A new field instrument for leaf volatiles reveals an unexpected vertical profile of isoprenoid emission capacities in a tropical forest.

Both plant physiology and atmospheric chemistry are substantially altered by the emission of volatile isoprenoids (VI), such as isoprene and monoterpenes, from plant leaves. Yet, since gaining scientific attention in the 1950?s, empirical research on leaf VI has been largely confined to laboratory experiments and atmospheric observations. Here, we introduce a new field instrument designed to bridge the scales from leaf to atmosphere, by enabling precision VI detection in real time from plants in their natural ecological setting. With a field campaign in the Brazilian Amazon, we reveal an unexpected distribution of leaf emission capacities (EC) across the vertical axis of the forest canopy, with EC peaking in the mid-canopy instead of the sun-exposed canopy surface, and moderately high emissions occurring in understory specialist species. Compared to the simple interpretation that VI protect leaves from heat stress at the hot canopy surface, our results encourage a more nuanced view of the adaptive role of VI in plants. We infer that forest emissions to the atmosphere depend on the dynamic microenvironments imposed by canopy structure, and not simply on canopy surface conditions. We provide a new emissions inventory from 52 tropical tree species, revealing moderate consistency in EC within taxonomic groups. We highlight priorities in leaf volatiles research that require field-portable detection systems. Our self-contained, portable instrument provides real-time detection and live measurement feedback with precision and detection limits better than 0.5 nmolVI m-2 leaf s-1. We call the instrument ?PORCO? based on the gas detection method: photoionization of organic compounds. We provide a thorough validation of PORCO and demonstrate its capacity to detect ecologically driven variation in leaf emission rates and thus accelerate a nascent field of science: the ecology and ecophysiology of plant volatiles

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.Financial support for this study was provided to: T.C.T. and S.R.S. by grants NSF-PIRE #OISE-0730305, USDOE #3002937712, NASA #NNX17AF65G and the University of AZ Agnes Nelms Haury Program in Environment and Social Justice; to M.N.S. and S.R.S. by NASA-ESSF #NNX14AK95H; to C.V. by ERCStG-2014-639706-CONSTRAINTS; to I.S. by Grant Agency of the Czech Republic #16-26369S; and to P.M. by NERC # NE/ N006852/1 and ARC #DP170104091

Intra- and interannual changes in isoprene emission from central Amazonia

Isoprene emissions are a key component in biosphere-atmosphere interactions, and the most significant global source is the Amazon rainforest. However, intra- and interannual variations in biological and environmental factors that regulate isoprene emission from Amazonia are not well understood and, thereby, are poorly represented in models. Here, with datasets covering several years of measurements at the Amazon Tall Tower Observatory (ATTO) in central Amazonia, Brazil, we (1) quantified canopy profiles of isoprene mixing ratios across seasons of normal and anomalous years and related them to the main drivers of isoprene emission - solar radiation, temperature, and leaf phenology; (2) evaluated the effect of leaf age on the magnitude of the isoprene emission factor (Es) from different tree species and scaled up to canopy with intra- and interannual leaf age distribution derived by a phenocam; and (3) adapted the leaf age algorithm from the Model of Emissions of Gases and Aerosols from Nature (MEGAN) with observed changes in Es across leaf ages. Our results showed that the variability in isoprene mixing ratios was higher between seasons (max during the dry-to-wet transition seasons) than between years, with values from the extreme 2015 El Niño year not significantly higher than in normal years. In addition, model runs considering in situ observations of canopy Es and the modification on the leaf age algorithm with leaf-level observations of Es presented considerable improvements in the simulated isoprene flux. This shows that MEGAN estimates of isoprene emission can be improved when biological processes are mechanistically incorporated into the model.This research was supported by the German Federal Ministry of Education and Research, BMBF funds 01LB1001A; Brazilian Ministry of Science, Technology, Innovation and Communication; FINEP/MCTIC contract 01.11.01248.00); UEA; FAPEAM; LBA/INPA; and SDS/CEUC/RDS-Uatumã. It was also supported by grant nos. NSF-PRFB-1711997 and NSF-1754163. The article processing charges for this open-access publication were covered by the Max Planck Society.Peer reviewe

Leaf Volatile Emissions Structure Tree Community Assembly and Mediate Climate Feedbacks in Tropical Forests

The biochemistry of leaves merges the fates of trees and the atmosphere. Leaf primary metabolism cycles carbon and indirectly drives atmospheric circulation via the latent heat of transpiration. Tropical forests contain half of global forest carbon, and actively cycle carbon and energy year round, making them critical components of the coupled biosphere-climate system. Climate change threatens tropical forests with rising temperatures and increasing variability of precipitation. Their response will influence future biodiversity as well as the fate of the climate. Understanding the physiological attributes that define tropical tree responses and feedbacks to climate is a current research priority. The emission of isoprene gas from plant leaves has been demonstrated to enhance leaf tolerance to high temperatures and drought. Isoprene is a volatile secondary metabolite produced in the chloroplast by approximately one-third of plant species. While the benefits of isoprene are supported by extensive laboratory and greenhouse-based research, work has only begun to explore how the trait is integrated in plant functional strategies. Whether isoprene influences differential species performance and survival across environments has yet to be tested. An impediment to filling this clear ecological research gap has been a lack of instrumentation capable of quantifying isoprene emissions from leaves in remote field settings. The first study presented here tests the hypothesis that isoprene emission influences plant community assembly shifts across environmental gradients and through time in tropical forests. The capacity for a species to produce isoprene was associated with increased relative abundance at higher temperatures and following drought anomalies. A negative relationship with the length of seasonal drought suggests a trade-off between isoprene emission and other plant traits, such as deciduous leaf habit. The second study presents the development of a new instrument that is uniquely optimized for field-based ecological research on leaf volatiles. The new system, named PORCO (Photoionization of Organic Compounds), utilizes custom leaf cuvettes, precision light control, and an optimized commercial photoionization detector to achieve real-time detection of leaf emissions with detection limits better than 0.5 nmol m⁻² leaf s⁻¹. The third study utilizes PORCO to test hypotheses about the structuring of isoprene within plant functional strategies and across forest microenvironments in an eastern Amazonian evergreen tropical forest. The results support the role of isoprene—and potentially other volatile isoprenoids—in mitigating effects of intermittent sun exposure in the sub-canopy. Emissions are structured in a complex, multivariate manner that depends on taxonomy, leaf and wood characteristics, tree height, and light environment. The results from this dissertation work demonstrate that isoprene emission from leaves affects plant responses to climate at ecologically relevant scales. Isoprene influences climate not only by its effect on primary leaf functions, but also by directly altering atmospheric chemistry, and contributing to aerosol and cloud properties. Understanding isoprene's role in forest responses to increasing temperatures and drought will help to predict the feedbacks between forest ecosystems and climatic change

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. That isoprene emission enhances the thermal tolerance of photosynthesis is supported by decades of experimental physiology. But whether isoprene differentiates the thermal niches of emitting from non‐emitting species remains untested in the real world. We provide evidence that isoprene‐emitting tropical woody plant species photosynthesize to higher maximum temperatures, and over a broader thermal range, compared with co‐occurring, non‐emitting species. Even accounting for the carbon cost of isoprene emissions, we find no substantial trade‐offs associated with this high‐temperature advantage

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

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’

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

International audiencePlant 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 model