Species intraspecific variation drives tropical forest drought resistance

Nature作者:Chris M. Smith-Martin2026年8月12日正文已收录本站
  • Aleixo, I. et al. Amazonian rainforest tree mortality driven by climate and functional traits. Nat. Clim. Change 9, 384–388 (2019).

    Article  ADS  Google Scholar 

  • Uriarte, M., Lasky, J. R., Boukili, V. K. & Chazdon, R. L. A trait-mediated, neighbourhood approach to quantify climate impacts on successional dynamics of tropical rainforests. Funct. Ecol. 30, 157–167 (2016).

    Article  Google Scholar 

  • Leitold, V. et al. El Niño drought increased canopy turnover in Amazon forests. N. Phytol. 219, 959–971 (2018).

    Article  CAS  Google Scholar 

  • Powers, J. S. et al. A catastrophic tropical drought kills hydraulically vulnerable tree species. Glob. Change Biol. 26, 3122–3133 (2020).

    Article  ADS  Google Scholar 

  • Rosas, T. et al. Adjustments and coordination of hydraulic, leaf and stem traits along a water availability gradient. N. Phytol. 223, 632–646 (2019).

    Article  CAS  Google Scholar 

  • Anderegg, L. D. L. et al. Aridity drives coordinated trait shifts but not decreased trait variance across the geographic range of eight Australian trees. N. Phytol. 229, 1375–1387 (2021).

    Article  Google Scholar 

  • López, R., Cano, F. J., Martin-StPaul, N. K., Cochard, H. & Choat, B. Coordination of stem and leaf traits define different strategies to regulate water loss and tolerance ranges to aridity. N. Phytol. 230, 497–509 (2021).

    Article  Google Scholar 

  • Alon, A. et al. Acclimation limits for embolism resistance and osmotic adjustment accompany the geographical dry edge of Mediterranean species. Funct. Ecol. 37, 1421–1435 (2023).

    Article  CAS  Google Scholar 

  • Maherali, H., Williams, B. L., Paige, K. N. & Delucia, E. H. Hydraulic differentiation of Ponderosa pine populations along a climate gradient is not associated with ecotypic divergence. Funct. Ecol. 16, 510–521 (2002).

    Article  Google Scholar 

  • Martínez-Vilalta, J. et al. Hydraulic adjustment of Scots pine across Europe. N. Phytol. 184, 353–364 (2009).

    Article  Google Scholar 

  • Lamy, J. B. et al. Limited genetic variability and phenotypic plasticity detected for cavitation resistance in a Mediterranean pine. N. Phytol. 201, 874–886 (2014).

    Article  Google Scholar 

  • Sáenz-Romero, C. et al. Genetic variation of drought-induced cavitation resistance among Pinus hartwegii populations from an altitudinal gradient. Acta Physiol. Plant. 35, 2905–2913 (2013).

    Article  Google Scholar 

  • Pan, Y. et al. A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011).

    Article  ADS  CAS  PubMed  Google Scholar 

  • Gatti, L. V. et al. Drought sensitivity of Amazonian carbon balance revealed by atmospheric measurements. Nature 506, 76–80 (2014).

    Article  ADS  CAS  PubMed  Google Scholar 

  • Seo, K.-W. et al. Abrupt sea level rise and Earth’s gradual pole shift reveal permanent hydrological regime changes in the 21st century. Science 387, 1408–1413 (2025).

    Article  ADS  CAS  PubMed  Google Scholar 

  • Brodribb, T. J., Powers, J., Cochard, H. & Choat, B. Hanging by a thread? Forests and drought. Science 368, 261–266 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  • Fauset, S. et al. Drought-induced shifts in the floristic and functional composition of tropical forests in Ghana. Ecol. Lett. 15, 1120–1129 (2012).

    Article  PubMed  Google Scholar 

  • Trugman, A. T., Anderegg, L. D. L., Shaw, J. D. & Anderegg, W. R. L. Trait velocities reveal that mortality has driven widespread coordinated shifts in forest hydraulic trait composition. Proc. Natl Acad. Sci. USA 17, 8532–8538 (2020).

    Article  ADS  Google Scholar 

  • Comita, L. S. et al. Limited intraspecific variation in drought resistance along a pronounced tropical rainfall gradient. Proc. Natl Acad. Sci. USA 121, e2316971121 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith-Martin, C. M. et al. Hydraulic variability of tropical forests is largely independent of water availability. Ecol. Lett. 26, 1829–1839 (2023).

    Article  PubMed  Google Scholar 

  • Vargas G, G. et al. Leaf habit affects the distribution of drought sensitivity but not water transport efficiency in the tropics. Ecol. Lett. 25, 2637–2650 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  • Tavares, J. V. et al. Basin-wide variation in tree hydraulic safety margins predicts the carbon balance of Amazon forests. Nature 617, 111–117 (2023).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Engelbrecht, B. M. J. et al. Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447, 80–82 (2007).

    Article  ADS  CAS  PubMed  Google Scholar 

  • Esquivel-Muelbert, A. et al. Seasonal drought limits tree species across the Neotropics. Ecography 40, 618–629 (2017).

    Article  ADS  Google Scholar 

  • Choat, B., Sack, L. & Holbrook, N. M. Diversity of hydraulic traits in nine Cordia species growing in tropical forests with contrasting precipitation. N. Phytol. 175, 686–698 (2007).

    Article  Google Scholar 

  • Westerband, A. C., Funk, J. L. & Barton, K. E. Intraspecific trait variation in plants: a renewed focus on its role in ecological processes. Ann. Bot. 127, 397–410 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tonet, V., Brodribb, T. & Bourbia, I. Variation in xylem vulnerability to cavitation shapes the photosynthetic legacy of drought. Plant Cell Environ. 47, 1160–1170 (2024).

    Article  CAS  PubMed  Google Scholar 

  • Garcia, M. N. et al. Local hydrological gradients structure high intraspecific variability in plant hydraulic traits in two dominant central Amazonian tree species. J. Exp. Bot. 73, 939–952 (2022).

    Article  CAS  PubMed  Google Scholar 

  • Benito Garzón, M., Alía, R., Robson, T. M. & Zavala, M. A. Intra-specific variability and plasticity influence potential tree species distributions under climate change. Glob. Ecol. Biogeogr. 20, 766–778 (2011).

    Article  Google Scholar 

  • Valladares, F. et al. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol. Lett. 17, 1351–1364 (2014).

    Article  PubMed  Google Scholar 

  • Blackman, C. J. et al. Leaf hydraulic vulnerability to drought is linked to site water availability across a broad range of species and climates. Ann. Bot. 114, 435–440 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  • Peters, J. M. R. et al. Living on the edge: a continental-scale assessment of forest vulnerability to drought. Glob. Change Biol. 27, 3620–3641 (2021).

    Article  ADS  CAS  Google Scholar 

  • Daly, C., Helmer, E. H. & Quiñones, M. Mapping the climate of Puerto Rico, Vieques and Culebra. Int. J. Climatol. 23, 1359–1381 (2003).

    Article  Google Scholar 

  • Miller, G. & Lugo, A. E. Guide to the Ecological Systems of Puerto Rico (US Department of Agriculture, 2009).

  • US Geological Survey Minerals Team. Geology, Geochemistry, Geophysics, Mineral Occurrences, and Mineral Resource Assessment for the Commonwealth of Puerto Rico Open-File Report 98-38 (US Geological Survey, 1998).

  • Muscarella, R., Kolyaie, S., Morton, D. C., Zimmerman, J. K. & Uriarte, M. Effects of topography on tropical forest structure depend on climate context. J. Ecol. 108, 145–159 (2020).

    Article  Google Scholar 

  • Binks, O. et al. Plasticity in leaf-level water relations of tropical rainforest trees in response to experimental drought. N. Phytol. 211, 477–488 (2016).

    Article  CAS  Google Scholar 

  • Schuldt, B. et al. How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction? N. Phytol. 210, 443–458 (2016).

    Article  Google Scholar 

  • Hajek, P., Kurjak, D., Von Wühlisch, G., Delzon, S. & Schuldt, B. Intraspecific variation in wood anatomical, hydraulic, and foliar traits in ten European beech provenances differing in growth yield. Front. Plant Sci. 7, 791 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  • Skelton, R. P. et al. Evolutionary relationships between drought-related traits and climate shape large hydraulic safety margins in western North American oaks. Proc. Natl Acad. Sci. USA 118, e2008987118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dick, C. W. & Pennington, R. T. History and geography of neotropical tree diversity. Ann. Rev. Ecol. Evol. Syst. 50, 279–301 (2019).

    Article  Google Scholar 

  • Baker, P. A. et al. in Neotropical Diversification: Patterns and Processes (eds Rull, V. & Carnaval, A. C.) 51–70 (Springer, 2020).

  • Knutzen, F., Meier, I. C. & Leuschner, C. Does reduced precipitation trigger physiological and morphological drought adaptations in European beech (Fagus sylvatica L.)? Comparing provenances across a precipitation gradient. Tree Physiol. 35, 949–963 (2015).

    Article  CAS  PubMed  Google Scholar 

  • McLean, E. H. et al. Plasticity of functional traits varies clinally along a rainfall gradient inEucalyptus tricarpa. Plant Cell Environ. 37, 1440–1451 (2014).

    Article  CAS  PubMed  Google Scholar 

  • Oyanoghafo, O. O. et al. Contributions of phenotypic integration, plasticity and genetic adaptation to adaptive capacity relating to drought in Banksia marginata (Proteaceae). Front. Plant Sci. 14, 1150116 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  • Vivas, M., Rolo, V., Wingfield, M. J. & Slippers, B. Maternal environment regulates morphological and physiological traits in Eucalyptus grandis. For. Ecol. Manage. 432, 631–636 (2019).

    Article  Google Scholar 

  • Ramírez-Valiente, J. A. et al. Limited plastic responses in safety traits support greater hydraulic risk under drier conditions. Nat. Ecol. Evol. 9, 1825–1836 (2025).

    Article  PubMed  Google Scholar 

  • Zanne, A. E. et al. Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89–92 (2014).

    Article  ADS  CAS  PubMed  Google Scholar 

  • Muscarella, R. et al. Variation of tropical forest assembly processes across regional environmental gradients. Perspect. Plant Ecol. Evol. Syst. 23, 52–62 (2016).

    Article  Google Scholar 

  • Ewel, J. J. & Whitmore, J. L. The Ecological Life Zones of Puerto Rico and the U.S. Virgin Islands (Institute of Tropical Forestry, 1973).

  • Lugo-Camacho, J. L. The Soil Climate Regimes of Puerto Rico: Reassessment and Implications. MSc thesis, Univ. of Puerto Rico (2005).

  • Sanchez, M. J., Lopez, E. & Lugo, A. E. Chemical and Physical Analyses of Selected Plants and Soils from Puerto Rico (1981-2000) (US Department of Agriculture, 2015).

  • Maréchaux, I., Bartlett, M. K., Iribar, A., Sack, L. & Chave, J. Stronger seasonal adjustment in leaf turgor loss point in lianas than trees in an Amazonian forest. Biol. Lett. 13, 20160819 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • Tyree, M. T. & Hammel, H. T. The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. J. Exp. Bot. 23, 267–282 (1972).

    Article  Google Scholar 

  • Sack, L. & Pasquet-Kok, J. Leaf pressure–volume curve parameters. Prometheus https://prometheusprotocols.net/function/water-relations/pressure-volume-curves/leaf-pressure-volume-curve-parameters/ (2011).

  • Brodribb, T. J. et al. Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. N. Phytol. 209, 1403–1409 (2016).

    Article  Google Scholar 

  • Brodribb, T. J., Carriqui, M., Delzon, S. & Lucani, C. Optical measurement of stem xylem vulnerability. Plant Physiol. 174, 2054–2061 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith-Martin, C. M., Skelton, R. P., Johnson, K. M., Lucani, C. & Brodribb, T. J. Lack of vulnerability segmentation among woody species in a diverse dry sclerophyll woodland community. Funct. Ecol. 34, 777–787 (2020).

    Article  Google Scholar 

  • Skelton, R. P. et al. Low vulnerability to xylem embolism in leaves and stems of North American oaks. Plant Physiol. 177, 1066–1077 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brodribb, T. J., Carriquí, M., Delzon, S., McAdam, S. A. M. & Holbrook, N. M. Advanced vascular function discovered in a widespread moss. Nat. Plants 6, 273–279 (2020).

    Article  CAS  PubMed  Google Scholar 

  • Gauthey, A. et al. Visual and hydraulic techniques produce similar estimates of cavitation resistance in woody species. N. Phytol. 228, 884–897 (2020).

    Article  Google Scholar 

  • Johnson, K. M., Brodersen, C., Carins-Murphy, M. R., Choat, B. & Brodribb, T. J. Xylem embolism spreads by single-conduit events in three dry forest angiosperm stems. Plant Physiol. 184, 212–222 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira, L. et al. The Pneumatron: an automated pneumatic apparatus for estimating xylem vulnerability to embolism at high temporal resolution. Plant Cell Environ. 43, 131–142 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  • Guan, X., Pereira, L., McAdam, S. A. M., Cao, K. F. & Jansen, S. No gas source, no problem: proximity to pre-existing embolism and segmentation affect embolism spreading in angiosperm xylem by gas diffusion. Plant Cell Environ. 44, 1329–1345 (2021).

    Article  CAS  PubMed  Google Scholar 

  • Smith-Martin, C. M. et al. Increasing air-filled vessels has little influence on vulnerability to drought-induced embolism in two species with long maximum xylem vessel length but low vessel connectivity. Tree Physiol. 45, tpaf041 (2025).

    Article  PubMed  Google Scholar 

  • Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article  Google Scholar 

  • Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).

    Article  Google Scholar 

  • Bürkner, P.-C. brms: an R package for bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28 (2017).

    Article  Google Scholar 

  • Lüdecke, D., Waggoner, P. & Makowski, D. insight: a unified interface to access information from model objects in R. J. Open Source Softw. 4, 1412 (2019).

    Article  ADS  Google Scholar 

  • Smith-Martin, C. M., Muscarella, R., Brodribb, T. J. & Uriarte, M. Data and code for ‘Species intraspecific variation drives tropical forest drought resistance’. Dryad https://doi.org/10.5061/dryad.r4xgxd2vb (2026).

  • PRISM Group. PRISM Database (2014, accessed 14 November 2025); https://prism.oregonstate.edu.

  • Karger, D. N. et al. Climatologies at high resolution for the earth’s land surface areas. Sci. Data 4, 170122 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • Little, A. L. & Wadsworth, F. H. Common Trees of Puerto Rico and the Virgin Islands Agriculture Handbook No. 249 (US Department of Agriculture, 1964).