Tree mortality is a key factor influencing forest functions and dynamics, but our understanding of the mechanisms leading to mortality and the associated changes in tree growth rates are still ...limited. We compiled a new pan‐continental tree‐ring width database from sites where both dead and living trees were sampled (2970 dead and 4224 living trees from 190 sites, including 36 species), and compared early and recent growth rates between trees that died and those that survived a given mortality event. We observed a decrease in radial growth before death in ca. 84% of the mortality events. The extent and duration of these reductions were highly variable (1–100 years in 96% of events) due to the complex interactions among study species and the source(s) of mortality. Strong and long‐lasting declines were found for gymnosperms, shade‐ and drought‐tolerant species, and trees that died from competition. Angiosperms and trees that died due to biotic attacks (especially bark‐beetles) typically showed relatively small and short‐term growth reductions. Our analysis did not highlight any universal trade‐off between early growth and tree longevity within a species, although this result may also reflect high variability in sampling design among sites. The intersite and interspecific variability in growth patterns before mortality provides valuable information on the nature of the mortality process, which is consistent with our understanding of the physiological mechanisms leading to mortality. Abrupt changes in growth immediately before death can be associated with generalized hydraulic failure and/or bark‐beetle attack, while long‐term decrease in growth may be associated with a gradual decline in hydraulic performance coupled with depletion in carbon reserves. Our results imply that growth‐based mortality algorithms may be a powerful tool for predicting gymnosperm mortality induced by chronic stress, but not necessarily so for angiosperms and in case of intense drought or bark‐beetle outbreaks.
• The extent to which water availability can be used to predict the enlargement and final dimensions of xylem conduits remains an open issue.
• We reconstructed the time course of tracheid ...enlargement in Pinus sylvestris trees in central Spain by repeated measurements of tracheid diameter on microcores sampled weekly during a 2 yr period. We analyzed the role of water availability in these dynamics empirically through time-series correlation analysis and mechanistically by building a model that simulates daily tracheid enlargement rate and duration based on Lockhart’s equation and water potential as the sole input.
• Tracheid enlargement followed a sigmoid-like time course, which varied intra- and interannually. Our empirical analysis showed that final tracheid diameter was strongly related to water availability during tracheid enlargement. The mechanistic model was calibrated and successfully validated (R² = 0.92) against the observed tracheid enlargement time course. The model was also able to reproduce the seasonal variations of tracheid enlargement rate, duration and final diameter (R² = 0.84–0.99).
• Our results support the hypothesis that tracheid enlargement and final dimensions can be modeled based on the direct effect of water potential on turgor-driven cell expansion. We argue that such a mechanism is consistent with other reported patterns of tracheid dimension variation.
Forest disturbances such as drought, fire, and logging affect the forest carbon dynamics and the terrestrial carbon sink. Forest mortality after disturbances creates uncertainties that need to be ...accounted for to understand forest dynamics and their associated C‐sink. We combined data from permanent resampling plots and biomass oriented dendroecological plots to estimate time series of annual woody biomass growth (ABI) in several forests. ABI time series were used to benchmark a vegetation model to analyze dynamics in forest productivity and carbon allocation forced by environmental variability. The model implements source and sink limitations explicitly by dynamically constraining carbon allocation of assimilated photosynthates as a function of temperature and moisture. Bias in tree‐ring reconstructed ABI increased back in time from data collection and with increasing disturbance intensity. ABI bias ranged from zero, in open stands without recorded mortality, to over 100% in stands with major disturbances such as thinning or snowstorms. Stand leaf area was still lower than in control plots decades after heavy thinning. Disturbances, species life‐history strategy and climatic variability affected carbon‐partitioning patterns in trees. Resprouting broadleaves reached maximum biomass growth at earlier ages than nonresprouting conifers. Environmental variability and leaf area explained much variability in woody biomass allocation. Effects of stand competition on C‐allocation were mediated by changes in stand leaf area except after major disturbances. Divergence between tree‐ring estimated and simulated ABI were caused by unaccounted changes in allocation or misrepresentation of some functional process independently of the model calibration approach. Higher disturbance intensity produced greater modifications of the C‐allocation pattern, increasing error in reconstructed biomass dynamics. Legacy effects from disturbances decreased model performance and reduce the potential use of ABI as a proxy to net primary productivity. Trait‐based dynamics of C‐allocation in response to environmental variability need to be refined in vegetation models.
Forest disturbances affect carbon dynamics. We used time series of woody biomass growth (ABI) to benchmark a vegetation model where carbon allocation of assimilated photosynthates is dynamically calculated as a function of temperature and moisture. Bias in tree‐ring reconstructed ABI increases back in time and with increasing disturbance intensity. Disturbances, species life‐history strategy and climatic variability modify carbon‐partitioning patterns in trees. Environmental variability explained much variability in woody biomass allocation. Effects of stand competition on C‐allocation were mediated by changes in leaf area except after major disturbances. Divergence between tree‐ring estimated and simulated ABI was independent of the model calibration approach. Higher disturbance intensity produced greater modifications of the C‐allocation pattern, increasing error in reconstructed biomass dynamics. Legacy effects from disturbances reduce the potential use of ABI as a proxy to net primary productivity. Trait‐based dynamics of C‐allocation in response to environmental variability need to be refined in vegetation models.
Climate change may reduce forest growth and increase forest mortality, which is connected to high carbon costs through reductions in gross primary production and net ecosystem exchange. Yet, the ...spatiotemporal patterns of vulnerability to both short‐term extreme events and gradual environmental changes are quite uncertain across the species’ limits of tolerance to dryness. Such information is fundamental for defining ecologically relevant upper limits of species tolerance to drought and, hence, to predict the risk of increased forest mortality and shifts in species composition. We investigate here to what extent the impact of short‐ and long‐term environmental changes determines vulnerability to climate change of three evergreen conifers (Scots pine, silver fir, Norway spruce) and two deciduous hardwoods (European beech, sessile oak) tree species at their southernmost limits of distribution in the Mediterranean Basin. Finally, we simulated future forest growth under RCP 2.6 and 8.5 emission scenarios using a multispecies generalized linear mixed model. Our analysis provides four key insights into the patterns of species’ vulnerability to climate change. First, site climatic marginality was significantly linked to the growth trends: increasing growth was related to less climatically limited sites. Second, estimated species‐specific vulnerability did not match their a priori rank in drought tolerance: Scots pine and beech seem to be the most vulnerable species among those studied despite their contrasting physiologies. Third, adaptation to site conditions prevails over species‐specific determinism in forest response to climate change. And fourth, regional differences in forests vulnerability to climate change across the Mediterranean Basin are linked to the influence of summer atmospheric circulation patterns, which are not correctly represented in global climate models. Thus, projections of forest performance should reconsider the traditional classification of tree species in functional types and critically evaluate the fine‐scale limitations of the climate data generated by global climate models.
Current and forecasted trends in tree growth from temperate and boreal tree species growing at the southernmost limit of their natural distribution in Europe. The tree growth projections by 2100 revealed a generalized decrease in growth under the climatic conditions derived from the RCP 8.5 emission scenario.
Forest decline under environmental stress is expressed by regeneration failure and accelerated mortality in all ontogenic stages at the population level. Characterizing functional traits and ...mechanisms that best capture species decline and mortality is essential to assess forest dynamics.
We analysed sensitivity to increasing water stress in two species with different water‐use strategies on a mixed Quercus pyrenaica–Pinus sylvestris forest where adult pines express vulnerability to climate change but oaks do not. We compared the dynamics of radial growth, wood δ13C and sapwood non‐structural carbohydrates (NSCs) in response to drought at different time‐scales in both species and two age cohorts in pine.
Both species were very sensitive to water stress, which influenced trait phenotypic plasticity at short‐ and long time‐scales. Water‐use strategy in pines of both ages was more conservative than in the more drought‐tolerant oak. Both species showed negative growth trends despite increasing intrinsic water‐use efficiency. Recent growth of pines is slower than it was in the past. Carbon isotope discrimination trends in young pines suggested increasing leaf gas exchange constraints. NSCs were far from depletion in both species and all pine ages. Intra‐ and inter‐annual NSC variability was higher in oaks than in pines and in soluble sugars (SS) than in starch. SS were lowest in young pines. Sensitivity of NSCs to contrasting climatic years was low in pines, and NSC levels mostly remained homeostatic for this species. The sensitivity to climate expressed suggests different C allocation strategies, with less coupling between radial growth and current‐year photosynthesis in young pines.
Synthesis. Pines expressed negative responses to increased water stress regardless of age, showing rising gas exchange constraints through tighter stomatal control of water losses than oaks. Young pines showed similar functional responses to water stress than old pines in decline, which suggests species‐level vulnerability and could be regarded as early warning signals anticipating mortality in pines. Yet, given the high sensitivity to drought also expressed by the non‐declining oak, it would have been difficult to unequivocally disentangle species decline based only on the functional traits analysed.
Resumen
La ausencia de regeneración y la mortalidad acelerada por estrés ambiental en todas las escalas ontogénicas y a nivel poblacional indican decaimiento forestal.
En este trabajo analizamos la sensibilidad al aumento del estrés hídrico en un bosque mixto de Quercus pyrenaica y Pinus sylvestris, dos especies con diferentes estrategias en el uso del agua. En esta masa los pinos adultos muestran síntomas de decaimiento pero los robles no. Comparamos las respuestas a la sequía del crecimiento radial, el δ13C de la madera y los carbohidratos no estructurales de la albura (NSC) a diferentes escalas temporales en las dos especies y en pinos de dos clases de edad.
Ambas especies mostraron una alta sensibilidad al estrés hídrico, el cual mostró una estrecha relación con la plasticidad fenotípica en escalas temporales cortas y largas. Los pinos de todas las edades estudiadas mostraron estrategias más conservadoras en el uso del agua que la especie más tolerante a la sequía, el roble. Las dos especies mostraron tendencias de crecimiento negativas, pese a mostrar tendencias positivas en iWUE. El crecimiento radial de los pinos es menor actualmente que a la misma edad en el pasado. Las tendencias de la discriminación isotópica del carbono en los pinos jóvenes sugieren un incremento de las limitaciones en el intercambio gaseoso foliar. Tanto la variabilidad intranual como la interanual en los NSC fueron mayores en los robles que en los pinos y en azúcares solubles (SS) que en almidón. Los pinos mostraron los valores más bajos de SS. La sensibilidad de los NSC a dos años climáticamente contrastados fue muy baja en pinos, cuyos niveles de NSC permanecieron homeostáticos en consecuencia. La sensibilidad al clima mostrada por los diferentes rasgos funcionales analizados sugiere diferencias en la redistribución del carbono dentro de la planta, con menor acoplamiento entre crecimiento radial y fotosíntesis en pinos jóvenes.
Síntesis. Los pinos respondieron negativamente al incremento del estrés hídrico independientemente de su edad, aumentando sus limitaciones en el intercambio gaseoso mediante un mayor control estomático que los robles. Los pinos jóvenes y viejos tuvieron una respuesta functional ante el estrés hídrico parecida. Esto sugiere vulnerabilidad a nivel de especie y podría considerarse como una señal de aviso temprano previa a futuros aumentos en la mortalidad en pinos. A pesar de ello, dada la alta sensibilidad a la sequía de los robles, que no están en decaimiento, hubiera sido difícil deducir solamente mediante el análisis de los caracteres funcionales estudiados si las especies están en decaimiento o no.
Pines expressed negative responses to increased water stress regardless of age, showing rising gas exchange constraints through tighter stomatal control of water losses than oaks. Young pines showed similar functional responses to water stress than old pines in decline, which suggests species‐level vulnerability and could be regarded as early‐warning signals anticipating mortality in pines.
Climate change scenarios forecast rising temperatures for the Mediterranean region, which could enhance the vulnerability to drought stress in forest ecosystems. The long‐term effects of climate ...forcing on tree performance can be, however, modulated by other environmental factors, such as competition and rising atmospheric CO₂ concentrations. We assessed the concomitant effect of competition, climate and CO₂ concentrations on the tree‐ring δ¹³C‐derived intrinsic water‐use efficiency (iWUE) and basal area increments (BAI) of species with different drought tolerance: two Mediterranean deciduous species (Quercus faginea Lam. and Quercus pyrenaica Willd.) and one conifer (Pinus sylvestris L.). Additionally, given that competition may be managed to mitigate the effect of increasing drought stress, we further examined the influence of this variable on iWUE and growth using data compiled from the literature, providing the first review on the response of iWUE to competition. Competition had no significant effect on iWUE in any of the three species studied, whereas, as expected, growth rates were significantly higher under low‐competition levels. This was consistent with the literature review, which showed that shifts in iWUE with competition changes are rare; supporting the hypothesis that leaf‐level gas exchange tends to be a homeostatic trait. In the long term, the three species exhibited a significant increasing trend in iWUE due to the combined effect of increased CO₂ concentration, climate and age. Growth, however, was mostly affected by competition and climate and in most cases was not enhanced as a result of the increase in iWUE. Synthesis. Regardless of their functional response to drought, trees respond to reduced competition through the structural shifts such as increased radial growth rather than leaf‐level gas exchange adjustments. CO₂ and climate are, therefore, the main drivers of iWUE variability, rather than competition. Thus, if temperature‐induced drought becomes limiting, reducing competition for resources may not offset the detrimental effect of increasing drought stress on tree physiology and growth decline may occur without a CO₂ fertilization effect.
Forest performance is challenged by climate change but higher atmospheric CO2 (ca) could help trees mitigate the negative effect of enhanced water stress. Forest projections using data assimilation ...with mechanistic models are a valuable tool to assess forest performance. Firstly, we used dendrochronological data from 12 Mediterranean tree species (six conifers and six broadleaves) to calibrate a process‐based vegetation model at 77 sites. Secondly, we conducted simulations of gross primary production (GPP) and radial growth using an ensemble of climate projections for the period 2010–2100 for the high‐emission RCP8.5 and low‐emission RCP2.6 scenarios. GPP and growth projections were simulated using climatic data from the two RCPs combined with (i) expected ca; (ii) constant ca = 390 ppm, to test a purely climate‐driven performance excluding compensation from carbon fertilization. The model accurately mimicked the growth trends since the 1950s when, despite increasing ca, enhanced evaporative demands precluded a global net positive effect on growth. Modeled annual growth and GPP showed similar long‐term trends. Under RCP2.6 (i.e., temperatures below +2 °C with respect to preindustrial values), the forests showed resistance to future climate (as expressed by non‐negative trends in growth and GPP) except for some coniferous sites. Using exponentially growing ca and climate as from RCP8.5, carbon fertilization overrode the negative effect of the highly constraining climatic conditions under that scenario. This effect was particularly evident above 500 ppm (which is already over +2 °C), which seems unrealistic and likely reflects model miss‐performance at high ca above the calibration range. Thus, forest projections under RCP8.5 preventing carbon fertilization displayed very negative forest performance at the regional scale. This suggests that most of western Mediterranean forests would successfully acclimate to the coldest climate change scenario but be vulnerable to a climate warmer than +2 °C unless the trees developed an exaggerated fertilization response to CO2.
We analyzed dynamics of forest growth and GPP in relation to climate change and CO2 across the western Mediterranean. Tree growth was not enhanced in the recent past despite raising CO2. Models suggest that forests would mostly resist an increase in temperature below +2 °C. Further warming over that threshold would result in very negative Mediterranean forest performance. A strong fertilization effect in response to exponentially raising CO2 could counteract the negative effect of a warmer climate, but this effect seems unrealistic.
Severe droughts have the potential to reduce forest productivity and trigger tree mortality. Most trees face several drought events during their life and therefore resilience to dry conditions may be ...crucial to long-term survival. We assessed how growth resilience to severe droughts, including its components resistance and recovery, is related to the ability to survive future droughts by using a tree-ring database of surviving and now-dead trees from 118 sites (22 species, >3,500 trees). We found that, across the variety of regions and species sampled, trees that died during water shortages were less resilient to previous non-lethal droughts, relative to coexisting surviving trees of the same species. In angiosperms, drought-related mortality risk is associated with lower resistance (low capacity to reduce impact of the initial drought), while it is related to reduced recovery (low capacity to attain pre-drought growth rates) in gymnosperms. The different resilience strategies in these two taxonomic groups open new avenues to improve our understanding and prediction of drought-induced mortality.
Plant-plant interactions influence how forests cope with climate and contribute to modulate species response to future climate scenarios. We analysed the functional relationships between growth, ...climate and competition for Pinus sylvestris, Quercus pyrenaica and Quercus faginea to investigate how stand competition modifies forest sensitivity to climate and simulated how annual growth rates of these species with different drought tolerance would change throughout the 21st century. Dendroecological data from stands subjected to thinning were modelled using a novel multiplicative nonlinear approach to overcome biases related to the general assumption of a linear relationship between covariates and to better mimic the biological relationships involved. Growth always decreased exponentially with increasing competition, which explained more growth variability than climate in Q. faginea and P. sylvestris. The effect of precipitation was asymptotic in all cases, while the relationship between growth and temperature reached an optimum after which growth declined with warmer temperatures. Our growth projections indicate that the less drought-tolerant P. sylvestris would be more negatively affected by climate change than the studied sub-Mediterranean oaks. Q. faginea and P. sylvestris mean growth would decrease under all the climate change scenarios assessed. However, P. sylvestris growth would decline regardless of the competition level, whereas this decrease would be offset by reduced competition in Q. faginea. Conversely, Q. pyrenaica growth would remain similar to current rates, except for the warmest scenario. Our models shed light on the nature of the species-specific interaction between climate and competition and yield important implications for management. Assuming that individual growth is directly related to tree performance, trees under low competition would better withstand the warmer conditions predicted under climate change scenarios but in a variable manner depending on the species. Thinning following an exponential rule may be desirable to ensure long-term conservation of high-density Mediterranean woodlands, particularly in drought-limited sites.
Premise
Maternal effects have been demonstrated to affect offspring performance in many organisms, and in plants, seeds are important mediators of these effects. Some woody plant species maintain ...long‐lasting canopy seed banks as an adaptation to wildfires. Importantly, these seeds stored in serotinous cones are produced by the mother plant under varying ontogenetic and physiological conditions.
Methods
We sampled the canopy seed bank of a highly serotinous population of Pinus pinaster to test whether maternal age and growth and the environmental conditions during each crop year affected seed mass and ultimately germination and early survival. After determining retrospectively the year of each seed cohort, we followed germination and early survival in a semi‐natural common garden.
Results
Seed mass was related to maternal age and growth at the time of seed production; i.e., slow‐growing, older mothers had smaller seeds, and fast‐growing, young mothers had larger seeds, which could be interpreted either as a proxy of senescence or as a maternal strategy. Seed mass had a positive effect on germination success, but aside from differences in seed mass, maternal age had a negative effect and diameter had a positive effect on germination timing and subsequent survival.
Conclusions
The results highlight the importance of maternal conditions combined with seed mass in shaping seedling establishment. Our findings open new insights in the offspring performance deriving from long‐term canopy seed banks, which may have high relevance for plant adaptation.
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