Nicolas K. Martin-StPaul

Growth duration is a better predictor of stem increment than carbon supply in a Mediterranean oak forest: implications for assessing forest productivity under climate change

Understanding whether tree growth is limited by carbon gain (source limitation) or by the direct effect of environmental factors such as water deficit or temperature (sink limitation) is crucial for improving projections of the effects of climate change on forest productivity. We studied the relationships between tree basal area (BA) variations, eddy covariance carbon fluxes, predawn water potential (Ψpd ) and temperature at different timescales using an 8-yr dataset and a rainfall exclusion experiment in a Quercus ilex Mediterranean coppice. At the daily timescale, during periods of low temperature (< 5°C) and high water deficit (< -1.1 MPa), gross primary productivity and net ecosystem productivity remained positive whereas the stem increment was nil. Thus, stem increment appeared limited by drought and temperature rather than by carbon input. Annual growth was accurately predicted by the duration of BA increment during spring (Δtt0-t1 ). The onset of growth (t0 ) was related to winter temperatures and the summer interruption of growth (t1 ) to a threshold Ψpd value of -1.1 MPa. We suggest that using environmental drivers (i.e. drought and temperature) to predict stem growth phenology can contribute to an improvement in vegetation models and may change the current projections of Mediterranean forest productivity under climate change scenarios.

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.

Plant resistance to drought depends on timely stomatal closure

Stomata play a significant role in the Earths water and carbon cycles, by regulating gaseous exchanges between the plant and the atmosphere. Under drought conditions, stomatal control of transpiration has long been thought to be closely coordinated with the decrease in hydraulic capacity (hydraulic failure due to xylem embolism). We tested this hypothesis by coupling a meta-analysis of functional traits related to the stomatal response to drought and embolism resistance with simulations from a soil-plant hydraulic model. We report here a previously unreported phenomenon: the existence of an absolute limit by which stomata closure must occur to avoid rapid death in drought conditions. The water potential causing stomatal closure and the xylem pressure at the onset of embolism formation were equal for only a small number of species, and the difference between these two traits (i.e. safety margins) increased continuously with increasing embolism resistance. Our findings demonstrate the need to revise current views about the functional coordination between stomata and hydraulic traits and provide a mechanistic framework for modeling plant mortality under drought conditions.

Evidence for hydraulic vulnerability segmentation and lack of xylem refilling under tension

Direct, noninvasive observations of embolism formation and repair reveal a lack of refilling under negative pressure and a xylem hydraulic vulnerability segmentation in grapevine. The vascular system of grapevine (Vitis spp.) has been reported as being highly vulnerable, even though grapevine regularly experiences seasonal drought. Consequently, stomata would remain open below water potentials that would generate a high loss of stem hydraulic conductivity via xylem embolism. This situation would necessitate daily cycles of embolism repair to restore hydraulic function. However, a more parsimonious explanation is that some hydraulic techniques are prone to artifacts in species with long vessels, leading to the overestimation of vulnerability. The aim of this study was to provide an unbiased assessment of (1) the vulnerability to drought-induced embolism in perennial and annual organs and (2) the ability to refill embolized vessels in two Vitis species X-ray micro-computed tomography observations of intact plants indicated that both Vitis vinifera and Vitis riparia were relatively vulnerable, with the pressure inducing 50% loss of stem hydraulic conductivity = −1.7 and −1.3 MPa, respectively. In V. vinifera, both the stem and petiole had similar sigmoidal vulnerability curves but differed in pressure inducing 50% loss of hydraulic conductivity (−1.7 and −1 MPa for stem and petiole, respectively). Refilling was not observed as long as bulk xylem pressure remained negative (e.g. at the apical part of the plants; −0.11 ± 0.02 MPa) and change in percentage loss of conductivity was 0.02% ± 0.01%. However, positive xylem pressure was observed at the basal part of the plant (0.04 ± 0.01 MPa), leading to a recovery of conductance (change in percentage loss of conductivity = −0.24% ± 0.12%). Our findings provide evidence that grapevine is unable to repair embolized xylem vessels under negative pressure, but its hydraulic vulnerability segmentation provides significant protection of the perennial stem.

Differential regional responses in drought length, intensity and timing to recent climate changes in a Mediterranean forested ecosystem

The Mediterranean area is one of the regions of the world where GCMs agree the most on precipitation changes due to climate change. In this study we aim to assess the impact of recent climate change on drought features of Mediterranean ecosystems in Southern France. Regional climatic trends for the 1971–2006 period are compared to drought trends based on a water balance model accounting for soil properties, vegetation structure and functioning. Drought, defined here as periods when soil water potentials drop below − 0.5 MPa, is described in terms of intensity, duration and timing, which are integrative of both climate variability and site conditions. Temporal trends in precipitation, temperature and solar radiation lead altogether to drier and warmer conditions over the region but with a high spatial heterogeneity; for similar climatic trends, a significant increase in drought intensity was detected in the wettest areas of the region, whereas drought intensity in the driest areas did not change. Indeed, in the wettest areas, we observed an earlier onset of drought by about 1 month, but a constant end of drought. In the driest areas of the region, we observed the same earlier onset of drought but combined with an earlier end of drought, thus leading to a shift of the dry season without increasing its duration. The definition of drought features both in terms of intensity but also of seasonal timing appears relevant to capture historical or forecasted changes in ecosystem functioning. Studies concerning climate change impacts on forested ecosystems should be interpreted with caution when using climate proxies alone.

How do leaf and ecosystem measures of water-use efficiency compare?

The terrestrial carbon and water cycles are intimately linked: the carbon cycle is driven by photosynthesis, while the water balance is dominated by transpiration, and both fluxes are controlled by plant stomatal conductance. The ratio between these fluxes, the plant water-use efficiency (WUE), is a useful indicator of vegetation function. WUE can be estimated using several techniques, including leaf gas exchange, stable isotope discrimination, and eddy covariance. Here we compare global compilations of data for each of these three techniques. We show that patterns of variation in WUE across plant functional types (PFTs) are not consistent among the three datasets. Key discrepancies include the following: leaf-scale data indicate differences between needleleaf and broadleaf forests, but ecosystem-scale data do not; leaf-scale data indicate differences between C3 and C4 species, whereas at ecosystem scale there is a difference between C3 and C4 crops but not grasslands; and isotope-based estimates of WUE are higher than estimates based on gas exchange for most PFTs. Our study quantifies the uncertainty associated with different methods of measuring WUE, indicates potential for bias when using WUE measures to parameterize or validate models, and indicates key research directions needed to reconcile alternative measures of WUE.

Xylem resistance to embolism: Presenting a simple diagnostic test for the open vessel artefact

Xylem vulnerability to embolism represents an essential trait for the evaluation of the impact of hydraulics in plant function and ecology. The standard centrifuge technique is widely used for the construction of vulnerability curves, although its accuracy when applied to species with long vessels remains under debate. We developed a simple diagnostic test to determine whether the open-vessel artefact influences centrifuge estimates of embolism resistance. Xylem samples from three species with differing vessel lengths were exposed to less negative xylem pressures via centrifugation than the minimum pressure the sample had previously experienced. Additional calibration was obtained from non-invasive measurement of embolism on intact olive plants by X-ray microtomography. Results showed artefactual decreases in hydraulic conductance (k) for samples with open vessels when exposed to a less negative xylem pressure than the minimum pressure they had previously experienced. X-Ray microtomography indicated that most of the embolism formation in olive occurs at xylem pressures below -4.0 MPa, reaching 50% loss of hydraulic conductivity at -5.3 MPa. The artefactual reductions in k induced by centrifugation underestimate embolism resistance data of species with long vessels. A simple test is suggested to avoid this open vessel artefact and to ensure the reliability of this technique in future studies.

Gas exchange and leaf aging in an evergreen oak: causes and consequences for leaf carbon balance and canopy respiration

Leaves of Mediterranean evergreens experience large variations in gas exchange rates over their life span due to aging and seasonally changing environmental conditions. Accounting for the changing respiratory physiology of leaves over time will help improve estimations of leaf and whole-plant carbon balances. Here we examined seasonal variations in light-saturated net CO(2) assimilation (A(max)), dark respiration (R(d)) and the proportional change in R(d) per 10 °C change in temperature (Q(10) of R(d)) in previous-year (PY) and current-year (CY) leaves of the broadleaved evergreen tree Quercus ilex L. A(max) and R(d) were lower in PY than in CY leaves. Differences in nitrogen between cohorts only partly explained such differences, and rates of A(max) and R(d) expressed per unit of leaf nitrogen were still significantly different between cohorts. The decline in A(max) in PY leaves did not result in the depletion of total non-structural carbohydrates, whose concentration was in fact higher in PY than CY leaves. Leaf-level carbon balance modeled from gas exchange data was positive at all ages. Q(10) of R(d) did not differ significantly between leaf cohorts; however, failure to account for distinct R(d) between cohorts misestimated canopy leaf respiration by 13% across dates when scaling up leaf measurements to the canopy. In conclusion, the decline in A(max) in old leaves that are close to or exceed their mean life span does not limit the availability of carbohydrates, which are probably needed to sustain new growth, as well as R(d) and nutrient resorption during senescence. Accounting for leaf age as a source of variation of R(d) improves the estimation of foliar respiratory carbon release at the stand scale.

Environmental control of carbon allocation matters for modelling forest growth

We aimed to evaluate the importance of modulations of within-tree carbon (C) allocation by water and low-temperature stress for the prediction of annual forest growth with a process-based model. A new C allocation scheme was implemented in the CASTANEA model that accounts for lagged and direct environmental controls of C allocation. Different approaches (static vs dynamic) to modelling C allocation were then compared in a model-data fusion procedure, using satellite-derived leaf production estimates and biometric measurements at c. 104 sites. The modelling of the environmental control of C allocation significantly improved the ability of CASTANEA to predict the spatial and year-to-year variability of aboveground forest growth along regional gradients. A significant effect of the previous years water stress on the C allocation to leaves and wood was reported. Our results also are consistent with a prominent role of the environmental modulation of sink demand in the wood growth of the studied species. Data available at large scales can inform forest models about the processes driving annual and seasonal C allocation. Our results call for a greater consideration of C allocation drivers, especially sink-demand fluctuations, for the simulations of current and future forest productivity with process-based models.

Testing climate models using an impact model: what are the advantages?

Global and regional climate model (GCM and RCM) outputs are often used as climate forcing for ecological impact models, and this potentially results in large cumulative errors because information and error are passed sequentially along the modeling chain from GCM to RCM to impact model. There are also a growing number of Earth system modeling platforms in which climate and ecological models are dynamically coupled, and in this case error amplification due to feedbacks can lead to even more serious problems. It is essential in both cases to rethink the organization of evaluation which typically relies on independent validation at each successive step, and to rely more heavily on analyses that cover the full modeling chain and thus require stronger interactions between climate and impact modelers. In this paper, we illustrate the benefits of using impact models as an additional source of information for evaluating climate models. Four RCMs that are part of the HyMeX (Hydrological cycle in Mediterranean EXperiment) and Mediterranean CORDEX projects (MED-CORDEX) were tested with observed climatology and a process-based model of European beech (Fagus sylvatica L.) tree growth and forest ecosystem functioning that has been rigorously validated. This two part analysis i) indicates that evaluation of RCMs on climate variables alone may be insufficient to determine the suitability of RCMs for studies of climate-forest interactions and ii) points to areas of improvement in these RCMs that would improve impact studies or behavior in coupled climate-ecosystem models over the spatial domain studied.