Jean-Marc Limousin

Mast seeding under increasing drought: results from a long-term data set and from a rainfall exclusion experiment

Mast seeding, the synchronous, highly variable seed production among years, is very common in tree species, but there is no consensus about its main causes and the main environmental factors affecting it. In this study, we first analyze a long-term data set on reproductive and vegetative growth of Quercus ilex in a mediterranean woodland in order to identify the main environmental drivers of interannual variation in flower and seed production and contrast the impact of climate vs. adaptive factors as main causes of masting. Second, we conducted an experiment of rainfall exclusion to evaluate the effects of an increasing drought (simulating predictions of global change models) on both reproductive processes. The annual seed crop was always affected by environmental factors related to the precipitation pattern, these abiotic factors disrupting the fruiting process at different periods of time. Seed production was strongly dependent upon water availability for the plant at initial (spring) and advanced (summer) stages of the acorn maturation cycle, whereas the final step of seed development was negatively affected by the frequency of torrential-rain events. We also found clear evidence that seed masting in the study species is not only regulated by selective endogenous rhythms, but is mainly a physiological response to the variable environment. Our results from the rainfall exclusion experiment corroborated the conclusions obtained from the 26-year fruiting record and demonstrated that the high interannual variation in seed crop was mainly determined by the success in seed development rather than by the flowering effort. Under a global change scenario, it could be expected that the drier conditions predicted by climate models reinforce the negative effects of summer drought on seed production, leading to negative consequences for tree recruitment and forest dynamics.

Mast seeding and flowering in Mediterranean oak woodlands under increasing drought: results from a long-term dataset and from a rainfall exclusion experiment

Mast seeding, the synchronous, highly variable seed production among years, is very common in tree species, but there is no consensus about its main causes and the main environmental factors affecting it. In this study, we first analyze a long-term data set on reproductive and vegetative growth of Quercus ilex in a mediterranean woodland in order to identify the main environmental drivers of interannual variation in flower and seed production and contrast the impact of climate vs. adaptive factors as main causes of masting. Second, we conducted an experiment of rainfall exclusion to evaluate the effects of an increasing drought (simulating predictions of global change models) on both reproductive processes. The annual seed crop was always affected by environmental factors related to the precipitation pattern, these abiotic factors disrupting the fruiting process at different periods of time. Seed production was strongly dependent upon water availability for the plant at initial (spring) and advanced (summer) stages of the acorn maturation cycle, whereas the final step of seed development was negatively affected by the frequency of torrential-rain events. We also found clear evidence that seed masting in the study species is not only regulated by selective endogenous rhythms, but is mainly a physiological response to the variable environment. Our results from the rainfall exclusion experiment corroborated the conclusions obtained from the 26-year fruiting record and demonstrated that the high interannual variation in seed crop was mainly determined by the success in seed development rather than by the flowering effort. Under a global change scenario, it could be expected that the drier conditions predicted by climate models reinforce the negative effects of summer drought on seed production, leading to negative consequences for tree recruitment and forest dynamics.

Do photosynthetic limitations of evergreen Quercus ilex leaves change with long-term increased drought severity?

Seasonal drought can severely impact leaf photosynthetic capacity. This is particularly important for Mediterranean forests, where precipitation is expected to decrease as a consequence of climate change. Impacts of increased drought on the photosynthetic capacity of the evergreen Quercus ilex were studied for two years in a mature forest submitted to long-term throughfall exclusion. Gas exchange and chlorophyll fluorescence were measured on two successive leaf cohorts in a control and a dry plot. Exclusion significantly reduced leaf water potential in the dry treatment. In both treatments, light-saturated net assimilation rate (A(max)), stomatal conductance (g(s)), maximum carboxylation rate (V(cmax)), maximum rate of electron transport (J(max)), mesophyll conductance to CO2 (g(m)) and nitrogen investment in photosynthesis decreased markedly with soil water limitation during summer. The relationships between leaf photosynthetic parameters and leaf water potential remained identical in the two treatments. Leaf and canopy acclimation to progressive, long-term drought occurred through changes in leaf area index, leaf mass per area and leaf chemical composition, but not through modifications of physiological parameters.

On the differential advantages of evergreenness and deciduousness in mediterranean oak woodlands: a flux perspective

We assessed the differential advantages of deciduousness and evergreenness by examining 26 site-years of carbon dioxide, water vapor, and energy flux measurements from five comparable oak woodlands in France, Italy, Portugal, and California (USA). On average, the evergreen and deciduous oak woodlands assimilated and respired similar amounts of carbon while using similar amounts of water. These results suggest that evergreen and deciduous woodlands have specific, and similar, ecological costs in mediterranean climates, and that both leaf habits are able to meet these costs. What are the mechanisms behind these findings? Deciduous oaks compensated for having a shorter growing season by attaining a greater capacity to assimilate carbon for a given amount of intercepted solar radiation during the well-watered spring period; at saturating light levels, deciduous oaks gained carbon at six times the rate of evergreen oaks. Otherwise, the two leaf habits experienced similar efficiencies in carbon use (the change in carbon respired per change in carbon assimilated), water use (the change in carbon assimilation per change in water evaporated), and rainfall use (the change in evaporation per change in rainfall). Overall, leaf area index, rather than leaf habit, was the significant factor in determining the absolute magnitude of carbon gained and water lost by each evergreen and deciduous oak woodland over an annual interval; the closed canopies assimilated and respired more carbon and transpired more water than the open canopies. Both deciduous and evergreen mediterranean oaks survive in their seasonally hot/dry, wet/ cool native range by ensuring that actual evaporation is less than the supply of water. This feat is accomplished by adjusting the leaf area index to reduce total water loss at the landscape scale, by down-regulating photosynthesis, respiration, and stomatal conductance with progressive seasonal soil water deficits, and by extending their root systems to tap groundwater.

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere–atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.The mechanisms underlying drought-induced tree mortality are not fully resolved. Here, the authors show that, across multiple tree species, loss of xylem conductivity above 60% is associated with mortality, while carbon starvation is not universal.

Leaf physiological responses to extreme droughts in Mediterranean Quercus ilex forest

Global climate change is expected to result in more frequent and intense droughts in the Mediterranean region. To understand forest response to severe drought, we used a mobile rainfall shelter to examine the impact of spring and autumn rainfall exclusion on stomatal (S(L) ) and non-stomatal (NS(L) ) limitations of photosynthesis in a Quercus ilex ecosystem. Spring rainfall exclusion, carried out during increasing atmospheric demand and leaf development, had a larger impact on photosynthesis than autumn exclusion, conducted at a time of mature foliage and decreasing vapour pressure deficit. The relative importance of NS(L) increased with drought intensity. S(L) and NS(L) were equal once total limitation (T(L) ) reached 60%, but NS(L) greatly exceeded S(L) during severe drought, with 76% NS(L) partitioned equally between mesophyll conductance (MC(L) ) and biochemical (B(L) ) limitations when T(L) reached 100%. Rainfall exclusion altered the relationship between leaf water potential and photosynthesis. In response to severe mid-summer drought stress, A(n) and V(cmax) were 75% and 72% lower in the spring exclusion plot than in the control plot at the same pre-dawn leaf water potential. Our results revealed changes in the relationship between photosynthetic parameters and water stress that are not currently included in drought parameterizations for modelling applications.

Regulation and acclimation of leaf gas exchange in a piñon–juniper woodland exposed to three different precipitation regimes

Leaf gas-exchange regulation plays a central role in the ability of trees to survive drought, but forecasting the future response of gas exchange to prolonged drought is hampered by our lack of knowledge regarding potential acclimation. To investigate whether leaf gas-exchange rates and sensitivity to drought acclimate to precipitation regimes, we measured the seasonal variations of leaf gas exchange in a mature piñon-juniper Pinus edulis-Juniperus monosperma woodland after 3 years of precipitation manipulation. We compared trees receiving ambient precipitation with those in an irrigated treatment (+30% of ambient precipitation) and a partial rainfall exclusion (-45%). Treatments significantly affected leaf water potential, stomatal conductance and photosynthesis for both isohydric piñon and anisohydric juniper. Leaf gas exchange acclimated to the precipitation regimes in both species. Maximum gas-exchange rates under well-watered conditions, leaf-specific hydraulic conductance and leaf water potential at zero photosynthetic assimilation all decreased with decreasing precipitation. Despite their distinct drought resistance and stomatal regulation strategies, both species experienced hydraulic limitation on leaf gas exchange when precipitation decreased, leading to an intraspecific trade-off between maximum photosynthetic assimilation and resistance of photosynthesis to drought. This response will be most detrimental to the carbon balance of piñon under predicted increases in aridity in the southwestern USA.

Change in hydraulic traits of Mediterranean Quercus ilex subjected to long-term throughfall exclusion

Mediterranean tree species experience unpredictable climate environments and severe summer droughts and they may be impaired by the trend of decline in precipitation projected as a consequence of global climate change. The response of Quercus ilex to drought was studied by measuring hydraulic traits of trees growing in a mature forest subjected to partial throughfall exclusion for 6 years. We measured hydraulic conductivity, xylem vulnerability to embolism, and anatomical features in branches and roots. Xylem vulnerability to embolism was higher in the dry treatment than in the control treatment, P₅₀ of branches was on average -3.88 +/- 0.80 MPa for the control treatment compared with -3.41 +/- 0.80 MPa for the dry treatment, but the difference was not statistically significant. A similar difference between treatments was observed for roots, which exhibited lower P₅₀ values. This change of xylem vulnerability to embolism was not linked to modification of the hydraulic conductivity or vessel anatomy, which remained unaffected by the throughfall exclusion treatment. The xylem density of branches was lower in the dry treatment. The hydraulic conductivity was correlated with the mean vessel diameter of xylem, but the P₅₀ was not. The main response of trees from the dry treatment to reduced water availability appeared to be a reduction in the transpiring leaf area, which resulted in significantly increased leaf-specific conductivity.

Photosynthetic sensitivity to drought varies among populations of Quercus ilex along a rainfall gradient

Drought frequency and intensity are expected to increase in the Mediterranean as a consequence of global climate change. To understand how photosynthetic capacity responds to long-term water stress, we measured seasonal patterns of stomatal (SL), mesophyll (MCL) and biochemical limitations (BL) to net photosynthesis (Amax) in three Quercus ilex (L.) populations from sites differing in annual rainfall. In the absence of water stress, stomatal conductance (gs), maximum carboxylation capacity (Vcmax), photosynthetic electron transport rate (Jmax) and Amax were similar among populations. However, as leaf predawn water potential (Ψl,pd) declined, the population from the wettest site showed steeper declines in gs, Vcmax, Jmax and Amax than those from the drier sites. Consequently, SL, MCL and BL increased most steeply in response to decreasing Ψl,pd in the population from the wettest site. The higher sensitivity of Amax to drought was primarily the result of stronger stomatal regulation of water loss. Among-population differences were not observed when gs was used instead of Ψl,pd as a drought stress indicator. Given that higher growth rates, stature and leaf area index were observed at the wettest site, we speculate that hydraulic architecture may explain the greater drought sensitivity of this population. Collectively, these results highlight the importance of considering among-population differences in photosynthetic responses to seasonal drought in large scale process-based models of forest ecosystem function.

Few multiyear precipitation-reduction experiments find a shift in the productivity-precipitation relationship.

Well-defined productivity-precipitation relationships of ecosystems are needed as benchmarks for the validation of land models used for future projections. The productivity-precipitation relationship may be studied in two ways: the spatial approach relates differences in productivity to those in precipitation among sites along a precipitation gradient (the spatial fit, with a steeper slope); the temporal approach relates interannual productivity changes to variation in precipitation within sites (the temporal fits, with flatter slopes). Precipitation-reduction experiments in natural ecosystems represent a complement to the fits, because they can reduce precipitation below the natural range and are thus well suited to study potential effects of climate drying. Here, we analyse the effects of dry treatments in eleven multiyear precipitation-manipulation experiments, focusing on changes in the temporal fit. We expected that structural changes in the dry treatments would occur in some experiments, thereby reducing the intercept of the temporal fit and displacing the productivity-precipitation relationship downward the spatial fit. The majority of experiments (72%) showed that dry treatments did not alter the temporal fit. This implies that current temporal fits are to be preferred over the spatial fit to benchmark land-model projections of productivity under future climate within the precipitation ranges covered by the experiments. Moreover, in two experiments, the intercept of the temporal fit unexpectedly increased due to mechanisms that reduced either water loss or nutrient loss. The expected decrease of the intercept was observed in only one experiment, and only when distinguishing between the late and the early phases of the experiment. This implies that we currently do not know at which precipitation-reduction level or at which experimental duration structural changes will start to alter ecosystem productivity. Our study highlights the need for experiments with multiple, including more extreme, dry treatments, to identify the precipitation boundaries within which the current temporal fits remain valid.