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Abstract Severe droughts have led to lower plant growth and high mortality in many ecosystems worldwide, including tropical forests. Drought vulnerability differs among species, but there is limited consensus on the nature and degree of this variation in tropical forest communities. Understanding species‐level vulnerability to drought requires examination of hydraulic traits since these reflect the different strategies species employ for surviving drought.Here, we examined hydraulic traits and growth reductions during a severe drought for 12 common woody species in a wet tropical forest community in Puerto Rico to ask: Q1. To what extent can hydraulic traits predict growth declines during drought? We expected that species with more hydraulically vulnerable xylem and narrower safety margins (SMP50) would grow less during drought. Q2. How does species successional association relate to the levels of vulnerability to drought and hydraulic strategies? We predicted that early‐ and mid‐successional species would exhibit more acquisitive strategies, making them more susceptible to drought than shade‐tolerant species. Q3. What are the different hydraulic strategies employed by species and are there trade‐offs between drought avoidance and drought tolerance? We anticipated that species with greater water storage capacity would have leaves that lose turgor at higher xylem water potential and be less resistant to embolism forming in their xylem (P50).We found a large range of variation in hydraulic traits across species; however, they did not closely capture the magnitude of growth declines during drought. Among larger trees (≥10 cm diameter at breast height—DBH), some tree species with high xylem embolism vulnerability (P50) and risk of hydraulic failure (SMP50) experienced substantial growth declines during drought, but this pattern was not consistent across species. We found a trade‐off among species between drought avoidance (capacitance) and drought tolerating (P50) in this tropical forest community. Hydraulic strategies did not align with successional associations. Instead, some of the more drought‐vulnerable species were shade‐tolerant dominants in the community, suggesting that a drying climate could lead to shifts in long‐term forest composition and function in Puerto Rico and the Caribbean. Read the freePlain Language Summaryfor this article on the Journal blog.
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Importance of hydraulic strategy trade-offs in structuring response of canopy trees to extreme drought in central Amazon
Plant ecophysiological trade-offs between different strategies for tolerating stresses are widely theorized to shape forest functional diversity and vulnerability to climate change. However, trade-offs between hydraulic and stomatal regulation during natural droughts remain under-studied, especially in tropical forests. We investigated eleven mature forest canopy trees in central Amazonia during the strong 2015 El Niño. We found greater xylem embolism resistance (P50 = − 3.3 ± 0.8 MPa) and hydraulic safety margin (HSM = 2.12 ± 0.57 MPa) than previously observed in more precipitation-seasonal rainforests of eastern Amazonia and central America. We also discovered that taller trees exhibited lower embolism resistance and greater stomatal sensitivity, a height-structured trade-off between hydraulic resistance and active stomatal regulation. Such active regulation of tree water status, triggered by the onset of stem embolism, acted as a feedback to avoid further increases in embolism, and also explained declines in photosynthesis and transpiration. These results suggest that canopy trees exhibit a conservative hydraulic strategy to endure drought, with trade-offs between investment in xylem to reduce vulnerability to hydraulic failure, and active stomatal regulation to protect against low water potentials. These findings improve our understanding of strategies in tropical forest canopies and contribute to more accurate prediction of drought responses.
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- PAR ID:
- 10252600
- Date Published:
- Journal Name:
- Oecologia
- ISSN:
- 0029-8549
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary Deep‐water access is arguably the most effective, but under‐studied, mechanism that plants employ to survive during drought. Vulnerability to embolism and hydraulic safety margins can predict mortality risk at given levels of dehydration, but deep‐water access may delay plant dehydration. Here, we tested the role of deep‐water access in enabling survival within a diverse tropical forest community in Panama using a novel data‐model approach.We inversely estimated the effective rooting depth (ERD, as the average depth of water extraction), for 29 canopy species by linking diameter growth dynamics (1990–2015) to vapor pressure deficit, water potentials in the whole‐soil column, and leaf hydraulic vulnerability curves. We validated ERD estimates against existing isotopic data of potential water‐access depths.Across species, deeper ERD was associated with higher maximum stem hydraulic conductivity, greater vulnerability to xylem embolism, narrower safety margins, and lower mortality rates during extreme droughts over 35 years (1981–2015) among evergreen species. Species exposure to water stress declined with deeper ERD indicating that trees compensate for water stress‐related mortality risk through deep‐water access.The role of deep‐water access in mitigating mortality of hydraulically‐vulnerable trees has important implications for our predictive understanding of forest dynamics under current and future climates.more » « less
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Abstract The coordination of plant leaf water potential (ΨL) regulation and xylem vulnerability to embolism is fundamental for understanding the tradeoffs between carbon uptake and risk of hydraulic damage. There is a general consensus that trees with vulnerable xylem more conservatively regulate ΨLthan plants with resistant xylem. We evaluated if this paradigm applied to three important eastern US temperate tree species,Quercus albaL.,Acer saccharumMarsh. andLiriodendron tulipiferaL., by synthesizing 1600 ΨLobservations, 122 xylem embolism curves and xylem anatomical measurements across 10 forests spanning pronounced hydroclimatological gradients and ages. We found that, unexpectedly, the species with the most vulnerable xylem (Q. alba) regulated ΨLless strictly than the other species. This relationship was found across all sites, such that coordination among traits was largely unaffected by climate and stand age.Quercusspecies are perceived to be among the most drought tolerant temperate US forest species; however, our results suggest their relatively loose ΨLregulation in response to hydrologic stress occurs with a substantial hydraulic cost that may expose them to novel risks in a more drought‐prone future.more » « less
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• Drought-induced xylem embolism is a primary cause of plant mortality. Although ~70% of cycads are threatened by extinction and extant cycads diversified during a period of increasing aridification, the vulnerability of cycads to embolism spread has been overlooked. • We quantified the vulnerability to drought-induced embolism, pressure-volume curves, in situ water potentials, and a suite of xylem anatomical traits of leaf pinnae and rachises for 20 cycad species. We tested whether anatomical traits were linked to hydraulic safety in cycads. • Compared to other major vascular plant clades, cycads exhibited similar embolism resistance to angiosperms and pteridophytes but were more vulnerable to embolism than non-cycad gymnosperms. All 20 cycads had both tracheids and vessels, the proportions of which were unrelated to embolism resistance. Only vessel pit membrane fraction was positively correlated to embolism resistance, contrary to angiosperms. Water potential at turgor loss was significantly correlated to embolism resistance among cycads. • Our results show that cycads exhibit low resistance to xylem embolism and that xylem anatomical traits–particularly vessels–may influence embolism resistance together with tracheids. This study highlights the importance of understanding the mechanisms of drought resistance in evolutionarily unique and threatened lineages like the cycads.more » « less
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null (Ed.)Quantitative knowledge of xylem physical tolerance limits to dehydration is essential to understanding plant drought tolerance but is lacking in many long-vessel angiosperms. We examine the hypothesis that a fundamental association between sustained xylem water transport and downstream tissue function should select for xylem that avoids embolism in long-vessel trees by quantifying xylem capacity to withstand air entry of western North American oaks ( Quercus spp.). Optical visualization showed that 50% of embolism occurs at water potentials below −2.7 MPa in all 19 species, and −6.6 MPa in the most resistant species. By mapping the evolution of xylem vulnerability to embolism onto a fossil-dated phylogeny of the western North American oaks, we found large differences between clades (sections) while closely related species within each clade vary little in their capacity to withstand air entry. Phylogenetic conservatism in xylem physical tolerance, together with a significant correlation between species distributions along rainfall gradients and their dehydration tolerance, suggests that closely related species occupy similar climatic niches and that species' geographic ranges may have shifted along aridity gradients in accordance with their physical tolerance. Such trends, coupled with evolutionary associations between capacity to withstand xylem embolism and other hydraulic-related traits, yield wide margins of safety against embolism in oaks from diverse habitats. Evolved responses of the vascular system to aridity support the embolism avoidance hypothesis and reveal the importance of quantifying plant capacity to withstand xylem embolism for understanding function and biogeography of some of the Northern Hemisphere’s most ecologically and economically important plants.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1007/s00442-021-04924-9
