The impact of Cu, Zn and Cr salts on the relationship between insect and plant parasitic nematodes: A reduction in biocontrol efficacy

Accumulation and potential health risks of toxic elements are associated with excessive fertilizer and manure applications in vegetable production systems. The goal of the present study was to explore the effects of potential toxic elements on the function of a cohort of beneficial organisms, specifically, the insect parasitic nematodes known as entomopathogenic nematodes. We assessed the impact of heavy metal accumulation on entomopathogenic nematodes (Steinernema carpocapsae and Heterorhabditis bacteriophora) and plant parasitic nematodes (Meloidogyne incognita). Genearlly, pretreatment with 1.5 mg Cu/L, 50 mg Zn/L or 7.5 mg Cr/L solution for 24 h caused direct mortality of infective juvenile S. carpocapsae and H. bacteriophora nematodes, and lowered virulence of H. bacteriophora against Galleria mellonella. Interestingly, we found that 24 h exposure to 4.5 mg Cu/L, 50 mg Zn/L or 7.5 mg Cr/L solution already caused higher mortality in H. bacteriophora than M. incognita in a laboratory assay. Moreover, in a potted plant experiment, pretreatment of H. bacteriophora with Cu, Zn or Cr salts resulted in increased penetration of M. incognita into cucumber roots compared with H. bacteriophora that were not treated (thus reducing biocontrol efficacy). Pretreatment of S. carpocapsae with Cu also caused increased penetration of M. incognita into cucumber roots; however, none of the Zn and Cr pretreatment concentrations exposed to S. carpocapsae resulted in increased M. incognita root penetration, and lower concentrations of these elements caused decreased penetration (enhancing biocontrol efficacy). Our results indicate that heavy metals can have a direct negative effect on entomopathogenic nematodes (via direct mortality) and also an indirect effect by disrupting biocontrol efficacy against plant parasitic nematodes, but in some cases low concentration may stimulate biocontrol activity. High levels of heavy metal accumulation in greenhouse vegetable production systems could substantially influence nematode community structure and impact other soil biota as well.