Contribution of anecic and epigeic earthworms to biological control of Fusarium graminearum in wheat straw

Earthworms have proved to contribute to plant health indirectly, by improvement of soil physical and chemical properties, as well as directly, through suppression of plant pathogens. Fusarium Head Blight, caused primarily by Fusarium graminearum, is one of the most important cereal diseases, with severe detrimental effects on yield and grain quality worldwide, and significant effect on grain safety due to the accumulation of mycotoxins produced by the fungus. Earthworms could reduce the residue-borne inoculum density of F. graminearum through different mechanisms, including direct competition by residue consumption, growth inhibition caused by the earthworm coelomic fluid, mechanical disruption of fungal hyphae, and burying crop residue which reduce the chances for the fungus to release spores for head infection. Thus, the aim of this study was to assess the effects of anecic and epigeic earthworms on wheat straw and on F. graminearum inoculum. For this, PVC cylinders (microcosms 14.5 cm diameter, 30 cm height) were filled with moist soil mix, wheat straw was evenly distributed on the soil surface (inoculated with Fusarium, soil microorganisms or sterile) and three earthworm species (Aporrectodea longa, Lumbricus rubellus or Lumbricus terrestris) were tested. Since the response of earthworms may change according to conditions of soil moisture and food availability, two different experiments were arranged. The first Experiment represented a sub-optimal situation for earthworms regarding soil moisture and feeding conditions, which was obtained by scarce watering of the microcosms with a consequent decrease in soil water content during incubation, and by not adding cow manure as supplementary food source. In the second experiment, soil was enriched with cow manure as feed for the earthworms and soil moisture was maintained above 25%. Results from qPCR analysis revealed that F. graminearum inoculum on straw was reduced to undetectable amounts by L. rubellus and A. longa when the feeding conditions were limited, while no significant differences compared with the control without earthworms were found when earthworms had high food availability (α = 0.05). Straw coverage on soil surface was reduced by L. rubellus (epigeic) in both experiments (p < 0.0001), while A. longa (anecic) just did so under optimal conditions. L. terrestris (anecic), only tested under optimal conditions, reduced soil cover significantly more than the other two species (p < 0.0001). Negative effect of this fungus was not observed on the studied earthworms. Both anecic and epigeic earthworms tested showed potential to contribute to biological control of F. graminearum in wheat straw. This control may occur by reducing straw on surface, reducing the pathogen inoculum on straw, or both, depending on the environmental conditions and their response according to their ecological group and species. The possibilities to optimize earthworm capacity for biological control of fungal diseases in practical agriculture, under changing weather and organic matter supply conditions, are discussed.