Rooting depth and xylem vulnerability are independent woody plant traits jointly selected by aridity, seasonality, and water table depth
Language English Country Great Britain, England Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
Grant support
FZT 118
Deutsche Forschungsgemeinschaft
202548816
Deutsche Forschungsgemeinschaft
2019528
National Science Foundation
PubMed
37743552
DOI
10.1111/nph.19276
Knihovny.cz E-resources
- Keywords
- cavitation, drought avoider, drought resistant, embolism, species distribution modeling, trees, water availability,
- MeSH
- Wood physiology MeSH
- Embolism * MeSH
- Plant Leaves physiology MeSH
- Droughts MeSH
- Groundwater * MeSH
- Plants MeSH
- Water physiology MeSH
- Xylem physiology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Water MeSH
Evolutionary radiations of woody taxa within arid environments were made possible by multiple trait innovations including deep roots and embolism-resistant xylem, but little is known about how these traits have coevolved across the phylogeny of woody plants or how they jointly influence the distribution of species. We synthesized global trait and vegetation plot datasets to examine how rooting depth and xylem vulnerability across 188 woody plant species interact with aridity, precipitation seasonality, and water table depth to influence species occurrence probabilities across all biomes. Xylem resistance to embolism and rooting depth are independent woody plant traits that do not exhibit an interspecific trade-off. Resistant xylem and deep roots increase occurrence probabilities in arid, seasonal climates over deep water tables. Resistant xylem and shallow roots increase occurrence probabilities in arid, nonseasonal climates over deep water tables. Vulnerable xylem and deep roots increase occurrence probabilities in arid, nonseasonal climates over shallow water tables. Lastly, vulnerable xylem and shallow roots increase occurrence probabilities in humid climates. Each combination of trait values optimizes occurrence probabilities in unique environmental conditions. Responses of deeply rooted vegetation may be buffered if evaporative demand changes faster than water table depth under climate change.
Agronomy Department University of Florida Gainesville FL 32611 USA
Biodiversity Research Institute Mieres Asturias Spain
Botanical Garden Polish Academy of Sciences Warsaw Poland
Botany and Microbiology Department Tanta University Tanta 3527 Egypt
CIRAD UPR Forêts et Sociétés F 34398 Montpellier France
CREAF Cerdanyola del Vallès 08193 Barcelona Catalonia Spain
Crop Science and Plant Biology Estonian University of Life Sciences Tartu 51006 Estonia
Department of Biological Science Andong National University Andong si 36729 South Korea
Department of Biology University of Copenhagen 2100 Copenhagen Ø Denmark
Department of Botany and Biodiversity Research Universitiy of Vienna 1030 Vienna Austria
Department of Botany and Nature Protection University of Warmia and Mazury Olsztyn Poland
Department of Botany Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic
Department of Botany University of Wyoming Laramie WY 82071 USA
Department of Environmental Biology Sapienza University of Rome Rome 00185 Italy
Department of Functional Ecology Institute of Botany Czech Academy of Sciences Trebon Czech Republic
Faculty of Forestry and Wood Technology University of Zagreb 10000 Zagreb Croatia
Forêts et Sociétés Univ Montpellier CIRAD Montpellier France
German Centre for Integrative Biodiversity Research Halle Jena Leipzig Leipzig 04103 Germany
Global Ecology Unit CREAF CSIC UAB CSIC Bellaterra 08193 Barcelona Catalonia Spain
Harvard Forest Harvard University Petersham MA 01366 USA
Institute of Botany Ulm University Albert Einstein Allee 11 Ulm 89081 Germany
Manaaki Whenua Landcare Research Lincoln 7640 New Zealand
Max Planck Institute for Biogeochemistry Jena Germany
Naturalis Biodiversity Center Darwinweg 2 2333 CR Leiden the Netherlands
Palmengarten der Stadt Frankfurt am Main 60323 Frankfurt am Main Germany
Plant Ecology and Ecosystems Research University of Goettingen 37073 Goettingen Germany
Research School of Biology Australian National University Canberra ACT Australia
Resource Management HAWK University of Applied Sciences and Arts 37077 Goettingen Germany
School of Geography University of Leeds Leeds LS2 9JT UK
School of Geography University of Nottingham University Park Nottingham NG7 2RD UK
School of Geosciences University of Edinburgh Edinburgh UK
Vegetation Ecology Research Group Institute of Natural Resource Sciences 8820 Wädenswil Switzerland
See more in PubMed
Aubin I, Munson AD, Cardou F, Burton PJ, Isabel N, Pedlar JH, Paquette A, Taylor AR, Delagrange S, Kebli H et al. 2016. Traits to stay, traits to move: a review of functional traits to assess sensitivity and adaptive capacity of temperate and boreal trees to climate change. Environmental Reviews 24: 164-186.
Bauman D, Fortunel C, Delhaye G, Malhi Y, Cernusak LA, Bentley LP, Rifai SW, Aguirre-Gutiérrez J, Menor IO, Phillips OL et al. 2022. Tropical tree mortality has increased with rising atmospheric water stress. Nature 608: 528-533.
Bouda M, Huggett BA, Prats KA, Wason JW, Wilson JP, Brodersen CR. 2022. Hydraulic failure as a primary driver of xylem network evolution in early vascular plants. Science 378: 642-646.
Bruelheide H, Dengler J, Jiménez-Alfaro B, Purschke O, Hennekens SM, Chytrý M, Pillar VD, Jansen F, Kattge J, Sandel B et al. 2019. sPlot - a new tool for global vegetation analyses. Journal of Vegetation Science 30: 161-186.
Bruelheide H, Vonlanthen B, Jandt U, Thomas FM, Foetzki A, Gries D, Wang G, Zhang X, Runge M. 2010. Life on the edge - to which degree does phreatic water sustain vegetation in the periphery of the Taklamakan Desert? Applied Vegetation Science 13: 56-71.
Brum M, Vadeboncoeur MA, Ivanov V, Asbjornsen H, Saleska S, Alves LF, Penha D, Dias JD, Aragão LEOC, Barros F et al. 2019. Hydrological niche segregation defines forest structure and drought tolerance strategies in a seasonal Amazon forest. Journal of Ecology 107: 318-333.
Canadell J, Jackson RB, Ehleringer JB, Mooney HA, Sala OE, Schulze ED. 1996. Maximum rooting depth of vegetation types at the global scale. Oecologia 108: 583-595.
Carlquist S. 1975. Ecological strategies of xylem evolution. Berkeley, CA, USA: University of California Press.
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG et al. 2012. Global convergence in the vulnerability of forests to drought. Nature 491: 752-755.
Cochard H, Badel E, Herbette S, Delzon S, Choat B, Jansen S. 2013. Methods for measuring plant vulnerability to cavitation: a critical review. Journal of Experimental Botany 64: 4779-4791.
Díaz S, Kattge J, Cornelissen JH, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Prentice IC. 2022. The global spectrum of plant form and function: enhanced species-level trait dataset. Scientific Data 9: 755.
Dinerstein E, Olson D, Joshi A, Vynne C, Burgess ND, Wikramanayake E, Hahn N, Palminteri S, Hedao P, Noss R et al. 2017. An ecoregion-based approach to protecting half the terrestrial realm. Bioscience 67: 534-545.
Döll P, Fiedler K. 2008. Global-scale modeling of groundwater recharge. Hydrology and Earth System Sciences 12: 863-885.
Ehleringer JR. 1993. Variation in leaf carbon isotope discrimination in Encelia farinosa: implications for growth, competition, and drought survival. Oecologia 95: 340-346.
Fan Y, Li H, Miguez-Macho G. 2013. Global patterns of groundwater table depth. Science 339: 940-943.
Fan Y, Miguez-Macho G, Jobbágy EG, Jackson RB, Otero-Casal C. 2017. Hydrologic regulation of plant rooting depth. Proceedings of the National Academy of Sciences, USA 114: 10572-10577.
Fick SE, Hijmans RJ. 2017. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37: 4302-4315.
Fischer RA, Maurer R. 1978. Drought resistance in spring wheat cultivars. I. Grain yield responses. Australian Journal of Agricultural Research 29: 897-912.
Grossiord C, Buckley TN, Cernusak LA, Novick KA, Poulter B, Siegwolf RTW, Sperry JS, McDowell NG. 2020. Plant responses to rising vapor pressure deficit. New Phytologist 226: 1550-1566.
Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA. 2001. Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126: 457-461.
Hammond WM, Williams AP, Abatzoglou JT, Adams HD, Klein T, López R, Sáenz-Romero C, Hartmann H, Breshears DD, Allen CD. 2022. Global field observations of tree die-off reveal hotter-drought fingerprint for Earth's forests. Nature Communications 13: 1761.
Hammond WM, Yu K, Wilson LA, Will RE, Anderegg WRL, Adams HD. 2019. Dead or dying? Quantifying the point of no return from hydraulic failure in drought-induced tree mortality. New Phytologist 223: 1834-1843.
Hartmann H, Bastos A, Das AJ, Esquivel-Muelbert A, Hammond WM, Martínez-Vilalta J, McDowell NG, Powers JS, Pugh TAM, Ruthrof KX et al. 2022. Climate change risks to global forest health: emergence of unexpected events of elevated tree mortality worldwide. Annual Review of Plant Biology 73: 673-702.
Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED. 1996. A global analysis of root distributions for terrestrial biomes. Oecologia 108: 389-411.
Jackson RB, Sperry JS, Dawson TE. 2000. Root water uptake and transport: using physiological processes in global predictions. Trends in Plant Science 5: 482-488.
Jin Y, Qian H. 2019. v.phylomaker: an R package that can generate very large phylogenies for vascular plants. Ecography 42: 1353-1359.
Larter M, Pfautsch S, Domec JC, Trueba S, Nagalingum N, Delzon S. 2017. Aridity drove the evolution of extreme embolism resistance and the radiation of conifer genus Callitris. New Phytologist 215: 97-112.
Laughlin DC, Delzon S, Clearwater MJ, Bellingham PJ, McGlone MS, Richardson SJ. 2020a. Climatic limits of temperate rainforest tree species are explained by xylem embolism resistance among angiosperms but not among conifers. New Phytologist 226: 727-740.
Laughlin DC, Gremer JR, Adler PB, Mitchell RM, Moore MM. 2020b. The net effect of functional traits on fitness. Trends in Ecology & Evolution 35: 1037-1047.
Laughlin DC, Mommer L, Sabatini FM, Bruelheide H, Kuyper TW, McCormack ML, Bergmann J, Freschet GT, Guerrero-Ramírez NR, Iversen CM et al. 2021. Root traits explain plant species distributions along climatic gradients yet challenge the nature of ecological trade-offs. Nature Ecology & Evolution 5: 1123-1134.
Laughlin DC, Strahan RT, Huffman DW, Sánchez Meador AJ. 2017. Using trait-based ecology to restore resilient ecosystems: historical conditions and the future of montane forests in western North America. Restoration Ecology 25(S2): S135-S146.
Levitt J. 1980. Responses of plants to environmental stress, vol. 2: Water, radiation, salt and other stresses. Cambridge, UK: Academic Press.
Loheide SP, Butler JJ, Gorelick SM. 2005. Estimation of groundwater consumption by phreatophytes using diurnal water table fluctuations: a saturated-unsaturated flow assessment. Water Resources Research 41: W07030.
Maherali H, Pockman WT, Jackson RB. 2004. Adaptive variation in the vulnerability of woody plant to xylem cavitation. Ecology 85: 2184-2199.
May LH, Milthorpe FL. 1962. Drought resistance of crop plants. Field Crop Abstracts 15: 171-179.
McDowell NG, Sapes G, Pivovaroff A, Adams HD, Allen CD, Anderegg WRL, Arend M, Breshears DD, Brodribb T, Choat B et al. 2022. Mechanisms of woody-plant mortality under rising drought, CO2 and vapour pressure deficit. Nature Reviews Earth & Environment 3: 294-308.
Merow C, Bois ST, Allen JM, Xie Y, Silander JA. 2017. Climate change both facilitates and inhibits invasive plant ranges in New England. Proceedings of the National Academy of Sciences, USA 114: E3276-E3284.
Miguez-Macho G, Fan Y. 2021. Spatiotemporal origin of soil water taken up by vegetation. Nature 598: 624-628.
Miller C, Ulate W. 2017. World flora online project: an online flora of all known plants. Biodiversity Information Science and Standards 1: e20529.
Nobre AD, Cuartas LA, Hodnett M, Rennó CD, Rodrigues G, Silveira A, Waterloo M, Saleska S. 2011. Height above the nearest drainage - a hydrologically relevant new terrain model. Journal of Hydrology 404: 13-29.
Oliveira RS, Costa FRC, van Baalen E, de Jonge A, Bittencourt PR, Almanza Y, Barros FV, Cordoba EC, Fagundes MV, Garcia S et al. 2019. Embolism resistance drives the distribution of Amazonian rainforest tree species along hydro-topographic gradients. New Phytologist 221: 1457-1465.
Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D'amico JA, Itoua I, Strand HE, Morrison JC et al. 2001. Terrestrial ecoregions of the world: a new map of life on earth: a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. Bioscience 51: 933-938.
Pagel M. 1999. Inferring the historical patterns of biological evolution. Nature 401: 877-884.
Qian H, Jin Y. 2016. An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. Journal of Plant Ecology 9: 233-239.
Revell LJ. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3: 217-223.
Revell LJ, Harmon LJ. 2022. Phylogenetic comparative methods in R. Princeton, NJ, USA: Princeton University Press.
Ryel RJ, Ivans CY, Peek MS, Leffler AJ. 2008. Functional differences in soil water pools: a new perspective on plant water use in water-limited ecosystems. In: Lüttge U, Beyschlag W, Murata J, eds. Progress in botany. Berlin, Heidelberg, Germany: Springer Berlin Heidelberg, 397-422.
Schenk HJ, Jackson RB. 2002. Rooting depths, lateral root spreads and below-ground/above-ground allometries of plants in water-limited ecosystems. Journal of Ecology 90: 480-494.
Schenk HJ, Jackson RB. 2005. Mapping the global distribution of deep roots in relation to climate and soil characteristics. Geoderma 126: 129-140.
Schwinning S, Ehleringer JR. 2001. Water use trade-offs and optimal adaptations to pulse-driven arid ecosystems. Journal of Ecology 89: 464-480.
Seyfried MS, Schwinning S, Walvoord MA, Pockman WT, Newman BD, Jackson RB, Phillips FM. 2005. Ecohydrological control of deep drainage in arid and semiarid regions. Ecology 86: 277-287.
Sousa TR, Schietti J, Coelho de Souza F, Esquivel-Muelbert A, Ribeiro IO, Emílio T, Pequeno PACL, Phillips O, Costa FRC. 2020. Palms and trees resist extreme drought in Amazon forests with shallow water tables. Journal of Ecology 108: 2070-2082.
Sousa TR, Schietti J, Ribeiro IO, Emílio T, Fernández RH, ter Steege H, Castilho CV, Esquivel-Muelbert A, Baker T, Pontes-Lopes A et al. 2022. Water table depth modulates productivity and biomass across Amazonian forests. Global Ecology and Biogeography 31: 1571-1588.
Spinoni J, Vogt JV, Naumann G, Barbosa P, Dosio A. 2018. Will drought events become more frequent and severe in Europe? International Journal of Climatology 38: 1718-1736.
Trabucco A, Zomer RJ. 2018. Global aridity index and potential evapotranspiration (ET0) climate database v2. Consortium for Spatial Information (CGIAR-CSI). CGIAR-CSI GeoPortal. [WWW document] URL https://cgiarcsi.community [accessed 10 October 2022].
Tumber-Dávila SJ, Schenk HJ, Du E, Jackson RB. 2022. Plant sizes and shapes above and belowground and their interactions with climate. New Phytologist 235: 1032-1056.
Volaire F. 2018. A unified framework of plant adaptive strategies to drought: crossing scales and disciplines. Global Change Biology 24: 2929-2938.
Whittaker RH. 1975. Communities and Ecosystems. New York, NY, USA: Macmillan.
Willis KJ, McElwain JC. 2014. The evolution of plants. Oxford, UK: Oxford University Press.
Wood SN. 2011. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 73: 3-36.
Zomer RJ, Trabucco A, Bossio DA, Verchot LV. 2008. Climate change mitigation: a spatial analysis of global land suitability for clean development mechanism afforestation and reforestation. Agriculture, Ecosystems & Environment 126: 67-80.
