Linking physiology, epidemiology, and demography: Understanding how lianas outcompete trees in a changing world.

Extending and safeguarding tropical forest ecosystems is critical for combating climate change and biodiversity loss. One of its constituents, lianas, is spreading and increasing in abundance on a global scale. This is particularly concerning as lianas negatively impact forests' carbon fluxes, dynamics, and overall resilience, potentially exacerbating both crises. While possibly linked to climate-change-induced atmospheric CO2 elevation and drought intensification, the reasons behind their increasing abundance remain elusive. Prior research shows distinct physiological differences between lianas and trees, but it is unclear whether these differences confer a demographic advantage to lianas with climate change. Guided by extensive datasets collected in Panamanian tropical forests, we developed a tractable model integrating physiology, demography, and epidemiology. Our findings suggest that CO2 fertilization, a climate change factor promoting forest productivity, gives lianas a demographic advantage. Conversely, factors such as extreme drought generally cause a decrease in liana prevalence. Such a decline in liana prevalence is expected from a physiological point of view because lianas have drought-sensitive traits. However, our analysis underscores the importance of not exclusively relying on physiological processes, as interactions with demographic mechanisms (i.e., the forest structure) can contrast these expectations, causing an increase in lianas with drought. Similarly, our results emphasize that identical physiological responses between lianas and trees still lead to liana increase. Even if lianas exhibit collinear but weaker responses in their performance compared to trees, a temporary liana prevalence increase might manifest driven by the faster response time of lianas imposed by their distinct life-history strategies than trees.

Abrupt loss and uncertain recovery from fires of Amazon forests under low climate mitigation scenarios.

Tropical forests contribute a major sink for anthropogenic carbon emissions essential to slowing down the buildup of atmospheric CO2 and buffering climate change impacts. However, the response of tropical forests to more frequent weather extremes and long-recovery disturbances like fires remains uncertain. Analyses of field data and ecological theory raise concerns about the possibility of the Amazon crossing a tipping point leading to catastrophic tropical forest loss. In contrast, climate models consistently project an enhanced tropical sink. Here, we show a heterogeneous response of Amazonian carbon stocks in GFDL-ESM4.1, an Earth System Model (ESM) featuring dynamic disturbances and height-structured tree-grass competition. Enhanced productivity due to CO2 fertilization promotes increases in forest biomass that, under low emission scenarios, last until the end of the century. Under high emissions, positive trends reverse after 2060, when simulated fires prompt forest loss that results in a 40% decline in tropical forest biomass by 2100. Projected fires occur under dry conditions associated with El Niño Southern Oscillation and the Atlantic Multidecadal Oscillation, a response observed under current climate conditions, but exacerbated by an overall decline in precipitation. Following the initial disturbance, grassland dominance promotes recurrent fires and tree competitive exclusion, which prevents forest recovery. EC-Earth3-Veg, an ESM with a dynamic vegetation model of similar complexity, projected comparable wildfire forest loss under high emissions but faster postfire recovery rates. Our results reveal the importance of complex nonlinear responses to assessing climate change impacts and the urgent need to research postfire recovery and its representation in ESMs.

Competition for time: Evidence for an overlooked, diversity-maintaining competitive mechanism.

Understanding how diversity is maintained in plant communities requires that we first understand the mechanisms of competition for limiting resources. In ecology, there is an underappreciated but fundamental distinction between systems in which the depletion of limiting resources reduces the growth rates of competitors and systems in which resource depletion reduces the time available for competitors to grow, a mechanism we call 'competition for time'. Importantly, modern community ecology and our framing of the coexistence problem are built on the implicit assumption that competition reduces the growth rate. However, recent theoretical work suggests competition for time may be the predominant competitive mechanism in a broad array of natural communities, a significant advance given that when species compete for time, diversity-maintaining trade-offs emerge organically. In this study, we first introduce competition for time conceptually using a simple model of interacting species. Then, we perform an experiment in a Mediterranean annual grassland to determine whether competition for time is an important competitive mechanism in a field system. Indeed, we find that species respond to increased competition through reductions in their lifespan rather than their rate of growth. In total, our study suggests competition for time may be overlooked as a mechanism of biodiversity maintenance.

Hydraulic diversity of forests regulates ecosystem resilience during drought.

Plants influence the atmosphere through fluxes of carbon, water and energy1, and can intensify drought through land-atmosphere feedback effects2-4. The diversity of plant functional traits in forests, especially physiological traits related to water (hydraulic) transport, may have a critical role in land-atmosphere feedback, particularly during drought. Here we combine 352 site-years of eddy covariance measurements from 40 forest sites, remote-sensing observations of plant water content and plant functional-trait data to test whether the diversity in plant traits affects the response of the ecosystem to drought. We find evidence that higher hydraulic diversity buffers variation in ecosystem flux during dry periods across temperate and boreal forests. Hydraulic traits were the predominant significant predictors of cross-site patterns in drought response. By contrast, standard leaf and wood traits, such as specific leaf area and wood density, had little explanatory power. Our results demonstrate that diversity in the hydraulic traits of trees mediates ecosystem resilience to drought and is likely to have an important role in future ecosystem-atmosphere feedback effects in a changing climate.

Detecting and interpreting higher-order interactions in ecological communities.

When species simultaneously compete with two or more species of competitor, higher-order interactions (HOIs) can lead to emergent properties not present when species interact in isolated pairs. To extend ecological theory to multi-competitor communities, ecologists must confront the challenges of measuring and interpreting HOIs in models of competition fit to data from nature. Such efforts are hindered by the fact that different studies use different definitions, and these definitions have unclear relationships to one another. Here, we propose a distinction between 'soft' HOIs, which identify possible interaction modification by competitors, and 'hard' HOIs, which identify interactions uniquely emerging in systems with three or more competitors. We show how these two classes of HOI differ in their motivation and interpretation, as well as the tests one uses to identify them in models fit to data. We then show how to operationalise this structure of definitions by analysing the results of a simulated competition experiment underlain by a consumer resource model. In the course of doing so, we clarify the challenges of interpreting HOIs in nature, and suggest a more precise framing of this research endeavour to catalyse further investigations.

Competition for water and species coexistence in phenologically structured annual plant communities.

Both competition for water and phenological variation are important determinants of plant community structure, but ecologists lack a synthetic theory for how they affect coexistence outcomes. We developed an analytically tractable model of water competition for Mediterranean annual communities and demonstrated that variation in phenology alone can maintain high diversity in spatially homogenous assemblages of water-limited plants. We modelled a system where all water arrives early in the season and species vary in their ability to grow under drying conditions. As a consequence, species differ in growing season length and compete by shortening the growing season of their competitors. This model replicates and offers mechanistic explanations for patterns observed in empirical studies of how phenology influences coexistence among Mediterranean annuals. Additionally, we found that a decreasing, concave-up trade-off between growth rate and access to water can maintain high diversity under simple but realistic assumptions. High diversity is possible because: (1) later plants escape competition after their earlier season competitors have gone to seed and (2) early-season species are more than compensated for their shortened growing season by a growth rate advantage. Together, these mechanisms provide an explanation for how phenologically variable annual plant species might coexist when competing only for water.

Plant hydraulics, stomatal control, and the response of a tropical forest to water stress over multiple temporal scales.

Many tropical regions are experiencing an intensification of drought, with increasing severity and frequency. The ecosystem response to these changes is still highly uncertain. On short time scales (from diurnal to seasonal), tropical forests respond to water stress by physiological controls, such as stomatal regulation and phenological adjustment, to cope with increasing atmospheric water demand and reduced water supply. However, the interactions among biological processes and co-varying environmental factors that determine the ecosystem-level fluxes are still unclear. Furthermore, climate variability at longer time scales, such as that generated by ENSO, produces less predictable effects because it depends on a highly stochastic combination of factors that might vary among forests and even between events in the same forest. This study will present some emerging patterns of response to water stress from 5 years of water, carbon, and energy fluxes observed on a seasonal tropical forest in central Panama, including an increase in productivity during the 2015 El Niño. These responses depend on the combination of environmental factors experienced by the forest throughout the seasonal cycle, in particular, increase in solar radiation, stimulating productivity, and increasing vapor pressure deficit (VPD) and decreasing soil moisture, limiting stomata opening. These results suggest a critical role of plant hydraulics in mediating the response to water stress over a broad range of temporal scales (diurnal, intraseasonal, seasonal, and interannual), by acclimating canopy conductance to light and VPD during different soil moisture regimes. A multilayer photosynthesis model coupled with a plant hydraulics scheme can reproduce these complex responses. However, results depend critically on parameters regulating water transport efficiency and the cost of water stress. As these costs have not been properly identified and quantified yet, more empirical research is needed to elucidate physiological mechanisms of hydraulic failure and recover, for example embolism repair and xylem regrowth.

Unusual characteristics of the carbon cycle during the 2015-2016 El Niño.

The 2015-2016 El Niño was one of the strongest on record, but its influence on the carbon balance is less clear. Using Northern Hemisphere atmospheric CO2 observations, we found both detrended atmospheric CO2 growth rate (CGR) and CO2 seasonal-cycle amplitude (SCA) of 2015-2016 were much higher than that of other El Niño events. The simultaneous high CGR and SCA were unusual, because our analysis of long-term CO2 observations at Mauna Loa revealed a significantly negative correlation between CGR and SCA. Atmospheric inversions and terrestrial ecosystem models indicate strong northern land carbon uptake during spring but substantially reduced carbon uptake (or high emissions) during early autumn, which amplified SCA but also resulted in a small anomaly in annual carbon uptake of northern ecosystems in 2015-2016. This negative ecosystem carbon uptake anomaly in early autumn was primarily due to soil water deficits and more litter decomposition caused by enhanced spring productivity. Our study demonstrates a decoupling between seasonality and annual carbon cycle balance in northern ecosystems over 2015-2016, which is unprecedented in the past five decades of El Niño events.

Divergent drivers of leaf trait variation within species, among species, and among functional groups.

Understanding variation in leaf functional traits-including rates of photosynthesis and respiration and concentrations of nitrogen and phosphorus-is a fundamental challenge in plant ecophysiology. When expressed per unit leaf area, these traits typically increase with leaf mass per area (LMA) within species but are roughly independent of LMA across the global flora. LMA is determined by mass components with different biological functions, including photosynthetic mass that largely determines metabolic rates and contains most nitrogen and phosphorus, and structural mass that affects toughness and leaf lifespan (LL). A possible explanation for the contrasting trait relationships is that most LMA variation within species is associated with variation in photosynthetic mass, whereas most LMA variation across the global flora is associated with variation in structural mass. This hypothesis leads to the predictions that (i) gas exchange rates and nutrient concentrations per unit leaf area should increase strongly with LMA across species assemblages with low LL variance but should increase weakly with LMA across species assemblages with high LL variance and that (ii) controlling for LL variation should increase the strength of the above LMA relationships. We present analyses of intra- and interspecific trait variation from three tropical forest sites and interspecific analyses within functional groups in a global dataset that are consistent with the above predictions. Our analysis suggests that the qualitatively different trait relationships exhibited by different leaf assemblages can be understood by considering the degree to which photosynthetic and structural mass components contribute to LMA variation in a given assemblage.

Allometric constraints and competition enable the simulation of size structure and carbon fluxes in a dynamic vegetation model of tropical forests (LM3PPA-TV).

Tropical forests are a key determinant of the functioning of the Earth system, but remain a major source of uncertainty in carbon cycle models and climate change projections. In this study, we present an updated land model (LM3PPA-TV) to improve the representation of tropical forest structure and dynamics in Earth system models (ESMs). The development and parameterization of LM3PPA-TV drew on extensive datasets on tropical tree traits and long-term field censuses from Barro Colorado Island (BCI), Panama. The model defines a new plant functional type (PFT) based on the characteristics of shade-tolerant, tropical tree species, implements a new growth allocation scheme based on realistic tree allometries, incorporates hydraulic constraints on biomass accumulation, and features a new compartment for tree branches and branch fall dynamics. Simulation experiments reproduced observed diurnal and seasonal patterns in stand-level carbon and water fluxes, as well as mean canopy and understory tree growth rates, tree size distributions, and stand-level biomass on BCI. Simulations at multiple sites captured considerable variation in biomass and size structure across the tropical forest biome, including observed responses to precipitation and temperature. Model experiments suggested a major role of water limitation in controlling geographic variation forest biomass and structure. However, the failure to simulate tropical forests under extreme conditions and the systematic underestimation of forest biomass in Paleotropical locations highlighted the need to incorporate variation in hydraulic traits and multiple PFTs that capture the distinct floristic composition across tropical domains. The continued pressure on tropical forests from global change demands models which are able to simulate alternative successional pathways and their pace to recovery. LM3PPA-TV provides a tool to investigate geographic variation in tropical forests and a benchmark to continue improving the representation of tropical forests dynamics and their carbon storage potential in ESMs.

Predicting shifts in the functional composition of tropical forests under increased drought and CO2 from trade-offs among plant hydraulic traits.

Tropical forest responses are an important feedback on global change, but changes in forest composition with projected increases in CO2 and drought are highly uncertain. Here we determine shifts in the most competitive plant hydraulic strategy (the evolutionary stable strategy or ESS) from changes in CO2 and drought frequency and intensity. Hydraulic strategies were defined along a spectrum from drought avoidance to tolerance by physiology traits. Drought impacted competition more than CO2 , with elevated CO2 reducing but not reversing drought-induced shifts in the ESS towards more tolerant strategies. Trait plasticity and/or adaptation intensified these shifts by increasing the competitive ability of the drought tolerant relative to the avoidant strategies. These findings predict losses of drought avoidant evergreens from tropical forests under global change, and point to the importance of changes in precipitation during the dry season and constraints on plasticity and adaptation in xylem traits to forest responses.

Bias in the detection of negative density dependence in plant communities.

Regression dilution is a statistical inference bias that causes underestimation of the strength of dependency between two variables when the predictors are error-prone proxies (EPPs). EPPs are widely used in plant community studies focused on negative density-dependence (NDD) to quantify competitive interactions. Because of the nature of the bias, conspecific NDD is often overestimated in recruitment analyses, and in some cases, can be erroneously detected when absent. In contrast, for survival analyses, EPPs typically cause NDD to be underestimated, but underestimation is more severe for abundant species and for heterospecific effects, thereby generating spurious negative relationships between the strength of NDD and the abundances of con- and heterospecifics. This can explain why many studies observed rare species to suffer more severely from conspecific NDD, and heterospecific effects to be disproportionally smaller than conspecific effects. In general, such species-dependent bias is often related to traits associated with likely mechanisms of NDD, which creates false patterns and complicates the ecological interpretation of the analyses. Classic examples taken from literature and simulations demonstrate that this bias has been pervasive, which calls into question the emerging paradigm that intraspecific competition has been demonstrated by direct field measurements to be generally stronger than interspecific competition.

Optimal stomatal behavior with competition for water and risk of hydraulic impairment.

For over 40 y the dominant theory of stomatal behavior has been that plants should open stomates until the carbon gained by an infinitesimal additional opening balances the additional water lost times a water price that is constant at least over short periods. This theory has persisted because of its remarkable success in explaining strongly supported simple empirical models of stomatal conductance, even though we have also known for over 40 y that the theory is not consistent with competition among plants for water. We develop an alternative theory in which plants maximize carbon gain without pricing water loss and also add two features to both this and the classical theory, which are strongly supported by empirical evidence: (i) water flow through xylem that is progressively impaired as xylem water potential drops and (ii) fitness or carbon costs associated with low water potentials caused by a variety of mechanisms, including xylem damage repair. We show that our alternative carbon-maximization optimization is consistent with plant competition because it yields an evolutionary stable strategy (ESS)-species with the ESS stomatal behavior that will outcompete all others. We further show that, like the classical theory, the alternative theory also explains the functional forms of empirical stomatal models. We derive ways to test between the alternative optimization criteria by introducing a metric-the marginal xylem tension efficiency, which quantifies the amount of photosynthesis a plant will forego from opening stomatal an infinitesimal amount more to avoid a drop in water potential.

Edge fires drive the shape and stability of tropical forests.

In tropical regions, fires propagate readily in grasslands but typically consume only edges of forest patches. Thus, forest patches grow due to tree propagation and shrink by fires in surrounding grasslands. The interplay between these competing edge effects is unknown, but critical in determining the shape and stability of individual forest patches, as well the landscape-level spatial distribution and stability of forests. We analyze high-resolution remote-sensing data from protected Brazilian Cerrado areas and find that forest shapes obey a robust perimeter-area scaling relation across climatic zones. We explain this scaling by introducing a heterogeneous fire propagation model of tropical forest-grassland ecotones. Deviations from this perimeter-area relation determine the stability of individual forest patches. At a larger scale, our model predicts that the relative rates of tree growth due to propagative expansion and long-distance seed dispersal determine whether collapse of regional-scale tree cover is continuous or discontinuous as fire frequency changes.

Woody plants optimise stomatal behaviour relative to hydraulic risk.

Stomatal response to environmental conditions forms the backbone of all ecosystem and carbon cycle models, but is largely based on empirical relationships. Evolutionary theories of stomatal behaviour are critical for guarding against prediction errors of empirical models under future climates. Longstanding theory holds that stomata maximise fitness by acting to maintain constant marginal water use efficiency over a given time horizon, but a recent evolutionary theory proposes that stomata instead maximise carbon gain minus carbon costs/risk of hydraulic damage. Using data from 34 species that span global forest biomes, we find that the recent carbon-maximisation optimisation theory is widely supported, revealing that the evolution of stomatal regulation has not been primarily driven by attainment of constant marginal water use efficiency. Optimal control of stomata to manage hydraulic risk is likely to have significant consequences for ecosystem fluxes during drought, which is critical given projected intensification of the global hydrological cycle.

Differential declines in Alaskan boreal forest vitality related to climate and competition.

Rapid warming and changes in water availability at high latitudes alter resource abundance, tree competition, and disturbance regimes. While these changes are expected to disrupt the functioning of boreal forests, their ultimate implications for forest composition are uncertain. In particular, recent site-level studies of the Alaskan boreal forest have reported both increases and decreases in productivity over the past few decades. Here, we test the idea that variations in Alaskan forest growth and mortality rates are contingent on species composition. Using forest inventory measurements and climate data from plots located throughout interior and south-central Alaska, we show significant growth and mortality responses associated with competition, midsummer vapor pressure deficit, and increased growing season length. The governing climate and competition processes differed substantially across species. Surprisingly, the most dramatic climate response occurred in the drought tolerant angiosperm species, trembling aspen, and linked high midsummer vapor pressure deficits to decreased growth and increased insect-related mortality. Given that species composition in the Alaskan and western Canadian boreal forests is projected to shift toward early-successional angiosperm species due to fire regime, these results underscore the potential for a reduction in boreal productivity stemming from increases in midsummer evaporative demand.

Decreased water limitation under elevated CO2 amplifies potential for forest carbon sinks.

Increasing atmospheric CO2 concentrations and changing rainfall regimes are creating novel environments for plant communities around the world. The resulting changes in plant productivity and allocation among tissues will have significant impacts on forest carbon storage and the global carbon cycle, yet these effects may depend on mechanisms not included in global models. Here we focus on the role of individual-level competition for water and light in forest carbon allocation and storage across rainfall regimes. We find that the complexity of plant responses to rainfall regimes in experiments can be explained by individual-based competition for water and light within a continuously varying soil moisture environment. Further, we find that elevated CO2 leads to large amplifications of carbon storage when it alleviates competition for water by incentivizing competitive plants to divert carbon from short-lived fine roots to long-lived woody biomass. Overall, we find that plant dependence on rainfall regimes and plant responses to added CO2 are complex, but understandable. The insights developed here will serve as an important foundation as we work to predict the responses of plants to the full, multidimensional reality of climate change, which involves not only changes in rainfall and CO2 but also changes in temperature, nutrient availability, and disturbance rates, among others.

Tropical nighttime warming as a dominant driver of variability in the terrestrial carbon sink.

The terrestrial biosphere is currently a strong carbon (C) sink but may switch to a source in the 21st century as climate-driven losses exceed CO2-driven C gains, thereby accelerating global warming. Although it has long been recognized that tropical climate plays a critical role in regulating interannual climate variability, the causal link between changes in temperature and precipitation and terrestrial processes remains uncertain. Here, we combine atmospheric mass balance, remote sensing-modeled datasets of vegetation C uptake, and climate datasets to characterize the temporal variability of the terrestrial C sink and determine the dominant climate drivers of this variability. We show that the interannual variability of global land C sink has grown by 50-100% over the past 50 y. We further find that interannual land C sink variability is most strongly linked to tropical nighttime warming, likely through respiration. This apparent sensitivity of respiration to nighttime temperatures, which are projected to increase faster than global average temperatures, suggests that C stored in tropical forests may be vulnerable to future warming.

Reconciling divergent estimates of oil and gas methane emissions.

Published estimates of methane emissions from atmospheric data (top-down approaches) exceed those from source-based inventories (bottom-up approaches), leading to conflicting claims about the climate implications of fuel switching from coal or petroleum to natural gas. Based on data from a coordinated campaign in the Barnett Shale oil and gas-producing region of Texas, we find that top-down and bottom-up estimates of both total and fossil methane emissions agree within statistical confidence intervals (relative differences are 10% for fossil methane and 0.1% for total methane). We reduced uncertainty in top-down estimates by using repeated mass balance measurements, as well as ethane as a fingerprint for source attribution. Similarly, our bottom-up estimate incorporates a more complete count of facilities than past inventories, which omitted a significant number of major sources, and more effectively accounts for the influence of large emission sources using a statistical estimator that integrates observations from multiple ground-based measurement datasets. Two percent of oil and gas facilities in the Barnett accounts for half of methane emissions at any given time, and high-emitting facilities appear to be spatiotemporally variable. Measured oil and gas methane emissions are 90% larger than estimates based on the US Environmental Protection Agency's Greenhouse Gas Inventory and correspond to 1.5% of natural gas production. This rate of methane loss increases the 20-y climate impacts of natural gas consumed in the region by roughly 50%.

Variations of leaf longevity in tropical moist forests predicted by a trait-driven carbon optimality model.

Leaf longevity (LL) varies more than 20-fold in tropical evergreen forests, but it remains unclear how to capture these variations using predictive models. Current theories of LL that are based on carbon optimisation principles are challenging to quantitatively assess because of uncertainty across species in the 'ageing rate:' the rate at which leaf photosynthetic capacity declines with age. Here, we present a meta-analysis of 49 species across temperate and tropical biomes, demonstrating that the ageing rate of photosynthetic capacity is positively correlated with the mass-based carboxylation rate of mature leaves. We assess an improved trait-driven carbon optimality model with in situLL data for 105 species in two Panamanian forests. We show that our model explains over 40% of the cross-species variation in LL under contrasting light environment. Collectively, our results reveal how variation in LL emerges from carbon optimisation constrained by both leaf structural traits and abiotic environment.