Functional susceptibility of tropical forests to climate change.
Journal
Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577
Informations de publication
Date de publication:
07 2022
07 2022
Historique:
received:
02
09
2021
accepted:
24
03
2022
pubmed:
17
5
2022
medline:
12
7
2022
entrez:
16
5
2022
Statut:
ppublish
Résumé
Tropical forests are some of the most biodiverse ecosystems in the world, yet their functioning is threatened by anthropogenic disturbances and climate change. Global actions to conserve tropical forests could be enhanced by having local knowledge on the forests' functional diversity and functional redundancy as proxies for their capacity to respond to global environmental change. Here we create estimates of plant functional diversity and redundancy across the tropics by combining a dataset of 16 morphological, chemical and photosynthetic plant traits sampled from 2,461 individual trees from 74 sites distributed across four continents together with local climate data for the past half century. Our findings suggest a strong link between climate and functional diversity and redundancy with the three trait groups responding similarly across the tropics and climate gradient. We show that drier tropical forests are overall less functionally diverse than wetter forests and that functional redundancy declines with increasing soil water and vapour pressure deficits. Areas with high functional diversity and high functional redundancy tend to better maintain ecosystem functioning, such as aboveground biomass, after extreme weather events. Our predictions suggest that the lower functional diversity and lower functional redundancy of drier tropical forests, in comparison with wetter forests, may leave them more at risk of shifting towards alternative states in face of further declines in water availability across tropical regions.
Identifiants
pubmed: 35577983
doi: 10.1038/s41559-022-01747-6
pii: 10.1038/s41559-022-01747-6
doi:
Substances chimiques
Water
059QF0KO0R
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
878-889Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Barlow, J. et al. Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation. Nature 535, 144–147 (2016).
pubmed: 27362236
doi: 10.1038/nature18326
Beech, E., Rivers, M., Oldfield, S. & Smith, P. P. GlobalTreeSearch: the first complete global database of tree species and country distributions. J. Sustain. 36, 454–489 (2017).
doi: 10.1080/10549811.2017.1310049
ter Steege, H. et al. The discovery of the Amazonian tree flora with an updated checklist of all known tree taxa. Sci. Rep. 6, 29549 (2016).
pubmed: 27406027
pmcid: 4942782
doi: 10.1038/srep29549
Hubau, W. et al. Asynchronous carbon sink saturation in African and Amazonian tropical forests. Nature 579, 80–87 (2020).
pubmed: 32132693
doi: 10.1038/s41586-020-2035-0
Pan, Y. et al. A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011).
pubmed: 21764754
doi: 10.1126/science.1201609
Maia, V. A. et al. The carbon sink of tropical seasonal forests in southeastern Brazil can be under threat. Sci. Adv. 6, eabd4548 (2020).
pubmed: 33355136
doi: 10.1126/sciadv.abd4548
Malhi, Y. et al. The regional variation of aboveground live biomass in old‐growth Amazonian forests. Glob. Change Biol. 12, 1107–1138 (2006).
doi: 10.1111/j.1365-2486.2006.01120.x
Phillips, O. L. et al. Drought sensitivity of the Amazon rainforest. Science 323, 1344–1347 (2009).
pubmed: 19265020
doi: 10.1126/science.1164033
Malhi, Y. et al. Climate change, deforestation, and the fate of the Amazon. Science 319, 169–172 (2008).
pubmed: 18048654
doi: 10.1126/science.1146961
Gatti, L. V. et al. Amazonia as a carbon source linked to deforestation and climate change. Nature 595, 388–393 (2021).
pubmed: 34262208
doi: 10.1038/s41586-021-03629-6
Hisano, M., Searle, E. B. & Chen, H. Y. Biodiversity as a solution to mitigate climate change impacts on the functioning of forest ecosystems. Biol. Rev. 93, 439–456 (2018).
pubmed: 28695682
doi: 10.1111/brv.12351
Pecl, G. T. et al. Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355, eaai9214 (2017).
pubmed: 28360268
doi: 10.1126/science.aai9214
Malhi, Y. et al. Exploring the likelihood and mechanism of a climate-change-induced dieback of the Amazon rainforest. Proc. Natl Acad. Sci. USA 106, 20610–20615 (2009).
pubmed: 19218454
pmcid: 2791614
doi: 10.1073/pnas.0804619106
Seager, R. et al. Climatology, variability, and trends in the US vapor pressure deficit, an important fire-related meteorological quantity. J. Appl. Meteorol. Climatol. 54, 1121–1141 (2015).
doi: 10.1175/JAMC-D-14-0321.1
Smith, M. N. et al. Empirical evidence for resilience of tropical forest photosynthesis in a warmer world. Nat. Plants 6, 1225–1230 (2020).
pubmed: 33051618
doi: 10.1038/s41477-020-00780-2
Yuan, W. et al. Increased atmospheric vapor pressure deficit reduces global vegetation growth. Sci. Adv. 5, eaax1396 (2019).
pubmed: 31453338
pmcid: 6693914
doi: 10.1126/sciadv.aax1396
Costa, F. R. C., Schietti, J., Stark, S. C. & Smith, M. N. The other side of tropical forest drought: do shallow water table regions of Amazonia act as large‐scale hydrological refugia from drought?. New Phytol. https://doi.org/10.1111/nph.17914 (2022).
Brodribb, T. J., Powers, J., Cochard, H. & Choat, B. Hanging by a thread? Forests and drought. Science 368, 261–266 (2020).
pubmed: 32299945
doi: 10.1126/science.aat7631
Allen, K. et al. Will seasonally dry tropical forests be sensitive or resistant to future changes in rainfall regimes? Environ. Res. Lett. 12, 023001 (2017).
doi: 10.1088/1748-9326/aa5968
Esquivel‐Muelbert, A. et al. Compositional response of Amazon forests to climate change. Glob. Change Biol. 25, 39–56 (2019).
doi: 10.1111/gcb.14413
Aguirre‐Gutiérrez, J. et al. Drier tropical forests are susceptible to functional changes in response to a long‐term drought. Ecol. Lett. 22, 855–865 (2019).
pubmed: 30828955
doi: 10.1111/ele.13243
Cadotte, M. W., Carscadden, K. & Mirotchnick, N. Beyond species: functional diversity and the maintenance of ecological processes and services. J. Appl. Ecol. 48.5, 1079–1087 (2011).
doi: 10.1111/j.1365-2664.2011.02048.x
Aguirre‐Gutiérrez, J. et al. Butterflies show different functional and species diversity in relationship to vegetation structure and land use. Glob. Ecol. Biogeogr. 26, 1126–1137 (2017).
doi: 10.1111/geb.12622
Arruda Almeida, B. et al. Comparing species richness, functional diversity and functional composition of waterbird communities along environmental gradients in the neotropics. PLoS ONE 13, e0200959 (2018).
pubmed: 30028866
pmcid: 6054399
doi: 10.1371/journal.pone.0200959
Yachi, S. & Loreau, M. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc. Natl Acad. Sci. USA 96, 1463–1468 (1999).
pubmed: 9990046
pmcid: 15485
doi: 10.1073/pnas.96.4.1463
Correia, D. L. P., Raulier, F., Bouchard, M. & Filotas, É. Response diversity, functional redundancy, and post‐logging productivity in northern temperate and boreal forests. Ecol. Appl. 28, 1282–1291 (2018).
pubmed: 29672967
doi: 10.1002/eap.1727
Elmqvist, T. et al. Response diversity, ecosystem change, and resilience. Front. Ecol. Environ. 1, 488–494 (2003).
doi: 10.1890/1540-9295(2003)001[0488:RDECAR]2.0.CO;2
Loreau, M. & de Mazancourt, C. Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol. Lett. 16, 106–115 (2013).
pubmed: 23346947
doi: 10.1111/ele.12073
Petchey, O. L., Evans, K. L., Fishburn, I. S. & Gaston, K. J. Low functional diversity and no redundancy in British avian assemblages. J. Anim. Ecol. 76, 977–985 (2007).
pubmed: 17714276
doi: 10.1111/j.1365-2656.2007.01271.x
Jucker, T. et al. Stabilizing effects of diversity on aboveground wood production in forest ecosystems: linking patterns and processes. Ecol. Lett. 17, 1560–1569 (2014).
pubmed: 25308256
doi: 10.1111/ele.12382
Fonseca, C. R. & Ganade, G. Species functional redundancy, random extinctions and the stability of ecosystems. J. Ecol. 89, 118–125 (2001).
doi: 10.1046/j.1365-2745.2001.00528.x
Aguirre-Gutiérrez, J. et al. Long-term droughts may drive drier tropical forests towards increased functional, taxonomic and phylogenetic homogeneity. Nat. Commun. 11, 3346 (2020).
pubmed: 32620761
pmcid: 7335099
doi: 10.1038/s41467-020-16973-4
Fauset, S. et al. Drought‐induced shifts in the floristic and functional composition of tropical forests in Ghana. Ecol. Lett. 15, 1120–1129 (2012).
pubmed: 22812661
doi: 10.1111/j.1461-0248.2012.01834.x
Laliberté, E. & Legendre, P. A distance‐based framework for measuring functional diversity from multiple traits. Ecology 91, 299–305 (2010).
pubmed: 20380219
doi: 10.1890/08-2244.1
Bauman, D. et al. Tropical tree growth sensitivity to climate is driven by species intrinsic growth rate and leaf traits. Glob. Change Biol. 28, 1414–1432 (2022).
doi: 10.1111/gcb.15982
Quesada, C. et al. Basin-wide variations in Amazon forest structure and function are mediated by both soils and climate. Biogeosciences 9, 2203–2246 (2012).
doi: 10.5194/bg-9-2203-2012
Bennett, A. C. et al. Resistance of African tropical forests to an extreme climate anomaly. Proc. Natl Acad. Sci. USA 118, e2003169118 (2021).
pubmed: 34001597
pmcid: 8166131
doi: 10.1073/pnas.2003169118
Climate Change and Land: An IPCC Special Report on Climate Change, Desertification, Land Degradation, Sustainable Land Management, Food Security, and Greenhouse Gas Fluxes in Terrestrial Ecosystems (eds Shukla, P.R. et al.) (IPCC, 2019).
Ashton, I. W., Miller, A. E., Bowman, W. D. & Suding, K. N. Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91, 3252–3260 (2010).
pubmed: 21141186
doi: 10.1890/09-1849.1
Petchey, O. L. On the statistical significance of functional diversity effects. Funct. Ecol. 18, 297–303 (2004).
doi: 10.1111/j.0269-8463.2004.00852.x
Bruno, J. F., Stachowicz, J. J. & Bertness, M. D. Inclusion of facilitation into ecological theory. Trends Ecol. Evol. 18, 119–125 (2003).
doi: 10.1016/S0169-5347(02)00045-9
ter Steege, H. et al. Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443, 444–447 (2006).
pubmed: 17006512
doi: 10.1038/nature05134
Raes, N. et al. Botanical richness and endemicity patterns of Borneo derived from species distribution models. Ecography 32, 180–192 (2009).
doi: 10.1111/j.1600-0587.2009.05800.x
Shenkin, A. et al. The influence of ecosystem and phylogeny on tropical tree crown size and shape. Front. For. Glob. Change 3, 501757 (2020).
doi: 10.3389/ffgc.2020.501757
Harrison, S., Spasojevic, M. J. & Li, D. Climate and plant community diversity in space and time. Proc. Natl Acad. Sci. USA 117, 4464–4470 (2020).
pubmed: 32071212
pmcid: 7060689
doi: 10.1073/pnas.1921724117
Grossman, J. J., Cavender‐Bares, J., Hobbie, S. E., Reich, P. B. & Montgomery, R. A. Species richness and traits predict overyielding in stem growth in an early‐successional tree diversity experiment. Ecology 98, 2601–2614 (2017).
pubmed: 28727905
doi: 10.1002/ecy.1958
Williams, L. J. et al. Remote spectral detection of biodiversity effects on forest biomass. Nat. Ecol. Evol. 5, 46–54 (2021).
pubmed: 33139920
doi: 10.1038/s41559-020-01329-4
Hutchison, C., Gravel, D., Guichard, F. & Potvin, C. Effect of diversity on growth, mortality, and loss of resilience to extreme climate events in a tropical planted forest experiment. Sci. Rep. 8, 15443 (2018).
pubmed: 30337582
pmcid: 6193960
doi: 10.1038/s41598-018-33670-x
González-M, R. et al. Diverging functional strategies but high sensitivity to an extreme drought in tropical dry forests. Ecol. Lett. 24, 451–463 (2021).
pubmed: 33316132
doi: 10.1111/ele.13659
Hoegh-Guldberg, O. et al. in IPCC Special Report on Global Warming of 1.5 °C (eds Masson-Delmotte, V. et al.) Ch. 3 (WMO, 2018).
de la Riva, E. G. et al. The importance of functional diversity in the stability of Mediterranean shrubland communities after the impact of extreme climatic events. J. Plant Ecol. 10, 281–293 (2017).
Reich, P. B. The world-wide “fast-slow” plant economics spectrum: a traits manifesto. J. Ecol. 102, 275–301 (2014).
doi: 10.1111/1365-2745.12211
Oliveira, R. S. et al. Linking plant hydraulics and the fast–slow continuum to understand resilience to drought in tropical ecosystems. New Phytol. 230, 904–923 (2021).
pubmed: 33570772
doi: 10.1111/nph.17266
Anderegg, W. R. L. & Meinzer, F. C. in Functional and Ecological Xylem Anatomy (ed Hacke, U.) Ch. 9 (Springer, 2015).
Chave, J. et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009).
pubmed: 19243406
doi: 10.1111/j.1461-0248.2009.01285.x
Pratt, R., Jacobsen, A., Ewers, F. & Davis, S. Relationships among xylem transport, biomechanics and storage in stems and roots of nine Rhamnaceae species of the California chaparral. New Phytol. 174, 787–798 (2007).
pubmed: 17504462
doi: 10.1111/j.1469-8137.2007.02061.x
Zanne, A. E. et al. Angiosperm wood structure: global patterns in vessel anatomy and their relation to wood density and potential conductivity. Am. J. Bot. 97, 207–215 (2010).
pubmed: 21622380
doi: 10.3732/ajb.0900178
Bucci, S. J. et al. The stem xylem of Patagonian shrubs operates far from the point of catastrophic dysfunction and is additionally protected from drought‐induced embolism by leaves and roots. Plant Cell Environ. 36, 2163–2174 (2013).
pubmed: 23639077
doi: 10.1111/pce.12126
Meinzer, F. C. et al. Coordination of leaf and stem water transport properties in tropical forest trees. Oecologia 156, 31–41 (2008).
pubmed: 18253753
doi: 10.1007/s00442-008-0974-5
Scholz F. G., Phillips N. G., Bucci S. J., Meinzer F. C. & Goldstein G. in Size- and Age-Related Changes in Tree Structure and Function (eds Meinzer F. C. C. et al.) 341–361 (Springer, 2011).
Mitchell, P. J. et al. Using multiple trait associations to define hydraulic functional types in plant communities of south-western Australia. Oecologia 158, 385–397 (2008).
pubmed: 18839215
doi: 10.1007/s00442-008-1152-5
Villagra, Mariana et al. Functional relationships between leaf hydraulics and leaf economic traits in response to nutrient addition in subtropical tree species. Tree Physiol. 33, 1308–1318 (2013).
pubmed: 24284866
doi: 10.1093/treephys/tpt098
Ishida, Atsushi et al. Coordination between leaf and stem traits related to leaf carbon gain and hydraulics across 32 drought-tolerant angiosperms. Oecologia 156, 193–202 (2008).
pubmed: 18297313
doi: 10.1007/s00442-008-0965-6
Malhi, Y. et al. The Global Ecosystems Monitoring network: monitoring ecosystem productivity and carbon cycling across the tropics. Biol. Conserv. 253, 108889 (2021).
doi: 10.1016/j.biocon.2020.108889
Martin, R. E. et al. Covariance of sun and shade leaf traits along a tropical forest elevation gradient. Front. Plant Sci. 10, 1810 (2020).
pubmed: 32076427
pmcid: 7006543
doi: 10.3389/fpls.2019.01810
Enquist, B. J. et al. Assessing trait‐based scaling theory in tropical forests spanning a broad temperature gradient. Glob. Ecol. Biogeogr. 26, 1357–1373 (2017).
doi: 10.1111/geb.12645
Both, S. et al. Logging and soil nutrients independently explain plant trait expression in tropical forests. New Phytol. 221, 1853–1865 (2019).
pubmed: 30238458
doi: 10.1111/nph.15444
Oliveras, I. et al. The influence of taxonomy and environment on leaf trait variation along tropical abiotic gradients. Front. For. Glob. Change https://doi.org/10.3389/ffgc.2020.00018 (2020).
Gvozdevaite, A. et al. Leaf-level photosynthetic capacity dynamics in relation to soil and foliar nutrients along forest–savanna boundaries in Ghana and Brazil. Tree Physiol. 38, 1912–1925 (2018).
pubmed: 30388271
doi: 10.1093/treephys/tpy117
Aguirre-Gutiérrez, J. et al. Pantropical modelling of canopy functional traits using Sentinel-2 remote sensing data. Remote Sens. Environ. 252, 112122 (2021).
doi: 10.1016/j.rse.2020.112122
Pavoine, S. adiv: an R package to analyse biodiversity in ecology. Methods Ecol. Evol. 11, 1106–1112 (2020).
doi: 10.1111/2041-210X.13430
Pavoine, S. & Ricotta, C. A simple translation from indices of species diversity to indices of phylogenetic diversity. Ecol. Ind. 101, 552–561 (2019).
doi: 10.1016/j.ecolind.2019.01.052
Ricotta, C. et al. Measuring the functional redundancy of biological communities: a quantitative guide. Methods Ecol. Evol. 7, 1386–1395 (2016).
doi: 10.1111/2041-210X.12604
Díaz, S. et al. The global spectrum of plant form and function. Nature 529, 167–171 (2016).
pubmed: 26700811
doi: 10.1038/nature16489
van der Plas, F., Van Klink, R., Manning, P., Olff, H. & Fischer, M. Sensitivity of functional diversity metrics to sampling intensity. Methods Ecol. Evol. 8, 1072–1080 (2017).
doi: 10.1111/2041-210X.12728
Rao, C. R. Diversity and dissimilarity coefficients: a unified approach. Theor. Popul. Biol. 21, 24–43 (1982).
doi: 10.1016/0040-5809(82)90004-1
Simpson, E. H. Measurement of diversity. Nature https://doi.org/10.1038/163688a0 (1949).
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).
Abatzoglou, J. T., Dobrowski, S. Z., Parks, S. A. & Hegewisch, K. C. TerraClimate, a high-resolution global dataset of monthly climate and climatic water balance from 1958–2015. Sci. Data 5, 170191 (2018).
pubmed: 29313841
pmcid: 5759372
doi: 10.1038/sdata.2017.191
Fan, Y. Groundwater in the earth’s critical zone: relevance to large-scale patterns and processes. Water Resour. Res. 51, 3052–3069 (2015).
doi: 10.1002/2015WR017037
Moulatlet, G. M. et al. Using digital soil maps to infer edaphic affinities of plant species in Amazonia: problems and prospects. Ecol. Evol. 7, 8463–8477 (2017).
pubmed: 29075463
pmcid: 5648677
doi: 10.1002/ece3.3242
Dormann, C. F. et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27–46 (2013).
doi: 10.1111/j.1600-0587.2012.07348.x
Vehtari, A., Gelman, A. & Gabry, J. Practical Bayesian model evaluation using leave-one-out cross-validation and WAIC. Stat. Comput. 27, 1413–1432 (2017).
doi: 10.1007/s11222-016-9696-4
Makowski, D., Ben-Shachar, M. S. & Lüdecke, D. bayestestR: Describing effects and their uncertainty, existence and significance within the Bayesian framework. J. Open Source Softw. 4, 1541 (2019).
doi: 10.21105/joss.01541
Kruschke, J. K. Doing Bayesian Data Analysis: A Tutorial with R, JAGS, and Stan (Academic Press, 2014).