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.

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.

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.

Botanic gardens are an untapped resource for studying the functional ecology of tropical plants.

Functional traits are increasingly used to understand the ecology of plants and to predict their responses to global changes. Unfortunately, trait data are unavailable for the majority of plant species. The lack of trait data is especially prevalent for hard-to-measure traits and for tropical plant species, potentially owing to the many inherent difficulties of working with species in remote, hyperdiverse rainforest systems. The living collections of botanic gardens provide convenient access to large numbers of tropical plant species and can potentially be used to quickly augment trait databases and advance our understanding of species' responses to climate change. In this review, we quantitatively assess the availability of trait data for tropical versus temperate species, the diversity of species available for sampling in several exemplar tropical botanic gardens and the validity of garden-based leaf and root trait measurements. Our analyses support the contention that the living collections of botanic gardens are a valuable scientific resource that can contribute significantly to research on plant functional ecology and conservation.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

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.