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Use of Anthelmintics in Herbivores and Evaluation of Risks for the Non Target Fauna of Pastures

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Use of Anthelmintics in Herbivores and Evaluation of Risks for the Non Target Fauna of Pastures Vet. Res. 33 (2002) 547–562 INRA, EDP Sciences, 2002 547 DOI: 10.1051/vetres:2002038 Review article Use of anthelmintics in herbivores and evaluation of risks for the non target fauna of pastures Jean-Pierre LUMARET*, Faiek ERROUISSI Laboratoire de Zoogéographie, Université Paul Valéry-Montpellier 3, route de Mende, 34199 Montpellier Cedex 5, France (Received 14 January 2002; accepted 30 April 2002) Abstract – The overall purpose of this paper was to review the major and most recent literature relat- ing 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, pheno- thiazine, 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 organ- isms has been considered acceptable in eradicating the parasites because of their economic impor- tance 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 relative- ment 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, dora- mectine), la moxidectine étant la moins toxique pour la faune coprophage. Jusqu’à présent, cet im- pact 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 trai- tements de routine sont discutées en considérant que l’absence de dégradation des bouses constatée *Correspondence and reprints Tel.: (33) 4 67 14 23 16; fax: (33) 4 67 14 24 59; e-mail: [email protected] 548 J.P. Lumaret, F. Errouissi localement peut malgré tout s’accompagner d’une érosion silencieuse de la biodiversité, avec un dé- séquilibre à long terme du fonctionnement des pâturages. anthelminthique / résidus / coléoptère coprophage / diptère / contrôle raisonné des parasites Table of contents 1. Introduction. 548 2. Pharmacokinetics and routes of elimination. 549 3. Concentration, stability and activity of anthelmintics in the faeces; effects on non-target dung-feeding fauna . 550 4. Influence of anthelmintics on dung degradation . 554 5. Indirect effects of antiparasitic use . 556 6. Conclusion . 556 1. INTRODUCTION affect the development and survival of non-target organisms in estuarine and ma- Over the past decade, concerns have rine ecosystems [17, 18, 23, 36, 37]. been increasingly expressed by the scien- The development of anthelmintics and tific community regarding the possible un- latterly endectocides with a broad range of intended side effects of chemicals used in target pathogens has provided more effi- veterinary and agricultural practices and, cient and economic options for the treat- more particularly, in the widespread use of ment and control of parasitic disease both in the macrocyclic lactone class of chemicals ruminant and monogastric animals. In pas- such as anthelmintics used to control gas- tures, most antiparasitic agents are ex- trointestinal parasites of grazing livestock creted, to some extent, in the faeces of and companion animals. In the scientific treated animals, creating a concern for their community there is a lack of consensus effect on the organisms that feed and/or over the potential of macrocyclic lactone breed in animal excrements. As the spec- residues, excreted in the dung of treated an- trum of activity of the antiparasitic agents imals, to harm dung beetles that utilise this has enlarged, the potential for affecting dung. Scientists do not agree on the extent non-target organisms has increased equally of such risks, mainly because of the com- [81]. Many of the non-target organisms plex dynamics of insect populations that play a vital role in the processes of dung fluctuates widely according to factors such dispersal. They are crucial for maintaining as climatic fluctuations, rainfall, cattle pasture hygiene, nutrient cycling, soil aera- management and pasture quality [6, 98]. tion, humus content, water percolation and This situation has raised concerns not only pasture productivity. In addition, they also for the possible impact on dung degradation ensure that the livestock grazing area is not but also for the consequences on pastu- drastically reduced by an accumulation of reland insect communities and ecosystem dung [50]. In the cow dung community, stability and on the sustainability of pasture dung feeder flies [42], coprophagous bee- fertility [8, 41, 50, 64, 68, 81, 107, 115, tles [43, 44, 53] and annelid worms [54, 55, 117]. At the same time, it has been shown 85] are the most important organisms. Un- that modern anthelmintics also adversely der warm and dry climate conditions, dung Use of anthelmintics and risks for the fauna 549 beetles appear the most important organ- some anthelmintics on non-target inverte- isms to degrade dung pats, while earth- brates. Faecal residues or metabolites of worms predominate both in activity and drugs belonging to the benzimidazole and biomass under temperate and more mesic levamisole/morantel groups are thought to conditions [85]. Earthworms aggregate un- be relatively harmless to dung fauna [81, der dung pats [15] and it has been demon- 110], on the contrary to other anthelmintics strated that dung is readily eaten and such as coumaphos, dichlorvos, phenothi- removed from the surface by these organ- azine, piperazine [12, 64], synthetic isms which are therefore presumed to play pyrethroids [10, 115], and most macrocyclic an important role in the decay and disap- lactones [25, 50, 99, 100, 102] which have pearance of dung [38]. However, it has been been shown to be highly toxic for dung bee- shown that earthworm activity in pats may tles. strongly depend on beetle occurrence and Several factors can modify the environ- activity. Beetles rapidly colonise and mental risks: (i) The amount of the active oviposite in dung pats in the first few days agent which enters the environment; this after they are dropped, facilitating the ini- amount depends on the route or delivery tial breakdown of dung and allowing the system of administration [50], and on the subsequent entry of earthworms which physiology of the treated animals [3, 4]; continue to degrade the dung [15, 38, 55, (ii) The concentration and persistence of 107]. The occurrence of many species is fa- the drug in the faeces, and the total amount cilitated by the activities of other species of droppings from treated animals com- which colonise droppings earlier. When pared to the total faecal deposits in the pas- beetles utilise dung pats, they dig small tun- ture [30, 81]; (iii) Environmental factors nels which weaken the pats and, at the same (light, rainfall, temperature…) and the co- time, beetles inoculate the heart of pats with incidence of deposits with activity of microorganisms as they carry spores of tel- non-target organisms [30, 41]; (iv) The sus- luric fungi and microorganisms on their in- ceptibility of organisms, some taxa are tegument. Consequently, the presence of more susceptible than others, and some are beetles stimulates the microbial activity. highly resistant [24, 25, 28, 29, 35, 39, 41, Normally, about 80% of the ammonia re- 112, 113]. lease from dung pats is lost during the first five days, but when sufficient numbers of In the present paper, the environmental beetles are present for quick burial, the loss effects and fates of anthelmintics are re- is reduced to 5–15% and permits the use of viewed from data collected for the registra- this N by plants for up to two years. Under tion of some compounds and from scientific such conditions, pats become progressively literature. soil annexes, with the network of tunnels making colonisation of pats by edaphic fauna easier [25]. Tunnels made by beetles 2. PHARMACOKINETICS improve the oxygen supply to copro- AND ROUTES OF ELIMINATION phagous flies but also provide runways so predatory Staphylinids can get at the flies In a recent and exhaustive report, [105]. Dung burial by beetles decreases Wardhaugh [110] reviewed the parasiti- wastage of herbage through the rejection of cides registered for use in cattle in Austra- fouled herbage and smothering of pasture lia. The author gave information on the leaf area [68]. excretion route and insecticidal activity of particular chemicals and cites literature that There is now a considerable amount of contains relevant information.
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