gerardo A Aymard C (GA)

UNELLEZ-Guanare, Programa del Agro y del Mar, Herbario Universitario PORT, Mesa de Cavacas, Venezuela.

Olaf Bánki (O)

Naturalis Biodiversity Center, Leiden, the Netherlands.

Christopher Baraloto (C)

International Center for Tropical Botany, Department of Biological Sciences, Florida International University, Miami, FL, USA.

Jorcely G Barroso (JG)

Universidade Federal do Acre, Rio Branco, Brazil.

Rene G A Boot (RGA)

Tropenbos International, Wageningen, the Netherlands.

Roel J W Brienen (RJW)

School of Geography, University of Leeds, Leeds, UK.

Foster Brown (F)

Woods Hole Research Center, Boston, MA, USA.

José Luís C Camargo (JLC)

Biological Dynamics of Forest Fragment Project, INPA and STRI, Manaus, Brazil.

Wendeson Castro (W)

Programa de Pós-Graduação em Ecologia e Manejo de Recursos Naturais, Universidade Federal do Acre, Rio Branco, Brazil.

Jerome Chave (J)

Laboratoire Evolution et Diversité Biologique, Université Toulouse III Paul Sabatier, Toulouse, France.

Alvaro Cogollo (A)

Jardín Botánico de Medellín Joaquín Antonio Uribe, Medellin, Colombia.

James A Comiskey (JA)

National Park Service, Fredericksburg, VA, USA.
Smithsonian Institution, Washington DC, USA.

Fernando Cornejo-Valverde (F)

Proyecto Castaña, Madre de Dios, Peru.

Antonio Lola da Costa (AL)

Centro de Geociencias, Universidade Federal do Para, Belem, Brazil.

Plínio B de Camargo (PB)

Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, São Paulo, Brazil.

Anthony Di Fiore (A)

Department of Anthropology, University of Texas at Austin, Austin, TX, USA.

Ted R Feldpausch (TR)

Geography Department, College of Life and Environmental Sciences, University of Exeter, Exeter, UK.

David R Galbraith (DR)

School of Geography, University of Leeds, Leeds, UK.

Emanuel Gloor (E)

School of Geography, University of Leeds, Leeds, UK.

Rosa C Goodman (RC)

Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, Umeå, Sweden.

Martin Gilpin (M)

School of Geography, University of Leeds, Leeds, UK.

Rafael Herrera (R)

Centro de Ecología, IVIC, Caracas, Venezuela.
Institut für Geographie und Regionalforschung, Univerity of Vienna, Vienna, Austria.

Niro Higuchi (N)

Instituto Nacional de Pesquisas da Amazônia, Manaus, Brasil.

Eurídice N Honorio Coronado (EN)

Instituto de Investigaciones de la Amazonia Peruana, Iquitos, Peru.

Eliana Jimenez-Rojas (E)

Universidad Nacional de Colombia, Bogotá, Colombia.

Timothy J Killeen (TJ)

GTECA-Amazonica, Santa Cruz, Bolivia.

Susan Laurance (S)

Centre for Tropical Environmental and Sustainability Science and College of Science and Engineering, James Cook University, Cairns, Queensland, Australia.

William F Laurance (WF)

Centre for Tropical Environmental and Sustainability Science and College of Science and Engineering, James Cook University, Cairns, Queensland, Australia.

Gabriela Lopez-Gonzalez (G)

School of Geography, University of Leeds, Leeds, UK.

Thomas E Lovejoy (TE)

Environmental Science and Policy Department, George Mason University, Washington DC, USA.

Yadvinder Malhi (Y)

Environmental Change Institute, School of Geography and the Environment, University of Oxford, Oxford, UK.

Beatriz S Marimon (BS)

Universidade do Estado de Mato Grosso, Nova Xavantina, Brazil.

Ben Hur Marimon-Junior (BH)

Universidade do Estado de Mato Grosso, Nova Xavantina, Brazil.

Casimiro Mendoza (C)

Unidad Académica del Trópico, Escuela de Ciencias Forestales, Universidad Mayor de San Simón, Sacta, Bolivia.

Abel Monteagudo-Mendoza (A)

Jardín Botánico de Missouri, Pasco, Peru.

David A Neill (DA)

Facultad de Ingeniería Ambiental, Universidad Estatal Amazónica, Puyo, Ecuador.

Percy Núñez Vargas (PN)

Universidad Nacional San Antonio Abad del Cusco, Cusco, Peru.

Maria C Peñuela Mora (MC)

Universidad Regional Amazónica Ikiam, Tena, Ecuador.

Georgia C Pickavance (GC)

School of Geography, University of Leeds, Leeds, UK.

John J Pipoly (JJ)

Broward County Parks and Recreation Division, Davie, FL, USA.

Nigel C A Pitman (NCA)

Center for Tropical Conservation, Duke University, Durham, NC, USA.

Lourens Poorter (L)

Forest Ecology and Forest Management Group, Wageningen University and Research, Wageningen, the Netherlands.

Adriana Prieto (A)

Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogota, Colombia.

Freddy Ramirez (F)

Universidad Nacional de la Amazonía Peruana, Iquitos, Peru.

Anand Roopsind (A)

Department of Biological Sciences, Boise State University, Boise, ID, USA.

Agustin Rudas (A)

Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogota, Colombia.

Rafael P Salomão (RP)

Museu Paraense Emilio Goeldi, Belém, Brazil.
Universidade Federal Rural da Amazônia, Belém, Brasil.

Natalino Silva (N)

Universidade Federal Rural da Amazônia, Belém, Brasil.

Marcos Silveira (M)

Museu Universitário, Centro de Ciências Biológicas e da Natureza, Universidade Federal do Acre, Rio Branco, Brazil.

James Singh (J)

Guyana Forestry Commission, Georgetown, Guyana.

Juliana Stropp (J)

Institute of Biological and Health Sciences, Federal University of Alagoas Maceio, Maceio, Brazil.

Hans Ter Steege (H)

Naturalis Biodiversity Center, Leiden, the Netherlands.
Systems Ecology, Vrije Universiteit, Amsterdam, the Netherlands.

John Terborgh (J)

Department of Biology and Florida Museum of Natural History, University of Florida, Gainesville, FL, USA.
School of Science and Engineering, James Cook University, Cairns, Queensland, Australia.

Raquel Thomas-Caesar (R)

Iwokrama International Centre for Rainforest Conservation and Development, Georgetown, Guyana.

Ricardo K Umetsu (RK)

Universidade do Estado de Mato Grosso, Nova Xavantina, Brazil.

Rodolfo V Vasquez (RV)

Jardín Botánico de Missouri, Pasco, Peru.

Ima Célia-Vieira (I)

Museu Paraense Emilio Goeldi, Belém, Brazil.

Simone A Vieira (SA)

Núcleo de Estudos e Pesquisas Ambientais, Universidade Estadual de Campinas, Campinas, Brazil.

Vincent A Vos (VA)

Centro de Investigación y Promoción del Campesinado-Regional Norte Amazónico, Riberalta, Bolivia.
Universidad Autónoma del Beni, Riberalta, Bolivia.

Roderick J Zagt (RJ)

Tropenbos International, Wageningen, the Netherlands.

Timothy R Baker (TR)

School of Geography, University of Leeds, Leeds, UK.

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