Aboveground Herbivory Influences Belowground Defense Responses in Maize

The European corn borer (ECB; Ostrinia nubilalis) is an economically damaging insect pest of maize (Zea mays L.), an important cereal crop widely grown globally. Among inbred lines, the maize genotype Mp708 has shown resistance to diverse herbivorous insects, although several aspects of the defense mechanisms of Mp708 plants are yet to be explored. Here, the changes in root physiology arising from short-term feeding by ECB on the shoot tissues of Mp708 plants was evaluated directly using transcriptomics, and indirectly by monitoring changes in growth of western corn rootworm (WCR; Diabrotica virgifera virgifera) larvae. Mp708 defense responses negatively impacted both ECB and WCR larval weights, providing evidence for changes in root physiology in response to ECB feeding on shoot tissues. There was a significant downregulation of genes in the root tissues following short-term ECB feeding, including genes needed for direct defense (e.g., proteinase inhibitors and chitinases). Our transcriptomic analysis also revealed specific regulation of the genes involved in hormonal and metabolite pathways in the roots of Mp708 plants subjected to ECB herbivory. These data provide support for the long-distance signaling-mediated defense in Mp708 plants and suggest that altered metabolite profiles of roots in response to ECB feeding of shoots likely negatively impacted WCR growth.

Plant diversity effects on herbivory are mediated by soil biodiversity and plant chemistry

Insect herbivory is a key process in ecosystem functioning. While theory predicts that plant diversity modulates herbivory, the mechanistic links remain unclear. We postulated that the plant metabolome mechanistically links plant diversity and herbivory. In autumn and in spring, we assessed aboveground herbivory rates and plant metabolomes of seven plant species in experimental plant communities varying in plant species and resource acquisition strategy diversity. In the same plots, we also measured plant individual biomass as well as soil microbial and nematode community composition. Herbivory rates decreased with increasing plant species richness. Path modelling revealed that plant species richness and community resource acquisition strategy affected soil community composition. In particular, changes in nematode community composition affected plant metabolomes and thereby herbivory rates. These results provide experimental evidence that soil community composition plays an important role in reducing herbivory rates with increasing plant diversity by changing plant metabolomes.

Potato Tuberworm Phthorimaea operculella (Zeller) (Lepidoptera: Gelechioidea) Leaf Infestation Effects Performance of Conspecific Larvae on Harvested Tubers by Inducing Chemical Defenses

Conspecific aboveground and belowground herbivores can interact with each other, mediated by plant secondary chemicals; however, little attention has been paid to the interaction between leaf feeders and tuber-feeders. Here, we evaluated the effect of the foliar feeding of P. operculella larvae on the development of conspecific larvae feeding on harvested tubers by determining the nutrition and defense metabolites in the whole plant (leaf, root and tuber). We found that leaf feeding negatively affected tuber larval performance by increasing the female larval developmental time and reducing the male pupal weight. In addition, aboveground herbivory increased α-chaconine and glycoalkaloids in tubers and α-solanine in leaves, but decreased α-chaconine and glycoalkaloids in leaves. Aboveground herbivory also altered the levels of soluble sugar, soluble protein, starch, carbon (C), nitrogen (N), as well as the C:N ratio in both leaves and tubers. Aboveground P. operculella infestations could affect the performance of conspecific larvae feeding on harvested tubers by inducing glycoalkaloids in the host plant. Our findings indicate that field leaf herbivory should be considered when assessing the quality of potato tubers and their responses to pests during storage.

Aboveground herbivory increases soil nematode abundance of an invasive plant

Aims Plant invasions have the potential to affect the community structure of soil nematodes, but little is known about whether such effects are mediated by aboveground herbivores since invasive plants are not completely released from herbivores in the introduced range. In this study, we explored how aboveground insect herbivores mediated the effect of invasive plant Alternanthera philoxeroides on soil nematodes and examined the temporal variations of such an herbivory-elicited effect. Methods We conducted a greenhouse experiment by applying different herbivory treatments (no insect herbivores, specialist Agasicles hygrophila and generalist Cassida piperata) to potted A. philoxeroides, and then measured the community compositions of soil nematodes in corresponding pots on the 1st, 10th and 20th day after removal of all herbivores. In addition, the carbon content of roots and root exudate of A. philoxeroides were also measured. Important Findings Our results showed that aboveground herbivory significantly increased the abundance of soil nematodes of A. philoxeroides, likely plant feeder nematodes, after insect herbivores were removed immediately (1st day). However, such impacts waned with time and there was no significant difference at later stages (10th and 20th days). Furthermore, the effects of specialist A. hygrophila and generalist C. piperata herbivory were consistent on the abundance of soil nematodes. Overall, our results suggest that aboveground insect herbivores have the potential to alter the effects of plant invasions on soil nematodes, but such impacts are transient. Furthermore, our study highlighted the importance of integrating the effects of above- and belowground organisms when evaluating the impacts of plant invasions.

While shoot herbivory mitigates, root herbivory exacerbates eutrophication’s impact on diversity in a grassland model

1AbstractEutrophication is widespread throughout grassland systems and expected to increase during the Anthropocene. Trophic interactions, like aboveground herbivory, have been shown to mitigate its effect on plant diversity. Belowground herbivory may also impact these habitats’ response to eutrophication, but the direction of its influence is much less understood, and likely to depend on factors such as the herbivores’ preference for dominant species and the symmetry of belowground competition. If preferential towards the dominant, fastest growing species, root herbivores may reduce these species’ relative fitness and support diversity during eutrophication. However, as plant competition belowground is commonly considered to be symmetric, root herbivores may be less impactful than shoot herbivores because they do not reduce any competitive asymmetry between the dominant and subordinate plants.To better understand this system, we used an established, two-layer, grassland community model to run a full-factorially designed simulation experiment, crossing the complete removal of aboveground herbivores and belowground herbivores with eutrophication. After 100 years of simulation, we analyzed communities’ diversity, competition on the individual-level, as well as their resistance and recovery. The model reproduced both observed general effects of eutrophication in grasslands and the short-term trends of specific experiments. We found that belowground herbivores exacerbate the negative influence of eutrophication on Shannon diversity within our model grasslands, while aboveground herbivores mitigate its effect. Indeed, data on individuals’ above- and belowground resource uptake reveals that root herbivory reduces resource limitation belowground. As with eutrophication, this shifts competition aboveground. Since shoot competition is asymmetric—with larger, taller individuals gathering disproportionate resources compared to their smaller, shorter counterparts—this shift promotes the exclusion of the smallest species. While increasing the root herbivores’ preferences towards dominant species lessens their negative impact, at best they are only mildly advantageous, and they do very little reduce the negative consequences of eutrophication. Because our model’s belowground competition is symmetric, we hypothesize that root herbivores may be beneficial when root competition is asymmetric. Future research into belowground herbivory should account for the nature of competition belowground to better understand the herbivores’ true influence.