Climate Change Modulates Multitrophic Interactions Between Maize, A Root Herbivore, and Its Enemies

How climate change will modify belowground tritrophic interactions is poorly understood, despite their importance for agricultural productivity. Here, we manipulated the three major abiotic factors associated with climate change (atmospheric CO2, temperature, and soil moisture) and investigated their individual and joint effects on the interaction between maize, the banded cucumber beetle (Diabrotica balteata), and the entomopathogenic nematode (EPN) Heterorhabditis bacteriophora. Changes in individual abiotic parameters had a strong influence on plant biomass, leaf wilting, sugar concentrations, protein levels, and benzoxazinoid contents. Yet, when combined to simulate a predicted climate scenario (Representative Concentration Pathway 8.5, RCP 8.5), their effects mostly counter-balanced each other. Only the sharp negative impact of drought on leaf wilting was not fully compensated. In both current and predicted scenarios, root damage resulted in increased leaf wilting, reduced root biomass, and reconfigured the plant sugar metabolism. Single climatic variables modulated the herbivore performance and survival in an additive manner, although slight interactions were also observed. Increased temperature and CO2 levels both enhanced the performance of the insect, but elevated temperature also decreased its survival. Elevated temperatures and CO2 further directly impeded the EPN infectivity potential, while lower moisture levels improved it through plant- and/or herbivore-mediated changes. In the RCP 8.5 scenario, temperature and CO2 showed interactive effects on EPN infectivity, which was overall decreased by 40%. We conclude that root pest problems may worsen with climate change due to increased herbivore performance and reduced top-down control by biological control agents.

Foliar Aphid Herbivory Alters the Tomato Rhizosphere Microbiome, but Initial Soil Community Determines the Legacy Effects

Aboveground herbivory can impact the root-associated microbiome, while simultaneously different soil microbial communities influence herbivore performance. It is currently unclear how these reciprocal top-down and bottom-up interactions between plants, insects and microbes vary across different soils and over successive plant generations. In this study, we examined top-down impacts of above-ground herbivory on the rhizosphere microbiome across different soils, assessed bottom-up impacts of soil microbial community variation on herbivore performance, and evaluated their respective contributions to soil legacy effects on herbivore performance. We used Macrosiphum euphorbiae (potato aphid) and Solanum pimpinellifolium (wild tomato) to capture pre-domestication microbiome interactions with a specialist pest. First, using 16S rRNA sequencing we compared bacterial communities associated with rhizospheres of aphid-infested and uninfested control plants grown in three different soils over three time points. High aphid infestation impacted rhizosphere bacterial diversity in a soil-dependent manner, ranging from a 22% decrease to a 21% increase relative to uninfested plants and explained 6–7% of community composition differences in two of three soils. We next investigated bottom-up and soil legacy effects of aphid herbivory by growing wild tomatoes in each of the three soils and a sterilized “no microbiome” soil, infesting with aphids (phase one), then planting a second generation (phase two) of plants in the soil conditioned with aphid-infested or uninfested control plants. In the first phase, aphid performance varied across plants grown in different soil sources, ranging from a 20 to 50% increase in aphid performance compared to the “no microbiome” control soil, demonstrating a bottom-up role for soil microbial community. In the second phase, initial soil community, but not previous aphid infestation, impacted aphid performance on plants. Thus, while herbivory altered the rhizosphere microbiome in a soil community-dependent manner, the bottom-up interaction between the microbial community and the plant, not top-down effects of prior herbivore infestation, affected herbivore performance in the following plant generation. These findings suggest that the bottom-up effects of the soil microbial community play an overriding role in herbivore performance in both current and future plant generations and thus are an important target for sustainable control of herbivory in agroecosystems.

Anti-herbivore silicon defences in a model grass are greatest under Miocene levels of atmospheric CO2

<p>Silicon (Si) has important role in mitigating diverse biotic and abiotic stresses, mainly via silicification of plant tissues. However, environmental changes such as reduced atmospheric CO<sub>2</sub> concentrations may affect grass Si concentration which, in turn, can alter herbivore performance. Recently, we demonstrated that pre-industrial atmospheric CO<sub>2</sub> increased Si accumulation in a grass, however, how Si is deposited and whether this affects insect herbivores performance is unknown. We, therefore, investigated how pre-industrial (reduced) (rCO<sub>2</sub>, 200 ppm), ambient (aCO<sub>2</sub>, 410 ppm) and elevated (eCO<sub>2</sub>, 640 ppm) CO<sub>2</sub> concentrations and Si-treatments (Si+ or Si-) affect Si accumulation in the model grass, <em>Brachypodium distachyon</em> and its subsequent effects on the performance of the global insect, <em>Helicoverpa armigera</em>. rCO<sub>2</sub> caused Si concentrations to increase by 29% and 36% compared to aCO<sub>2</sub> and eCO<sub>2</sub>, respectively. Furthermore, increased Si accumulation under rCO<sub>2</sub> decreased herbivore relative growth rate (RGR) by 120% relative to eCO<sub>2, </sub>whereas<sub></sub> rCO<sub>2</sub> caused herbivore RGR to decrease by 26% compared to eCO<sub>2</sub>. Moreover, Si supplementation increased the density of trichomes, silica and prickle cells, and these changes in leaf surface morphology reduced larval feeding performance. The observed negative correlation between macrohair density, silica cell density, prickle cell density and herbivore RGR supports this. To our knowledge, this is the first study to demonstrate that increased Si accumulation under pre-industrial CO<sub>2</sub> environment reduced the performance of this generalist insect herbivore performance.<strong> </strong>Contrastingly, we found  reduced Si accumulation under higher CO<sub>2</sub>, which suggests  that some grasses might become more susceptible to insect herbivore under the projected climate change scenarios.</p>

Ground Cover Vegetation Promotes Ecological Intensification of Pear Production

The use of ground cover vegetation is becoming a prominent intervention for promoting biodiversity and associated ecosystem services in Chinese orchards. Despite the large number of studies that have examined the effects of ground cover vegetation on promoting natural enemy populations and related natural pest control, it is less understood whether enhanced natural pest control translates to increase yield and reduced pesticide use. We conducted a 2-year experiment comparing three cover vegetation (ryegrass, clover, and hairy vetch) practices versus a bare ground control in commercial pear orchards in the Yangtze River Delta of East China (YRDEC), China. Natural enemy density (predator and parasitoid abundance), invertebrate herbivore performance (piercing-sucking herbivore abundance and branch-boring and fruit-boring percentage), pesticide input and pear fruit yield were recorded. The results indicated that cover vegetation decreased herbivore abundance and boring percentage by 49.95 and 63.6% respectively, and thus decreased pesticide use by 26.10%. Meanwhile, we found that cover vegetation increased the abundance of natural enemies by 620.75%, and increased pear fruit yield by 6.82%. Piecewise structural equation modelling indicated that increased natural enemy densities, decreased herbivore performance and pesticide use, while increasing fruit yield. Our results confirm that the use of ground cover vegetations (especially with clover and hairy vetch) can promote ecological intensification and biological pest control in pear orchards.

Data on Herbivore Performance and Plant Herbivore Damage Identify the Same Plant Traits as the Key Drivers of Plant–Herbivore Interaction

Data on plant herbivore damage as well as on herbivore performance have been previously used to identify key plant traits driving plant–herbivore interactions. The extent to which the two approaches lead to similar conclusions remains to be explored. We determined the effect of a free-living leaf-chewing generalist caterpillar, Spodoptera littoralis (Lepidoptera: Noctuidae), on leaf damage of 24 closely related plant species from the Carduoideae subfamily and the effect of these plant species on caterpillar growth. We used a wide range of physical defense leaf traits and leaf nutrient contents as the plant traits. Herbivore performance and leaf damage were affected by similar plant traits. Traits related to higher caterpillar mortality (higher leaf dissection, number, length and toughness of spines and lower trichome density) also led to higher leaf damage. This fits with the fact that each caterpillar was feeding on a single plant and, thus, had to consume more biomass of the less suitable plants to obtain the same amount of nutrients. The key plant traits driving plant–herbivore interactions identified based on data on herbivore performance largely corresponded to the traits identified as important based on data on leaf damage. This suggests that both types of data may be used to identify the key plant traits determining plant–herbivore interactions. It is, however, important to carefully distinguish whether the data on leaf damage were obtained in the field or in a controlled feeding experiment, as the patterns expected in the two environments may go in opposite directions.

Author Correction: Increased insect herbivore performance under elevated CO2 is associated with lower plant defence signalling and minimal declines in nutritional quality

An amendment to this paper has been published and can be accessed via a link at the top of the paper.