Mark A. Adams

Legumes are different: Leaf nitrogen, photosynthesis, and water use efficiency

Significance Leaf traits are used to drive models of global carbon fluxes and understand plant evolution. Many syntheses have highlighted relationships between plant leaf nitrogen and photosynthesis as evidence of a strong evolutionary drive to “intercept light and capture CO2.” Different from previous studies, we compiled a global dataset constrained to sites and studies where nitrogen-fixing plants (N2FP) and nonfixing species [other plants (OP)] could be directly compared. We show that photosynthesis is not related to leaf nitrogen for N2FP, irrespective of climate or growth form. N2FP have clear advantages in water use efficiency over OP. These findings contribute to a more complete explanation of global distributions of N2FP and can help improve models of global carbon and nitrogen cycles. Using robust, pairwise comparisons and a global dataset, we show that nitrogen concentration per unit leaf mass for nitrogen-fixing plants (N2FP; mainly legumes plus some actinorhizal species) in nonagricultural ecosystems is universally greater (43–100%) than that for other plants (OP). This difference is maintained across Koppen climate zones and growth forms and strongest in the wet tropics and within deciduous angiosperms. N2FP mostly show a similar advantage over OP in nitrogen per leaf area (Narea), even in arid climates, despite diazotrophy being sensitive to drought. We also show that, for most N2FP, carbon fixation by photosynthesis (Asat) and stomatal conductance (gs) are not related to Narea—in distinct challenge to current theories that place the leaf nitrogen–Asat relationship at the center of explanations of plant fitness and competitive ability. Among N2FP, only forbs displayed an Narea–gs relationship similar to that for OP, whereas intrinsic water use efficiency (WUEi; Asat/gs) was positively related to Narea for woody N2FP. Enhanced foliar nitrogen (relative to OP) contributes strongly to other evolutionarily advantageous attributes of legumes, such as seed nitrogen and herbivore defense. These alternate explanations of clear differences in leaf N between N2FP and OP have significant implications (e.g., for global models of carbon fluxes based on relationships between leaf N and Asat). Combined, greater WUE and leaf nitrogen—in a variety of forms—enhance fitness and survival of genomes of N2FP, particularly in arid and semiarid climates.

Simple models for stomatal conductance derived from a process model: cross-validation against sap flux data

Representation of stomatal physiology in models of plant-atmosphere gas exchange is minimal, and direct application of process-based models is limited by difficulty of parameter estimation. We derived simple models of stomatal conductance from a recent process-based model, and cross-validated them against measurements of sap flux (176-365 d in length) in 36 individual trees of two age classes for two Eucalyptus species across seven sites in the mountains of southeastern Australia. The derived models - which are driven by irradiance and evaporative demand and have two to four parameters that represent sums and products of biophysical parameters in the process model - reproduced a median 83-89% of observed variance in half-hourly and diurnally averaged sap flux, and performed similarly whether fitted using a random sample of all data or using 1 month of data from spring or autumn. Our simple models are an advance in predicting plant water use because their parameters are transparently related to reduced processes and properties, enabling easy accommodation of improved knowledge about how those parameters respond to environmental change and differ among species.

Diurnal patterns of water use in Eucalyptus victrix indicate pronounced desiccation-rehydration cycles despite unlimited water supply

Knowledge about nocturnal transpiration (E(night)) of trees is increasing and its impact on regional water and carbon balance has been recognized. Most of this knowledge has been generated in temperate or equatorial regions. Yet, little is known about E(night) and tree water use (Q) in semi-arid regions. We investigated the influence of atmospheric conditions on daytime (Q(day)) and nighttime water transport (Q(night)) of Eucalyptus victrix L.A.S. Johnson & K.D. Hill growing over shallow groundwater (not >1.5 m in depth) in semi-arid tropical Australia. We recorded Q(day) and Q(night) at different tree heights in conjunction with measurements of stomatal conductance (g(s)) and partitioned E(night) from refilling processes. Q of average-sized trees (200-400 mm diameter) was 1000-3000 l month(-1), but increased exponentially with diameter such that large trees (>500 mm diameter) used up to 8000 l month(-1). Q was remarkably stable across seasons. Water flux densities (J(s)) varied significantly at different tree heights during day and night. We show that g(s) remained significantly different from zero and E(night) was always greater than zero due to vapor pressure deficits (D) that remained >1.5 kPa at night throughout the year. Q(night) reached a maximum of 50% of Q(day) and was >0.03 mm h(-1) averaged across seasons. Refilling began during afternoon hours and continued well into the night. Q(night) eventually stabilized and closely tracked D(night). Coupling of Q(night) and D(night) was particularly strong during the wet season (R2u2009=u20090.95). We suggest that these trees have developed the capacity to withstand a pronounced desiccation-rehydration cycle in a semi-arid environment. Such a cycle has important implications for local and regional hydrological budgets of semi-arid landscapes, as large nighttime water fluxes must be included in any accounting.

Nocturnal water loss in mature subalpine Eucalyptus delegatensis tall open forests and adjacent E. pauciflora woodlands

We measured sap flux (S) and environmental variables in four monospecific stands of alpine ash (Eucalyptus delegatensis R. Baker, AA) and snowgum (E. pauciflora Sieb. ex Spreng., SG) in Australias Victorian Alps. Nocturnal S was 11.8 ± 0.8% of diel totals. We separated transpiration (E) and refilling components of S using a novel modeling approach based on refilling time constants. The nocturnal fraction of diel water loss (fn) averaged 8.6 ± 0.6% for AA and 9.8 ± 1.7% for SG; fn differed among sites but not species. Evaporative demand (D) was the strongest driver of nocturnal E (En). The ratio En/D (Gn) was positively correlated to soil moisture in most cases, whereas correlations between wind speed and Gn varied widely in sign and strength. Our results suggest (1) the large, mature trees at our subalpine sites have greater fn than the few Australian native tree species that have been studied at lower elevations, (2) AA and SG exhibit similar fn despite very different size and life history, and (3) fn may differ substantially among sites, so future work should be replicated across differing sites. Our novel approach to quantifying fn can be applied to S measurements obtained by any method.

Photosynthetic benefits of ultraviolet-A to Pimelea ligustrina, a woody shrub of sub-alpine Australia

The definition of photosynthetically active radiation (Q) as the visible waveband (λ 400–700xa0nm) is a core assumption of much of modern plant biology and global models of carbon and water fluxes. On the other hand, much research has focused on potential mutation and damage to leaves caused by ultraviolet (UV) radiation (280–400xa0nm), and anatomical and physiological adaptations that help avoid such damage. Even so, plant responses to UV-A are poorly described and, until now, photosynthetic utilization of UV-A has not been elucidated under full light conditions in the field. We found that the UV-A content of sunlight increased photosynthetic rates in situ by 12xa0% in Pimelea ligustrina Labill., a common and indigenous woody shrub of alpine ecosystems of the Southern Hemisphere. Compared to companion shrubs, UV-A-induced photosynthesis in P. ligustrina resulted from reduced physical and chemical capacities to screen UV-A at the leaf surface (illustrated by a lack of cuticle and reduced phenol index) and the resulting ability of UV-A to excite chlorophyll (Chl) a directly, and via energy provided by the carotenoid lutein. A screening of 55 additional sub-alpine species showed that 47xa0% of the plant taxa also display Chl a fluorescence under UV-A. If Chl a fluorescence indicates potential for photosynthetic gain, continued exclusion of UV-A from definitions of Q in this ecosystem could result in underestimates of measured and modeled rates of photosynthesis and miscalculation of potential for carbon sequestration. We suggest that carbon gain for alpine environs across the globe could be similarly underestimated given that UV-A radiation increases with altitude and that the frequently dominant herb and grass life-forms often transmit UV-A through the epidermis.

Disentangling respiratory acclimation and adaptation to growth temperature by Eucalyptus

• Respiratory acclimation to growth temperature differs between species, but underlying mechanisms are poorly understood. In the present study, we tested the hypothesis that respiratory acclimation of CO(2) release is a consequence of growth regulation such that growth rates of young foliage of Eucalyptus spp. are similar at contrasting growth temperatures. Further, we tested whether such a response is affected by adaptation of Eucalyptus to different thermal environments via growth at different altitudes in the Australian Alps. • We employed calorimetric methods to relate rates of CO(2) release (mainly from substrate oxidation) and rates of O(2) reduction to conservation of energy. Temperature responses of these processes provided insight into mechanisms that control energy conservation and expenditure, and helped define instantaneous enthalpic growth capacity (CapG). • CapG increased with altitude, but was counteracted by other factors in species adapted to highland habitats. The acclimation response was partly driven by changes in respiratory capacity (CapR(CO2)), and partly by more pronounced dynamic responses of CO(2) release (δ(R(CO2))) to measurement temperature. We observed enhanced temperature sensitivity of O(2) reduction (E(o)(R(O2))) at higher altitudes. • Adaptation to growth temperature included differences in respiration and growth capacities, but there was little evidence that Eucalyptus species vary in metabolic flexibility.

The Kok effect in Vicia faba cannot be explained solely by changes in chloroplastic CO2 concentration

The Kok effect - an abrupt decline in quantum yield (QY) of net CO2 assimilation at low photosynthetic photon flux density (PPFD) - is widely used to estimate respiration in the light (R), which assumes the effect is caused by light suppression of R. A recent report suggested much of the Kok effect can be explained by declining chloroplastic CO2 concentration (cc ) at low PPFD. Several predictions arise from the hypothesis that the Kok effect is caused by declining cc , and we tested these predictions in Vicia faba. We measured CO2 exchange at low PPFD, in 2% and 21% oxygen, in developing and mature leaves, which differed greatly in R in darkness. Our results contradicted each of the predictions based on the cc effect: QY exceeded the theoretical maximum value for photosynthetic CO2 uptake; QY was larger in 21% than 2% oxygen; and the change in QY at the Kok effect breakpoint was unaffected by oxygen. Our results strongly suggest the Kok effect arises largely from a progressive decline in R with PPFD that includes both oxygen-sensitive and -insensitive components. We suggest an improved Kok method that accounts for high cc at low PPFD.

Crops, Nitrogen, Water: Are Legumes Friend, Foe, or Misunderstood Ally?

Biological nitrogen fixation (BNF) by crop legumes reduces demand for industrial nitrogen fixation (INF). Nonetheless, rates of BNF in agriculture remain low, with strong negative feedback to BNF from reactive soil nitrogen (N) and drought. We show that breeding for yield has resulted in strong relationships between photosynthesis and leaf N in non-leguminous crops, whereas grain legumes show strong relations between leaf N and water use efficiency (WUE). We contrast these understandings with other studies that draw attention to the water costs of grain legume crops, and their potential for polluting the biosphere with N. We propose that breeding grain legumes for reduced stomatal conductance can increase WUE without compromising production or BNF. Legume crops remain a better bet than relying on INF.

Stomatal structure and physiology do not explain differences in water use among montane eucalypts

Understanding the regulation of water use at the whole-tree scale is critical to advancing the utility of physiological ecology, for example in its role in predictive hydrology of forested catchments. For three eucalypt species that dominate high-elevation catchments in south-eastern Australia, we examined if whole-tree water use could be related to three widely discussed regulators of water use: stomatal anatomy, sensitivity of stomata [i.e. stomatal conductance (gs)] to environmental influences, and sapwood area. While daily tree water use varied sixfold among species, sap velocity and sapwood area varied in parallel. Combined, stomatal structure and physiology could not explain differences in species-specific water use. Species which exhibited the fastest (Eucalyptus delegatensis) and slowest (Eucalyptus pauciflora) rates of water use both exhibited greater capacity for physiological control of gs [indicated by sensitivity to vapour pressure deficit (VPD)] and a reduced capacity to limit gs anatomically [indicated by greater potential gs (gmax)]. Conversely, gs was insensitive to VPD and gmax was lowest for Eucalyptus radiata, the species showing intermediate rates of water use. Improved knowledge of stomatal anatomy will help us to understand the capacity of species to regulate leaf-level water loss, but seems likely to remain of limited use for explaining rates of whole-tree water use in montane eucalypts at the catchment scale.

Anatomical and physiological regulation of post-fire carbon and water exchange in canopies of two resprouting Eucalyptus species.

The great majority of Eucalyptus spp. are facultative resprouters, and they dominate the eucalypt forests of Australia. Despite this numeric and geographic dominance, there is a general lack of knowledge of their capacity for carbon capture and water loss during canopy reinstation. After a crown-removing fire, we measured leaf-level determinants of carbon and water flux in resprouting canopies of Eucalyptus dives and E. radiata over the 3xa0years that followed. Leaf anatomy and physiology changed markedly during canopy reinstation, and leaves produced in the second year (2010) were distinct from those produced later. Leaves produced in 2010 were thicker (all measures of leaf anatomy), yet more porous (increased intercellular airspace), causing specific leaf area also to be greater. Indicators of heterotrophic activity, leaf respiration rate and light compensation point, were twofold greater in 2010, whereas all measures of photosynthetic capacity were greatest in leaves produced in 2011 and 2012. Whilst stomatal density, vein density and leaf hydraulic conductance all progressively decreased with time, neither leaf water status nor carbon isotope discrimination were affected. We conclude that canopy reinstation is primarily limited by pre-fire carbon stores, rather than by post-fire edaphic conditions (e.g., water availability), and thus argue that capacity for recovery is directly linked to pre-fire forest health.