Environmental assessment of veterinary avermectins in temperate pastoral ecosystems

zyxwvutsrqpo Ann. appl. Biol. (1996), 128:329-348 Printed in Great Britain zyx zyxwvut 329 Environmental assessment of veterinary avermectins in temperate pastoral ecosystems By S D WRATTEN' and A B FORBES' Department of Entomology and Animal Ecology, Lincoln University, Canterbury, New Zealand 2Merck AgVet, Merck & C o . , Inc., Rahway, NJ 07065, USA (Accepted 12 February 1996) Summary Avermectins and their metabolites are excreted mainly in the faeces; they do not readily move from the site of dung deposition because of their low solubility in water and their tight binding to organic matter. Avermectins degrade in the environment through photodegradation and aerobic breakdown by soil organisms. The dung mesofauna potentially exposed to avermectin residues includes insects, earthworms, springtails, mites and nematodes. These organisms occupy a variety of different niches within the ecosystem and the faunal composition changes as the pats age. Some members of this fauna act in concert with soil microbial flora and assist in the breakdown of dung and consequent nutrient re-cycling on pasture. There are marked seasonal patterns of faunal abundance and behaviour which affect their relative importance in the decomposer community. Some species of the coprophagous insect fauna, particularly in the larval stages, can be adversely affected by the presence of avermectin residues in the faeces. Veterinary use patterns of avermectins in temperate regions indicate that peak periods of insect activity and peak times of avermectin use are often asynchronous. When avermectin usage and insect activity do coincide, the heterogeneous patterns of administration to livestock and the focus of treatment on young animals result in the deposition on pasture of faeces which are predominantly free of avermectin residues. Results of large scale, long term studies indicate that, even under conditions of relatively high levels of avermectin use in cattle, the impact on non-target insect populations and their function is limited. Key words: Avermectins, cattle, faecal residues, dung fauna, environmental assessment introduction The avermectins comprise a group of highly effective, broad-spectrum antiparasitic agents used in the control of parasitic diseases in livestock. Avermectin B, (abamectin) is isolated following fermentation of the actinomycete Streptomyces avermitilis Burg; this compound possesses high potency against a broad spectrum of endo- and ecto-parasites of cattle and also mite and insect pests in agriculture and horticulture. The semi-synthetic 22. 23-dihydro analogue of abamectin, ivermectin, is used in domestic livestock for the prevention and cure of parasitic infections. Ivermectin is also used in humans, notably in a World Health Organization (WHO) sponsored programme to eliminate River Blindness. transmitted by blackflies (Diptera: Simuliidae) and caused by the filarial worm Onchocerca volvulus Leuckart (Campbell, 1991). The veterinary avermectins used in farm livestock currently zyxwvutsrqp @ 1996 Association of Applied Biologists 330 zyxwvuts zyxwvu zyxwvu S D WRATTEN AND A B FORBES comprise abamectin, doramectin and ivermectin; also available is moxidectin from the closely related milbemycin class of compounds. This review will focus on abamectin and ivermectin; the details of their discovery, isolation and chemistry have been reviewed on several occasions (see Campbell, 1989). The avermectins are closely related 16-membered macrocyclic lactones. Although they share structural features with the antibacterial macrolides and the antifungal macrocyclic polyenes, the avermectins are not usually grouped with those compounds. Avermectins have neither antibacterial nor antifungal activities and do not inhibit protein or chitin syntheses (Gordnier, Brezner & Tananbaum, 1987; Halley, Jacob & Lu, 1989). In target organisms, the effects of avermectins are mediated via specific, high-affinity binding sites. The physiological response to this binding is an increase in membrane permeability to chloride ions, which appears to be modulated by a glutamate-gated chloride channel in invertebrates (Arena et al., 1995). Avermectins exhibit this activity in both nematodes and arthropods, but have no activity against cestodes or trematodes because these parasites lack appropriate receptor sites (Shoop et af, 1995). After administration to the host animal, avermectins become widely distributed throughout the body; there is limited metabolism and the main route of excretion is the faeces. Parent compound is the major (40-75%) component excreted in the faeces, the remainder comprising less active polar metabolites. Avermectins have a low solubility in water, they do not accumulate in tissues and are readily eliminated from the treated animal. The constant for binding to organic carbon (K,) is high and this results in a strong affinity to particulate matter in faeces and soil. The avermectins are photolytically unstable and are rapidly destroyed by sunlight, having a half-life of the order of 3 h in the most extreme tests. The other main method of degradation is through the activity of soil microbial flora which break down the macromolecules to simple organic compounds over a relatively short period of time (Halley et af.,1989). Because the avermectins appear largely unaltered in the dung after treatment and because they have insecticidal properties, there has been concern over the potential environmental consequences arising from their use in livestock. There have been a large number of publications purporting to deal with the environmental or ecological effects of avermectins on the invertebrate fauna of dung and on the consequences for dung decomposition. However, much of the published work does not actually address the effects, if any, of the avermectins at the invertebrate population or community level, concentrating instead on small-scale, laboratory or semi-field, short-term studies, often at the spatial scale of single dung pats. Many of these publications do, nevertheless, contain considerable speculation as to potential ‘environmental’ consequences. The aim of the present review is to re-evaluate the most substantial studies from an ecological perspective. There are obvious parallels with the interpretation of the environmental effects of agrochemicals in agriculture and horticulture (Jepson, 1989). In both cases, the fundamental question is not solely one of toxicity to non-target fauna, but that of what constitutes a significant ecological effect. This review will address primarily the subject of the possible consequences arising from the insecticidal activity of avermectin residues present in the faeces of animals following treatment, with examples drawn mainly from the use of ivermectin and abamectin in cattle. The broader aspects of environmental safety of these compounds have been thoroughly reviewed previously (Halley et al., 1989; Halley VandenHeuvel & Wislocki, 1993). zyxwvut zyxwvutsr zyxwvutsr zyxwvu Temporal and spatial patterns of avermectin use in cattle Although certain, non-target, invertebrate species may be at risk from the avermectins, the actual hazard depends on their exposure. Under field conditions, exposure is a function zyxwv zyxw zy Environmental assessment of avermectins 331 of factors which include the temporal and spatial aspects of dung faunal distribution, abundance and behaviour, the timing of treatments and the type and proportion of cattle treated. An outline of the principles behind modern approaches to parasite control in livestock and of the usage patterns of antiparasitic druFs, including avermectins, is given here. Because of their spectrum of activity, avermectins can be used in control programmes for either nematodes or arthropods, or both. Control is normally targeted at one or two key parasites of importance; these are usually nematodes, but may be insects or arachnids (Forbes 1993). In cattle, programmes are typically centered on control of the economically important nematodes, such as Ostertagia ostertagi Stiles, Haemonchus placei Place or Dictyocaulus uiviparus Bloch; these approaches generally provide concurrent control of several other important nematode genera. Target ectoparasites include lice, mites, warbles, ticks and nuisance flies and strategically timed avermectin treatments can on occasion provide simultaneous control of some of these important ectoparasites. The control of parasites is ideally based on practices which integrate chemotherapy with animal husbandry, pasture management and immunity in the host (Brunsdon, 1980; Sutherst, 1983); the objective is to maintain parasite levels below thresholds of significance to animal health, welfare and productivity. Control measures for nematode parasitism are typically concentrated on first-season grazing calves, as these are immunologically naive and consequently are at greatest risk from parasites (Michel, 1976; Anderson, Donald & Waller, 1983). The role of anthelmintics in parasite control is to enhance other management strategies by reducing parasite numbers at key times. The various options can be described in several ways according to the pattern of use, for example, evasive, strategic or therapeutic treatments (Herd, 1988; McKellar, 1988). zyxwvu First season calves Evasive strategies can be used when young cattle graze a pasture until contamination with infective larvae becomes high, generally around the middle of the grazing season. Calves are then treated with an anthelmintic to remove existing worm burdens and transferred to a parasitologically ‘clean’ pasture where further acquisition of infective larvae is minimal; this is also known as the ‘dose and move’ strategy. If ‘clean’ pastures are unavailable. an alternative is to delay treatment until mid-season and then to initiate a prophylactic regimen using sustained-release delivery devices or repeated treatments with anthelmintics, while the animals continue to graze contaminated pasture. Strategic programmes are based on the use of anthelmintics early in the grazing season to prevent calves acquiring burdens of fecund adult worms which would contaminate the pasture with their eggs and lead to an accumulation of infective larvae on pasture. This can be achieved with serial anthelmintic treatments or the use of a continuous or pulse release devices (e.g. Taylor, Mallon & Kenny, 1985; Herd, Reinemeyer & Heider, 1987). The net result of these programmes is a marked reduction in the level of pasture contamination, which would typically peak from mid-season onwards in the absence of treatment. and consequent control of parasites, manifest as lack of clinical disease and improved animal performance. In the absence of any preventative practices, clinical parasitism can appear, usually in the second half of the grazing season. and under these circumstances therapeutic anthelmintic treatment must be administered on health and welfare grounds. If the calves continue to graze the same contaminated pasture, then it may be necessary to treat on more than one occasion because reinfection can lead to further clinical episodes. 332 zyxwvu zyxwvutsrq zyxwvutsr zyxwvut S D WRATTEN AND A B FORBES Whichever tactics are adopted, a treatment at the end of the period of transmission is commonly recommended to remove worm burdens acquired late in the grazing season. A t the same season of the year prophylactic treatments for ectoparasites are commonly given; the broad spectrum of the avermectins means that a single therapy at this time can eliminate not only parasitic nematodes, but also several potentially damaging ectoparasites from the animals (Ryan & Guerrero, 1987). Second season and adult cattle There is not always a perceived need for anthelmintic treatment of second-season and older cattle, as these animals are generally not affected severely by helminth parasites because of the acquisition of functional immunity (Herd, 1988). However, benefits which have been demonstrated following parasite control in more mature cattle include: maintenance of growth rates up to adult size, earlier and consistent achievement of ovarian cyclicity in both maiden heifers and in the post-partum cow, improved pregnancy rate, increased milk yield and higher calf weaning weight. Nevertheless, for several reasons - for example, farm policy, cost considerations, scarcity of labour - anthelmintic treatment of older stock is undertaken at a much lower level and frequency than young stock. Such treatments are mainly opportunistic in that the timing is related to convenient management practices, such as handling stock for other reasons, rather than to epidemiological considerations. Summary Published data (Michel, Latham, Church & Leech, 1981) illustrates this overall pattern of anthelmintic use in different categories and ages of cattle in England and Wales (Table 1). The highest usage of avermectins in cattle occurs in the autumn/fall season, which marks the end of the period of parasitic nematode transmission, and frequently coincides with weaning of calves and movement of stock (sometimes into housing). There is a lower level of use during spring when early season strategic treatments of young stock occur. The bulk of the animals treated are less than a year old. If treatment of older, adult cattle occurs, this typically takes place in the autumn/fall to coincide with practices, such as weaning or pregnancy checking. Potential exposure of non-target insects to avermectins The general patterns of avermectin use described in the previous section and the associated spatial and temporal heterogeneity of practical usage give an indication of the potential zyxw Table 1. Anthelmintic doses administered to various categories of cattle (from Michel et al., 1981) 70of animals in each category by number of times dosed Category 1st year diary beef Dairy calves 2nd year dairy beef 2-3 year calves Suckled calves 2-3 year beef Beef cows Dairy cows Mean no. doses head-' 0 1 2+ 2.0 1.8 1.5 1.2 1.o 1 .o 0.8 0.3 11 14 26 35 33 31 43 74 23 32 30 30 48 41 37 17 66 54 zyxw zyxwv 44 35 19 28 20 9 zyx zyxwvuts zyxwv Environmental assessment of avermectins 333 levels of exposure of non-target species of the dung fauna. In this context therefore, treatment of housed and feedlot animals with avermectins is not relevant to exposure of insects which utilise fresh dung deposited on pasture, nor to grassland ecology. Additionally, some of the seasonal treatments are given at times when the insect dung fauna are reduced and inactive, for example during temperate winters; this further reduces the exposure of dung insects to avermectin residues (Ridsdill-Smith, 1993). The wet weight of fresh faeces produced per day by cattle is approximately 6% of their body weight (Marsh & Campling, 1970); young animals, because of their lower body weight, deposit relatively less faecal material on the pasture than their older herdmates. On a farm basis, considering typical herd structures, it can be calculated that the young stock (the primary targets for anthelmintic treatment) contribute about 20% of the annual total dung deposited by a beef herd and less than 10% of that by a dairy herd (Forbes, 1993). From the above outline of the use patterns of avermectins in cattle, with their demographic, temporal and spatial heterogeneity, it is likely that environmental effects would not be great, even without consideration of ecological and ecotoxicological factors. However, the use of dung invertebrates and dung degradation rates as ‘biomarkers’ of avermectin effects also needs to be analysed. In order to understand the environmental consequences which might arise following the use of avermectins in cattle, it is necessary to appreciate the population biology of the dung invertebrate fauna and its function, so that the impact of any perturbations can be objectively assessed. Dung flora and fauna Cattle dung provides a habitat for a variety of organisms including bacteria, fungi, earthworms, nematodes and arthropods - the latter comprising mainly flies, beetles and mites (Hanski & Cambefort, 1991; Skidmore, 1991). The relative composition of the fauna varies seasonally, and geographically; additionally there is a succession of different species as the dung ages after deposition (Laurence, 1954; Denholm-Young, 1978); Fig. 1. In northern temperate regions, the dung insect fauna comprises mainly fly larvae and adult and larval beetles. Beetles of the genus Aphodius have been described as “the dung beetles of the North” (Hanski, 1986); there are about 130 species in Europe and 210 in North America. The European species are coprophages, feeding and breeding mainly within the dung of herbivores such as cattle. Some of these European species have become established in North America and now supplement the native Aphodius spp. which typically utilise faeces of native rodents, reptiles and deer. Adult beetles may live up to 2 months during their breeding season; during this time they will visit around 10 different, freshly deposited, pats, staying in each one for around five days (Hanski, 19800). In addition, though less numerous, species of the genus Geotrupes which are large tunneling beetles, are found in Europe as are other tunnelers of the genera Copris, and Onthophagus. Species of Onthophugus have also been introduced into North America, either deliberately or accidentally, where they supplement the indigenous fauna. At times, the most abundant beetles in dung pats in northern temperate regions are predaceous species from the families Hydrophilidae and Staphylinidae. The dung beetle community of northern latitudes, including northern Europe and much of North America is, however, relatively depauperate in both species and numbers of individuals compared with that found in warmer climates (Hanski & Cambefort, 1991). Whilst adult flies may visit pats to feed on surface fluids, to prey on other insects or to mate and lay eggs, they do not penetrate the pat. Some fly larvae are truly coprophagous, some are saprophagous and many are obligatory or facultative carnivores. There are also hymenopteran parasitoids present and these parasitise dipteran pupae which are found in zyxw 334 zyxwvutsr zyxwvutsrqpo S D WRAl’TEN AND A B FORBES Days 0 1 2 3 4 Weeks 5 6 7 2 3 4 5 Months 6 7 8 3 4 Large Diptera Geotnipes spp hgc Staphyhudae Sindl Stapliylidae zyxwvutsr Spliaetidiuni SPP. Cetryoji spp Histeridac I Iyinenopten ~l~vorms Colleinbola Fig. 1. Dung pat succession after Denholm-Young (1978) in Putman (1983) zyxwv dung. In the UK, 266 insect species are associated with dung (Skidmore, 1991). Other arthropod groups which occur in dung are the Collembola, or springtails, which are essentially part of the soil fauna, but which can be found in aged dung, and the Acari, which include saprophagous and coprophagous species, some of which are phoretic and are transported to dung by insect colonisers such as dung beetles. Insect breeding biology The population dynamics of dung insects are a function of the relative rates of mortality, natality, immigration and emigration. Particular facets of these parameters will be considered as they relate to dung beetles and dung flies. Factors which can affect birth and death rates can be considered as abiotic or biotic (Valiela, 1969) and they frequently interact. Such factors include: Environmental assessment of auermectins Abiotic Temperature Rainfall Moisture content of faeces At deposition Subsequent to deposition Physico-chemical composition of faeces Site of deposition Underlying soil characteristics Biotic zyxw zyxw 335 Competition for resources: Interspecific Intraspecific Parasitism Predation By invertebrates By vertebrates Disease Dung composition The value of dung as a resource for coprophagous insects depends on a number of intrinsic factors which can markedly affect their breeding success. The quantity of dung passed by grazing cattle varies according to animal factors such as liveweight and physiological state and to dietary factors like forage type and digestibility. Availability of cattle faeces for the obligate, dung insect fauna is primarily a function of cattle demographics and grazing management. The propensity of cattle dung to support feeding and breeding activities of adult and larval coprophagous beetles and flies is related to its composition. There are several publications reporting the variation in breeding success of various species of dung beetles and flies resulting from differences in dung composition. Differences in dung quality resulting from variations in forage quality or type have been shown to affect the egg-laying, development and emergence of several species of beetles, including Aphodius erraticus (L.), Platystethus arenarius (Fourc.) and Cercyon lateralis Marsh (Barth. Karrer, Heinze-Mutz & Elster, 1994a) and flies, for example Haematobia irritans (L.) and Musca autumnalis (Deg.) (Schmidt, 1985; Dougherty & Knapp, 1994). The reasons for these differences have not been precisely determined, but factors such as the moisture content, pH and nitrogen level in faeces have all been shown to play a role. Moisture content alone, regardless of other differences in faeces composition, has been shown to have a profound effect on the colonisation and utilisation of dung by insects (Barth, Karrer & Heinze-Mutz, 1995). One hundred-fold differences in reproductive rate in dung beetles, resulting from differences in dung quality have been recorded (Edwards, 1991). The importance of these observations is that, when assessing the potential impact of specific perturbations on dung fauna or function, the variability of the dung substrate must be considered, both with respect to experimental design (Barth, 1993) and in considerations of insect abundance and population dynamics. zyxwvutsr Intra- and interspecific competition Intraspecific competition amongst dung insects results from resource availability and stochasticity. The finite amount of dung in a pat means that, above certain thresholds, the quantity of faeces required for feeding and breeding can become limiting. Under such conditions, compensatory density-dependent processes may come into play. Density-dependence has been demonstrated for example in the dung beetle, Aphodiur rufipes (L.) (Holter, 1979a) and in the horn fly Haematobia irritans (Lysyk, 1991). Optimum survival, reproductive performance and resource utilisation often occur at densities below the maximum carrying capacity of a dung pat. Perturbations which occur at high population 336 zyxwvutsrq zyxwvu zyxwvuts zyxwvuts S D WRATTEN AND A B FORBES densities may have little net effect on the overall abundance of an insect species because intraspecific competition will be less intense and compensation occurs. Interspecific competition amongst insects, and other members of the fauna, is also a feature of community life within a dung pat. Competition can arise through simultaneous utilisation of the same resource for food and breeding, in the same way as intra-specific competition arises, and also through changes in the physico-chemical nature of the dung substrate and removal of dung by tunneling (paracoprid) beetles. Larvae of flies which feed and develop within the confines of the pat can be displaced and compromised by the activities of dung beetles and this underpins biological control programs for certain pest species of flies. In addition fragmentation of the pat increases the surface area of the faeces which consequently dehydrate more rapidly and become inhospitable to endocoprid coleopteran and dipteran larvae Dung insect mobility Mobility can be considered to be a crucial behaviour for insects which feed, mate and reproduce in fresh dung - a habitat described in ecological terms as patchy and ephemeral. The implications of this are that the resource on which these insects depend is distributed discretely throughout the range of the animal which is producing it, and that this resource is present for a limited period of time and may only be attractive and suitable for insects for a short time. In livestock farming, it is common practice for cattle to regularly move, or be moved, around the grazing area o r farm in order to utilise the available grazing. It is important therefore that the local insect dung fauna be able to locate and move to where the cattle are pastured in order to survive. This must occur regularly and would apply particularly for example when over-wintering stages emerge as adults when cattle may be grazing distant from their location the previous year, when the dung in which development took place was deposited. The beetles of the genus Aphodius, the most common dung beetles of the northern temperate climes, have been shown to routinely travel distances up to 2 kilometres and less frequently considerably farther (Hanski, 1980a,b, 1986). The records derived from beetle introductions in North America provide evidence for greater distances travelled. In North America Onthophagus gazella Fabricius was shown to spread at the rate of 58 km year-', whilst another introduced species, Onthophagus taurus Schreber, moved at 129 km year-' following its initial colonisation in Florida (Fincher, Stewart & Hunter, 1983). Dung breeding flies are also mobile; studies on the horn fly, Haematobia irritans, in North America have shown that adults readily move distances of 1.7 to 11.7 kilometres within a few days following emergence (Kinzer & Reeves, 1974; Byford et al., 1987). Dispersal and host location by horn flies were influenced by ambient temperature, wind velocity, humidity and local topography. Aggregation Initial pat colonisation by insects appears to be random, however beetles leave some pats at a faster rate than others, so that aggregation is common (Holter, 1982; Hanski, 1986). This results in a distribution of beetles amongst pats in which only a proportion of apparently similar pats deposited at the same time on the same pasture will be colonised (Hanski & Cambefort, 1991). Aggregation is probably essential for reproduction as pats provide sites where dung beetles can prospect for mates and continue their life cycle. Field observations indicate that aggregation within a pat is not confined to single species of coprophagous beetles, so it is assumed that non-specific attractants within the dung must initiate colonisation prior to any insect-derived mechanisms. Insect aggregation in pats is important zyxwv zyx zyxw zyxwv Environmental assessment of avermectins 337 from an experimental perspective in that adequate replication is required in trials whose objective is to measure differences in insect abundance or function between individual pats. Earthworms Earthworms are terrestrial invertebrates belonging to the Order Oligochaeta. There are five families and about 1800 species of earthworms distributed all over the world. Factors which affect numbers and distribution of earthworms include climate, soil pH, moisture, temperature, soil type, organic matter content and agricultural practices. Substrates rich in organic matter such as rotting vegetation and animal dung are attractive to detrivorous earthworms. Earthworms of several species are found in greater profusion in soil underlying dung than in surrounding areas of pasture (Knight, Elliott, Anderson & Scholefield, 1992). It has been calculated that a modest population of 120000 earthworms per hectare could remove up to 20 tons of dung per hectare annually (Edwards & Lofty, 1972). The contribution of detrivorous earthworms to dung degradation can be considerable; not only can they physically disrupt the pat and transport the faeces into the soil, but further breakdown is enhanced by their feeding and digestion (Hendriksen, 1991a,b). Under European conditions, and in other similar temperate regions of the world, earthworms are considered to be amongst the foremost biotic agents in dung decomposition (Holter, 1979b; Martin & Charles, 1979). There is some seasonal variation in their activity; it has been estimated that in England, during winter and spring, earthworms account for some 3040% of the material removed from dung during decomposition; during summer and autumn these figures rise to 5 0 4 0 % (Denholm-Young, 1978). Major constraints on earthworm activity include low temperatures and, particularly, low soil moisture; in hot, dry spells many species enter a period of aestivation or burrow much deeper into the soil to layers of higher humidity (Edwards & Lofty, 1972). The process of dung decomposition The process of dung decomposition is complex and takes a variable amount of time depending on the relative interaction of many factors. Table 2 gives some examples from the published data of the range of time over which decomposition takes place on temperate grasslands. The results are not necessarily directly comparable because of differences in experimental protocols, criteria for evaluating decomposition and defined end-points, nevertheless, the range of time - from a few weeks to more than a year - is representative of typical disappearance times. It should also be noted that these times can vary according to season. This was observed in a study under temperate conditions in England (DenholmYoung, 1978), Table 3. zyx zyxwv zyxwvut Table 2. Rates of cow dung decomposition recorded in temperate regions Decay time (in days) Denmark 45+ Authors (Sommer er of., 1992) (Madsen et al.. 1990) (Barth et a/., 19940) (Weeda, 1%7) (Bastiman, 1970) (Denholm-Young, 1978) (Merritt & Andenon, 1977) zyxwvutsr Germany New Zealand United Kingdom 90+ 63+ up to 520 35-140 1W150+ United States 360-1000+ 338 zyxwvutsrqp zyxwvu zyxwvutsrqp zyxwvutsrq zyxwv zyxwv S D W R A T E N AND A B FORBES Table 3 . Total decay times and dry weight ‘half-lives’(time taken to 50% loss) of cattle dung. Figures show results of a number of replicated experiments in different seasons in the U K , modified from Denholm-Young (1978), in Putman (1983) Season Spring Summer Autumn Winter Total pat life. mean days Dry weight. mean halflife in days 150 114 140 39 173 53 53 92 The decomposition process itself was studied in detail by Denholm-Young (1978) working with cattle dung in pasture. In the seasons, winter/spring and summer/autumn, the various possible pathways for loss of dung material were identified and the material lost was monitored through each route. The results, in terms of percentage dry weight of the initial dungpile ‘processed’ by each decomposer route are summarised in Fig. 2 ( from Putman, 1983). Denholm-Young’s work (1978) showed that individual dungpiles showed some variation around the ‘seasonal norm’. In some autumn experiments, for example, Geotrupes spiniger Marsh removed up to 13% by dry weight of the dungpile and obviously reduced in consequence the amounts of material passing along other routes. However, the main outlet for the energy in dung materials is in the metabolism of insect larvae and micro-organisms (fungi and bacteria) colonising the dung pat. Supporting this conclusion are the data of Holter (1979b) who showed that dung beetle larvae (in Denmark) were responsible for a maximum of 1 6 2 0 % of gross removal. Worm and beetle effects were additive, not synergistic (Holter, 1977). A major role is sometimes played in the dung system by earthworms. Denholm-Young (1978) found that they are greatly limited by lack of moisture and their differential contribution to the decomposition of dung in different seasons accounted for much of the variation in decay time. One factor of considerable influence on the decomposition of dung is the degree of fragmentation by physical factors. To the effects of weathering may be added those of trampling or disturbance by animals, particularly birds (Laurence, 1954; Anderson & Menitt, 1977; McCracken, Foster, Bignal & Bignal, 1992), which may peck open a dungpile in search of insects and earthworms. Denholm-Young (1978), for example, found that up to 66% of cattle dung pats were pecked open and scattered by birds during autumn and winter, although the effect was less pronounced in spring and summer (15-30%). Fragmentation of the dung, by whatever agent, dramatically affects its subsequent rate of decomposition. Under experimental conditions, Denholm-Young (1978) showed that dungpat fragments lose 20-30% more weight in the first 50 days of decay than d o normal dung pats (presumably through an increase in the surface/volume ratio and increased aeration to assist microbial activity). In terms of a ) flow of dung material and b) energy flow, insects are of limited importance in temperate systems; 1-5% of the dung material leaves via insects (Fig. 2) while a maximum of 160kJ of energy follow this route from a total energy starting point of 3140kJ. Also, Stevenson & Dindal(l987) indicate that it is unlikely that coprophagous fly larvae consume enough organic matter in dung to have a significant effect on dung degradation. As fly larvae in dung consume only liquid food, they cannot fragment dung, although their burrowing activity probably helps aerate the pat. In the same way, though adult dung zyxwvuts-rqponmlkjihgfedcba zyxw zy zyxwvutsr Environmental assessment of avermectins 1 Initial dung pile 100 339 WINTER & SPRING Respiratory COI Total consumption Insect consumption zyxwvuts u zyxwv exported from dung Leachate SUMMER & AUTUMN Initial dung pile -U IU I , I Total consumption 7 Respiratory c02 Insect consumption Fig. 2. Major routes for flow of material from cattle dung in England; numbers are percentage of dry weight of the initial pat and may exceed 100% since certain processes are not mutually exclusive, from Denholm-Young (1978) in Putman (1983). beetles have limited ability to digest dung because they also feed only on the liquid component, they contribute beyond this by fragmenting the pat and hence facilitating decomposition. Effects of avermectin use on dung fauna It is well known that the avermectins have broad-spectrum insecticidal properties and these have been extensively reviewed (Strong & Brown, 1987). The temporal and spatial scale of any effects of avermectins on dung invertebrates through their use in cattle will now be considered, and the evidence for a significant ecological effect assessed where 340 zyxwvutsr zyxwv zyxwv zyxwvuts zyx S D WRATTEN AND A B FORBES possible. Most studies d o not address this latter aspect, because of the methodologies chosen. The range of spatial scales over which environmental impact studies could be carried out is shown in Table 4 (from Wratten & Forbes, 1995). zyxwvutsrqp Table 4. Temporal and spatial scales for environmental impact studies for faecally excreted veterinary products (Wratten & Forbes, 1995) MICRO MESO MACRO Sampling Unit Individual Spatial Scale Temporal Scale Pat Days - weeks Method of Investigation Laboratory/semi-field (Individual)/population/ function Pat/pasture Weeks - months (within season) Whole pasture/ between field effects Population/community/ function Pasture/farm Months - years (within/between seasons) Between/beyond field effects up to scale of commercial usage zyxwvu Micro-scale work on the effects of ivermectin on dung insect fauna The micro-scale experiments demonstrate effects on some non-target insects of the dung fauna in animals treated with avermectins, and these are essentially as would be expected from a knowledge of avermectin pharmacokinetics, formulations and innate biological properties. Adverse effects in non-target dung-insects ascribed to the presence of avermectin residues show considerable variation, some species being apparently unaffected, others being more sensitive. Generally, the literature on micro-scale studies shows larvae of coprophagous insects to be more susceptible than adults; in fact, effects on adult dung insects are generally absent, although non-specific reductions in reproductive capacity have been described in some species following exposure to avermectin residues. Cyclorrhaphan (Diptera) larvae have frequently been shown to be sensitive to faecal avermectin residues, whilst Nematocera (Diptera) may be largely unaffected. The time following treatment over which adverse effects on dung insect larvae have been noted reflects the apparent innate susceptibility of the different insects and depends on the formulation of avermectin used and the route of administration. Tables 5 and 6 summarise much of the available data derived from micro-scale experiments in which the effects of the avermectins on individual species, genera or sub-orders of dung insect have been recorded. Most data are available for ivermectin injection and in general results from studies with topical ivermectin and abamectin injection are qualitatively and quantitatively similar to ivermectin injection. These Tables illustrate the likely maximum duration of effect following treatment with these formulations, which for dung beetle larvae is up to 21 days and for fly larvae can be several weeks. In terms of feeding or breeding behaviours, body size or taxonomic grouping, there are no immediately apparent explanations for these differences in response. From an ecological perspective, the precise number of days over which effects are noted at the micro-scale is relatively unimportant, what is important is the ability of the dung fauna communities to show resilience to, or recover from, such perturbations in the field, and this cannot normally be assessed in micro-scale experiments. Results obtained at the lower levels are not necessarily predictive of the results of experiments at a higher scale Environmental assessment of avermectins zyx zyx zyx 341 Table 5. sensitivity of dipteran larvae to avermectins, indicated by days post-treatment (injection or topical) until adult emergence from dung equalled that of controls zyxwvut Species Days post-treatment with no effect on adult emergence Haematobia irritans 56 (Miller et al., 1981) 63 (Fincher, 1992) 42 (Schmidt, 1983) 14 (Meyer, Simco & Lancaster, 1980) 32 (Wardhaugh & Rodreguez-Menendez, 1988) 17 (Lumaret et al., 1993) 14 (Schmidt, 1983) >30 (Madsen et al., 1990) 42 (Sommer et al., 1992) 20 (Madsen er al., 1990) 0 (Sommer et al., 1992) Musca autumnalis Neomyia cornicina Stomoxys calcitrans ‘Cyclorrapha’ ‘Nematocera’ zyxwv Table 6. Sensitivity of coleopteran larvae to auermectins, as indicated by days post-treatment (injection or topical) until adult emergence from dung equalled that of control Species Days post-treatment with no effect on adult emergence Onthophagus gazella 17 (Sommer & Nielsen, 1992) 21 (Fincher, 1992) 10 (Madsen er al., 1990) 13-14 (Sommer er al., 1992) 14 (Strong & Wall, 1994) 16 (Wardhaugh & Rodriguez-Menendez, 1988) 10 (Lumaret et al., 1993) Aphodius spp. Copris hispanus Euoniticellus fuluus and cannot alone be considered predictive of ecological impact at the population or community level (Brown & Stephenson, 1990). Nevertheless, results of this type of experiment, used in conjunction with quantified estimates of actual or maximal exposure levels in the field, are used in environmental risk characterisation. From the preceding sections on use patterns, it can be calculated that the proportion of dung insects which could be exposed to avermectin residues during the grazing season would be extremely low. Computer simulations incorporating parameters such as dung insect biology, avermectin effects, avermectin use, cattle herd structures, dung production and period of attraction indicate that on a typical farm, only a very small percentage of the non-target, dung insect population would be exposed to avermectin residues over a grazing season (Sherratt, MacDougall & Forbes, submitted). As a result of asynchrony and heterogeneity of use, at any particular time in the grazing season, the great majority of freshly deposited dung in any one area will be free of avermectin residues and available as a resource for both multivoltine and univoltine species of insect. Meso- and macro- scale studies on the effects of ivermectin on dung insect fauna Large scale, longer term trials, in which pastures containing avermectin-treated cattle were separated from pastures with control animals, show that dung insect populations possess resilience to perturbations and appear to be able to recover from any local effects attributed to treatment. 342 zyxwvutsrq zyxwvu S D WRAITEN AND A B FORBES Germany was the location for studies in which four matched groups of young cattle were each assigned to one of two pairs of paddocks (Barth et al., 19946). One group of each pair was treated with ivermectin injection at the recommended dose, administered at 3, 8 and 13 wk after turnout. Naturally deposited pats, passed at 0, 7, 14 and 28 days after the first treatment (in June) were examined at weekly intervals after deposition for 7 wk before a final evaluation at 9 wk. A similar sampling regime was used for one of the pairs of paddocks after the third treatment (August). The results of these trials demonstrated that a dung fauna, considered typical for that region, was present throughout the grazing season. The species present and their distribution was similar between pastures containing treated cattle and those with untreated cattle. The total number of beetle adults and larvae recovered from the pats was also similar. The number of fly larvae collected was however reduced by some 36% in the pats from treated calves. Given the relatively high proportion (50%) of cattle treated on this farm, compared with a commercial farm, these results indicate that treatment with avermectins may have some impact on numbers of dung insects for a limited time. The number of adult beetles and the species present in collections from dung the following year at the same site, were very similar to those of the previous year, indicating that any reduction in insect numbers had been only temporary (Barth el al., 19936). Lancaster et al. (1991) describe a series of trials in which the effects of treatment with topical ivermectin on hornfly (Haematobia irritans) numbers were evaluated. Ivermectin, when administered topically, is effective against the blood-feeding adult flies; in addition the resultant faecal residues inhibit the development of hornfly larvae in the dung. Each trial comprised groups of treated and untreated cattle allocated to pastures separated by distances of 500-1000m; in some of the studies, treatment was given on more than one occasion. The results of these studies demonstrated a high level of efficacy of ivermectin against this parasite, with fly numbers being suppressed on treated animals for a mean of 35 days after treatment. Given the fact that the hornfly is virtually an obligate parasite of cattle, it is a blood feeder and is almost completely dependent on dung for breeding, this effect of treatment is not surprising. Despite this local impact on hornfly populations and the fact that all animals on individual pastures were treated, the number of flies counted increased to the values of the control groups over time; the recovery of the population presumably resulted from larvae or pupae in pats deposited on the pasture prior to treatment and from immigration of adult flies from other cattle nearby. zyxwvut zyxwv Effects of auermectins on earthworms Effects of ivermectin on earthworms has been studied under laboratory and field conditions. In an in vitro experiment using the test organism Eisenia foetida Savigny, a worm associated with sewage rather than pasture, Halley et al. (1989) reported no effects at the lower test concentrations and mortality and weight loss at the higher levels. The concentrations of ivermectin at which effects were observed exceeded those expected after routine treatment and the conclusion drawn was that the residues of ivermectin present in faeces of cattle after treatment posed no risk to earthworms. A second experiment using the same earthworm species was conducted by Gunn & Sadd (1994); in this study formulated product (ivermectin sheep drench) was used for spiking the soil. Ivermectin comprises only 0.08% of the formulation used so the carrier was present at levels of between 2.5 and 60 ml kg-' to achieve the reported concentrations of ivermectin in the soil . As there was no carrier-spiked control, it is impossible to determine whether the vehicle or the ivermectin was responsible for the observed changes in the test earthworms. Contrary to the authors' beliefs, the excipients are extensively metabolised in the rumen and would not have been present in the faeces of treated animals in the same proportions as in the formulated product. zyxw zyxw zyx zyxwvuts Environmental assessment of averrnectins 343 Trials conducted outdoors at the semi-field or field scale have shown that under more natural conditions there are no adverse effects on the common earthworms found in pastures arising as a result of cattle having been treated with ivermectin (Wall & Strong, 1987; Madsen, Gronvold, Nansen & Holter, 1988; Madsen et al., 1990; Wratten et al., 1993; Barth et al., 1994b). The degradation of dung from cattle treated with avermectins Theoretically the use of avermectins in cattle could influence dung degradation in one of two ways: Residues of avermectins present in the faeces after treatment may result in reduced numbers and activity of certain insect larvae and hence lower their contribution to dung decomposition. (ii) By removing gastrointestinal parasites, avermectins (and other effective anthelmintics) can ameliorate their effects, which include diarrhoea. Treated animals may, therefore, produce dung with a lower water content and possibly different composition compared to that of untreated animals. (i) zyxwvut No observable effect on the rate of degradation was found in an early trial with ivermectin injection (Schmidt, 1983), although this paper contains no quantitative data. Three publications from Denmark (Madsen et al., 1988, 1990; Sommer et al., 1992) reported slightly slower rates of degradation of dung passed shortly after a single treatment with injectable or topical ivermectin; however, other trials also conducted under European conditions showed no effects. A pilot study in Scotland using dung spiked with various levels of ivermectin, all of which exceeded those which would occur after normal product use, showed little or no difference in the rate of dung disappearance in pats deposited in May, June, August or September (McCracken & Foster, 1990). A trial in Scotland (McKeand, Bairden & Ibarra-Silva, 1988), in which a 3, 8 and 13 wk treatment programme was used, showed that naturally deposited pats on pasture disappeared at a similar rate from control cattle and from those treated one week previously with topically applied ivermectin. Degradation was evaluated by measuring pat diameter, depth and wet weight. A study from southern England (Jacobs, Pilkington, Fisher & Fox, 1988) showed that by the commencement of the subsequent grazing season following a trial in which topical ivermectin had been used at 3 , 8 and 13 wk after turn-out, pats from treated and control paddocks had all disappeared. Two German studies (Schaper & Liebisch, 1991; Barth et al., 1994b) found no differences in degradation between control pats and those from animals treated with ivermectin injection 3 and 8, or 3, 8 and 13 wk after turnout; disappearance was measured by dung weight, organic matter content, diameter and photographic record. A trial in England, in which effects were evaluated over two successive years, showed that the use of ivermectin injection in a 3-8 and 13 wk schedule, was not associated with any significant negative effects on the rate of pat decomposition, grazing area or organic matter of soil (Wratten et al., 1993). An early report of a study in England (Wall & Strong, 1987) on the degradation of artificial pats derived from cattle treated with a prototype ivermectin sustained-release bolus noted a delay in the disappearance of dung from treated cattle. Subsequent publications which included evaluations of the effects on dung from cattle treated with an ivermectin bolus failed to confirm the earlier findings. A trial in the USA (Wallace. Holste, Roncalli & Gross, 1991), showed no difference in the rate of degradation of naturally deposited dung pats from control and ivermectin sustained-release bolus treatment groups. A further study in Germany with an ivermectin bolus found no significant differences between pats 344 zyxwvu zyxwvutsrq zyxwvutsrq zyxwv S D WRATTEN AND A 0 FORBES from treated and control animals in respect of pat surface area or residual organic matter (Barth et al., 19936). This applied to pats marked in June, July or September; by the commencement of the following year’s grazing season, all pats had virtually disappeared. A trial in England, carried out over two consecutive years, showed that the pastures grazed by cattle treated each year with an ivermectin bolus were not significantly different from pastures grazed by control cattle (Wratten et al., 1993). Parameters evaluated include pat dry weights, dry weight of accumulated standing dung, organic matter of soil and grazing avoidance. There is evidence from the literature that the partial or total exclusion of insects from dung either by mechanical means or by treating pats with insecticide can, at times, delay degradation (Holter, 19796; Anderson, Merritt & Loomis, 1984). It is, therefore, not unreasonable to speculate that the presence of residues of avermectins, or other insecticides, in the faeces of treated animals could sometimes produce similar effects. Nevertheless, the literature to date is equivocal and indicates that no consistent adverse effects on dung degradation or pasture quality are seen in association with the use of avermectins. Given that avermectin use produces no adverse effect on the dung aerating, removing and burying activity of adult dung beetles and given the variable, and generally minor, role of insect larvae in dung degradation in temperate regions, the overall absence of observed effect is not surprising. The reasons why results of individual studies are at variance with this general conclusion are probably related to the innate variability of biodegradation of dung and limitations in experimental design. Potential for avermectins to produce indirect ecological effects There remains only one other possible negative effect of avermectins, this is via foodweb effects, whereby dung invertebrates are consumed by vertebrates and invertebrates at the next trophic level (predation and parasitism). Most predators of dung fauna are likely to be polyphagous and mobile, with the ability to ‘switch’ prey types according to their relative availability. This polyphagy and mobility coupled with the low proportion of pats likely to contain avermectins, indicates that effects on these predator populations will be negligible. There is some published information (Schmidt, 1983; Fincher, 1992; Barth et al., 1994a,b) which indicates that predatory beetle numbers in dung pats are unaffected by avermectins, and so their role in dung pat communities remains and predatory beetles may complement the effects of avermectins on pest fly larvae in dung. A reduction in parasitoid wasp numbers in pats from treated cattle was noted by Schmidt (1983), but he attributed this to a lack of suitable hosts (dipteran larvae and pupae) rather than direct toxicity, a similar conclusion to that drawn by Floate (1995). Conclusion The bulk of experimental evidence from the field shows that the normal practical use of avermectins produces little measurable effect on the rate or extent of dung degradation. This can be explained by recognising that faeces of treated animals are readily colonised by the local dung fauna, including flies, dung beetles and earthworms. Disruption of the dung pat by adult beetles and earthworms can proceed normally. Avermectin faecal residues do not adversely affect earthworms, or the dung burying activity of adult dung beetles or the bacteria and fungi which complete the process of decomposition. The direct effects of avermectin residues on dung insect populations are restricted by the limited exposure resulting from the phenology of susceptible species and stages of insect zyxwv zyxw zyx Environmental assessment of avermectins 345 and the seasonality and heterogeneity of product use. Some important treatment times for avermectins, f o r example, a t housing or a t induction into a feedlot, are of no relevance t o the dung fauna found o n pasture. T h e great majority of faeces deposited during the grazing season will not contain avermectins because of the limited product use and the predominance amongst treated animals of first-year grazing stock, which are low net contributors t o the total amount of faeces deposited on pasture. Quantified extrapolations from small-scale, controlled experiments and the collective evidence from field studies indicate that even under relatively high levels of exposure t o avermectin residues in dung, populations of dung-dependent beetles and flies are affected t o a limited degree only and that recovery readily takes place from any local perturbations. zyxwvu References Anderson J R, Merritt R W. 1W7. The impact of foraging meadowlarks (Sturnella neglecta) on the degradation of dung pats. Journal of Applied Ecology 14:355362. 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