Ghosts of the past: how drought legacy effects shape forest functioning and carbon cycling

Multi‐year lags in tree drought recovery, termed ‘drought legacy effects’, are important for understanding the impacts of drought on forest ecosystems, including carbon (C) cycle feedbacks to climate change. Despite the ubiquity of lags in drought recovery, large uncertainties remain regarding the mechanistic basis of legacy effects and their importance for the C cycle. In this review, we identify the approaches used to study legacy effects, from tree rings to whole forests. We then discuss key knowledge gaps pertaining to the causes of legacy effects, and how the various mechanisms that may contribute these lags in drought recovery could have contrasting implications for the C cycle. Furthermore, we conduct a novel data synthesis and find that legacy effects differ drastically in both size and length across the US depending on if they are identified in tree rings versus gross primary productivity. Finally, we highlight promising approaches for future research to improve our capacity to model legacy effects and predict their impact on forest health. We emphasise that a holistic view of legacy effects – from tissues to whole forests – will advance our understanding of legacy effects and stimulate efforts to investigate drought recovery via experimental, observational and modelling approaches.     

树木年轮揭示的东灵山主要树种间干旱耐受性差异

近年来北京地区的森林随极端干旱加剧表现出脆弱性特征,为了解气候变化下不同树种的干旱耐受性,选择北京东灵山森林内3个乔木树种(华北落叶松、油松和辽东栎),利用树木年轮生态学方法分析了径向生长与气候的关系,以及对极端干旱事件的抵抗力和弹性。结果表明: 华北落叶松和油松与5—6月气温呈显著负相关,辽东栎与5月气温呈显著负相关;华北落叶松与6月降水量、5—6月和8—9月相对湿度呈显著正相关,油松与6—8月降水量和相对湿度呈显著正相关,辽东栎与2月和5月降水量、5月相对湿度呈显著正相关;所有树种均与当年5—7月标准化降水蒸散指数(SPEI)呈显著正相关。华北落叶松是干旱耐受性最弱的树种,径向生长在所选极端干旱事件中(1994年、2001—2002年和2007年)下降幅度最大(46.6%～69.6%),抵抗力(0.534、0.304、0.530)和弹性(0.686、0.570、0.753)显著低于辽东栎和油松,辽东栎在2007年抵抗力显著高于油松,弹性无显著差异。生长季持续的高温或降水减少引起的极端干旱是树木径向生长下降的主要原因,树种间各异的生理生态策略是干旱耐受性差异的可能原因。研究结果可为未来造林树种选择和森林管护措施制定提供新依据,以在气候压力持续增加背景下维持森林生态系统功能和服务。     

Assimilation exceeds respiration sensitivity to drought: A FLUXNET synthesis

The intensification of the hydrological cycle, with an observed and modeled increase in drought incidence and severity, underscores the need to quantify drought effects on carbon cycling and the terrestrial sink. FLUXNET, a global network of eddy covariance towers, provides dense data streams of meteorological data, and through flux partitioning and gap filling algorithms, estimates of net ecosystem productivity (F_NEP), gross ecosystem productivity (P), and ecosystem respiration (R). We analyzed the functional relationship of these three carbon fluxes relative to evaporative fraction (EF), an index of drought and site water status, using monthly data records from 238 micrometeorological tower sites distributed globally across 11 biomes. The analysis was based on relative anomalies of both EF and carbon fluxes and focused on drought episodes by biome and climatic season. Globally P was ≈50% more sensitive to a drought event than R. Network‐wide drought‐induced decreases in carbon flux averaged ?16.6 and ?9.3 g C m^?2 month^?1 for P and R, i.e., drought events induced a net decline in the terrestrial sink. However, in evergreen forests and wetlands drought was coincident with an increase in P or R during parts of the growing season. The most robust relationships between carbon flux and EF occurred during climatic spring for F_NEP and in climatic summer for P and R. Upscaling flux sensitivities to a global map showed that spatial patterns for all three carbon fluxes were linked to the distribution of croplands. Agricultural areas exhibited the highest sensitivity whereas the tropical region had minimal sensitivity to drought. Combining gridded flux sensitivities with their uncertainties and the spatial grid of FLUXNET revealed that a more robust quantification of carbon flux response to drought requires additional towers in all biomes of Africa and Asia as well as in the cropland, shrubland, savannah, and wetland biomes globally.     

Seasonal variability of forest sensitivity to heat and drought stresses: A synthesis based on carbon fluxes from North American forest ecosystems

Climate extremes such as heat waves and droughts are projected to occur more frequently with increasing temperature and an intensified hydrological cycle. It is important to understand and quantify how forest carbon fluxes respond to heat and drought stress. In this study, we developed a series of daily indices of sensitivity to heat and drought stress as indicated by air temperature (T_a) and evaporative fraction (EF). Using normalized daily carbon fluxes from the FLUXNET Network for 34 forest sites in North America, the seasonal pattern of sensitivities of net ecosystem productivity (NEP), gross ecosystem productivity (GEP) and ecosystem respiration (RE) in response to T_a and EF anomalies were compared for different forest types. The results showed that warm temperatures in spring had a positive effect on NEP in conifer forests but a negative impact in deciduous forests. GEP in conifer forests increased with higher temperature anomalies in spring but decreased in summer. The drought‐induced decrease in NEP, which mostly occurred in the deciduous forests, was mostly driven by the reduction in GEP. In conifer forests, drought had a similar dampening effect on both GEP and RE, therefore leading to a neutral NEP response. The NEP sensitivity to T_a anomalies increased with increasing mean annual temperature. Drier sites were less sensitive to drought stress in summer. Natural forests with older stand age tended to be more resilient to the climate stresses compared to managed younger forests. The results of the Classification and Regression Tree analysis showed that seasons and ecosystem productivity were the most powerful variables in explaining the variation of forest sensitivity to heat and drought stress. Our results implied that the magnitude and direction of carbon flux changes in response to climate extremes are highly dependent on the seasonal dynamics of forests and the timing of the climate extremes.     

Patterns and drivers of Araucaria araucana forest growth along a biophysical gradient in the northern Patagonian Andes: Linking tree rings with satellite observations of soil moisture

Araucaria araucana (Araucaria) is a long‐lived conifer growing along a sharp west–east biophysical gradient in the Patagonian Andes. The patterns and climate drivers of Araucaria growth have typically been documented on the driest part of the gradient relying on correlations with meteorological records, but the lack of in situ soil moisture observations has precluded an assessment of the growth responses to soil moisture variability. Here, we use a network of 21 tree‐ring width chronologies to investigate the spatiotemporal patterns of tree growth through the entire gradient and evaluate their linkages with regional climate and satellite‐observed surface soil moisture variability. We found that temporal variations in tree growth are remarkably similar throughout the gradient and largely driven by soil moisture variability. The regional spatiotemporal pattern of tree growth was positively correlated with precipitation (r = 0.35 for January 1920–1974; P < 0.01) and predominantly negatively correlated with temperature (r = ?0.38 for January–March 1920–1974; P < 0.01) during the previous growing season. These correlations suggest a temporally lagged growth response to summer moisture that could be associated with known physiological carry‐over processes in conifers and to a response to moisture variability at deeper layers of the rooting zone. Notably, satellite observations revealed a previously unobserved response of Araucaria growth to summer surface soil moisture during the current rather than the previous growing season (r = 0.65 for 1979–2000; P < 0.05). This new response has a large spatial footprint across the mid‐latitudes of the South American continent (35°–45°S) and highlights the potential of Araucaria tree rings for palaeoclimatic applications. The strong moisture constraint on tree growth revealed by satellite observations suggests that projected summer drying during the coming decades may result in regional growth declines in Araucaria forests and other water‐limited ecosystems in the Patagonian Andes.     

Patterns and controls of the variability of radiation use efficiency and primary productivity across terrestrial ecosystems

Aim The controls of gross radiation use efficiency (RUE), the ratio between gross primary productivity (GPP) and the radiation intercepted by terrestrial vegetation, and its spatial and temporal variation are not yet fully understood. Our objectives were to analyse and synthesize the spatial variability of GPP and the spatial and temporal variability of RUE and its climatic controls for a wide range of vegetation types. Location A global range of sites from tundra to rain forest. Methods We analysed a global dataset on photosynthetic uptake and climatic variables from 35 eddy covariance (EC) flux sites spanning between 100 and 2200 mm mean annual rainfall and between ?13 and 26°C mean annual temperature. RUE was calculated from the data provided by EC flux sites and remote sensing (MODIS). Results Rainfall and actual evapotranspiration (AET) positively influenced the spatial variation of annual GPP, whereas temperature only influenced the GPP of forests. Annual and maximum RUE were also positively controlled primarily by annual rainfall. The main control parameters of the growth season variation of gross RUE varied for each ecosystem type. Overall, the ratio between actual and potential evapotranspiration and a surrogate for the energy balance explained a greater proportion of the seasonal variation of RUE than the vapour pressure deficit (VPD), AET and precipitation. Temperature was important for determining the intra‐annual variability of the RUE at the coldest energy‐limited sites. Main conclusions Our analysis supports the idea that the annual functioning of vegetation that is adapted to its local environment is more constrained by water availability than by temperature. The spatial variability of annual and maximum RUE can be largely explained by annual precipitation, more than by vegetation type. The intra‐annual variation of RUE was mainly linked to the energy balance and water availability along the climatic gradient. Furthermore, we showed that intra‐annual variation of gross RUE is only weakly influenced by VPD and temperature, contrary to what is frequently assumed. Our results provide a better understanding of the spatial and temporal controls of the RUE and thus could lead to a better estimation of ecosystem carbon fixation and better modelling.     

Forest resilience to drought varies across biomes

Forecasted increase drought frequency and severity may drive worldwide declines in forest productivity. Species‐level responses to a drier world are likely to be influenced by their functional traits. Here, we analyse forest resilience to drought using an extensive network of tree‐ring width data and satellite imagery. We compiled proxies of forest growth and productivity (TRWi, absolutely dated ring‐width indices; NDVI, Normalized Difference Vegetation Index) for 11 tree species and 502 forests in Spain corresponding to Mediterranean, temperate, and continental biomes. Four different components of forest resilience to drought were calculated based on TRWi and NDVI data before, during, and after four major droughts (1986, 1994–1995, 1999, and 2005), and pointed out that TRWi data were more sensitive metrics of forest resilience to drought than NDVI data. Resilience was related to both drought severity and forest composition. Evergreen gymnosperms dominating semi‐arid Mediterranean forests showed the lowest resistance to drought, but higher recovery than deciduous angiosperms dominating humid temperate forests. Moreover, semi‐arid gymnosperm forests presented a negative temporal trend in the resistance to drought, but this pattern was absent in continental and temperate forests. Although gymnosperms in dry Mediterranean forests showed a faster recovery after drought, their recovery potential could be constrained if droughts become more frequent. Conversely, angiosperms and gymnosperms inhabiting temperate and continental sites might have problems to recover after more intense droughts since they resist drought but are less able to recover afterwards.     

季节性高温和干旱对亚热带毛竹林碳通量的影响

采用涡度相关技术对安吉亚热带毛竹林生态系统碳通量进行连续观测,选取2011和2013年月尺度净生态系统生产力（NEP）、生态系统呼吸（R_e）和总生态系统生产力（GEP）数据,探讨季节性高温、干旱对毛竹林生态系统碳通量的影响.结果表明： 安吉毛竹林年际间NEP有较大差异;2013年7和8月由于水热不同步而造成的高温干旱使其NEP明显下降,相比于2011年同期分别下降了59.9%和80.0%.对2011和2013年月尺度下NEP、R_e和GEP与环境因子进行相关分析发现,R_e和GEP与温度因子均呈显著相关（P<0.05）,但两者对空气和土壤水分的响应方式和程度有所不同,GEP相比于R_e更易受到土壤水分降低的影响,而饱和水汽压差的升高会在一定程度上促进R_e、同时抑制GEP,这是造成2013年7和8月安吉毛竹林NEP降低的根本原因.     

Changes in timing of seasonal peak photosynthetic activity in northern ecosystems

Seasonality in photosynthetic activity is a critical component of seasonal carbon, water, and energy cycles in the Earth system. This characteristic is a consequence of plant's adaptive evolutionary processes to a given set of environmental conditions. Changing climate in northern lands (>30°N) alters the state of climatic constraints on plant growth, and therefore, changes in the seasonality and carbon accumulation are anticipated. However, how photosynthetic seasonality evolved to its current state, and what role climatic constraints and their variability played in this process and ultimately in carbon cycle is still poorly understood due to its complexity. Here, we take the “laws of minimum” as a basis and introduce a new framework where the timing (day of year) of peak photosynthetic activity (DOY_Pmax) acts as a proxy for plant's adaptive state to climatic constraints on its growth. Our analyses confirm that spatial variations in DOY_Pmax reflect spatial gradients in climatic constraints as well as seasonal maximum and total productivity. We find a widespread warming‐induced advance in DOY_Pmax (?1.66 ± 0.30 days/decade, p < 0.001) across northern lands, indicating a spatiotemporal dynamism of climatic constraints to plant growth. We show that the observed changes in DOY_Pmax are associated with an increase in total gross primary productivity through enhanced carbon assimilation early in the growing season, which leads to an earlier phase shift in land‐atmosphere carbon fluxes and an increase in their amplitude. Such changes are expected to continue in the future based on our analysis of earth system model projections. Our study provides a simplified, yet realistic framework based on first principles for the complex mechanisms by which various climatic factors constrain plant growth in northern ecosystems.     

Hippos alter their aggregations to mitigate density-dependent drought effects

Megaherbivores play a critical role in the ecology of African savannas and grasslands. In addition, these systems are forecast to experience more frequent and severe droughts as a product of changes in the global climate. Thus, the continued conservation of megaherbivores and their associated ecosystems will require a better understanding of how megaherbivores respond to drought by shifting their movement, diet and social behaviour. We address this need by investigating the factors affecting changes in the abundance of common hippopotamus (Hippopotamus amphibius; hereafter: ‘hippos’) throughout the six major rivers of Kruger National Park, South Africa, during and following the severe drought of 2015/2016. Specifically, we aimed to understand the role of two environmental characteristics that have relevance to hippos and that changed in response to drought: vegetation condition and the extent of pooled surface water. In addition, we investigated the extent to which pre-drought density affected changes in hippo abundance. Although vegetation and daytime refugia both appeared to influence pre-drought hippo abundance, these factors were less important to the change in hippo abundance related to the drought. Instead, the response to drought was most strongly related to the pre-drought abundance of hippos, where river segments supporting more than 50 individuals prior to the drought in 2015 decreased by more than half on average. Furthermore, we show that the degree of aggregation decreased from 2015 to 2016 because of the drought, but then began to increase again as the rains returned in 2017. Our results suggest that in addition to the large pools that support large aggregations of hippos in typical years, additional smaller pools are likely important for accommodating this drought-induced dispersion. However, maintaining this distribution of pools will likely become more challenging as southern Africa's population and water demands increase.     

Grazing-induced legacy effects enhance plant adaption to drought by larger root allocation plasticity

放牧诱导的植物遗留效应可以通过较大的根系分配可塑性增强其干旱适应性 为探索植物的放牧遗留效应是否有利于天然草原生态系统应对干旱环境,我们采集了 内蒙古典型草原自由放牧和多年围封样地内的冰草(Agropyron cristatum)和黄囊苔草(Carex korshinskyi)幼苗 进行了温室控水试验。研究结果表明,干旱处理对自由放牧样地采集的冰草和黄囊苔草子株生物量、子株数量和总生物量的影响较小;自由放牧区的冰草与黄囊苔草较强的干旱适应性可部分由干旱处理下较大的根系分配可塑性来解释。本研究结果表明合理放牧是天然草原适应气候变化的潜在管理办法之一。     

Investigating the long‐term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems

We investigated how the legacy of warming and summer drought affected microbial communities in five different replicated long‐term (>10 years) field experiments across Europe (EU‐FP7 INCREASE infrastructure). To focus explicitly on legacy effects (i.e., indirect rather than direct effects of the environmental factors), we measured microbial variables under the same moisture and temperature in a brief screening, and following a pre‐incubation at stable conditions. Specifically, we investigated the size and composition of the soil microbial community (PLFA) alongside measurements of bacterial (leucine incorporation) and fungal (acetate in ergosterol incorporation) growth rates, previously shown to be highly responsive to changes in environmental factors, and microbial respiration. We found no legacy effects on the microbial community size, composition, growth rates, or basal respiration rates at the effect sizes used in our experimental setup (0.6 °C, about 30% precipitation reduction). Our findings support previous reports from single short‐term ecosystem studies thereby providing a clear evidence base to allow long‐term, broad‐scale generalizations to be made. The implication of our study is that warming and summer drought will not result in legacy effects on the microbial community and their processes within the effect sizes here studied. While legacy effects on microbial processes during perturbation cycles, such as drying–rewetting, and on tolerance to drought and warming remain to be studied, our results suggest that any effects on overall ecosystem processes will be rather limited. Thus, the legacies of warming and drought should not be prioritized factors to consider when modeling contemporary rates of biogeochemical processes in soil.     

基于多源遥感数据的农业干旱监测模型构建及应用

干旱监测问题是干旱灾害模拟与预警及旱灾防灾减灾的关键。基于2001-2013年淮河流域40个气象站资料、28个土壤墒情站点和中分辨率成像光谱仪（MODIS）多源遥感数据,采用SEN趋势法和标准化降水蒸散指数（SPEI）等方法,综合了大气-植被-土壤相互作用等多元成因,构建了适用于淮河流域多源综合遥感干旱监测模型,探讨淮河流域干旱时空规律。研究表明：（1）基于多源数据构建综合干旱监测模型,利用土壤墒情和典型年份干旱监测对综合干旱监测模型适用性进行评价,通过了P < 0.01的显著性检验,构建的模型可综合反映出农业和气象干旱多源信息;（2）淮河流域干旱面积和干旱频率大都集中在4-5月和7-9月,9月份受旱面积最大。河南省是淮河流域受旱频率最高,其干旱面积占淮河流域多年平均干旱面积比重最大（38%）,其次是安徽（22%）,旱地受旱面积比重大于水田受旱面积比重;（3）淮河流域2、3和5月干旱有显著减弱趋势;而1、4和6月则有增强趋势。淮河流域小麦灌浆-成熟时期（4-6月）缺水对小麦粮食产量影响显著,综合淮河流域干旱趋势变化,需强化淮河流域4月份小麦的干旱监测与旱灾预警。     

Drought-induced increase in tree mortality and corresponding decrease in the carbon sink capacity of Canada's boreal forests from 1970 to 2020

Canada's boreal forests, which occupy approximately 30% of boreal forests worldwide, play an important role in the global carbon budget. However, there is little quantitative information available regarding the spatiotemporal changes in the drought-induced tree mortality of Canada's boreal forests overall and their associated impacts on biomass carbon dynamics. Here, we develop spatiotemporally explicit estimates of drought-induced tree mortality and corresponding biomass carbon sink capacity changes in Canada's boreal forests from 1970 to 2020. We show that the average annual tree mortality rate is approximately 2.7%. Approximately 43% of Canada's boreal forests have experienced significantly increasing tree mortality trends (71% of which are located in the western region of the country), and these trends have accelerated since 2002. This increase in tree mortality has resulted in significant biomass carbon losses at an approximate rate of 1.51 ± 0.29 MgC ha⁻¹ year⁻¹ (95% confidence interval) with an approximate total loss of 0.46 ± 0.09 PgC year⁻¹ (95% confidence interval). Under the drought condition increases predicted for this century, the capacity of Canada's boreal forests to act as a carbon sink will be further reduced, potentially leading to a significant positive climate feedback effect.     

Remote sensing of sun-induced fluorescence to improve modeling of diurnal courses of gross primary production (GPP)

Terrestrial gross primary production (GPP) is an important parameter to explore and quantify carbon fixation by plant ecosystems at various scales. Remote sensing (RS) offers a unique possibility to investigate GPP in a spatially explicit fashion; however, budgeting of terrestrial carbon cycles based on this approach still remains uncertain. To improve calculations, spatio-temporal variability of GPP must be investigated in more detail on local and regional scales. The overarching goal of this study is to enhance our knowledge on how environmentally induced changes of photosynthetic light-use efficiency (LUE) are linked with optical RS parameters. Diurnal courses of sun-induced fluorescence yield ( F _Syield) and the photochemical reflectance index of corn were derived from high-resolution spectrometric measurements and their potential as proxies for LUE was investigated. GPP was modeled using Monteith's LUE-concept and optical-based GPP and LUE values were compared with synoptically acquired eddy covariance data. It is shown that the diurnal response of complex physiological regulation of photosynthesis can be tracked reliably with the sun-induced fluorescence. Considering structural and physiological effects, this research shows for the first time that including sun-induced fluorescence into modeling approaches improves their results in predicting diurnal courses of GPP. Our results support the hypothesis that air- or spaceborne quantification of sun-induced fluorescence yield may become a powerful tool to better understand spatio-temporal variations of fluorescence yield, photosynthetic efficiency and plant stress on a global scale.     

A cross-biome comparison of daily light use efficiency for gross primary production

Vegetation light use efficiency is a key physiological parameter at the canopy scale, and at the daily time step is a component of remote sensing algorithms for scaling gross primary production (GPP) and net primary production (NPP) over regional to global domains. For the purposes of calibrating and validating the light use efficiency ( ε _g) algorithms, the components of ε _g– absorbed photosynthetically active radiation (APAR) and ecosystem GPP – must be measured in a variety of environments. Micrometeorological and mass flux measurements at eddy covariance flux towers can be used to estimate APAR and GPP, and the emerging network of flux tower sites offers the opportunity to investigate spatial and temporal patterns in ε _g at the daily time step. In this study, we examined the relationship of daily GPP to APAR, and relationships of ε _g to climatic variables, at four micrometeorological flux tower sites – an agricultural field, a tallgrass prairie, a deciduous forest, and a boreal forest. The relationship of GPP to APAR was close to linear at the tallgrass prairie site but more nearly hyperbolic at the other sites. The sites differed in the mean and range of daily ε _g, with higher values associated with the agricultural field than the boreal forest. ε_g decreased with increasing APAR at all sites, a function of mid‐day saturation of GPP and higher ε _g under overcast conditions. ε _g was generally not well correlated with vapor pressure deficit or maximum daily temperature. At the agricultural site, a ε _g decline towards the end of the growing season was associated with a decrease in foliar nitrogen concentration. At the tallgrass prairie site, a decline in ε _g in August was associated with soil drought. These results support inclusion of parameters for cloudiness and the phenological status of the vegetation, as well as use of biome‐specific parameterization, in operational ε _g algorithms.