Drought increases Norway spruce susceptibility to the Eurasian spruce bark beetle and its associated fungi.

Drought affects the complex interactions between Norway spruce, the bark beetle Ips typographus and associated microorganisms. We investigated the interplay of tree water status, defense and carbohydrate reserves with the incidence of bark beetle attack and infection of associated fungi in mature spruce trees. We installed roofs to induce a 2-yr moderate drought in a managed spruce stand to examine a maximum of 10 roof and 10 control trees for resin flow (RF), predawn twig water potentials, terpene, phenolic and carbohydrate bark concentrations, and bark beetle borings in field bioassays before and after inoculation with Endoconidiophora polonica and Grosmannia penicillata. Drought-stressed trees showed more attacks and significantly longer fungal lesions than controls, but maintained terpene resin defenses at predrought levels. Reduced RF and lower mono- and diterpene, but not phenolic concentrations were linked with increased host selection. Bark beetle attack and fungi stimulated chemical defenses, yet G. penicillata reduced phenolic and carbohydrate contents. Chemical defenses did not decrease under mild, prolonged drought in our simulated small-scale biotic infestations. However, during natural mass attacks, reductions in carbon fixation under drought, in combination with fungal consumption of carbohydrates, may deplete tree defenses and facilitate colonization by I. typographus.

The quandary of sources and sinks of CO2 efflux in tree stems-new insights and future directions.

Stem respiration (RS) substantially contributes to the return of photo assimilated carbon to the atmosphere and, thus, to the tree and ecosystem carbon balance. Stem CO2 efflux (ECO2) is often used as a proxy for RS. However, this metric has often been challenged because of the uncertain origin of CO2 emitted from the stem due to post-respiratory processes. In this Insight, we (i) describe processes affecting the quantification of RS, (ii) review common methodological approaches to quantify and model RS and (iii) develop a research agenda to fill the most relevant knowledge gaps that we identified. Dissolution, transport and accumulation of respired CO2 away from its production site, reassimilation of respired CO2 via stem photosynthesis and the enzyme phosphoenolpyruvate carboxylase, axial CO2 diffusion in the gas phase, shifts in the respiratory substrate and non-respiratory oxygen (O2) consumption are the most relevant processes causing divergence between RS and measured stem gas exchange (ECO2 or O2 influx, IO2). Two common methodological approaches to estimate RS, namely the CO2 mass balance approach and the O2 consumption technique, circumvent some of these processes but have yielded inconsistent results regarding the fate of respired CO2. Stem respiration modelling has recently progressed at the organ and tree levels. However, its implementation in large-scale models, commonly operated from a source-driven perspective, is unlikely to reflect adequate mechanisms. Finally, we propose hypotheses and approaches to advance the knowledge of the stem carbon balance, the role of sap pH on RS, the reassimilation of respired CO2, RS upscaling procedures, large-scale RS modelling and shifts in respiratory metabolism during environmental stress.

The mobilization and transport of newly fixed carbon are driven by plant water use in an experimental rainforest under drought.

Non-structural carbohydrates (NSCs) are building blocks for biomass and fuel metabolic processes. However, it remains unclear how tropical forests mobilize, export, and transport NSCs to cope with extreme droughts. We combined drought manipulation and ecosystem 13CO2 pulse-labeling in an enclosed rainforest at Biosphere 2, assessed changes in NSCs, and traced newly assimilated carbohydrates in plant species with diverse hydraulic traits and canopy positions. We show that drought caused a depletion of leaf starch reserves and slowed export and transport of newly assimilated carbohydrates below ground. Drought effects were more pronounced in conservative canopy trees with limited supply of new photosynthates and relatively constant water status than in those with continual photosynthetic supply and deteriorated water status. We provide experimental evidence that local utilization, export, and transport of newly assimilated carbon are closely coupled with plant water use in canopy trees. We highlight that these processes are critical for understanding and predicting tree resistance and ecosystem fluxes in tropical forest under drought.

Mother trees, altruistic fungi, and the perils of plant personification.

There are growing doubts about the true role of the common mycorrhizal networks (CMN or wood wide web) connecting the roots of trees in forests. We question the claims of a substantial carbon transfer from 'mother trees' to their offspring and nearby seedlings through the CMN. Recent reviews show that evidence for the 'mother tree concept' is inconclusive or absent. The origin of this concept seems to stem from a desire to humanize plant life but can lead to misunderstandings and false interpretations and may eventually harm rather than help the commendable cause of preserving forests. Two recent books serve as examples: The Hidden Life of Trees and Finding the Mother Tree.

Carbon dynamics during long-term starving poplar trees-the importance of older carbohydrates and a shift to lipids during survival.

Carbon (C) assimilation can be severely impaired during periods of environmental stress like drought or defoliation, making trees heavily dependent on the use of C reserve pools for survival; yet, dynamics of reserve use during periods of reduced C supply are still poorly understood. We used stem girdling in mature poplar trees (Populus tremula L. hybrids), a lipid-storing species, to permanently interrupt phloem C transport and induced C shortage in the isolated stem section below the girdle and monitored metabolic activity during three campaigns in the growing seasons of 2018, 2019, and 2021. We measured respiratory fluxes (CO2 and O2), NSC concentration, the respiratory substrate (based on isotopic analysis and CO2/O2 ratio) and the age of the respiratory substrate (based on radiocarbon analysis). Our study shows that poplar trees can survive long periods of reduced C supply from the canopy by switching in metabolism from recent carbohydrates to older storage pools with a potential mixture of respiratory substrates, including lipids. This mechanism of stress resilience can explain why tree decline may take many years until death occurs.

The Database of European Forest Insect and Disease Disturbances: DEFID2.

Insect and disease outbreaks in forests are biotic disturbances that can profoundly alter ecosystem dynamics. In many parts of the world, these disturbance regimes are intensifying as the climate changes and shifts the distribution of species and biomes. As a result, key forest ecosystem services, such as carbon sequestration, regulation of water flows, wood production, protection of soils, and the conservation of biodiversity, could be increasingly compromised. Despite the relevance of these detrimental effects, there are currently no spatially detailed databases that record insect and disease disturbances on forests at the pan-European scale. Here, we present the new Database of European Forest Insect and Disease Disturbances (DEFID2). It comprises over 650,000 harmonized georeferenced records, mapped as polygons or points, of insects and disease disturbances that occurred between 1963 and 2021 in European forests. The records currently span eight different countries and were acquired through diverse methods (e.g., ground surveys, remote sensing techniques). The records in DEFID2 are described by a set of qualitative attributes, including severity and patterns of damage symptoms, agents, host tree species, climate-driven trigger factors, silvicultural practices, and eventual sanitary interventions. They are further complemented with a satellite-based quantitative characterization of the affected forest areas based on Landsat Normalized Burn Ratio time series, and damage metrics derived from them using the LandTrendr spectral-temporal segmentation algorithm (including onset, duration, magnitude, and rate of the disturbance), and possible interactions with windthrow and wildfire events. The DEFID2 database is a novel resource for many large-scale applications dealing with biotic disturbances. It offers a unique contribution to design networks of experiments, improve our understanding of ecological processes underlying biotic forest disturbances, monitor their dynamics, and enhance their representation in land-climate models. Further data sharing is encouraged to extend and improve the DEFID2 database continuously. The database is freely available at https://jeodpp.jrc.ec.europa.eu/ftp/jrc-opendata/FOREST/DISTURBANCES/DEFID2/.

Ambient and substrate energy influence decomposer diversity differentially across trophic levels.

The species-energy hypothesis predicts increasing biodiversity with increasing energy in ecosystems. Proxies for energy availability are often grouped into ambient energy (i.e., solar radiation) and substrate energy (i.e., non-structural carbohydrates or nutritional content). The relative importance of substrate energy is thought to decrease with increasing trophic level from primary consumers to predators, with reciprocal effects of ambient energy. Yet, empirical tests are lacking. We compiled data on 332,557 deadwood-inhabiting beetles of 901 species reared from wood of 49 tree species across Europe. Using host-phylogeny-controlled models, we show that the relative importance of substrate energy versus ambient energy decreases with increasing trophic levels: the diversity of zoophagous and mycetophagous beetles was determined by ambient energy, while non-structural carbohydrate content in woody tissues determined that of xylophagous beetles. Our study thus overall supports the species-energy hypothesis and specifies that the relative importance of ambient temperature increases with increasing trophic level with opposite effects for substrate energy.

Differences between tree stem CO2 efflux and O2 influx rates cannot be explained by internal CO2 transport or storage in large beech trees.

Tree stem respiration (RS ) is a substantial component of the forest carbon balance. The mass balance approach uses stem CO2 efflux and internal xylem fluxes to sum up RS , while the oxygen-based method assumes O2 influx as a proxy of RS . So far, both approaches have yielded inconsistent results regarding the fate of respired CO2 in tree stems, a major challenge for quantifying forest carbon dynamics. We collected a data set of CO2 efflux, O2 influx, xylem CO2 concentration, sap flow, sap pH, stem temperature, nonstructural carbohydrates concentration and potential phosphoenolpyruvate carboxylase (PEPC) capacity on mature beech trees to identify the sources of differences between approaches. The ratio of CO2 efflux to O2 influx was consistently below unity (0.7) along a 3-m vertical gradient, but internal fluxes did not bridge the gap between influx and efflux, nor did we find evidence for changes in respiratory substrate use. PEPC capacity was comparable with that previously reported in green current-year twigs. Although we could not reconcile differences between approaches, results shed light on the uncertain fate of CO2 respired by parenchyma cells across the sapwood. Unexpected high values of PEPC capacity highlight its potential relevance as a mechanism of local CO2 removal, which merits further research.

Addressing a century-old hypothesis - do pioneer beetles of Ips typographus use volatile cues to find suitable host trees?

Global warming and more frequent climate extremes have caused bark beetle outbreaks of unprecedented scale of these insects in many conifer forests world-wide. Conifers that have been weakened by drought and heat or damaged by storms are highly susceptible to bark beetle infestation. A large proportion of trees with impaired defences provides good conditions for beetle population build-up of beetles, but mechanisms driving host search of pioneer beetles are still uncertain in several species, including the Eurasian spruce bark beetle Ips typographus. Despite a two-century-long history of bark beetle research, we still lack a sufficient understanding of interactions between I. typographus and its host Norway spruce (Picea abies) to forecast future disturbance regimes and forest dynamics. Depending on the scale (habitat or patch) and beetle population state (endemic or epidemic), host selection is likely driven by a combination of pre and postlanding cues, including visual selection or olfactory detection (kairomones). Here, we discuss primary attraction mechanisms and how volatile emission profiles of Norway spruce may provide cues on tree vitality and suitability for attacks by I. typographus, in particular during the endemic phase. We identify several crucial knowledge gaps and provide a research agenda addressing the experimental challenges of such investigations.

Conifer-killing bark beetles locate fungal symbionts by detecting volatile fungal metabolites of host tree resin monoterpenes.

Outbreaks of the Eurasian spruce bark beetle (Ips typographus) have decimated millions of hectares of conifer forests in Europe in recent years. The ability of these 4.0 to 5.5 mm long insects to kill mature trees over a short period has been sometimes ascribed to two main factors: (1) mass attacks on the host tree to overcome tree defenses and (2) the presence of fungal symbionts that support successful beetle development in the tree. While the role of pheromones in coordinating mass attacks has been well studied, the role of chemical communication in maintaining the fungal symbiosis is poorly understood. Previous evidence indicates that I. typographus can distinguish fungal symbionts of the genera Grosmannia, Endoconidiophora, and Ophiostoma by their de novo synthesized volatile compounds. Here, we hypothesize that the fungal symbionts of this bark beetle species metabolize spruce resin monoterpenes of the beetle's host tree, Norway spruce (Picea abies), and that the volatile products are used as cues by beetles for locating breeding sites with beneficial symbionts. We show that Grosmannia penicillata and other fungal symbionts alter the profile of spruce bark volatiles by converting the major monoterpenes into an attractive blend of oxygenated derivatives. Bornyl acetate was metabolized to camphor, and α- and ß-pinene to trans-4-thujanol and other oxygenated products. Electrophysiological measurements showed that I. typographus possesses dedicated olfactory sensory neurons for oxygenated metabolites. Both camphor and trans-4-thujanol attracted beetles at specific doses in walking olfactometer experiments, and the presence of symbiotic fungi enhanced attraction of females to pheromones. Another co-occurring nonbeneficial fungus (Trichoderma sp.) also produced oxygenated monoterpenes, but these were not attractive to I. typographus. Finally, we show that colonization of fungal symbionts on spruce bark diet stimulated beetles to make tunnels into the diet. Collectively, our study suggests that the blends of oxygenated metabolites of conifer monoterpenes produced by fungal symbionts are used by walking bark beetles as attractive or repellent cues to locate breeding or feeding sites containing beneficial microbial symbionts. The oxygenated metabolites may aid beetles in assessing the presence of the fungus, the defense status of the host tree and the density of conspecifics at potential feeding and breeding sites.

Amplifying effects of recurrent drought on the dynamics of tree growth and water use in a subalpine forest.

Despite recent advances in our understanding of drought impacts on tree functioning, we lack knowledge about the dynamic responses of mature trees to recurrent drought stress. At a subalpine forest site, we assessed the effects of three years of recurrent experimental summer drought on tree growth and water relations of Larix decidua Mill. and Picea abies (L. Karst.), two common European conifers representative for contrasting water-use strategies. We combined dendrometer and xylem sap flow measurements with analyses of xylem anatomy and non-structural carbohydrates and their carbon-isotope composition. Recurrent drought increased the effects of soil moisture limitation on growth and xylogenesis, and to a lesser extent on xylem sap flow. P. abies showed stronger growth responses to recurrent drought, reduced starch concentrations in branches and increased water-use efficiency when compared to L. decidua. Despite comparatively larger maximum tree water deficits than in P. abies, xylem formation of L. decidua was less affected by drought, suggesting a stronger capacity of rehydration or lower cambial turgor thresholds for growth. Our study shows that recurrent drought progressively increases impacts on mature trees of both species, which suggests that in a future climate increasing drought frequency could impose strong legacies on carbon and water dynamics of treeline species.

Global field observations of tree die-off reveal hotter-drought fingerprint for Earth's forests.

Earth's forests face grave challenges in the Anthropocene, including hotter droughts increasingly associated with widespread forest die-off events. But despite the vital importance of forests to global ecosystem services, their fates in a warming world remain highly uncertain. Lacking is quantitative determination of commonality in climate anomalies associated with pulses of tree mortality-from published, field-documented mortality events-required for understanding the role of extreme climate events in overall global tree die-off patterns. Here we established a geo-referenced global database documenting climate-induced mortality events spanning all tree-supporting biomes and continents, from 154 peer-reviewed studies since 1970. Our analysis quantifies a global "hotter-drought fingerprint" from these tree-mortality sites-effectively a hotter and drier climate signal for tree mortality-across 675 locations encompassing 1,303 plots. Frequency of these observed mortality-year climate conditions strongly increases nonlinearly under projected warming. Our database also provides initial footing for further community-developed, quantitative, ground-based monitoring of global tree mortality.

Climate Change Risks to Global Forest Health: Emergence of Unexpected Events of Elevated Tree Mortality Worldwide.

Recent observations of elevated tree mortality following climate extremes, like heat and drought, raise concerns about climate change risks to global forest health. We currently lack both sufficient data and understanding to identify whether these observations represent a global trend toward increasing tree mortality. Here, we document events of sudden and unexpected elevated tree mortality following heat and drought events in ecosystems that previously were considered tolerant or not at risk of exposure. These events underscore the fact that climate change may affect forests with unexpected force in the future. We use the events as examples to highlight current difficulties and challenges for realistically predicting such tree mortality events and the uncertainties about future forest condition. Advances in remote sensing technology and greater availably of high-resolution data, from both field assessments and satellites, are needed to improve both understanding and prediction of forest responses to future climate change.

Differential responses of grassland community nonstructural carbohydrate to experimental drought along a natural aridity gradient.

Plant nonstructural carbohydrates (NSC) can reflect community and ecosystem responses to environmental changes such as water availability. Climate change is predicted to increase aridity and the frequency of extreme drought events in grasslands, but it is unclear how community-scale NSC will respond to drought or how such responses may vary along aridity gradients. We experimentally imposed a 4-year drought in six grasslands along a natural aridity gradient and measured the community-weighted mean of leaf soluble sugar (SSCWM) and total leaf NSC (NSCCWM) concentrations. We observed a bell-shape relationship across this gradient, where SSCWM and total NSCCWM concentrations were lowest at intermediate aridity, with this pattern driven primarily by species turnover. Drought manipulation increased both SSCWM and total NSCCWM concentrations at one moderately arid grassland but decreased total NSCCWM concentrations at one moist site. These differential responses to experimental drought depended on the relative role of species turnover and intraspecific variation in driving shifts in SSCWM and total NSCCWM concentrations. Specifically, the synergistic effects of species turnover and intraspecific variation drove the responses of leaf NSC concentrations to drought, while their opposing effects diminished the effect of drought on plant SSCWM and total NSCCWM concentrations. Plant resource strategies were more acquisitive, via higher chlorophyllCWM concentration, to offset reduced NSCCWM concentrations and net aboveground primary productivity (ANPP) with increasing aridity at more mesic sites, but more conservative (i.e., decreased plant heightCWM and ANPP) to reduce NSC consumption at drier sites. The relationship between water availability and NSCCWM concentrations may contribute to community drought resistance and improve plant viability and adaptation strategies to a changing climate.

Nature-based framework for sustainable afforestation in global drylands under changing climate.

Drylands cover more than 40% of Earth's land surface and occur at the margin of forest distributions due to the limited availability of water for tree growth. Recent elevated temperature and low precipitation have driven greater forest declines and pulses of tree mortality on dryland sites compared to humid sites, particularly in temperate Eurasia and North America. Afforestation of dryland areas has been widely implemented and is expected to increase in many drylands globally to enhance carbon sequestration and benefits to the human environment, but the interplay of sometimes conflicting afforestation outcomes has not been formally evaluated yet. Most previous studies point to conflicts between additional forest area and water consumption, in particular water yield and soil conservation/desalinization in drylands, but were generally confined to local and regional scales. Our global synthesis demonstrates that additional tree cover can amplify water consumption through a nonlinear increase in evapotranspiration-depending on tree species, age, and structure-which will be further intensified by future climate change. In this review we identify substantial knowledge gaps in addressing the dryland afforestation dilemma, where there are trade-offs with planted forests between increased availability of some resources and benefits to human habitats versus the depletion of other resources that are required for sustainable development of drylands. Here we propose a method of addressing comprehensive vegetation carrying capacity, based on regulating the distribution and structure of forest plantations to better deal with these trade-offs in forest multifunctionality. We also recommend new priority research topics for dryland afforestation, including: responses and feedbacks of dryland forests to climate change; shifts in the ratio of ecosystem ET to tree cover; assessing the role of scale of afforestation in influencing the trade-offs of dryland afforestation; and comprehensive modeling of the multifunctionality of dryland forests, including both ecophysiological and socioeconomic aspects, under a changing climate.

Freshwater wetland plants respond nonlinearly to inundation over a sustained period.

PREMISE: Wetland plants regularly experience physiological stresses resulting from inundation; however, plant responses to the interacting effects of water level and inundation duration are not fully understood. METHODS: We conducted a mesocosm experiment on two wetland species, sawgrass (Cladium jamaicense) and muhly grass (Muhlenbergia filipes), that co-dominate many freshwater wetlands in the Florida Everglades. We tracked photosynthesis, respiration, and growth at water levels of -10 (control), 10 (shallow), and 35 cm (deep) with reference to soil surface over 6 months. RESULTS: The response of photosynthesis to inundation was nonlinear. Specifically, photosynthetic capacity (Amax ) declined by 25% in sawgrass and by 70% in muhly grass after 1-2 months of inundation. After 4 months, Amax of muhly grass in the deep-water treatment declined to near zero. Inundated sawgrass maintained similar leaf respiration and growth rates as the control, whereas inundated muhly grass suppressed both respiration and growth. At the end of the experiment, sawgrass had similar nonstructural carbohydrate pools in all treatments. By contrast, muhly grass in the deep-water treatment had largely depleted sugar reserves but maintained a similar starch pool as the control, which is critical for post-stress recovery. CONCLUSIONS: Overall, the two species exhibited nonlinear and contrasting patterns of carbon uptake and use under inundation stress, which ultimately defines their strategies of surviving regularly flooded habitats. The results suggest that a future scenario with more intensive inundation, due to the water management and climate change, may weaken the dominance of muhly grass in many freshwater wetlands of the Everglades.

Storage of carbon reserves in spruce trees is prioritized over growth in the face of carbon limitation.

Climate change is expected to pose a global threat to forest health by intensifying extreme events like drought and insect attacks. Carbon allocation is a fundamental process that determines the adaptive responses of long-lived late-maturing organisms like trees to such stresses. However, our mechanistic understanding of how trees coordinate and set allocation priorities among different sinks (e.g., growth and storage) under severe source limitation remains limited. Using flux measurements, isotopic tracing, targeted metabolomics, and transcriptomics, we investigated how limitation of source supply influences sink activity, particularly growth and carbon storage, and their relative regulation in Norway spruce (Picea abies) clones. During photosynthetic deprivation, absolute rates of respiration, growth, and allocation to storage all decline. When trees approach neutral carbon balance, i.e., daytime net carbon gain equals nighttime carbon loss, genes encoding major enzymes of metabolic pathways remain relatively unaffected. However, under negative carbon balance, photosynthesis and growth are down-regulated while sucrose and starch biosynthesis pathways are up-regulated, indicating that trees prioritize carbon allocation to storage over growth. Moreover, trees under negative carbon balance actively increase the turnover rate of starch, lipids, and amino acids, most likely to support respiration and mitigate stress. Our study provides molecular evidence that trees faced with severe photosynthetic limitation strategically regulate storage allocation and consumption at the expense of growth. Understanding such allocation strategies is crucial for predicting how trees may respond to extreme events involving steep declines in photosynthesis, like severe drought, or defoliation by heat waves, late frost, or insect attack.

Contrasting life-history traits of black spruce and jack pine influence their physiological response to drought and growth recovery in northeastern boreal Canada.

An increase in frequency, intensity and duration of drought events affects forested ecosystems. Trees react to these changes by adjusting stomatal conductance to maximize the trade-off between carbon gains and water losses. A better understanding of the consequences of these drought-induced physiological adjustments for tree growth could help inferring future productivity potentials of boreal forests. Here, we used samples from a forest inventory network in Canada where a decline in growth rates of black spruce (Picea mariana (Mill.) B.S.P.) and jack pine (Pinus banksiana Lamb.) occurred in 1988-1992, an exceptionally dry period, to verify if this growth decline resulted from physiological adjustments of trees to drought. We measured carbon and oxygen isotope ratios in growth rings of 95 spruces and 49 pines spanning 1985-1993. We used 13C discrimination (Δ13C) and 18O enrichment (Δ18O) as proxies for intrinsic water use efficiency and stomatal conductance, respectively. We studied how inter-annual variability in isotopic signals was linked to climate moisture index, vapor pressure deficit and annual snowfall amount. We found significantly lower Δ13C values over 1988-1990, and significantly higher Δ18O values in 1988-1989 and 1991 compared to the 1985-1993 averages. We also observed that a low climatic water balance and a high vapor pressure deficit were linked with low Δ13C and high Δ18O in the two study species, in parallel with low growth rates. The latter effect persisted into the year following drought for black spruce, but not for jack pine. These findings highlight that small differences in physiological parameters between species could translate into large differences in post-drought recovery. The stronger and longer lasting impact on black spruce compared to jack pine suggests a less efficient carbon use and a lower acclimation potential to future warmer and drier climate conditions.

Low-cost chamber design for simultaneous CO2 and O2 flux measurements between tree stems and the atmosphere.

Tree stem CO2 efflux is an important component of ecosystem carbon fluxes and has been the focus of many studies. While CO2 efflux can easily be measured, a growing number of studies have shown that it is not identical with actual in situ respiration. Complementing measurements of CO2 flux with simultaneous measurements of O2 flux provides an additional proxy for respiration, and the combination of both fluxes can potentially help getting closer to actual measures of respiratory fluxes. To date, however, the technical challenge to measure relatively small changes in O2 concentration against its high atmospheric background has prevented routine O2 measurements in field applications. Here, we present a new and low-cost field-tested device for autonomous real-time and quasi-continuous long-term measurements of stem respiration by combining CO2 (NDIR-based) and O2 (quenching-based) sensors in a tree stem chamber. Our device operates as a cyclic-closed system and measures changes in both CO2 and O2 concentration within the chamber over time. The device is battery powered with a >1-week power independence, and data acquisition is conveniently achieved by an internal logger. Results from both field and laboratory tests document that our sensors provide reproducible measurements of CO2 and O2 exchange fluxes under varying environmental conditions.