Understanding insect foraging in complex habitats by comparing trophic levels: insights from specialist host-parasitoid-hyperparasitoid systems

Insects typically forage in complex habitats in which their resources are surrounded by non-resources. For herbivores, pollinators, parasitoids, and higher level predators research has focused on how specific trophic levels filter and integrate information from cues in their habitat to locate resources. However, these insights frequently build specific theory per trophic level and seldom across trophic levels. Here, we synthesize advances in understanding of insect foraging behavior in complex habitats by comparing trophic levels in specialist host-parasitoid-hyperparasitoid systems. We argue that resources may become less apparent to foraging insects when they are member of higher trophic levels and hypothesize that higher trophic level organisms require a larger number of steps in their foraging decisions. We identify important knowledge gaps of information integration strategies by insects that belong to higher trophic levels

Deciphering Plant-Insect-Microorganism Signals for Sustainable Crop Production

Agricultural crop productivity relies on the application of chemical pesticides to reduce pest and pathogen damage. However, chemical pesticides also pose a range of ecological, environmental and economic penalties. This includes the development of pesticide resistance by insect pests and pathogens, rendering pesticides less effective. Alternative sustainable crop protection tools should therefore be considered. Semiochemicals are signalling molecules produced by organisms, including plants, microbes, and animals, which cause behavioural or developmental changes in receiving organisms. Manipulating semiochemicals could provide a more sustainable approach to the management of insect pests and pathogens across crops. Here, we review the role of semiochemicals in the interaction between plants, insects and microbes, including examples of how they have been applied to agricultural systems. We highlight future research priorities to be considered for semiochemicals to be credible alternatives to the application of chemical pesticides

Within-individual phenotypic plasticity in flowers fosters pollination niche shift

Authors thank Raquel Sánchez, Angel Caravante, Isabel Sánchez Almazo, Tatiana López Pérez, Samuel Cantarero, María José Jorquera and Germán Fernández for helping us during several phases of the study and Iván Rodríguez Arós for drawing the insect silhouettes. This research is supported by grants from the Spanish Ministry of Science, Innovation and Universities (CGL2015-71634-P, CGL2015-63827-P, CGL2017-86626-C2-1-P, CGL2017- 86626-C2-2-P, UNGR15-CE-3315, including EU FEDER funds), Junta de Andalucía (P18- FR-3641), Xunta de Galicia (CITACA), BBVA Foundation (PR17_ECO_0021), and a contract grant to C.A. from the former Spanish Ministry of Economy and Competitiveness (RYC-2012-12277). This is a contribution to the Research Unit Modeling Nature, funded by the Consejería de Economía, Conocimiento, Empresas y Universidad, and European Regional Development Fund (ERDF), reference SOMM17/6109/UGR.Phenotypic plasticity, the ability of a genotype of producing different phenotypes when exposed to different environments, may impact ecological interactions. We study here how within-individual plasticity in Moricandia arvensis flowers modifies its pollination niche. During spring, this plant produces large, cross-shaped, UV-reflecting lilac flowers attracting mostly long-tongued large bees. However, unlike most co-occurring species, M. arvensis keeps flowering during the hot, dry summer due to its plasticity in key vegetative traits. Changes in temperature and photoperiod in summer trigger changes in gene expression and the production of small, rounded, UV-absorbing white flowers that attract a different assemblage of generalist pollinators. This shift in pollination niche potentially allows successful reproduction in harsh conditions, facilitating M. arvensis to face anthropogenic perturbations and climate change. Floral phenotypes impact interactions between plants and pollinators. Here, the authors show that Moricandia arvensis displays discrete seasonal plasticity in floral phenotype, with large, lilac flowers attracting long-tongued bees in spring and small, rounded, white flowers attracting generalist pollinators in summer.Spanish Ministry of Science, Innovation and Universities (EU FEDER funds) CGL2015-71634-P CGL2015-63827-P CGL2017-86626-C2-1-P CGL2017-86626-C2-2-P UNGR15-CE-3315Junta de Andalucia P18-FR-3641Xunta de GaliciaBBVA Foundation PR17_ECO_0021Spanish Ministry of Economy and Competitiveness RYC-2012-12277Consejeria de Economia, Conocimiento, Empresas y Universidad SOMM17/6109/UGREuropean Union (EU) SOMM17/6109/UG

En route to resources: Foraging strategies of plant‐associated insects to identify resources in complex dynamic environments

Abstract In plant‐associated communities, foraging insects aim to find different resources of interest. Herbivores look for the most nutritious plant tissues, pollinators for sweet nectar and protein‐rich pollen, and carnivores for their preferred prey. Although these foragers look for different resources, they face similar problems: resource cues are often highly variable and need to be detected in complex environments among non‐resources. Search templates—a subset of stimuli that is likely correlated with the occurrence of a particular resource—help foragers across trophic levels to find their resources. However, search‐template‐based foraging can also cause perception errors. Here, we synthesize knowledge on foraging by insects from functional groups belonging to different trophic levels to reveal common problems experienced by foragers and strategies to solve such problems. We focus mostly on volatile‐based foraging because this searching strategy is best studied across functional groups. We argue that search templates are both multimodal (including multiple trait types, e.g. odour and visual) and hierarchical (including multiple foraging steps). Search templates are plastic and updated by experience to match the dynamic foraging environment over time. By comparing insects from different functional groups spanning multiple trophic levels, we have identified important missing gaps on cue use and foraging strategies which should be addressed in the future in order to reduce knowledge asymmetries among functional groups about search‐template‐based foraging. We propose a way to achieve this goal arguing that studies on less well investigated functional groups can advance rapidly by borrowing, testing and adjusting already available hypotheses and theories formulated for other insect groups. Knowledge of search‐template‐based foraging across functional groups will give new insights into the evolution of foraging behaviour in complex ecological communities, help predict ecological consequences of large‐scale human‐made disturbances and help optimize insect‐delivered ecosystem services (pollination and biological control) in cropping systems. Read the free Plain Language Summary for this article on the Journal blog

Data from: Dealing with mutualists and antagonists: specificity of plant-mediated interactions between herbivores and flower visitors, and consequences for plant fitness

1. Plants need to deal with antagonists, such as herbivores, while maintaining interactions with mutualists, such as pollinators that help plants to maximize their reproductive output. Although many plant species have inducible defences to save metabolic costs of defence in the absence of herbivores, plant responses induced by herbivore attack can have ecological costs. For example, herbivore-induced responses can affect flower traits and alter interactions with flower visitors. Such plant-mediated interactions between herbivores and flower visitors can affect plant reproductive output. Current knowledge on the generality and specificity of plant-mediated herbivore-flower-visitor interactions and its consequences for plant fitness is limited. 2. In this study, we investigated whether a broad range of herbivores feeding on the annual plant Brassica nigra affect interactions with flower visitors, whether the direction of interactions is predicted by the feeding modes (chewing and sap-feeding) and sites (above- and belowground) of the herbivores, and whether it results in fitness consequences for the plant. 3. Our results show that attack of B. nigra by a range of different herbivores influenced plant interactions with mutualist pollinators and an antagonist florivore, the pollen beetle Meligethes aeneus. Pollinator community composition was affected by herbivory, whereas overall pollinator attraction was maintained. Pollinator community composition of uninfested plants differed from that of chewing and root herbivore-infested plants. Main responders in the pollinator communities to changes induced by herbivory were syrphid flies, bumblebees, and solitary bees. Although the preference of pollen beetle adults was not affected by herbivory, beetle larvae performed best on plants infested with the nematode Heterodera schachtii. The changes in pollinator community composition and syrphid fly visitation can explain the observed increase in seed set of root herbivore-infested plants. 4. Interactions of flowering B. nigra plants with mutualist and antagonist insects are well integrated and conflicting interactions do not reduce reproductive output. Our results suggest some degree of specificity in herbivore-flower-visitor interactions with consequences for plant fitness. Specificity of plant responses were determined at the species level as well as the herbivore functional group level , and differed depending on the flower visitor. Because plant reproduction was affected by indirect plant-mediated interactions, these can potentially result in selection on plant strategies to optimize growth, defence, and reproduction

A meta-analysis of herbivore effects on plant attractiveness to pollinators

Herbivores may directly or indirectly affect plant attractiveness to pollinators. Although several studies have reported on these effects, there is yet no general consensus on the strength and sign of such interactions or their contingency on herbivory features such as the plant tissue attacked. We performed a meta-analysis of studies testing for effects of herbivores on floral traits, plant attractiveness to pollinators, and plant reproductive success. We also assessed whether herbivore effects depended on the plant tissue attacked by herbivores and if real or simulated herbivory was used. We found an overall significant negative effect of herbivores on floral traits, plant attractiveness to pollinators, and plant reproductive success. These effects were, however, contingent on the plant tissue attacked and on whether real or simulated damage was used. Real floral and leaf, but not root, herbivores showed detrimental effects on floral traits and plant attractiveness to pollinators. In addition, real leaf, but not floral or root herbivory, lowered plant reproductive success. Contrastingly, simulated leaf and floral herbivory showed no effect on any of the response variables. These findings help move forward our understanding of the strength and directionality of herbivore effects on plant attractiveness to pollinators and their underlying mechanisms