Unraveling the intraguild competition between Oscheius spp. nematodes and entomopathogenic nematodes: Implications for their natural distribution in Swiss agricultural soils

Entomopathogenic nematodes (EPN) are excellent biological control agents to fight soil-dwelling insect pests. In a previous survey of agricultural soils of Switzerland, we found mixtures of free-living nematodes (FLN) in the genus Oscheius, which appeared to be in intense competition with EPN. As this may have important implications for the long-term persistence of EPN, we studied this intraguild competition in detail. We hypothesized that (i) Oscheius spp. isolates act as scavengers rather than entomopathogens, and (ii) cadavers with relatively small numbers of EPN are highly suitable resources for Oscheius spp. reproduction. To study this, we identified Oscheius spp. isolated from Swiss soils, quantified the outcome of EPN/Oscheius competition in laboratory experiments, developed species-specific primers and probe for quantitative real-time PCR, and evaluated their relative occurrence in the field in the context of the soil food web. Molecular analysis (ITS/D2D3) identified MG-67/MG-69 as Oscheius onirici and MG-68 as O. tipulae (Dolichura-group). Oscheius spp. indeed behaved as scavengers, reproducing in ∼64% of frozen-killed cadavers from controlled experiments. Mixed infection in the laboratory by Oscheius spp. with low (3 IJs) or high (20 IJs) initial EPN numbers revealed simultaneous reproduction in double-exposed cadavers which resulted in a substantial reduction in the number of EPN progeny from the cadaver. This effect depended on the number of EPN in the initial inoculum and differed by EPN species; Heterorhabditis megidis was better at overcoming competition. This study reveals Oscheius spp. as facultative kleptoparasites that compete with EPN for insect cadavers. Using real-time qPCR, we were able to accurately quantify this strong competition between FLN and EPN in cadavers that were recovered after soil baiting (∼86% cadavers with >50% FLN production). The severe competition within the host cadavers and the intense management of the soils in annual crops readily explain the low EPN numbers in Swiss field samples. The developed molecular tools can be used to elucidate the extent to which the competitive interactions affect EPN populations. This can help to develop strategies to achieve good persistence and natural EPN recycling, in particular in systems where native EPN levels are low, such as annual crops.