A synthesis of radial growth patterns preceding tree mortality

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.     

No evidence for depletion of carbohydrate pools in Scots pine (Pinus sylvestris L.) under drought stress

The physiological mechanisms leading to Scots pine (Pinus sylvestris L.) decline in the dry inner alpine valleys are still unknown. Testing the carbon starvation hypothesis, we analysed the seasonal course of mobile carbohydrate pools (NSC) of Scots pine growing at a xeric and a dry-mesic site within an inner alpine dry valley (750 m a.s.l., Tyrol, Austria) during 2009, which was characterised by exceptional soil dryness. Although, soil moisture content dropped to ca. 10% at both sites during the growing season, NSC concentrations rose in all tissues (branch, stem, root) until the end of July, except in needles, where maxima were reached around bud break. NSC concentrations were not significantly different in the analysed tissues at the xeric and the dry-mesic site. At the dry-mesic site, NSC concentrations in the aboveground tree biomass were significantly higher during the period of radial growth. An accumulation of NSC in roots at the end of July indicates a change in carbon allocation after an early cessation in aboveground growth, possibly due to elevated belowground carbon demand. In conclusion, our results revealed that extensive soil dryness during the growing season did not lead to carbon depletion. However, even though carbon reserves were not exhausted, sequestration of carbohydrate pools during drought periods might lead to deficits in carbon supply that weaken tree vigour and drive tree mortality.     

Tree carbon allocation explains forest drought‐kill and recovery patterns

The mechanisms governing tree drought mortality and recovery remain a subject of inquiry and active debate given their role in the terrestrial carbon cycle and their concomitant impact on climate change. Counter‐intuitively, many trees do not die during the drought itself. Indeed, observations globally have documented that trees often grow for several years after drought before mortality. A combination of meta‐analysis and tree physiological models demonstrate that optimal carbon allocation after drought explains observed patterns of delayed tree mortality and provides a predictive recovery framework. Specifically, post‐drought, trees attempt to repair water transport tissue and achieve positive carbon balance through regrowing drought‐damaged xylem. Furthermore, the number of years of xylem regrowth required to recover function increases with tree size, explaining why drought mortality increases with size. These results indicate that tree resilience to drought‐kill may increase in the future, provided that CO₂ fertilisation facilitates more rapid xylem regrowth.     

Frost and drought: Effects of extreme weather events on stem carbon dynamics in a Mediterranean beech forest

The effects of short-term extreme events on tree functioning and physiology are still rather elusive. European beech is one of the most sensitive species to late frost and water shortage. We investigated the intra-annual C dynamics in stems under such conditions. Wood formation and stem CO₂ efflux were monitored in a Mediterranean beech forest for 3 years (2015–2017), including a late frost (2016) and a summer drought (2017). The late frost reduced radial growth and, consequently, the amount of carbon fixed in the stem biomass by 80%. Stem carbon dioxide efflux in 2016 was reduced by 25%, which can be attributed to the reduction of effluxes due to growth respiration. Counter to our expectations, we found no effects of the 2017 summer drought on radial growth and stem carbon efflux. The studied extreme weather events had various effects on tree growth. Even though late spring frost had a strong impact on beech radial growth in the current year, trees fully recovered in the following growing season, indicating high resilience of beech to this stressful event.     

Stable carbon isotope analysis reveals widespread drought stress in boreal black spruce forests

Unprecedented rates of climate warming over the past century have resulted in increased forest stress and mortality worldwide. Decreased tree growth in association with increasing temperatures is generally accepted as a signal of temperature‐induced drought stress. However, variations in tree growth alone do not reveal the physiological mechanisms behind recent changes in tree growth. Examining stable carbon isotope composition of tree rings in addition to tree growth can provide a secondary line of evidence for physiological drought stress. In this study, we examined patterns of black spruce growth and carbon isotopic composition in tree rings in response to climate warming and drying in the boreal forest of interior Alaska. We examined trees at three nested scales: landscape, toposequence, and a subsample of trees within the toposequence. At each scale, we studied the potential effects of differences in microclimate and moisture availability by sampling on northern and southern aspects. We found that black spruce radial growth responded negatively to monthly metrics of temperature at all examined scales, and we examined ?¹³C responses on a subsample of trees as representative of the wider region. The negative ?¹³C responses to temperature reveal that black spruce trees are experiencing moisture stress on both northern and southern aspects. Contrary to our expectations, ?¹³C from trees on the northern aspect exhibited the strongest drought signal. Our results highlight the prominence of drought stress in the boreal forest of interior Alaska. We conclude that if temperatures continue to warm, we can expect drought‐induced productivity declines across large regions of the boreal forest, even for trees located in cool and moist landscape positions.     

How do trees die? A test of the hydraulic failure and carbon starvation hypotheses

Despite decades of research on plant drought tolerance, the physiological mechanisms by which trees succumb to drought are still under debate. We report results from an experiment designed to separate and test the current leading hypotheses of tree mortality. We show that piñon pine (Pinus edulis) trees can die of both hydraulic failure and carbon starvation, and that during drought, the loss of conductivity and carbohydrate reserves can also co‐occur. Hydraulic constraints on plant carbohydrate use determined survival time: turgor loss in the phloem limited access to carbohydrate reserves, but hydraulic control of respiration prolonged survival. Our data also demonstrate that hydraulic failure may be associated with loss of adequate tissue carbohydrate content required for osmoregulation, which then promotes failure to maintain hydraulic integrity.     

Stomatal conductance and intrinsic water use efficiency in the drought year 2003: a case study of European beech

Key message

Beech trees were able to cope with the drought of 2003. Harmful water shortage has been avoided by an effective stomatal closure while use of carbon storage pools may have prevented carbon starvation and growth reduction.

Abstract

We applied hydrodynamic modeling together with a tree ring stable isotope approach to identify the physiological responses of beech trees to changing environmental conditions. The drought conditions of the extreme hot and dry summer in 2003 were hypothesized to significantly influence the radial growth of European beech mainly triggered by the stomatal response towards water scarcity leading, in turn, to a decline in carbon assimilation. The functional–structural single tree modeling approach applied, revealed in fact a strong limitation of water use and carbon gain during drought. However, tree ring width data did not show a clear drought response and no differentiation in radial growth during six subsequent years examined (2002–2007) has been observed. Using integrated results from mechanistic carbon–water balance simulations, tree ring carbon and oxygen isotope analysis and tree ring width measurements we postulate that the suggested drought-induced growth decline has been prevented by the remobilization of stored carbohydrates, an early onset in growth and the relatively late occurrence of the severe drought in 2003. Furthermore, we demonstrate that the stomatal response played a significant role in avoiding harmful water tension that would have caused xylem dysfunction. As a result of the combined investigation with physiological measurements (stable isotope approach) and hydrodynamic modeling of stomatal aperture, we could give insights into the physiological control of mature beech tree functioning under drought. We conclude that beech trees have been operating at their hydraulic limits and that the longer or repeated drought periods would have affected the growth considerably.

     

Pinyon pine (Pinus edulis) mortality and response to water addition across a three million year substrate age gradient in northern Arizona, USA

Background and aims

Pinyon pine (Pinus edulis Engelm.) is an important tree species in the western United States that has experienced large-scale mortality during recent severe drought. The influence of soil conditions on pinyon pine response to water availability is poorly understood. We investigated patterns of tree mortality and response of tree water relations and growth to experimental water addition at four sites across a three million year soil-substrate age gradient.

Methods

We measured recent pinyon mortality at four sites, and tree predawn water potential, leaf carbon isotope signature, and branch, leaf, and stem radial growth on 12 watered and unwatered trees at each site. Watered trees recieved fifty percent more than growing season precipitation for 6 years.

Results

Substrate age generally had a greater effect on tree water stress and growth than water additions. Pinyon mortality was higher on intermediate-aged substrates (50–55%) than on young (15%) and old (17%) substrates, and mortality was positively correlated with pinyon abundance prior to drought.

Conclusions

These results suggest high soil resource availability and consequent high stand densities at intermediate-age substrates predisposes trees to drought-induced mortality in semi-arid regions. The response of tree water relations to water addition was consistent with the inverse texture hypothesis; watering reduced tree water stress most in young, coarsely textured soil, likely because water rapidly penetrated deep in the soil profile where it was protected from evapotranspiration.     

树木年内径向生长对干旱事件的响应——以贺兰山油松为例

在贺兰山苏峪口国家森林公园,利用径向生长测量仪监测2017和2018年2个生长季内、2个海拔(2010和2330 m)油松的径向生长,研究树木径向生长对干旱的响应。结果表明: 2018年6月的干旱事件使得油松径向生长速率减慢,生长量减小;而7—8月的降水使油松的径向生长重新激活。2018年油松的径向生长主要发生在6—8月,相比2017年延长一个月。油松径向生长与气候因子的响应关系在不同海拔间没有明显的差异。生长季早期干旱对树木径向生长有抑制作用,生长季中后期降水对树木径向生长具有促进作用。该区的气候重建工作中应当充分考虑8月的气候要素对树轮宽度的影响。     

Linking drought legacy effects across scales: From leaves to tree rings to ecosystems

Severe drought can cause lagged effects on tree physiology that negatively impact forest functioning for years. These “drought legacy effects” have been widely documented in tree‐ring records and could have important implications for our understanding of broader scale forest carbon cycling. However, legacy effects in tree‐ring increments may be decoupled from ecosystem fluxes due to (a) postdrought alterations in carbon allocation patterns; (b) temporal asynchrony between radial growth and carbon uptake; and (c) dendrochronological sampling biases. In order to link legacy effects from tree rings to whole forests, we leveraged a rich dataset from a Midwestern US forest that was severely impacted by a drought in 2012. At this site, we compiled tree‐ring records, leaf‐level gas exchange, eddy flux measurements, dendrometer band data, and satellite remote sensing estimates of greenness and leaf area before, during, and after the 2012 drought. After accounting for the relative abundance of tree species in the stand, we estimate that legacy effects led to ~10% reductions in tree‐ring width increments in the year following the severe drought. Despite this stand‐scale reduction in radial growth, we found that leaf‐level photosynthesis, gross primary productivity (GPP), and vegetation greenness were not suppressed in the year following the 2012 drought. Neither temporal asynchrony between radial growth and carbon uptake nor sampling biases could explain our observations of legacy effects in tree rings but not in GPP. Instead, elevated leaf‐level photosynthesis co‐occurred with reduced leaf area in early 2013, indicating that resources may have been allocated away from radial growth in conjunction with postdrought upregulation of photosynthesis and repair of canopy damage. Collectively, our results indicate that tree‐ring legacy effects were not observed in other canopy processes, and that postdrought canopy allocation could be an important mechanism that decouples tree‐ring signals from GPP.     

Radial growth response of trees to seasonal soil humidity in a subtropical forest

Tree growth is the most important factor in determining the carbon sequestration processes of forest ecosystems. However, the growth phenology (seasonal growth pattern) and responses of tree growth to climatic variables vary considerably among different species, especially between deciduous and evergreen species. Thus, it is crucial to explore the seasonal growth patterns of different tree species in relation to climate to better understand the responses of tree physiology to climate changes, especially in mixed-species forest stands. In this study, we monitored the daily basal area increments of 220 individuals belonging to 15 common broadleaved tree species, nine deciduous and six evergreen species, in mixed-species experimental stands in subtropical China and analysed the relationships between radial stem growth and seasonal climate at a high-temporal resolution. We fitted daily increments of stem diameters with four frequently used nonlinear models and chose the best model for each species. The results showed that the evergreen trees grew faster than the deciduous trees, both annually and within the growing season. The tested nonlinear models (Korf, Weibull, logistic and Gompertz) produced good fits for the growth patterns of all species. Overall, the evergreen species began stem growth earlier and finished later during the growing season than that of the deciduous species. Within the growing season, the radial growth of trees in mixed stands containing both types of species was strongly positively correlated with humidity. In spring, increases in both temperature and moisture increased the daily relative basal area increment of all species. Maximum growth rates occurred when the soil water content reached its highest level and gradually decreased when the soil water content decreased. In summer, high temperatures combined with low amounts of precipitation led to heat-induced summer drought, to which the evergreen trees appeared to be more tolerant than the deciduous trees, which was reflected in the reduced stem growth of the latter. These results indicate the different climate-dependent seasonal growth strategies of evergreen and deciduous trees related to the trade-off described by the leaf economics spectrum, i.e., short-lived leaves with higher assimilation rates in deciduous and longer-lived leaves with a greater drought tolerance in evergreen species.     

Impact of long-term drought on xylem embolism and growth in Pinus halepensis Mill.

 The present study was carried out to elucidate the response mechanisms of 50-year-old Pinus halepensis Mill. trees to a long-term and severe drought. The amount of water available to trees was artificially restricted for 12 months by covering the soil with a plastic roof. Over the short term a direct and rapid impact of drought was evident on the water relations and gas exchanges of trees: as the soil dried out in the Spring, there was a concurrent decrease of predawn water potential; transpiration was strongly reduced by stomatal closure. Seasonal changes in the water volume fractions of twig and stem xylem were observed and interpreted as the result of cavitation and refilling in the xylem. When droughted trees recovered to a more favourable water status, refilling of embolized xylem was observed; twig predawn water potentials were still negative in the period when the embolism was reversed in the twig xylem. A few months after the removal of the covering, no differences in whole plant hydraulic resistance were observed between droughted and control trees. Needle and shoot elongation and stem radial growth were considerably reduced in droughted trees; no strategy of trees to allocate carbon preferentially to the stem conducting tissues was apparent throughout the experiment. An after-effect of the drought on growth was observed. Received: 4 August 1997 / Accepted: 1 October 1997     

Advancement in studies of tree growth and ecophysiology incorporating micro-sampling approach

The recently developed micro-sampling approach has been widely used to extract micro-tree-cores at weekly intervals to monitor the process of stem cambial activity and xylem formation. Compared with the traditional dendrochronology, the micro-sampling approach enables us to better understand the inherent physiological processes in tree growth and their relationships with the environment at a more precise level. This review article aims to: 1) summarize the progresses in the micro-sampling approach-based studies published over recent years and its potential applications, and 2) elucidate the relationships between primary growth and secondary growth and the response mechanisms of radial growth of trees to global change (global warming, drought, and carbon and nitrogen fertilization effects) based on information from literature. It is anticipated that this review will assist with predicting productivity and carbon sink potential of forests, and help policy-makers with sustainable forest management decisions.     

Replicated throughfall exclusion experiment in an Indonesian perhumid rainforest: wood production,litter fall and fine root growth under simulated drought

Climate change scenarios predict increases in the frequency and duration of ENSO‐related droughts for parts of South‐East Asia until the end of this century exposing the remaining rainforests to increasing drought risk. A pan‐tropical review of recorded drought‐related tree mortalities in more than 100 monitoring plots before, during and after drought events suggested a higher drought‐vulnerability of trees in South‐East Asian than in Amazonian forests. Here, we present the results of a replicated (n = 3 plots) throughfall exclusion experiment in a perhumid tropical rainforest in Sulawesi, Indonesia. In this first large‐scale roof experiment outside semihumid eastern Amazonia, 60% of the throughfall was displaced during the first 8 months and 80% during the subsequent 17 months, exposing the forest to severe soil desiccation for about 17 months. In the experiment's second year, wood production decreased on average by 40% with largely different responses of the tree families (ranging from −100 to +100% change). Most sensitive were trees with high radial growth rates under moist conditions. In contrast, tree height was only a secondary factor and wood specific gravity had no influence on growth sensitivity. Fine root biomass was reduced by 35% after 25 months of soil desiccation while fine root necromass increased by 250% indicating elevated fine root mortality. Cumulative aboveground litter production was not significantly reduced in this period. The trees from this Indonesian perhumid rainforest revealed similar responses of wood and litter production and root dynamics as those in two semihumid Amazonian forests subjected to experimental drought. We conclude that trees from paleo‐ or neotropical forests growing in semihumid or perhumid climates may not differ systematically in their growth sensitivity and vitality under sublethal drought stress. Drought vulnerability may depend more on stem cambial activity in moist periods than on tree height or wood specific gravity.     

Importance of resin ducts in reducing ponderosa pine mortality from bark beetle attack

The relative importance of growth and defense to tree mortality during drought and bark beetle attacks is poorly understood. We addressed this issue by comparing growth and defense characteristics between 25 pairs of ponderosa pine (Pinus ponderosa) trees that survived and trees that died from drought-associated bark beetle attacks in forests of northern Arizona, USA. The three major findings of our research were: (1) xylem resin ducts in live trees were >10% larger (diameter), >25% denser (no. of resin ducts mm⁻²), and composed >50% more area per unit ring growth than dead trees; (2) measures of defense, such as resin duct production (no. of resin ducts year⁻¹) and the proportion of xylem ring area to resin ducts, not growth, were the best model parameters of ponderosa pine mortality; and (3) most correlations between annual variation in growth and resin duct characteristics were positive suggesting that conditions conducive to growth also increase resin duct production. Our results suggest that trees that survive drought and subsequent bark beetle attacks invest more carbon in resin defense than trees that die, and that carbon allocation to resin ducts is a more important determinant of tree mortality than allocation to radial growth.     

Drought and shade deplete nonstructural carbohydrate reserves in seedlings of five temperate tree species

Plants that store nonstructural carbohydrates (NSC) may rely on carbon reserves to survive carbon‐limiting stress, assuming that reserves can be mobilized. We asked whether carbon reserves decrease in resource stressed seedlings, and if NSC allocation is related to species' relative stress tolerances. We tested the effects of stress (shade, drought, and defoliation) on NSC in seedlings of five temperate tree species (Acer rubrum Marsh., Betula papyrifera Marsh., Fraxinus americana L., Quercus rubra L., and Quercus velutina Lam.). In a greenhouse experiment, seedlings were subjected to combinations of shade, drought, and defoliation. We harvested seedlings over 32–97 days and measured biomass and NSC concentrations in stems and roots to estimate depletion rates. For all species and treatments, except for defoliation, seedling growth and NSC accumulation ceased. Shade and drought combined caused total NSC decreases in all species. For shade or drought alone, only some species experienced decreases. Starch followed similar patterns as total NSC, but soluble sugars increased under drought for drought‐tolerant species. These results provide evidence that species deplete stored carbon in response to carbon limiting stress and that species differences in NSC response may be important for understanding carbon depletion as a buffer against shade‐ and drought‐induced mortality.     

干旱-高钙对麻栎幼苗非结构性碳水化合物含量和分配的影响

土壤高钙胁迫是干旱-半干旱区影响树木生长的重要环境因子,为阐明干旱-高钙对树木非结构性碳水化合物(Non-structural carbohydrate,NSC)的含量和分配的影响,以麻栎幼苗为研究对象,阐明干旱和干旱-高钙条件对其生长、光合特征及非结构碳水化合物含量与分配的影响。结果表明:干旱显著降低麻栎幼苗生物量,而干旱-高钙处理较干旱进一步降低了麻栎生物量;干旱-高钙在处理初期就能显著抑制麻栎幼苗净光合速率,处理3个月后干旱和干旱-高钙处理的麻栎幼苗光合速率均显著低于对照;干旱处理麻栎幼苗平均非结构性碳水化合物含量增加19.90%,干旱-高钙处理麻栎幼苗整株的平均NSC含量则显著降低25.62%;干旱和干旱-高钙对麻栎幼苗NSC在不同器官间分配也产生不同影响,干旱条件下麻栎幼苗茎中NSC含量增加最多,较对照增加了52.34%,且淀粉的增高幅度(61.94%)高于可溶性糖(25.53%),干旱、高钙共同作用下麻栎幼苗全株平均NSC含量显著减少的同时,NSC积累在叶中,叶NSC含量显著提高32.31%,根、茎中NSC含量则分别显著降低了49.38%和35.31%。干旱-高钙胁迫降低麻栎幼苗NSC含量,且会减少NSC向枝干和根系分配。     

Infestation and hydraulic consequences of induced carbon starvation

Drought impacts on forests, including widespread die-off, are likely to increase with future climate change, although the physiological responses of trees to lethal drought are poorly understood. In particular, in situ examinations of carbon starvation and its interactions with and effects on infestation and hydraulic vulnerability are largely lacking. In this study, we conducted a controlled, in situ, repeated defoliation experiment to induce carbon stress in isolated trembling aspen (Populus tremuloides) ramets. We monitored leaf morphology, leaves per branch, and multitissue carbohydrate concentrations during canopy defoliation. We examined the subsequent effects of defoliation and defoliation-induced carbon stress on vulnerability to insect/fungus infestation and hydraulic vulnerability the following year. Defoliated ramets flushed multiple canopies, which coincided with moderate drawdown of nonstructural carbohydrate reserves. Infestation frequency greatly increased and hydraulic conductivity decreased 1 year after defoliation. Despite incomplete carbohydrate drawdown from defoliation and relatively rapid carbohydrate recovery, suggesting considerable carbohydrate reserves in aspen, defoliation-induced carbon stress held significant consequences for vulnerability to mortality agents and hydraulic performance. Our results indicate that multiyear consequences of drought via feedbacks are likely important for understanding forests' responses to drought and climate change over the coming decades.     

Stand- and tree-level determinants of the drought response of Scots pine radial growth

Characterizing the responses of key tree species to extreme climatic events may provide important information for predicting future forest responses to increased climatic variability. Here we aimed at determining which tree- and stand-level attributes were more closely associated with the effect of a severe drought on the radial growth of Scots pine, both in terms of immediate impact and recovery after the drought event. Our dataset included tree-ring series from 393 plots located close to the dry limit of the species range. Time series analysis and mixed-effects models were used to study the growth of each tree and its detailed response to a severe drought event that occurred in 1986. Our results showed that the radial growth responses of Scots pine were determined primarily by tree-level characteristics, such as age and previous growth rate, and secondarily by stand basal area and species richness, whereas local climate had a relatively minor effect. Fast-growing trees were more severely affected by the drought and retained proportionally lower growth rates up to three years after the episode. In absolute terms, however, fast-growing trees performed better both during and after the event. Older trees were found to be less resilient to drought. The effect of stand basal area and species richness indicated that competition for resources worsened the effects of drought, and suggested that the effect of interspecific competition may be particularly detrimental during the drought year.     

Climatic stress increases forest fire severity across the western United States

Pervasive warming can lead to chronic stress on forest trees, which may contribute to mortality resulting from fire‐caused injuries. Longitudinal analyses of forest plots from across the western US show that high pre‐fire climatic water deficit was related to increased post‐fire tree mortality probabilities. This relationship between climate and fire was present after accounting for fire defences and injuries, and appeared to influence the effects of crown and stem injuries. Climate and fire interactions did not vary substantially across geographical regions, major genera and tree sizes. Our findings support recent physiological evidence showing that both drought and heating from fire can impair xylem conductivity. Warming trends have been linked to increasing probabilities of severe fire weather and fire spread; our results suggest that warming may also increase forest fire severity (the number of trees killed) independent of fire intensity (the amount of heat released during a fire).