Abstract

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.

Highlights

  • 1.1 Importance of parasitoids in biological controlParasitoids are insects whose larvae develop in or on the bodies of other arthropods, whereas the adults are free living

  • Three different pheromones have been described so far for the aphid wileyonlinelibrary.com/journal/ps ecto-hyperparasitoid Dendrocerus carpenteri: (i) a volatile sex pheromone released by females that attracts males,[42] (ii) an external marking pheromone deposited on mummies after oviposition that prevents superparasitism,[43] and (iii) external marks applied on the substrate that reduce repeated exploration of previously visited patches.[44]

  • To exploit infochemicals in hyperparasitoid management strategies to enhance biological pest control, a more thorough understanding of their chemical ecology is needed. This will be challenging given the diversity of hyperparasitoid communities that may attack the parasitoid species used for biological control

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Summary

Importance of parasitoids in biological control

Parasitoids are insects whose larvae develop in or on the bodies of other arthropods (mostly other insects), whereas the adults are free living. Parasitoid guilds include specialized egg, egg-larval, larval, larval-pupal, pupal, and adult parasitoids Because they are much more specialized than most predators, parasitoids have been extensively used in biological control programs for over a century, with often quite spectacular success both in open field and protected cropping systems.[2] today, parasitoids are of tremendous importance in biological control of arthropod pests worldwide.[3] Well over 100 different species are commercially available for biological control of pest insects, making hymenopteran parasitoids the most diverse group of arthropod biocontrol agents. Parasitoids are very effective biocontrol agents of pest insects on ornamental or vegetable crops in greenhouses, including Encarsia spp. against whiteflies and Aphidius spp. against aphids In their native ranges, naturally occurring parasitoids are important in controlling herbivore populations, especially in cropping systems that are highly prone to pest infestations from native herbivores.

Hyperparasitoids are specialized natural enemies of parasitoids
IMPACT OF HYPERPARASITOIDS ON BIOLOGICAL CONTROL
Impact of hyperparasitoids on biological control programs
INFOCHEMICALS THAT CAN BE USED TO MANIPULATE HYPERPARASITOID BEHAVIOR
Push-pull strategies to manipulate hyperparasitoids
CONCLUSION AND FUTURE RESEARCH
Findings
Challenges and perspectives for infochemical-based hyperparasitoid management

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