Leaf Induction Impacts Behavior and Performance of a Pollinating Herbivore

Flowering plants use volatiles to attract pollinators while deterring herbivores. Vegetative and floral traits may interact to affect insect behavior. Pollinator behavior is most likely influenced by leaf traits when larval stages interact with plants in different ways than adult stages, such as when larvae are leaf herbivores but adult moths visit flowers as pollinators. Here, we determine how leaf induction and corresponding volatile differences in induced plants influence behavior in adult moths and whether these preferences align with larval performance. We manipulated vegetative induction in four Nicotiana species. Using paired induced and control plants of the same species with standardized artificial flowers, we measured foraging and oviposition choices by their ecologically and economically important herbivore/pollinator, Manduca sexta. In parallel, we measured growth rates of M. sexta larvae fed leaves from control or induced plants to determine if this was consistent with female oviposition preference. Lastly, we used plant headspace collections and gas chromatography to quantify volatile compounds from both induced and control leaves to link changes in plant chemistry with moth behavior. In the absence of floral chemical cues, vegetative defensive status influenced adult moth foraging preference from artificial flowers in one species (N. excelsior), where females nectared from induced plants more often than control plants. Plant vegetative resistance consistently influenced oviposition choice such that moths deposited more eggs on control plants than on induced plants of all four species. This oviposition preference for control plants aligned with higher larval growth rates on control leaves compared with induced leaves. Control and induced plants of each species had similar leaf volatile profiles, but induced plants had higher emission levels. Leaves of N. excelsior produced the most volatile compounds, including some inducible compounds typically associated with floral scent. We demonstrate that vegetative plant defensive volatiles play a role in host plant selection and that insects assess information from leaves differently when choosing between nectaring and oviposition locations. These results underscore the complex interactions between plants, their pollinators, and herbivores.

Fitness Consequences of Oviposition Choice by an Herbivorous Insect on a Host Plant Colonized by an Endophytic Entomopathogenic Fungus

Entomopathogenic fungi (EPF), often considered as a bioinsecticide, are also able to colonize and establish a symbiotic relationship with plants as an endophyte. Recent studies demonstrated that endophytic EPF can enhance plant growth and are antagonistic to fungal pathogens. These newly emerging, but not yet fully understood, ecological roles suggest the possibility that EPF may further mediate oviposition preferences and offspring performance of an herbivorous insect. However, such EPF-mediated effects and underlying mechanisms are largely unexplored. Here, we examined the hypothesis that the endophytic EPF Beauveria bassiana can modulate oviposition behavior of the Asian corn borer Ostrinia furnacalis. We observed that O. furnacalis females preferred to lay eggs on B. bassiana inoculated maize plants. This is likely attributed to the net effects of plant volatile profiles induced by B. bassiana, with an increase in emitted amount of insect-attractive compounds 2-ethyl-1-hexanol and 3-hexen-1-ol and a decrease in insect-repellent compounds β-caryophyllene, naphthalene, and α-pinene. This finding provides an example of EPF-induced plant volatile-mediated interaction between plants and insects. However, fewer O. furnacalis larvae, pupae, and adults survived on the oviposition-preferred maize possibly due to lower plant nitrogen content. These results indicated that oviposition selection by O. furnacalis did not reflect the maximization of offspring fitness following B. bassiana inoculation. We suggest that fitness consequences of oviposition preferences should be considered when incorporating EPF as a biopesticide and as a potential biofertilizer within an integrated pest management programs.

Fitness Landscapes Reveal Context-Dependent Benefits of Oviposition Choice

Resource choice behaviour has enormous fitness consequences and can drive niche expansion. However, individual behavioural choices are often mediated by past experience. Are such context-dependent behaviours adaptive? Using the red flour beetle, we demonstrate that context-dependent oviposition choice indeed reflects distinct, context-specific local fitness peaks. Manipulating female egg allocation in a habitat containing optimal and novel resource patches, we measured offspring fitness to generate fitness landscapes as a function of all possible oviposition behaviours (i.e. combinations of fecundity and resource preference). Females from different age and density contexts exhibit distinct behaviours that optimize different fitness components. With increasing age and experienced population density, they produce few but fast-developing offspring that are advantageous under high resource competition; whereas young naive females produce many slow-developing offspring, which is beneficial under weak competition. Systematically mapping complete context-dependent fitness landscapes is thus critical to infer behavioural optimality, and offers predictive power in novel contexts.

Effects of water deficiency on preference and performance of an insect herbivore Ostrinia furnacalis

With further climate change still expected, it is predicted to increase the frequency with plants will be water stressed, which subsequently influences phytophagous insects, particularly Lepidoptera with limited mobility of larvae. Previous studies have indicated that oviposition preference and offspring performance of Lepidoptera insects are sensitive to drought separately. However, the integration of their two properties is not always seen. Here, we evaluated changes in oviposition selection and offspring fitness of a Lepidoptera insect under three water-stressed treatments using a model agroecosystem consisting of maize Zea mays, and Asian corn borer Ostrinia furnacalis. Results found that female O. furnacalis preferred to laying their eggs on well-watered maize, and then their offspring tended to survive better, attained bigger larvae mass, and developed more pupae and adults on the preferred maize. Oviposition selection of O. furnacalis positively correlated with height and leaf traits of maize, and offspring fitness positively related with water content and phytochemical traits of hosts. Overall, these results suggest that oviposition choice performed by O. furnacalis reflects the maximization of offspring fitness, supporting preference–performance hypothesis. This finding further highlights that the importance of simultaneous evaluation of performance and performance for water driving forces should be involved, in order to accurately predict population size of O. furnacalis under altered precipitation pattern.

Laboratory Oviposition Choice of Aedes aegypti (Diptera: Culicidae) From Kenya and Gabon: Effects of Conspecific Larvae, Salinity, Shading, and Microbiome

The mosquito Aedes aegypti (L.) is the primary vector of several arboviruses. Mosquito control and surveillance are essential to restrict disease transmission, the effectiveness of which depends on our understanding of the mosquito’s behaviors, including oviposition. Previous studies have identified a variety of oviposition cues. However, most of these studies involved only Ae. aegypti outside of the species’ native range, Africa. Populations outside Africa differ in their genetics and some behaviors from their African counterparts, suggesting possibly different oviposition preferences. Within Africa, Ae. aegypti can be found in both ancestral forest habitats and domestic habitats. The African domestic populations may represent an intermediate state between the forest and the truly domesticated non-African populations. Comparing mosquitoes from these three habitats (African forest, African domestic, and non-African domestic) might provide insight into the evolution of oviposition behavior. In this study, I examined the oviposition choices of multiple Ae. aegypti colonies from all three habitats in laboratory settings. I applied a two-choice assay to test four oviposition cues: the preexistence of conspecific larvae, salinity, shading, and microbiome. A subset of African colonies showed similar oviposition choices as their non-African counterparts, whereas the rest show little response to the factors tested. Within the African colonies, oviposition choices of the domestic colonies were significantly different from the forest colonies in most experiments. Yet, their preferences were not always intermediate between that of mosquitoes from the other two habitats. Collectively, this study adds to our understanding of Ae. aegypti oviposition, especially in previously understudied African populations.

Drosophila suzukii avoidance of microbes in oviposition choice

While the majority of Drosophila species lays eggs onto fermented fruits, females of Drosophila suzukii pierce the skin and lay eggs into ripening fruits using their serrated ovipositors. The changes of oviposition site preference must have accompanied this niche exploitation. In this study, we established an oviposition assay to investigate the effects of commensal microbes deposited by conspecific and heterospecific individuals and showed that the presence of microbes on the oviposition substrate enhances egg laying of Drosophila melanogaster and Drosophila biarmipes , but discourages that of D. suzukii . This result suggests that a drastic change has taken place in the lineage leading to D. suzukii in how females respond to chemical cues produced by microbes. We also found that hardness of the substrate, resembling that of either ripening or damaged and fermenting fruits, affects the response to microbial growth, indicating that mechanosensory stimuli interact with chemosensory-guided decisions to select or avoid oviposition sites.

Drosophila suzukii avoidance of microbes in oviposition choice

While the majority of Drosophila species lay eggs onto fermented fruits, females of D. suzukii pierce the skin and lay eggs into ripening fruits using their serrated ovipositors. The changes of oviposition site preference must have accompanied this niche exploitation. In this study, we established an oviposition assay to investigate the effects of commensal microbes deposited by conspecific and heterospecific individuals, and showed that presence of microbes on the oviposition substrate enhances egg-laying of D. melanogaster and D. biarmipes, but discourages that of D. suzukii. This result suggests that a drastic change has taken place in the lineage leading to D. suzukii in how females respond to chemical cues produced by microbes. We also found that hardness of the substrate affects the response to microbial growth, indicating that mechanosensory stimuli interact with chemosensory invoked decisions to select or avoid oviposition sites.

Oviposition of the mosquito Aedes aegypti in forest and domestic habitats in Africa

The theory of ecological divergence provides a useful framework to understand the adaptation of many species to anthropogenic (‘domestic’) habitats. The mosquito Aedes aegypti, a global vector of several arboviral diseases, presents an excellent study system. Ae. aegypti originated in African forests, but the populations that invaded other continents have specialized in domestic habitats. In its African native range, the species can be found in both forest and domestic habitats like villages. A crucial behavioral change between mosquitoes living in different habitats is their oviposition choices. Forest Ae. aegypti lay eggs in natural water containers like tree holes, while their domestic counterparts heavily rely on artificial containers such as plastic buckets. These habitat-specific containers likely have different environmental conditions, which could drive the incipient divergent evolution of oviposition in African Ae. aegypti. To examine this hypothesis, we conducted field research in two African locations, La Lopé, Gabon and Rabai, Kenya, where Ae. aegypti live in both forests and nearby villages. We first characterized a series of environmental conditions of natural oviposition sites, including physical characteristics, microbial density, bacterial composition, and volatile profiles. Our data showed that in both locations, environmental conditions of oviposition sites did differ between habitats. To examine potential behavioral divergence, we then conducted field and laboratory oviposition choice experiments to compare the oviposition preference of forest and village mosquitoes. The field experiment suggested that forest mosquitoes readily accepted artificial containers. In laboratory oviposition assays, forest and village mosquito colonies did not show a differential preference towards several conditions that featured forest versus village oviposition sites. Collectively, there is little evidence from our study that environmental differences lead to strong and easily measurable divergence in oviposition behavior between Ae. aegypti that occupy nearby forest and domestic habitats within Africa, despite clear divergence between African and non-African Ae. aegypti.

Evaluation of Trap Cropping for Control of Diamondback Moth (Lepidoptera: Plutellidae) in a Broccoli Production System

Trap cropping, in which a trap crop is planted near a cash crop, has been used successfully for reducing pest damage in some agricultural systems. We used a meta-analysis of extensive data on two trap cropping systems, diamondback moth, Plutella xylostella (Linnaeus), exploiting cabbage and Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) exploiting maize, to show that oviposition preference for, and high larval mortality on trap crops are important indicators of effectiveness of trap cropping systems. We then evaluated Indian mustard (Brassica juncea var. juncea L. Czern.) (Capparidales: Brassicaceae) and yellow rocket (Barbarea vulgaris W. T. Aiton) (Brassicales: Brassicaceae) as trap crops for protecting broccoli (Brassica oleracea var. italica Plenck) (Capparidales: Brassicaceae) against diamondback moth in Yuma, AZ, using planting configurations compatible with current practices for commercial production and without use of insecticides. In oviposition choice tests, both yellow rocket and Indian mustard were highly preferred over broccoli in the field. Furthermore, the number of larvae and pupae was significantly lower on yellow rocket and Indian mustard compared to broccoli, indicating relatively high mortality on these trap crops. Nevertheless, during the fall and spring growing seasons, no significant differences in the number of individuals on broccoli or proportion of broccoli crowns infested at harvest occurred between plots with trap crops relative to plots exclusively planted to broccoli. Thus, with the plant density and planting patterns used and without use of insecticides, there was no evidence that trap cropping was effective for reducing diamondback moth infestation of broccoli.