Large physiological plasticity of water- and nutrient-use traits in Quercus ilex L. within and across populations: Implications for Mediterranean forest persistence under global change

Abstract

Functional traits are essential for predicting plant responses to environmental changes, yet understanding within-species trait variability is complex due to multiple influencing factors. Long-lived trees, like the holm oak (Quercus ilex L.), are expected to respond to abiotic variations largely through phenotypic plasticity, so a better understanding of these plastic responses is key to managing climate change impacts on forests. To investigate intra-specific variations in ecophysiological performance under dry Mediterranean conditions, we measured isotopic, nutrient, and growth traits in 240 four-year-old holm oaks from various populations and mother trees grown in a common garden experiment. Contrary to expectations, we found little ecotypic differentiation in isotopic, nutrient, or growth traits among geographically distant populations with contrasting climates, elevations, and lithologies. Leaf Δ¹⁸O_enrichment and δ¹³C values ranged widely across and within populations, indicating large variability in time-integrated stomatal conductance and water-use efficiency among neighboring oaks grown under the same dry conditions. Both Δ¹⁸O_enrichment and δ¹³C exhibited negative relationships with leaf C/P and C/K ratios, revealing a trade-off between water-use efficiency and nutrient-use efficiency that was primarily driven by changes in stomatal regulation stringency depending on leaf nutrient status. Holm oaks from all populations were capable of fine-tuning their leaf gas exchange to prioritize efficient use of the most limiting resource for photosynthesis and growth (water versus nutrients). Phosphorus deficiency and stoichiometric N/P imbalance led to lower water-use efficiency and poorer growth. We conclude that all studied holm oak populations possess sufficient phenotypic plasticity and/or genetic diversity to withstand heat and drought stress intensification through adaptive adjustments of their physiological and nutrient traits. Nonetheless, phosphorus fertilization could greatly enhance forest restoration success amid increasing climatic aridity and human-driven N/P imbalance. These findings hold important implications for a better understanding of holm oaks persistence under rapid climate warming and aridification across the Mediterranean region.