Environmentally-realistic concentrations of anthelmintic drugs affect survival and motility in the cosmopolitan earthworm Lumbricus terrestris (Linnaeus, 1758)

Abstract

Anthelmintic drugs are used to control intestinal parasitic worms in animals worldwide. Although generally effective in managing animal health, such treatment can introduce anthelminthic compounds to the wider environment as active ingredients and metabolites are often excreted. This can have detrimental effects on non-target species, especially when drugs are used excessively. Here, we examine the effects that two environmentally-realistic concentrations of four anthelminthics have on the common earthworm Lumbricus terrestris (Linnaeus, 1758), a species with a cosmopolitan distribution and that is often vital in maintaining functional edaphic ecosystems. The drugs were ivermectin (0.502 and 2.511 mg kG−1 active ingredient), fenbendazole (0.309 and 1.547 mg kG−1), pyrantel (79.480 and 397.400 mg kG−1), and praziquantel (2.299 and 11.499 mg kG−1): these concentrations were typical of soils where pasture grazed by animals treated with anthelminthics. Both lethal effects (mortality) and sub-lethal effects (motility) were considered. Earthworms exposed to fenbendazole and praziquantel over a 12-week period experienced high mortality (55.0% and 32.5%, respectively). Mortality rates among earthworms exposed to pyrantel and ivermectin were much lower (2.5% and 7.5%, respectively). However, earthworms exposed to pyrantel and ivermectin suffered decreased motility (time to burrow into substrate when exposed to heat and light) relative to a control group. Burrowing times were up to 40% longer for pyrantyl-exposed earthworms and 28% longer for ivermectin-exposed earthworms. For both drugs, the magnitude of the effect increased as concentration increased; all differences were statistically significant. There was little effect of fenbendazole and praziquantel on motility. Based on this study, which is seemingly the first to examine effects of ivermectin/fenbendazole on earthworm motility and the first to consider any effects of praziquantel/pyrantel, we conclude that environmentally-realistic concentrations of all four anthelmintics have sub-lethal (pyrantel and ivermectin) or lethal (fenbendazole and praziquantel) effects on a vital keystone species. Methods to reduce carry-over effects in ecologically-important, non-target, organisms should be urgently sought and care should be taken not to use anthelminthics routinely without first testing helminth burden to determine whether there is clinical need.