No evidence of canopy-scale leaf thermoregulation to cool leaves below air temperature across a range of forest ecosystems.

Understanding and predicting the relationship between leaf temperature (Tleaf) and air temperature (Tair) is essential for projecting responses to a warming climate, as studies suggest that many forests are near thermal thresholds for carbon uptake. Based on leaf measurements, the limited leaf homeothermy hypothesis argues that daytime Tleaf is maintained near photosynthetic temperature optima and below damaging temperature thresholds. Specifically, leaves should cool below Tair at higher temperatures (i.e., > ∼25-30°C) leading to slopes <1 in Tleaf/Tair relationships and substantial carbon uptake when leaves are cooler than air. This hypothesis implies that climate warming will be mitigated by a compensatory leaf cooling response. A key uncertainty is understanding whether such thermoregulatory behavior occurs in natural forest canopies. We present an unprecedented set of growing season canopy-level leaf temperature (Tcan) data measured with thermal imaging at multiple well-instrumented forest sites in North and Central America. Our data do not support the limited homeothermy hypothesis: canopy leaves are warmer than air during most of the day and only cool below air in mid to late afternoon, leading to Tcan/Tair slopes >1 and hysteretic behavior. We find that the majority of ecosystem photosynthesis occurs when canopy leaves are warmer than air. Using energy balance and physiological modeling, we show that key leaf traits influence leaf-air coupling and ultimately the Tcan/Tair relationship. Canopy structure also plays an important role in Tcan dynamics. Future climate warming is likely to lead to even greater Tcan, with attendant impacts on forest carbon cycling and mortality risk.

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.

Soils and topography control natural disturbance rates and thereby forest structure in a lowland tropical landscape.

Tree mortality is a major control over tropical forest carbon stocks globally but the strength of associations between abiotic drivers and tree mortality within forested landscapes is poorly understood. Here, we used repeat drone photogrammetry across 1500 ha of forest in Central Panama over 5 years to quantify spatial variation in canopy disturbance rates and its predictors. We identified 11,153 canopy disturbances greater than 25 m2 in area, including treefalls, large branchfalls and standing dead trees, affecting 1.9% of area per year. Soil type, forest age and topography explained up to 46%-67% of disturbance rate variation at spatial grains of 58-64 ha, with higher rates in older forests, steeper slopes and local depressions. Furthermore, disturbance rates predicted the proportion of low canopy area across the landscape, and mean canopy height in old growth forests. Thus abiotic factors drive variation in disturbance rates and thereby forest structure at landscape scales.

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.

Liana optical traits increase tropical forest albedo and reduce ecosystem productivity.

Lianas are a key growth form in tropical forests. Their lack of self-supporting tissues and their vertical position on top of the canopy make them strong competitors of resources. A few pioneer studies have shown that liana optical traits differ on average from those of colocated trees. Those trait discrepancies were hypothesized to be responsible for the competitive advantage of lianas over trees. Yet, in the absence of reliable modelling tools, it is impossible to unravel their impact on the forest energy balance, light competition, and on the liana success in Neotropical forests. To bridge this gap, we performed a meta-analysis of the literature to gather all published liana leaf optical spectra, as well as all canopy spectra measured over different levels of liana infestation. We then used a Bayesian data assimilation framework applied to two radiative transfer models (RTMs) covering the leaf and canopy scales to derive tropical tree and liana trait distributions, which finally informed a full dynamic vegetation model. According to the RTMs inversion, lianas grew thinner, more horizontal leaves with lower pigment concentrations. Those traits made the lianas very efficient at light interception and significantly modified the forest energy balance and its carbon cycle. While forest albedo increased by 14% in the shortwave, light availability was reduced in the understorey (-30% of the PAR radiation) and soil temperature decreased by 0.5°C. Those liana-specific traits were also responsible for a significant reduction of tree (-19%) and ecosystem (-7%) gross primary productivity (GPP) while lianas benefited from them (their GPP increased by +27%). This study provides a novel mechanistic explanation to the increase in liana abundance, new evidence of the impact of lianas on forest functioning, and paves the way for the evaluation of the large-scale impacts of lianas on forest biogeochemical cycles.

Imaging canopy temperature: shedding (thermal) light on ecosystem processes.

Canopy temperature Tcan is a key driver of plant function that emerges as a result of interacting biotic and abiotic processes and properties. However, understanding controls on Tcan and forecasting canopy responses to weather extremes and climate change are difficult due to sparse measurements of Tcan at appropriate spatial and temporal scales. Burgeoning observations of Tcan from thermal cameras enable evaluation of energy budget theory and better understanding of how environmental controls, leaf traits and canopy structure influence temperature patterns. The canopy scale is relevant for connecting to remote sensing and testing biosphere model predictions. We anticipate that future breakthroughs in understanding of ecosystem responses to climate change will result from multiscale observations of Tcan across a range of ecosystems.

Hydraulically-vulnerable trees survive on deep-water access during droughts in a tropical forest.

Deep-water access is arguably the most effective, but under-studied, mechanism that plants employ to survive during drought. Vulnerability to embolism and hydraulic safety margins can predict mortality risk at given levels of dehydration, but deep-water access may delay plant dehydration. Here, we tested the role of deep-water access in enabling survival within a diverse tropical forest community in Panama using a novel data-model approach. We inversely estimated the effective rooting depth (ERD, as the average depth of water extraction), for 29 canopy species by linking diameter growth dynamics (1990-2015) to vapor pressure deficit, water potentials in the whole-soil column, and leaf hydraulic vulnerability curves. We validated ERD estimates against existing isotopic data of potential water-access depths. Across species, deeper ERD was associated with higher maximum stem hydraulic conductivity, greater vulnerability to xylem embolism, narrower safety margins, and lower mortality rates during extreme droughts over 35 years (1981-2015) among evergreen species. Species exposure to water stress declined with deeper ERD indicating that trees compensate for water stress-related mortality risk through deep-water access. The role of deep-water access in mitigating mortality of hydraulically-vulnerable trees has important implications for our predictive understanding of forest dynamics under current and future climates.

Optimal leaf life strategies determine Vc,max dynamic during ontogeny.

Leaf photosynthetic properties, for example the maximum carboxylation velocity or Vc,max , change with leaf age due to ontogenetic processes. This study introduces an optimal dynamic allocation scheme to model changes in leaf-level photosynthetic capacity as a function of leaf biochemical constraints (costs of synthesis and defence), nitrogen availability and other environmental factors (e.g. light). The model consists of a system of equations describing RuBisCO synthesis and degradation within chloroplasts, defence and ageing at leaf levels, nitrogen transfer and carbon budget at plant levels. Model results show that optimal allocation principles explained RuBisCO dynamics with leaf age. An approximated analytical solution can reproduce the basic pattern of RuBisCO and Vc,max in rice and in two tropical tree species. The model also reveals leaf life complementarities that remained unexplained in previous approaches, as the interplay between Vc,max at maturation, life span and the decline in photosynthetic capacity with age. Furthermore, it explores the role of defence, which is not implemented in current models. This framework covers some of the existing gaps in integrating multiple processes across plant organs (chloroplast, leaf and whole plant) and is a first-step towards representing mechanistically leaf ontogenetic processes into physiological and ecosystem models.

Lightning is a major cause of large tree mortality in a lowland neotropical forest.

The mortality rates of large trees are critical to determining carbon stocks in tropical forests, but the mechanisms of tropical tree mortality remain poorly understood. Lightning strikes thousands of tropical trees every day, but is commonly assumed to be a minor agent of tree mortality in most tropical forests. We use the first systematic quantification of lightning-caused mortality to show that lightning is a major cause of death for the largest trees in an old-growth lowland forest in Panama. A novel lightning strike location system together with field surveys of strike sites revealed that, on average, each strike directly kills 3.5 trees (> 10 cm diameter) and damages 11.4 more. Given lightning frequency data from the Earth Networks Total Lightning Network and historical total tree mortality rates for this site, we conclude that lightning accounts for 40.5% of the mortality of large trees (> 60 cm diameter) in the short term and probably contributes to an additional 9.0% of large tree deaths over the long term. Any changes in cloud-to-ground lightning frequency due to climatic change will alter tree mortality rates; projected 25-50% increases in lightning frequency would increase large tree mortality rates in this forest by 9-18%. The results of this study indicate that lightning plays a critical and previously underestimated role in tropical forest dynamics and carbon cycling.

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.

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.

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.

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.

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.

Climate and plant trait strategies determine tree carbon allocation to leaves and mediate future forest productivity.

Forest leaf area has enormous leverage on the carbon cycle because it mediates both forest productivity and resilience to climate extremes. Despite widespread evidence that trees are capable of adjusting to changes in environment across both space and time through modifying carbon allocation to leaves, many vegetation models use fixed carbon allocation schemes independent of environment, which introduces large uncertainties into predictions of future forest responses to atmospheric CO2 fertilization and anthropogenic climate change. Here, we develop an optimization-based model, whereby tree carbon allocation to leaves is an emergent property of environment and plant hydraulic traits. Using a combination of meta-analysis, observational datasets, and model predictions, we find strong evidence that optimal hydraulic-carbon coupling explains observed patterns in leaf allocation across large environmental and CO2 concentration gradients. Furthermore, testing the sensitivity of leaf allocation strategy to a diversity in hydraulic and economic spectrum physiological traits, we show that plant hydraulic traits in particular have an enormous impact on the global change response of forest leaf area. Our results provide a rigorous theoretical underpinning for improving carbon cycle predictions through advancing model predictions of leaf area, and underscore that tree-level carbon allocation to leaves should be derived from first principles using mechanistic plant hydraulic processes in the next generation of vegetation models.

Precipitation mediates sap flux sensitivity to evaporative demand in the neotropics.

Transpiration in humid tropical forests modulates the global water cycle and is a key driver of climate regulation. Yet, our understanding of how tropical trees regulate sap flux in response to climate variability remains elusive. With a progressively warming climate, atmospheric evaporative demand [i.e., vapor pressure deficit (VPD)] will be increasingly important for plant functioning, becoming the major control of plant water use in the twenty-first century. Using measurements in 34 tree species at seven sites across a precipitation gradient in the neotropics, we determined how the maximum sap flux velocity (vmax) and the VPD threshold at which vmax is reached (VPDmax) vary with precipitation regime [mean annual precipitation (MAP); seasonal drought intensity (PDRY)] and two functional traits related to foliar and wood economics spectra [leaf mass per area (LMA); wood specific gravity (WSG)]. We show that, even though vmax is highly variable within sites, it follows a negative trend in response to increasing MAP and PDRY across sites. LMA and WSG exerted little effect on vmax and VPDmax, suggesting that these widely used functional traits provide limited explanatory power of dynamic plant responses to environmental variation within hyper-diverse forests. This study demonstrates that long-term precipitation plays an important role in the sap flux response of humid tropical forests to VPD. Our findings suggest that under higher evaporative demand, trees growing in wetter environments in humid tropical regions may be subjected to reduced water exchange with the atmosphere relative to trees growing in drier climates.

Rates of formation and dissipation of clumping reveal lagged responses in tropical tree populations.

The dynamics of spatial patterns of plant populations can provide important information about underlying processes, yet they have received relatively little attention to date. Here we investigate the rates of formation and dissipation of clusters and the relationship of these rates to the degree of aggregation (clumping) in models and in empirical data for tropical trees. In univariate models, exact solutions and simulations show that the rate of change of spatial patterns has a specific, linear relationship to the degree of aggregation at all scales. Shorter dispersal and/or weaker negative density dependence (NDD) result in both denser and longer-lasting clusters. In multivariate host-parasite models in contrast, the rate of change of spatial pattern is faster relative to the level of aggrega- tion. We then analyzed the dynamics of spatial patterns of stems ≥ 1 cm diameter in 221 tropical tree species from seven censuses spanning 28 yr. We found that for most species, the rates of change in spatial patterns were faster than predicted from univariate models given their aggregation. This indicates that more complex dynamics involving multivariate interactions induce time lags in responses to aggregation in these species. Such lags could arise, for example, if it takes time for natural enemies to locate aggregations of their hosts. This combination of theoretical and empirical results thus shows that complex multilevel models are needed to capture spatiotemporal dynamics of tropical forests and provides new insights into the processes structuring tropical plant communities.

Interspecific associations in seed arrival and seedling recruitment in a Neotropical forest.

Contagious seed dispersal refers to the tendency for some sites to receive many dispersed seeds while other sites receive few dispersed seeds. Contagious dispersal can lead to interspecific associations in seed arrival, and this in turn might lead to interspecific associations in seedling recruitment. We evaluate the extent of spatially contagious seed arrival, the frequency of positive interspecific associations in seed arrival, and their consequences for seedling recruitment at the community level in a tropical moist forest. We quantified seed arrival to 200 passive seed traps for 28 yr of weekly censuses and seedling recruitment to 600 1-m2 quadrats for 21 yr of annual censuses on Barro Colorado Island, Panama. We assessed whether spatially contagious seed dispersal was more important among zoochorous species than among anemochorous species, increased in importance with similarity in fruiting times, and led to interspecific associations in seed arrival and seedling recruitment. We controlled adult seed source associations statistically to evaluate predicted relationships. We found that spatially contagious seed arrival was widespread among zoochorous species, but also occurred among anemochorous species when the strong, consistent trade winds were present. Significant interspecific associations in seed arrival were more likely for pairs of species with zoochorous seeds and similar fruiting times and persisted through seedling recruitment. Thus, interspecifically contagious seed dispersal affects local species composition and alters the mixture of interspecific interactions through the seed, germination, and early seedling stages in this forest. Future investigations should consider the implications of interspecific association at the regeneration stages documented here for later life stages and species coexistence.