Drought- and heat-induced mortality of conifer trees is explained by leaf and growth legacies.

An increased frequency and severity of droughts and heat waves have resulted in increased tree mortality and forest dieback across the world, but underlying mechanisms are poorly understood. We used a common garden experiment with 20 conifer tree species to quantify mortality after three consecutive hot, dry summers and tested whether mortality could be explained by putative underlying mechanisms, such as stem hydraulics and legacies affected by leaf life span and stem growth responses to previous droughts. Mortality varied from 0 to 79% across species and was not affected by hydraulic traits. Mortality increased with species' leaf life span probably because leaf damage caused crown dieback and contributed to carbon depletion and bark beetle damage. Mortality also increased with lower growth resilience, which may exacerbate the contribution of carbon depletion and bark beetle sensitivity to tree mortality. Our study highlights how ecological legacies at different time scales can explain tree mortality in response to hot, dry periods and climate change.

Coupled hydraulics and carbon economy underlie age-related growth decline and revitalisation of sand-fixing shrubs after crown removal.

Crown removal revitalises sand-fixing shrubs that show declining vigour with age in drought-prone environments; however, the underlying mechanisms are poorly understood. Here, we addressed this knowledge gap by comparing the growth performance, xylem hydraulics and plant carbon economy across different plant ages (10, 21 and 33 years) and treatments (control and crown removal) using a representative sand-fixing shrub (Caragana microphylla Lam.) in northern China. We found that growth decline with plant age was accompanied by simultaneous decreases in soil moisture, plant hydraulic efficiency and photosynthetic capacity, suggesting that these interconnected changes in plant water relations and carbon economy were responsible for this decline. Following crown removal, quick resprouting, involving remobilisation of root nonstructural carbohydrate reserves, contributed to the reconstruction of an efficient hydraulic system and improved plant carbon status, but this became less effective in older shrubs. These age-dependent effects of carbon economy and hydraulics on plant growth vigour provide a mechanistic explanation for the age-related decline and revitalisation of sand-fixing shrubs. This understanding is crucial for the development of suitable management strategies for shrub plantations constructed with species having the resprouting ability and contributes to the sustainability of ecological restoration projects in water-limited sandy lands.

Diel and seasonal stem growth responses to climatic variation are consistent across species in a subtropical tree community.

Understanding how intra-annual stem growth responds to atmospheric and soil conditions is essential for assessing the effects of climate extremes on forest productivity. In species-poor forests, such understanding can be obtained by studying stem growth of the dominant species. Yet, in species-rich (sub-)tropical forests, it is unclear whether these responses are consistent among species. We monitored intra-annual stem growth with high-resolution dendrometers for 27 trees belonging to 14 species over 5 yr in a montane subtropical forest. We quantified diel and seasonal stem growth patterns, verified to what extent observed growth patterns coincide across species and analysed their main climatic drivers. We found very consistent intra-annual growth patterns across species. Species varied in the rate but little in the timing of growth. Diel growth patterns revealed that - across species - trees mainly grew before dawn when vapour pressure deficit (VPD) was low. Within the year, trees mainly grew between May and August driven by temperature and VPD, but not by soil moisture. Our study reveals highly consistent stem growth patterns and climatic drivers at community level. Further studies are needed to verify whether these results hold across climates and forests, and whether they can be scaled up to estimate forest productivity.

High vapour pressure deficit enhances turgor limitation of stem growth in an Asian tropical rainforest tree.

Tropical forests are experiencing increases in vapour pressure deficit (D), with possible negative impacts on tree growth. Tree-growth reduction due to rising D is commonly attributed to carbon limitation, thus overlooking the potentially important mechanism of D-induced impairment of wood formation due to an increase in turgor limitation. Here we calibrate a mechanistic tree-growth model to simulate turgor limitation of radial stem growth in mature Toona cilitata trees in an Asian tropical forest. Hourly sap flow and dendrometer measurements were collected to simulate turgor-driven growth during the growing season. Simulated seasonal patterns of radial stem growth matched well with growth observations. Growth mainly occurred at night and its pre-dawn build-up appeared to be limited under higher D. Across seasons, the night-time turgor pressure required for growth was negatively related to previous midday D, possibly due to a relatively high canopy conductance at high D, relative to stem rehydration. These findings provide the first evidence that tropical trees grow at night and that turgor pressure limits tree growth. We suggest including turgor limitation of tree stem growth in models also for tropical forest carbon dynamics, in particular, if these models simulate effects of warming and increased frequency of droughts.

Networking the forest infrastructure towards near real-time monitoring - A white paper.

Forests account for nearly 90 % of the world's terrestrial biomass in the form of carbon and they support 80 % of the global biodiversity. To understand the underlying forest dynamics, we need a long-term but also relatively high-frequency, networked monitoring system, as traditionally used in meteorology or hydrology. While there are numerous existing forest monitoring sites, particularly in temperate regions, the resulting data streams are rarely connected and do not provide information promptly, which hampers real-time assessments of forest responses to extreme climate events. The technology to build a better global forest monitoring network now exists. This white paper addresses the key structural components needed to achieve a novel meta-network. We propose to complement - rather than replace or unify - the existing heterogeneous infrastructure with standardized, quality-assured linking methods and interacting data processing centers to create an integrated forest monitoring network. These automated (research topic-dependent) linking methods in atmosphere, biosphere, and pedosphere play a key role in scaling site-specific results and processing them in a timely manner. To ensure broad participation from existing monitoring sites and to establish new sites, these linking methods must be as informative, reliable, affordable, and maintainable as possible, and should be supplemented by near real-time remote sensing data. The proposed novel meta-network will enable the detection of emergent patterns that would not be visible from isolated analyses of individual sites. In addition, the near real-time availability of data will facilitate predictions of current forest conditions (nowcasts), which are urgently needed for research and decision making in the face of rapid climate change. We call for international and interdisciplinary efforts in this direction.

Ring- and diffuse-porous tree species from a cold temperate forest diverge in stem hydraulic traits, leaf photosynthetic traits, growth rate and altitudinal distribution.

In cold and humid temperate forests, low temperature, late frost and frequent freeze-thaw cycles are the main factors limiting tree growth and survival. Ring- and diffuse-porous tree species differing in xylem anatomy coexist in these forests, but their divergent adaptations to these factors have been poorly explored. To fill this knowledge gap, we compared four ring-porous and four diffuse-porous tree species from the same temperate forest in Northeast China by quantifying their leaf and stem functional traits, their stem growth rates using tree ring analysis and their resistance to cold represented by upper altitude species distribution borders from survey data. We found that the ring-porous trees were characterized by traits related to more rapid water transport, carbon gain and stem growth rates than those of the diffuse-porous species. Compared with the diffuse-porous species, the ring-porous species had a significantly higher shoot hydraulic conductance (Ks-shoot, 0.52 vs 1.03 kg m-1 s-1 MPa-1), leaf photosynthetic rate (An, 11.28 vs 15.83 µmol m-2 s-1), relative basal area increment (BAIr, 2.28 vs 0.72 cm year-1) and stem biomass increment (M, 0.34 vs 0.09 kg year-1 m-1). However, the observed upper elevational distribution limit of the diffuse-porous species was higher than that of the ring-porous species and was associated with higher values of conservative traits, such as longer leaf life span (R2 = 0.52). Correspondingly, BAIr and M showed significant positive correlations with acquisitive traits such as Ks-shoot (R2 = 0.77) and leaf photosynthetic rate (R2 = 0.73) across the eight species, with the ring-porous species occurring at the fast-acquisitive side of the spectrum and the diffuse-porous species located on the opposite side. The observed contrasts in functional traits between the two species groups improved our understanding of their differences in terms of growth strategies and adaptive capabilities in the cold, humid temperate forests.

Vegetative phenologies of lianas and trees in two Neotropical forests with contrasting rainfall regimes.

Among tropical forests, lianas are predicted to have a growth advantage over trees during seasonal drought, with substantial implications for tree and forest dynamics. We tested the hypotheses that lianas maintain higher water status than trees during seasonal drought and that lianas maximize leaf cover to match high, dry-season light conditions, while trees are more limited by moisture availability during the dry season. We monitored the seasonal dynamics of predawn and midday leaf water potentials and leaf phenology for branches of 16 liana and 16 tree species in the canopies of two lowland tropical forests with contrasting rainfall regimes in Panama. In a wet, weakly seasonal forest, lianas maintained higher water balance than trees and maximized their leaf cover during dry-season conditions, when light availability was high, while trees experienced drought stress. In a drier, strongly seasonal forest, lianas and trees displayed similar dry season reductions in leaf cover following strong decreases in soil water availability. Greater soil moisture availability and a higher capacity to maintain water status allow lianas to maintain the turgor potentials that are critical for plant growth in a wet and weakly seasonal forest but not in a dry and strongly seasonal forest.

Drought resilience of conifer species is driven by leaf lifespan but not by hydraulic traits.

Increased droughts impair tree growth worldwide. This study analyzes hydraulic and carbon traits of conifer species, and how they shape species strategies in terms of their growth rate and drought resilience. We measured 43 functional stem and leaf traits for 28 conifer species growing in a 50-yr-old common garden experiment in the Netherlands. We assessed: how drought- and carbon-related traits are associated across species, how these traits affect stem growth and drought resilience, and how traits and drought resilience are related to species' climatic origin. We found two trait spectra: a hydraulics spectrum reflecting a trade-off between hydraulic and biomechanical safety vs hydraulic efficiency, and a leaf economics spectrum reflecting a trade-off between tough, long-lived tissues vs high carbon assimilation rate. Pit aperture size occupied a central position in the trait-based network analysis and also increased stem growth. Drought recovery decreased with leaf lifespan. Conifer species with long-lived leaves suffer from drought legacy effects, as drought-damaged leaves cannot easily be replaced, limiting growth recovery after drought. Leaf lifespan, rather than hydraulic traits, can explain growth responses to a drier future.

Stem Trait Spectra Underpin Multiple Functions of Temperate Tree Species.

A central paradigm in comparative ecology is that species sort out along a slow-fast resource economy spectrum of plant strategies, but this has been rarely tested for a comprehensive set of stem traits and compartments. We tested how stem traits vary across wood and bark of temperate tree species, whether a slow-fast strategy spectrum exists, and what traits make up this plant strategy spectrum. For 14 temperate tree species, 20 anatomical, chemical, and morphological traits belonging to six key stem functions were measured for three stem compartments (inner wood, outer wood, and bark). The trait variation was explained by major taxa (38%), stem compartments (24%), and species within major taxa (19%). A continuous plant strategy gradient was found across and within taxa, running from hydraulic safe gymnosperms to conductive angiosperms. Both groups showed a second strategy gradient related to chemical defense. Gymnosperms strongly converged in their trait strategies because of their uniform tracheids. Angiosperms strongly diverged because of their different vessel arrangement and tissue types. The bark had higher concentrations of nutrients and phenolics whereas the wood had stronger physical defense. The gymnosperms have a conservative strategy associated with strong hydraulic safety and physical defense, and a narrow, specialized range of trait values, which allow them to grow well in drier and unproductive habitats. The angiosperm species show a wider trait variation in all stem compartments, which makes them successful in marginal- and in mesic, productive habitats. The associations between multiple wood and bark traits collectively define a slow-fast stem strategy spectrum as is seen also for each stem compartment.

Stem traits, compartments and tree species affect fungal communities on decaying wood.

Dead wood quantity and quality is important for forest biodiversity, by determining wood-inhabiting fungal assemblages. We therefore evaluated how fungal communities were regulated by stem traits and compartments (i.e. bark, outer- and inner wood) of 14 common temperate tree species. Fresh logs were incubated in a common garden experiment in a forest site in the Netherlands. After 1 and 4 years of decay, the fungal composition of different compartments was assessed using Internal Transcribed Spacer amplicon sequencing. We found that fungal alpha diversity differed significantly across tree species and stem compartments, with bark showing significantly higher fungal diversity than wood. Gymnosperms and Angiosperms hold different fungal communities, and distinct fungi were found between inner wood and other compartments. Stem traits showed significant afterlife effects on fungal communities; traits associated with accessibility (e.g. conduit diameter), stem chemistry (e.g. C, N, lignin) and physical defence (e.g. density) were important factors shaping fungal community structure in decaying stems. Overall, stem traits vary substantially across stem compartments and tree species, thus regulating fungal communities and the long-term carbon dynamics of dead trees.

Pit and tracheid anatomy explain hydraulic safety but not hydraulic efficiency of 28 conifer species.

Conifers face increased drought mortality risks because of drought-induced embolism in their vascular system. Variation in embolism resistance may result from species differences in pit structure and function, as pits control the air seeding between water-transporting conduits. This study quantifies variation in embolism resistance and hydraulic conductivity for 28 conifer species grown in a 50-year-old common garden experiment and assesses the underlying mechanisms. Conifer species with a small pit aperture, high pit aperture resistance, and large valve effect were more resistant to embolism, as they all may reduce air seeding. Surprisingly, hydraulic conductivity was only negatively correlated with tracheid cell wall thickness. Embolism resistance and its underlying pit traits related to pit size and sealing were more strongly phylogenetically controlled than hydraulic conductivity and anatomical tracheid traits. Conifers differed in hydraulic safety and hydraulic efficiency, but there was no trade-off between safety and efficiency because they are driven by different xylem anatomical traits that are under different phylogenetic control.

Number of growth days and not length of the growth period determines radial stem growth of temperate trees.

Radial stem growth dynamics at seasonal resolution are essential to understand how forests respond to climate change. We studied daily radial growth of 160 individuals of seven temperate tree species at 47 sites across Switzerland over 8 years. Growth of all species peaked in the early part of the growth season and commenced shortly before the summer solstice, but with species-specific seasonal patterns. Day length set a window of opportunity for radial growth. Within this window, the probability of daily growth was constrained particularly by air and soil moisture, resulting in intermittent growth to occur only on 29 to 77 days (30% to 80%) within the growth period. The number of days with growth largely determined annual growth, whereas the growth period length contributed less. We call for accounting for these non-linear intra-annual and species-specific growth dynamics in tree and forest models to reduce uncertainties in predictions under climate change.

Hydraulic prediction of drought-induced plant dieback and top-kill depends on leaf habit and growth form.

Hydraulic failure caused by severe drought contributes to aboveground dieback and whole-plant death. The extent to which dieback or whole-plant death can be predicted by plant hydraulic traits has rarely been tested among species with different leaf habits and/or growth forms. We investigated 19 hydraulic traits in 40 woody species in a tropical savanna and their potential correlations with drought response during an extreme drought event during the El Niño-Southern Oscillation in 2015. Plant hydraulic trait variation was partitioned substantially by leaf habit but not growth form along a trade-off axis between traits that support drought tolerance versus avoidance. Semi-deciduous species and shrubs had the highest branch dieback and top-kill (complete aboveground death) among the leaf habits or growth forms. Dieback and top-kill were well explained by combining hydraulic traits with leaf habit and growth form, suggesting integrating life history traits with hydraulic traits will yield better predictions.

Growth of 19 conifer species is highly sensitive to winter warming, spring frost and summer drought.

BACKGROUND AND AIMS: Conifers are key components of many temperate and boreal forests and are important for forestry, but species differences in stem growth responses to climate are still poorly understood and may hinder effective management of these forests in a warmer and drier future. METHODS: We studied 19 Northern Hemisphere conifer species planted in a 50-year-old common garden experiment in the Netherlands to (1) assess the effect of temporal dynamics in climate on stem growth, (2) test for a possible positive relationship between the growth potential and climatic growth sensitivity across species, and (3) evaluate the extent to which stem growth is controlled by phylogeny. KEY RESULTS: Eighty-nine per cent of the species showed a significant reduction in stem growth to summer drought, 37 % responded negatively to spring frost and 32 % responded positively to higher winter temperatures. Species differed largely in their growth sensitivity to climatic variation and showed, for example, a four-fold difference in growth reduction to summer drought. Remarkably, we did not find a positive relationship between productivity and climatic sensitivity, but instead observed that some species combined a low growth sensitivity to summer drought with high growth potential. Both growth sensitivity to climate and growth potential were partly phylogenetically controlled. CONCLUSIONS: A warmer and drier future climate is likely to reduce the productivity of most conifer species. We did not find a relationship between growth potential and growth sensitivity to climate; instead, some species combined high growth potential with low sensitivity to summer drought. This may help forest managers to select productive species that are able to cope with a warmer and drier future.

Why trees grow at night.

The timing of diel stem growth of mature forest trees is still largely unknown, as empirical data with high temporal resolution have not been available so far. Consequently, the effects of day-night conditions on tree growth remained uncertain. Here we present the first comprehensive field study of hourly-resolved radial stem growth of seven temperate tree species, based on 57 million underlying data points over a period of up to 8 yr. We show that trees grow mainly at night, with a peak after midnight, when the vapour pressure deficit (VPD) is among the lowest. A high VPD strictly limits radial stem growth and allows little growth during daylight hours, except in the early morning. Surprisingly, trees also grow in moderately dry soil when the VPD is low. Species-specific differences in diel growth dynamics show that species able to grow earlier during the night are associated with the highest number of hours with growth per year and the largest annual growth increment. We conclude that species with the ability to overcome daily water deficits faster have greater growth potential. Furthermore, we conclude that growth is more sensitive than carbon uptake to dry air, as growth stops before stomata are known to close.

Traits, strategies, and niches of liana species in a tropical seasonal rainforest.

Plant functional traits and strategies hold the promise to explain species distribution, but few studies have linked multiple traits to multiple niche dimensions (i.e., light, water, and nutrients). Here, we analyzed for 29 liana species in a Chinese tropical seasonal rainforest how: (1) trait associations and trade-offs lead to different plant strategies; and (2) how these traits shape species' niche dimensions. Eighteen functional traits related to light, water, and nutrient use were measured and species niche dimensions were quantified using species distribution in a 20-ha plot combined with data on canopy gaps, topographic water availability, and soil nutrients. We found a tissue toughness spectrum ranging from soft to hard tissues along which species also varied from acquisitive to conservative water use, and a resource acquisition spectrum ranging from low to high light capture and nutrient use. Intriguingly, each spectrum partly reflected the conservative-acquisitive paradigm, but at the same time, the tissue toughness and the resource acquisition spectrum were uncoupled. Resource niche dimensions were better predicted by individual traits than by multivariate plant strategies. This suggests that trait components that underlie multivariate strategy axes, rather than the plant strategies themselves determine species distributions. Different traits were important for different niche dimensions. In conclusion, plant functional traits and strategies can indeed explain species distributions, but not in a simple and straight forward way. Although the identification of global plant strategies has significantly advanced the field, this research shows that global, multivariate generalizations are difficult to translate to local conditions, as different components of these strategies are important under different local conditions.

Differential determinants of growth rates in subtropical evergreen and deciduous juvenile trees: carbon gain, hydraulics and nutrient-use efficiencies.

Growth rate varies across plant species and represents an important ecological strategy for competition, resource-use and fitness. However, empirical studies often show a low predictability of functional traits to tree growth. We measured stem diameter and height growth rates (DGRs and HGRs) of 96 juvenile trees (2-5 m tall) of eight evergreen and eight deciduous broadleaf tree species over three consecutive years in a subtropical forest in south-western China. We examined the relationships between tree growth rates and 20 leaf/stem traits that are associated with carbon gain, stem hydraulics and nutrient-use efficiency, as well as the difference between evergreen and deciduous trees. We found that cross-species variations of stem DGR/HGR can be predicted by leaf photosynthetic capacity, leaf mass per area, xylem-theoretical-specific hydraulic conductivity, wood density (WD) and photosynthetic-nutrient-use efficiencies. Higher leaf carbon assimilation and lower leaf/stem constructing costs facilitate deciduous species to be more resource acquisitive and consequently faster growth within a relatively shorter growing season, whereas evergreen species exhibit more conservative strategies and thus slower growth. Furthermore, stem growth rates of evergreen species showed were more dependence on leaf carbon gains, whereas stem hydraulic efficiency was more important for deciduous tree growth. Our results suggest that physiological traits (photosynthesis, hydraulics and nutrient-use efficiency) can predict tree diameter and height growth of subtropical tree species. The differential resource acquisition and use strategies and their associations with tree growth between evergreen and deciduous trees provide insights into explaining the coexistence of evergreen and deciduous tree species in subtropical forests.

Determinants of legacy effects in pine trees - implications from an irrigation-stop experiment.

Tree responses to altered water availability range from immediate (e.g. stomatal regulation) to delayed (e.g. crown size adjustment). The interplay of the different response times and processes, and their effects on long-term whole-tree performance, however, is hardly understood. Here we investigated legacy effects on structures and functions of mature Scots pine in a dry inner-Alpine Swiss valley after stopping an 11-yr lasting irrigation treatment. Measured ecophysiological time series were analysed and interpreted with a system-analytic tree model. We found that the irrigation stop led to a cascade of downregulations of physiological and morphological processes with different response times. Biophysical processes responded within days, whereas needle and shoot lengths, crown transparency, and radial stem growth reached control levels after up to 4 yr only. Modelling suggested that organ and carbon reserve turnover rates play a key role for a tree's responsiveness to environmental changes. Needle turnover rate was found to be most important to accurately model stem growth dynamics. We conclude that leaf area and its adjustment time to new conditions is the main determinant for radial stem growth of pine trees as the transpiring area needs to be supported by a proportional amount of sapwood, despite the growth-inhibiting environmental conditions.

Scots pine trees react to drought by increasing xylem and phloem conductivities.

Drought limits the long-distance transport of water in the xylem due to the reduced leaf-to-soil water potential difference and possible embolism-related losses of conductance and of sugars in the phloem due to the higher viscosity of the dehydrated sugary solution. This condition can have cascading effects in water and carbon (C) fluxes that may ultimately cause tree death. We hypothesize that the maintenance of xylem and phloem conductances is fundamental for survival also under reduced resource availability, when trees may produce effective and low C cost anatomical adjustments in the xylem and phloem close to the treetop where most of the hydraulic resistance is concentrated. We analyzed the treetop xylem and phloem anatomical characteristics in coexisting Scots pine trees, symptomatic and non-symptomatic of drought-induced dieback. We selected the topmost 55 cm of the main stem and selected several sampling positions at different distances from the stem apex to test for differences in the axial patterns between the two groups of trees. We measured the annual ring area, the tracheid hydraulic diameter (Dh) and cell wall thickness (CWT), the conductive phloem area and the average lumen diameter of the 20 largest phloem sieve cells (Dph). Declining trees grew less than the non-declining ones, and despite the similar axial scaling of anatomical traits, had larger Dh and lower CWT. Moreover, declining trees had wider Dph. Our results demonstrate that even under drought stress, maintenance of xylem and phloem efficiencies is of primary importance for survival, even if producing fewer larger tracheids may lead to a xylem more vulnerable to embolism formation.

Low growth resilience to drought is related to future mortality risk in trees.

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.