The avermectins, milbemycins and spinosyns are collectively referred to as macrocyclic lactones (MLs) which comprise several classes of chemicals derived from cultures of soil micro-organisms. These compounds are extensively and increasingly used in veterinary medicine and agriculture. Due to their potential effects on non-target organisms, large amounts of information on their impact in the environment has been compiled in recent years, mainly caused by legal requirements related to their marketing authorization or registration. The main objective of this paper is to critically review the present knowledge about the acute and chronic ecotoxicological effects of MLs on organisms, mainly invertebrates, in the terrestrial and aquatic environment. Detailed information is presented on the mode-of-action as well as the ecotoxicity of the most important compounds representing the three groups of MLs. This information, based on more than 360 references, is mainly provided in nine tables, presenting the effects of abamectin, ivermectin, eprinomectin, doramectin, emamectin, moxidectin, and spinosad on individual species of terrestrial and aquatic invertebrates as well as plants and algae. Since dung dwelling organisms are particularly important non-targets, as they are exposed via dung from treated animals over their whole life-cycle, the information on the effects of MLs on dung communities is compiled in an additional table. The results of this review clearly demonstrate that regarding environmental impacts many macrocyclic lactones are substances of high concern particularly with larval instars of invertebrates. Recent studies have also shown that susceptibility varies with life cycle stage and impacts can be mitigated by using MLs when these stages are not present. However information on the environmental impact of the MLs is scattered across a wide range of specialised scientific journals with research focusing mainly on ivermectin and to a lesser extent on abamectin doramectin and moxidectin. By comparison, information on compounds such as eprinomectin, emamectin and selamectin is still relatively scarce.

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Ivermectin is a veterinary pharmaceutical generally used to control the ecto- and endoparasites of livestock, but its use has resulted in adverse effects on coprophilous insects, causing population decline and biodiversity loss. There is currently no information regarding the direct effects of ivermectin on dung beetle physiology and behaviour. Here, based on electroantennography and spontaneous muscle force tests, we show sub-lethal disorders caused by ivermectin in sensory and locomotor systems of Scarabaeus cicatricosus, a key dung beetle species in Mediterranean ecosystems. Our findings show that ivermectin decreases the olfactory and locomotor capacity of dung beetles, preventing them from performing basic biological activities. These effects are observed at concentrations lower than those usually measured in the dung of treated livestock. Taking into account that ivermectin acts on both glutamate-gated and GABA-gated chloride ion channels of nerve and muscle cells, we predict that ivermectin’s effects at the physiological level could influence many members of the dung pat community. The results indicate that the decline of dung beetle populations could be related to the harmful effects of chemical contamination in the dung.

SUMMARYThe effects of insect larval diet on adult olfactory responses to host-plant or food volatiles are still debated. The induction of adult host preferences has been studied in insects with diverse ecologies, including parasitoids, flower-visitors and phytophagous species. We investigated this question for the first time in a coprophagous insect species. Larvae of the French scarab dung beetle Agrilinus constans were reared on four different artificial substrates containing dung from cattle, horse, sheep or wild boar, and responses of imagos to dung volatiles were then behaviourally tested in an olfactometer. We also reported the first analysis of the composition of different mammal dung volatiles. We showed that adult beetles were more attracted to cattle and sheep dung odours, and that larval feeding experience had no effect on the adult olfactory responses to dung volatiles. A second experiment showed that the presence of other insects inside the dung resource affects the process of dung selection by adults. We identified 64 chemical compounds from dung emissions, and showed that dung volatiles clearly differed among different mammal species, allowing olfactory discrimination by dung beetles. Our results suggest that resource selection in coprophagous insects may be based on innate olfactory preferences. Further experiments should examine whether Agrilinus adults can learn new dung odours, and whether larval diet may influence the behaviour of adults in other coprophagous species.

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-The overall purpose of this paper was to review the major and most recent literature relating the effects of anthelmintics on dung breeding invertebrates and dung degradation. Faecal residues or metabolites of drugs belonging to the benzimidazole and levamisole/morantel groups are relatively harmless to dung fauna, on the contrary to other anthelmintics such as coumaphos, dichlorvos, phenothiazine, piperazine, synthetic pyrethroids, and most macrocyclic lactones which have been shown to be highly toxic for dung beetles (abamectin, ivermectin, eprinomectin, doramectin), among which moxidectin was the less toxic for dung beetles. To date, the detrimental impact upon non-target organisms has been considered acceptable in eradicating the parasites because of their economic importance to commercial livestock production. The consequences of routine treatments are discussed with consideration of the long-term consequences for cow pat fauna and sustainable pastureland ecology.anthelmintic / residue / dung beetle / Diptera / sustainable parasite control Résumé -Usage des anthelminthiques en élevage et évaluation des risques pour la faune non cible du pâturage. Cet article de synthèse passe en revue les travaux de la littérature les plus récents concernant les effets secondaires des principaux produits vétérinaires utilisés en routine sur la faune coprophage et sur la dégradation des excréments dans les pâturages. Les résidus (ou les métabolites) des groupes du benzimidazole et levamisole/morantel trouvés dans les excréments s'avèrent relativement peu toxiques pour la faune coprophage. Au contraire les anthelminthiques des groupes suivants s'avèrent hautement toxiques: coumaphos, dichlorvos, phénothiazine, pipérazine, pyréthroïdes de synthèse, et la plupart des lactones macrocycliques (abamectine, ivermectine, éprinomectine, doramectine), la moxidectine étant la moins toxique pour la faune coprophage. Jusqu'à présent, cet impact négatif a été considéré comme acceptable par les éleveurs et firmes pharmaceutiques en regard de l'importance économique du contrôle et/ou l'éradication des parasites. Les conséquences des traitements de routine sont discutées en considérant que l'absence de dégradation des bouses constatée 547

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The environmental risk assessment of veterinary pharmaceuticals for dung beetles is strongly hampered because no standardized test method is available so far. Therefore, a test with the temperate dung beetle species Aphodius constans was developed. The survival of beetle larvae was determined after exposure to four veterinary parasitical pharmaceuticals (ivermectin, moxidectin, dicyclanil, and praziquantel) representing different treatment regimes, modes of action, and effect levels. The test was performed in the laboratory (three week duration) with fresh dung, as well as formulated (dried, ground, and rewetted) dung as test substrate (i.e., at least one range-finding test, two definitive test runs per pharmaceutical). Ivermectin was the most toxic substance (median lethal concentration [LC50] = 0.88-0.98 mg of active substance per kilogram of dung dry weight [mg a.s./kg dung (dry wt)] followed by dicyclanil (LC50 = 1.5-6.0 mg a.s./kg dung [dry wt]) and moxidectin (LC50 = 4.0-5.4 mg a.s./kg dung [dry wt]), whereas praziquantel showed very low toxicity (LC50 > 1,000 mg a.s./kg dung [dry wt]). The toxicity in fresh and formulated dung differed by a factor of between 1.1 and 4. The comparison with literature data on toxic effects of these substances on dung beetles in the laboratory or in the field is difficult because no results for praziquantel and dicyclanil have been published so far. With the use of data from ivermectin and moxidectin, the test results are on the same order of magnitude as those known from other studies. On the basis of the experiments reported here, it is recommended that this test be standardized in an international ring test so that it can be incorporated into the risk assessment process as described in the respective international guidelines for the registration of veterinary pharmaceuticals.