Microbial competition for phosphorus limits the CO2 response of a mature forest.

The capacity for terrestrial ecosystems to sequester additional carbon (C) with rising CO2 concentrations depends on soil nutrient availability1,2. Previous evidence suggested that mature forests growing on phosphorus (P)-deprived soils had limited capacity to sequester extra biomass under elevated CO2 (refs. 3-6), but uncertainty about ecosystem P cycling and its CO2 response represents a crucial bottleneck for mechanistic prediction of the land C sink under climate change7. Here, by compiling the first comprehensive P budget for a P-limited mature forest exposed to elevated CO2, we show a high likelihood that P captured by soil microorganisms constrains ecosystem P recycling and availability for plant uptake. Trees used P efficiently, but microbial pre-emption of mineralized soil P seemed to limit the capacity of trees for increased P uptake and assimilation under elevated CO2 and, therefore, their capacity to sequester extra C. Plant strategies to stimulate microbial P cycling and plant P uptake, such as increasing rhizosphere C release to soil, will probably be necessary for P-limited forests to increase C capture into new biomass. Our results identify the key mechanisms by which P availability limits CO2 fertilization of tree growth and will guide the development of Earth system models to predict future long-term C storage.

The fate of carbon in a mature forest under carbon dioxide enrichment.

Atmospheric carbon dioxide enrichment (eCO2) can enhance plant carbon uptake and growth1-5, thereby providing an important negative feedback to climate change by slowing the rate of increase of the atmospheric CO2 concentration6. Although evidence gathered from young aggrading forests has generally indicated a strong CO2 fertilization effect on biomass growth3-5, it is unclear whether mature forests respond to eCO2 in a similar way. In mature trees and forest stands7-10, photosynthetic uptake has been found to increase under eCO2 without any apparent accompanying growth response, leaving the fate of additional carbon fixed under eCO2 unclear4,5,7-11. Here using data from the first ecosystem-scale Free-Air CO2 Enrichment (FACE) experiment in a mature forest, we constructed a comprehensive ecosystem carbon budget to track the fate of carbon as the forest responded to four years of eCO2 exposure. We show that, although the eCO2 treatment of +150 parts per million (+38 per cent) above ambient levels induced a 12 per cent (+247 grams of carbon per square metre per year) increase in carbon uptake through gross primary production, this additional carbon uptake did not lead to increased carbon sequestration at the ecosystem level. Instead, the majority of the extra carbon was emitted back into the atmosphere via several respiratory fluxes, with increased soil respiration alone accounting for half of the total uptake surplus. Our results call into question the predominant thinking that the capacity of forests to act as carbon sinks will be generally enhanced under eCO2, and challenge the efficacy of climate mitigation strategies that rely on ubiquitous CO2 fertilization as a driver of increased carbon sinks in global forests.

When resistance is futile, tolerate instead: silicon promotes plant compensatory growth when attacked by above- and belowground herbivores.

Plants have evolved numerous herbivore defences that are resistance- or tolerance-based. Resistance involves physical and chemical traits that deter and/or harm herbivores whereas tolerance minimizes fitness costs of herbivory, often via compensatory growth. The Poaceae frequently accumulate large amounts of silicon (Si), which can be used for herbivore resistance, including biomechanical and (indirectly) biochemical defences. To date, it is unclear whether Si improves tolerance of herbivory. Here we report how Si enabled a cereal (Triticum aestivum) to tolerate damage inflicted by above- and belowground herbivores. Leaf herbivory increased Si concentrations in the leaves by greater than 50% relative to herbivore-free plants, indicating it was an inducible defensive response. In plants without Si supplementation, leaf herbivory reduced shoot biomass by 52% and root herbivory reduced root biomass by 68%. Si supplementation, however, facilitated compensatory growth such that shoot losses were more than compensated for (+14% greater than herbivore-free plants) and root losses were minimized to -16%. Si supplementation did not improve plant resistance since Si did not enhance biomechanical resistance (i.e. force of fracture) or reduce leaf consumption and herbivore relative growth rates. We propose that Si-based defence operates in wheat via tolerance either in addition or as an alternative to resistance-based defence.

Benefits from Below: Silicon Supplementation Maintains Legume Productivity under Predicted Climate Change Scenarios.

Many studies demonstrate that elevated atmospheric carbon dioxide concentrations (eCO2) can promote root nodulation and biological nitrogen fixation (BNF) in legumes such as lucerne (Medicago sativa). But when elevated temperature (eT) conditions are applied in tandem with eCO2, a more realistic scenario for future climate change, the positive effects of eCO2 on nodulation and BNF in M. sativa are often much reduced. Silicon (Si) supplementation of M. sativa has also been reported to promote root nodulation and BNF, so could potentially restore the positive effects of eCO2 under eT. Increased nitrogen availability, however, could also increase host suitability for aphid pests, potentially negating any benefit. We applied eCO2 (+240 ppm) and eT (+4°C), separately and in combination, to M. sativa growing in Si supplemented (Si+) and un-supplemented soil (Si-) to determine whether Si moderated the effects of eCO2 and eT. Plants were either inoculated with the aphid Acyrthosiphon pisum or insect-free. In Si- soils, eCO2 stimulated plant growth by 67% and nodulation by 42%, respectively, whereas eT reduced these parameters by 26 and 48%, respectively. Aphids broadly mirrored these effects on Si- plants, increasing colonization rates under eCO2 and performing much worse (reduced abundance and colonization) under eT when compared to ambient conditions, confirming our hypothesized link between root nodulation, plant growth, and pest performance. Examined across all CO2 and temperature regimes, Si supplementation promoted plant growth (+93%), and root nodulation (+50%). A. pisum abundance declined sharply under eT conditions and was largely unaffected by Si supplementation. In conclusion, supplementing M. sativa with Si had consistent positive effects on plant growth and nodulation under different CO2 and temperature scenarios. These findings offer potential for using Si supplementation to maintain legume productivity under predicted climate change scenarios without making legumes more susceptible to insect pests.

Insect herbivory in a mature Eucalyptus woodland canopy depends on leaf phenology but not CO2 enrichment.

BACKGROUND: Climate change factors such as elevated atmospheric carbon dioxide concentrations (e[CO2]) and altered rainfall patterns can alter leaf composition and phenology. This may subsequently impact insect herbivory. In sclerophyllous forests insects have developed strategies, such as preferentially feeding on new leaf growth, to overcome physical or foliar nitrogen constraints, and this may shift under climate change. Few studies of insect herbivory at elevated [CO2] have occurred under field conditions and none on mature evergreen trees in a naturally established forest, yet estimates for leaf area loss due to herbivory are required in order to allow accurate predictions of plant productivity in future climates. Here, we assessed herbivory in the upper canopy of mature Eucalyptus tereticornis trees at the nutrient-limited Eucalyptus free-air CO2 enrichment (EucFACE) experiment during the first 19 months of CO2 enrichment. The assessment of herbivory extended over two consecutive spring-summer periods, with a first survey during four months of the [CO2] ramp-up phase after which full [CO2] operation was maintained, followed by a second survey period from months 13 to 19. RESULTS: Throughout the first 2 years of EucFACE, young, expanding leaves sustained significantly greater damage from insect herbivory (between 25 and 32 % leaf area loss) compared to old or fully expanded leaves (less than 2 % leaf area loss). This preference of insect herbivores for young expanding leaves combined with discontinuous production of new foliage, which occurred in response to rainfall, resulted in monthly variations in leaf herbivory. In contrast to the significant effects of rainfall-driven leaf phenology, elevated [CO2] had no effect on leaf consumption or preference of insect herbivores for different leaf age classes. CONCLUSIONS: In the studied nutrient-limited natural Eucalyptus woodland, herbivory contributes to a significant loss of young foliage. Leaf phenology is a significant factor that determines the level of herbivory experienced in this evergreen sclerophyllous woodland system, and may therefore also influence the population dynamics of insect herbivores. Furthermore, leaf phenology appears more strongly impacted by rainfall patterns than by e[CO2]. e[CO2] responses of herbivores on mature trees may only become apparent after extensive CO2 fumigation periods.

Boom and bust: rapid feedback responses between insect outbreak dynamics and canopy leaf area impacted by rainfall and CO2.

Frequency and severity of insect outbreaks in forest ecosystems are predicted to increase with climate change. How this will impact canopy leaf area in future climates is rarely tested. Here, we document function of insect outbreaks that fortuitously and rapidly occurred in an ecosystem under free-air CO2 enrichment. Over the first 2 years of CO2 fumigation of a naturally established mature Eucalyptus woodland, we continuously assessed population responses of three sap-feeding insect species of the psyllid genera Cardiaspina, Glycaspis and Spondyliaspis for up to ten consecutive generations. Concurrently, we quantified changes in the canopy leaf area index (LAI). Large and rapid shifts in psyllid community composition were recorded between species with either flush (Glycaspis) or senescence-inducing (Cardiaspina, Spondyliaspis) feeding strategies. Within the second year, two psyllid species experienced significant and rapid population build-up resulting in two consecutive outbreaks: first, rainfall stimulated Eucalyptus leaf production increasing LAI, which supported population growth of flush-feeding Glycaspis without impacting LAI. Glycaspis numbers then crashed and were followed by the outbreak of senescence-feeding Cardiaspina fiscella that led to significant defoliation and reduction in LAI. For all three psyllid species, the abundance of lerps, protective coverings excreted by the sessile nymphs, decreased at e[CO2 ]. Higher lerp weight at e[CO2 ] for Glycaspis but not the other psyllid species provided evidence for compensatory feeding by the flush feeder but not the two senescence feeders. Our study demonstrates that rainfall drives leaf phenology, facilitating the rapid boom-and-bust succession of psyllid species, eventually leading to significant defoliation due to the second but not the first outbreaking psyllid species. In contrast, e[CO2 ] may impact psyllid abundance and feeding behaviour, with psyllid species-specific outcomes for defoliation severity, nutrient transfer and trophic cascades. Psyllid populations feeding on Eucalyptus experience rapid boom-and-bust cycles depending on availability of suitable foliage driven by rainfall patterns and leaf phenology.

Climate change, nutrition and immunity: Effects of elevated CO2 and temperature on the immune function of an insect herbivore.

Balanced nutrition is fundamental to health and immunity. For herbivorous insects, nutrient-compositional shifts in host plants due to elevated atmospheric CO2 concentrations and temperature may compromise this balance. Therefore, understanding their immune responses to such shifts is vital if we are to predict the outcomes of climate change for plant-herbivore-parasitoid and pathogen interactions. We tested the immune response of Paropsis atomaria Olivier (Coleoptera: Chrysomelidae) feeding on Eucalyptus tereticornis Sm. seedlings exposed to elevated CO2 (640 µmol mol(-1); CE) and temperature (ambient plus 4 °C; TE). Larvae were immune-challenged with a nylon monofilament in order to simulate parasitoid or pathogen attack without other effects of actual parasitism or pathology. The cellular (in vivo melanisation) and humoral (in vitro phenoloxidase PO activity) immune responses were assessed, and linked to changes in leaf chemistry. CE reduced foliar nitrogen (N) concentrations and increased C:N ratios and concentrations of total phenolics. The humoral response was reduced at CE. PO activity and haemolymph protein concentrations decreased at CE, while haemolymph protein concentrations were positively correlated with foliar N concentrations. However, the cellular response increased at CE and this was not correlated with any foliar traits. Immune parameters were not impacted by TE. Our study revealed that opposite cellular and humoral immune responses occurred as a result of plant-mediated effects at CE. In contrast, elevated temperatures within the tested range had minimal impact on immune responses. These complex interactions may alter the outcomes of parasitoid and pathogen attack in future climates.

Amino acid-mediated impacts of elevated carbon dioxide and simulated root herbivory on aphids are neutralized by increased air temperatures.

Changes in host plant quality, including foliar amino acid concentrations, resulting from global climate change and attack from multiple herbivores, have the potential to modify the pest status of insect herbivores. This study investigated how mechanically simulated root herbivory of lucerne (Medicago sativa) before and after aphid infestation affected the pea aphid (Acyrthosiphon pisum) under elevated temperature (eT) and carbon dioxide concentrations (eCO2). eT increased plant height and biomass, and eCO2 decreased root C:N. Foliar amino acid concentrations and aphid numbers increased in response to eCO2, but only at ambient temperatures, demonstrating the ability of eT to negate the effects of eCO2. Root damage reduced aboveground biomass, height, and root %N, and increased root %C and C:N, most probably via decreased biological nitrogen fixation. Total foliar amino acid concentrations and aphid colonization success were higher in plants with roots cut early (before aphid arrival) than those with roots cut late (after aphid arrival); however, this effect was counteracted by eT. These results demonstrate the importance of amino acid concentrations for aphids and identify individual amino acids as being potential factors underpinning aphid responses to eT, eCO2, and root damage in lucerne. Incorporating trophic complexity and multiple climatic factors into plant-herbivore studies enables greater insight into how plants and insects will interact in the future, with implications for sustainable pest control and future crop security.

Responses of leaf beetle larvae to elevated [CO2] and temperature depend on Eucalyptus species.

It is essential to understand the combined effects of elevated [CO2] and temperature on insect herbivores when attempting to forecast climate change responses of diverse ecosystems. Plant species differ in foliar chemistry, and this may result in idiosyncratic plant-mediated responses of insect herbivores at elevated [CO2] and temperature. We measured the response of the eucalypt leaf beetle Paropsis atomaria (Coleoptera: Chrysomelidae) feeding on Eucalyptus tereticornis and Eucalyptus robusta. Seedlings were grown at ambient (400 µmol mol(-1)) or elevated (640 µmol mol(-1)) [CO2] and ambient (26/18 °C day/night) or elevated (ambient + 4 °C) temperature in a greenhouse for 7 months. Larvae fed on flush leaves from egg hatch to pupation while being directly exposed to these conditions. Elevated [CO2] reduced foliar [N] and [P], while it increased total nonstructural carbohydrates and the C:N ratio. Elevated temperature increased foliar [N] in E. robusta but not E. tereticornis. Plant-mediated effects of elevated [CO2] reduced female pupal weight and increased developmental time and leaf consumption. Larval survival at elevated [CO2] was impacted differently by the two host plant species; survival increased on E. robusta while it decreased on E. tereticornis. Elevated temperature accelerated larval development but did not impact other insect parameters. We did not detect a CO2 × temperature interaction, suggesting that elevated temperature as a combined direct and plant-mediated effect may not be able to ameliorate the negative plant-mediated effects of elevated [CO2] on insect herbivores. Our study highlighted host-plant-specific responses of insect herbivores to climate change factors that resulted in host-plant-specific survival.