Sequence of plant responses to droughts of different timescales: lessons from holm oak (Quercus ilex) forests

The functional traits of plants in regions of the world with a Mediterranean climate have been shaped to tolerate periods of water deficit. These species are adapted to summer droughts but may not be able to cope with future increases in drought intensity, duration, and/or frequency. Here, we review the mechanisms and traits of drought resistance and recovery of the well-studied holm oak (Quercus ilex), which we propose as a model species for Mediterranean-type ecosystems. Our aim was to understand the differences and links between the responses of Q. ilex to summer droughts, extreme droughts, and long-term drought experiments. A main goal was to provide an integral picture of drought responses across organisational and temporal scales for identifying the most relevant processes that are likely to contribute to determining the future of Mediterranean vegetation. Evidence from long-term drought experiments showed that acclimation processes from the molecular (e.g. epigenetic changes) to the ecosystem level (e.g. reductions in stand density) mitigate the effects of drought. Changes in leaf morphology and hydraulics, leaf-to-shoot allometry, and root functioning are among the key mechanisms for overcoming increasing drought. The duration of drought determines its severity in terms of canopy loss and stem mortality. Although Q. ilex can vigorously resprout after such episodes, its resilience may be subsequently reduced. In the future, higher frequency of return of extreme droughts will challenge thus the capacity of these forests to recover. The insights provided by this review of the complex interplay of processes that determine the response of trees to droughts of different duration, intensity, and frequency will also help us to understand the likely responses of other resprouting angiosperms in seasonally dry ecosystems that share similar functional traits with Q. ilex.     

Establishment of co‐existing Mediterranean tree species under a varying soil moisture regime

We investigated the responses of two co‐existing Mediterranean trees with different regeneration strategies (Phillyrea latifolia seedlings and Quercus ilex sprouts) to experimental drought below the forest canopy. We considered different recruitment stages and used leaf isotopic discrimination to estimate water use efficiency (WUE) and nitrogen availability and use. Drought decreased the emergence and survival of seedlings and sprouts. Survival and growth of older saplings were not influenced by drought. Seedling emergence of P. latifolia was higher than Q. ilex sprout production, but Q. ilex sprouts had higher survival and growth rates. These differences disappeared in the sapling stage. Carbon isotopic discrimination suggested that Q. ilex sprouts had higher WUE than P. latifolia seedlings. Drought increased WUE of recruits, particularly in Q. ilex. Water use regulation increased with ageing, particularly in P. latifolia. Q. ilex had higher δ¹⁵N values than P. latifolia; these were also higher under drier soil conditions. Current year seedlings had higher δ¹⁵N than saplings, particularly in P. latifolia, suggesting they exploit superficial soil layers. These results suggest that sprouts obtain benefit from resources stored in parent plants. At earlier stages, they perform better than seedlings. This response is not coupled to adult vulnerability to drought for these species, revealing the difficulty of predicting species dynamics during climate change.     

Dampening effects of long‐term experimental drought on growth and mortality rates of a Holm oak forest

Forests respond to increasing intensities and frequencies of drought by reducing growth and with higher tree mortality rates. Little is known, however, about the long‐term consequences of generally drier conditions and more frequent extreme droughts. A Holm oak forest was exposed to experimental rainfall manipulation for 13 years to study the effect of increasing drought on growth and mortality of the dominant species Quercus ilex, Phillyrea latifolia, and Arbutus unedo. The drought treatment reduced stem growth of A. unedo (?66.5%) and Q. ilex (?17.5%), whereas P. latifolia remained unaffected. Higher stem mortality rates were noticeable in Q. ilex (+42.3%), but not in the other two species. Stem growth was a function of the drought index of early spring in the three species. Stem mortality rates depended on the drought index of winter and spring for Q. ilex and in spring and summer for P. latifolia, but showed no relation to climate in A. unedo. Following a long and intense drought (2005–2006), stem growth of Q. ilex and P. latifolia increased, whereas it decreased in A. unedo. Q. ilex also enhanced its survival after this period. Furthermore, the effect of drought treatment on stem growth in Q. ilex and A. unedo was attenuated as the study progressed. These results highlight the different vulnerabilities of Mediterranean species to more frequent and intense droughts, which may lead to partial species substitution and changes in forest structure and thus in carbon uptake. The response to drought, however, changed over time. Decreased intra‐ and interspecific competition after extreme events with high mortality, together with probable morphological and physiological acclimation to drought during the study period, may, at least in the short term, buffer forests against drier conditions. The long‐term effects of drought consequently deserve more attention, because the ecosystemic responses are unlikely to be stable over time.Nontechnical summaryIn this study, we evaluate the effect of long‐term (13 years) experimental drought on growth and mortality rates of three forest Mediterranean species, and their response to the different intensities and durations of natural drought. We provide evidence for species‐specific responses to drought, what may eventually lead to a partial community shift favoring the more drought‐resistant species. However, we also report a dampening of the treatment effect on the two drought‐sensitive species, which may indicate a potential adaptation to drier conditions at the ecosystem or population level. These results are thus relevant to account for the stabilizing processes that would alter the initial response of ecosystem to drought through changes in plant physiology, morphology, and demography compensation.     

Contrasting impacts of continuous moderate drought and episodic severe droughts on the aboveground‐biomass increment and litterfall of three coexisting Mediterranean woody species

Climate change is predicted to increase the aridity in the Mediterranean Basin and severely affect forest productivity and composition. The responses of forests to different timescales of drought, however, are still poorly understood because extreme and persistent moderate droughts can produce nonlinear responses in plants. We conducted a rainfall‐manipulation experiment in a Mediterranean forest dominated by Quercus ilex, Phillyrea latifolia, and Arbutus unedo in the Prades Mountains in southern Catalonia from 1999 to 2014. The experimental drought significantly decreased forest aboveground‐biomass increment (ABI), tended to increase the litterfall, and decreased aboveground net primary production throughout the 15 years of the study. The responses to the experimental drought were highly species‐specific. A. unedo suffered a significant reduction in ABI, Q. ilex experienced a decrease during the early experiment (1999–2003) and in the extreme droughts of 2005–2006 and 2011–2012, and P. latifolia was unaffected by the treatment. The drought treatment significantly increased branch litterfall, especially in the extremely dry year of 2011, and also increased overall leaf litterfall. The drought treatment reduced the fruit production of Q. ilex, which affected seedling recruitment. The ABIs of all species were highly correlated with SPEI in early spring, whereas the branch litterfalls were better correlated with summer SPEIs and the leaf and fruit litterfalls were better correlated with autumn SPEIs. These species‐specific responses indicated that the dominant species (Q. ilex) could be partially replaced by the drought‐resistant species (P. latifolia). However, the results of this long‐term study also suggest that the effect of drought treatment has been dampened over time, probably due to a combination of demographic compensation, morphological and physiological acclimation, and epigenetic changes. However, the structure of community (e.g., species composition, dominance, and stand density) may be reordered when a certain drought threshold is reached.     

Biodiversity in different successional stages of Mediterranean enclaves distributed along Sinop Peninsula (Turkey)

The aim of this research was to evaluate plant diversity and the relationships between the distribution of Raunkiaer life forms and community structure, and species richness, at different successional stages in communities of Quercus ilex L., Erica arborea L. and Sarcopoterium spinosum (L.) Spach., distributed as enclaves in Sinop Province. Permanent sample plots were selected to determine plant diversity. The cover percentage of each plant species was recorded monthly during two vegetation periods. Raunkiaer life forms, and the Shannon–Wiener, Evenness, Simpson and Margalef indexes were determined. Twenty-three species in Quercus ilex, 96 species in Erica arborea, and 148 species in Sarcopoterium spinosum were identified. Hemicryptophyte dominancy was observed followed by phanerophytes in the Q. ilex community, and therophyte and hemicryptophyte dominancy in the E. arborea and S. spinosum communities, respectively. It was determined that the S. spinosum community was the most heterogeneous community while the Q. ilex community was more uniform than other communities. The variation in diversity indexes, homogeneity, and composition of life forms among communities adopting a similar climatic environment could result from a differentiation of environmental factors, which impact on community structuring, from biotic to abiotic at different successional stages of Mediterranean communities.     

Drought stress does not protect Quercus ilex L. from ozone effects: results from a comparative study of two subspecies differing in ozone sensitivity

Long‐term effects of ozone (O₃) exposure and drought stress were assessed on two subspecies of Quercus ilex: ssp. ilex and ssp. ballota. Two‐year‐old seedlings were continuously exposed for 26 months in open‐top chambers to three O₃ treatments: charcoal filtered air, non‐filtered air and non‐filtered air supplemented with 40 nl·l^?1 O₃. Additionally, two irrigation regimes were adopted: half of the plants were well‐watered and the others received half of the water supplied to control plants. Growth, shoot water potential and gas exchange rates were assessed seasonally, and biomass accumulation was determined at the end of the experiment. Drought stress caused higher reductions of gas exchange, growth and biomass accumulation than O₃ exposure in both subspecies. The combination of O₃ and drought stress caused further decreases of accumulated aboveground biomass but no additive effects were observed on gas exchange rates or root biomass. Thus, drought stress did not protect Q. ilex from O₃ effects on biomass when the response of the whole plant was considered. Q. ilex ssp. ballota was more sensitive to O₃ and ssp. ilex was more affected by drought stress. The different O₃ sensitivity was not only related to pollutant uptake but also to the ability of plants for resource acquisition and allocation. Based on biomass dose–response functions, Q. ilex is more resistant to O₃ than other European evergreen tree species, however, O₃ represents an additional stress factor that might be impairing plant ability to withstand current and future climate change.     

Effects of a severe drought on Quercus ilex radial growth and xylem anatomy

We assessed the response of Quercus ilex subsp. ballota to the severe summer drought recorded in 1994 in NE Spain through the study of changes in radial growth and wood anatomy. We selected a coppice stand in the Iberian Peninsula, which is characterized by a Mediterranean climate under continental influence. We measured internode length, tree-ring width, mean and maximum vessel diameter, and vessel density for 1981–1997. The annual predicted hydraulic conductance (K_h) was calculated following Hagen-Poisseuille's law. We compared the tree-ring width, vessel diameter and K_h of Q. ilex subsp. ballota and co-existing ring-porous oaks (Q. faginea, Q. pyrenaica) for a dry summer (1994) and a wet summer (1997). To evaluate the drought-resistance of xylem for Q. ilex subsp. ballota (dominant under continental conditions) and Q. ilex subsp. ilex (dominant in mild areas) we determined vulnerability curves. Dimensionless indices of internode length, tree-ring width, and vessel density were compared with climatic data (monthly total precipitation and mean temperature) using correlation analyses. Internode length, tree-ring width, K_h, and mean and maximum vessel diameter declined in 1994. According to vulnerability curves, Q. ilex subsp. ballota showed a greater drought resistance than Q. ilex subsp. ilex. During the year of growth, we found a positive influence of January and June–August precipitation on the internode length, tree-ring width, and vessel density. The response of Q. ilex subsp. ballota radial-growth to summer drought was comparable to that of Q. faginea latewood. Overall, growth and wood anatomy of Q. ilex subsp. ballota showed a plastic response to drought.     

Summer-drought constrains the phenology and growth of two coexisting Mediterranean oaks with contrasting leaf habit: implications for their persistence and reproduction

This study analyses how coexisting evergreen and deciduous oaks adjust their phenology to cope with the stressful Mediterranean summer conditions. We test the hypothesis that the vegetative and reproductive growth of the winter deciduous (Quercus faginea Lam.) is more affected by summer drought than that of the evergreen [Quercus ilex L. subsp. ballota (Desf.) Samp.]. First, we assessed the complete aboveground phenology of both species during two consecutive years. Shoot and litter production and bud, acorn and secondary growth were monitored monthly. Second, we identified several parameters affected by summer conditions: apical bud size, individual leaf area (LA), leaf mass per area (LMA) and acorn yield in both species, and leaf-fall in Q. faginea; and analysed their variation over 10 years. Q. ilex performed up to 25% of shoot growth and most leaf development during summer, whereas Q. faginea completed most of both phenophases during spring. Secondary growth was arrested in summer under drought conditions. Approximately, 30–40% of bud and 40–50% of acorn growth was undertaken during summer in both species. Summer drought related to differences in LA, LMA and leaf senescence, but not to acorn yield. Both species had similar year-to-year patterns of acorn production, though yields were always lower in Q. faginea. Bud size decreased severely in both species during extremely dry years. In Q. ilex, bud size tended to alternate between years of large and small buds, and these patterns were followed by opposite trends in stem length. In Q. faginea, bud size was more stable through time. Q. ilex was more phenologically active during summer than Q. faginea, indicating a higher tolerance to drought. Furthermore, bud and fruit growth (the only two phenophases that both species performed during summer) were more severely affected by summer drought in Q. faginea than in the evergreen. The differential effects of summer drought on key phenophases for the persistence (bud growth) and colonization ability (fruit production) of both species may have consequences for their coexistence.     

Field-simulated droughts affect elemental leaf stoichiometry in Mediterranean forests and shrublands

This study evaluated the change induced by the year season and by experimentally induced drought on foliar element stoichiometry of the predominant woody species (Quercus ilex and Erica multiflora) in two Mediterranean ecosystems, a forest and a shrubland. This study is based in two long-term (11 yr) field experiments that simulated drought throughout the annual cycle.The effects of experimental droughts were significant but weaker than the changes produced by ontogeny and seasonality. Leaf N and P concentrations were higher in spring (the main growing season) in E. multiflora and, in Q. ilex in autumn (a period of additional growth). Leaf N:P ratios were lower in spring. In Q. ilex, the highest leaf K concentrations and leaf K:P ratios, and the lowest leaf C:K and N:K ratios, occurred in summer, the season when water stress was greatest. In E. multiflora, leaf K concentrations and K:P ratios were highest, and leaf C:K and N:K ratios were lowest in the plants from the drought-treated plots.The plant capacity to change K concentrations in response to seasonality and to drought is at least as great as the capacity to change N and P concentrations. The results underscore the importance of K and its stoichiometry relative to C, N and P in dry environments. These results indicate first, that N:P ratio shifts are not uniquely related to growth rate in Mediterranean plants but also to drought, and second, that there is a need to take into account K in ecological stoichiometry studies of terrestrial plants.     

Tissue-water relations of two co-occurring evergreen Mediterranean species in response to seasonal and experimental drought conditions

Tissue-water relations were used to characterize the responses of two Mediterranean co-occurring woody species (Quercus ilex L. and Phillyrea latifolia L.) to seasonal and experimental drought conditions. Soil water availability was reduced 15% by partially excluding rain throughfall and lateral flow (water runoff). Seasonal and experimental drought elicited physiological and morphological adaptations other than osmotic adjustment: both species showed large increases in cell-wall elasticity and decreased saturated-to-dry-mass ratio. Increased elasticity (lower elastic modulus) resulted in concurrent decreases in relative water content at turgor loss. In addition, P. latifolia showed significant increases in apoplastic water fraction. Decreased saturated-to-dry-mass ratio and increased apoplastic water fraction were accompanied by an increased range of turgor maintenance, which indicates that leaf sclerophyllous traits might be advantageous in drier scenarios. In contrast, the degree of sclerophylly (as assessed by the leaf mass-to-area ratio) was not related to tissue elasticity. An 15% reduction in soil water availability resulted in significant reductions in diameter growth when compared to control plants in both species. Moreover, although P. latifolia underwent larger changes in tissue water-related traits than Q. ilex in response to decreasing water availability, growth was more sensitive to water stress in P. latifolia than in Q. ilex. Differences in diameter growth between species might be partially linked to the effects of cell-wall elasticity and turgor pressure on growth, since Q. ilex showed higher tissue elasticity and higher intrinsic tolerance to water deficit (as indicated by lower relative water content at turgor loss) than P. latifolia.     

Variation in radial growth responses to drought among species, site, and canopy strata

 Radial growth responses to drought were examined in the tree-ring records of six species growing within two locations of differing land-use history and soil moisture characteristics, and in overstory and understory canopy positions in northern Virginia. Tree species experienced differential ring-width reductions during or immediately following four severe drought periods occurring from 1930 to 1965 and were influenced by climatic variables including annual and summer temperatures, annual precipitation, and annual Palmer Drought Severity Index. Relative growth comparisons averaged across species before and after drought years indicated that understory trees on dry-mesic sites grew 11% faster after drought compared to pre-drought rates while mesic site trees in both canopy positions grew approximately 4% slower. Superposed epoch analysis indicated that Liriodendron tulipifera growing on mesic sites experienced greater ring-width reductions associated with drought than co-occurring, more drought-tolerant Quercus alba and Q. velutina. On dry-mesic sites, L. tulipifera also experienced greatly reduced growth as a result of drought but exhibited significant growth increases following individual drought events. Quercus alba was the only species that exhibited a consistent, significant ring-width decrease associated with all droughts on dry-mesic sites. In contrast, Pinus virginiana was least impacted by drought on dry-mesic sites but was much more impacted by drought on mesic sites, indicating a drought×site interaction for this species. Overstory Carya glabra and Q. alba experienced larger growth decreases during drought on dry-mesic versus mesic sites. Understory tree growth reductions did not differ between site types but were often significantly larger than overstory responses of the same species on mesic sites. Following drought, most trees exhibited growth reductions lasting 2–3 years, although several species experienced reductions lasting up to 6 years. The results of this study suggest that tree rings represent an important long-term proxy for leaf-level ecophysiological measurements of growth responses to drought periods. Received: 31 July 1996 / Accepted: 16 April 1997     

Different responses to drought and freeze stress of Quercus ilex L. growing along a latitudinal gradient

The vulnerability to drought and freeze stress was measured in young plants of Quercus ilex L. growing in the field in two natural sites within the Italian distribution area of this species, i.e. Sicily (Southern Mediterranean Basin) and Venezia Giulia (Northeastern Italy), respectively. In particular, the resistance strategies adopted by Q. ilex to withstand the two stresses were estimated in terms of seasonal and/or diurnal changes in leaf conductance to water vapour (g_L), water potential (_L) and relative water content (RWC) as well as of xylem embolism in the stem and root hydraulic conductance (K_RL). Sicilian (SI) plants showed to reduce water loss by stomatal closure (g_L decreased) in summer, thus maintaining average RWCs at 88–90%. Moreover, SI plants showed considerable resistance to xylem cavitation in the stem (the loss of hydraulic conductance, PLC, was less than 12% throughout the year) and to maintain the hydraulic conductance of their roots (K_RL), constantly high even in summer. Plants growing in Venezia Giulia (VG plants), on the contrary, underwent leaf dehydration in the winter due to freeze stress so that RWC measured in April was still 78% on a diurnal basis. This was apparently due to consistent xylem embolism in the stem. In fact, PLC was as high as 40% between November and March. Only in the summer was PLC similar to that recorded in SI plants. Moreover, K_RL of VG plants decreased in November from about 1.5 to 0.8×10^–4 kg s^–1 m^–2 MPa^–1, i.e. about 50%, and in February K_RL dropped further to 0.4×10^–4 kg s^–1 m^–2 MPa^–1. On the basis of the above, we conclude that: (a) Q. ilex was more sensitive to freeze than to drought stress so that freeze stress can be considered as a factor limiting the distribution area of this species; (b) drought and freeze stress were faced by Q. ilex adopting two different resistance strategies, i.e. drought avoidance based on water saving in Sicily and freeze tolerance in Venezia Giulia.     

Tree growth,mortality, and above-ground biomass accumulation in a holm oak forest under a five-year experimental field drought

A holm oak forest was exposed to an experimental drought during 5 years to elucidate the growth responses of the dominant species Quercus ilex, Arbutus unedo and Phillyrea latifolia. Soil water availability was partially reduced, about 15% as predicted for this area for the next decades by GCM and ecophysiological models, by plastic strips intercepting rainfall and by ditch exclusion of water runoff. The stem diameter increment was highly correlated with annual rainfall in all species, and drought treatment strongly reduced the diameter increment of Q. ilex (41%) and specially of A. unedo (63%), the species showing higher growth rates. Stem mortality rates were highly correlated with previous stem density, but drought treatment increased mortality rates in all species. Q. ilex showed the highest mortality rates (9% and 18% in control and drought plots, respectively), and P. latifolia experienced the lowest mortality rates (1% and 3% in control and drought plots, respectively). Drought strongly reduced the increment of live aboveground biomass during these 5 years (83%). A. unedo and Q. ilex experienced a high reduction in biomass increment by drought, whereas P. latifolia biomass increment was insensitive to drought. The different sensitivity to drought of the dominant species of the holm oak forest may be very important determining their future development and distribution in a drier environment as expected in Mediterranean areas for the next decades. These drier conditions could thus have strong effects on structure (species composition) and functioning (carbon uptake and biomass accumulation) of these Mediterranean forests.     

The influence of summer and winter stress and water relationships on the distribution of Quercus ilex L.

Several aspects of plant-water relationships and canopy behaviour have been studied over several years in two experimental areas of Quercus ilex L. forests in the northeastern Iberian Peninsula. Water requirements, water status limits necessary for a positive carbon budget and the functional canopy behaviour in the face of abiotic stress were evaluated, in order to determine which factors influence the geographical range of these forests.The results showed that holm oak has a conservative water use, a low cuticular transpiration, a high capacity for osmotic adjustement and xerophytic characteristics in leaf morphology and canopy arrangement. More than 440 mm of annual rainfall are required for these forests to persist. Summer drought and winter cold are thus important abiotic factors limiting the distribution of Quercus ilex. In both cases, drought stress is involved.     

The combined effects of a long‐term experimental drought and an extreme drought on the use of plant‐water sources in a Mediterranean forest

Vegetation in water‐limited ecosystems relies strongly on access to deep water reserves to withstand dry periods. Most of these ecosystems have shallow soils over deep groundwater reserves. Understanding the functioning and functional plasticity of species‐specific root systems and the patterns of or differences in the use of water sources under more frequent or intense droughts is therefore necessary to properly predict the responses of seasonally dry ecosystems to future climate. We used stable isotopes to investigate the seasonal patterns of water uptake by a sclerophyll forest on sloped terrain with shallow soils. We assessed the effect of a long‐term experimental drought (12 years) and the added impact of an extreme natural drought that produced widespread tree mortality and crown defoliation. The dominant species, Quercus ilex, Arbutus unedo and Phillyrea latifolia, all have dimorphic root systems enabling them to access different water sources in space and time. The plants extracted water mainly from the soil in the cold and wet seasons but increased their use of groundwater during the summer drought. Interestingly, the plants subjected to the long‐term experimental drought shifted water uptake toward deeper (10–35 cm) soil layers during the wet season and reduced groundwater uptake in summer, indicating plasticity in the functional distribution of fine roots that dampened the effect of our experimental drought over the long term. An extreme drought in 2011, however, further reduced the contribution of deep soil layers and groundwater to transpiration, which resulted in greater crown defoliation in the drought‐affected plants. This study suggests that extreme droughts aggravate moderate but persistent drier conditions (simulated by our manipulation) and may lead to the depletion of water from groundwater reservoirs and weathered bedrock, threatening the preservation of these Mediterranean ecosystems in their current structures and compositions.     

Variations in physiological and biochemical traits of oak seedlings grown under drought and ozone stress

Despite the huge biodiversity characterizing the Mediterranean environment, environmental constraints, such as high sunlight and high temperatures alongside with dry periods, make plant survival hard. In addition, high irradiance leads to increasing ozone (O₃) concentrations in ambient air. In this era of global warming, it is necessary to understand the mechanisms that allow native species to tolerate these environmental constraints and how such mechanisms interact. Three Mediterranean oak species (Quercus ilex, Quercus pubescens and Quercus cerris) with different features (drought tolerant, evergreen or deciduous species) were selected to assess their biometrical, physiological and biochemical responses under drought and/or O₃ stress (80–100 nl l^?1 of O₃ for 5 h day^?1 for 77 consecutive days). Leaf visible injury appeared only under drought stress (alone or combined with O₃) in all three species. Drought × O₃ induced strong reductions in leaf dry weight in Q. pubescens and Q. cerris (?70 and ?75%, respectively). Alterations in physiological (i.e. decrease in maximum carboxylation rate) and biochemical parameters (i.e. increase in proline content and build‐up of malondialdehyde by‐products) occurred in all the three species, although drought represented the major determinant. Quercus ilex and Q. pubescens, which co‐occur in dry environments, were more tolerant to drought and drought × O₃. Quercus ilex was the species in which oxidative stress occurred only when drought was applied with O₃. High plasticity at a biochemical level (i.e. proline content) and evergreen habitus are likely on the basis of the higher tolerance of Q. ilex.     

The South Hesse Oak Project (SHOP): Species- and site-specific efficiency of the photosynthetic apparatus of Mediterranean and Central European Oaks

In three experimental sites in Southern Hesse, differing in management procedures, one- to three-year-old saplings of Quercus robur, Q.pubescens, and Q.ilex were planted to study their performance under Central European climate conditions. Toward the end of the growth period (mid–late September 2011), during a very dry period, we measured JIP transients of photosystem II chlorophyll fluorescence induction curves to evaluate the effects of abiotic site factors on the photosynthetic apparatus by comparing them to data from well-watered saplings measured before the onset of senescence processes. In all three sites, Q. robur saplings in September showed the strongest deviation from the measurements in August, followed by Q. pubescens. Q. ilex, in general, was nearly unaffected by September climate conditions or performed better than plants measured in August. Differences in the behavior between species and sites could be explained by the species’ different drought susceptibility and by differential induction of early leaf senescence (in Q. robur and Q. pubescens). We conclude that measurement of the JIP transient is a feasible method in forestry to compare adverse microclimatic site effects and genetically fixed reactions of the photosynthetic apparatus in the field.     

Species-specific,seasonal, inter-annual,and historically-accumulated changes in foliar terpene emission rates in <Emphasis Type="Italic">Phillyrea latifolia</Emphasis> and <Emphasis Type="Italic">Quercus ilex</Emphasis> submitted to rain exclusion in the Prades Mountains (Catalonia)

Mediterranean vegetation emits large amounts of terpenes. We aimed to study the effects of the decreases in soil water availability forecast for the next decades by global circulation models and ecophysiological models on the terpene emissions by two widely distributed Mediterranean woody species, Phillyrea latifolia L. and Quercus ilex L. We subjected holm oak forest plots to an experimental soil drought of ca. 20% decrease in soil moisture by partial rainfall exclusion and runoff exclusion. We measured the emission rates throughout the seasons for two years with contrasting precipitation and soil moisture (16.6% average in 2003 vs. 6.4% as average in 2005). Among the detected volatile terpenes, only α-pinene and limonene were present in detectable quantities in all of the studied periods. Total terpene emitted ranged from practically zero (spring 2003) to 3.6 and 58.3 μg/(g dry wt h) (winter 2005 and summer 2003 for P. latifolia and Q. ilex, respectively). A clear seasonality was found in the emission rates (they were the highest in summer in both species) and also in the qualitative composition of the emission mix. Maximum emissions of α-pinene occurred in spring and maximum emissions of limonene in winter. Neither the inter-annual differences in water availability nor the rain exclusion treatment significantly affected the emissions in P. latifolia, but Q. ilex showed by 17% lower emissions during the drier second year of study, 2005, but more than two- and threefold increases with the drought treatment in summer 2003 and in summer 2005, respectively, showing historical accumulated effects. These results, which show increased monoterpene emission under the moderate drought produced by the treatment and decreased emission under the severe second year drought, and a much higher sensitivity to drought in Q. ilex than in P. latifolia, are useful in understanding the behavior of plant volatiles under Mediterranean conditions and in modeling future emission under changing climate conditions. They show that the usage of current models could lead to under- and overestimations of the emission under summer dry conditions, because most current algorithms are based on light and temperature only.     

Recent climate hiatus revealed dual control by temperature and drought on the stem growth of Mediterranean Quercus ilex

A better understanding of stem growth phenology and its climate drivers would improve projections of the impact of climate change on forest productivity. Under a Mediterranean climate, tree growth is primarily limited by soil water availability during summer, but cold temperatures in winter also prevent tree growth in evergreen forests. In the widespread Mediterranean evergreen tree species Quercus ilex, the duration of stem growth has been shown to predict annual stem increment, and to be limited by winter temperatures on the one hand, and by the summer drought onset on the other hand. We tested how these climatic controls of Q. ilex growth varied with recent climate change by correlating a 40‐year tree ring record and a 30‐year annual diameter inventory against winter temperature, spring precipitation, and simulated growth duration. Our results showed that growth duration was the best predictor of annual tree growth. We predicted that recent climate changes have resulted in earlier growth onset (?10 days) due to winter warming and earlier growth cessation (?26 days) due to earlier drought onset. These climatic trends partly offset one another, as we observed no significant trend of change in tree growth between 1968 and 2008. A moving‐window correlation analysis revealed that in the past, Q. ilex growth was only correlated with water availability, but that since the 2000s, growth suddenly became correlated with winter temperature in addition to spring drought. This change in the climate–growth correlations matches the start of the recent atmospheric warming pause also known as the ‘climate hiatus’. The duration of growth of Q. ilex is thus shortened because winter warming has stopped compensating for increasing drought in the last decade. Decoupled trends in precipitation and temperature, a neglected aspect of climate change, might reduce forest productivity through phenological constraints and have more consequences than climate warming alone.     

The temporal response to drought in a Mediterranean evergreen tree: comparing a regional precipitation gradient and a throughfall exclusion experiment

Like many midlatitude ecosystems, Mediterranean forests will suffer longer and more intense droughts with the ongoing climate change. The responses to drought in long‐lived trees differ depending on the time scale considered, and short‐term responses are currently better understood than longer term acclimation. We assessed the temporal changes in trees facing a chronic reduction in water availability by comparing leaf‐scale physiological traits, branch‐scale hydraulic traits, and stand‐scale biomass partitioning in the evergreen Quercus ilex across a regional precipitation gradient (long‐term changes) and in a partial throughfall exclusion experiment (TEE, medium term changes). At the leaf scale, gas exchange, mass per unit area and nitrogen concentration showed homeostatic responses to drought as they did not change among the sites of the precipitation gradient or in the experimental treatments of the TEE. A similar homeostatic response was observed for the xylem vulnerability to cavitation at the branch scale. In contrast, the ratio of leaf area over sapwood area (LA/SA) in young branches exhibited a transient response to drought because it decreased in response to the TEE the first 4 years of treatment, but did not change among the sites of the gradient. At the stand scale, leaf area index (LAI) decreased, and the ratios of stem SA to LAI and of fine root area to LAI both increased in trees subjected to throughfall exclusion and from the wettest to the driest site of the gradient. Taken together, these results suggest that acclimation to chronic drought in long‐lived Q. ilex is mediated by changes in hydraulic allometry that shift progressively from low (branch) to high (stand) organizational levels, and act to maintain the leaf water potential within the range of xylem hydraulic function and leaf photosynthetic assimilation.