Plant-associated CO2 mediates long-distance host location and foraging behaviour of a root herbivore.

Insect herbivores use different cues to locate host plants. The importance of CO2 in this context is not well understood. We manipulated CO2 perception in western corn rootworm (WCR) larvae through RNAi and studied how CO2 perception impacts their interaction with their host plant. The expression of a carbon dioxide receptor, DvvGr2, is specifically required for dose-dependent larval responses to CO2. Silencing CO2 perception or scrubbing plant-associated CO2 has no effect on the ability of WCR larvae to locate host plants at short distances (<9 cm), but impairs host location at greater distances. WCR larvae preferentially orient and prefer plants that grow in well-fertilized soils compared to plants that grow in nutrient-poor soils, a behaviour that has direct consequences for larval growth and depends on the ability of the larvae to perceive root-emitted CO2. This study unravels how CO2 can mediate plant-herbivore interactions by serving as a distance-dependent host location cue.

Living deep in the ground and surrounded by darkness, soil insects must rely on the chemicals released by plants to find the roots they feed on. Carbon dioxide, for example, is a by-product of plant respiration, which, above ground, is thought to attract moths to flowers and flies to apples; underground, however, its role is still unclear. This gaseous compound can travel through soil and potentially act as a compass for root-eating insects. Yet, it is also produced by decaying plants or animals, which are not edible. It is therefore possible that insects use this signal as a long-range cue to orient themselves, but then switch to another chemical when closer to their target to narrow in on an actual food source. To test this idea, Arce et al. investigated whether carbon dioxide guides the larvae of Western corn rootworm to maize roots. First, the rootworm genes responsible for sensing carbon dioxide were identified and switched off, making the larvae unable to detect this gas. When the genetically engineered rootworms were further than 9cm from maize roots, they were less able to locate that food source; closer to the roots, however, the insects could orient themselves towards the plant. This suggests that the insects use carbon dioxide at long distances but rely on another chemicals to narrow down their search at close range. To confirm this finding, Arce et al. tried absorbing the carbon dioxide using soda lime, leading to similar effects: carbon dioxide sensitive insects stopped detecting the roots at long but not short distances. Additional experiments then revealed that the compound could help insects find the best roots to feed on. Indeed, eating plants that grow on rich terrain ­ for instance, fertilized soils ­ helps insects to grow bigger and faster. These roots also release more carbon dioxide, in turn attracting rootworms more frequently. In the United States and Eastern Europe, Western corn rootworms inflict major damage to crops, highlighting the need to understand and manage the link between fertilization regimes, carbon dioxide release and how these pests find their food.

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

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.