Stem and leaf xylem of angiosperm trees experiences minimal embolism in temperate forests during two consecutive summers with moderate drought

Abstract

Drought events may increase the likelihood that the plant water transport system becomes interrupted by embolism. Yet our knowledge about the temporal frequency of xylem embolism in the field is frequently lacking, as it requires detailed, long‐term measurements. We measured xylem embolism resistance and midday xylem water potentials during the consecutive summers of 2019 and 2020 to estimate maximum levels of embolism in leaf and stem xylem of ten temperate angiosperm tree species. We also studied vessel and pit membrane characteristics based on light and electron microscopy to corroborate potential differences in embolism resistance between leaves and stems. Apart from A. pseudoplatanus and Q. petraea, eight species experienced minimum xylem water potentials that were close to or below those required to initiate embolism. Water potentials corresponding to ca. 12% loss of hydraulic conductivity (PLC) could occur in six species, while considerable levels of embolism around 50% PLC were limited to B. pendula and C. avellana. There was a general agreement in embolism resistance between stems and leaves, with leaves being equally or more resistant than stems. Also, xylem embolism resistance was significantly correlated to intervessel pit membrane thickness (TPM) for stems, but not to vessel diameter and total intervessel pit membrane surface area of a vessel. Our data indicate that low amounts of embolism occur in most species during moderate summer drought, and that considerable levels of embolism are uncommon. Moreover, our experimental and TPM data show that leaf xylem is generally no more vulnerable than stem xylem.

Functional xylem characteristics associated with drought‐induced embolism in angiosperms

“…For instance, various papers have suggested that leaves with narrow vessels have more vulnerable xylem than the xylem in perennial shoots including wider vessels (Pivovaroff et al ., 2014; Charrier et al ., 2016; Johnson et al ., 2016; Creek et al ., 2018; Skelton et al ., 2019), or that roots are more vulnerable than stems (Alder et al ., 1996; Hacke et al ., 2000; Martínez‐Vilalta et al ., 2002; Maherali et al ., 2006; Pratt et al ., 2007, 2015a), although the generally longer vessels in roots may have led to an overestimation of root vulnerability in some angiosperm studies (as mentioned previously). Other studies found that the xylem tissue of leaves, stems, and roots is more or less equally resistant to embolism (Skelton et al ., 2017; Creek et al ., 2018; Wason et al ., 2018; Losso et al ., 2019; Smith‐Martin et al ., 2020; Wu et al ., 2020; Levionnois et al ., 2020b; Lübbe et al ., 2022), or that leaves are more resistant to embolism than stems in some species (Zhu et al ., 2016; Klepsch et al ., 2018; Levionnois et al ., 2020b; Guan et al ., 2022). What clearly emerges from these studies is that (1) conduit diameter is not a good proxy for drought‐induced embolism resistance at the whole‐plant level, (2) distal tissues (leaves, twigs) are not necessarily more vulnerable than proximal tissues (main roots, stems) in the same individuals as predicted by the vulnerability segmentation hypothesis (Tyree & Ewers, 1991), (3) hydraulic measurements from only the most resistant organ may lead to a poor correlation between traits and climate, and (4) methodological differences should be carefully considered.…”

“…Assuming that embolism is strongly determined by the water potential of xylem sap, the case for drought‐induced embolism being a rare event is supported by the most negative water potential measurements within a growing season ( P min ). Indeed, P min was found to account for < 20% loss of stem conductivity among grasses (Lens et al ., 2016) and < 12% in various temperate tree species (Wason et al ., 2018; Guan et al ., 2022). Furthermore, it has been shown that the hydraulic safety margin (HSM), which can be defined as the difference between P min and P 88 , is overall positive (+2 MPa) across angiosperm species and biomes (Choat et al ., 2012), suggesting that lethal levels of embolism are only reached after an exceptionally intense episode of drought (Delzon & Cochard, 2014).…”

Seeing is believing: what visualising bubbles in the xylem has revealed about plant hydraulic function

“…Another intrinsic limitation to the OV method is that it cannot detect native or pre-existing embolism (Chen et al 2021), which can impact quantification of relative xylem embolism resistance (Avila et al 2022), and the translation of embolised xylem area to a percent loss of K. As such, only plants cultivated under well-water conditions, plants that have been previously exposed to drought but are known to refill their xylem (Cardoso et al 2018), and branches and leaves formed during wet seasons (which are expected to have very low levels of pre-existing embolism) are ideal to construct VCs with the OV method. Recently, it has been suggested that significant native embolism produced by drought is restricted to very extreme events in field grown trees, so the issue of pre-existing embolism on accurate VC determination in field grown plants may be minimal (Guan et al 2022;Wagner et al 2022). It is important to maintain the plant material in plastic bags with damp paper towels until the beginning of experiments whenever collecting branches in the field to construct VCs in order to prevent excessive water loss and any potential embolism prior to analysis (Skelton et al 2021).…”

Vessel tapering is conserved along a precipitation gradient in tropical trees of the genus Cedrela

“…Whilst there is some debate about whether embolism occurs in the trunks of tall trees, Wason et al (2018) show that water potentials may become low enough in the trunks of canopy trees to cause air seeding in some species. Furthermore, Guan et al 2022 showed little difference between leaves and stems in their hydraulic safety margins, thereby suggesting that stems are as likely to form embolism as more apical tissues. Observations suggest that tall trees suffer indeed higher mortality during droughts (Bennett et al 2015;Johnson et al 2018b;Stovall et al 2019), possibly due to greater occurrences of embolism.…”