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.

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.

Morphological and phenological shoot plasticity in a Mediterranean evergreen oak facing long-term increased drought.

Mediterranean trees must adjust their canopy leaf area to the unpredictable timing and severity of summer drought. The impact of increased drought on the canopy dynamics of the evergreen Quercus ilex was studied by measuring shoot growth, leaf production, litterfall, leafing phenology and leaf demography in a mature forest stand submitted to partial throughfall exclusion for 7 years. The leaf area index rapidly declined in the throughfall-exclusion plot and was 19% lower than in the control plot after 7 years of treatment. Consequently, leaf litterfall was significantly lower in the dry treatment. Such a decline in leaf area occurred through a change in branch allometry with a decreased number of ramifications produced and a reduction of the leaf area supported per unit sapwood area of the shoot (LA/SA). The leafing phenology was slightly delayed and the median leaf life span was slightly longer in the dry treatment. The canopy dynamics in both treatments were driven by water availability with a 1-year lag: leaf shedding and production were reduced following dry years; in contrast, leaf turnover was increased following wet years. The drought-induced decrease in leaf area, resulting from both plasticity in shoot development and slower leaf turnover, appeared to be a hydraulic adjustment to limit canopy transpiration and maintain leaf-specific hydraulic conductivity under drier conditions.

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.

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.

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.

What the towers don't see at night: nocturnal sap flow in trees and shrubs at two AmeriFlux sites in California.

At the leaf scale, it is a long-held assumption that stomata close at night in the absence of light, causing transpiration to decrease to zero. Energy balance models and evapotranspiration equations often rely on net radiation as an upper bound, and some models reduce evapotranspiration to zero at night when there is no solar radiation. Emerging research is showing, however, that transpiration can occur throughout the night in a variety of vegetation types and biomes. At the ecosystem scale, eddy covariance measurements have provided extensive data on latent heat flux for a multitude of ecosystem types globally. Nighttime eddy covariance measurements, however, are generally unreliable because of low turbulence. If significant nighttime water loss occurs, eddy flux towers may be missing key information on latent heat flux. We installed and measured rates of sap flow by the heat ratio method (Burgess et al. 2001) at two AmeriFlux (part of FLUXNET) sites in California. The heat ratio method allows measurement and quantification of low rates of sap flow, including negative rates (i.e., hydraulic lift). We measured sap flow in five Pinus ponderosa Dougl. ex Laws. trees and three Arctostaphylos manzanita Parry and two Ceanothus cordulatus A. Kellog shrubs in the Sierra Nevada Mountains, and in five Quercus douglasii Hook and Arn. trees at an oak savanna in the Central Valley of California. Nocturnal sap flow was observed in all species, and significant nighttime water loss was observed in both species of trees. Vapor pressure deficit and air temperature were both well correlated with nighttime transpiration; the influence of wind speed on nighttime transpiration was insignificant at both sites. We distinguished between storage-tissue refilling and water loss based on data from Year 2005, and calculated the percentage by which nighttime transpiration was underestimated by eddy covariance measurements at both sites.

Influences of canopy photosynthesis and summer rain pulses on root dynamics and soil respiration in a young ponderosa pine forest.

Our first objective was to link the seasonality of fine root dynamics with soil respiration in a ponderosa pine (Pinus ponderosa P. & C. Lawson) plantation located in the Sierra Nevada of California. The second objective was to examine how canopy photosynthesis influences fine root initiation, growth and mortality in this ecosystem. We compared CO2 flux measurements with aboveground and belowground root dynamics. Initiation of fine root growth coincided with tree stem thickening and shoot elongation, preceding new needle growth. In the spring, root, shoot and stem growth occurred simultaneously with the increase in canopy photosynthesis. Compared with the other tree components, initial growth rate of fine roots was the highest and their growing period was the shortest. Both above and belowground components completed 90% of their growth by the end of July and the growing season lasted approximately 80 days. The period for optimal growth is short at the study site because of low soil temperatures during winter and low soil water content during summer. High photosynthetic rates were observed following unusual late-summer rains, but tree growth did not resume. The autotrophic contribution to soil respiration was 49% over the whole season, with daily contributions ranging between 18 and 87%. Increases in soil and ecosystem respiration were observed during spring growth; however, the largest variation in soil respiration occurred during summer rain events when no growth was observed. Both the magnitude and persistence of the soil respiration pulses were positively correlated with the amount of rain. These pulses accounted for 16.5% of soil respiration between Days 130 and 329.

Seasonality of photosynthetic parameters in a multi-specific and vertically complex forest ecosystem in the Sierra Nevada of California.

Understanding seasonal variations of photosynthetic parameters is critical for accurate modeling of carbon dioxide (CO2) uptake by ecosystems. Maximum carboxylation velocity (Vcmax), maximum rate of electron transport (Jmax), leaf respiration in the light (R(day)), light-saturated assimilation (Amax) and maximum quantum yield (Phi) were calculated from leaf gas exchange measurements made monthly throughout the year on leaves of three co-occuring evergreen species in a Pinus ponderosa Dougl. ex P. Laws. & C. Laws. forest with shrubs in the understory (Arctostaphylos manzanita Parry and Ceanothus cordulatus Kellogg.). The seasonality and relationships of the photosynthetic parameters with environmental and physiological variables differed among the species. The nitrogen-fixing species, C. cordulatus had the highest values of the parameters and the largest seasonal variation, whereas A. manzanita exhibited the lowest seasonality and weaker correlations with environmental variables. In general, variations in Vcmax were highly correlated with light, leaf mass per area and leaf nitrogen content on an area basis. Temporal scaling of the parameters with each other seemed possible for C. cordulatus and P. ponderosa. However, lags between these variables and Vcmax likely reflect the influences of other factors. The acclimation relationships found along vertical light gradients within canopies in other studies cannot be applied to seasonal variations. The Jmax to Vcmax ratio varied seasonally for P. ponderosa and A. manzanita, being lower at high light, high air temperature and low soil water content.

Forest thinning and soil respiration in a ponderosa pine plantation in the Sierra Nevada.

Soil respiration is controlled by soil temperature, soil water, fine roots, microbial activity, and soil physical and chemical properties. Forest thinning changes soil temperature, soil water content, and root density and activity, and thus changes soil respiration. We measured soil respiration monthly and soil temperature and volumetric soil water continuously in a young ponderosa pine (Pinus ponderosa Dougl. ex P. Laws. & C. Laws.) plantation in the Sierra Nevada Mountains in California from June 1998 to May 2000 (before a thinning that removed 30% of the biomass), and from May to December 2001 (after thinning). Thinning increased the spatial homogeneity of soil temperature and respiration. We conducted a multivariate analysis with two independent variables of soil temperature and water and a categorical variable representing the thinning event to simulate soil respiration and assess the effect of thinning. Thinning did not change the sensitivity of soil respiration to temperature or to water, but decreased total soil respiration by 13% at a given temperature and water content. This decrease in soil respiration was likely associated with the decrease in root density after thinning. With a model driven by continuous soil temperature and water time series, we estimated that total soil respiration was 948, 949 and 831 g C m(-2) year(-1) in the years 1999, 2000 and 2001, respectively. Although thinning reduced soil respiration at a given temperature and water content, because of natural climate variability and the thinning effect on soil temperature and water, actual cumulative soil respiration showed no clear trend following thinning. We conclude that the effect of forest thinning on soil respiration is the combined result of a decrease in root respiration, an increase in soil organic matter, and changes in soil temperature and water due to both thinning and interannual climate variability.

A comparison of three approaches to modeling leaf gas exchange in annually drought-stressed ponderosa pine forests.

We tested, compared and modified three models of stomatal conductance at the leaf level in a forest ecosystem where drought stress is a major factor controlling forest productivity. The models were tested against 2 years (1999 and 2000) of leaf-level measurements on ponderosa pine (Pinus ponderosa Dougl. ex Laws.) growing in the Mediterranean climate of California, USA. The Ball, Woodrow and Berry (1987) (BWB) model was modified to account for soil water stress. Among the models, results of the modified BWB model were in the closest agreement with observations (r2 = 0.71). The Jarvis (1976) model showed systematic simulation errors related to vapor pressure deficit (r2 = 0.65). Results of the Williams, Rastetter, Fernandes et al. (1996) (SPA) model showed the poorest correlation with empirical data, but this model has only one calibration parameter (r2 = 0.60). Sensitivity analyses showed that, in all three models, predictions of stomatal conductance were most responsive to photosynthetically active radiation and soil water content. Stomatal conductance showed little sensitivity to vapor pressure deficit in the Jarvis model, whereas in both the BWB and SPA models, vapor pressure deficit (or relative humidity) was the third most important variable. Parameterization of the SPA model was in accordance with the parameterization of the modified BWB model, although the two models differ greatly. Measured and modeled results indicate that stomatal behavior is not water conservative during spring; however, during summer, when soil water content is low and vapor pressure deficit is high, stomatal conductance decreases and, according to the models, intrinsic water- use efficiency increases.