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Hyperparasitoids are some of the most diverse members of insect food webs. True hyperparasitoids parasitize the larvae of other parasitoids, reaching these larvae with their ovipositor through the herbivore that hosts the parasitoid larva. During pupation, primary parasitoids also may be attacked by pseudohyperparasitoids that lay their eggs on the parasitoid (pre)pupae. By attacking primary parasitoids, hyperparasitoids may affect herbivore population dynamics, and they have been identified as a major challenge in biological control. Over the past decades, research, especially on aphid- and caterpillar-associated hyperparasitoids, has revealed that hyperparasitoids challenge rules on nutrient use efficiency in trophic chains, account for herbivore outbreaks, or stabilize competitive interactions in lower trophic levels, and they may use cues derived from complex interaction networks to locate their hosts. This review focuses on the fascinating ecology of hyperparasitoids related to how they exploit and locate their often inconspicuous hosts and the insect community processes in which hyperparasitoids are prominent players. [ABSTRACT FROM AUTHOR]

Insect hyperparasitoids are fourth trophic level organisms that commonly occur in terrestrial food webs, yet they are relatively understudied. These top‐carnivores can disrupt biological pest control by suppressing the populations of their parasitoid hosts, leading to pest outbreaks, especially in confined environments such as greenhouses where augmentative biological control is used. There is no effective eco‐friendly strategy that can be used to control hyperparasitoids. Recent advances in the chemical ecology of hyperparasitoid foraging behavior have opened opportunities for manipulating these top‐carnivores in such a way that biological pest control becomes more efficient. We propose various infochemical‐based strategies to manage hyperparasitoids. We suggest that a push‐pull strategy could be a promising approach to 'push' hyperparasitoids away from their parasitoid hosts and 'pull' them into traps. Additionally, we discuss how infochemicals can be used to develop innovative tools improving biological pest control (i) to restrict accessibility of resources (e.g. sugars and alternative hosts) to primary parasitoid only or (ii) to monitor hyperparasitoid presence in the crop for early detection. We also identify important missing information in order to control hyperparasitoids and outline what research is needed to reach this goal. Testing the efficacy of synthetic infochemicals in confined environments is a crucial step towards the implementation of chemical ecology‐based approaches targeting hyperparasitoids. © 2019 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. [ABSTRACT FROM AUTHOR]

Parasitoids depend on other insects for the development of their offspring. Their eggs are laid in or on a host insect that is consumed during juvenile development. Parasitoids harbor a diversity of microbial symbionts including viruses, bacteria, and fungi. In contrast to symbionts of herbivorous and hematophagous insects, parasitoid symbionts do not provide nutrients. Instead, they are involved in parasitoid reproduction, suppression of host immune responses, and manipulation of the behavior of herbivorous hosts. Moreover, recent research has shown that parasitoid symbionts such as polydnaviruses may also influence plant-mediated interactions among members of plant-associated communities at different trophic levels, such as herbivores, parasitoids, and hyperparasitoids. This implies that these symbionts have a much more extended phenotype than previously thought. This review focuses on the effects of parasitoid symbionts on direct and indirect species interactions and the consequences for community ecology. [ABSTRACT FROM AUTHOR]

Symbiotic relationships may provide organisms with key innovations that aid in the establishment of new niches. For example, during oviposition, some species of parasitoid wasps, whose larvae develop inside the bodies of other insects, inject polydnaviruses into their hosts. These symbiotic viruses disrupt host immune responses, allowing the parasitoid's progeny to survive. Here we show that symbiotic polydnaviruses also have a downside to the parasitoid's progeny by initiating a multitrophic chain of interactions that reveals the parasitoid larvae to their enemies. These enemies are hyperparasitoids that use the parasitoid progeny as host for their own offspring. We found that the virus and venom injected by the parasitoid during oviposition, but not the parasitoid progeny itself, affected hyperparasitoid attraction toward plant volatiles induced by feeding of parasitized caterpillars. We identified activity of virus-related genes in the caterpillar salivary gland. Moreover, the virus affected the activity of elicitors of salivary origin that induce plant responses to caterpillar feeding. The changes in caterpillar saliva were critical in inducing plant volatiles that are used by hyperparasitoids to locate parasitized caterpillars. Our results show that symbiotic organismsmay be key drivers of multitrophic ecological interactions. We anticipate that this phenomenon is widespread in nature, because of the abundance of symbiotic microorganisms across trophic levels in ecological communities. Their role should be more prominently integrated in community ecology to understand organization of natural and managed ecosystems, as well as adaptations of individual organisms that are part of these communities. [ABSTRACT FROM AUTHOR]

Infochemicals play an important role in structuring intra- and interspecific interactions. Many parasitoid wasp species rely on herbivory or oviposition-induced plant volatiles (HIPVs/OIPVs) to locate their herbivorous hosts, and must cope with variation in the volatile blends due to factors such as plant/host species, herbivore density or attack by several herbivores. However, little is known about how dual herbivory or changes in herbivore density affect multiple parasitoid species, each attacking a different herbivore, in the same system. In a natural system, we investigated the effect of dual attack on the ability of three parasitoid species to differentiate between volatiles induced by hosts and those induced by a combination of hosts and nonhosts. Black mustard, Brassica nigra, plants were infested with eggs or caterpillars of Pieris brassicae, alone or in combination with different densities of Brevicoryne brassicae aphids. We determined the ability of three different parasitoid species that parasitize either P. brassicae eggs (Trichogramma brassicae), caterpillars (Cotesia glomerata) or B. brassicae aphids (Diaeretiella rapae) to discriminate between the induced volatiles, and analysed the plant volatile blends. Dual infestation did not affect the parasitoid species equally and aphid infestation altered, in a density-dependent manner, the volatile-mediated foraging of all three parasitoid species. Chemical analyses of the volatile blends revealed nonlinear emission patterns in relation to aphid density in both plants attacked by aphids alone and in plants attacked by a combination of aphids and caterpillars. Simple correlations between behaviour and volatile emissions in pairwise comparisons suggest the importance of certain volatiles explaining attraction, whereas dose-response type analyses reveal that these simple correlation analyses provide an incomplete picture. [ABSTRACT FROM AUTHOR]