Abstract

Herbivore natural enemies protect plants by regulating herbivore populations. Whether they can alter the behavior of their prey to increase predation success is unknown. We investigate if and how infection by the entomopathogenic nematode Heterorhabditis bacteriophora changes the behavior of healthy larvae of the western corn rootworm (Diabrotica virgifera), a major pest of maize. We found that nematode-infected rootworm cadavers are attractive to rootworm larvae, and that this behavior increases nematode reproductive success. Nematode-infected rootworms release distinct volatile bouquets, including the unusual volatile butylated hydroxytoluene (BHT). BHT alone attracts rootworms, and increases nematode reproductive success. A screen of different nematode and herbivore species shows that attraction of healthy hosts to nematode-infected cadavers is widespread and likely involves species-specific volatile cues. This study reveals a new facet of the biology of herbivore natural enemies that boosts their predation success by increasing the probability of host encounters.

Highlights

  • Herbivore natural enemies such as predators, parasites and parasitoids play a key role in terrestrial ecosystems by reducing herbivore abundance (Vidal and Murphy, 2018)

  • We found WCR larvae were attracted to WCR cadavers infested by H. bacteriophora, H. beicherriana, H. georgiana and S. feltiae (Figure 6B), showing that attraction to cadavers occurs upon infestation with different Entomopathogenic nematodes (EPNs) species

  • Parasites with indirect life cycles are well known to be able to increase their transmission by manipulating host behavior (Poulin, 2012; Poulin and Maure, 2015), but the prevalence and importance of this phenomenon in parasites with direct life cycles, including herbivore natural enemies, remains largely unexplored

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Summary

Introduction

Herbivore natural enemies such as predators, parasites and parasitoids play a key role in terrestrial ecosystems by reducing herbivore abundance (Vidal and Murphy, 2018). In order to exert their effects, herbivore natural enemies need to make contact with their hosts. Natural enemies have evolved various behavioral strategies to maximize their chances for host encounters (Jackson and Pollard, 1996; Olberg et al, 2000; de Rijk et al, 2013; de Rijk et al, 2016). Predators and parasitoids for instance can use herbivore-induced plant volatiles to locate herbivores (Turlings et al, 1990). Herbivores on the other hand can detect and actively avoid contact with natural enemies (Lima and Dill, 1990). The interplay between behavioral adaptations of herbivores and natural enemies is likely to be an important determinant for the success of herbivore natural enemies and their capacity to suppress herbivore pests

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