Effects of CO2 and temperature on Eucalyptus insect herbivores from individuals to communities

Atmospheric CO2 concentrations and temperatures are predicted to increase dramatically during this century. Changes in these environmental factors may impact insect herbivore physiology, abundance and community structure. In general, elevated CO2 (CE) reduces foliar nitrogen concentrations while increasing the carbon to nitrogen ratio. These changes in foliar chemistry often result in slower development and increased mortality of insect herbivores. Elevated temperatures (TE) can directly accelerate the development of insects by increasing their metabolic rates. TE may also indirectly impact insect herbivores through plant-mediated effects. CE and TE may have opposing or interactive effects on insect herbivores, so it is important to understand how concurrent changes to these two climate change factors impact herbivorous insects. Further to this, the impact of CE on insect herbivores and insect-mediated processes (such as herbivory and nutrient transfer) is rarely quantified in mature forests. Field sites present the opportunity to understand how insects in complex environments respond to CE under conditions that are difficult to simulate in greenhouse environments. The main and interactive effects of CE and TE were examined for an insect herbivore feeding on two different Eucalyptus species (chapter 2). Paropsis atomaria (Coleoptera: Chrysomelidae) fed on the flush leaves of either Eucalyptus tereticornis or Eucalyptus robusta in a greenhouse. CE reduced the nutritional quality of both Eucalyptus species, while TE increased foliar concentration of nitrogen in E. robusta only. Larval developmental time and leaf consumption increased while female pupal weight decreased at CE via plant-mediated effects. Larval survival increased at CE on E. robusta but decreased on E. tereticornis. TE only accelerated larval developmental time. No interactive effects between CE and TE were observed in this study indicating CE is a stronger driver of changes in insect growth and survival via plant-mediated effects than TE under the experimental conditions in this study. As an extension to examining the effects of CE and TE on the growth and development of an insect herbivore, the immune response of P. atomaria was also assessed when it was feeding on E. tereticornis under CE and TE conditions (chapter 3). The cellular (melanisation) and humoral (phenoloxidase or PO activity) components of the insect’s immune response to the implantation of a nylon filament was assessed and linked to changes in leaf chemistry. Haemolymph protein content and PO activity decreased at CE, however, the melanisation response increased at CE. TE had no effect on any immune parameters. Complex interactions of immune responses such as these occurring at CE may alter the outcomes of parasitoid or pathogen attack. Based on results obtained from these greenhouse studies (chapter 2 and 3), two field experiments were undertaken within a mature Eucalyptus woodland undergoing CO2 fumigation to investigate the effect of CE on herbivory and insect-mediated nutrient transfer. The impact of CE on insect-mediated nutrient cycling over two years at the Eucalyptus free-air enrichment (EucFACE) site is reported in chapter 4. CE did not impact the quantity or chemical composition of frass deposited at the site nor did it affect foliar nitrogen. Frass deposition showed a positive-lagged correlation with precipitation and average maximum temperatures likely linked to leaf phenology. CE may have a limited effect on insect-mediated nutrient cycling of mature forests in the short-term as the response of mature trees to CE may be lagged. The effect of CE on herbivory at the EucFACE site, and the role of leaf phenology on herbivory are reported in chapter 5. Young expanding leaves sustained significantly greater damage compared to fully-expanded or mature leaves. Thus, the availability of young expanding leaves drove monthly variations in leaf consumption. CE had no effect on leaf consumption or leaf age preference by herbivorous insects. Leaf phenology may be a significant factor in determining insect herbivory in sclerophyllous forests. Alterations in leaf phenology as a result of climate change may negatively impact insect herbivores particularly if insect phenology is synchronised with leaf phenology. The results of this Ph.D. research contribute to the understanding of (a) the main and interactive effects of CE and TE on the growth, development and immunity of insect herbivores; (b) the role of host-plant species in altering the response of insect herbivores to CE and TE; (c) the impact of CE on insect-mediated forest nutrient cycling and the interaction with rainfall and temperature; (d) the influence of leaf phenology and CE on leaf consumption. This work provides important information for the predictions of insect responses to CE and TE and this information is essential for the modelling of ecosystem responses. Results obtained from greenhouse studies in this thesis indicate insect herbivores may find refuge from the negative effects of CE in some growth, development and immunity traits particularly if they inhabit mixed-species forests. Furthermore, strong effects of CE on individuals of an important insect herbivore species of the EucFACE site in greenhouse experiments were not confirmed at herbivore community scales in the field due to complex interactions which may be unique to mature nutrient-limited forests

Silicon-induced root nodulation and synthesis of essential amino acids in a legume is associated with higher herbivore abundance

Ecologists have become increasingly aware that silicon uptake by plants, especially the Poaceae, can have beneficial effects on both plant growth and herbivore defence. The effects of silicon on other plant functional groups, such as nitrogen-fixing legumes, have been less well studied. Silicon could, however, indirectly promote herbivore performance in this group if reported increases in N2 fixation caused improvements in host plant quality for herbivores. We tested how silicon supplementation in the legume (Medicago sativa) affected plant growth rates, root nodulation and foliage quality (silicon content and amino acid profiles) for an insect herbivore (Acyrthosiphon pisum). Plants supplemented with silicon (Si+) grew three times as quickly as those without supplementation (Si−), almost entirely in shoot mass. While root growth was unaffected by silicon uptake, root nodules containing nitrogen-fixing bacteria were 44% more abundant on Si+ plants. Aphid abundance was twice as high on Si+ plants compared to Si− plants and was positively correlated with silicon-stimulated plant growth. Si+ plants accumulated more than twice as much silicon as Si− plants, but did not have higher silicon concentrations because of dilution effects linked to the rapid growth of Si+ plants. Si+ plants showed a 65% increase in synthesis of essential foliar amino acids, probably due to increased levels of root nodulation. These results suggest that increased silicon supply makes M. sativa more susceptible to A. pisum, mainly because of increased plant growth and resource availability (i.e. essential amino acids). While silicon augmentation of the Poaceae frequently improves herbivore defence, the current study illustrates that this cannot be assumed for other plant families where the beneficial effects of silicon on plant growth and nutrition may promote herbivore performance in some instances

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

Forest invertebrate communities and atmospheric change

Predicting the responses of invertebrate species, and the communities they form, to global change is one of the great challenges facing modern ecology. Invertebrates play vitally important roles in forests, underpinning fundamental ecosystem processes like nutrient cycling and pollination. Changes in the composition of our atmosphere, associated with increased levels of carbon dioxide (CO2) and ozone (O3), have the potential to affect the abundance, diversity and structure of invertebrate communities and the ecosystems they support. This chapter reviews the findings from the body of work looking at the responses of invertebrates to changes inCO2 and O3 concentrations with a special focus on the results from Free-Air Enrichment studies. The most consistent finding across the studies we review is the idiosyncratic nature of the responses of invertebrate species to the elevation of CO2 and/or O3. This finding can be explained to some extent by bottom-up and top-down processes. These include the species- and genotype-specific responses of host plant chemistry and differences in the abilities of individual insect species to physiologically and behaviourally overcome changes in resource quality. Although evidence is clearly mixed, certain general conclusions can be made regarding the influence of CO2 and/or O3 on invertebrates. Forest invertebrate herbivores tend to respond negatively to elevated concentrations of CO2. This response is likely due to diminished food-plant quality. Conversely, predators and parasitoids may benefit under enriched-CO2 conditions as prey susceptibility increases. Elevated O3 concentrations generally have opposing effects: herbivores show a tendency to consume more and develop faster while higher trophic levels experience declines in performance. Therefore, simultaneous elevation of both gases, such as is found in reality, may moderate the effects of either gas in isolation. There also appears to be some capacity for invertebrate communities to rebound over time, as evidenced by long-term studies. From the few community-level studies available, the current conclusion is that the structure of invertebrate communities will not be strongly disrupted by increases in CO2 and O3. This suggests that the ecosystem processes underpinned by these communities may be maintained under future atmospheres in these systems, though more work is needed. Looking forward, we emphasize the critical need for long-term studies of invertebrate responses at the population and community-level within natural systems. Such studies will be particularly important in tropical regions where no such information currently exists. Studies incorporating multiple climatic and atmospheric factors will also be of great value, such as those looking at the combined effects of atmospheric change and alterations in water availability. These studies will allow us to better predict the effects of future climates on these fundamental ecological systems

Root silicon

Data from silicon analysis of sugarcane roots. The 'plant' column is the identifier to be used in conjunction with the 'treatments' file for analysis

biomass

Biomass data from sugarcane plants. The column 'plant' is the identifier and can be used in conjunction with 'treatments' file for analysis

pot trial

Data from pot trial on insect performance including controls accounting for direct effects of treatments on insects

Cereal aphid performance and feeding behaviour largely unaffected by silicon enrichment of host plants

There is growing interest in using silicon (Si) for pest and disease management in cropping systems, notably in cereals which have the capacity to hyper-accumulate Si from the soil. Si-mediated pest resistance is thought to operate via physical and allelochemical mechanisms, but it is unclear whether phloem-feeders (e.g. aphids) are as adversely affected as chewing pests. To date, the role of Si in wheat (Triticum aestivum) against aphid pests has focussed almost exclusively on one species (Schizaphis graminum). We investigated the impacts of Si supplementation on plant growth and foliar chemistry (concentrations of carbon, nitrogen and Si) and associated changes in performance parameters of two global aphid pests (Rhopalosiphum maidis and Diuraphis noxia). In addition, we used electrical penetration graphs to determine how Si supplementation affected aphid feeding behaviour. Si supplementation increased foliar Si concentrations by 170% and decreased foliar C by c. 5%. Si impacts on aphid performance were only observed for D. noxia. Longevity and intrinsic rates of increase (rm) decreased by c. 8 days and were c. 13.5% lower, respectively, on Si-supplemented plants. The performance of R. maidis was unaffected by Si supplementation, and neither species was affected in terms of feeding behaviour. We conclude that Si enrichment of wheat is unlikely to be an effective pest control strategy for R. maidis and D. noxia. In reporting these findings, we aim to help identify patterns in Si-based crop resistance and inform future directions (e.g. alternative pest species) for research

treatments

Identifier file to allow allocation of 'plant' to treatment combinations for analysis

Leaf silicon

Data from silicon analysis of sugarcane leaves. The 'plant' column is the identifier to be used in conjunction with the 'treatments' file for analysis