The role of root architecture in foraging behavior of entomopathogenic nematodes

- We documented the impact of root architecture on entomopathogenic nematodes behavior.
- Increasing complexity of model-roots reduced the performances of the nematodes.
- Root volatiles significantly led nematodes in the vicinity model-roots, even with high architectural complexity.
- Nematodes also moved along natural root systems.
- Root architecture not only impacts plants but also upper trophic levels.

As obligate parasites, entomopathogenic nematodes (EPN) rely on insect hosts to complete their development. In insect pest management, EPN infectiousness has varied a lot. A better understanding of their host-finding behavior in the rhizosphere is therefore crucial to enhance EPN potential in biological control. As previously demonstrated, roots can be used as a pathway to insect hosts by EPN, but this interaction and its impact on EPN foraging remain poorly documented. Three artificial model-roots with different degrees of complexity and connectivity were designed to investigate the impact of root architecture on foraging behavior of the EPN Heterorhabditis megidis. Insect baits were placed at the bottom of each model-root that was subsequently buried in moist sand. After injection of the EPN, the number of EPN-infected baits as well as the number of mature nematodes inside each individual carcass was recorded. The influence of insect-induced root volatiles was also evaluated by spiking the baits with a synthetic version of a natural insect-induced root cue. The ecological relevance of the results was tested in soil with two maize genotypes each exhibiting broadly different root architectures. H. megidi performed better in presence of model-roots. Foraging performances of H. megidis declined with the increasing model-root complexity. Adding the synthetic root volatile dramatically changed this pattern and favored the EPN on the most complex model-roots. H. megidis also moved in the vicinity of maize roots to find the insect baits in soil, and natural root architecture also tended to shape H. megidis foraging behavior. This study adds to the scarce body of literature characterizing physical and chemical interactions between EPN and roots. The present data illustrate that root architecture not only modifies plant quality but also shapes upper trophic levels' ecology.