Mediterranean forests in a changing environment - Impacts of drought and temperature stress on tree physiology

Abstract

The Mediterranean Basin is a climate-change hotspot of the world. Predicted reductions in annual precipitation, increases in mean temperature, and increases in the variability and occurrence of extreme droughts and heat waves are likely to affect species abundance and distribution. The existence of sympatric plants with different morphological and phenological strategies raises the question how they will respond to novel climate conditions. There is a strong need to improve the mechanistic understanding of key foliar ecophysiological parameters in response to abiotic stressors on a small scale if we are to predict the carbon budget of plant ecosystems in larger scales. We first reviewed contrasting growth responses to temperature of angio- and gymnosperms in the Iberian Peninsula. Secondly, we studied the seasonal acclimation of different foliar ecophysiological traits in two leaf positions of four Mediterranean tree species in extensive field experiments. We aimed to shed light on the mechanistic understanding of the foliar respiratory and photosynthetic responses to abiotic stress such as drought and temperature.

We found contrasting demographic responses in Mediterranean conifer and angiosperm trees. Widespread forest successional advance of angiosperms and negative growth responses of gymnosperms to temperature are currently occurring in the Iberian Peninsula. Trait-based differences in these two groups contribute to explain their different responses to temperature and their different role during successional processes. The acclimation behaviour of photosynthetic and morphological traits to seasonal variable growth conditions was strongly pronounced in all tree species. Photosynthetic machineries were resilient to moderate drought, whereas severe drought induced acclimation of morphological traits, photosynthetic downregulation and leaf abscission. The lack of replenishment of soil-water reserves during the early growing season critically enforced the summer drought. We also observed a notable seasonal acclimation of the thermal optima and of the curvature of temperature responses of photosynthetic assimilation. The photosynthetic system was better acclimated to lower temperatures in winter and to heat stress in the drier and hotter year. Mild winter temperatures provided a period of growth and recovery that resulted in biochemical recovery, new shoot growth, and moderate transpiration across all evergreen species. High radiation and sudden low temperatures had a combinatory negative effect on the photosynthetic apparatus leading to photoinhibitory stress -especially in sunlit leaves.

Species-specific acclimation partly offset these overall trends in responses to drought and temperature stress. Quercus ilex L. and to a lesser extent Q. pubescens Wild. showed the highest plasticity in photosynthetic traits whereas Pinus halepensis Mill. was most tolerant across the seasons with the most stable temperature response pattern. Arbutus. unedo L. was the most vulnerable to drought and photoinhibitory stress in winter. A. unedo and Q. pubescens had a less sclerophyllic leaf habit and invested the least in acclimation of the morphological structure being most vulnerable to drought-induced leaf abscission. Shaded leaves showed generally a lower photosynthetic potential, but cushioned negative impacts under stress periods. A long-term rainfall-exclusion experiment in a Q. ilex forest increased the foliar carbon-use efficiency and the plasticity of foliar respiratory and photosynthetic traits, but did not affect the biochemical photosynthetic potential. A favourable growth period was thus exploited more efficiently. Overall, our results indicate that Mediterranean climax-species exhibit a strong acclimatory capacity to warmer and drier conditions, but can be sensitive to extreme drought and extreme temperature stress. The performance of the plants during winter might give important insights in the dynamics of Mediterranean forest communities under novel environmental conditions. Leaf position is an indispensable factor when estimating the canopy carbon balance. Angiosperms and gymnosperms had fundamental different photosynthetic strategies of stress-avoidance versus stress-tolerance, respectively.

El cambio climático aumentará la sequía en la Cuenca Mediterránea y posiblemente afectará a la abundancia y la distribución de especies. Revisamos las respuestas contrastadas del crecimiento a la temperatura de angio- y gimnospermas en la Península Ibérica. Estudiamos la variación de los efectos del estrés térmico y por sequía en rasgos morfológicos, fotosintéticos y de la respiración foliar según la especie y la posición en el dosel. Además, evaluamos el efecto de una sequía crónica sobre la respiración foliar y la fotosíntesis de Quercus ilex L. La maquinaria fotosintética se mostró resiliente frente a la sequía moderada, mientras que la sequía extrema, agravada por las bajas reservas de agua en el suelo, indujo la aclimatación de la morfología foliar, la inhibición de la bioquímica fotosintética y la abscisión foliar. El sistema fotosintético se aclimató mejor a las temperaturas bajas que al estrés por calor. Las temperaturas suaves en invierno derivaron en la recuperación bioquímica, un nuevo crecimiento de los brotes y una transpiración moderada. La elevada radiación y el frío repentino mostraron un efecto combinado negativo, causando estrés fotoinhibitorio. El estrés térmico y por sequía fue más pronunciado en hojas de sol y aminorado en hojas de sombra. Q.ilex y, en menor grado, Q. pubescens Wild. mostraron la plasticidad más elevada de los rasgos fotosintéticos, mientras que Pinus halepensis Mill. fue más tolerante, mostrando la respuesta más estable a la temperatura. Arbutus unedo L. fue la especie más vulnerable a la sequía y al estrés fotoinhibitorio. En respuesta a la sequía crónica, Q. ilex incrementó la eficiencia en el uso del carbono y la plasticidad de los atributos fotosintéticos y de respiración foliar, pero no afectó al potencial fotosintético. En resumen, las especies climácicas mediterráneas se aclimatan frente a condiciones más cálidas y secas, pero pueden ser sensibles ante sequías extremas. El funcionamiento durante el invierno es vital para entender la dinámica de los bosques mediterráneos. La posición de las hojas en la copa es indispensable para estimar el balance de carbono del dosel. Angiospermas y gimnospermas presentan estrategias fotosintéticas contrastadas, de evitación y tolerancia del estrés, respectivamente.