‘Tuning’ communication among four trophic levels of the root biome to facilitate biological control

Abstract

Plants can facilitate attraction of herbivore predators and parasites with herbivore-induced volatiles (HIPVs). However, a central unknown of manipulating a natural environment is how the interactive effects of multiple plant stressors impacts belowground multi-trophic interactions. Agricultural systems, while disturbed, are useful model systems for investigating the effects of multiple stressors on plants and their related interactions because of the redundancy of pests and pathogens and thus, the predictability of the species occurring in these environments. Chemical communication among plants and animals belowground remains behind analogous current understanding of terrestrial systems both fundamentally, and from an applied perspective. Entomopathogenic nematodes (EPNs) infect and kill insects with the aid of symbiotic bacteria and can serve a biological control function in agro-ecosystems. EPNs are known to respond to herbivore-induced plant volatiles (HIPVs) that act as attractant cues increasing nematodes numbers in response to herbivory and concurrently increasing mortality of root pests. Microcosm and semi-field investigations have shown evidence that small scale numerical increases of EPN can be artificially caused by targeted applications or increases in HIPV production near the location of herbivore feeding. Community scale field experiments will be necessary to fully describe plant-herbivore-EPN interactions that also include other players such as plant parasitic nematodes (PPNs) and nematophagous fungi (NF), which may have unintended, negative consequences on plant production and natural enemy numerical response, respectively. Drawing upon the existing body of information on multi-trophic belowground communication, we propose development of a method to strategically and dynamically manipulate systems in a manner analogous to ‘tuning an audio mixer’ with hypothetical ‘knobs’ that could be adjusted by the user for human benefit. We suggest that biological control could be artificially up-regulated or down regulated by the action of a pest management practitioner using external forces such as HIPVs to regulate predator-prey interactions with the ultimate goal of sustainable plant production.