How to test nontarget effects of veterinary pharmaceutical residues in livestock dung in the field

To register veterinary medicinal products (VMPs) as parasiticides on pastured animals, legislation in the European Union requires an environmental risk assessment to test the potential nontarget effects of fecal residues on dung-dwelling organisms. Products with adverse effects in single-species laboratory tests require further, higher-tier testing to assess the extent of these effects on entire communities of dung-dwelling organisms under more realistic field or semifield conditions. Currently, there are no documents specifically written to assist researchers in conducting higher-tier tests or to assist regulators in interpreting the results of such tests in an appropriate context. Here we provide such a document, written by members of the SETAC Advisory Group DOTTS (Dung Organism Toxicity Testing Standardization) with research experience on dung fauna in central and southern Europe, Canada, Australia, and South Africa. This document briefly reviews the organisms that make up the dung community and their role in dung degradation, identifies key considerations in the design and interpretation of experimental studies, and makes recommendations on how to proceed.

[1]  Mitsuhiro Iwasa,et al.  Effects of moxidectin on coprophagous insects in cattle dung pats in Japan , 2008 .

[2]  B. R. Laurence The Larval Inhabitants of Cow Pats , 1954 .

[3]  John R. Anderson,et al.  The Effects of Different Pasture and Rangeland Ecosystems on the Annual Dynamics of Insects in Cattle Droppings , 1977 .

[4]  P. Galtier,et al.  The negative effects of the residues of ivermectin in cattle dung using a sustained-release bolus on Aphodius constans (Duft.) (Coleoptera: Aphodiidae). , 2001, Veterinary research.

[5]  C. Scholtz,et al.  Effects of cattle treatment with a fluazuron pour-on on survival and reproduction of the dung beetle species Onthophagus gazella (Fabricius). , 2007, Veterinary parasitology.

[6]  D. Borror,et al.  An introduction to the study of insects , 1954 .

[7]  M. Alvinerie,et al.  New screening test to predict the potential impact of ivermectin-contaminated cattle dung on dung beetles. , 2007, Veterinary research.

[8]  I. Hanski,et al.  Chapter 3. Dung beetle population biology , 1991 .

[9]  P. Chapman Integrating toxicology and ecology: putting the "eco" into ecotoxicology. , 2002, Marine pollution bulletin.

[10]  T. Maruo,et al.  Adverse effects of ivermectin on the dung beetles, Caccobius jessoensis Harold, and rare species, Copris ochus Motschulsky and Copris acutidens Motschulsky (Coleoptera: Scarabaeidae), in Japan , 2007, Bulletin of Entomological Research.

[11]  D. Colwell,et al.  Larvicidal activity of endectocides against pest flies in the dung of treated cattle , 2001, Medical and veterinary entomology.

[12]  R. Nager,et al.  Effects of avermectin residues in cattle dung on yellow dung fly Scathophaga stercoraria (Diptera: Scathophagidae) populations in grazed pastures , 2007, Bulletin of Entomological Research.

[13]  K. Floate Does a repellent effect contribute to reduced levels of insect activity in dung from cattle treated with ivermectin , 1998 .

[14]  M. Alvinerie,et al.  Environmental risk assessment of veterinary pharmaceuticals: development of a standard laboratory test with the dung beetle Aphodius constans. , 2007, Chemosphere.

[15]  K. Floate,et al.  No Support for Fluctuating Asymmetry as a Biomarker of Chemical Residues in Livestock Dung1 , 2010, The Canadian Entomologist.

[16]  H. Ahmad,et al.  Efficacy of macrocyclic lactones for the control of larvae of the Old World screw-worm fly (Chrysomya bezziana). , 2001, Australian veterinary journal.

[17]  R. Morton,et al.  A comparison of the development and survival of the dung beetle, Onthophagus taurus (Schreb.) when fed on the faeces of cattle treated with pour-on formulations of eprinomectin or moxidectin. , 2001, Veterinary parasitology.

[18]  P. Holter,et al.  Attractiveness of dung from ivermectin-treated cattle to Danish and afrotropical scarabaeid dung beetles. , 1993, Veterinary parasitology.

[19]  P. Holter,et al.  The development and survival of three species of coprophagous insect after feeding on the faeces of sheep treated with controlled-release formulations of ivermectin or albendazole. , 2001, Australian veterinary journal.

[20]  C. Dewhurst,et al.  Biological and chemical assays of pyrethroids in cattle dung , 2004, Bulletin of Entomological Research.

[21]  G A Vale,et al.  Modelled impact of insecticide-contaminated dung on the abundance and distribution of dung fauna , 2002, Bulletin of Entomological Research.

[22]  A. Lifschitz,et al.  Effects of faecal residues of moxidectin and doramectin on the activity of arthropods in cattle dung. , 2009, Ecotoxicology and environmental safety.

[23]  P. B. Edwards,et al.  A simple assay to determine the nutritional suitability of cattle dung for coprophagous beetles , 1989 .

[24]  K. Wardhaugh Insecticidal activity of synthetic pyrethroids, organophosphates, insect growth regulators, and other livestock parasiticides: An Australian perspective , 2005, Environmental toxicology and chemistry.

[25]  P. Holter Effect of dung-beetles (Aphodius spp.) and earthworms on the disappearance of cattle dung , 1979 .

[26]  C. Scholtz,et al.  Effects of fluazuron and ivermectin treatment of cattle on the structure of dung beetle communities , 2005 .

[27]  Alistair B A Boxall,et al.  A screening level index for assessing the impacts of veterinary medicines on dung flies. , 2007, Environmental science & technology.

[28]  W. Terra Evolution of Digestive Systems of Insects , 1990 .

[29]  P. Skidmore Insects of the British cow-dung community. , 1991 .

[30]  K. Floate,et al.  FLIES UNDER STRESS: A TEST OF FLUCTUATING ASYMMETRY AS A BIOMONITOR OF ENVIRONMENTAL QUALITY , 2000 .

[31]  I. Dadour,et al.  Effect of diet on the excretion profile of ivermectin in cattle faeces. , 1996, International journal for parasitology.

[32]  K. Floate Off-target effects of ivermectin on insects and on dung degradation in southern Alberta, Canada , 1998 .

[33]  M. Alvinerie,et al.  Toxicity of four veterinary parasiticides on larvae of the dung beetle Aphodius constans in the laboratory , 2006, Environmental toxicology and chemistry.

[34]  R. J. Mahon,et al.  Avermectin residues in sheep and cattle dung and their effects on dung-beetle (Coleoptera: Scarabaeidae) colonization and dung burial , 1991 .

[35]  Troy I. Wellicome,et al.  Does Doramectin Use on Cattle Indirectly Affect the Endangered Burrowing Owl , 2008 .

[36]  W. Blanckenhorn,et al.  Lethal and sublethal toxic effects of a test chemical (ivermectin) on the yellow dung fly (Scathophaga stercoraria) based on a standardized international ring test. , 2009, Environmental toxicology and chemistry.

[37]  J. Lumaret,et al.  Use of anthelmintics in herbivores and evaluation of risks for the non target fauna of pastures. , 2002, Veterinary research.

[38]  L. Strong,et al.  Some effects of ivermectin on the yellow dung fly, Scatophaga stercoraria. , 1993, Veterinary parasitology.

[39]  H. Marion Antimicrobial resistance and the guidelines of the International Cooperation on Harmonisation of Technical Requirements for Registration of Veterinary Medicinal Products (VICH). , 2012, Revue scientifique et technique.

[40]  Peter Calow,et al.  Ecology in ecotoxicology: some possible ‘rules of thumb’ , 1996 .

[41]  R. Nager,et al.  Field-scale dispersal of Aphodius dung beetles (Coleoptera: Scarabaeidae) in response to avermectin treatments on pastured cattle , 2009, Bulletin of Entomological Research.

[42]  C. Scholtz,et al.  Changes in the structure of dung insect communities after ivermectin usage in a grassland ecosystem. II. Impact of ivermectin under high-rainfall conditions , 1998 .

[43]  I. Cuthill,et al.  Effect size, confidence interval and statistical significance: a practical guide for biologists , 2007, Biological reviews of the Cambridge Philosophical Society.

[44]  W. Taylor,et al.  Thin-layer chromatographic detection of ivermectin in cattle dung. , 1997, Journal of chromatography. B, Biomedical sciences and applications.

[45]  P. Holter Particle feeding in Aphodius dung beetles (Scarabaeidae): old hypotheses and new experimental evidence , 2000 .

[46]  M. Alvinerie,et al.  Endectocide exchanges between grazing cattle after pour-on administration of doramectin, ivermectin and moxidectin. , 2004, International journal for parasitology.

[47]  K. Floate,et al.  Endectocide residues affect insect attraction to dung from treated cattle: implications for toxicity tests , 2007, Medical and veterinary entomology.

[48]  C. Scholtz,et al.  Effects of cattle treatment with a cypermethrin/cymiazol spray on survival and reproduction of the dung beetle species Euoniticellus intermedius (Coleoptera: Scarabaeidae) , 2006, Bulletin of entomological research.

[49]  D. Baird,et al.  Ecotoxicology: ecological dimensions. , 1996 .

[50]  C. O. Mohr Cattle Droppings as Ecological Units , 1943 .

[51]  D. Colwell,et al.  Reductions of non-pest insects in dung of cattle treated with endectocides: a comparison of four products , 2002, Bulletin of Entomological Research.

[52]  P. Galtier,et al.  Pour‐on formulation of eprinomectin for cattle: Fecal elimination profile and effects on the development of the dung‐inhabiting Diptera Neomyia cornicina (L.) (Muscidae) , 2005, Environmental toxicology and chemistry.

[53]  Alistair B A Boxall,et al.  Fecal residues of veterinary parasiticides: nontarget effects in the pasture environment. , 2005, Annual review of entomology.