Entomopathogenic nematodes increase predation success by inducing specific cadaver volatiles that attract healthy herbivores

Abstract

Herbivore natural enemies, including predators, parasitoids and parasites, protect plants by regulating herbivore populations. Some parasites can increase their transmission efficiency by manipulating host behavior. Whether natural enemies can manipulate herbivore behavior to increase top-down control, however, is unknown. Here, we investigate if and how the entomopathogenic nematode Heterorhabditis bacteriophora, an important biocontrol agent, modulates the behavior of the western corn rootworm, Diabrotica virgifera virgifera, a major maize pest, and how these behavioral changes affect the capacity of the nematode to control the rootworm. We found that healthy rootworm larvae are attracted to nematode-infected cadavers shortly before the emergence of the next generation of nematodes. Nematode-infected rootworms release distinct volatile bouquets, including butylated hydroxytoluene (BHT), which attracts rootworms to infected cadavers. In a soil setting, BHT attracts rootworms and reduces nematode resistance, resulting in increased infection rates and rootworm mortality as well as increased nematode reproductive success. Five out of seven tested insect species were found to be attracted to nematode-infected conspecifics, suggesting that attraction of healthy hosts to nematode-infected cadavers is widespread. This study reveals a new facet of the biology of entomopathogenic nematodes that increases their capacity to control a major root pest by increasing the probability of host encounters.