ADAPTIVE VARIATION IN THE VULNERABILITY OF WOODY PLANTS TO XYLEM CAVITATION

Abstract

The ability of plants to supply water to their leaves is intimately associated with survival. Water supply to leaves depends on maintaining an intact water column in the xylem from the roots to shoots. Because this hydraulic pathway is under tension, it is vulnerable to breakage through the induction of air emboli (cavitation). Although the physiological benefit of resistance to water-stress-induced xylem cavitation for desiccation tolerance is clear, there is considerable interspecific variation within and across climates. To understand the adaptive significance of this variation and the potential trade-off with water transport, we compiled a database of 167 species from 50 seed plant families and examined relationships among resistance to xylem cavitation, water transport capacity (as determined by the specific conductivity of xylem [KS]), and climate. Relationships were evaluated using standard cross-species correlations (r). Because inferences about the adaptive significance of these correlations can be biased by the potential similarity of closely related species, we also analyzed our data using phylogenetically independent contrast correlations (PIC) calculated over a range of alternate seed plant phylogenies. Resistance to cavitation, expressed as the xylem tension at which 50% of hydraulic conductivity was lost (Ψ50), ranged from −0.18 to −9.9 MPa for angiosperms and from −1.5 to −14.1 MPa for conifers. Conifers were most resistant to cavitation, with mean Ψ50 80% more negative than angiosperms. In contrast, KS was 270% higher in angiosperms than conifers. Across all species, cavitation resistance increased with decreasing mean annual precipitation. However, significant phylogenetically independent contrast correlations between Ψ50 and annual precipitation were found within the evergreen angiosperms and conifers but not in the deciduous angiosperms. Thus, the adaptive significance of increased resistance to cavitation as a mechanism of drought tolerance may be of primary importance in evergreen angiosperms and conifers. In contrast, analysis of independent contrasts indicated that KS increased with decreasing rainfall in deciduous angiosperms, whereas there was no association between KS and water availability for evergreen angiosperms and conifers. These results suggest that the evolution of increased KS may be a critical adaptation to water limitation in deciduous angiosperms. Although there was a significant cross-species correlation between Ψ50 and KS, this relationship was not supported by the independent contrast correlation, suggesting that the evolutionary basis for a trade-off between cavitation resistance and water transport capacity is weak.