Elevated atmospheric carbon dioxide concentrations alter root morphology and reduce the effectiveness of entomopathogenic nematodes

Abstract

The effects of increasing atmospheric carbon dioxide (CO2) concentrations on beneficial soil fauna, such as entomopathogenic nematodes (EPNs), are poorly understood. We hence aimed to characterize how elevated CO2 (eCO2) affects maize plant (Zea mays) growth, root morphology and the effectiveness of the EPN Heterorhabditis bacteriophora. We grew plants under ambient CO2 (aCO2; 400 μmol mol-1) and eCO2 (640 μmol mol-1) and quantified shoot growth and six root traits. We simultaneously quantified the effectiveness of EPNs (mortality of insect hosts (Galleria mellonella) and EPN density within hosts) when foraging in planted and plant-free environments. Structural equation modeling (SEM) was used to model direct and indirect relationships between atmospheric CO2, root morphology and EPN effectiveness. Root systems of plants grown under eCO2 grew faster, longer, denser, and larger than plants grown under aCO2. This in turn reduced EPN effectiveness as, despite no significant difference between aCO2 and eCO2 in host mortality, significantly more nematodes were recovered from hosts in the vicinity of plants grown in aCO2 environment. The SEM model revealed that this impact was indirect and mediated by the increased root morphological traits. We provide the first example of how changes in atmospheric CO2 indirectly reduce the effectiveness of an EPN used globally for crop protection. Other factors (e.g. plant volatile emissions) may moderate or exacerbate these patterns but our findings suggest that modifications in root traits at eCO2 negatively impact EPN effectiveness and therefore soil-dwelling insect pest management.