Thermal sensitivity across forest vertical profiles: patterns, mechanisms, and ecological implications.

Rising temperatures are influencing forests on many scales, with potentially strong variation vertically across forest strata. Using published research and new analyses, we evaluate how microclimate and leaf temperatures, traits, and gas exchange vary vertically in forests, shaping tree, and ecosystem ecology. In closed-canopy forests, upper canopy leaves are exposed to the highest solar radiation and evaporative demand, which can elevate leaf temperature (Tleaf ), particularly when transpirational cooling is curtailed by limited stomatal conductance. However, foliar traits also vary across height or light gradients, partially mitigating and protecting against the elevation of upper canopy Tleaf . Leaf metabolism generally increases with height across the vertical gradient, yet differences in thermal sensitivity across the gradient appear modest. Scaling from leaves to trees, canopy trees have higher absolute metabolic capacity and growth, yet are more vulnerable to drought and damaging Tleaf than their smaller counterparts, particularly under climate change. By contrast, understory trees experience fewer extreme high Tleaf 's but have fewer cooling mechanisms and thus may be strongly impacted by warming under some conditions, particularly when exposed to a harsher microenvironment through canopy disturbance. As the climate changes, integrating the patterns and mechanisms reviewed here into models will be critical to forecasting forest-climate feedback.

The other side of tropical forest drought: do shallow water table regions of Amazonia act as large-scale hydrological refugia from drought?

Tropical forest function is of global significance to climate change responses, and critically determined by water availability patterns. Groundwater is tightly related to soil water through the water table depth (WT), but historically neglected in ecological studies. Shallow WT forests (WT < 5 m) are underrepresented in forest research networks and absent in eddy flux measurements, although they represent c. 50% of the Amazon and are expected to respond differently to global-change-related droughts. We review WT patterns and consequences for plants, emerging results, and advance a conceptual model integrating environment and trait distributions to predict climate change effects. Shallow WT forests have a distinct species composition, with more resource-acquisitive and hydrologically vulnerable trees, shorter canopies and lower biomass than deep WT forests. During 'normal' climatic years, shallow WT forests have higher mortality and lower productivity than deep WT forests, but during moderate droughts mortality is buffered and productivity increases. However, during severe drought, shallow WT forests may be more sensitive due to shallow roots and drought-intolerant traits. Our evidence supports the hypothesis of neglected shallow WT forests being resilient to moderate drought, challenging the prevailing view of widespread negative effects of climate change on Amazonian forests that ignores WT gradients, but predicts they could collapse under very strong droughts.

O funcionamento da floresta tropical é de importância global para as respostas às mudanças climáticas e é criticamente determinado pelos padrões de disponibilidade de água. A água subterrânea está intimamente relacionada à água do solo através da profundidade do lençol freático, que tem sido historicamente negligenciado em estudos ecológicos. Florestas com lençol freático raso (< 5 m) estão sub-representadas nas redes de pesquisa florestal e ausentes nas medições de fluxo de gases, embora representem ~ 50% da Amazônia e devam responder de forma diferente às secas relacionadas às mudanças globais. Aqui revisamos os padrões de profundidade do lençol freático e suas consequências para plantas, resultados emergentes, e avançamos em um modelo conceitual que integra o ambiente e as distribuições de características funcionais para prever os efeitos das mudanças climáticas. As florestas com lençol freático raso têm uma composição de espécies distinta, com árvores mais aquisitivas na obtenção de recursos e hidrologicamente vulneráveis, dosséis mais baixos e menor biomassa do que as florestas com lençol freático profundo. Durante os anos climáticos 'normais', as florestas com lençol freático raso têm maior mortalidade e menor produtividade do que as florestas com lençol freático profundo, mas durante secas moderadas, a mortalidade é amortecida e a produtividade aumenta. No entanto, durante secas severas, as florestas com lençol freático raso podem ser mais sensíveis devido às raízes superficiais e características funcionais de intolerância à seca. Nossas evidências apoiam a hipótese de que as florestas com lençol freático raso, historicamente negligenciadas, sejam resilientes à seca moderada, desafiando a visão predominante dos efeitos negativos generalizados da mudança climática nas florestas amazônicas que ignora gradientes de profundidade do lençol freático, mas prevê que elas podem entrar em colapso sob secas muito fortes.

La función de los bosques tropicales es de importancia mundial para las respuestas al cambio climático y está críticamente determinada por los patrones de disponibilidad de agua. El agua subterránea está estrechamente relacionada con el agua del suelo a través de la profundidad del nivel freático (NF), pero históricamente se há negligenciado en los estudios ecológicos. Los bosques con NF poco profundos (NF < 5 m) están subrepresentados en las redes de investigación forestal y ausentes en las mediciones de flujo de gases, aunque representan ~ 50% de la Amazonía y se espera que respondan de manera diferente a las sequías relacionadas con el cambio climático global. Aquí revisamos los patrones de NF y las consecuencias para las plantas, los resultados emergentes y avanzamos en un modelo conceptual que integra distribuciones ambientales y de rasgos funcionales para predecir los efectos del cambio climático. Los bosques con NF poco profundos tienen una composición de especies distinta, con árboles más adquisitivos en la obtención de recursos e hidrológicamente más vulnerables, dosel más bajo y menor biomasa que los bosques de NF profundo. Durante los años climáticos 'normales', los bosques con NF poco profundos tienen una mayor mortalidad y menor productividad que los bosques con NF profundos, pero durante sequías moderadas la mortalidad se amortigua y la productividad aumenta. Sin embargo, durante una sequía severa, los bosques de NF poco profundos pueden ser más sensibles debido a raíces poco profundas y rasgos de intolerancia a la sequía. Nuestra evidencia apoya la hipótesis de que los bosques de NF poco profundos, mayoritariamente desconsiderados, son resistentes a sequías moderadas, desafiando la visión predominante de impactos negativos generalizados del cambio climático en los bosques amazónicos, que ignora los gradientes de NF, pero predice que podrían colapsar bajo sequías muy fuertes.

Forest fragmentation impacts the seasonality of Amazonian evergreen canopies.

Predictions of the magnitude and timing of leaf phenology in Amazonian forests remain highly controversial. Here, we use terrestrial LiDAR surveys every two weeks spanning wet and dry seasons in Central Amazonia to show that plant phenology varies strongly across vertical strata in old-growth forests, but is sensitive to disturbances arising from forest fragmentation. In combination with continuous microclimate measurements, we find that when maximum daily temperatures reached 35 °C in the latter part of the dry season, the upper canopy of large trees in undisturbed forests lost plant material. In contrast, the understory greened up with increased light availability driven by the upper canopy loss, alongside increases in solar radiation, even during periods of drier soil and atmospheric conditions. However, persistently high temperatures in forest edges exacerbated the upper canopy losses of large trees throughout the dry season, whereas the understory in these light-rich environments was less dependent on the altered upper canopy structure. Our findings reveal a strong influence of edge effects on phenological controls in wet forests of Central Amazonia.

Empirical evidence for resilience of tropical forest photosynthesis in a warmer world.

Tropical forests may be vulnerable to climate change1-3 if photosynthetic carbon uptake currently operates near a high temperature limit4-6. Predicting tropical forest function requires understanding the relative contributions of two mechanisms of high-temperature photosynthetic declines: stomatal limitation (H1), an indirect response due to temperature-associated changes in atmospheric vapour pressure deficit (VPD)7, and biochemical restrictions (H2), a direct temperature response8,9. Their relative control predicts different outcomes-H1 is expected to diminish with stomatal responses to future co-occurring elevated atmospheric [CO2], whereas H2 portends declining photosynthesis with increasing temperatures. Distinguishing the two mechanisms at high temperatures is therefore critical, but difficult because VPD is highly correlated with temperature in natural settings. We used a forest mesocosm to quantify the sensitivity of tropical gross ecosystem productivity (GEP) to future temperature regimes while constraining VPD by controlling humidity. We then analytically decoupled temperature and VPD effects under current climate with flux-tower-derived GEP trends in situ from four tropical forest sites. Both approaches showed consistent, negative sensitivity of GEP to VPD but little direct response to temperature. Importantly, in the mesocosm at low VPD, GEP persisted up to 38 °C, a temperature exceeding projections for tropical forests in 2100 (ref. 10). If elevated [CO2] mitigates VPD-induced stomatal limitation through enhanced water-use efficiency as hypothesized9,11, tropical forest photosynthesis may have a margin of resilience to future warming.

Cryptic phenology in plants: Case studies, implications, and recommendations.

Plant phenology-the timing of cyclic or recurrent biological events in plants-offers insight into the ecology, evolution, and seasonality of plant-mediated ecosystem processes. Traditionally studied phenologies are readily apparent, such as flowering events, germination timing, and season-initiating budbreak. However, a broad range of phenologies that are fundamental to the ecology and evolution of plants, and to global biogeochemical cycles and climate change predictions, have been neglected because they are "cryptic"-that is, hidden from view (e.g., root production) or difficult to distinguish and interpret based on common measurements at typical scales of examination (e.g., leaf turnover in evergreen forests). We illustrate how capturing cryptic phenology can advance scientific understanding with two case studies: wood phenology in a deciduous forest of the northeastern USA and leaf phenology in tropical evergreen forests of Amazonia. Drawing on these case studies and other literature, we argue that conceptualizing and characterizing cryptic plant phenology is needed for understanding and accurate prediction at many scales from organisms to ecosystems. We recommend avenues of empirical and modeling research to accelerate discovery of cryptic phenological patterns, to understand their causes and consequences, and to represent these processes in terrestrial biosphere models.

Persistent effects of fragmentation on tropical rainforest canopy structure after 20 yr of isolation.

Assessing the persistent impacts of fragmentation on aboveground structure of tropical forests is essential to understanding the consequences of land use change for carbon storage and other ecosystem functions. We investigated the influence of edge distance and fragment size on canopy structure, aboveground woody biomass (AGB), and AGB turnover in the Biological Dynamics of Forest Fragments Project (BDFFP) in central Amazon, Brazil, after 22+ yr of fragment isolation, by combining canopy variables collected with portable canopy profiling lidar and airborne laser scanning surveys with long-term forest inventories. Forest height decreased by 30% at edges of large fragments (>10 ha) and interiors of small fragments (<3 ha). In larger fragments, canopy height was reduced up to 40 m from edges. Leaf area density profiles differed near edges: the density of understory vegetation was higher and midstory vegetation lower, consistent with canopy reorganization via increased regeneration of pioneers following post-fragmentation mortality of large trees. However, canopy openness and leaf area index remained similar to control plots throughout fragments, while canopy spatial heterogeneity was generally lower at edges. AGB stocks and fluxes were positively related to canopy height and negatively related to spatial heterogeneity. Other forest structure variables typically used to assess the ecological impacts of fragmentation (basal area, density of individuals, and density of pioneer trees) were also related to lidar-derived canopy surface variables. Canopy reorganization through the replacement of edge-sensitive species by disturbance-tolerant ones may have mitigated the biomass loss effects due to fragmentation observed in the earlier years of BDFFP. Lidar technology offered novel insights and observational scales for analysis of the ecological impacts of fragmentation on forest structure and function, specifically aboveground biomass storage.

The capacity to emit isoprene differentiates the photosynthetic temperature responses of tropical plant species.

Experimental research shows that isoprene emission by plants can improve photosynthetic performance at high temperatures. But whether species that emit isoprene have higher thermal limits than non-emitting species remains largely untested. Tropical plants are adapted to narrow temperature ranges and global warming could result in significant ecosystem restructuring due to small variations in species' thermal tolerances. We compared photosynthetic temperature responses of 26 co-occurring tropical tree and liana species to test whether isoprene-emitting species are more tolerant to high temperatures. We classified species as isoprene emitters versus non-emitters based on published datasets. Maximum temperatures for net photosynthesis were ~1.8°C higher for isoprene-emitting species than for non-emitters, and thermal response curves were 24% wider; differences in optimum temperatures (Topt ) or photosynthetic rates at Topt were not significant. Modelling the carbon cost of isoprene emission, we show that even strong emission rates cause little reduction in the net carbon assimilation advantage over non-emitters at supraoptimal temperatures. Isoprene emissions may alleviate biochemical limitations, which together with stomatal conductance, co-limit photosynthesis above Topt . Our findings provide evidence that isoprene emission may be an adaptation to warmer thermal niches, and that emitting species may fare better under global warming than co-occurring non-emitting species.

Seasonal and drought-related changes in leaf area profiles depend on height and light environment in an Amazon forest.

Seasonal dynamics in the vertical distribution of leaf area index (LAI) may impact the seasonality of forest productivity in Amazonian forests. However, until recently, fine-scale observations critical to revealing ecological mechanisms underlying these changes have been lacking. To investigate fine-scale variation in leaf area with seasonality and drought we conducted monthly ground-based LiDAR surveys over 4 yr at an Amazon forest site. We analysed temporal changes in vertically structured LAI along axes of both canopy height and light environments. Upper canopy LAI increased during the dry season, whereas lower canopy LAI decreased. The low canopy decrease was driven by highly illuminated leaves of smaller trees in gaps. By contrast, understory LAI increased concurrently with the upper canopy. Hence, tree phenological strategies were stratified by height and light environments. Trends were amplified during a 2015-2016 severe El Niño drought. Leaf area low in the canopy exhibited behaviour consistent with water limitation. Leaf loss from short trees in high light during drought may be associated with strategies to tolerate limited access to deep soil water and stressful leaf environments. Vertically and environmentally structured phenological processes suggest a critical role of canopy structural heterogeneity in seasonal changes in Amazon ecosystem function.

Isoprene emission structures tropical tree biogeography and community assembly responses to climate.

The prediction of vegetation responses to climate requires a knowledge of how climate-sensitive plant traits mediate not only the responses of individual plants, but also shifts in the species and functional compositions of whole communities. The emission of isoprene gas - a trait shared by one-third of tree species - is known to protect leaf biochemistry under climatic stress. Here, we test the hypothesis that isoprene emission shapes tree species compositions in tropical forests by enhancing the tolerance of emitting trees to heat and drought. Using forest inventory data, we estimated the proportional abundance of isoprene-emitting trees (pIE) at 103 lowland tropical sites. We also quantified the temporal composition shifts in three tropical forests - two natural and one artificial - subjected to either anomalous warming or drought. Across the landscape, pIE increased with site mean annual temperature, but decreased with dry season length. Through time, pIE strongly increased under high temperatures, and moderately increased following drought. Our analysis shows that isoprene emission is a key plant trait determining species responses to climate. For species adapted to seasonal dry periods, isoprene emission may tradeoff with alternative strategies, such as leaf deciduousness. Community selection for isoprene-emitting species is a potential mechanism for enhanced forest resilience to climatic change.

Age-dependent leaf physiology and consequences for crown-scale carbon uptake during the dry season in an Amazon evergreen forest.

Satellite and tower-based metrics of forest-scale photosynthesis generally increase with dry season progression across central Amazônia, but the underlying mechanisms lack consensus. We conducted demographic surveys of leaf age composition, and measured the age dependence of leaf physiology in broadleaf canopy trees of abundant species at a central eastern Amazon site. Using a novel leaf-to-branch scaling approach, we used these data to independently test the much-debated hypothesis - arising from satellite and tower-based observations - that leaf phenology could explain the forest-scale pattern of dry season photosynthesis. Stomatal conductance and biochemical parameters of photosynthesis were higher for recently mature leaves than for old leaves. Most branches had multiple leaf age categories simultaneously present, and the number of recently mature leaves increased as the dry season progressed because old leaves were exchanged for new leaves. These findings provide the first direct field evidence that branch-scale photosynthetic capacity increases during the dry season, with a magnitude consistent with increases in ecosystem-scale photosynthetic capacity derived from flux towers. Interactions between leaf age-dependent physiology and shifting leaf age-demographic composition are sufficient to explain the dry season photosynthetic capacity pattern at this site, and should be considered in vegetation models of tropical evergreen forests.

Revisiting Darwin's hypothesis: Does greater intraspecific variability increase species' ecological breadth?

PREMISE OF THE STUDY: Darwin first proposed that species with larger ecological breadth have greater phenotypic variation. We tested this hypothesis by comparing intraspecific variation in specific leaf area (SLA) to species' local elevational range and by assessing how external (abiotic) filters may influence observed differences in ecological breadth among species. Understanding the patterns of individual variation within and between populations will help evaluate differing hypotheses for structuring of communities and distribution of species. METHODS: We selected 21 species with varying elevational ranges and compared the coefficient of variation of SLA for each species against its local elevational range. We examined the influence of external filters on local trait composition by determining if intraspecific changes in SLA with elevation have the same direction and similar rates of change as the change in community mean SLA value. KEY RESULTS: In support of Darwin's hypothesis, we found a positive relationship between species' coefficient of variation for SLA with species' local elevational range. Intraspecific changes in SLA had the same sign, but generally lower magnitude than the community mean SLA. CONCLUSIONS: The results indicate that wide-ranging species are indeed characterized by greater intraspecific variation and that species' phenotypes shift along environmental gradients in the same direction as the community phenotypes. However, across species, the rate of intraspecific trait change, reflecting plastic and/or adaptive changes across populations, is limited and prevents species from adjusting to environmental gradients as quickly as interspecific changes resulting from community assembly.