Drought-induced defoliation and long periods of near-zero gas exchange play a key role in accentuating metabolic decline of Scots pine

1. Chronic and episodic drought drive physiological and structural adjustments in trees, allowing them to survive under severe water deficits, but, sometimes, compromising their long-term survival and resilience in response to reduced water availability.
2. Recent evidence has shown that drought-induced defoliation in southern populations of Scots pine (Pinus sylvestris L) is associated with carbon depletion and increased mortality risk. However, whether defoliated trees also show an enhanced physiological sensitivity to drought has never been addressed.
3. We measured leaf area-based sap flow, predawn and midday needle water potentials and whole-tree hydraulic conductance in a declining Scots pine population in NE Spain during typical (2010) and extreme drought conditions (2011). Seasonal courses and drought sensitivity of these variables was assessed for defoliated and non-defoliated pines growing side by side, and analysed using linear and non-linear mixed-effects models.
4. Defoliated Scots pines showed higher maximum sap flow per unit leaf area during late spring but were more sensitive to summer drought, compared to non-defoliated pines. This pattern was associated to a steeper decline in soil-to-leaf hydraulic conductance with drought and an enhanced sensitivity of canopy conductance to soil water availability in defoliated pines.
5. Near-homeostasis in midday water potentials was observed across years and defoliation classes, with minimum midday values of -2.5 MPa, which are at the lower limit of the range of values observed for the species.
6. Reduced canopy leaf area, enhanced sensitivity to drought and prolonged periods of near-zero gas exchange (up to 5 months for the extreme drought in 2011) were consistent with decreased vigour and low levels of carbohydrate reserves in defoliated trees.
7. Our results support the critical link between defoliation, water and carbon availability and their key role determining tree survival and recovery under drought. Nevertheless, biotic factors may also amplify the effects of drought and increase mortality risk in vulnerable trees.