Drought-induced dieback of Pinus nigra: a tale of hydraulic failure and carbon starvation

Abstract

Ongoing climate change is apparently increasing tree mortality rates, and understanding mechanisms of drought-induced tree decline can improve mortality projections. Differential drought impact on conspecific individuals within a population has been reported, but no clear mechanistic explanation for this pattern has emerged. Following a severe drought (summer 2012), we monitored over a 3-year period healthy (H) and declining (D) Pinus nigra trees co-occurring in a karstic woodland to highlight eventual individual-specific physiological differences underlying differential canopy dieback. We investigated differences in water and carbon metabolism, and xylem anatomy as a function of crown health status, as well as eventual genotypic basis of contrasting drought responses. H and D trees exploited the same water pools and relied on similar hydraulic strategies to cope with drought stress. Genetic analyses did not highlight differences between groups in terms of geographical provenance. Hydraulic and anatomical analyses showed conflicting results. The hydraulic tracheid diameter and theoretical hydraulic conductivity were similar, but D trees were characterized by lower water transport efficiency, greater vulnerability to xylem conduit implosion and reduced carbohydrate stores. Our results suggest that extreme drought events can have different impacts on conspecific individuals, with differential vulnerability to xylem embolism likely playing a major role in setting the fate of trees under climate change.

Keywords: Black pine; carbon metabolism; drought; plastome; rooting depth; water status.

Figure 1

Vulnerability curves (VCs) reporting the relationship between stem-specific hydraulic conductivity (K_s) and xylem water potential (Ψ_xyl), as measured for healthy (H, closed circles, solid line) and desiccated (D, open circles, dashed line) P. nigra trees. The sigmoidal regressions are also reported. The Ψ_xyl inducing 20 (P₂₀) and 50 (P₅₀) % loss of K_s were −1.67 and −3.24 MPa, and −1.42 and −3.63 MPa for H and D group, respectively (fit-PLC, Duursma and Choat, 2016). The insets show the VC of H trees based on K_s data that were within the observable range for both populations (0.03–0.68 kg s⁻¹ MPa⁻¹ m⁻¹).

Figure 2

Relationship between relative leaf conductance to water vapour (g_{L_REL}), as measured in H (closed circles, solid line) and D (open circles, dashed line) branches at progressively lower leaf water potential (Ψ_leaf). Coefficients of the linear regressions are also reported.

Figure 3

Oxygen isotopic composition of xylem sap (δ¹⁸O) extracted from branches of healthy (H, black columns) and desiccated (D, grey columns) individuals in June and July 2015. Mean ± standard error of the mean (SEM) are reported. Lower-case letters denote a significant difference between sampling seasons (June vs July), while differences between D and H trees were not significant (two-way ANOVA). No statistically significant interaction between factors was observed.

Figure 4

Glucose (a), fructose (b), sucrose (c) and starch (d) concentration measured in bark and wood of H (black and grey dashed columns, respectively) and D (white and white dashed columns, respectively) trees in June and July 2015. Mean ± SEM are reported. Upper-case letters and asterisks indicate statistically significant difference (P < 0.05) between health classes (Factor I) and growing seasons (Factor III), respectively. For sucrose and starch statistically significant differences between wood and bark tissue (Factor II) was also observed. Complete output of the three-way ANOVA in Table S2