Abstract
Earthworms are ecological engineers that can contribute to the displacement of biological control agents such as the entomopathogenic nematodes (EPNs) and fungi (EPF). However, a previous study showed that the presence of cutaneous excreta (CEx) and feeding behavior of the earthworm species Eisenia fetida (Haplotaxida: Lumbricidae) compromise the biocontrol efficacy of certain EPN species by reducing, for example, their reproductive capability. Whether this phenomenon is a general pattern for the interaction of earthworms-entomopathogens is still unknown. We hypothesized that diverse earthworm species might differentially affect EPN and EPF infectivity and reproductive capability. Here we investigated the interaction of different earthworm species (Eisenia fetida, Lumbricus terrestris, and Perionyx excavatus) (Haplotaxida) and EPN species (Steinernema feltiae, S. riojaense, and Heterorhabditis bacteriophora) (Rhabditida) or EPF species (Beauveria bassiana and Metarhizium anisopliae) (Hypocreales), in two independent experiments. First, we evaluated the application of each entomopathogen combined with earthworms or their CEx in autoclaved soil. Hereafter, we studied the impact of the earthworms' CEx on entomopathogens applied at two different concentrations in autoclaved sand. Overall, we found that the effect of earthworms on entomopathogens was species-specific. For example, E. fetida reduced the virulence of S. feltiae, resulted in neutral effects for S. riojaense, and increased H. bacteriophora virulence. However, the earthworm P. excavates increased the virulence of S. feltiae, reduced the activity of H. bacteriophora, at least at specific timings, while S. riojaense remained unaffected. Finally, none of the EPN species were affected by the presence of L. terrestris. Also, the exposure to earthworm CEx resulted in a positive, negative or neutral effect on the virulence and reproduction capability depending on the earthworm-EPN species interaction. Concerning EPF, the impact of earthworms was also differential among species. Thus, E. fetida was detrimental to M. anisopliae and B. bassiana after eight days post-exposure, whereas Lumbricus terrestris resulted only detrimental to B. bassiana. In addition, most of the CEx treatments of both earthworm species decreased B. bassiana virulence and growth. However, the EPF M. anisopliae was unaffected when exposed to L. terrestris CEx, while the exposure to E. fetida CEx produced contrasting results. We conclude that earthworms and their CEx can have positive, deleterious, or neutral impacts on entomopathogens that often coinhabit soils, and that we must consider the species specificity of these interactions for mutual uses in biological control programs. Additional studies are needed to verify these interactions under natural conditions.
Highlights
Soil is a complex matrix composed of unconsolidated mineral material, organic matter, air, water, and a large number and variety of organisms
We found that the impact of earthworms and their cutaneous excreta (CEx) on entomopathogenic nematodes (EPNs) virulence was species-specific, for S. feltiae and H. bacteriophora (Fig. 1), but not on EPN reproductive capability (Fig. 2)
We observed opposite results for H. bacteriophora: its virulence was significantly higher for E. fetida treatments and lower when com bined with P. excavatus CEx (Fig. 1C)
Summary
Soil is a complex matrix composed of unconsolidated mineral material, organic matter, air, water, and a large number and variety of organisms. Earthworms can contribute to reduce the numbers of plant-parasitic nematodes (Dash et al, 1980; Boyer et al, 2013) and enhance the movement of other beneficial soil organisms such as entomopathogenic nematodes and fungi (Shapiro-Ilan and Brown, 2013) Depending on their drilling capability, feeding ac tivity, and oxygen availability, earthworms are categorized into three main groups: epigeic, anecic, and endogeic (Bouche, 1977; Rombke et al, 2005; Guhra et al, 2020; Sapkota et al, 2020). Endogeic species move randomly across the soil, making horizontal burrows all over the upper part of the ground (Bouche, 1977; Lavelle, 1988)
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