Elevated atmospheric CO2 suppresses silicon accumulation and exacerbates endophyte reductions in plant phosphorus

Many temperate grasses are both hyper-accumulators of silicon (Si) and hosts of Epichloë fungal endophytes, functional traits which may alleviate environmental stresses such as herbivore attack. Si accumulation and endophyte infection may operate synergistically, but this has not been tested in a field setting, nor in the context of changing environmental conditions. Predicted increases in atmospheric CO2 concentrations can affect both Si accumulation and endophyte function, but these have not been studied in combination. We investigated how elevated atmospheric CO2 (eCO2), Si supplementation, endophyte-presence and insect herbivory impacted plant growth, stoichiometry (C, N, P and Si), leaf gas exchange (rates of photosynthesis, stomatal conductance, transpiration rates) and endophyte production of anti-herbivore defences (alkaloids) of an important pasture grass (tall fescue; Lolium arundinaceum) in the field. eCO2 and Si supplementation increased shoot biomass (+52% and +31%, respectively), whereas herbivory reduced shoot biomass by at least 35% and induced Si accumulation by 24%. Shoot Si concentrations, in contrast, decreased by 17%–21% under eCO2. Si supplementation and herbivory reduced shoot C concentrations. eCO2 reduced shoot N concentrations which led to increased shoot C:N ratios. Overall, shoot P concentrations were 26% lower in endophytic plants compared to non-endophytic plants, potentially due to decreased mass flow (i.e. observed reductions in stomatal conductance and transpiration). Alkaloid production was not discernibly affected by any experimental treatment. The negative impacts of endophytes on P uptake were particularly strong under eCO2. We show that eCO2 and insect herbivory reduce and promote Si accumulation, respectively, incorporating some field conditions for the first time. This indicates that these drivers operate in a more realistic ecological context than previously demonstrated. Reduced uptake of P in endophytic plants may adversely affect plant productivity in the future, particularly if increased demand for P due to improved plant growth under eCO2 cannot be met. Read the free Plain Language Summary for this article on the Journal blog. © 2023 The Authors. Functional Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society

Photosynthetic enhancement by elevated CO2 depends on seasonal temperatures for warmed and non-warmed Eucalyptus globulus trees

Arguments based on the biochemistry of photosynthesis predict a positive interaction between elevated atmospheric [CO2] and temperature on photosynthesis as well as growth. In contrast, few long-term studies on trees find greater stimulation of photosynthesis in response to elevated [CO2] at warmer compared with cooler temperatures. To test for CO2 × temperature interactions on leaf photosynthesis and whole-plant growth, we planted Eucalyptus globulus Labill. in climate-controlled chambers in the field at the Hawkesbury Forest Experiment research site, and investigated how photosynthetic enhancement changed across a range of seasonal temperatures. Trees were grown in a complete two-way factorial design with two CO2 concentrations (ambient and ambient + 240 ppm) and two temperatures (ambient and ambient + 3 °C) for 15 months until they reached ∼10 m height, after which they were harvested for biomass. There was significant enhancement of photosynthesis and growth with elevated [CO2], with the photosynthetic stimulation varying with season, but there was no significant effect of warming. Photosynthetic enhancement was higher in summer (+46% at 28 °C) than in winter (+14% at 20 °C). Photosynthetic enhancement as a function of leaf temperature was consistent with theoretical expectations, but was strongly mediated by the intercellular [CO2]/ambient [CO2] (Ci/Ca) ratio across seasons. Total tree biomass after 15 months was 66% larger in elevated CO2 (P = 0.017) with no significant warming effect detected. The fraction of biomass in coarse roots was reduced in warmed trees compared with ambient temperature controls, but there was no evidence of changed biomass allocation patterns in elevated CO2. We conclude that there are strong and consistent elevated CO2 effects on photosynthesis and biomass of E. globulus. It is crucial to consider stomatal conductance under a range of conditions to appraise the interactive effect of [CO2] and temperature on photosynthetic enhancement and subsequent implications for tree growth and forest productivity in future climates

Whole‐tree mesophyll conductance reconciles isotopic and gas‐exchange estimates of water‐use efficiency

Photosynthetic water-use efficiency (WUE) describes the link between terrestrial carbon (C) and water cycles. Estimates of intrinsic WUE (iWUE) from gas exchange and C isotopic composition (δ13C) differ due to an internal conductance in the leaf mesophyll (gm) that is variable and seldom computed. We present the first direct estimates of whole-tree gm, together with iWUE from whole-tree gas exchange and δ13C of the phloem (δ13Cph). We measured gas exchange, online 13C-discrimination, and δ13Cph monthly throughout spring, summer, and autumn in Eucalyptus tereticornis grown in large whole-tree chambers. Six trees were grown at ambient temperatures and six at a 3°C warmer air temperature; a late-summer drought was also imposed. Drought reduced whole-tree gm. Warming had few direct effects, but amplified drought-induced reductions in whole-tree gm. Whole-tree gm was similar to leaf gm for these same trees. iWUE estimates from δ13Cph agreed with iWUE from gas exchange, but only after incorporating gm. δ13Cph was also correlated with whole-tree 13C-discrimination, but offset by −2.5 ± 0.7‰, presumably due to post-photosynthetic fractionations. We conclude that δ13Cph is a good proxy for whole-tree iWUE, with the caveats that post-photosynthetic fractionations and intrinsic variability of gm should be incorporated to provide reliable estimates of this trait in response to abiotic stress

Climate warming and tree carbon use efficiency in a whole-tree 13 CO2 tracer study

Autotrophic respiration is a major driver of the global C cycle and may contribute a positive climate warming feedback through increased atmospheric concentrations of CO2 . The extent of this feedback depends on plants' ability to acclimate respiration to maintain a constant carbon use efficiency (CUE). We quantified respiratory partitioning of gross primary production (GPP) and CUE of field-grown trees in a long-term warming experiment (+3°C). We delivered a 13 C–CO2 pulse to whole tree crowns and chased that pulse in the respiration of leaves, whole crowns, roots, and soil. We also measured the isotopic composition of soil microbial biomass and the respiration rates of leaves and whole crowns. We documented homeostatic respiratory acclimation of foliar and whole-crown respiration rates; the trees adjusted to experimental warming such that leaf-level respiration rates were not increased. Experimental warming had no detectable impact on respiratory partitioning or mean residence times. Of the 13C label acquired by the trees, aboveground respiration consumed 10%, belowground respiration consumed 40%, and the remaining 50% was retained. Experimental warming of +3°C did not alter respiratory partitioning at the scale of entire trees, suggesting that complete acclimation of respiration to warming is likely to dampen a positive climate warming feedback

Whole-tree mesophyll conductance reconciles isotopic and gas-exchange estimates of water-use efficiency

Photosynthetic water-use efficiency (WUE) describes the link between terrestrial carbon (C) and water cycles. Estimates of intrinsic WUE (iWUE) from gas exchange and C isotopic composition (δ13C) differ due to an internal conductance in the leaf mesophyll (gm) that is variable and seldom computed. We present the first direct estimates of whole-tree gm, together with iWUE from whole-tree gas exchange and δ13C of the phloem (δ13Cph). We measured gas exchange, online 13C-discrimination, and δ13Cph monthly throughout spring, summer, and autumn in Eucalyptus tereticornis grown in large whole-tree chambers. Six trees were grown at ambient temperatures and six at a 3°C warmer air temperature; a late-summer drought was also imposed. Drought reduced whole-tree gm. Warming had few direct effects, but amplified drought-induced reductions in whole-tree gm. Whole-tree gm was similar to leaf gm for these same trees. iWUE estimates from δ13Cph agreed with iWUE from gas exchange, but only after incorporating gm. δ13Cph was also correlated with whole-tree 13C-discrimination, but offset by −2.5 ± 0.7‰, presumably due to post-photosynthetic fractionations. We conclude that δ13Cph is a good proxy for whole-tree iWUE, with the caveats that post-photosynthetic fractionations and intrinsic variability of gm should be incorporated to provide reliable estimates of this trait in response to abiotic stress

Using a paired tower approach and remote sensing to assess carbon sequestration and energy distribution in a heterogeneous sclerophyll forest

The critically endangered Cumberland Plain woodland within the greater Sydney metropolitan area hosts a dwindling refuge for melaleuca trees, an integral part of Australia's native vegetation. Despite their high carbon stocks, melaleucas have not explicitly been targeted for studies assessing their carbon sequestration potential, and especially little is known about their energy cycling or their response to increasing climate stress, precluding a holistic assessment of the resilience of Australia's forests to climate change. To improve our understanding of the role of melaleuca forest responses to climate stress, we combined forest inventory and airborne LiDAR data to identify species distribution and associated variations in forest structure, and deployed flux towers in a melaleuca-dominated (AU-Mel) and in a eucalypt-dominated (AU-Cum) stand to simultaneously monitor carbon and energy fluxes under typical growing conditions, as well as during periods with high atmospheric demand and low soil water content. We discovered that the species distribution at our study site affected the vertical vegetation structure, leading to differences in canopy coverage (75% at AU-Cum vs. 84% at AU-Mel) and plant area index (2.1 m2 m−2 at AU-Cum vs. 2.6 m2 m−2 at AU-Mel) that resulted in a heterogeneous forest landscape. Furthermore, we identified that both stands had comparable net daytime carbon exchange and sensible heat flux, whereas daytime latent heat flux (115.8 W m−2 at AU-Cum vs 119.4 W m−2 at AU-Mel, respectively) was higher at the melaleuca stand, contributing to a 0.3 °C decrease in air temperature and reduced vapor pressure deficit above the melaleuca canopy. However, increased canopy conductance and higher latent heat flux during moderate VPD or when soil moisture was low indicated a lack of water preservation at the melaleuca stand, highlighting the potential for increased vulnerability of melaleucas to projected hotter and drier future climates

No evidence of homeostatic regulation of leaf temperature in Eucalyptus parramattensis trees : integration of CO2 flux and oxygen isotope methodologies

Thermoregulation of leaf temperature (Tleaf) may foster metabolic homeostasis in plants, but the degree to which Tleaf is moderated, and under what environmental contexts, is a topic of debate. Isotopic studies inferred the temperature of photosynthetic carbon assimilation to be a constant value of c. 20°C; by contrast, leaf biophysical theory suggests a strong dependence of Tleaf on environmental drivers. Can this apparent disparity be reconciled? We continuously measured Tleaf and whole-crown net CO2 uptake for Eucalyptus parramattensis trees growing in field conditions in whole-tree chambers under ambient and +3°C warming conditions, and calculated assimilation-weighted leaf temperature (TL-AW) across 265 d, varying in air temperature (Tair) from −1 to 45°C. We compared these data to TL-AW derived from wood cellulose δ18O. Tleaf exhibited substantial variation driven by Tair, light intensity, and vapor pressure deficit, and Tleaf was strongly linearly correlated with Tair with a slope of c. 1.0. TL-AW values calculated from cellulose δ18O vs crown fluxes were remarkably consistent; both varied seasonally and in response to the warming treatment, tracking variation in Tair. The leaves studied here were nearly poikilothermic, with no evidence of thermoregulation of Tleaf towards a homeostatic value. Importantly, this work supports the use of cellulose δ18O to infer TL-AW, but does not support the concept of strong homeothermic regulation of Tleaf

The partitioning of gross primary production for young Eucalyptus tereticornis trees under experimental warming and altered water availability

The allocation of carbon (C) is an important component of tree physiology that influences growth and ecosystem C storage. Allocation is challenging to measure, and its sensitivity to environmental changes such as warming and altered water availability is uncertain. We exposed young Eucalyptus tereticornis trees to +3C warming and elimination of summer precipitation in the field using whole-tree chambers. We calculated C allocation terms using detailed measurements of growth and continuous whole-crown CO2 and water exchange measurements. Trees grew from small saplings to nearly 9m height during this 15-month experiment. Warming accelerated growth and leaf area development, and it increased the partitioning of gross primary production (GPP) to aboveground respiration and growth while decreasing partitioning below ground. Eliminating summer precipitation reduced C gain and growth but did not impact GPP partitioning. Trees utilized deep soil water and avoided strongly negative water potentials. Warming increased growth respiration, but maintenance respiration acclimated homeostatically. The increasing growth in the warmed treatment resulted in higher rates of respiration, even with complete acclimation of maintenance respiration. Warming-induced stimulations of tree growth likely involve increased C allocation above ground, particularly to leaf area development, whereas reduced water availability may not stimulate allocation to roots

Elevated CO2 alters the temperature sensitivity of stem CO2 efflux in a mature eucalypt woodland

The CO2 efflux from tree stem surfaces to atmosphere (RS) is an important component in the carbon (C) balance of forest ecosystems. Rising atmospheric carbon dioxide concentrations [CO2] are expected to stimulate RS, because of greater C assimilation and carbohydrate supply to stems under rising [CO2]. Growth respiration (Rg) and maintenance respiration (Rm) during the warm growing season may respond differently to rising [CO2] due to different metabolic demands. To test the effect of elevated [CO2] (eCO2, ambient +150 ppm) on RS, we examined RS in mature Eucalyptus trees on a monthly basis for an entire year during the seventh year of exposure to eCO2. RS varied seasonally and mirrored seasonal variation in temperature. While RS was not significantly increased under eCO2 compared to ambient CO2 (aCO2), its temperature sensitivity was significantly decreased (Q10 of 1.92 for aCO2 and 1.56 for eCO2). The estimated annual Rg accounted for approximately 7–8% of annual total RS, 419 ± 103 g C m− 2 yr-1, indicating that Rm contributes substantially to total RS in this mature woodland. Monthly mean RS was correlated with monthly mean soil temperature, soil moisture and monthly stem growth rate in this dry year, but soil moisture levels may have been insufficient to observe the impacts of eCO2 on stem growth in this droughted and phosphorous limited site. Our results highlight that eCO2 tends to increase Rm at low temperatures during the non-growing season, thus decreasing the temperature sensitivity of RS, despite a neutral effect of eCO2 on RS rates on a yearly basis

Does physiological acclimation to climate warming stabilize the ratio of canopy respiration to photosynthesis?

Given the contrasting short-term temperature dependences of gross primary production (GPP) and autotrophic respiration, the fraction of GPP respired by trees is predicted to increase with warming, providing a positive feedback to climate change. However, physiological acclimation may dampen or eliminate this response. We measured the fluxes of aboveground respiration (Ra), GPP and their ratio (Ra/GPP) in large, field-grown Eucalyptus tereticornis trees exposed to ambient or warmed air temperatures (+3°C). We report continuous measurements of whole-canopy CO2 exchange, direct temperature response curves of leaf and canopy respiration, leaf and branch wood respiration, and diurnal photosynthetic measurements. Warming reduced photosynthesis, whereas physiological acclimation prevented a coincident increase in Ra. Ambient and warmed trees had a common nonlinear relationship between the fraction of GPP that was respired above ground (Ra/GPP) and the mean daily temperature. Thus, warming significantly increased Ra/GPP by moving plants to higher positions on the shared Ra/GPP vs daily temperature relationship, but this effect was modest and only notable during hot conditions. Despite the physiological acclimation of autotrophic respiration to warming, increases in temperature and the frequency of heat waves may modestly increase tree Ra/GPP, contributing to a positive feedback between climate warming and atmospheric CO2 accumulation