The carbon balance of plants: economics, optimization, and trait spectra in a historical perspective.

Over fifty years have passed since the publication of Harold Mooney's formative paper, "The Carbon Balance of Plants" on pages 315-346 of Volume 3 (1972) of Annual Review of Ecology and Systematics. Arguably, the conceptual framework presented in that paper, and the work by Mooney and his students leading up to the paper, provided the foundational principles from which core disciplines emerged in plant economic theory, functional trait theory and, more generally, plant physiological ecology. Here, we revisit the primary impacts of those early discoveries to understand how researchers constructed major concepts in our understanding of plant adaptations, and where those concepts are likely to take us in the near future. The discipline of functional trait ecology, which is rooted in the principles of evolutionary and economic optimization, has captured the imagination of the plant physiological ecology research community, though its emphasis has shifted toward predicting species distributions and ecological roles across resource gradients. In the face of 'big-data' research pursuits that are revealing trait expression patterns at the cellular level and mass and energy exchange patterns at the planetary scale, an opportunity exists to reconnect the principles of plant carbon balance and evolutionary optimization with trait origins at the genetic and cellular scales and trait impacts at the global scale.

The North American Monsoon buffers forests against the ongoing megadrought in the Southwestern United States.

The US Southwest has been entrenched in a two-decade-long megadrought (MD), the most severe since 800 CE, which threatens the long-term vitality and persistence of regional montane forests. Here, we report that in the face of record low winter precipitation and increasing atmospheric aridity, seasonal activity of the North American Monsoon (NAM) climate system brings sufficient precipitation during the height of the summer to alleviate extreme tree water stress. We studied seasonally resolved, tree-ring stable carbon isotope ratios across a 57-year time series (1960-2017) in 17 Ponderosa pine forests distributed across the NAM geographic domain. Our study focused on the isotope dynamics of latewood (LW), which is produced in association with NAM rains. During the MD, populations growing within the core region of the NAM operated at lower intrinsic and higher evaporative water-use efficiencies (WUEi and WUEE , respectively), compared to populations growing in the periphery of the NAM domain, indicating less physiological water stress in those populations with access to NAM moisture. The disparities in water-use efficiencies in periphery populations are due to a higher atmospheric vapor pressure deficit (VPD) and reduced access to summer soil moisture. The buffering advantage of the NAM, however, is weakening. We observed that since the MD, the relationship between WUEi and WUEE in forests within the core NAM domain is shifting toward a drought response similar to forests on the periphery of the NAM. After correcting for past increases in the atmospheric CO2 concentration, we were able to isolate the LW time-series responses to climate alone. This showed that the shift in the relation between WUEi and WUEE was driven by the extreme increases in MD-associated VPD, with little advantageous influence on stomatal conductance from increases in atmospheric CO2 concentration.

Tree growth sensitivity to climate varies across a seasonal precipitation gradient.

Spatial patterns of precipitation in the southwestern United States result in a complex gradient from winter-to-summer moisture dominance that influences tree growth. In response, tree growth exhibits seasonal-to-annual variability that is evident in the growth of whole tree rings, and in sub-annual sections such as earlywood and latewood. We evaluated the influence of precipitation and temperature on the growth of Pinus ponderosa trees in 11 sites in the southwestern US. Precipitation during the year of growth and the prior year accounted for about half of the climate influence on annual growth, with the other half reflecting conditions 2-4 years prior to growth, indicating that individual trees do indeed exhibit multi-year "memory" of climate. Trees in wetter sites exhibited weaker influence of past precipitation inputs, but longer memory of climatic variability. Conversely, trees in dry sites exhibited shorter memory of long-term climatic variability, but greater sensitivity to past precipitation effects. These results are consistent with the existence of complex interactions between endogenous (phenotype) effects and exogenous (climate) effects in controlling climate memory in trees. After accounting for climate, residual variability in latewood growth was negatively correlated with earlywood growth, indicating a potential tradeoff between latewood versus earlywood growth. This study provides new insights that will assist the accurate prediction of woody biomass growth and forest carbon sequestration across a southwestern US precipitation gradient.

Heterogeneous isotope effects decouple conifer leaf and branch sugar δ18O and δ13C.

Isotope ratios of tree-ring cellulose are a prominent tool to reconstruct paleoclimate and plant responses to environmental variation. Current models for cellulose isotope ratios assume a transfer of the environmental signals recorded in bulk leaf water to carbohydrates and ultimately into stem cellulose. However, the isotopic signal of carbohydrates exported from leaf to branch may deviate from mean leaf values if spatial heterogeneity in isotope ratios exists in the leaf. We tested whether the isotopic heterogeneity previously observed along the length of a ponderosa pine (Pinus ponderosa) leaf water was preserved in photosynthetic products. We observed an increase in both sugar and bulk tissue δ18O values along the needle, but the increase in carbohydrate δ18O values was dampened relative to the trend observed in leaf water. In contrast, δ13C values of both sugar and bulk organic matter were invariant along the needle. Phloem-exported sugar measured in the branch below the needles did not match whole-needle values of δ18O or δ13C. Instead, there was a near-constant offset observed between the branch and needle sugar δ13C values, while branch δ18O values were most similar to δ18O values observed for sugar at the base of the needle. The observed offset between the branch and needle sugar δ18O values likely arises from partial isotope oxygen exchange between sugars and water during phloem loading and transport. An improved understanding of the conditions producing differential δ13C and δ18O isotope effects between branch phloem and needle sugars could improve tree-ring-based climate reconstructions.

Coordinated resource allocation to plant growth-defense tradeoffs.

Plant resource allocation patterns often reveal tradeoffs that favor growth (G) over defense (D), or vice versa. Ecologists most often explain G-D tradeoffs through principles of economic optimality, in which negative trait correlations are attributed to the reconciliation of fitness costs. Recently, researchers in molecular biology have developed 'big data' resources including multi-omic (e.g. transcriptomic, proteomic and metabolomic) studies that describe the cellular processes controlling gene expression in model species. In this synthesis, we bridge ecological theory with discoveries in multi-omics biology to better understand how selection has shaped the mechanisms of G-D tradeoffs. Multi-omic studies reveal strategically coordinated patterns in resource allocation that are enabled by phytohormone crosstalk and transcriptional signal cascades. Coordinated resource allocation justifies the framework of optimality theory, while providing mechanistic insight into the feedbacks and control hubs that calibrate G-D tradeoff commitments. We use the existing literature to describe the coordinated resource allocation hypothesis (CoRAH) that accounts for balanced cellular controls during the expression of G-D tradeoffs, while sustaining stored resource pools to buffer the impacts of future stresses. The integrative mechanisms of the CoRAH unify the supply- and demand-side perspectives of previous G-D tradeoff theories.

Stable isotopes of tree rings reveal seasonal-to-decadal patterns during the emergence of a megadrought in the Southwestern US.

Recent evidence has revealed the emergence of a megadrought in southwestern North America since 2000. Megadroughts extend for at least 2 decades, making it challenging to identify such events until they are well established. Here, we examined tree-ring growth and stable isotope ratios in Pinus ponderosa at its driest niche edge to investigate whether trees growing near their aridity limit were sensitive to the megadrought climatic pre-conditions, and were capable of informing predictive efforts. During the decade before the megadrought, trees in four populations revealed increases in the cellulose δ13C content of earlywood, latewood, and false latewood, which, based on past studies are correlated with increased intrinsic water-use efficiency. However, radial growth and cellulose δ18O were not sensitive to pre-megadrought conditions. During the 2 decades preceding the megadrought, at all four sites, the changes in δ13C were caused by the high sensitivity of needle carbon and water exchange to drought trends in key winter months, and for three of the four sites during crucial summer months. Such pre-megadrought physiological sensitivity appears to be unique for trees near their arid range limit, as similar patterns were not observed in trees in ten reference sites located along a latitudinal gradient in the same megadrought domain, despite similar drying trends. Our results reveal the utility of tree-ring δ13C to reconstruct spatiotemporal patterns during the organizational phase of a megadrought, demonstrating that trees near the arid boundaries of a species' distribution might be useful in the early detection of long-lasting droughts.

Vapor pressure deficit helps explain biogenic volatile organic compound fluxes from the forest floor and canopy of a temperate deciduous forest.

Biogenic volatile organic compounds (BVOCs) play critical roles in ecological and earth-system processes. Ecosystem BVOC models rarely include soil and litter fluxes and their accuracy is often challenged by BVOC dynamics during periods of rapid ecosystem change like spring leaf out. We measured BVOC concentrations within the air space of a mixed deciduous forest and used a hybrid Lagrangian/Eulerian canopy transport model to estimate BVOC flux from the forest floor, canopy, and whole ecosystem during spring. Canopy flux measurements were dominated by a large methanol source and small isoprene source during the leaf-out period, consistent with past measurements of leaf ontogeny and theory, and indicative of a BVOC flux situation rarely used in emissions model testing. The contribution of the forest floor to whole-ecosystem BVOC flux is conditional on the compound of interest and is often non-trivial. We created linear models of forest floor, canopy, and whole-ecosystem flux for each study compound and used information criteria-based model selection to find the simplest model with the best fit. Most published BVOC flux models do not include vapor pressure deficit (VPD), but it entered the best canopy, forest floor, and whole-ecosystem BVOC flux model more than any other study variable in the present study. Since VPD is predicted to increase in the future, future studies should investigate how it contributes to BVOC flux through biophysical mechanisms like evaporative demand, leaf temperature and stomatal function.

Leaf isoprene emission as a trait that mediates the growth-defense tradeoff in the face of climate stress.

Plant isoprene emissions are known to contribute to abiotic stress tolerance, especially during episodes of high temperature and drought, and during cellular oxidative stress. Recent studies have shown that genetic transformations to add or remove isoprene emissions cause a cascade of cellular modifications that include known signaling pathways, and interact to remodel adaptive growth-defense tradeoffs. The most compelling evidence for isoprene signaling is found in the shikimate and phenylpropanoid pathways, which produce salicylic acid, alkaloids, tannins, anthocyanins, flavonols and other flavonoids; all of which have roles in stress tolerance and plant defense. Isoprene also influences key gene expression patterns in the terpenoid biosynthetic pathways, and the jasmonic acid, gibberellic acid and cytokinin signaling networks that have important roles in controlling inducible defense responses and influencing plant growth and development, particularly following defoliation. In this synthesis paper, using past studies of transgenic poplar, tobacco and Arabidopsis, we present the evidence for isoprene acting as a metabolite that coordinates aspects of cellular signaling, resulting in enhanced chemical defense during periods of climate stress, while minimizing costs to growth. This perspective represents a major shift in our thinking away from direct effects of isoprene, for example, by changing membrane properties or quenching ROS, to indirect effects, through changes in gene expression and protein abundances. Recognition of isoprene's role in the growth-defense tradeoff provides new perspectives on evolution of the trait, its contribution to plant adaptation and resilience, and the ecological niches in which it is most effective.

Seasonal and diurnal trends in progressive isotope enrichment along needles in two pine species.

The Craig-Gordon type (C-G) leaf water isotope enrichment models assume a homogeneous distribution of enriched water across the leaf surface, despite observations that Δ18 O can become increasingly enriched from leaf base to tip. Datasets of this 'progressive isotope enrichment' are limited, precluding a comprehensive understanding of (a) the magnitude and variability of progressive isotope enrichment, and (b) how progressive enrichment impacts the accuracy of C-G leaf water model predictions. Here, we present observations of progressive enrichment in two conifer species that capture seasonal and diurnal variability in environmental conditions. We further examine which leaf water isotope models best capture the influence of progressive enrichment on bulk needle water Δ18 O. Observed progressive enrichment was large and equal in magnitude across both species. The magnitude of this effect fluctuated seasonally in concert with vapour pressure deficit, but was static in the face of diurnal cycles in meteorological conditions. Despite large progressive enrichment, three variants of the C-G model reasonably successfully predicted bulk needle Δ18 O. Our results thus suggest that the presence of progressive enrichment does not impact the predictive success of C-G models, and instead yields new insight regarding the physiological and anatomical mechanisms that cause progressive isotope enrichment.

High productivity in hybrid-poplar plantations without isoprene emission to the atmosphere.

Hybrid-poplar tree plantations provide a source for biofuel and biomass, but they also increase forest isoprene emissions. The consequences of increased isoprene emissions include higher rates of tropospheric ozone production, increases in the lifetime of methane, and increases in atmospheric aerosol production, all of which affect the global energy budget and/or lead to the degradation of air quality. Using RNA interference (RNAi) to suppress isoprene emission, we show that this trait, which is thought to be required for the tolerance of abiotic stress, is not required for high rates of photosynthesis and woody biomass production in the agroforest plantation environment, even in areas with high levels of climatic stress. Biomass production over 4 y in plantations in Arizona and Oregon was similar among genetic lines that emitted or did not emit significant amounts of isoprene. Lines that had substantially reduced isoprene emission rates also showed decreases in flavonol pigments, which reduce oxidative damage during extremes of abiotic stress, a pattern that would be expected to amplify metabolic dysfunction in the absence of isoprene production in stress-prone climate regimes. However, compensatory increases in the expression of other proteomic components, especially those associated with the production of protective compounds, such as carotenoids and terpenoids, and the fact that most biomass is produced prior to the hottest and driest part of the growing season explain the observed pattern of high biomass production with low isoprene emission. Our results show that it is possible to reduce the deleterious influences of isoprene on the atmosphere, while sustaining woody biomass production in temperate agroforest plantations.

Recent increases in drought frequency cause observed multi-year drought legacies in the tree rings of semi-arid forests.

Recent analyses on the length of drought recovery in forests have shown multi-year legacies, particularly in semi-arid, coniferous ecosystems. Such legacies are usually attributed to ecophysiological memory, although drought frequency itself, and its effect on overlapping recovery times, could also contribute. Here, we describe a multi-decadal study of drought legacies using tree-ring carbon-isotope ratios (δ13C) and ring-width index (RWI) in Pinus ponderosa at 13 montane sites traversing a winter-summer precipitation gradient in the Southwestern U.S. Sites and trees were selected to avoid collection biases that exist in archived tree-ring databanks. The spatial hydroclimate gradient and winter-summer seasonal patterns were well predicted by seasonal and inter-annual correlations between δ13C and atmospheric vapor pressure deficit (VPD). Using VPD, we found that the probability of extreme drought has increased up to 70% in this region during the past two decades. When the recent increase in drought frequency was not considered, multi-year legacies in both δ13C and RWI were observed at most sites. When the increase in drought frequency was detrended from tree-ring chronologies, some sites exhibited short legacies (1-2 years) in both δ13C and RWI, and there was a sight trend for longer legacies in RWI. However, when considered broadly across the region and multiple decades, no significant legacies were observed, which contrasts with past studies. Our results reveal that a contribution to observed multi-year legacies is related to shifts in the climate system itself, an exogenous factor, that must be considered along with physiological memory.

Disentangling seasonal and interannual legacies from inferred patterns of forest water and carbon cycling using tree-ring stable isotopes.

Tree-ring carbon and oxygen isotope ratios have been used to understand past dynamics in forest carbon and water cycling. Recently, this has been possible for different parts of single growing seasons by isolating anatomical sections within individual annual rings. Uncertainties in this approach are associated with correlated climate legacies that can occur at a higher frequency, such as across successive seasons, or a lower frequency, such as across years. The objective of this study was to gain insight into how legacies affect cross-correlation in the δ13 C and δ18 O isotope ratios in the earlywood (EW) and latewood (LW) fractions of Pinus ponderosa trees at thirteen sites across a latitudinal gradient influenced by the North American Monsoon (NAM) climate system. We observed that δ13 C from EW and LW has significant positive cross-correlations at most sites, whereas EW and LW δ18 O values were cross-correlated at about half the sites. Using combined statistical and mechanistic models, we show that cross-correlations in both δ13 C and δ18 O can be largely explained by a low-frequency (multiple-year) mode that may be associated with long-term climate change. We isolated, and statistically removed, the low-frequency correlation, which resulted in greater geographical differentiation of the EW and LW isotope signals. The remaining higher-frequency (seasonal) cross-correlations between EW and LW isotope ratios were explored using a mechanistic isotope fractionation-climate model. This showed that lower atmospheric vapor pressure deficits associated with monsoon rain increase the EW-LW differentiation for both δ13 C and δ18 O at southern sites, compared to northern sites. Our results support the hypothesis that dominantly unimodal precipitation regimes, such as near the northern boundary of the NAM, are more likely to foster cross-correlations in the isotope signals of EW and LW, potentially due to greater sharing of common carbohydrate and soil water resource pools, compared to southerly sites with bimodal precipitation regimes.

Carbon and oxygen isotope fractionations in tree rings reveal interactions between cambial phenology and seasonal climate.

We developed novel approaches for using the isotope composition of tree-ring subdivisions to study seasonal dynamics in tree-climate relations. Across a 30-year time series, the δ13 C and δ18 O values of the earlywood (EW) cellulose in the annual rings of Pinus ponderosa reflected relatively high intrinsic water-use efficiencies and high evaporative fractionation of 18 O/16 O, respectively, compared with the false latewood (FLW), summerwood (SW), and latewood (LW) subdivisions. This result is counterintuitive, given the spring origins of the EW source water and midsummer origins of the FLW, SW, and LW. With the use of the Craig-Gordon (CG), isotope-climate model revealed that the isotope ratios in all of the ring subdivision are explained by the existence of seasonal lags, lasting several weeks, between the initial formation of tracheids and the production of cellulosic secondary cell walls during maturation. In contrast to some past studies, modification of the CG model according to conventional methods to account for mixing of needle water between fractionated and nonfractionated sources did not improve the accuracy of predictions. Our results reveal new potential in the use of tree-ring isotopes to reconstruct past intra-annual tree-climate relations if lags in cambial phenology are reconciled with isotope ratio observations and included in theoretical treatments.

Some like it hot: the physiological ecology of C4 plant evolution.

The evolution of C4 photosynthesis requires an intermediate phase where photorespiratory glycine produced in the mesophyll cells must flow to the vascular sheath cells for metabolism by glycine decarboxylase. This glycine flux concentrates photorespired CO2 within the sheath cells, allowing it to be efficiently refixed by sheath Rubisco. A modest C4 biochemical cycle is then upregulated, possibly to support the refixation of photorespired ammonia in sheath cells, with subsequent increases in C4 metabolism providing incremental benefits until an optimized C4 pathway is established. 'Why' C4 photosynthesis evolved is largely explained by ancestral C3 species exploiting photorespiratory CO2 to improve carbon gain and thus enhance fitness. While photorespiration depresses C3 performance, it produces a resource (photorespired CO2) that can be exploited to build an evolutionary bridge to C4 photosynthesis. 'Where' C4 evolved is indicated by the habitat of species branching near C3-to-C4 transitions on phylogenetic trees. Consistent with the photorespiratory bridge hypothesis, transitional species show that the large majority of > 60 C4 lineages arose in hot, dry, and/or saline regions where photorespiratory potential is high. 'When' C4 evolved has been clarified by molecular clock analyses using phylogenetic data, coupled with isotopic signatures from fossils. Nearly all C4 lineages arose after 25 Ma when atmospheric CO2 levels had fallen to near current values. This reduction in CO2, coupled with persistent high temperature at low-to-mid-latitudes, met a precondition where photorespiration was elevated, thus facilitating the evolutionary selection pressure that led to C4 photosynthesis.

Beyond greenness: Detecting temporal changes in photosynthetic capacity with hyperspectral reflectance data.

Earth's future carbon balance and regional carbon exchange dynamics are inextricably linked to plant photosynthesis. Spectral vegetation indices are widely used as proxies for vegetation greenness and to estimate state variables such as vegetation cover and leaf area index. However, the capacity of green leaves to take up carbon can change throughout the season. We quantify photosynthetic capacity as the maximum rate of RuBP carboxylation (Vcmax) and regeneration (Jmax). Vcmax and Jmax vary within-season due to interactions between ontogenetic processes and meteorological variables. Remote sensing-based estimation of Vcmax and Jmax using leaf reflectance spectra is promising, but temporal variation in relationships between these key determinants of photosynthetic capacity, leaf reflectance spectra, and the models that link these variables has not been evaluated. To address this issue, we studied hybrid poplar (Populus spp.) during a 7-week mid-summer period to quantify seasonally-dynamic relationships between Vcmax, Jmax, and leaf spectra. We compared in situ estimates of Vcmax and Jmax from gas exchange measurements to estimates of Vcmax and Jmax derived from partial least squares regression (PLSR) and fresh-leaf reflectance spectroscopy. PLSR models were robust despite dynamic temporal variation in Vcmax and Jmax throughout the study period. Within-population variation in plant stress modestly reduced PLSR model predictive capacity. Hyperspectral vegetation indices were well-correlated to Vcmax and Jmax, including the widely-used Normalized Difference Vegetation Index. Our results show that hyperspectral estimation of plant physiological traits using PLSR may be robust to temporal variation. Additionally, hyperspectral vegetation indices may be sufficient to detect temporal changes in photosynthetic capacity in contexts similar to those studied here. Overall, our results highlight the potential for hyperspectral remote sensing to estimate determinants of photosynthetic capacity during periods with dynamic temporal variations related to seasonality and plant stress, thereby improving estimates of plant productivity and characterization of the associated carbon budget.

Climate controls over ecosystem metabolism: insights from a fifteen-year inductive artificial neural network synthesis for a subalpine forest.

Eddy covariance (EC) datasets have provided insight into climate determinants of net ecosystem productivity (NEP) and evapotranspiration (ET) in natural ecosystems for decades, but most EC studies were published in serial fashion such that one study's result became the following study's hypothesis. This approach reflects the hypothetico-deductive process by focusing on previously derived hypotheses. A synthesis of this type of sequential inference reiterates subjective biases and may amplify past assumptions about the role, and relative importance, of controls over ecosystem metabolism. Long-term EC datasets facilitate an alternative approach to synthesis: the use of inductive data-based analyses to re-examine past deductive studies of the same ecosystem. Here we examined the seasonal climate determinants of NEP and ET by analyzing a 15-year EC time-series from a subalpine forest using an ensemble of Artificial Neural Networks (ANNs) at the half-day (daytime/nighttime) time-step. We extracted relative rankings of climate drivers and driver-response relationships directly from the dataset with minimal a priori assumptions. The ANN analysis revealed temperature variables as primary climate drivers of NEP and daytime ET, when all seasons are considered, consistent with the assembly of past studies. New relations uncovered by the ANN approach include the role of soil moisture in driving daytime NEP during the snowmelt period, the nonlinear response of NEP to temperature across seasons, and the low relevance of summer rainfall for NEP or ET at the same daytime/nighttime time step. These new results offer a more complete perspective of climate-ecosystem interactions at this site than traditional deductive analyses alone.

Isoprene research - 60 years later, the biology is still enigmatic.

Isoprene emission is a major component of biosphere-atmosphere interactions. It is the single largest source of non-methane hydrocarbon in the atmosphere. The first report of isoprene emission from plants was published in 1957 by Professor Guivi Sanadze. While humans have smelled the monoterpene hydrocarbons made by coniferous trees since their earliest migrations, only in 1957 did the world became aware that other trees make a type of hydrocarbon in even greater amounts but one to which the human nose is much less sensitive. For this 60th anniversary of the first report of isoprene emission from leaves, we trace the discovery and development of the research field, highlighting some of the most seminal observations and theoretical interpretations. This is not an exhaustive review, and many important papers are not cited, but we hope it will be of general interest to read how research in this field developed, how new observations forced us to reevaluate our theories about the significance of isoprene biosynthesis to plant physiology and adaptation and how scientific serendipity can sometimes drive a topic forward.

Partitioning controls on Amazon forest photosynthesis between environmental and biotic factors at hourly to interannual timescales.

Gross ecosystem productivity (GEP) in tropical forests varies both with the environment and with biotic changes in photosynthetic infrastructure, but our understanding of the relative effects of these factors across timescales is limited. Here, we used a statistical model to partition the variability of seven years of eddy covariance-derived GEP in a central Amazon evergreen forest into two main causes: variation in environmental drivers (solar radiation, diffuse light fraction, and vapor pressure deficit) that interact with model parameters that govern photosynthesis and biotic variation in canopy photosynthetic light-use efficiency associated with changes in the parameters themselves. Our fitted model was able to explain most of the variability in GEP at hourly (R2  = 0.77) to interannual (R2  = 0.80) timescales. At hourly timescales, we found that 75% of observed GEP variability could be attributed to environmental variability. When aggregating GEP to the longer timescales (daily, monthly, and yearly), however, environmental variation explained progressively less GEP variability: At monthly timescales, it explained only 3%, much less than biotic variation in canopy photosynthetic light-use efficiency, which accounted for 63%. These results challenge modeling approaches that assume GEP is primarily controlled by the environment at both short and long timescales. Our approach distinguishing biotic from environmental variability can help to resolve debates about environmental limitations to tropical forest photosynthesis. For example, we found that biotically regulated canopy photosynthetic light-use efficiency (associated with leaf phenology) increased with sunlight during dry seasons (consistent with light but not water limitation of canopy development) but that realized GEP was nonetheless lower relative to its potential efficiency during dry than wet seasons (consistent with water limitation of photosynthesis in given assemblages of leaves). This work highlights the importance of accounting for differential regulation of GEP at different timescales and of identifying the underlying feedbacks and adaptive mechanisms.