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 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.

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.

Heterogeneous isotope effects decouple conifer leaf and branch sugar δO and δC.

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.

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.

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.

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.

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.

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 Δ 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.

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.

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 (δC) and ring-width index (RWI) in Pinus ponderosa at 13 montane sites traversing a winter-summer precipitation gradient in the Southwestern U.

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.

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 δ C and δ 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 O/ 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.

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

The evolution of C 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 CO within the sheath cells, allowing it to be efficiently refixed by sheath Rubisco. A modest C biochemical cycle is then upregulated, possibly to support the refixation of photorespired ammonia in sheath cells, with subsequent increases in C metabolism providing incremental benefits until an optimized C pathway is established.

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.

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.

Conifer Monoterpene Chemistry during an Outbreak Enhances Consumption and Immune Response of an Eruptive Folivore.

Changes in the chemical composition of plant defense compounds during herbivory can impact herbivore resource allocation patterns and thereby herbivore survival, growth, and immune response against endoparasitoid infection. Few studies have investigated folivore responses to changes in plant chemistry that occur under outbreak conditions in mature conifer systems. Using data from an earlier observational field study, we carried out laboratory bioassays to test how variation in monoterpenes in piñon pine trees (Pinus edulis, Pinaceae) during an outbreak affects growth, consumption, and immune response of a specialist herbivore, the Southwestern tiger moth (Lophocampa ingens, Arctiidae).

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 (R = 0.

Interactions between temperature and intercellular CO concentration in controlling leaf isoprene emission rates.

Plant isoprene emissions have been linked to several reaction pathways involved in atmospheric photochemistry. Evidence exists from a limited set of past observations that isoprene emission rate (I ) decreases as a function of increasing atmospheric CO concentration, and that increased temperature suppresses the CO effect. We studied interactions between intercellular CO concentration (C ) and temperature as they affect I in field-grown hybrid poplar trees in one of the warmest climates on earth - the Sonoran Desert of the southwestern United States.

Differential controls by climate and physiology over the emission rates of biogenic volatile organic compounds from mature trees in a semi-arid pine forest.

Drought has the potential to influence the emission of biogenic volatile organic compounds (BVOCs) from forests and thus affect the oxidative capacity of the atmosphere. Our understanding of these influences is limited, in part, by a lack of field observations on mature trees and the small number of BVOCs monitored. We studied 50- to 60-year-old Pinus ponderosa trees in a semi-arid forest that experience early summer drought followed by late-summer monsoon rains, and observed emissions for five BVOCs-monoterpenes, methylbutenol, methanol, acetaldehyde and acetone.