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Veterinary Parasitology 189 (2012) 113– 124
Contents lists available at SciVerse ScienceDirect
Veterinary Parasitology
jo u rn al hom epa ge : www.elsev ier .com/ locate /vetpar
otential environmental consequences of administration ofnthelmintics to sheep
.A. Beynonepartment of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, England, United Kingdom
r t i c l e i n f o
eywords:nthelminticichorium intybusuddingtonia flagransung beetlescotoxicologyvermectinheep
a b s t r a c t
Anthelmintics, veterinary medicines for the control of endoparasites, enter into the envi-ronment largely through faeces of the treated animals. Sheep dung is a patchily distributed,ephemeral resource, with a functionally important decomposer community. The nature ofthis community and the pharmacokinetics of anthelmintics in sheep mean that the ecotoxicimpacts of these drugs in sheep dung may differ markedly from those in cattle dung, wheremost research has been focussed. The period of maximum residue excretion is generallymore transient in sheep than cattle dung, but low-level excretion may continue for longer,giving the potential for extended sub-lethal effects. Here, the environmental impacts ofsheep anthelmintics, as well as alternative endoparasite control methods are reviewed.Impacts are discussed in terms of the potential for residues to enter into the environ-ment, the toxicity and the impact on ecosystem functioning at an appropriate scale. Futureresearch priorities are also discussed; these include the need for studies of the functional
contributions of dung-colonising species, as well as the development of higher-tier ecotox-icological methods bridging the gap between laboratory and field experiments. Large-scaleand long-term studies, including the development of appropriate models, are necessary toallow the consequences of anthelmintic administration to be assessed, particularly withinthe remit of sustainable animal production.© 2012 Elsevier B.V. All rights reserved.
. Introduction
The control of internal parasites is vital for sustainableheep production; however, it comes at a cost. For example,nternal parasite control costs the UK sheep industry aboutBP 84 million annually (Nieuwhof and Bishop, 2005).heep anthelmintics, veterinary medicines that controlastro-intestinal helminthes, liver fluke and lungwormsFloate et al., 2005), may be applied topically, orally, viantraruminal boluses, by injection or in-feed. Anthelminticsdministered to sheep enter into the environment pri-
arily through their excretion in faeces (Halling-Sørensent al., 2001); for example, >98% of ivermectin (regardlessf route of administration) is excreted in faeces (Halley
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304-4017/$ – see front matter © 2012 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.vetpar.2012.03.040
et al., 1989a). However, the precise excretion profile islinked to the mode of administration (Boxall et al., 2003).Pour-on administered drugs are excreted largely unalteredin the faeces, whereas compounds administered orally orby injection are metabolised to a greater degree prior toexcretion (Wardhaugh, 2005). The exceptions are the ben-zimidazoles, imidazothiazoles and tetrahydropyrimidines,which are mainly excreted in urine (McKellar, 1997). Thewash-off of topically applied compounds from the fleece,spillage during application and inappropriate disposal ofcompounds provide other important environmental entrypoints (Boxall et al., 2002). Contamination is not limitedto soil and dung; drugs may leach into groundwater and
reach water-bodies through surface run-off or be excretedor washed-off treated animals directly into a watercourse(Boxall et al., 2002). The entry of anthelmintics into theenvironment due to the manufacturing process is likely to
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114 S.A. Beynon / Veterinary Pbe low in the European Union (EU) or the USA, due to strin-gent manufacture and formulation regulations. For othercountries, this contribution is largely unknown (Boxallet al., 2003).
Here, the potential ecotoxic impacts of anthelminticsadministered to sheep for the control of internal parasitesare considered (Table 1). An evaluation of the environmen-tal impact of alternative products marketed for parasitecontrol is also included, where sufficient data allows. Stud-ies of cattle dung are not reviewed systematically here andare referred to only where required to highlight differencesin excretion and ecotoxicity between sheep and cattle.
2. Ecotoxicity tests
Ecotoxicity tests have been required for veterinarymedicines by the EU since the early 1990s and by theU.S. Food and Drugs Administration (FDA) since 1980(European Commission, 1992; Boxall et al., 2003). Discus-sions for new guidance documents are underway, involvingEU countries, the USA and Japan, with Australia, NewZealand and Canada as observers (VICH, 2004). Currentecotoxicity tests focus on fish, daphnids, algae, microbes,earthworms, plants and dung invertebrates. The Environ-ment Agency of England and Wales uses the results froma targeted monitoring study of veterinary medicines toassess potential ecotoxic impacts of veterinary medicines,with information gathered from the United Kingdom,Germany, the Netherlands and Denmark (Boxall et al.,2006). The majority of sheep anthelmintics are classifiedas high possible impact, with high usage/impact productsalso identified as such in other countries (Jorgensen andHalling-Sørensen, 2000).
The main focus of study for the ecotoxic effects ofanthelmintics has been the macrocyclic lactones (MLs), inparticular ivermectin. Lumaret (1986) was the first to sug-gest a field impact of ivermectin on cattle dung fauna, withWall and Strong (1987) finding an associated retardationof dung decomposition. Since then, many studies, both inthe field and in the laboratory, have confirmed this. Thewide spectrum of activity of ivermectin against endo- andectoparasites increases the potential for impacts on non-target organisms. As ivermectin may be stored for longperiods in soil (Mougin et al., 2003), impacts on soil faunahave also been comprehensively assessed. More recently,work has focussed on single- or multi-species laboratorytoxicity tests, where coprophagous fly and dung beetle lar-vae are particularly sensitive (Hempel et al., 2006; OECD,2007, 2009; Römbke et al., 2007a,b, 2009a,b). Earthwormsappear to be less sensitive to residues, but with possi-ble sub-lethal effects on some species from exposure toabamectin (Diao et al., 2007; Jensen et al., 2007). Toxic andsub-lethal effects of abamectin, doramectin and ivermectinhave been reported on collembolans and predatory mites(Römbke et al., 2010), enchytraeids (Jensen et al., 2003) andisopods (Kolar et al., 2010); impact of ivermectin on soilfauna feeding rates has also been reported (Förster et al.,
2011). However, the impact of residues excreted in urineon soil biota is still largely unknown (McKellar, 1997).Macrocyclic lactone residues have been found in aer-obic water sediments (Prasse et al., 2009) and have been
ogy 189 (2012) 113– 124
shown to be toxic to a number of aquatic invertebrates(OECD, 1984, 1998; Burridge and Haya, 1993). This raisesconcerns over the possible non-target aquatic impact ofanthelmintics, from incorrect disposal, fleece wash-offor faecal/urinary contamination of water courses. MLshave not been shown to exhibit antifungal, antibacte-rial, antiprotozoal and anti-algal effects in the laboratory(Halley et al., 1989a; Escher et al., 2008) or at field concen-trations, with no impact on soil microbe nitrification andrespiration (Halley et al., 1989a,b). However, there may bea long-term effect of ivermectin to the soil fungus Fusar-ium oxysporum, where both production and germination ofspores were reduced after exposure; in contrast, spore pro-duction doubled in Phanerochaete chrysosporium and Mucorracemosus (Kollmann et al., 2003). However, the concentra-tions used in the latter study were far higher than predictedsoil or dung concentrations. It is widely accepted that ben-zimidazoles have a fungicidal effect (Araujo et al., 1995;Sanyal et al., 2004). Decomposition of cattle dung in soilhas been shown to be retarded by both levamisole and fen-bendazole (Sommer and Bibby, 2002), but this has not beendirectly linked to a fungicidal impact.
The benzimidazoles and imidazothiazoles havereceived some coverage in the literature, showing lit-tle ecotoxic impact to dung or soil fauna. Similarly,literature on the ecotoxic impact of hexahydropyrazines,tetrahydropyimidines and aminoacetonitrile derivativesis limited to one or two studies for each group. Labo-ratory studies have recorded no effects of praziquantelon dung beetles (Hempel et al., 2006) and no effects ofmorantel on soil mesofauna (Jensen et al., 2009). Thereappear to be no independent ecotoxicity studies on thesalicylanilides, the diphenylsulphides, clorsulon, pyrantelembonate or tetramisol. Various aspects of similar effectsof anthelmintics on dung, soil and aquatic fauna afteradministration to cattle have been described by Strong(1992, 1993), Herd and Wardhaugh (1993), McKellar(1997), Spratt (1997), Wardhaugh and Ridsdill-Smith(1998), Floate (1999), Lumaret and Errouissi (2002),Suarez (2002), Boxall et al. (2003), Floate et al. (2005),Floate (2006) and Schmitt and Römbke (2008). How-ever, the environmental impact of anthelmintics afteradministration to sheep is less well-known.
3. The sheep dung decomposer community
The ecology, as well as functional and economic impor-tance of cattle dung communities on dung decomposition,parasite bio-control, pasture fertility, soil health and asprey for higher vertebrates have been well documentedand reviewed (Landin, 1961; Bergstrom et al., 1976;Fincher, 1981; Anderson et al., 1984; Hanski, 1991; Gittingset al., 1994; Ward and Wilhelm, 1994; Spratt, 1997;Manfredi, 2006; Yamada et al., 2007; Nichols et al., 2008;Rosenlew and Roslin, 2008; d’Alexis et al., 2009; Wall andBeynon, 2012). Indeed, the ecosystem function of dungdecomposition in agricultural grasslands has been identi-
fied as one of the key questions of high policy relevance inthe UK (Sutherland et al., 2006). However, the ecology ofsheep dung decomposing communities is much less wellknown.
S.A. Beynon / Veterinary Parasitology 189 (2012) 113– 124 115
Table 1Veterinary anthelmintics commonly used against sheep endoparasites.
Anthelmintic group Examples
Benzimidazoles and pro-benzimidazoles Albendazole, fenbendazole, mebendazole, netobimin, oxfendazole, oxibendazole, triclabendazoleDiphenylsulphides BithionolHexahydropyrazines PraziquantelImidazothiazoles Levamisole, tetramisoleMacrocyclic lactones Abamectin, doramectin, eprinomectin, ivermectin, moxidectinSalicylanilides Closantel, nicloclosamide-bases, oxyclozanide, rafoxanideTetrahydropyrimidines Morantel, pyrantel embonate
il, dicyc
CeqpactshdllctHis1
(adem(dooshtabfpsdspbttiloiA
Aminoacetonitrile derivatives (AAD’s) MonepantelOthers Clorsulon, nitroxyn
Cattle dung pats are very different from sheep dung.attle dung is voided throughout the pasture, with gen-rally no latrine areas. The cattle pat is of large volume anduickly forms a skin preventing further desiccation. Thisrolongs the pat as a feeding site for dung invertebratesllowing, particularly in temperate zones, a complex, suc-essional community to develop (Skidmore, 1991). In theropics however, large-bodied, paracoprid dung beetlepecies may remove the entire pat within a matter ofours, removing the resource (Slade et al., 2007). Sheepung consists either of compact lumps or clusters of pel-
ets, often deposited in groups, creating highly aggregatedatrine areas (King, 1993a). Sheep dung is attractive to aomplex community of insects and the microhabitat condi-ions created within it allows distinct resource partitioning.owever, sheep dung is a highly ephemeral resource; it
s susceptible to desiccation and may be attractive for ahorter time period than cattle dung (Sowig and Wassmer,994).
Sheep dung is an important resource for dung beetlesDavis et al., 2010) and an increase in sheep dung avail-bility may increase dung beetle abundance and speciesiversity at a site (Lobo et al., 2006). The highly het-rogeneous nature of sheep droppings means that theicroclimate within them is strongly influenced by climate
Sowig and Wassmer, 1994) and they may support higherung beetle abundance and larval production than cattler horse dung (Finn and Giller, 2002). Despite dung beetlesften being viewed as generalists (Hanski, 1991) and sometudies concluding no preference for a particular type oferbivore dung (Doube and Wardhaugh, 1991), both northemperate (Gittings and Giller, 1998; Finn and Giller, 2002)nd Mediterranean (Martin-Piera and Lobo, 1996) dungeetles have been shown to display preference for dungrom particular mammal species. Recent work on olfactoryreferences in dung beetles [Aphodius (Agrilinus) constans]uggests that they may innately discriminate betweenung from different mammal species based on mammalpecies-specific dung volatiles (Dormont et al., 2010). Dungreference experiments with 27 species of French dungeetles identified sheep dung as the most attractive dungype, colonised by 2257 individuals, whereas other dungypes attracted fewer: cattle = 1294, deer = 768, horse = 622ndividuals. Eleven of the 27 species identified were more
ikely to colonise one dung type in the field, confirmed bylfactometer bioassays in the laboratory. Species includ-ng Trypocopris pyrenaeus, Anoplotrupes stercorosus andphodius rufipes were more likely to be attracted to sheeplanil, synthetic pyrethroids, organophosphates
dung than to other species dung, in both laboratory andfield experiments and Geotrupes stercorarius in field exper-iments only (Dormont et al., 2007).
4. Differences between sheep and cattle
4.1. Pharmacokinetics
Two reviews on the impact of avermectins on sheep pas-tures (King, 1993a,b) highlight the fact that data on theecotoxic effects on the fauna of sheep dung have rarelybeen studied, with no work on the ecosystem function ofnutrient cycling. Despite these reviews having been pub-lished almost two decades ago, this is still the case. Thereis very little literature on the non-target impact of benz-imidazoles, the imidazothiazoles or tetrahydropyrimidineson sheep dung colonisers. Similarly, other anthelminticswhich have been shown to be highly toxic to beetles incattle dung (Blume et al., 1976; Lumaret, 1986) and whichare comprehensively reviewed by Lumaret and Errouissi(2002), have received no attention in the sheep literature.
When interpreting field studies of residue excre-tion, there are many confounding factors that makecomparisons between studies difficult. These include envi-ronmental factors (e.g. rainfall, sunlight, temperature),physical properties of the dung (often due to animal diet),activity of dung- and soil-invertebrates and the extent ofsheep parasitism (Kolar and Erzen, 2007; Perez et al., 2010).In addition, many studies have compared faecal excretionof drugs between sheep and cattle after using differentmodes of administration. For all grazing livestock, dura-tion of excretion of anthelmintics relates to their methodof delivery, with duration after intraruminal administra-tion being greater to that after pour-on or subcutaneousadministration and those being greater to that after oraladministration (Steel, 1993). Factors, such as feed dry massdigestibility, which are increased in cattle compared tosheep, suggest differences in faecal properties and drugexcretion profiles (Playne, 1978).
Whilst excretion of ivermectin after oral administra-tion has been suggested to take place significantly fasterin sheep than cattle, it is impossible to make directcomparisons from the literature alone due to differentmethods of dosing. After oral administration in sheep, mox-
idectin was excreted in faeces at a peak level of over 16times that excreted by cattle when pour-on administra-tion, even though cattle were given a higher dose (Steel,1998). Initial faecal concentration of orally administered
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116 S.A. Beynon / Veterinary Pmoxidectin to sheep was 10 times greater in sheep thancattle after subcutaneous injection (Lumaret and Errouissi,2002). Therefore, despite limitations in comparing thesedata, in the period immediately following treatment,residue-containing dung from orally treated sheep mayrepresent a higher potential ecotoxic risk than dung fromcattle treated with injection or pour-on.
When administered as intraruminal bolus in sheep orcattle, ivermectin has been shown to remain active forover 100 days (O’Brien et al., 1999); however, 80% of thedose was found to be excreted within 7 days from cattleas opposed to 69% from sheep (Steel, 1993). An albenda-zole bolus, provided sustained concentrations of measuredmetabolites for 105 days in sheep and 85 days in cat-tle (Delatour et al., 1990), resulting in prolonged residueexposure to invertebrates (Kolar et al., 2006). Cattle andsheep may also show differential excretion profiles whenanthelmintics are used in combination; use of a formula-tion of ivermectin and rafoxanide delayed 50% eliminationfrom 2.04 days for ivermectin alone to 3.3 days when usedin combination in sheep and from 4.95 days to 5.5 days,respectively, in cattle (El-Banna et al., 2008).
Faecal excretion following pour-on administration hasbeen shown to be similar in sheep and cattle; eprinomectin,after pour-on administration gave peak concentrations infaeces after 3 days in both cattle and sheep, and wasdetectable in dung for >29 days in cattle and >32 days insheep (Lumaret et al., 2005; Erzen et al., 2007). However,there are clear excretion differences following treatmentwith injectable products (Sommer et al., 1992; Lumaretet al., 1993; Cook et al., 1996).
Following injection, ivermectin and moxidectin wereshown to have persistent activity against gastrointestinalparasites for 21 days and 33 days in cattle, respectively,and for 10 and 35 days in sheep, respectively (McKellar,1997). After a subcutaneous injection of abamectin, peakexcretion in faeces occurred 3 days after treatment in bothsheep and cattle (Goudie et al., 1993), whilst doramectincan persist in sheep faeces for up to 32 days in the fieldcompared to a half-life of 15 days in cattle dung (Dadouret al., 2000).
4.2. Ecotoxic impacts
As with faecal excretion, the ecotoxic impacts ofanthelmintics in sheep may be considerably different tothose seen in cattle (Table 2); generally they are muchmore transient in sheep than in cattle dung. However, inalmost all studies, different modes of endectocide admin-istration in cattle and sheep make interpretation difficult.The dung beetles Ap. constans and Aphodius haemorrhoidalisand the fly Neomyia cornicina were reared in dung, whichhad been collected immediately after and up to 38 daysafter treatment from cattle given an injectable anthelminticor sheep given an anthelmintic drench administration. Incattle dung, there was no effect of either moxidectin orivermectin on Ap. haemorrhoidalis emergence, although in
sheep dung, emergence of Ap. constans was reduced for 6days (ivermectin) or 2 days (moxidectin) post-treatment.In cattle dung, moxidectin reduced N. cornicina emergencefor >10 days and ivermectin caused 100% mortality for >20ogy 189 (2012) 113– 124
days, reducing emergence until 34 days after treatment;in sheep dung, moxidectin reduced emergence of N. cor-nicina for 3 days post-treatment and ivermectin caused100% mortality for 5 days, with no impact >6 days post-treatment (Kadiri et al., 1999). Larval mortality of theAustralian bushfly Musca vetustissima was 100% after expo-sure to cattle dung from 3 to 25 days post-administration ofan abamectin injection, as well as after exposure to sheepdung for up to 6 days post-administration of ivermectindrench; no toxic effects in sheep dung were detectable 28days after administration (Wardhaugh and Mahon, 1991),suggesting more transient toxicity in sheep when com-pared to cattle dung. However, effects of the residues mustbe distinguished from administration method and possi-ble underlying differences in dipteran larval developmentrates in sheep or cattle dung (Wardhaugh and Rodriguez-Menendez, 1988; Wardhaugh et al., 1993).
Dung attractiveness may also vary between sheep andcattle dung. A study with sheep and cattle in Australiacompared the attractiveness and fly survival in dung fromanthelmintic-treated animals (Wardhaugh and Mahon,1991). Cattle were given a subcutaneous injection of iver-mectin, whilst sheep were treated orally with the samedrug. Dung beetles appeared to be more attracted to thecattle dung containing residues of ivermectin (∼61%) thancontrol cattle dung (∼39%), but the attractive effect of treat-ment was reduced somewhat in sheep dung (treated ∼54%,control ∼46%). This can have implications for terms of thenumber of dung beetles likely to come into contact withtreated dung.
5. Ecotoxic impacts of sheep anthelmintics on dungand soil fauna
5.1. Toxicity of anthelmintics
Ivermectin, after oral administration to sheep, has beenshown to have both a lethal and sub-lethal effect oncoprophagous flies and dung beetles. Much of the work hasfocussed on the impact of residues on the blowfly, Luciliacuprina, since this is an economically important agent ofcutaneous myiasis in sheep, which can be controlled withtopical treatment of ivermectin. Nevertheless, it is possibleto infer similar effects on non-pest species, as confirmedin the cattle literature. Impacts of orally administered iver-mectin in sheep dung on L. cuprina include adverse effectson male mating behaviour, ovarian development, egg pro-duction, oviposition and adult survival (Cook, 1991, 1993;Mahon and Wardhaugh, 1991; Mahon et al., 1993). How-ever, such impacts are likely to be reduced in the field, sinceL. cuprina require a high-protein food source, in additionto dung, to ensure egg development. Faeces from sheeptreated orally with ivermectin have also been shown tobe toxic to the bush fly, M. vetustissima, for dung collectedfor up to 1 week post-treatment (Wardhaugh et al., 1993).Dung from ivermectin treated sheep collected 1 day post-treatment caused a reduction in fecundity of the dung
beetle, Euoniticellus fulvus and delayed reproductive devel-opment. Interestingly, this effect was transient and beetlesre-gained reproductive capacity when transferred to un-treated dung; immediately post-treatment, dung caused
S.A. Beynon / Veterinary Parasitology 189 (2012) 113– 124 117
Table 2Duration (days) of lethal, sub-lethal and attractive effects of avermectins and moxidectin in sheep and cattle dung.
Insect/parametre tested Anthelmintic used Mode of anthelminticadministration
Duration of effectsin sheep dung
Duration of effectsin cattle dung
Fly larval mortality Avermectin B1 Subcutaneous injection 4–8 28–56Fly fluctuating asymmetry Ivermectin Subcutaneous injection ND 28–77Fly emergence Moxidectin Subcutaneous injection/oral 1–3 >10Fly adult mortality Ivermectin Subcutaneous injection/oral 1–5 >20Fly larval development Ivermectin Subcutaneous injection 1–7 1–32Fly larval mortality Ivermectin Subcutaneous injection/oral 1–6 3–25Dung beetle larval mortality Ivermectin Subcutaneous injection 2–5 14–28Dung beetle adult mortality Ivermectin Subcutaneous injection 1–2 3–5Dung beetle adult fecundity Ivermectin Subcutaneous injection 1–2 7–14Dung beetle emergence Moxidectin Subcutaneous injection 1–2 NDDung beetle emergence Ivermectin Subcutaneous injection 1–6 NDDung attractiveness Ivermectin Subcutaneous injection/oral 1 >25
Table compiled from data published by Gover and Strong (1995, 1996a,b), Houlding et al. (1991), Kadiri et al. (1999), Ridsill-Smith (1988), Roncalli (1989),S 993) an
1(
tfwdetlmOef
atoimrfetctcfiegor
oidppdWtm
ommer et al. (1992), Wardhaugh and Mahon (1991), Wardhaugh et al. (1
00% larval mortality, which had disappeared 5 days laterWardhaugh et al., 1993).
Sustained release boluses are of particular concern inerms of long-lasting potential ecotoxic impacts. Faecesrom sheep treated with an albendazole or ivermectin bolusere fed to larvae of the face fly, Musca autumnalis, and theung beetles, Onthophagus taurus and E. fulvus (Wardhaught al., 2001). There was no impact of albendazole on bee-le or fly survival. However, no fly and almost no beetlearvae survived for up to 39 days post-treatment with iver-
ectin. Ivermectin affected the survival of newly emerged. taurus, but not of sexually mature adults, with sub-lethalffects including delayed sexual maturation and reducedecundity.
The few studies, which investigated the impact of sheepnthelmintics on soil fauna and functioning, provide con-rasting results. Yeates et al. (2007a) found no impactn soil nematodes of faeces from sheep treated withntraruminal boluses containing benzimidazole or iver-
ectin. However, using the same treatments, a reducedate of decomposition was found in plots with dungrom benzimidazole or ivermectin treated sheep (Yeatest al., 2007b). After 50 days, there were fewer soil nema-odes in plots with dung from ivermectin treated sheep,ompared to plots with no dung at all. There was noreatment effect on enchytraeids, rotifers, tardigrades oropepods. Nevertheless, comprehensive new designs foreld (Römbke et al., 2009b) and laboratory (Römbket al., 2009a, 2010) assessments of pesticide impacts, sug-est that the effects of anthelmintics on nematodes andther soil meso- and macro-fauna need further explo-ation.
There may also be marked differences in the durationf toxicity between studies. A comparison of two stud-es by the same authors concluded that dung from sheeprenched with ivermectin was toxic to L. cuprina for 24 host-treatment (Mahon et al., 1993) as opposed to 138 host-treatment (Mahon and Wardhaugh, 1991). Reduced
ung protein content due to pasture quality in Mahon andardhaugh (1991) was associated with an extended dura-ion of toxicity, suggesting that flies may have had to eatore dung to meet their protein requirements. The authors
d Wardhaugh and Rodriguez-Menendez (1988). ND: no data.
suggested that there may be an interaction between toxic-ity and protein; the drug may be less toxic to flies receivingadequate protein resources. Alternatively, freezing of dungmay have reduced toxicity.
Amino aceto-nitrile derivatives are a new class ofanthelmintics (Ducray et al., 2008; Kaminsky et al., 2008).Monepantel is the first member of that group and acts bymeans of a nematode-specific molecular target (Monganet al., 2002); therefore, it has been suggested that thesedrugs should not have any impact on non-target dunginvertebrates. As with other drugs, pharmacokinetics ofmonepantel can vary with factors, such as sheep breed,age and sex, with monepantel sulfone as the primaryresidue in sheep faeces (Hosking et al., 2010). In a eco-toxicity study, monepantel or its sulfone metabolite weremixed with cattle dung for testing on the yellow dungfly, Scathophaga stercoraria (eggs), and the dung beetle Ap.constans (larvae) (Skripsky and Hoffmann, 2010). The no-observed effect concentrations (NOECs) for monepanteland the sulfone metabolite respectively were >1000 mg/kgand 500 mg/kg substrate for S. stercoraria and 250 mg/kgand 125 mg/kg, respectively, for Ap. constans. When sheepwere treated with a 42% higher than recommended doseof monepantel, respective faecal concentrations of thedrug and its sulfone metabolite, were 15 and 4.5 mg/kg(at 24 h after treatment) and 6.4 and 4 mg/kg (at 48 hafter treatment). This suggests that faecal concentrationswere not high enough to cause an eco-toxic effect onthese non-target dung fauna. However, the nematode-specific action of monepantel requires further research ona possible impact on soil nematodes, a functionally veryimportant group of organisms, but still understudied in thiscontext. Higher-tier tests on community interactions arealso necessary to validate that monepantel has no impacton dung-fauna, underlying soil communities or on dungdecomposition.
5.2. Toxicity of alternative treatments
There is a wealth of literature on the in vitro and,to a lesser extent, the in vivo efficacy of putative alter-native agents for parasite control in sheep, but there
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118 S.A. Beynon / Veterinary Pare environment-fate data for only two: the nematode-trapping fungus, Duddingtonia flagrans, and grazing thehigh-tannin forage, chicory, Cichorium intybus.
Under some circumstances, D. flagrans may significantlyreduce parasite burdens in sheep and infective nematodelarvae on pasture (Githigia et al., 1997; Larsen, 2000; Penaet al., 2002). Concerns regarding spread of D. flagrans out-side the faecal pat have been highlighted, with the potentialfor the fungus to impact the soil food-web. However, lit-tle or no growth beyond the pat was recorded when D.flagrans was fed to either cattle or sheep (Faedo et al.,2002; Knox et al., 2002). However, D. flagrans may dis-perse as mycelium and soil dilution methods used in thisstudy would underestimate soil fungus concentration. Inaddition, overall recovery was low. D. flagrans is indiscrim-inate in its infection of nematodes and, thus, may impactbeneficial soil nematode populations, which have beensuggested as bio-indicators in environmental monitoring(Bongers and Ferris, 1999). In a field study, no impact ofD. flagrans was found on sheep dung disappearance, earth-worms or other macro/meso-invertebrates (Yeates et al.,2007b). However, a reduction in nematode channel ratiowas detected in D. flagrans plots, which could be explainedby an increase in earthworm activity, rather than a directimpact of D. flagrans on soil nematodes. No other impactson soil nematodes or other nematode-trapping fungi werefound, in agreement with other studies (Yeates et al., 1997,2002, 2003, 2007a; Dimander et al., 2003). A single studysuggests no impact of D. flagrans on the emergence of thedung beetle Ap. constans when eggs were added to dungfrom goats fed a daily dose of D. flagrans spores (Paraudet al., 2007). However, mean percentage of adult beetlesemerging from eggs (n = 10) was low, ranging from 29% to36% in treatment groups, compared with 37% in the control.Hence, it seems difficult to conclude whether D. flagransmight affect dung beetle emergence. No effect of D. flagranshas been seen on the degradation of cattle dung pats fromtreated animals (Fernandez et al., 1999; Dimander et al.,2003). However, it is worth noting that Fernandez et al.(1999) also failed to detect an impact of ivermectin on thedecomposition of dung and Dimander et al. (2003) onlyweighed pats once at 8 weeks post-deposition, hence nottaking into account decomposition rate or post-8th weekdecomposition. Nevertheless, there is clearly a need for fur-ther work on dung insects, as well as long-term studies toassess the possibility of the establishment of D. flagrans insoil, where animals have been treated repeatedly. Studiesmust take into account the effect of climate, soil type, soilmicroorganisms and macro-fauna present, all which havebeen suggested to affect D. flagrans establishment (Faedoet al., 2002) and have been shown to affect the establish-ment of other nematophagous fungi in soil (Jensen et al.,1997).
Grazing sheep on chicory has also been suggested as aneffective alternative method for control of internal para-sites (Marley et al., 2003, 2006; Heckendorn et al., 2007).The impact on non-target invertebrates has been investi-
gated in only one study by Williams and Warren (2004).Faecal decomposition was compared between four veg-etation types: chicory, two species of rye grass, Loliumperenne and L. repens, and white clover, Trifolium repens.ogy 189 (2012) 113– 124
Interactions between treatments made interpretation ofthe results complex but, overall, faecal decomposition(from all treatments), was slower in chicory than in otherplots. Faster rates of decomposition were associated witha higher abundance of insects attracted to un-baited pit-fall traps. Interestingly, when sheep were introduced to theplots, the results were reversed with dung breaking downmore quickly in chicory plots. In a common rye grass, L.perenne, sward, there was no effect of treatment on break-down, but rather surprisingly, chicory faeces in chicoryplots broke down more quickly than rye grass faeces inrye grass plots. The authors suggested that in the chicoryplots, sheep developed more latrine areas, which may havebeen more attractive to dung insects than dung in the moreevenly distributed rye grass plots. It should be taken intoconsideration that the methods used would have excludedany dung beetles >0.8 cm in diameter and un-baited pit-fall traps would not have trapped dung-fauna, but ratherbeen targeted at surface-active insects, such as the groundbeetles (Coleoptera: Carabidae). Nevertheless, this studyhighlights the fact that alternative methods of parasite con-trol may also affect dung insect populations and associateddung breakdown, necessitating further study on dung andsoil invertebrates as well as faecal decomposition.
5.3. Dung decomposition
For many years there has been an on-going debate asto the potential of anthelmintics to affect dung decom-position, as despite decomposition retardation beingwell-documented, some studies fail to detect any effect(e.g. Wratten et al., 1993; Hirschberger and Bauer, 1994).Studies of decomposition data following treatment withanthelmintics other than ivermectin are relatively sparse,with what evidence there is suggesting that functionalimpacts are likely to be common. One exception to thismay be dichlorvos (Lumaret, 1986; Kruger et al., 1998).Whilst most studies concentrate on dung beetles as themost functionally important group of dung fauna, anassociated functional effect of dipterans on dung decom-position has been suggested (Madsen et al., 1990; Hanski,1991). A sophisticated experimental approach manipu-lated evenness levels of a three-species assemblage ofdung beetles, dung flies and epigeic earthworms. Theresults suggested positive, predictable impacts on dungdecomposition with positive (fly-earthworm), negative(beetle-earthworm) and neutral (beetle-fly) species inter-actions (O’Hea et al., 2010a,b). The heightened toxic impactof anthelmintics on flies when compared to beetles maytherefore have a functional impact greater than previouslysuggested. However, further work is necessary to clarifythese relationships. King (1993a) suggested that if sheepwere treated orally with ivermectin three times a year anddung was toxic to dung insects for 6 days post-treatment,toxic dung would be present on pasture for 18/365 dayseach year, causing a 5% reduction in pasture phosphorus if
no biological cycling occurred during this period. Althoughthis simplistic approach may not realistically representwhat would happen in a complex pasture environment, itnevertheless presents a road for further work.
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.4. Area-wide and long-term impacts
The functional effect, if any, of effects on the wider land-cape level, pastureland community and pasture fertilityas received less attention to date, probably because ofhe huge difficulties associated with its study on an appro-riate ecological scale. However, the large-scale ecotoxicffects of ivermectin (Wall and Beynon, 2012) excreted inattle dung have been deemed of sufficient magnitude toontribute to significant reductions in dung beetle popu-ations in the field. A model simulating the effect of drugesidues on dung beetle populations (Wardhaugh et al.,998) suggested that intraruminal boluses have the poten-ial to cause significant impacts on dung beetle populations,specially if their use coincides with beetle emergenceWardhaugh et al., 1993, 2001). It has been suggested thathe rapid excretion of orally administered anthelminticsn sheep will result in little impacts on insect populationsWardhaugh et al., 1993; King, 1993a). However, intraru-
inal boluses, and to a lesser extent, pour-on and injectableharmaceutical forms may impact dung beetle popula-ions.
Perhaps because of the considerable difficulty associ-ted with large-scale field studies, more recent attentionas focussed on the use of modelling to try to esti-ate likely impacts (Sherratt et al., 1998; Wardhaugh andahon, 1998; Wardhaugh et al., 2001; Vale and Grant,
002; Boxall et al., 2007). Models are currently limited toffects of cattle anthelmintics, but could easily be mod-fied for sheep. Currently, the models have a numberf limitations, focusing on the short-term, within-seasonnsect mortality and without considering species inter-ctions, such as competition, density-dependent effectsHirschberger, 1995, 1999) or sub-lethal impacts (Strongnd James, 1993). However, they offer great potential inssisting in the understanding of area-wide impacts ofnthelmintics.
. Future directions
The impact of sheep anthelmintics on the environments still largely unknown. Despite a large body of work withattle dung, it is not possible to compare that directly toheep dung, as pharmokinetics and ecotoxicity of drugsave marked differences in these two species (Table 2).dditionally, ecotoxic risks associated with drug interac-
ions is something that has received very little attentionThompson, 1996). The main question remains as: ‘whatre the large-scale, long-term effects of anthelmintic drugs onhe environment?’ Opinion is currently split; whilst impactsre seen at the species level, more important in terms ofcosystem functioning are those effects and interactions athe population, community, food web, ecosystem and land-cape level (Edwards, 2002). Collating spatial and temporalsage patterns on the use of anthelmintics from coun-ries where little data are available and the developmentf analytical procedures to measure parent drugs and their
etabolites and degradation products is vital in assessingarge-scale environmental impacts. Additionally, studieso compare excretion profiles between sheep and cattlesing the same mode of application are vital in moving
ogy 189 (2012) 113– 124 119
knowledge forward on the environmental impacts of sheepanthelmintics.
Care must be taken in inferring from standardised eco-toxicity tests for veterinary medicines, which focus onlaboratory-derived, species-specific impacts, as often field-effects involve more complicated interactions and thusdiffer. For example, both abamectin and doramectin may bemore toxic in faeces from recently treated sheep than stan-dard soil toxicity tests using the parent compound (Kolaret al., 2008). The need for work on the pharmokineticsand ecotoxicity of the parent compound and its metabo-lites is thus a priority. However, field-effects are oftenunpredictable, due to these complex patterns and pro-cesses within natural communities. Additionally, speciesinteractions may influence the response of test organismsto toxic substances (Jensen et al., 2009). Very few stud-ies have assessed the impact of veterinary medicines oncommunity interactions, largely due to the complex natureof such systems. It is necessary to validate higher-tiermethods to be incorporated in anthelmintic environmen-tal impact testing (e.g. Jochmann et al., 2011). Semi-fieldmicrocosm/mesocosm studies may be able to bridge thegap between laboratory and field experiments, allow-ing structural and functional impacts to be measuredunder semi-controlled conditions (Edwards, 2002). Such anapproach is time, labour- and space-efficient when com-pared to field trials and can be used to extrapolate speciesdata to the ecosystem level. Methods as those suggestedby King (1993b) may be adapted to allow the simultaneousstudy of macro-arthropod, meso-arthropod and microbialeffects of parasiticides. At a landscape scale, learning fromwork on spatial patterns and process (e.g. Roslin, 2001)would be beneficial.
The development of modelling approaches should allowscaling-up from species- or pasture-specific studies toenable predictions to be made of impacts at the ecosys-tem scale. In doing this, it is important to quantify therole of refugia in the pasture system (Wardhaugh andRidsdill-Smith, 1998). Reducing the proportion of ani-mals treated within a flock or undertaking rotation ofanthelmintic compounds administered to animals aremethods to minimising any large-scale impacts (Webbet al., 2010). However, sub-lethal effects of anthelminticsin the environment may reduce refugia effectiveness. Thepotential chronic effects from long-term low exposures arealso cause for concern. Additionally, when treatment coin-cides with the emergence of poor-dispersing non-targetspecies (e.g. flightless Geotrupidae, such as G. vernalis), localextinction may occur.
Lumaret and Errouissi (2002) asked the importantquestion whether we protect the ecosystem function(decomposition) or the ecosystem structure (speciesor populations). However, autecology of species-specificfunctioning and responses to anthelmintics are lack-ing. Experiments are generally limited to commonspecies, with field studies taking place on species-impoverished improved grassland. Such species-specific
toxicity responses have been reported in flies (Mahon et al.,1993), dung beetles (Sommer et al., 1993) and soil fauna(Kolar et al., 2008). Linking a species-specific toxic effect tothe species role in functioning is an important next stage in
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120 S.A. Beynon / Veterinary Pidentifying functionally important species. This is not lim-ited to dung biota; with the odd exception (Westergaardet al., 2001; Sommer and Bibby, 2002), effects on soilbiota functioning, the risk to aquatic invertebrates (Boxallet al., 2007) and possible bio-magnification through thefood chain to higher vertebrates have been ignored. Theindirect impact of removal of prey items impacting insec-tivorous vertebrates that rely on coprophagous insectsis notoriously difficult to assess and has received littleattention with the exception of a study on the burrow-ing owl (Athene culicularia). It was concluded that relianceon coprophagous insects was not sufficient to impact owlfood supply (Floate et al., 2008). However, coprophagousinsects are important in the diet of vertebrates, includ-ing the greater horseshoe bat (Rhinolophus ferrumequinum)(Ransome and Priddis, 2004) and the chough (Pyrrhoco-rax pyrrhocorax) (Kerbiriou and Julliard, 2007), so ecotoxiceffects on dung invertebrates have the potential to impactthese species.
To date, the non-target impacts of sheep para-siticides have been considered acceptable, because ofthe economic importance of parasite control. However,increasing parasite resistance and the beginnings ofinsights into long-term effects on species, communitiesand ecosystem functioning are leading to conclusionsthat more sustainable approaches utilising both conven-tional anthelmintics and alternative methods need to beinvestigated. Research into the potential environmentalimpacts of new anthelmintic classes (e.g. monepantel), aswell as new modes of application (e.g. long-acting injec-tions) are obvious research priorities. There is no doubtthat veterinary anthelmintics are important in sustainablesheep production, but in order to prolong their efficacyand reduce their environmental impacts, other strategiesshould be investigated. These include housing sheep aftertreatment (Lumaret et al., 2005), breeding for resistance(Hooda et al., 1999) and rotational pasture managementwith other livestock species (Barger, 1997). Research intoalternative treatments may also help to provide answers formore sustainable control. High-tannin forages and herbshave shown promise in vitro and in vivo, whilst nutraceu-ticals, including protein supplementation, can enhanceperi-parturient immunity and contribute in managementof parasitic infections (Kidane et al., 2009; Iposu et al.,2010; Kidane et al., 2010). Minerals and trace elements,such as copper (Burke et al., 2004) and other high-tanninforages, such as birdsfoot trefoil, Lotus corniculatus (Marleyet al., 2003) also demonstrate efficacy against gastrointesti-nal parasites. However, the environmental impact of suchalternatives must also be assessed.
7. Concluding remarks
The impact of veterinary anthelmintics on soil anddung biota provides an ecologically interesting model tostudy biological interactions, thus offering research oppor-tunities. Integrated ecological and applied parasitological
studies should combine to provide an insight into theways in which large-scale and long-term fundamentalecological patterns and processes are disrupted by veteri-nary anthelmintics. Additionally, an integrated approachogy 189 (2012) 113– 124
between ecologists and economists should be furtherexplored, as put forward by (Folke et al., 1993), in orderto increase understanding and awareness of the economicimportance of maintaining functional pasture systems.Importance should also be placed on the disseminationof knowledge to the farmers, who are directly involved inmaking decisions about the type and frequency of antipar-asitic treatments. Farmers’ concerns regarding overuseof parasiticides are almost entirely based on the prob-lem of parasite resistance, due to a lack of knowledge orunderstanding of the functional consequences of eco-toxicresidue effects. The approach by Losey and Vaughan (2006),who put an economic value on ecosystem function, shouldbe expanded if the grass-roots decision-makers are to makethe applied changes that could reduce the impact of sheepanthelmintics on the environment.
Conflict of interest statement
The author has no conflicts of interest that might undulyinfluence their work.
Acknowledgements
Thanks to Richard Wall and Owen Lewis for their helpfulcomments on an earlier version of this review.
References
Anderson, J.R., Merritt, R.W., Loomis, E.C., 1984. The insect-free cattledropping and its relationship to increased dung fouling of rangelandpastures. J. Econ. Entomol. 77, 133–141.
Araujo, J.V.D., Santos, M.A.D., Ferraz, S., 1995. Effect of anthelmintic drugson predacious fungi Arthrobotrys. Naturalia (Rio Claro) 20, 157–163.
Barger, I., 1997. Control by management. Vet. Parasitol. 72, 493–500.Bergstrom, R.C., Maki, L.R., Werner, B.A., 1976. Small dung beetles as bio-
logical control agents—laboratory studies of dung beetles action onTrichostrongylid eggs in sheep and cattle feces. Proc. Helm. Soc. Wash.43, 171–174.
Blume, R.R., Younger, R.L., Aga, A., Myers, C.J., 1976. Effects of residues ofcertain anti helminthics in bovine manure on Onthophagus gazella anon-target organism. Southwest. Entomol. 1, 100–103.
Bongers, T., Ferris, H., 1999. Nematode community structure as a bioindi-cator in environmental monitoring. Trends Ecol. Evol. 14, 224–228.
Boxall, A.B.A., Fogg, L.A., Baird, D.J., Lewis, C., Telfer, T.C., Kolpin, D., Grav-ell, A., Pemberton, E., Boucard, T., 2006. Targeted Monitoring Studyfor Veterinary Medicines in the Environment. Environment AgencyReport.
Boxall, A.B.A., Fogg, L.A., Blackwell, P.A., Kay, P., Pemberton, E., 2002.Review of Veterinary Medicines in the Environment. EnvironmentAgency Report.
Boxall, A.B.A., Kolpin, D.W., Halling-Sørensen, B., Tolls, J., 2003. Are veteri-nary medicines causing environmental risks? Environ. Sci. Technol.37, 286A–294A.
Boxall, A.B.A., Sherratt, T.N., Pudner, V., Pope, L.J., 2007. A screening levelindex for assessing the impacts of veterinary medicines on dung flies.Environ. Sci. Technol. 41, 2630–2635.
Burke, J.M., Miller, J.E., Olcott, D.D., Olcott, B.M., Terrill, T., 2004. Effectof copper oxide wire particles dosage and feed supplement level onHaemonchus contortus infection in lambs. Vet. Parasitol. 123, 235–243.
Burridge, L.E., Haya, K., 1993. The lethality of ivermectin, a potential agentfor treatment of salmonids against sea lice, to the shrimp Crangonseptemspinosa. Aquaculture 117, 9–14.
Cook, D.F., 1991. Ovarian development in females of the Australian sheepblowfly Lucilia cuprina (Diptera, Calliphoridae) fed of sheep feces andthe effect of ivermectin residues. Bull. Entomol. Res. 81, 249–256.
Cook, D.F., 1993. Effect of avermectin residues in sheep dung on mat-ing of the Australian sheep blowfly Lucilia cuprina. Vet. Parasitol. 48,205–214.
Cook, D.F., Dadour, I.R., Ali, D.N., 1996. Effect of diet on the excretion profileof ivermectin in cattle faeces. Int. J. Parasitol. 26, 291–295.
arasitol
d
D
D
D
D
D
D
D
D
D
E
E
E
E
E
F
F
F
F
F
F
F
F
S.A. Beynon / Veterinary P
’Alexis, S., Loranger-Merciris, G., Mahieu, M., Boval, M., 2009. Influenceof earthworms on development of the free-living stages of gastroin-testinal nematodes in goat faeces. Vet. Parasitol. 163, 171–174.
adour, I.R., Cook, D.F., Hennessy, D., 2000. Reproduction and survivalof the dung beetle Onthophagus binodis (Coleoptera: Scarabaeidae)exposed to abamectin and doramectin residues in cattle dung. Envi-ron. Entomol. 29, 1116–1122.
avis, A.L.V., Scholtz, C.H., Kryger, U., Deschodt, C.M., Strumpher, W.P.,2010. Dung beetle assemblage structure in Tswalu Kalahari Reserve:responses to a mosaic of landscape types, vegetation communities,and dung types. Environ. Entomol. 39, 811–820.
elatour, P., Benoit, E., Lechenet, J., Besse, S., 1990. Pharmokinetics insheep and cattle of albendazole administered by an intraruminal slowrelease capsule. Res. Vet. Sci. 48, 271–275.
iao, X.P., Jensen, J., Hansen, A.D., 2007. Toxicity of the anthelminticabamectin to four species of soil invertebrates. Environ. Pollut. 148,514–519.
imander, S.O., Hoglund, J., Waller, P.J., 2003. Disintegration of dungpats from cattle treated with the ivermectin anthelmintic bolus,or the biocontrol agent Duddingtonia flagrans. Acta Vet. Scand. 44,171–180.
ormont, L., Jay-Robert, P., Bessiere, J.M., Rapior, S., Lumaret, J.P., 2010.Innate olfactory preferences in dung beetles. J. Exp. Biol. 213,3177–3186.
ormont, L., Rapior, S., McKey, D.B., Lumaret, J.P., 2007. Influence of dungvolatiles on the process of resource selection by coprophagous beetles.Chemoecology 17, 23–30.
oube, B.M., Wardhaugh, K.G., 1991. Habitat associations and niche par-titioning in an island dung beetle community. Acta Oecol. Int. J. Ecol.12, 451–459.
ucray, P., Gauvry, N., Pautrat, F., Goebel, T., Fruechtel, J., Desaules, Y.,Weber, S.S., Bouvier, J., Wagner, T., Froelich, O., Kaminsky, R., 2008.Discovery of amino-acetonitrile derivatives, a new class of syntheticanthelmintic compounds. Bioorg. Med. Chem. Lett. 18, 2935–2938.
dwards, C.A., 2002. Assessing the effects of environmental pollutants onsoil organisms, communities, processes and ecosystems. Eur. J. SoilBiol. 38, 225–231.
l-Banna, H.A., Goudah, A., El-Zorba, H., Abd-El-Rahman, S., 2008. Compar-ative pharmacokinetics of ivermectin alone and a novel formulationof ivermectin and rafoxanide in calves and sheep. Parasitol. Res. 102,1337–1342.
rzen, N.K., Hodoscek, L., Cerkvenik-Flajs, V., 2007. Analytical procedurefor determination of the time profile of eprinomectin excretion insheep faeces. Anal. Bioanal. Chem. 387, 1329–1335.
scher, B.I., Berger, C., Bramaz, N., Kwon, J.H., Richter, M., Tsin-man, O., Avdeef, A., 2008. Membrane-water partitioning, membranepermeability, and baseline toxicity of the parasiticides iver-mectin, albendazole, and morantel. Environ. Toxicol. Chem. 27,909–918.
uropean Commission, 1992. Directive 92/18/ECC, 20th March 1992,Modifying the Annex to Council Directive 81/852/ECC on theapproximation of the laws of Member States relating to analytical,pharmacotoxicological and clinical standards and protocols in respectof the testing of veterinary medicinal products. Off. J. Eur. CommissionL097, 1–23.
aedo, M., Larsen, M., Dimander, S.O., Yeates, G.W., Hoglund, J., Waller, P.J.,2002. Growth of the fungus Duddingtonia flagrans in soil surroundingfeces deposited by cattle or sheep fed the fungus to control nematodeparasites. Biol. Contr. 23, 64–70.
ernandez, A.S., Larsen, M., Nansen, P., Henningsen, E., Gronvold, J.,Wolstrup, J., Henriksen, S.A., Bjorn, H., 1999. The ability of thenematode-trapping fungus Duddingtonia flagrans to reduce the trans-mission of infective Ostertagia ostertagi larvae from faeces to herbage.J. Helminthol. 73, 115–122.
incher, G.T., 1981. The potential value of dung beetles in pasture ecosys-tems. J. Ga. Entomol. Soc. 16, 316–333.
inn, J.A., Giller, P.S., 2002. Experimental investigations of colonisation bynorth temperate dung beetles of different types of domestic herbivoredung. Appl. Soil Ecol. 20 (1), 1–13.
loate, K.D., 1999. Environmental concerns regarding the use of the iver-mectin sustained-release bolus in cattle. Can. Vet. J. 40, 151–152.
loate, K.D., 2006. Endectocide use in cattle and fecal residues: environ-mental effects in Canada. Can. J. Vet. Res. 70, 1–10.
loate, K.D., Bouchard, P., Holroyd, G., Poulin, R., Wellicome, T.I., 2008. Does
doramectin use on cattle indirectly affect the endangered burrowingowl? Rangel. Ecol. Manag. 61, 543–553.loate, K.D., Wardhaugh, K.G., Boxall, A.B.A., Sherratt, T.N., 2005. Fecalresidues of veterinary parasiticides: nontarget effects in the pastureenvironment. Annu. Rev. Entomol. 50, 153–179.
ogy 189 (2012) 113– 124 121
Folke, C., Perrings, C., McNeely, J.A., Myers, N., 1993. Biodiversity conser-vation with a human face—ecology, economics and policy. Ambio 22,62–63.
Förster, B., Boxall, A.B.A., Coors, A., Jensen, J., Liebig, M., Pope, L.J., Moser, T.,Römbke, J., 2011. Fate and effects of ivermectin on soil invertebratesin terrestrial model ecosystems. Ecotoxicology 20, 234–245.
Githigia, S.M., Thamsborg, S.M., Larsen, M., Kyvsgaard, N.C., Nansen, P.,1997. The preventive effect of the fungus Duddingtonia flagrans ontrichostrongyle infections of lambs on pasture. Int. J. Parasitol. 27,931–939.
Gittings, T., Giller, P.S., 1998. Resource quality and the colonisation andsuccession of coprophagous dung beetles. Ecography 21, 581–592.
Gittings, T., Giller, P.S., Stakelum, G., 1994. Dung decomposition in con-trasting temperate pastures in relation to dung beetle and earthwormactivity. Pedobiologia 38, 455–474.
Goudie, A.C., Evans, N.A., Gration, K.A.F., Bishop, B.F., Gibson, S.P., Holdom,K.S., Kaye, B., Wicks, S.R., Lewis, D., Weatherley, A.J., Bruce, C.I., Herbert,A., Seymour, D.J., 1993. Doramectin—a potent novel endectocide. Vet.Parasitol. 49, 5–15.
Gover, J., Strong, L., 1995. Effects of ingested ivermectin on body massand excretion in the dung fly, Neomyia cornicina. Physiol. Entomol. 20,93–99.
Gover, J., Strong, L., 1996a. Determination of the toxicity of faeces of cattletreated with an ivermectin sustained-release bolus and preferencetrials using a dung fly, Neomyia cornicina. Entomol. Exp. Appl. 81,133–139.
Gover, J., Strong, L., 1996b. Effects of ingestion of dung containing iver-mectin on aspects of behaviour in the fly, Neomyia cornicina. Physiol.Entomol. 21, 51–58.
Halley, B.A., Jacob, T.A., Lu, A.Y.H., 1989a. The environmental impact of theuse of ivermectin—environmental effects and fate. Chemosphere 18,1543–1563.
Halley, B.A., Nessel, R.J., Lu, A.Y.H., 1989b. Environmental aspects of iver-mectin usage in livestock: general considerations. In: Campbell, W.C.(Ed.), Ivermectin and Abamectin. Springer, Berlin, Heidelberg, NewYork, pp. 163–172.
Halling-Sørensen, B., Jensen, J., Tjornelund, J., Montforts, M.H.M.M., 2001.Worst-case estimates of predicted environmental soil concentrations(PEC) of selected veterinary antibiotics and residues used in Danishagriculture. In: Kummerer, K. (Ed.), Pharmaceuticals in the Environ-ment. Springer Verlag, Berlin, pp. 143–157.
Hanski, I., 1991. The dung insect community. In: Hanski, I., Camberfort, Y.(Eds.), Dung Beetle Ecology. Princeton University Press, Princeton, NJ,pp. 5–22.
Heckendorn, F., Haring, D.A., Maurer, V., Senn, M., Hertzberg, H., 2007.Individual administration of three tanniferous forage plants to lambsartificially infected with Haemonchus contortus and Cooperia curticei.Vet. Parasitol. 146, 123–134.
Hempel, H., Scheffczyk, A., Schallnass, H.J., Lumaret, J.P., Alvinerie, M.,Römbke, J., 2006. Toxicity of four veterinary parasiticides on larvae ofthe dung beetle Aphodius constans in the laboratory. Environ. Toxicol.Chem. 25, 3155–3163.
Herd, R., Wardhaugh, K., 1993. Environmental-impact of avermectin usagein livestock—preface. Vet. Parasitol. 48, 1–2.
Hirschberger, P., 1995. Does competition in dung beetles of thegenus Aphodius exist? Mitt. Dtsch. Ges. Allg. Angew. Entomol. 10,481–484.
Hirschberger, P., 1999. Larval population density affects female weightand fecundity in the dung beetle Aphodius ater. Ecol. Entomol. 24,316–322.
Hirschberger, P., Bauer, T., 1994. The coprophagous insect fauna in sheepdung and its influence on dung disappearance. Pedobiologia 38,375–384.
Hooda, P.S., Yadav, C.L., Chaudhuri, S., Rajpurohitz, B.S., 1999. Variationin resistance to haemonchosis: selection of female sheep resistant toHaemonchus contortus. J. Helminthol. 73, 137–142.
Hosking, B.C., Kaminsky, R., Sager, H., Karadzovska, D., Seewald, W.,Giraudel, J.M., Vercruysse, J., 2010. The effect of sheep breed, age,and gender on the pharmacokinetics and efficacy of monepantel, anamino-acetonitrile derivative. Parasitol. Res. 106, 367–375.
Houlding, B., Ridsdillsmith, T.J., Bailey, W.J., 1991. Injectable abamectincauses a delay in Scarabaeine dung beetle egg-laying in cattle dung.Aust. Vet. J. 68, 185–186.
Iposu, S.O., Greer, A.W., McAnulty, R.W., Stankiewicz, M., Sykes, A.R.,
2010. Does milk supply have long-term benefits for resistance andresilience to nematode parasites in sheep? Small Ruminant Res. 94,142–149.Jensen, C.H., Neumeister, H.G., Lysek, G., 1997. Nematophagousfungi—study by fluorescence microscopy and EDX-technique of
arasitol
122 S.A. Beynon / Veterinary Pthe periodicity of trap formation in soil. Biol. Rhythm Res. 28,365–373.
Jensen, J., Diao, X.P., Hansen, A.D., 2009. Single and two-species tests tostudy effects of the anthelmnintics ivermectin and morantel and thecoccidiostatic monesin on soil invertebrates. Environ. Toxicol. Chem.28, 316–323.
Jensen, J., Diao, X.P., Scott-Fordsmand, J.J., 2007. Sub-lethal toxicityof the antiparasitic abamectin on earthworms and the applicationof neutral red retention time as a biomarker. Chemosphere 68,744–750.
Jensen, J., Krogh, P.H., Sverdrup, L.E., 2003. Effects of the antibacterialagents tiamulin, olanquindox and metronidazole and the anthelminticivermectin on the soil invertebrate species Folsomia fimetaria (Collem-bola) and Enchytraeus crypticus (Enchytraeidae). Chemosphere 50,437–443.
Jochmann, R., Blanckenhorn, W.U., Bussière, L., Eirkson, C.E., Jensen, J.,Kryger, U., Lahr, J., Lumaret, J.P., Römbke, J., Wardhaugh, K.G., Floate,K.D., 2011. How to test non-target effects of veterinary pharmaceu-tical residues in livestock dung in the field. Integr. Environ. Assess.Manag. 7, 287–296.
Jorgensen, S.E., Halling-Sørensen, B., 2000. Drugs in the environment.Chemosphere 40, 691–699.
Kadiri, N., Lumaret, J.P., Janati-Idrissi, A., 1999. Macrocyclic lactones:impact on non-target fauna in pastures. Ann. Soc. Entomol. France35, 222–229.
Kaminsky, R., Ducray, P., Jung, M., Clover, R., Rufener, L., Bouvier, J., Weber,S.S., Wenger, A., Wieland-Berghausen, S., Goebel, T., Gauvry, N., Pau-trat, F., Skripsky, T., Froelich, O., Komoin-Oka, C., Westlund, B., Sluder,A., Maser, P., 2008. A new class of anthelmintics effective against drug-resistant nematodes. Nature 452, 176–U119.
Kerbiriou, C., Julliard, R., 2007. Demographic consequences of prey avail-ability and diet of red-billed choughs Pyrrhocorax pyrrhocorax. BirdStudy 54, 296–306.
Kidane, A., Houdijk, J.G.M., Athanasiadou, S., Tolkamp, B.J., Kyriazakis, I.,2010. Effects of maternal protein nutrition and subsequent grazing onchicory (Cichorium intybus) on parasitism and performance of lambs.J. Anim. Sci. 88, 1513–1521.
Kidane, A., Houdijk, J.G.M., Tolkamp, B.J., Athanasiadou, S., Kyriazakis,I., 2009. Consequences of infection pressure and protein nutritionon periparturient resistance to Teladorsagia circumcincta and perfor-mance in ewes. Vet. Parasitol. 165, 78–87.
King, K.L., 1993a. The potential for avermectins to affect thenutrient economy of grazed pastures. Vet. Parasitol. 48,261–271.
King, K.L., 1993b. Methods for assessing the impact of avermectins onthe decomposer community of sheep pastures. Vet. Parasitol. 48,87–97.
Knox, M.R., Josh, P.F., Anderson, L.J., 2002. Deployment of Duddingtoniaflagrans in an improved pasture system: dispersal, persistence, andeffects on free-living soil nematodes and microarthropods. Biol. Con-trol 24, 176–182.
Kolar, L., Erzen, N.K., 2007. Degradation of abamectin and doramectin insheep faeces under different experimental conditions. Int. J. Environ.Pollut. 31, 22–33.
Kolar, L., Erzen, N.K., Hogerwerf, L., van Gestel, C.A.M., 2008. Toxicity ofabamectin and doramectin to soil invertebrates. Environ. Pollut. 151,182–189.
Kolar, L., Flajs, V.C., Kuzner, J., Marc, I., Pogacnik, M., Bidovec, A., vanGestel, C.A.M., Nevenka, K., 2006. Time profile of abamectin anddoramectin excretion and degradation in sheep faeces. Environ. Pollut.144, 197–202.
Kolar, L., Jemec, A., van Gestel, C.A.M., Valant, J., Hrzenjak, R., Erzen, N.K.,Zidar, P., 2010. Toxicity of abamectin to the terrestrial isopod Porcellioscaber (Isopoda, Crustacea). Ecotoxicology 19, 917–927.
Kollmann, A., Touton, I., Brault, A., Alvinerie, M., Galtier, P., Mougin, C.,2003. Effect of the endectocide ivermectin on filamentous fungi. Env-iron. Chem. Lett. 1, 215–218.
Kruger, K., Scholtz, C.H., Reinhardt, K., 1998. Effects of the pyrethroidflumethrin on colonisation and degradation of cattle dung by adultinsects. S. Afr. J. Sci. 94, 129–133.
Landin, B.-O., 1961. Ecological Studies on Dung-beetles (Coleoptera:Scarabaeidae). Berlingska Boktryckeriet, Lund.
Larsen, M., 2000. Prospects for controlling animal parasitic nematodes bypredacious micro fungi. Parasitology 120, S121–S131.
Lobo, J.M., Hortal, J., Cabrero-Sanudo, F.J., 2006. Regional and local influ-ence of grazing activity on the diversity of a semi-arid dung beetlecommunity. Divers. Distrib. 12, 111–123.
Losey, J.E., Vaughan, M., 2006. The economic value of ecological servicesprovided by insects. Bioscience 56, 311–323.
ogy 189 (2012) 113– 124
Lumaret, J.P., 1986. Deleterious effects of some helminthicids oncoprophagous insects and consequences on the disintegration of dungpads. Acta Oecol. Oec. Appl. 7, 313–324.
Lumaret, J.P., Errouissi, F., 2002. Use of anthelmintics in herbivores andevaluation of risks for the non target fauna of pastures. Vet. Res. 33,547–562.
Lumaret, J.P., Errouissi, F., Galtier, P., Alvinerie, M., 2005. Pour-on formu-lation of eprinomectin for cattle: fecal elimination profile and effectson the development of the dung-inhabiting Diptera Neomyia cornicina(L.) (Muscidae). Environ. Toxicol. Chem. 24, 797–801.
Lumaret, J.P., Galante, E., Lumbreras, C., Mena, J., Bertrand, M., Bernal,J.L., Cooper, J.F., Kadiri, N., Crowe, D., 1993. Field effects of ivermectinresidues on dung beetles. J. Appl. Ecol. 30, 428–436.
Madsen, M., Nielsen, B.O., Holter, P., Pedersen, O.C., Jespersen, J.B.,Jensen, K.M.V., Nansen, P., Gronvold, J., 1990. Treating cattle withivermectin—effects on the fauna and decomposition of dung pats. J.Appl. Ecol. 27, 1–15.
Mahon, R.J., Wardhaugh, K.G., 1991. Impact of dung from ivermectin-treated sheep on oogenesis and survival of adult Lucilia cuprina. Aust.Vet. J. 68, 173–177.
Mahon, R.J., Wardhaugh, K.G., Vangerwen, A.C.M., Whitby, W.A., 1993.Reproductive development and survival of Lucilia cuprina Wiede-mann when fed sheep dung containing ivermectin. Vet. Parasitol. 48,193–204.
Manfredi, M.T., 2006. Biology of gastro-intestinal nematodes of ruminants.Parasitologia (Rome) 48, 397–401.
Marley, C.L., Cook, R., Barrett, J., Keatinge, R., Lampkin, N.H., 2006. Theeffect of birdsfoot trefoil (Lotus corniculatus) and chicory (Cichoriumintybus) when compared with perennial ryegrass (Lolium perenne) onovine gastrointestinal parasite development, survival and migration.Vet. Parasitol. 138, 280–290.
Marley, C.L., Cook, R., Keatinge, R., Barrett, J., Lampkin, N.H., 2003. Theeffect of birdsfoot trefoil (Lotus corniculatus) and chicory (Cichoriumintybus) on parasite intensities and performance of lambs naturallyinfected with helminth parasites. Vet. Parasitol. 112, 147–155.
Martin-Piera, F., Lobo, J.M., 1996. A comparative discussion of trophicpreferences in dung beetle communities. Misc. Zool. (Barcelona) 19,13–31.
McKellar, Q.A., 1997. Ecotoxicology and residues of anthelmintic com-pounds. Vet. Parasitol. 72, 413–426.
Mongan, N.P., Jones, A.K., Smith, G.R., Sansom, M.S.P., Sattelle, D.B., 2002.Novel alpha 7-like nicotinic acetylcholine receptor subunits in thenematode Caenorhabditis elegans. Protein Sci. 11, 1162–1171.
Mougin, C., Kollmann, A., Dubroca, J., Ducrot, P.H., Alvinerie, M., Galtier,P., 2003. Fate of the veterinary medicine ivermectin in soil. Environ.Chem. Lett. 1, 131–134.
Nichols, E., Spector, S., Louzada, J., Larsen, T., Amequita, S., Favila, M.E.,Scarabaeinae Res, N., 2008. Ecological functions and ecosystem ser-vices provided by Scarabaeinae dung beetles. Biol. Conserv. 141,1461–1474.
Nieuwhof, G.J., Bishop, S.C., 2005. Costs of the major endemic diseasesof sheep in Great Britain and the potential benefits of reduction indisease impact. Anim. Sci. 81, 23–29.
O’Brien, D.J., Forbes, A.B., Pitt, S.R., Baggott, D.G., 1999. Treatment andprophylaxis of psoroptic mange (sheep scab) using an ivermectinintraruminal controlled-release bolus for sheep. Vet. Parasitol. 85,79–85.
O’Hea, N.M., Kirwan, L., Finn, J.A., 2010a. Experimental mixtures of dungfauna affect dung decomposition through complex effects of speciesinteractions. Oikos 119, 1081–1088.
O’Hea, N.M., Kirwan, L., Giller, P.S., Finn, J.A., 2010b. Lethal and sub-lethal effects of ivermectin on north temperate dung beetles. Aphodiusater and Aphodius rufipes (Coleoptera: Scarabaeidae). Insect Conserv.Divers. 3, 24–33.
OECD, 1984. Daphnia sp., acute immobilisation test and reproduction test.OECD Guidelines for Testing Chemicals, 202.
OECD, 1998. Daphnia magna reproduction test. OECD Guidelines for Test-ing Chemicals, 211.
OECD, 2007. Determination of developmental toxicity of a test chemicalto dipteran dung flies (Scathophaga stercoraria L. (Scathophagidae),Musca autumnalis De Geer (Muscidae)). OECD Guidelines for TestingChemicals.
OECD, 2009. Guidance document on the determination of the toxicity of atest chemical to the dung beetle Aphodius constans. OECD Guidelines
for Testing Chemicals.Paraud, C., Lumaret, J.P., Chartier, C., 2007. Lack of effect of thenematophagous fungus Duddingtonia flagrans on the developmentof the dung beetle, Aphodius constans. Small Ruminant Res. 70,276–279.
arasitol
P
P
P
P
R
R
R
R
R
R
R
R
R
R
S
S
S
S
S
S
S
S
S
S.A. Beynon / Veterinary P
ena, M.T., Miller, J.E., Fontenot, M.E., Gillespie, A., Larsen, M., 2002.Evaluation of Duddingtonia flagrans in reducing infective larvae ofHaemonchus contortus in feces of sheep. Vet. Parasitol. 103, 259–265.
erez, R., Palma, C., Cabezas, I., Rubilar, L., Arboix, M., 2010. The influenceof gastrointestinal parasitism on fecal elimination of doramectin, inlambs. Ecotoxicol. Environ. Saf. 73, 2017–2021.
layne, M.J., 1978. Differences between cattle and sheep in tier diges-tion and relative intake of a mature tropical grass hay. Anim. FeedSci. Technol. 3, 41–49.
rasse, C., Loffler, D., Ternes, T.A., 2009. Environmental fate of theanthelmintic ivermectin in an aerobic sediment/water system.Chemosphere 77, 1321–1325.
ansome, R.D., Priddis, D.J., 2004. Slaughter of grazers due to foot andmouth disease confirms the importance of Aphodius dung beetles tothe greater horseshoe bat, Rhinolophus ferrumequinum. Bat Res. News45, 143–144.
idsill-Smith, T.J., 1988. Survival and reproduction of Musca vetustimssimaWalker (Diptera, Muscidae) and a scarabaeine dung beetle in dung ofcattle treated with avermectin B1. Aust. J. Entomol. 27, 175–178.
ömbke, J., Floate, K.D., Jochmann, R., Schaefer, M.A., Puniamoorthy,N., Knaebe, S., Lehmhus, J., Rosenkranz, B., Scheffczyk, A., Schmidt,T., Sharples, A., Blanckenhorn, W.U., 2009a. Lethal and sublethaltoxic effects of a test chemical (ivermectin) on the yellow dung fly(Scathophaga stercoraria) based on a standardized international ringtest. Environ. Toxicol. Chem. 28, 2117–2124.
ömbke, J., Hempel, H., Scheffczyk, A., Schallnass, H., Alvinerie, M.,Lumaret, J.P., 2007a. Environmental risk assessment of veterinarypharmaceuticals: development of a standard laboratory test with thedung beetle Aphodius constans. Chemosphere 70, 57–64.
ömbke, J., Hempel, H., Scheffczyk, A., Schallnass, H.J., Alvinerie, M.,Lumaret, J.P., Koschorrek, J., 2007b. Development and application of astandardized test system for the dung beetle species (Aphodius con-stans) to assess the ecotoxicity of veterinary pharmaceuticals. UWSF19, 197–205.
ömbke, J., Krogh, K.A., Moser, T., Scheffczyk, A., Liebig, M., 2010. Effectsof the veterinary pharmaceutical ivermectin on soil invertebrates inlaboratory tests. Arch. Environ. Contam. Toxicol. 58, 332–340.
ömbke, J., Schmelz, R.M., Knaebe, S., 2009b. Field studies for the assess-ment of pesticides with soil mesofauna, in particular enchytraeids,mites and nematodes: design and first results. Soil Organ. 81, 237–264.
oncalli, R.A., 1989. Environmental aspects of the use of ivermectin andabamectin in livestock: Effects on cattle dung fauna. In: Campbell, W.C.(Ed.), Ivermectin and Abamectin. Springer, New York, pp. 173–181.
osenlew, H., Roslin, T., 2008. Habitat fragmentation and the functionalefficiency of temperate dung beetles. Oikos 117, 1659–1666.
oslin, T., 2001. Large-scale spatial ecology of dung beetles. Ecography 24,511–524.
anyal, P.K., Chauhan, J.B., Mukhopadhyaya, P.N., 2004. Implications offungicidal effects of benzimidazole compounds on Duddingtonia fla-grans in integrated nematode parasite management in livestock. Vet.Res. Commun. 28, 375–385.
chmitt, H., Römbke, J., 2008. The ecotoxicological effects of phar-maceuticals (antibiotics and antiparasiticides) in the terrestrialenvironment—a review. In: Kummerer, K. (Ed.), Pharmaceuticals inthe Environment: Sources, Fate, Effects and Risks. , third ed. Springer,Heidelberg, Germany, pp. 285–303.
herratt, T.N., Macdougall, A.D., Wratten, S.D., Forbes, A.B., 1998. Modelsto assist the evaluation of the impact of avermectins on dung insectpopulations. Ecol. Model. 110, 165–173.
kidmore, P., 1991. Insects of the British Cow-dung Community, vol. 21.Field Studies Council.
kripsky, T., Hoffmann, S., 2010. Assessment of risk of monepantel faecalresidues to dung fauna. Aust. Vet. J. 88, 490–496.
lade, E.M., Mann, D.J., Villanueva, J.F., Lewis, O.T., 2007. Experimentalevidence for the effects of dung beetle functional group richness andcomposition on ecosystem function in a tropical forest. J. Anim. Ecol.76, 1094–1104.
ommer, C., Bibby, B.M., 2002. The influence of veterinary medicines onthe decomposition of dung organic matter in soil. Eur. J. Soil Biol. 38,155–159.
ommer, C., Gronvold, J., Holter, P., Nansen, P., 1993. Effects of ivermectinon 2 Afrotropical dung beetles, Onthophagus gazella and Diastel-lopalpus quinquedens (Coleoptera, Scarabaeidae). Vet. Parasitol. 48,171–179.
ommer, C., Steffansen, B., Nielsen, B.O., Gronvold, J., Jensen, K.M.V.,Jespersen, J.B., Springborg, J., Nansen, P., 1992. Ivermectinexcreted in cattle dung after subcutaneous injection or pour-ontreatment—concentrations and impact on dung fauna. Bull. Entomol.Res. 82, 257–264.
ogy 189 (2012) 113– 124 123
Sowig, P., Wassmer, T., 1994. Resource partitioning in coprophagous bee-tles from sheep dung: phenology and microhabitat preferences. Zool.Jahrb. Abt. Syst. Oekol. Geogr. Tiere 121, 171–192.
Spratt, D.M., 1997. Endoparasite control strategies: implications for bio-diversity of native fauna. Int. J. Parasitol. 27, 173–180.
Steel, J.W., 1993. Pharmacokinetics and metabolism of avermectins inlivestock. Vet. Parasitol. 48, 45–57.
Steel, J.W., 1998. Assessment of the effects of the macrocyclic lactone classof chemicals on dung beetles and dung degradation in Australia. In:NRA Special Review of Macrocyclic Lactones. National RegistrationAuthority for Agricultural and Veterinary Chemicals, Canberra, pp.15–79.
Strong, L., 1992. Avermectins—a review of their impact on insects of cattledung. Bull. Entomol. Res. 82, 265–274.
Strong, L., 1993. Overview—the impact of avermectins on pasturelandecology. Vet. Parasitol. 48, 3–17.
Strong, L., James, S., 1993. Some effects of ivermectin on the yellow dungfly, Scatophaga stercoraria. Vet. Parasitol. 48, 181–191.
Suarez, V.H., 2002. Helminthic control on grazing ruminants and environ-mental risks in South America. Vet. Res. 33, 563–573.
Sutherland, W.J., Armstrong-Brown, S., Armsworth, P.R., Brereton, T.,Brickland, J., Campbell, C.D., Chamberlain, D.E., Cooke, A.I., Dulvy,N.K., Dusic, N.R., Fitton, M., Freckleton, R.P., Godfray, H.C.J., Grout, N.,Harvey, H.J., Hedley, C., Hopkins, J.J., Kift, N.B., Kirby, J., Kunin, W.E.,Macdonald, D.W., Marker, B., Naura, M., Neale, A.R., Oliver, T., Osborn,D., Pullin, A.S., Shardlow, M.E.A., Showler, D.A., Smith, P.L., Smithers,R.J., Solandt, J.L., Spencer, J., Spray, C.J., Thomas, C.D., Thompson, J.,Webb, S.E., Yalden, D.W., Watkinson, A.R., 2006. The identification of100 ecological questions of high policy relevance in the UK. J. Appl.Ecol. 43, 617–627.
Thompson, H.M., 1996. Interactions between pesticides: a review ofreported effects and their implications for wildlife risk assessment.Ecotoxicology 5, 59–81.
Vale, G.A., Grant, I.F., 2002. Modelled impact of insecticide-contaminateddung on the abundance and distribution of dung fauna. Bull. Entomol.Res. 92, 251–263.
VICH, 2004. Environmental Impact Assessment for Veterinary MedicinalProducts—Phase 2, Report No. VICH GL38 (Ecotoxicity Phase II). Inter-national Cooperation on Harmonization of Technical requirements forRegistration of Veterinary Medicinal Products, London, UK.
Wall, R., Beynon, S., 2012. Area-wide impact of macrocyclic lactone para-siticides in cattle dung. Med. Vet. Entomol. 26, 1–8.
Wall, R., Strong, L., 1987. Environmental consequences of treating cattlewith the antiparasitic drug ivermectin. Nature 327, 418–421.
Ward, P.I., Wilhelm, A., 1994. Degradation of pats of cow dung populatedby different insect communities. Trends Agric. Sci. Entomol. 2, 89–94.
Wardhaugh, K.G., 2005. Insecticidal activity of synthetic pyrethroids,organophosphates, insect growth regulators, and other livestock par-asiticides: an Australian perspective. Environ. Toxicol. Chem. 24,789–796.
Wardhaugh, K.G., Holter, P., Longstaff, B., 2001. The development andsurvival of three species of coprophagous insect after feeding on thefaeces of sheep treated with controlled-release formulations of iver-mectin or albendazole. Aust. Vet. J. 79, 125–132.
Wardhaugh, K.G., Longstaff, B.C., Lacey, M.J., 1998. Effects of residues ofdeltamethrin in cattle faeces on the development and survival of threespecies of dung-breeding insect. Aust. Vet. J. 76, 273–280.
Wardhaugh, K.G., Mahon, R.J., 1991. Avermectin residues in sheepand cattle dung and their effects on dung beetle (Coleoptera,Scarabaeidae) colonization and dung burial. Bull. Entomol. Res. 81,333–339.
Wardhaugh, K.G., Mahon, R.J., 1998. Comparative effects of abamectin andtwo formulations of ivermectin on the survival of larvae of a dung-breeding fly. Aust. Vet. J. 76, 270–272.
Wardhaugh, K.G., Mahon, R.J., Axelsen, A., Rowland, M.W., Wanjura, W.,1993. Effects of ivermectin residues in sheep dung on the develop-ment and survival of the bushfly. Musca vetustissima Walker and aScarabaeine dung beetle, Euoniticellus fulvus Goeze. Vet. Parasitol. 48,139–157.
Wardhaugh, K.G., Ridsdill-Smith, T.J., 1998. Antiparasitic drugs, the live-stock industry and dung beetles—cause for concern? Aust. Vet. J. 76,259–261.
Wardhaugh, K.G., Rodriguez-Menendez, H., 1988. The effects of theantiparasitic drug, ivermectin, on the development and survival of
the dung-breeding fly, Orthelia cornicina (F.) and the Scarabaeine dungbeetles, Copris hispanus L. Bubas bubalus (Oliver) and Onitis belial F. J.Appl. Entomol. 106, 381–389.Webb, L., Beaumont, D.J., Nager, R.G., McCracken, D.I., 2010. Field-scaledispersal of Aphodius dung beetles (Coleoptera: Scarabaeidae) in
arasitol
124 S.A. Beynon / Veterinary Presponse to avermectin treatments on pastured cattle. Bull. of Ento-mol. Res. 100, 175–183.
Westergaard, K., Muller, A.K., Christensen, S., Bloem, J., Sørensen, S.J., 2001.Effects of tylosin as a disturbance on the soil microbial community. SoilBiol. Biochem. 33, 2061–2071.
Williams, B., Warren, J., 2004. Effects of spatial distribution on the decom-position of sheep faeces in different vegetation types. Agric. Ecosyst.Environ. 103, 237–243.
Wratten, S.D., Meadbriggs, M., Gettinby, G., Ericsson, G., Baggott,D.G., 1993. An evaluation of the potential effects of ivermectinon the decomposition of cattle dung pats. Vet. Rec. 133, 365–371.
Yamada, D., Imura, O., Shi, K., Shibuya, T., 2007. Effect of tunneler dung bee-
tles on cattle dung decomposition, soil nutrients and herbage growth.Grassland Sci. 53, 121–129.Yeates, G., Dimander, S.O., Waller, P., Hoglund, J., 2003. Soil nematodepopulations beneath faecal pats from grazing cattle treated withthe ivermectin sustained-release bolus or fed the nematophagous
ogy 189 (2012) 113– 124
fungus Duddingtonia flagrans to control nematode parasites. ActaAgric. Scand. A-Anim. Sci. 53, 197–206.
Yeates, G.W., Dimander, S.O., Waller, P.J., Hoglund, J., 2002. Environmen-tal impact on soil nematodes following the use of the ivermectinsustained-release bolus or the nematophagous fungus Duddingtoniaflagrans to control nematode parasites of cattle in Sweden. Acta Agric.Scand. A-Anim. Sci. 52, 233–242.
Yeates, G.W., Skipp, R.A., Chen, L.Y., Waghorn, T.S., Potter, J.F., 2007a.Temporal and spatial aspects of the influence on soil nematodes ofdepositing artificial pats of sheep faeces containing a range of parasitemanagement agents. Appl. Soil Ecol. 37, 106–117.
Yeates, G.W., Skipp, R.A., Gray, R.A.J., Chen, L.Y., Waghorn, T.S., 2007b.Impact on soil fauna of sheep faeces containing a range of parasite
control agents. Appl. Soil Ecol. 35, 380–389.Yeates, G.W., Waller, P.J., King, K.L., 1997. Soil nematodes as indicators ofthe effect of management on grasslands in the New England Table-lands (NSW): effect of measures for control of parasites of sheep.Pedobiologia 41, 537–548.
