The “isohydric trap”: A proposed feedback between water shortage, stomatal regulation, and nutrient acquisition drives differential growth and survival of European pines under climatic dryness

Abstract

Climatic dryness imposes limitations on vascular plant growth by reducing stomatal conductance, thereby decreasing CO uptake and transpiration. Given that transpiration-driven water flow is required for nutrient uptake, climatic stress-induced nutrient deficit could be a key mechanism for decreased plant performance under prolonged drought. We propose the existence of an "isohydric trap," a dryness-induced detrimental feedback leading to nutrient deficit and stoichiometry imbalance in strict isohydric species. We tested this framework in a common garden experiment with 840 individuals of four ecologically contrasting European pines (Pinus halepensis, P. nigra, P. sylvestris, and P. uncinata) at a site with high temperature and low soil water availability. We measured growth, survival, photochemical efficiency, stem water potentials, leaf isotopic composition (δ C, δ O), and nutrient concentrations (C, N, P, K, Zn, Cu). After 2 years, the Mediterranean species Pinus halepensis showed lower δ O and higher δ C values than the other species, indicating higher time-integrated transpiration and water-use efficiency (WUE), along with lower predawn and midday water potentials, higher photochemical efficiency, higher leaf P, and K concentrations, more balanced N:P and N:K ratios, and much greater dry-biomass (up to 63-fold) and survival (100%). Conversely, the more mesic mountain pine species showed higher leaf δ O and lower δ C, indicating lower transpiration and WUE, higher water potentials, severe P and K deficiencies and N:P and N:K imbalances, and poorer photochemical efficiency, growth, and survival. These results support our hypothesis that vascular plant species with tight stomatal regulation of transpiration can become trapped in a feedback cycle of nutrient deficit and imbalance that exacerbates the detrimental impacts of climatic dryness on performance. This overlooked feedback mechanism may hamper the ability of isohydric species to respond to ongoing global change, by aggravating the interactive impacts of stoichiometric imbalance and water stress caused by anthropogenic N deposition and hotter droughts, respectively.

Chemical and isotopic markers detect water deficit and its influence on nutrient allocation in Phaseolus vulgaris

“…the 'isohydric trap' feedback loop in European Pines found that strong stomatal regulation led to a series of physiological changes (detected for example using carbon isotope abundance) that ultimately culminate in a severe mineral nutrient imbalance and reduced ability to tolerate drought stress. While some of the results described by Salazar-Tortosa et al (2018) were similar to the findings in this study for leaf and phloem tissue, we demonstrate that the investment in reproductive tissue, particularly important for crop species, overrides any concern for a long term feedback loop as was observed in European Pines. Fig.…”

“…Despite detecting a higher nutrient content in well‐watered compared to water deficit treatment plants, the results were variable, therefore no statistically significant differences for any nutrients or amino acids were found in response to treatment or development stage within the soluble leaf, soluble and total pod pools. The recent work of Salazar‐Tortosa et al () describing the ‘isohydric trap’ feedback loop in European Pines found that strong stomatal regulation led to a series of physiological changes (detected for example using carbon isotope abundance) that ultimately culminate in a severe mineral nutrient imbalance and reduced ability to tolerate drought stress. While some of the results described by Salazar‐Tortosa et al () were similar to the findings in this study for leaf and phloem tissue, we demonstrate that the investment in reproductive tissue, particularly important for crop species, overrides any concern for a long term feedback loop as was observed in European Pines.…”

“…Despite detecting a higher nutrient content in well-watered compared to water deficit treatment plants, the results were variable, therefore no statistically significant differences for any nutrients or amino acids were found in response to treatment or development stage within the soluble leaf, soluble and total pod pools. The recent work of Salazar-Tortosa et al (2018) describing Fig. 6.…”

Rooting big and deep rapidly: the ecological roots of pine species distribution in southern Europe

“…Pinus halepensis, P. pinea and to a lesser extent P. pinaster are less frost-tolerant than the high-mountain pines P. sylvestris and P. nigra (Climent et al 2009;Fernández et al 2017;Toca et al 2017). However, the fact that P. sylvestris and P. nigra do not occur at low-altitude locations where summers are dry and hot could be explained by a lower capacity to survive water stress than Mediterranean pines in the early life stages (Salazar-Tortosa et al 2018).…”

Effect of Herbaceous Layer Interference on the Post-Fire Regeneration of a Serotinous Pine (Pinus pinaster Aiton) across Two Seedling Ages

“…Larger pine seedlings (both within and across years) likely had a larger root system, which would have reduced competition with the shallow root system of most forbs and grasses [5]. In addition, nutrient acquisition by the pine seedlings may improve with better access to soil water [5,53], thereby reinforcing the positive effect of a larger size.…”