Cameron D. McIntire

Beech leaf disease (BLD) is a foliar disease of American beech ( Fagus grandifolia ) that manifests as gall symptoms in leaves caused by infestations from Litylenchus crenatae ssp. mccannii, a plant‐parasitic nematode. As the disease progresses, infestations lead to bud abortion, crown deterioration and branch dieback. While BLD is known to impair leaf function, the impacts of the disease on tree carbon allocation and growth are unresolved. Here, we sampled three forest stands across a gradient of disease severity to assess how BLD influences the storage of non‐structural carbohydrates (NSC) across different tissue pools (root, bole and twigs), used tree rings to estimate growth declines associated with the onset of BLD infestation and evaluated the fine root ectomycorrhizal communities. Our data show that BLD can negatively impact NSC storage across tissue pools in stands exhibiting both low‐ and high‐severity infestation. Diminished starch content with respect to the asymptomatic stand was shown to precede any reduction in growth, measured via post‐infestation basal area increment at the low‐severity stand (1–2 years of infestation). Growth reductions at the high‐severity stand (3+ years post infestation) were significant and coincided with low NSC content, though mortality was not observed among any mature trees. Root‐associated fungal community composition differed significantly among sites, with a trend towards reduced diversity in more severely impacted trees. Our results suggest that BLD disrupts carbon allocation and storage in beech trees, potentially compromising their resilience to future stressors. The complex interplay between nematode infestation, fungal community shifts and altered carbohydrate dynamics highlights the multifaceted nature of BLD and its potential long‐term consequences for beech forests.

Constrained carbon allocation toward secondary metabolites involved in chemical defense is a common explanation for widespread drought-related beetle-kill in conifers—we challenge the generality of this explanation. While monitoring drought stress (ψpd), we tracked both carbon reserves (non-structural carbohydrates) and chemical defenses (terpenes, phenolics, resin flow) in mature Pinus edulis Englem. trees experiencing either short-term (3-year) or a ‘legacy’ long-term (13-year) throughfall exclusion treatments, plus a control. We also quantified the Δ14C-age of resin to measure past allocation to current defense. While 72% of trees in short-term throughfall exclusion plots died (attacked by bark beetles, Ips confusus LeConte), mortality patterns were unrelated to throughfall exclusion intensity and all ‘legacy’ trees survived. We thus assessed trees in four survivorship categories: control, ‘legacy’, surviving, and dying trees. We found concentrations of certain defense compounds (leaf phenolics, twig monoterpenes) increased with drought stress, particularly in dying trees. In the main stem, dying trees exhibited similar terpene concentrations (94%) and phenolic concentrations (139%) relative to control trees. Compared with control trees, only ‘legacy’ trees had reduced stem terpenes (−49%, P < 0.05) after a decade of drought. Δ14C-age of resin could be up to 10.2 ± 0.5 years old, where the oldest resin was exuded from trees with low sugar concentrations and more negative Ψpd. Our results suggest that drought imposes a weak constraint on carbon allocation to resin-based defense. Instead, we primarily found evidence of increased concentrations of terpene and phenolic compounds under drought, even in dying trees, and only observed reductions in resin-based defenses after 10+ years of drought. Δ14C-ages demonstrate limited resin turnover and/or synthesis of resin from old reserves, suggesting that long-term drought is required to reduce resin-based defenses. Persistent allocation coupled with past investments appears to preserve or enhance concentrations of resin-based defenses even under lethal drought stress in P. edulis.

As droughts become longer and more intense, impacts on terrestrial primary productivity are expected to increase progressively. Yet, some ecosystems appear to acclimate to multiyear drought, with constant or diminishing reductions in productivity as drought duration increases. We quantified the combined effects of drought duration and intensity on aboveground productivity in 74 grasslands and shrublands distributed globally. Ecosystem acclimation with multiyear drought was observed overall, except when droughts were extreme (i.e., ≤1-in-100-year likelihood of occurrence). Productivity losses after four consecutive years of extreme drought increased by ~2.5-fold compared with those of the first year. These results portend a foundational shift in ecosystem behavior if drought duration and intensity increase, from maintenance of reduced functioning over time to progressive and profound losses of productivity when droughts are extreme.

Beech leaf disease (BLD) is an emerging threat to American beech (Fagus grandifolia Ehrh.) throughout North American forests attributable to the plant‐parasitic nematode Litylenchus crenatae ssp. mccannii (Lcm). This study describes the impacts of BLD on bud retention and subsequent leaf production, associated symptoms, and the abundance of Lcm throughout the course of a single growing season within two natural forest stands exposed to different levels of disease pressure. We found that trees with 2+ years of BLD infection exhibited reductions in bud retention that represented 52.3% fewer buds per branch (m⁻¹) relative to a control stand that did not exhibit BLD symptoms in the previous year. Diseased trees also produced less foliage following spring bud break, corresponding to 67.8% fewer leaves per branch (m⁻¹). Bud death among diseased trees resulted in a decoupling from the expected foliage production derived from winter bud inventories. Through the characterization of BLD symptom expression among emerging leaves, including the presence of second flush leaves, we measured casting of severely symptomatic leaves coordinated with a marked increase in second flush leaves in the late summer. Nematodes counted within infected trees ranged from 83 to 9800 individuals per bud, while the proportion of live motile stages, eggs, and dead Lcm varied significantly between the spring and late‐summer sampling periods. Together, our data provide important insights regarding the impact of a multi‐year BLD infection on bud and foliage production, which has the potential to adversely affect tree carbon assimilation and long‐term survival.

Summary: Stomatal closure during drought inhibits carbon uptake and may reduce a tree's defensive capacity. Limited carbon availability during drought may increase a tree's mortality risk, particularly if drought constrains trees' capacity to rapidly produce defenses during biotic attack. We parameterized a new model of conifer defense using physiological data on carbon reserves and chemical defenses before and after a simulated bark beetle attack in mature Pinus edulis under experimental drought. Attack was simulated using inoculations with a consistent bluestain fungus (Ophiostoma sp.) of Ips confusus, the main bark beetle colonizing this tree, to induce a defensive response. Trees with more carbon reserves produced more defenses but measured phloem carbon reserves only accounted for c. 23% of the induced defensive response. Our model predicted universal mortality if local reserves alone supported defense production, suggesting substantial remobilization and transport of stored resin or carbon reserves to the inoculation site. Our results show that de novo terpene synthesis represents only a fraction of the total measured phloem terpenes in P. edulis following fungal inoculation. Without direct attribution of phloem terpene concentrations to available carbon, many studies may be overestimating the scale and importance of de novo terpene synthesis in a tree's induced defense response.

Summary: Shifts in the age or turnover time of non‐structural carbohydrates (NSC) may underlie changes in tree growth under long‐term increases in drought stress associated with climate change. But NSC responses to drought are challenging to quantify, due in part to large NSC stores in trees and subsequently long response times of NSC to climate variation. We measured NSC age (Δ¹⁴C) along with a suite of ecophysiological metrics in Pinus edulis trees experiencing either extreme short‐term drought (−90% ambient precipitation plot, 2020–2021) or a decade of severe drought (−45% plot, 2010–2021). We tested the hypothesis that carbon starvation – consumption exceeding synthesis and storage – increases the age of sapwood NSC. One year of extreme drought had no impact on NSC pool size or age, despite significant reductions in predawn water potential, photosynthetic rates/capacity, and twig and needle growth. By contrast, long‐term drought halved the age of the sapwood NSC pool, coupled with reductions in sapwood starch concentrations (−75%), basal area increment (−39%), and bole respiration rates (−28%). Our results suggest carbon starvation takes time, as tree carbon reserves appear resilient to extreme disturbance in the short term. However, after a decade of drought, trees apparently consumed old stored NSC to support metabolism.

Beech leaf disease (BLD) damage is associated with the parasitic nematode Litylenchus crenatae ssp. mccannii. Foliar symptoms manifest as darkened or chlorotic galls in the interveinal portions in the leaf, which become leathery and crinkled under high severity of infection. Though nearly a decade has passed since the discovery of this disease, little is known regarding the impact of BLD on leaf function and physiology. This study assesses the variation in leaf gas exchange and physiological leaf traits among asymptomatic and BLD-infected leaves across a gradient of symptom severity within a natural forested stand in central Connecticut, USA. Leaves with BLD symptoms are found to have significantly reduced carbon assimilation and instantaneous water use efficiency, with increased levels of stomatal conductance as symptom severity progresses. Leaf response to light manipulation is also affected, with an increase in dark respiration and the light compensation point among banded and crinkled leaves. Additionally, BLD symptoms are found to have a significant influence on leaf water content, specific leaf area, and leaf nitrogen content. Relationships between gas exchange and these leaf traits yield linear correlations that are used to infer functional relationships impacted by the disease.

Pinus edulis Engelm. is a short-stature, drought-tolerant tree species that is abundant in piñon-juniper woodlands throughout semiarid ecosystems of the American Southwest. P. edulis is a model species among ecophysiological disciplines, with considerable research focus given to hydraulic functioning and carbon partitioning relating to mechanisms of tree mortality. Many ecological studies require robust estimates of tree structural traits such as biomass, active sapwood area, and leaf area. We harvested twenty trees from Central New Mexico ranging in size from 1.3 to 22.7 cm root crown diameter (RCD) to derive allometric relationships from measurements of RCD, maximum height, canopy area (CA), aboveground biomass (AGB), sapwood area (A_S), and leaf area (A_L). Total foliar mass was measured from a subset of individuals and scaled to A_L from estimates of leaf mass per area. We report a strong nonlinear relationship to AGB as a function of both RCD and height, whereas CA scaled linearly. Total A_S expressed a power relationship with RCD. Both A_S and CA exhibited strong linear relationships with A_L (R² = 0.99), whereas RCD increased nonlinearly with A_L. We improve on current models by expanding the size range of sampled trees and supplement the existing literature for this species. Study Implications: Land managers need to better understand carbon and water dynamics in changing ecosystems to understand how those ecosystems can be sustainably used now and in the future. This study of two-needle pinon (Pinus edulis Engelm.) trees in New Mexico, USA, uses observations from unoccupied aerial vehicles, field measurements, and harvesting followed by laboratory analysis to develop allometric models for this widespread species. These models can be used to understand plant traits such biomass partitioning and sap flow, which in turn will help scientists and land managers better understand the ecosystem services provided by pinon pine across North America.

Non‐forest ecosystems, dominated by shrubs, grasses and herbaceous plants, provide ecosystem services including carbon sequestration and forage for grazing, and are highly sensitive to climatic changes. Yet these ecosystems are poorly represented in remotely sensed biomass products and are undersampled by in situ monitoring. Current global change threats emphasize the need for new tools to capture biomass change in non‐forest ecosystems at appropriate scales. Here we developed and deployed a new protocol for photogrammetric height using unoccupied aerial vehicle (UAV) images to test its capability for delivering standardized measurements of biomass across a globally distributed field experiment. We assessed whether canopy height inferred from UAV photogrammetry allows the prediction of aboveground biomass (AGB) across low‐stature plant species by conducting 38 photogrammetric surveys over 741 harvested plots to sample 50 species. We found mean canopy height was strongly predictive of AGB across species, with a median adjusted R² of 0.87 (ranging from 0.46 to 0.99) and median prediction error from leave‐one‐out cross‐validation of 3.9%. Biomass per‐unit‐of‐height was similar within but different among, plant functional types. We found that photogrammetric reconstructions of canopy height were sensitive to wind speed but not sun elevation during surveys. We demonstrated that our photogrammetric approach produced generalizable measurements across growth forms and environmental settings and yielded accuracies as good as those obtained from in situ approaches. We demonstrate that using a standardized approach for UAV photogrammetry can deliver accurate AGB estimates across a wide range of dynamic and heterogeneous ecosystems. Many academic and land management institutions have the technical capacity to deploy these approaches over extents of 1–10 ha⁻¹. Photogrammetric approaches could provide much‐needed information required to calibrate and validate the vegetation models and satellite‐derived biomass products that are essential to understand vulnerable and understudied non‐forested ecosystems around the globe.