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

Abstract

14Herbivore natural enemies, including predators, parasitoids and parasites, protect plants by 15 regulating herbivore populations. Some parasites can increase their transmission efficiency by 16 manipulating host behavior. Whether natural enemies can manipulate herbivore behavior to 17 increase top-down control, however, is unknown. Here, we investigate if and how the 18 entomopathogenic nematode Heterorhabditis bacteriophora, an important biocontrol agent, 19 modulates the behavior of the western corn rootworm, Diabrotica virgifera virgifera, a major 20 maize pest, and how these behavioral changes affect the capacity of the nematode to control the 21 rootworm. We found that healthy rootworm larvae are attracted to nematode-infected cadavers 22 shortly before the emergence of the next generation of nematodes. Nematode-infected rootworms 23 release distinct volatile bouquets, including butylated hydroxytoluene (BHT), which attracts 24 rootworms to infected cadavers. In a soil setting, BHT attracts rootworms and reduces nematode 25 resistance, resulting in increased infection rates and rootworm mortality as well as increased 26 nematode reproductive success. Five out of seven tested insect species were found to be attracted 27 to nematode-infected conspecifics, suggesting that attraction of healthy hosts to nematode-infected 28 cadavers is widespread. This study reveals a new facet of the biology of entomopathogenic 29 nematodes that increases their capacity to control a major root pest by increasing the probability of 30 host encounters. 31 Keywords: Belowground tritrophic interactions, entomopathogenic nematodes, prey attraction, 32 parasitism strategies, butylated hydroxytoluene 33 34Herbivore natural enemies such as predators, parasites and parasitoids play a key role in terrestrial 35 ecosystems by reducing herbivore abundance (1). Biological control relies on this form of top-36 down control to protect crops from herbivores (2). In order to exert their effects, herbivore natural 37 enemies need to make contact with their hosts. Natural enemies have evolved various behavioral 38 strategies to maximize their chance to encounter herbivores (3-6). Predators and parasitoids for 39 instance can use herbivore-induced plant volatiles to locate herbivores (7). Herbivores on the other 40 hand can detect and actively avoid contact with natural enemies (8). The interplay between 41 behavioral adaptations of herbivores and natural enemies is likely to be an important determinant 42 for the success of herbivore natural enemies and their capacity to suppress herbivore pests. 43A key step in the life of many herbivore natural enemies is the acquisition of new hosts once the 44 old host is exploited. Predators and parasitoids acquire new hosts by hunting, ambushing and 45 trapping them. Parasites with indirect life cycles can also facilitate the transfer to new hosts through 46 host manipulation strategies, including changes in color, smell and behavior of their current hosts 47 to attract alternate hosts (9-12). How p...