Parasitoid Causes Cascading Effects on Plant-Induced Defenses Mediated Through the Gut Bacteria of Host Caterpillars

Koinobiont endoparasitoid wasps whose larvae develop inside a host insect alter several important facets of host physiology, potentially causing cascading effects across multiple trophic levels. For instance, the hijacking of the host immune responses may have effects on how insects interact with host plants and microbial associates. However, the parasitoid regulation of insect–plant–microbiome interactions is still understudied. In this study, we used the fall armyworm (FAW), Spodoptera frugiperda, and the braconid parasitoid Cotesia marginiventris to evaluate impacts of parasitism on the gut microbiome of FAW larvae, and respective maize plant defense responses. The level of reactive oxygen species and the microbial community in larval gut underwent significant changes in response to parasitism, leading to a significant reduction of Enterococcus, while elevating the relative abundance of Pseudomonas. FAW with parasitism had lower glucose oxidase (GOX) activity in salivary glands and triggered lower defense responses in maize plants. These changes corresponded to effects on plants, as Pseudomonas inoculated larvae had lower activity of salivary GOX and triggered lower defense responses in maize plants. Our results demonstrated that parasitism had cascading effects on microbial associates across trophic levels and also highlighted that insect gut bacteria may contribute to complex interrelationships among parasitoids, herbivores, and plants.

Global Habitat Suitability of Spodoptera frugiperda (JE Smith) (Lepidoptera, Noctuidae): Key Parasitoids Considered for Its Biological Control

The present study is the first modeling effort at a global scale to predict habitat suitability of fall armyworm (FAW), Spodoptera frugiperda and its key parasitoids, namely Chelonus insularis, Cotesia marginiventris,Eiphosoma laphygmae,Telenomus remus and Trichogramma pretiosum, to be considered for biological control. An adjusted procedure of a machine-learning algorithm, the maximum entropy (Maxent), was applied for the modeling experiments. Model predictions showed particularly high establishment potential of the five hymenopteran parasitoids in areas that are heavily affected by FAW (like the coastal belt of West Africa from Côte d’Ivoire (Ivory Coast) to Nigeria, the Congo basin to Eastern Africa, Eastern, Southern and Southeastern Asia and some portions of Eastern Australia) and those of potential invasion risks (western & southern Europe). These habitats can be priority sites for scaling FAW biocontrol efforts. In the context of global warming and the event of accidental FAW introduction, warmer parts of Europe are at high risk. The effect of winter on the survival and life cycle of the pest in Europe and other temperate regions of the world are discussed in this paper. Overall, the models provide pioneering information to guide decision making for biological-based medium and long-term management of FAW across the globe.

Potential Impacts of Translocation of Neonicotinoid Insecticides to Cotton (Gossypium hirsutum (Malvales: Malvaceae)) Extrafloral Nectar on Parasitoids

Neonicotinoid seed treatments are frequently used in cotton (Gossypium hirsutum L. [Malvales: Malvaceae]) production to provide protection against early-season herbivory. However, there is little known about how these applications affect extrafloral nectar (EFN), an important food resource for arthropod natural enemies. Using enzyme-linked immunosorbent assays, we found that neonicotinoids were translocated to the EFN of clothianidin- and imidacloprid-treated, greenhouse-grown cotton plants at concentrations of 77.3 ± 17.3 and 122.6 ± 11.5 ppb, respectively. We did not find differences in the quantity of EFN produced by neonicotinoid-treated cotton plants compared to untreated controls, either constitutively or after mechanical damage. Metabolomic analysis of sugars and amino acids from treated and untreated plants did not detect differences in overall composition of EFN. In bioassays, female Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae) parasitoid wasps that fed on EFN from untreated, clothianidin-treated, or imidacloprid-treated plants demonstrated no difference in mortality or parasitization success. We also conducted acute toxicity assays for C. marginiventris fed on honey spiked with clothianidin and imidacloprid and established LC50 values for male and female wasps. Although LC50 values were substantially higher than neonicotinoid concentrations detected in EFN, caution should be used when translating these results to the field where other stressors could alter the effects of neonicotinoids. Moreover, there are a wide range of possible sublethal impacts of neonicotinoids, none of which were explored here. Our results suggest that EFN is a potential route of exposure of neonicotinoids to beneficial insects and that further field-based studies are warranted.

Species and sexual differences in behavioural responses of a specialist and generalist parasitoid species to host-related volatiles

The relationship between the degree of specialization of parasitoids and their responses to host-related volatiles is an important and current evolutionary question. Specialist parasitoids which have evolved to attack fewer host species are predicted to be more responsive to host-related volatiles than generalists. We tested the above prediction by comparing behavioural responses of both sexes of two parasitoids (Hymenoptera: Braconidae) with different degrees of host specificity, Microplitis croceipes (Cresson) (specialist) and Cotesia marginiventris (generalist), to different suites of synthetic host-related volatile compounds. The compounds tested at two doses (1 and 100μg) include two green leaf volatiles (GLVs: hexanal and (Z)-3-hexen-1-ol) and four herbivore-induced plant volatiles (HIPVs: (Z)-3-hexenyl acetate, linalool, (Z)-3-hexenyl butyrate and (E,E)-α-farnesene). Two hypotheses were tested: (i) M. croceipes (specialist) would show relatively greater behavioural responses to the HIPVs, whereas C. marginiventris (generalist) would show greater behavioural responses to the GLVs, and (ii) females of both species would show greater responses than conspecific males to the host-related volatiles. At the low dose (1μg), females of the specialist showed significantly greater responses than females of the generalist to three of the tested HIPVs, (Z)-3-hexenyl acetate, linalool and (Z)-3-hexenyl butyrate. In contrast, females of the generalist showed relatively greater responses to the GLVs. The same trends were recorded at the high dose but fewer significant differences were detected. In general, similar results were recorded for males, with the exception of linalool (an HIPV) which elicited significantly greater response in the generalist than the specialist. Comparing the sexes, females of both species showed greater responses than conspecific males to most of the tested volatiles. The ecological significance of these findings is discussed.