Divergent Hydraulic Safety Strategies in Three Co-occurring Anacardiaceae Tree Species in a Chinese Savanna

Abstract

Vulnerability segmentation, the condition under which plant leaves are more vulnerable to drought-induced cavitation than stems, may act as a “safety valve” to protect stems from hydraulic failure. Evergreen, winter-deciduous, and drought-deciduous tree species co-occur in tropical savannas, but there have been no direct studies on the role of vulnerability segmentation and stomatal regulation in maintaining hydraulic safety in trees with these three leaf phenologies. To this end, we selected three Anacardiaceae tree species co-occurring in a Chinese savanna, evergreen Pistacia weinmanniifolia, drought-deciduous Terminthia paniculata, and winter-deciduous Lannea coromandelica, to study inter-species differentiation in leaf and stem hydraulic safety. We found that the two deciduous species had significantly higher sapwood-specific hydraulic conductivity and leaf-specific hydraulic conductance than the evergreen species. Moreover, two deciduous species were more vulnerable to stem cavitation than the evergreen species, although both drought-deciduous species and evergreen species had drought-resistance leaves. The evergreen species maintained a wide hydraulic safety margin (HSM) in stems and leaves; which was achieved by embolism resistance of both stems and leaves and isohydric stomatal control. Both deciduous species had limited HSMs in stems and leaves, being isohydric in the winter-deciduous species and anisohydric in drought-deciduous species. The difference in water potential at 50% loss of hydraulic conductivity between the leaves and the terminal stems (P50leaf−stem) was positive in P. weinmanniifolia and L. coromandelica, whereas, T. paniculata exhibited a lack of vulnerability segmentation. In addition, differences in hydraulic architecture were found to be closely related to other structural traits, i.e., leaf mass per area, wood density, and sapwood anatomy. Overall, the winter-deciduous species exhibits a drought-avoidance strategy that maintains the hydraulic safety of the more carbon-costly stems by sacrificing cheaper and more vulnerable leaves, while the evergreen species exhibits a hydraulic strategy of drought tolerance with strong stomatal regulation. In contrast, the drought-deciduous species lacks vulnerability segmentation and sheds leaves at the expense of top shoots during peak drought. This study demonstrates that even sympatric tree species that differ in leaf phenology can exhibit divergent adaptive hydraulic safety strategies.

More than iso/anisohydry: Hydroscapes integrate plant water use and drought tolerance traits in 10 eucalypt species from contrasting climates

“…The relationship between hydraulic segmentation and the degree of isohydricity has been rarely examined. In the study of Pivovaroff et al (), no clear pattern between daily range of leaf water potential and HSM HS was observed, but Zhang et al () reported positive safety margins in more isohydric species. In the current study, hydraulic vulnerability was less variable in leaves than stems, which may be due to the notion that leaf hydraulic traits, including embolism resistance, may be responsive to growth conditions (Blackman et al, ; Johnson et al, ).…”

“…These hydraulic traits characterizing plant vulnerability to embolism are often well correlated with climatic factors across species, therefore informing the evolutionary drivers shaping the adaptation of drought response strategies (Blackman et al, ; Bourne, Creek, Peters, Ellsworth, & Choat, ; Choat et al, ; Li, Blackman, Choat, et al, ; Skelton et al, ; Trueba et al, ). In addition, significant differences between leaf and stem vulnerability provide evidence for hydraulic vulnerability segmentation (HSM HS ), a strategy that minimizes water loss during drought via leaf shedding (Pivovaroff, Sack, & Santiago, ; Zhang, Zhang, & Cao, ; Zhu, Liu, Xu, Cao, & Ye, ). Given their functional significance, examining how different metrics are related to these key drought tolerance traits will advance our understanding on species life‐history strategies, as well as helping to identify species at risk of drought mortality and clarifying the underlying mechanisms providing drought tolerance.…”

“…These hydraulic traits characterizing plant vulnerability to embolism are often well correlated with climatic factors across species, therefore informing the evolutionary drivers shaping the adaptation of drought response strategies (Blackman et al, 2014;Bourne, Creek, Peters, Ellsworth, & Choat, 2017;Choat et al, 2012;Skelton et al, 2018;Trueba et al, 2017). In addition, significant differences between leaf and stem vulnerability provide evidence for hydraulic vulnerability segmentation (HSM HS ), a strategy that minimizes water loss during drought via leaf shedding (Pivovaroff, Sack, & Santiago, 2014;Zhang, Zhang, & Cao, 2017;Zhu, Liu, Xu, Cao, & Ye, 2016).…”

An experimental assessment of the impact of drought and fire on western larch injury, mortality and recovery

“…It is important to note that the mortality hypothesis presented in the present study may not translate to larger trees. For example, drought-induced crown dieback in larger trees often occurs at the periphery of the tree crown (Rood et al 2000;Sperry et al 2002;Zhang et al 2017), rather than sequential senescence observed in the current study, where older leaves senesce first to supply nutrients to younger leaves and shoots (Munné-Bosch and Alegre 2004). As low-intensity fires typically scorch tree crowns from the bottom up, senescing foliage at the periphery of a large tree crown may not provide the post-fire recovery advantage hypothesised for saplings.…”

Tree hydraulic traits are coordinated and strongly linked to climate‐of‐origin across a rainfall gradient

“…With regard to plant water relations, the trade‐off between hydraulic safety (P 50 ) and efficiency (K s ) has been intensively studied. Although this trade‐off has been observed in many studies (Bourne et al, ; Lens et al, ; Markesteijn, Poorter, Paz, Sack, & Bongers, ; Zhang, Zhang, & Cao, ), a meta‐analysis of diverse species across a global dataset suggests that the trade‐off between these two traits is significant but weak (Gleason et al, ). Another important facet of xylem structure and function is a proposed trait trade‐off between storage and biomechanical strength and support (McCulloh et al, ; Scholz et al, ).…”