Lucía Galiano

Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode

• Severe drought may increase physiological stress on long-lived woody vegetation, occasionally leading to mortality of overstory trees. Little is known about the factors determining tree survival and subsequent recovery after drought. • We used structural equation modeling to analyse the recovery of Scots pine (Pinus sylvestris) trees 4 yr after an extreme drought episode occurred in 2004-2005 in north-east Spain. Measured variables included the amount of green foliage, carbon reserves in the stem, mistletoe (Viscum album) infection, needle physiological performance and stem radial growth before, during and after the drought event. • The amount of green leaves and the levels of carbon reserves were related to the impact of drought on radial growth, and mutually correlated. However, our most likely path model indicated that current depletion of carbon reserves was a result of reduced photosynthetic tissue. This relationship potentially constitutes a feedback limiting tree recovery. In addition, mistletoe infection reduced leaf nitrogen content, negatively affecting growth. Finally, successive surveys in 2009-2010 showed a direct association between carbon reserves depletion and drought-induced mortality. • Severe drought events may induce long-term physiological disorders associated with canopy defoliation and depletion of carbon reserves, leading to prolonged recovery of surviving individuals and, eventually, to delayed tree death.

Drought-Induced Multifactor Decline of Scots Pine in the Pyrenees and Potential Vegetation Change by the Expansion of Co-occurring Oak Species

Episodes of drought-induced tree dieback have been recently observed in many forest areas of the world, particularly at the dry edge of species distributions. Under climate change, those effects could signal potential vegetation shifts occurring over large geographical areas, with major impacts on ecosystem form and function. In this article, we studied the effect of a single drought episode, occurred which in summer 2005, on a Scots pine population in central Pyrenees (NE Spain). Our main objective was to study the environmental correlates of forest decline and vegetation change at the plot level. General and generalized linear models were used to study the relationship between canopy defoliation, mortality and recruitment, and plot characteristics. A drought-driven multifactor dieback was observed in the study forest. Defoliation and mortality were associated with the local level of drought stress estimated at each plot. In addition, stand structure, soil properties, and mistletoe infection were also associated with the observed pattern of defoliation, presumably acting as long-term predisposing factors. Recruitment of Scots pine was low in all plots. In contrast, we observed abundant recruitment of other tree species, mostly Quercus ilex and Q. humilis, particularly in plots where Scots pine showed high defoliation and mortality. These results suggest that an altitudinal upwards migration of Quercus species, mediated by the dieback of the currently dominant species, may take place in the studied slopes. Many rear-edge populations of Scots pine sheltered in the mountain environments of the Iberian Peninsula could be at risk under future climate scenarios.

Non-structural carbohydrates in woody plants compared among laboratories

Non-structural carbohydrates (NSC) in plant tissue are frequently quantified to make inferences about plant responses to environmental conditions. Laboratories publishing estimates of NSC of woody plants use many different methods to evaluate NSC. We asked whether NSC estimates in the recent literature could be quantitatively compared among studies. We also asked whether any differences among laboratories were related to the extraction and quantification methods used to determine starch and sugar concentrations. These questions were addressed by sending sub-samples collected from five woody plant tissues, which varied in NSC content and chemical composition, to 29 laboratories. Each laboratory analyzed the samples with their laboratory-specific protocols, based on recent publications, to determine concentrations of soluble sugars, starch and their sum, total NSC. Laboratory estimates differed substantially for all samples. For example, estimates for Eucalyptus globulus leaves (EGL) varied from 23 to 116 (mean = 56) mg g(-1) for soluble sugars, 6-533 (mean = 94) mg g(-1) for starch and 53-649 (mean = 153) mg g(-1) for total NSC. Mixed model analysis of variance showed that much of the variability among laboratories was unrelated to the categories we used for extraction and quantification methods (method category R(2) = 0.05-0.12 for soluble sugars, 0.10-0.33 for starch and 0.01-0.09 for total NSC). For EGL, the difference between the highest and lowest least squares means for categories in the mixed model analysis was 33 mg g(-1) for total NSC, compared with the range of laboratory estimates of 596 mg g(-1). Laboratories were reasonably consistent in their ranks of estimates among tissues for starch (r = 0.41-0.91), but less so for total NSC (r = 0.45-0.84) and soluble sugars (r = 0.11-0.83). Our results show that NSC estimates for woody plant tissues cannot be compared among laboratories. The relative changes in NSC between treatments measured within a laboratory may be comparable within and between laboratories, especially for starch. To obtain comparable NSC estimates, we suggest that users can either adopt the reference method given in this publication, or report estimates for a portion of samples using the reference method, and report estimates for a standard reference material. Researchers interested in NSC estimates should work to identify and adopt standard methods.

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.

Determinants of drought effects on crown condition and their relationship with depletion of carbon reserves in a Mediterranean holm oak forest.

Severe droughts may increase physiological stress on long-lived woody vegetation, occasionally leading to rapid defoliation and progressive increase in mortality of overstorey trees. Over the last few years, episodes of drought-induced tree dieback have been documented in a variety of woodlands and forests around the world. However, the factors determining tree survival and subsequent recovery are still poorly understood, especially in resprouter species. We have studied the effects of a single drought episode on crown condition in a holm oak (Quercus ilex L.) forest located in NE Spain 7 years after the drought event. Generalized linear models were used to study the environmental correlates of forest crown condition 7 years after the drought event. Additionally, we evaluated the association between crown condition and the carbon and nutrient reserves stored in lignotubers 7 years after the drought. Our study reveals the multifactor nature of a drought-driven forest dieback in which soil depth and the characteristics of individual trees, particularly their number of stems, determined a complex spatial pattern of tree-level responses. This dieback was associated with a depletion of the carbon reserves in lignotubers 7 years after the episode, representing a reduction of up to 60% in highly drought-damaged trees. Interestingly, in the absence of new acute droughts, successive surveys in 2007-11 showed a direct association between carbon reserves depletion and further deterioration of crown condition. More frequent droughts, as predicted by climate change projections, may lead to a progressive depletion of carbon reserves and to a loss of resilience in Mediterranean resprouter species.

Patterns of Forest Decline and Regeneration Across Scots Pine Populations

To predict future changes in forest ecosystems, it is crucial to understand the complex processes involved in decline of tree species populations and to evaluate the implications for potential vegetation shifts. Here, we study patterns of decline (canopy defoliation and mortality of adults) of four Scots pine populations at the southern edge of its distribution and characterized by different combinations of climate dryness and intensity of past management. General linear and structural equation modeling were used to assess how biotic, abiotic, and management components interacted to explain the spatial variability of Scots pine decline across and within populations. Regeneration patterns of Scots pine and co-occurring oak species were analyzed to assess potential vegetation shifts. Decline trends were related to climatic dryness at the regional scale, but, ultimately, within-population forest structure, local site conditions, and past human legacies could be the main underlying drivers of Scots pine decline. Overall, Scots pine regeneration was negatively related to decline both within and between populations, whereas oak species responded to decline idiosyncratically across populations. Taken together, our results suggest that (1) patterns of decline are the result of processes acting at the plot level that modulate forest responses to local environmental stress and (2) decline of adult Scots pine trees seems not to be compensated by self-recruitment so that the future dynamics of these forest ecosystems are uncertain.

Dynamics of non-structural carbohydrates in three Mediterranean woody species following long-term experimental drought

Stored non-structural carbohydrates (NSC) have been proposed as a key determinant of drought resistance in plants. However, the evidence for this role is controversial, as it comes mostly from observational, short-term studies. Here, we take advantage of a long-term experimental throughfall reduction to elucidate the response of NSC to increased drought 14 years after the beginning of the treatment in three Mediterranean resprouter trees (Quercus ilex L., Arbutus unedo L. and Phillyrea latifolia L.). In addition, we selected 20 Q. ilex individuals outside the experimental plots to directly assess the relationship between defoliation and NSC at the individual level. We measured the seasonal course of NSC concentrations in leaves, branches and lignotuber in late winter, late spring, summer, and autumn 2012. Total concentrations of NSC were highest in the lignotuber for all species. In the long-term drought experiment we found significant depletion in concentrations of total NSC in treatment plots only in the lignotuber of A. unedo. At the same time, A. unedo was the only species showing a significant reduction in BAI under the drought treatment during the 14 years of the experiment. By contrast, Q. ilex just reduced stem growth only during the first 4 years of treatment and P. latifolia remained unaffected over the whole study period. However, we found a clear association between the concentrations of NSC and defoliation in Q. ilex individuals sampled outside the experimental plots, with lower total concentrations of NSC and lower proportion of starch in defoliated individuals. Taken together, our results suggest that stabilizing processes, probably at the stand level, may have been operating in the long-term to mitigate any impact of drought on NSC levels, and highlight the necessity to incorporate long-term experimental studies of plant responses to drought.

Impact of interspecific competition and drought on the allocation of new assimilates in trees.

In trees, the interplay between reduced carbon assimilation and the inability to transport carbohydrates to the sites of demand under drought might be one of the mechanisms leading to carbon starvation. However, we largely lack knowledge on how drought effects on new assimilate allocation differ between species with different drought sensitivities and how these effects are modified by interspecific competition. We assessed the fate of (13) C labelled assimilates in above- and belowground plant organs and in root/rhizosphere respired CO2 in saplings of drought-tolerant Norway maple (Acer platanoides) and drought-sensitive European beech (Fagus sylvatica) exposed to moderate drought, either in mono- or mixed culture. While drought reduced stomatal conductance and photosynthesis rates in both species, both maintained assimilate transport belowground. Beech even allocated more new assimilate to the roots under moderate drought compared to non-limited water supply conditions, and this pattern was even more pronounced under interspecific competition. Even though maple was a superior competitor compared to beech under non-limited soil water conditions, as indicated by the changes in above- and belowground biomass of both species in the interspecific competition treatments, we can state that beech was still able to efficiently allocate new assimilate belowground under combined drought and interspecific competition. This might be seen as a strategy to maintain root osmotic potential and to prioritise root functioning. Our results thus show that beech tolerates moderate drought stress plus competition without losing its ability to supply belowground tissues. It remains to be explored in future work if this strategy is also valid during long-term drought exposure.

Responses of sapwood ray parenchyma and non‐structural carbohydrates of Pinus sylvestris to drought and long‐term irrigation

Summary Non-structural carbohydrates (NSC) play a crucial role in tree resistance and resilience to drought. Stem sapwood parenchyma is among the largest storage tissue for NSC in mature trees. However, there is a limited mechanistic understanding of how NSC reserves, stem parenchyma abundance, and growth rates are interrelated, and how they respond to changing water availability. We quantified NSC, ray parenchyma abundance and ring width along four successive 5-year radial sapwood segments of the stem of 40 mature Pinus sylvestris trees from a 10-year irrigation experiment conducted at a xeric site in Switzerland. Percentage of ray volume (PERPAR) varied from 3.75 to 8.94% among trees, but showed low intra-individual variability. PERPAR responded positively to irrigation with a lag of several years, but was unrelated to %NSC. %NSC was lower in wider rings. However, wider rings still contained a larger NSC pool that was positively related to next years ring growth. Our results suggest that stem ray parenchyma does not limit NSC storage capacity, but responds to long-term environmental drivers with years of delay. The observed carbon allocation patterns indicate a prioritization of storage over growth independent of growth conditions, likely as a mechanism to ensure long-term survival. Furthermore, NSC pool size proved to be a determinant for the inter-annual auto-correlation in tree-ring growth. Our study highlights the importance of long-term multi-parameter studies to better understand tree responses to environmental variability at different time-scales. This article is protected by copyright. All rights reserved.

Top canopy nitrogen allocation linked to increased grassland carbon uptake in stands of varying species richness

Models predict that vertical gradients of foliar nitrogen (N) allocation, increasing from bottom to top of plant canopies, emerge as a plastic response to optimise N utilisation for carbon assimilation. While this mechanism has been well documented in monocultures, its relevance for mixed stands of varying species richness remains poorly understood. We used 21 naturally assembled grassland communities to analyse the gradients of N in the canopy using N allocation coefficients (KN) estimated from the distribution of N per foliar surface area (KN-F) and ground surface area (KN-G). We tested whether: 1) increasing plant species richness leads to more pronounced N gradients as indicated by higher KN-values, 2) KN is a good predictor of instantaneous net ecosystem CO2 exchange and 3) functional diversity of leaf N concentration as estimated by Rao’s Q quadratic diversity metric is a good proxy of KN. Our results show a negative (for KN-G) or no relationship (for KN-F) between species richness and canopy N distribution, but emphasize a link (positive relationship) between more foliar N per ground surface area in the upper layers of the canopy (i.e. under higher KN-G) and ecosystem CO2 uptake. Rao’s Q was not a good proxy for either KN.