Water inside plants forms a continuous chain from water in soils to the water evaporating from leaf surfaces. Failures in this chain result in reduced transpiration and photosynthesis and are caused by soil drying and/or cavitation‐induced xylem embolism. Xylem embolism and plant hydraulic failure share several analogies to ‘catastrophe theory’ in dynamical systems. These catastrophes are often represented in the physiological and ecological literature as tipping points when control variables exogenous (e.g., soil water potential) or endogenous (e.g., leaf water potential) to the plant are allowed to vary on time scales much longer than time scales associated with cavitation events. Here, plant hydraulics viewed from the perspective of catastrophes at multiple spatial scales is considered with attention to bubble expansion within a xylem conduit, organ‐scale vulnerability to embolism, and whole‐plant biomass as a proxy for transpiration and hydraulic function. The hydraulic safety‐efficiency tradeoff, hydraulic segmentation and maximum plant transpiration are examined using this framework. Underlying mechanisms for hydraulic failure at fine scales such as pit membranes and cell‐wall mechanics, intermediate scales such as xylem network properties and at larger scales such as soil–tree hydraulic pathways are discussed. Understudied areas in plant hydraulics are also flagged where progress is urgently needed.
The vast majority of measurements in the field of plant hydraulics have been on small‐diameter branches from woody species. These measurements have provided considerable insight into plant functioning, but our understanding of plant physiology and ecology would benefit from a broader view, because branch hydraulic properties are influenced by many factors. Here, we discuss the influence that other components of the hydraulic network have on branch vulnerability to embolism propagation. We also modelled the impact of changes in the ratio of root‐to‐leaf areas and soil texture on vulnerability to hydraulic failure along the soil‐to‐leaf continuum and showed that hydraulic function is better maintained through changes in root vulnerability and root‐to‐leaf area ratio than in branch vulnerability. Differences among species in the stringency with which they regulate leaf water potential and in reliance on stored water to buffer changes in water potential also affect the need to construct embolism resistant branches. Many approaches, such as measurements on fine roots, small individuals, combining sap flow and psychrometry techniques, and modelling efforts, could vastly improve our understanding of whole‐plant hydraulic functioning. A better understanding of how traits are coordinated across the whole plant will improve predictions for plant function under future climate conditions.
more » « less- Award ID(s):
- 1754893
- PAR ID:
- 10459771
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Plant, Cell & Environment
- Volume:
- 42
- Issue:
- 10
- ISSN:
- 0140-7791
- Page Range / eLocation ID:
- p. 2789-2807
- 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.
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Summary A surge of papers have reported low leaf vulnerability to xylem embolism during drought. Here, we focus on the less studied, and more sensitive, outside‐xylem leaf hydraulic responses to multiple internal and external conditions. Studies of 34 species have resolved substantial vulnerability to dehydration of the outside‐xylem pathways, and studies of leaf hydraulic responses to light also implicate dynamic outside‐xylem responses. Detailed experiments suggest these dynamic responses arise at least in part from strong control of radial water movement across the vein bundle sheath. While leaf xylem vulnerability may influence leaf and plant survival during extreme drought, outside‐xylem dynamic responses are important for the control and resilience of water transport and leaf water status for gas exchange and growth.
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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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Abstract Recent findings suggest that tree mortality and post‐drought recovery of gas exchange can be predicted from loss of function within the water transport system. Understanding the susceptibility of plants to hydraulic damage requires knowledge about the vulnerability of different plant organs to stress‐induced hydraulic dysfunction. This is particularly important in the context of vulnerability segmentation between plant tissues which is believed to protect more energetically ‘costly’ tissues, such as woody stems, by sacrificing ‘cheaper’ leaves early under drought conditions.
Differences in vulnerability segmentation between co‐occurring plant species could explain divergent behaviours during drought, yet there are few studies considering how this characteristic may vary within a plant community. Here we investigated community‐wide vulnerability segmentation by comparing leaf/shoot and stem vulnerability in all coexistent dominant canopy and understory woody species in a diverse dry sclerophyll woodland community, including multiple angiosperms and one gymnosperm.
Previously published terminal leaf/shoot vulnerability to loss of water transport capacity was compared with stem xylem vulnerability to embolism measured on the same species at the same site. We calculated hydraulic safety margins for stems to determine variation in the risk of hydraulic failure during drought among species.
The xylem of all species was found to be highly resistant to hydraulic dysfunction, with only two of the eight species exhibiting significantly different vulnerability to the overall mean. No evidence of vulnerability segmentation between shoots/leaves and stems was found in seven of the eight species.
Phylogenetically diverse canopy and understory species in this evergreen sclerophyll woodland appear to have evolved similar strategies of drought resistance, including low xylem vulnerability to embolism and general lack of vulnerability segmentation. This convergence in hydraulic safety indicates a lack of hydraulic niche partitioning in this woodland community.
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