High exposure of global tree diversity to human pressure.

Safeguarding Earth's tree diversity is a conservation priority due to the importance of trees for biodiversity and ecosystem functions and services such as carbon sequestration. Here, we improve the foundation for effective conservation of global tree diversity by analyzing a recently developed database of tree species covering 46,752 species. We quantify range protection and anthropogenic pressures for each species and develop conservation priorities across taxonomic, phylogenetic, and functional diversity dimensions. We also assess the effectiveness of several influential proposed conservation prioritization frameworks to protect the top 17% and top 50% of tree priority areas. We find that an average of 50.2% of a tree species' range occurs in 110-km grid cells without any protected areas (PAs), with 6,377 small-range tree species fully unprotected, and that 83% of tree species experience nonnegligible human pressure across their range on average. Protecting high-priority areas for the top 17% and 50% priority thresholds would increase the average protected proportion of each tree species' range to 65.5% and 82.6%, respectively, leaving many fewer species (2,151 and 2,010) completely unprotected. The priority areas identified for trees match well to the Global 200 Ecoregions framework, revealing that priority areas for trees would in large part also optimize protection for terrestrial biodiversity overall. Based on range estimates for >46,000 tree species, our findings show that a large proportion of tree species receive limited protection by current PAs and are under substantial human pressure. Improved protection of biodiversity overall would also strongly benefit global tree diversity.

Hotter is not (always) better: Embracing unimodal scaling of biological rates with temperature.

Rate-temperature scaling relationships have fascinated biologists for nearly two centuries and are increasingly important in our era of global climate change. These relationships are hypothesized to originate from the temperature-dependent kinetics of rate-limiting biochemical reactions of metabolism. Several prominent theories have formalized this hypothesis using the Arrhenius model, which characterizes a monotonic temperature dependence using an activation energy E. However, the ubiquitous unimodal nature of biological temperature responses presents important theoretical, methodological, and conceptual challenges that restrict the promise for insight, prediction, and progress. Here we review the development of key hypotheses and methods for the temperature-scaling of biological rates. Using simulations, we examine the constraints of monotonic models, illustrating their sensitivity to data nuances such as temperature range and noise, and their tendency to yield variable and underestimated E, with critical consequences for climate change predictions. We also evaluate the behaviour of two prominent unimodal models when applied to incomplete and noisy datasets. We conclude with recommendations for resolving these challenges in future research, and advocate for a shift to unimodal models that better characterize the full range of biological temperature responses.

Fast Assimilation-Temperature Response: a FAsTeR method for measuring the temperature dependence of leaf-level photosynthesis.

We present the Fast Assimilation-Temperature Response (FAsTeR) method, a new method for measuring plant assimilation-temperature (AT) response that reduces measurement time and increases data density compared with conventional methods. The FAsTeR method subjects plant leaves to a linearly increasing temperature ramp while taking rapid, nonequilibrium measurements of gas exchange variables. Two postprocessing steps are employed to correct measured assimilation rates for nonequilibrium effects and sensor calibration drift. Results obtained with the new method are compared with those from two conventional stepwise methods. Our new method accurately reproduces results obtained from conventional methods, reduces measurement time by a factor of c. 3.3 (from c. 90 to 27 min), and increases data density by a factor of c. 55 (from c. 10 to c. 550 observations). Simulation results demonstrate that increased data density substantially improves confidence in parameter estimates and drastically reduces the influence of noise. By improving measurement speed and data density, the FAsTeR method enables users to ask fundamentally new kinds of ecological and physiological questions, expediting data collection in short-field campaigns, and improving the representativeness of data across species in the literature.

Variation in leaf carbon economics, energy balance, and heat tolerance traits highlights differing timescales of adaptation and acclimation.

Multivariate leaf trait correlations are hypothesized to originate from natural selection on carbon economics traits that control lifetime leaf carbon gain, and energy balance traits governing leaf temperatures, physiological rates, and heat injury. However, it is unclear whether macroevolution of leaf traits primarily reflects selection for lifetime carbon gain or energy balance, and whether photosynthetic heat tolerance is coordinated along these axes. To evaluate these hypotheses, we measured carbon economics, energy balance, and photosynthetic heat tolerance traits for 177 species (157 families) in a common garden that minimizes co-variation of taxa and climate. We observed wide variation in carbon economics, energy balance, and heat tolerance traits. Carbon economics and energy balance (but not heat tolerance) traits were phylogenetically structured, suggesting macroevolution of leaf mass per area and leaf dry matter content reflects selection on carbon gain rather than energy balance. Carbon economics and energy balance traits varied along a common axis orthogonal to heat tolerance traits. Our results highlight a fundamental mismatch in the timescales over which morphological and heat tolerance traits respond to environmental variation. Whereas carbon economics and energy balance traits are constrained by species' evolutionary histories, photosynthetic heat tolerance traits are not and can acclimate readily to leaf microclimates.

Cone allometry and seed protection from fire are similar in serotinous and nonserotinous conifers.

Serotiny is an adaptive trait that allows certain woody plants to persist in stand-replacing fire regimes. However, the mechanisms by which serotinous cones avoid seed necrosis and nonserotinous species persist in landscapes with short fire cycles and serotinous competitors remain poorly understood. To investigate whether ovulate cone traits that enhance seed survival differ between serotinous and nonserotinous species, we examined cone traits in 24 species within Pinaceae and Cupressaceae based on physical measurements and cone heating simulations using a computational fluid dynamics model. Fire-relevant cone traits were largely similar between cone types; those that differed (e.g. density and moisture) conferred little seed survival advantage under simulated fire. The most important traits influencing seed survival were cone size and seed depth within the cone, which was found to be an allometric function of cone mass for both cone types. Thus, nonserotinous cones should not suffer significantly greater seed necrosis than serotinous cones of equal size. Closed nonserotinous cones containing mature seeds may achieve substantial regeneration after fire if they are sufficiently large relative to fire duration and temperature. To our knowledge, this is the most comprehensive study of the effects of fire-relevant cone traits on conifer regeneration supported by physics-based fire simulation.

Dimensions of invasiveness: Links between local abundance, geographic range size, and habitat breadth in Europe's alien and native floras.

Understanding drivers of success for alien species can inform on potential future invasions. Recent conceptual advances highlight that species may achieve invasiveness via performance along at least three distinct dimensions: 1) local abundance, 2) geographic range size, and 3) habitat breadth in naturalized distributions. Associations among these dimensions and the factors that determine success in each have yet to be assessed at large geographic scales. Here, we combine data from over one million vegetation plots covering the extent of Europe and its habitat diversity with databases on species' distributions, traits, and historical origins to provide a comprehensive assessment of invasiveness dimensions for the European alien seed plant flora. Invasiveness dimensions are linked in alien distributions, leading to a continuum from overall poor invaders to super invaders-abundant, widespread aliens that invade diverse habitats. This pattern echoes relationships among analogous dimensions measured for native European species. Success along invasiveness dimensions was associated with details of alien species' introduction histories: earlier introduction dates were positively associated with all three dimensions, and consistent with theory-based expectations, species originating from other continents, particularly acquisitive growth strategists, were among the most successful invaders in Europe. Despite general correlations among invasiveness dimensions, we identified habitats and traits associated with atypical patterns of success in only one or two dimensions-for example, the role of disturbed habitats in facilitating widespread specialists. We conclude that considering invasiveness within a multidimensional framework can provide insights into invasion processes while also informing general understanding of the dynamics of species distributions.

Plant water use theory should incorporate hypotheses about extreme environments, population ecology, and community ecology.

Plant water use theory has largely been developed within a plant-performance paradigm that conceptualizes water use in terms of value for carbon gain and that sits within a neoclassical economic framework. This theory works very well in many contexts but does not consider other values of water to plants that could impact their fitness. Here, we survey a range of alternative hypotheses for drivers of water use and stomatal regulation. These hypotheses are organized around relevance to extreme environments, population ecology, and community ecology. Most of these hypotheses are not yet empirically tested and some are controversial (e.g. requiring more agency and behavior than is commonly believed possible for plants). Some hypotheses, especially those focused around using water to avoid thermal stress, using water to promote reproduction instead of growth, and using water to hoard it, may be useful to incorporate into theory or to implement in Earth System Models.

Integrating plant physiology into simulation of fire behavior and effects.

Wildfires are a global crisis, but current fire models fail to capture vegetation response to changing climate. With drought and elevated temperature increasing the importance of vegetation dynamics to fire behavior, and the advent of next generation models capable of capturing increasingly complex physical processes, we provide a renewed focus on representation of woody vegetation in fire models. Currently, the most advanced representations of fire behavior and biophysical fire effects are found in distinct classes of fine-scale models and do not capture variation in live fuel (i.e. living plant) properties. We demonstrate that plant water and carbon dynamics, which influence combustion and heat transfer into the plant and often dictate plant survival, provide the mechanistic linkage between fire behavior and effects. Our conceptual framework linking remotely sensed estimates of plant water and carbon to fine-scale models of fire behavior and effects could be a critical first step toward improving the fidelity of the coarse scale models that are now relied upon for global fire forecasting. This process-based approach will be essential to capturing the influence of physiological responses to drought and warming on live fuel conditions, strengthening the science needed to guide fire managers in an uncertain future.

Leaves as bottlenecks: The contribution of tree leaves to hydraulic resistance within the soil-plant-atmosphere continuum.

Within vascular plants, the partitioning of hydraulic resistance along the soil-to-leaf continuum affects transpiration and its response to environmental conditions. In trees, the fractional contribution of leaf hydraulic resistance (Rleaf ) to total soil-to-leaf hydraulic resistance (Rtotal ), or fRleaf (=Rleaf /Rtotal ), is thought to be large, but this has not been tested comprehensively. We compiled a multibiome data set of fRleaf using new and previously published measurements of pressure differences within trees in situ. Across 80 samples, fRleaf averaged 0.51 (95% confidence interval [CI] = 0.46-0.57) and it declined with tree height. We also used the allometric relationship between field-based measurements of soil-to-leaf hydraulic conductance and laboratory-based measurements of leaf hydraulic conductance to compute the average fRleaf for 19 tree samples, which was 0.40 (95% CI = 0.29-0.56). The in situ technique produces a more accurate descriptor of fRleaf because it accounts for dynamic leaf hydraulic conductance. Both approaches demonstrate the outsized role of leaves in controlling tree hydrodynamics. A larger fRleaf may help stems from loss of hydraulic conductance. Thus, the decline in fRleaf with tree height would contribute to greater drought vulnerability in taller trees and potentially to their observed disproportionate drought mortality.

Trait phenology and fire seasonality co-drive seasonal variation in fire effects on tree crowns.

The plume of hot gases rising above a wildfire can heat and kill the buds in tree crowns. This can reduce leaf area and rates of photosynthesis, growth, and reproduction, and may ultimately lead to mortality. These effects vary seasonally, but the mechanisms governing this seasonality are not well understood. A trait-based physical model combining buoyant plume and energy budget theories shows the seasonality of bud necrosis height may originate from temporal variation in climate, fire behaviour, and/or bud functional traits. To assess the relative importance of these drivers, we parameterized the model with time-series data for air temperature, fireline intensity, and bud traits from Pinus contorta, Picea glauca, and Populus tremuloides. Air temperature, fireline intensity, and bud traits all varied significantly through time, causing significant seasonal variation in predicted necrosis height. Bud traits and fireline intensity explained almost all the variation in necrosis height, with air temperature explaining relatively minor amounts of variation. The seasonality of fire effects on tree crowns appears to originate from seasonal variation in functional traits and fire behaviour. Our approach and results provide needed insight into the physical mechanisms linking environmental variation to plant performance via functional traits.

Gas exchange analysers exhibit large measurement error driven by internal thermal gradients.

Portable gas exchange analysers provide critical data for understanding plant-atmosphere carbon and water fluxes, and for parameterising Earth system models that forecast climate change effects and feedbacks. We characterised temperature measurement errors in the Li-Cor LI-6400XT and LI-6800, and estimated downstream errors in derived quantities, including stomatal conductance (gsw ) and leaf intercellular CO2 concentration (Ci ). The LI-6400XT exhibited air temperature errors (differences between reported air temperature and air temperature measured near the leaf) up to 7.2°C, leaf temperature errors up to 5.3°C, and relative errors in gsw and Ci that increased as temperatures departed from ambient. This caused errors in leaf-to-air temperature relationships, assimilation-temperature curves and CO2 response curves. Temperature dependencies of maximum Rubisco carboxylation rate (Vcmax ) and maximum RuBP regeneration rate (Jmax ) showed errors of 12% and 35%, respectively. These errors are likely to be idiosyncratic and may differ among machines and environmental conditions. The LI-6800 exhibited much smaller errors. Earth system model predictions may be erroneous, as much of their parametrisation data were measured on the LI-6400XT system, depending on the methods used. We make recommendations for minimising errors and correcting data in the LI-6400XT. We also recommend transitioning to the LI-6800 for future data collection.

The acquisitive-conservative axis of leaf trait variation emerges even in homogeneous environments.

BACKGROUND AND AIMS: The acquisitive-conservative axis of plant ecological strategies results in a pattern of leaf trait covariation that captures the balance between leaf construction costs and plant growth potential. Studies evaluating trait covariation within species are scarcer, and have mostly dealt with variation in response to environmental gradients. Little work has been published on intraspecific patterns of leaf trait covariation in the absence of strong environmental variation. METHODS: We analysed covariation of four leaf functional traits [specific leaf area (SLA) leaf dry matter content (LDMC), force to tear (Ft) and leaf nitrogen content (Nm)] in six Poaceae and four Fabaceae species common in the dry Chaco forest of Central Argentina, growing in the field and in a common garden. We compared intraspecific covariation patterns (slopes, correlation and effect size) of leaf functional traits with global interspecific covariation patterns. Additionally, we checked for possible climatic and edaphic factors that could affect the intraspecific covariation pattern. KEY RESULTS: We found negative correlations for the LDMC-SLA, Ft-SLA, LDMC-Nm and Ft-Nm trait pairs. This intraspecific covariation pattern found both in the field and in the common garden and not explained by climatic or edaphic variation in the field follows the expected acquisitive-conservative axis. At the same time, we found quantitative differences in slopes among different species, and between these intraspecific patterns and the interspecific ones. Many of these differences seem to be idiosyncratic, but some appear consistent among species (e.g. all the intraspecific LDMC-SLA and LDMC-Nm slopes tend to be shallower than the global pattern). CONCLUSIONS: Our study indicates that the acquisitive-conservative leaf functional trait covariation pattern occurs at the intraspecific level even in the absence of relevant environmental variation in the field. This suggests a high degree of variation-covariation in leaf functional traits not driven by environmental variables.

Climate shapes and shifts functional biodiversity in forests worldwide.

Much ecological research aims to explain how climate impacts biodiversity and ecosystem-level processes through functional traits that link environment with individual performance. However, the specific climatic drivers of functional diversity across space and time remain unclear due largely to limitations in the availability of paired trait and climate data. We compile and analyze a global forest dataset using a method based on abundance-weighted trait moments to assess how climate influences the shapes of whole-community trait distributions. Our approach combines abundance-weighted metrics with diverse climate factors to produce a comprehensive catalog of trait-climate relationships that differ dramatically-27% of significant results change in sign and 71% disagree on sign, significance, or both-from traditional species-weighted methods. We find that (i) functional diversity generally declines with increasing latitude and elevation, (ii) temperature variability and vapor pressure are the strongest drivers of geographic shifts in functional composition and ecological strategies, and (iii) functional composition may currently be shifting over time due to rapid climate warming. Our analysis demonstrates that climate strongly governs functional diversity and provides essential information needed to predict how biodiversity and ecosystem function will respond to climate change.

Leaf heat tolerance of 147 tropical forest species varies with elevation and leaf functional traits, but not with phylogeny.

Exceeding thermal thresholds causes irreversible damage and ultimately loss of leaves. The lowland tropics are among the warmest forested biomes, but little is known about heat tolerance of tropical forest plants. We surveyed leaf heat tolerance of sun-exposed leaves from 147 tropical lowland and pre-montane forest species by determining the temperatures at which potential photosystem II efficiency based on chlorophyll a fluorescence started to decrease (TCrit ) and had decreased by 50% (T50 ). TCrit averaged 46.7°C (5th-95th percentile: 43.5°C-49.7°C) and T50 averaged 49.9°C (47.8°C-52.5°C). Heat tolerance partially adjusted to site temperature; TCrit and T50 decreased with elevation by 0.40°C and 0.26°C per 100 m, respectively, while mean annual temperature decreased by 0.63°C per 100 m. The phylogenetic signal in heat tolerance was weak, suggesting that heat tolerance is more strongly controlled by environment than by evolutionary legacies. TCrit increased with the estimated thermal time constant of the leaves, indicating that species with thermally buffered leaves maintain higher heat tolerance. Among lowland species, T50 increased with leaf mass per area, suggesting that in species with structurally more costly leaves the risk of leaf loss during hot spells is reduced. These results provide insight in variation in heat tolerance at local and regional scales.

Traits mediate drought effects on wood carbon fluxes.

CO2 fluxes from wood decomposition represent an important source of carbon from forest ecosystems to the atmosphere, which are determined by both wood traits and climate influencing the metabolic rates of decomposers. Previous studies have quantified the effects of moisture and temperature on wood decomposition, but these effects were not separated from the potential influence of wood traits. Indeed, it is not well understood how traits and climate interact to influence wood CO2 fluxes. Here, we examined the responses of CO2 fluxes from dead wood with different traits (angiosperm and gymnosperm) to 0%, 35%, and 70% rainfall reduction across seasonal temperature gradients. Our results showed that drought significantly decreased wood CO2 fluxes, but its effects varied with both taxonomical group and drought intensity. Drought-induced reduction in wood CO2 fluxes was larger in angiosperms than gymnosperms for the 35% rainfall reduction treatment, but there was no significant difference between these groups for the 70% reduction treatment. This is because wood nitrogen density and carbon quality were significantly higher in angiosperms than gymnosperms, yielding a higher moisture sensitivity of wood decomposition. These findings were demonstrated by a significant positive interaction effect between wood nitrogen and moisture on CO2 fluxes in a structural equation model. Additionally, we ascertained that a constant temperature sensitivity of CO2 fluxes was independent of wood traits and consistent with previous estimates for extracellular enzyme kinetics. Our results highlight the key role of wood traits in regulating drought responses of wood carbon fluxes. Given that both climate and forest management might extensively modify taxonomic compositions in the future, it is critical for carbon cycle models to account for such interactions between wood traits and climate in driving dynamics of wood decomposition.

The response of stomatal conductance to seasonal drought in tropical forests.

Stomata regulate CO2 uptake for photosynthesis and water loss through transpiration. The approaches used to represent stomatal conductance (gs ) in models vary. In particular, current understanding of drivers of the variation in a key parameter in those models, the slope parameter (i.e. a measure of intrinsic plant water-use-efficiency), is still limited, particularly in the tropics. Here we collected diurnal measurements of leaf gas exchange and leaf water potential (Ψleaf ), and a suite of plant traits from the upper canopy of 15 tropical trees in two contrasting Panamanian forests throughout the dry season of the 2016 El Niño. The plant traits included wood density, leaf-mass-per-area (LMA), leaf carboxylation capacity (Vc,max ), leaf water content, the degree of isohydry, and predawn Ψleaf . We first investigated how the choice of four commonly used leaf-level gs models with and without the inclusion of Ψleaf as an additional predictor variable influence the ability to predict gs , and then explored the abiotic (i.e. month, site-month interaction) and biotic (i.e. tree-species-specific characteristics) drivers of slope parameter variation. Our results show that the inclusion of Ψleaf did not improve model performance and that the models that represent the response of gs to vapor pressure deficit performed better than corresponding models that respond to relative humidity. Within each gs model, we found large variation in the slope parameter, and this variation was attributable to the biotic driver, rather than abiotic drivers. We further investigated potential relationships between the slope parameter and the six available plant traits mentioned above, and found that only one trait, LMA, had a significant correlation with the slope parameter (R2  = 0.66, n = 15), highlighting a potential path towards improved model parameterization. This study advances understanding of gs dynamics over seasonal drought, and identifies a practical, trait-based approach to improve modeling of carbon and water exchange in tropical forests.

Convergence of terrestrial plant production across global climate gradients.

Variation in terrestrial net primary production (NPP) with climate is thought to originate from a direct influence of temperature and precipitation on plant metabolism. However, variation in NPP may also result from an indirect influence of climate by means of plant age, stand biomass, growing season length and local adaptation. To identify the relative importance of direct and indirect climate effects, we extend metabolic scaling theory to link hypothesized climate influences with NPP, and assess hypothesized relationships using a global compilation of ecosystem woody plant biomass and production data. Notably, age and biomass explained most of the variation in production whereas temperature and precipitation explained almost none, suggesting that climate indirectly (not directly) influences production. Furthermore, our theory shows that variation in NPP is characterized by a common scaling relationship, suggesting that global change models can incorporate the mechanisms governing this relationship to improve predictions of future ecosystem function.

Fire effects on tree physiology.

Heat injuries sustained in a fire can initiate a cascade of complex mechanisms that affect the physiology of trees after fires. Uncovering the exact physiological mechanisms and relating specific injuries to whole-plant and ecosystem functioning is the focus of intense current research. Recent studies have made critical steps forward in our understanding of tree physiological processes after fires, and have suggested mechanisms by which fire injuries may interact with disturbances such as drought, insects and pathogens. We outline a conceptual framework that unifies the involved processes, their interconnections, and possible feedbacks, and contextualizes these responses with existing hypotheses for disturbance effects on plants and ecosystems. By focusing on carbon and water as currencies of plant functioning, we demonstrate fire-induced cambium/phloem necrosis and xylem damage to be main disturbance effects. The resulting carbon starvation and hydraulic dysfunction are linked with drought and insect impacts. Evaluating the precise process relationships will be crucial for fully understanding how fires can affect tree functionality, and will help improve fire risk assessment and mortality model predictions. Especially considering future climate-driven increases in fire frequency and intensity, knowledge of the physiological tree responses is important to better estimate postfire ecosystem dynamics and interactions with climate disturbances.

Homoeostatic maintenance of nonstructural carbohydrates during the 2015-2016 El Niño drought across a tropical forest precipitation gradient.

Nonstructural carbohydrates (NSCs) are essential for maintenance of plant metabolism and may be sensitive to short- and long-term climatic variation. NSC variation in moist tropical forests has rarely been studied, so regulation of NSCs in these systems is poorly understood. We measured foliar and branch NSC content in 23 tree species at three sites located across a large precipitation gradient in Panama during the 2015-2016 El Niño to examine how short- and long-term climatic variation impact carbohydrate dynamics. There was no significant difference in total NSCs as the drought progressed (leaf P = 0.32, branch P = 0.30) nor across the rainfall gradient (leaf P = 0.91, branch P = 0.96). Foliar soluble sugars decreased while starch increased over the duration of the dry period, suggesting greater partitioning of NSCs to storage than metabolism or transport as drought progressed. There was a large variation across species at all sites, but total foliar NSCs were positively correlated with leaf mass per area, whereas branch sugars were positively related to leaf temperature and negatively correlated with daily photosynthesis and wood density. The NSC homoeostasis across a wide range of conditions suggests that NSCs are an allocation priority in moist tropical forests.