SEARCH

SEARCH BY CITATION

Keywords:

  • Cattle;
  • community structure;
  • decomposition;
  • dung;
  • insect;
  • macrocyclic lactone;
  • mitigation

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Area-wide impact
  5. Impact amelioration
  6. Conclusions
  7. Acknowledgements
  8. References

Following the treatment of cattle with veterinary parasiticides and insecticides, residues are excreted into the dung in concentrations that may be toxic to functionally important dung-colonizing insects. In the dung, these residues cause a range of well-studied lethal and sub-lethal effects, the magnitudes of which vary with the compound used, mode of administration and concentration, and the insect species in question. Particular concern has been associated with the use of macrocyclic lactones in this context. Loss of insect colonizers may delay pat decomposition, but field studies report contrasting results that reflect confounding factors such as weather conditions, pat moisture content, pat location, time of year and dung insect species phenologies. The question of fundamental concern is whether the impacts seen in experimental or laboratory studies are likely to have a functional impact on insect populations, community interactions and the economically important process of dung decomposition. Recent studies which have attempted to address these wider, landscape-level impacts in temperate ecosystems are reviewed here. These show that the extent to which chemical residues may have any sustained ecological impact will depend on both a range of farm management factors, such as the temporal and spatial patterns of chemical use, the number of animals treated and the choice of active ingredient, and a range of insect-related factors, such as abundance, population dynamics and dispersal rates. However, they also demonstrate that considerable uncertainty remains about the likely extent of such effects and that current data are insufficient to support firm conclusions regarding sustained pasture-level effects. More large-scale, longterm field experiments are required, particularly in relation to insect dispersal and functional interactions within the dung insect community.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Area-wide impact
  5. Impact amelioration
  6. Conclusions
  7. Acknowledgements
  8. References

The dung of cattle is an abundant and rich resource that forms an ecologically distinct environment for a complex successional insect community (Landin, 1961). It is high in energy and can be relatively predictable in its occurrence compared with other patchily distributed resources, such as carrion, particularly where a large population of dung-producing vertebrates is present. Many insects, particularly Coleoptera and Diptera, exploit this valuable resource by feeding on dung throughout their larval stages (Strong, 1992).

The timely removal of dung from pastures by insect activity and weathering is both functionally and economically important. Dung insects may serve as an essential resource for insectivorous birds and small mammals (McCracken, 1993) and a range of other invertebrate predators (Vale et al., 2004). If appropriate decomposition does not occur, farmers may incur considerable economic losses arising from the fouling of pasture (Dickinson et al., 1981), increases in dung-breeding pest fly populations (Smith et al., 1989; Strong, 1992; Mendez & Linharez, 2002) and enhanced transmission of livestock endoparasites (Stevenson & Dindal, 1987a). The benefits of rapid dung removal are therefore considerable; not only does it reduce such losses, but it helps to return nutrients to the soil, particularly nitrogen, a large proportion of which would otherwise be lost as ammonia (Stevenson & Dindal, 1987a, 1987b; Lumaret & Kadiri, 1995). In an attempt to put an economic value on ecosystem services provided by insects, Losey & Vaughan (2006) concluded that dung invertebrates save the U.S. cattle industry US$380 million each year.

Many modern agricultural grazing practices, however, may profoundly damage this dung insect community. Soil disturbance through ploughing, the use of chemical fertilizers and the removal of herbaceous field borders have all been shown to affect dung-colonizing insects (Hutton & Giller, 2003). Of particular concern is the treatment of cattle with parasiticides and insecticides. Following the treatment of livestock with these compounds, chemical residues may be excreted in faeces in concentrations that are toxic to dung-colonizing insects. In the dung, these residues cause a range of lethal and sub-lethal insecticidal effects, the magnitudes of which vary with the compound used, mode of administration and concentration, and the insect species in question. The loss of insect colonizers may delay pat decomposition (Wall & Strong, 1987; Dadour et al., 1999; Lee & Wall, 2006a), but an effect on decomposition is not always evident, possibly as a result of the many confounding factors associated with field experiments. Numerous comprehensive reviews have detailed these effects, focusing particularly on the macrocyclic lactones (Strong & Brown, 1987; Strong, 1992; Lumaret & Errouissi, 2002; Floate et al., 2005; Wardhaugh, 2005).

Despite the extensive interest in this issue over many years, the majority of studies of the effects of macrocyclic lactone residues on dung-colonizing insects have been restricted either to single-target species/pesticide combinations or to the local effects of a compound on dung colonization and decomposition. The functional effects, if any, of these pat-level effects on the wider, landscape-level pastureland community and pasture fertility have received relatively little attention to date, particularly in temperate ecosystems, perhaps because of the huge difficulties associated with conducting such research on an appropriate ecological scale. Understanding the impact of livestock parasiticide treatments on biodiversity was identified by Sutherland et al. (2006) as one of the 100 most important policy issues in applied ecology. Evidence is required to show the extent to which these compounds have any real impact on: (a) distribution patterns and population dynamics of dung and soil invertebrate species; (b) the functional ecology of pastures; (c) the process of decomposition, and (d) the insectivorous animal community that depends on dung-breeding insects. The aim of this paper, therefore, is to synthesize the relatively small number of existing studies that consider the impacts of macrocyclic lactone residues at pasture level, focusing in particular on temperate ecosystems, and to highlight the key areas in which future studies are most urgently required.

Area-wide impact

  1. Top of page
  2. Abstract
  3. Introduction
  4. Area-wide impact
  5. Impact amelioration
  6. Conclusions
  7. Acknowledgements
  8. References

Experimental studies

Perhaps the earliest example of an attempt to consider the impact of the macrocyclic lactone, ivermectin, at pasture level is the work of Wratten et al. (1993). They examined the decomposition of pats over two grazing seasons in southern England in pastures grazed by cattle treated with either an injectable or a sustained-release intraruminal bolus formulation of ivermectin. They concluded that no impact on pat decomposition rate or soil organic matter content could be detected. However, this early study suffered from a number of serious methodological problems, including the use of an inappropriate approach for the measurement of soil organic matter and the fact that many of the experimental pats from treated animals were examined at a time after treatment by which no ivermectin would have been expected to be present in the voided faeces.

Dung decomposition studies are particularly vulnerable to the confounding effects of pasture heterogeneity, climatic stochasticity and dung invertebrate species phenology. For example, decomposition of dung from cattle treated with an ivermectin bolus in a 2-year study in Denmark was highly influenced by season, weather and local differences between plots. Although the decomposition of ivermectin-containing dung was significantly slower than that of untreated dung in the first year, decomposition was retarded in the ivermectin treatment group only in the spring of the second year of the study (Svendsen et al., 2003). In the first year, the percentage moisture content of control dung was higher than that of dung from ivermectin-treated cattle, but this difference was less pronounced in the second year. Barth et al. (1993, 1995) have shown that an increase in moisture of as little as 1–2% may increase the rate of dung decomposition. Svendsen et al. (2003) found no significant correlation between the initial moisture content of the dung and subsequent decomposition, but the lack of pasture replication made it impossible to conclude whether there was a confounding effect of dung moisture content on decomposition.

Changes in the structure of dung insect communities after the treatment of cattle with a single injection of ivermectin (200 µg/kg) were investigated in a relatively large-scale trial in South Africa, using 80-ha paddocks under extensive farming conditions. When the study was carried out during a period of drought, the results indicated that the use of ivermectin affected community structure through a reduction in species diversity and an increase in species dominance. These effects appeared to last for up to 3 months after ivermectin treatment (Krüger & Scholtz, 1998a). However, when the experiment was conducted in the wet season, no effect of ivermectin on dung insect communities was observable 1 year after the 1992–1993 treatment (Krüger & Scholtz, 1998b). The authors concluded that any large-scale impact of ivermectin is likely to depend on several factors, including climatic conditions, the spatial scale of treatment and the number of animals treated in a herd. This is in agreement with findings in another relatively large-scale South African study, in which dung beetles were monitored over a period of 8 months in a treated and untreated herd of cattle using dung-baited pitfall traps. No longterm impact of ivermectin injection (plus fluazuron) on dung beetle communities was detected during a year with above-average rainfall (Kryger et al., 2005).

The question of ecosystem service disruption is particularly pertinent in Australia, where several species of exotic dung beetles have been established in an attempt to improve the decomposition rate of the dung of introduced ruminants. A pasture-level study in Western Australia found that dung pats collected 7 and 10 days after cattle had been treated with ivermectin at 200 µg/kg, were dispersed significantly less by the introduced species of dung beetle, Onthophagus taurus (Schreber) (Coleoptera: Scarabaeidae), than were untreated dung pats (Dadour et al., 1999).

To assess the impact of farm management on dung beetles in Ireland, their abundance, biomass, diversity and species richness were compared using dung-baited pitfall traps on intensive, organic and rough-grazing farms (Hutton & Giller, 2003). The results showed that beetle biomass, diversity and species richness were significantly greater on organic farms compared with intensive and rough-grazing farms. Hutton & Giller (2003) ruled out an immediate effect of dung type by undertaking a colonization experiment with experimental pats made from homogenized dung from the three farms, which again demonstrated the greater abundance of dung beetles on organic farms. They concluded that intensive agricultural management, including the use of chemical fertilizers, veterinary drugs (e.g. ivermectin) and the removal of herbaceous field boundaries, could be detrimental to dung beetle biodiversity and dung decomposition (Hutton & Giller, 2003). However, although some of the results suggested that ivermectin use may have contributed to the effect, the authors were not able to clearly differentiate the impacts of the various possible contributory factors.

Studies of the effects of macrocyclic lactone residues on natural populations of the yellow dung fly, Scathophaga stercoraria (Linnaeus) (Diptera: Scathophagidae), in grazed pastures in Scotland showed that although the abundance of S. stercoraria varied significantly among years and with season, there was no difference in its abundance between fields grazed by avermectin-treated and those used by untreated cattle (Webb et al., 2007). However, this study also examined wing asymmetry and found that asymmetry was significantly higher in populations of S. stercoraria in fields grazed by doramectin-treated cattle. This suggested that exposure to doramectin during development may have imposed some degree of sub-lethal environmental stress, which might, in time, result in longer-term impacts on the population's abundance.

Modelling studies

Perhaps because of the considerable difficulty associated with large-scale field studies, recent attention has focused on the use of modelling in attempts to estimate likely impacts. In one such study, the impact of avermectins on dung insect populations was shown to be highly dependent on factors such as the proportion of cattle treated, the length of time faeces remain attractive and the time taken by cattle to excrete all active residues (Sherratt et al., 1998). In typical northern European cattle-farming systems, estimates of the maximum cumulative insect mortality in a given season were rarely >25% (Sherratt et al., 1998).

A model to assess the impact on univoltine and multivoltine dung beetle species of a single treatment of cattle with eprinomectin or moxidectin was developed by Wardhaugh et al. (2001). They concluded that multivoltine species would be more affected than univoltine species, with a maximum disturbance to populations if treatment occurred 2 weeks post-peak spring emergence. They suggested that beetle activity in the subsequent generation could be reduced by 35%, or by 25% in slow-developing species. However, this is likely to be a conservative estimate as the model was based solely upon juvenile mortality. Further, the models developed did not consider sub-lethal effects, such as a reduction in the reproductive ability of the insects, were relatively short-term in outlook, focusing on within-season insect mortality, and did not consider species interactions, such as competition and density-dependent effects (Hirschberger, 1995, 1999).

A novel attempt to develop a simple index for predicting the likely effects of veterinary parasiticides on some species of dung-breeding flies was developed by Boxall et al. (2007). These authors undertook a questionnaire survey of cattle farmers in the U.K., in which they asked about the products used, the frequency of use and the percentage of animals treated at any one time. They used published data on excretion rates and parasiticide toxicity against three species of pest fly to construct a simple risk model of the likely impact over time for these insect species, given the reported pattern of parasiticide use. For each of three pest fly species considered, a single season-long estimate of probable impact was presented (Boxall et al., 2007). Their analysis supported the conclusion of Sherratt et al. (1998) in suggesting that a large proportion (35%) of parasiticide treatments in England will have no impact on dung-breeding fly populations. In terms of individual parasiticides, the macrocyclic lactone doramectin (pour-on) was predicted to have the highest impact on fly populations with a maximum reduction in the population of the horn fly, Haematobia irritans (Linnaeus) (Diptera: Muscidae), of 28%. Ivermectin pour-on had the next highest impact (6.8%), followed by eprinomectin (6.4%) and ivermectin (4.1%) injection. However, for this study, useable questionnaire data were obtained from only 18 dairy farms, 10 mixed beef and dairy farms and 32 beef farms. Data from these three farm types were then pooled in the analysis, despite the fact that their very different patterns of parasiticide use were likely to have different ecological consequences. Toxicity data for each of the three insect species considered were used as a single time-weighted average in a manner that ignores that fact that complete toxicity for 1 week after treatment, followed by gradual loss of toxicity, has very different ecological consequences to survival averaged over 4 weeks. Finally, the model appears to ignore phenological changes in abundance, assuming instead that the three pest fly species in question were available continuously at a fixed population size from April to September. In reality, however, losses to the population in early spring, when beef cattle are treated after turnout, will result in a disproportionate reduction in population size later in the season. Clearly, the approaches of Sherratt et al. (1998) and Boxall et al. (2007) also give no prediction about the effect of parasiticide residues on community structure, but only on individual species. Nevertheless, the approaches used would appear to hold promise for development into more comprehensive tools in the future.

Probably the most sophisticated attempt to model the spatial impact of insecticide-treated cattle was undertaken by Vale & Grant (2002). They used spatially explicit, deterministic models to consider the importance of a wide range of treatment regime characteristics and insect life history characteristics on the abundance of hypothetical dung-colonizing insects. They concluded that, despite wide variations in the impact of contamination, in many situations the risk to dung fauna may be substantial, especially for slow-breeding beetles and muscid flies. They suggested that a number of factors would be important in explaining variations in the extent of this risk. Of particular significance were variations in pat toxicity, treatment interval, density-dependent death and recruitment, mortality during dormancy, frequency of pat occupation by breeding adults, general rate of dispersal, and the size and shape of the area containing treated cattle.

Impact amelioration

  1. Top of page
  2. Abstract
  3. Introduction
  4. Area-wide impact
  5. Impact amelioration
  6. Conclusions
  7. Acknowledgements
  8. References

Timing of application

Temperate habitats in particular are characterized by distinct seasonal changes in climate and photoperiod and the strongly seasonal phenology of individual insect species. In tropical habitats, species phenology is often associated with wet and dry seasons, and high rates of emergence occur at the beginning of the wet season. Any impact of parasiticide residues on dung-breeding insect populations might be particularly severe if it occurred during a critical breeding period. As the majority of cattle in temperate habitats are treated with macrocyclic lactones at and during the weeks immediately following spring turn-out (Boxall et al., 2007), insect populations might be expected to be particularly vulnerable at this time. In northern temperate environments any impact may be exacerbated by the fact that most Aphodius species (Coleoptera: Scarabaeidae), in particular, have a relatively short temporal occurrence during the year and most appear to be univoltine (Landin, 1961; White, 1960; Hanski & Koskela, 1977; Hanski, 1980; Holter, 1982). The study by Dadour et al. (1999) also concluded that, in order to minimize environmental impacts on introduced beetles in Australia, cattle treatments should be focused during the autumn and winter when there is negligible dung beetle activity.

However, several authors have previously found the temporal occurrence of natural communities of temperate dung beetle species to be well spaced throughout the year (White, 1960; Hanski & Koskela, 1977; Hanski, 1980; Holter, 1982; Sowig, 1997; Finn et al., 1998). It has been suggested that this pattern of phenology may be an important factor associated with niche separation in dung pats (Sowig, 1997). In Ireland, Finn et al. (1998) identified three seasonal groups of Aphodius species that appeared consistently in spring, early summer and late summer. In a 2-year study in southwest England, seasonal changes in community structure were relatively gradual and subtle, although Coleoptera were generally more abundant earlier and Diptera later in the season (Lee & Wall, 2006b). These studies suggest that spring treatment would be unlikely to have a disproportionate impact on dung beetle communities compared with treatments at other times of year. Nevertheless, although the abundance of the different species inhabiting dung may be fairly evenly spread throughout the season, it is important to distinguish species availability from activity and two distinct seasonal peaks in Aphodius activity were described by Holter (1982), the first in late May and early June and the second during August. In addition, it is notable that most studies are carried out on species-impoverished, agriculturally improved grasslands and therefore often exclude less eurytopic species.

Many studies have highlighted the pronounced stochastic variation in the mixture of species that find a given patch in dispersed, ephemeral habitats, such as dung, and have suggested that this is likely to contribute to community stability and coexistence (Hanski, 1987; Hanski & Cambefort, 1991). The functional impact of the loss of particularly sensitive species at specific times of year is not well understood. However, in a study of dung colonization in a temperate habitat, Wall & Lee (2010) noted that the dung-colonizing community contained, on average, only approximately half the total number of taxa that were available at any time. The majority of dipteran and coleopteran taxa showed significant aggregation, which appeared broadly binomial in distribution (see also Hutton & Giller, 2004). Based on this observation, a simulation analysis was used to demonstrate that the observed distribution of species did not differ from that to be expected if colonization occurred at random. The results supported the proposal that stochasticity in colonization plays a significant role in shaping the assembly of the dung-inhabiting community observed and aggregation is driven by differences in egg-batch size. In terms of practical implications, the highly aggregated distributions highlight the possibility that, in the short-term, populations of even highly abundant insects will be more susceptible to the deleterious effects of insecticide residues in dung than if they were evenly distributed, if by chance they colonize a pat containing chemical residues from a recently treated animal. Nevertheless, these results also suggest that there would be considerable resilience within the dung community and, although mortality for a particularly sensitive species might be high at a time when it was abundant, longterm impacts on the process of decomposition are less likely to be affected.

Hence, the results suggest that the focused treatment of cattle, such as at spring turn-out in temperate habitats, is particularly likely to adversely affect spring breeding populations of flies and beetles, as highlighted by Dadour et al. (1999). Nevertheless, the functional impact of the loss of particular species in most temperate habitats is less clear. The extent of any effect will depend on the numbers of animals treated in any one area. Losses early in the insect breeding season will have disproportionately large impacts in terms of population dynamics, compared with losses later in the year. However, the considerable resilience of the dung-decomposing community may compensate for individual species loss. Australian temperate habitats are likely to represent a key exception to this principle because the loss of even small numbers of introduced exotic species is likely to be highly detrimental. Clearly, a greater understanding of the functional interactions between the components of the dung-colonizing insect community is essential.

Spatial scale

On most farms, a mosaic of treatments will be administered to cattle, depending on cattle age and breed, and farm type (beef, dairy or mixed) (Boxall et al., 2007). As the modelling studies described above indicate, the proportion of animals excreting insecticidal residues simultaneously will have important consequences for the impact on the local insect population. One factor influencing this concerns whether the presence of residues can be detected by dung-colonizing insects. Webb et al. (2010) examined populations of Aphodius dung beetles in 26 pastures on eight farms in southwest Scotland over 2 years. The pastures were grazed either by cattle that were untreated or by cattle that had been treated with an avermectin product (doramectin or ivermectin). To measure beetle numbers, pitfall traps baited with dung from untreated cattle were deployed in all the pastures included in the study. Significantly more beetles were trapped in fields grazed by treated cattle than in fields in which cattle remained untreated. This result was explained by suggesting that the Aphodius were avoiding the dung of treated cattle and therefore were caught in greater numbers in the pitfall traps baited with the dung of untreated animals. Additional trials subsequently confirmed this, showing that beetles preferentially colonized dung of untreated vs. doramectin-treated cattle. Webb et al. (2010) concluded that, as the Aphodius beetles appeared to avoid the dung of treated cattle, the potential harmful effects of residues in cattle dung might be reduced through livestock management practices that maximize the availability of dung from untreated livestock in areas in which avermectins are being used. Lumaret et al. (1993) concluded that ivermectin residues excreted between 4 and 6 days post-injection were highly attractive to dung beetles. However, substantive species-specific differences in response to dung from cattle topically treated with doramectin, eprinomectin, ivermectin or moxidectin compared with responses to untreated dung have been recorded (Floate, 2007). In a 2-year study in Canada, both attractive and repellent effects were found. Eleven cases of attraction and 11 of repellence were associated with doramectin; eprinomectin tended to repel insects, and ivermectin and moxidectin showed strong attractive effects (Floate, 2007). Such species-specific responses were also recorded by Holter et al. (1993), who detected an attractive effect of ivermectin in a temperate climate (Denmark), but no overall difference in beetle numbers caught in tropical climates (Tanzania and Zimbabwe). Beetles tended to be more attracted to control dung in Tanzania, whereas, in Zimbabwe, two beetle species were more attracted to treated dung and three species showed no preference. These results have implications in the interpretation of field experiments and models that combine an element of dung attractiveness.

In the modelling study conducted by Vale & Grant (2002), which is probably the only attempt to consider explicitly the spatial scale of treatment relative to the dispersal abilities of insects, the authors concluded that the risk for impact extended well outside the treated areas for a distance equal to several daily displacements of the insects in question. They recommended that untreated refuges for species survival should be considered and that these should be compact blocks at least 25 daily displacements wide. This valuable study also serves to highlight the fact that, in the majority of cases, little detailed information exists on the dispersal movements of most dung-colonizing insects and that without these data, the impact of scale on the population dynamics of these species remains impossible to gauge. The inclusion of data from those large-scale spatial modelling studies of dung beetles that do exist (e.g. Roslin, 2001) would enable the complexity of the dung insect community to be incorporated into models assessing the area-wide impact of parasiticides.

Mechanical fragmentation

Microorganisms probably perform the majority of the degradation of dung (White, 1960; Holter, 1979, 1982), whereas the activities of the arthropod community and the weather influence the rate at which this degradation proceeds (Marsh & Campling, 1970). Insects tunnel through the dung and thereby increase the surface area available to the microorganisms that break it down. The actions of insects also enhance degradation through fragmentation, aeration, removal by assimilation and conversion into insect faeces with differing properties (Lussenhop et al., 1980). Aeration is particularly important in the early stages of succession when degradation may be limited by anaerobic conditions, although such activity also accelerates the drying of the dung, which may limit decomposition in the later stages (Stevenson & Dindal, 1987b). A high density of insects present in dung also attracts insectivores such as birds and small mammals, which may contribute by disintegrating pats in search of food (Laurence, 1954; Marsh & Campling, 1970; Anderson & Merritt, 1977). Clearly, therefore, mechanical processes such as harrowing, which serve to break up standing dung in the field, are likely to significantly contribute to its decomposition by microorganisms. However, it is likely that this would be disastrous to coprophagous insects, especially slow-developing endocoprid beetle species, and whether such mechanical approaches would ever be practical and cost-effective on cattle farms is open to question.

Compound and application method differences

The macrocyclic residue profile in dung varies with a range of factors, particularly the route of administration. For example, typical mean concentrations of ivermectin (in p.p.m. dry matter) after subcutaneous injection at 0.22 mg/kg bodyweight were shown to be 3.70 ± 0.65, 5.12 ± 0.13, 3.82 ± 0.28 and 0.38 ± 0.17 at 1, 2, 5 and 13–14 days after treatment, respectively (Sommer et al., 1992). By contrast, pour-on formulations applied at 0.5 mg/kg bodyweight showed a slightly shorter excretion half-life but higher peak concentrations immediately after dosing, reaching 9 p.p.m. at 2 days after treatment (Sommer et al., 1992). Different compounds also vary in their impact on dung insects. For example, studies in which cattle were treated with a subcutaneous injection of either ivermectin (at 200 µg/kg) or moxidectin (at 200 µg/kg) found no difference in the numbers of cyclorrhaphous flies in untreated control dung and dung from moxidectin-treated animals. By contrast, these fly larvae were almost completely absent from the dung of animals treated with ivermectin and collected up to 14 days after treatment (Strong & Wall, 1994). This conclusion was supported by a comparative study of ivermectin, doramectin, eprinomectin and moxidectin, which found that suppression of insects was associated with the application of doramectin, eprinomectin and ivermectin, but not with the application of moxidectin (Floate, 1998). Based on the number of species affected and duration of suppression, these products were ranked in descending order (doramectin > ivermectin > eprinomectin ≫ moxidectin) according to adverse effect (Floate, 1998). Nevertheless, in some circumstances moxidectin may still have an adverse effect on coprophagous flies (Farkas et al., 2003; Iwasa et al., 2008).

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Area-wide impact
  5. Impact amelioration
  6. Conclusions
  7. Acknowledgements
  8. References

Macrocyclic lactone parasiticide treatments, which result in insecticide residues in cattle faeces, will inevitably have some degree of adverse effect on the abundance of non-target, dung-colonizing insect larvae in pats. However, the spatial and temporal impact of these effects will depend on a range of farm management factors, such as the patterns of anthelmintic use, the number of animals treated and the choice of active ingredient, and a range of insect-related factors, such as abundance, population dynamics and dispersal rates. The extent to which current use patterns will result in any impact at an ecosystem level is currently unclear and the economic importance of parasite control is such that the non-target impacts of endectocides have generally been considered to represent a low research priority and an acceptable risk. Nevertheless, despite the studies reviewed here, the magnitude of this risk remains unclear and no clear consensus exists about the impacts of macrocyclic lactone use on the persistence of the dung-decomposing community, pasture fertility or insectivorous vertebrates. A great deal of recent research effort has been directed towards the development of standardized laboratory tests to assess ecotoxic impacts (Hempel et al., 2006; Skripsky & Hoffmann, 2010). Although such tests are clearly of importance, they usually focus on a small number of common, well-studied species. Further work that takes into account sub-lethal, species-specific responses and community interactions to allow the resolution of issues related to impacts on complex pastureland systems is required. With some notable exceptions (Westergaard et al., 2001; Sommer & Bibby, 2002), the effects of ectoparasiticides on soil and dung community functioning have also been neglected.

Where ecosystem-level experimental studies have been undertaken, they have generally recorded transient or inconclusive results, although this perhaps reflects the complexity of the system and the difficulty inherent in conducting work on a scale sufficiently large to produce robust data as a result of the many confounding factors. The development of robust experiments, possibly at the more easily manipulated mesocosm level, is likely to be an important future challenge (Van den Brink et al., 2005). Although some modelling studies have suggested that only a small proportion of the local coprophilous insect population will be exposed to the active compound at any one time, leading to minimal pasture-level effects, most of the models developed to date have lacked the necessary level of sophistication to give confidence in this conclusion. Clearly, more advanced modelling, in addition to more extensive fieldwork, is required to fully resolve these issues. More information is particularly required on insect dispersal behaviour and population dynamics, for which large-scale field trials are needed. Changes in approaches to ectoparasiticide use, such as evidenced by the development of combination products or long-acting compounds, combined with little understanding of their longterm environmental impact, clearly highlight the substantial gaps in our knowledge. Without this work, recommendations about the optimum use of parasiticides in specific situations will be uncertain. Dung decomposition in Australian temperate habitats is likely to be particularly sensitive as the loss of even small numbers of introduced exotic species is likely to be highly detrimental. At present, where grazed grassland is managed specifically for the conservation of invertebrates or insectivorous bird and mammal species, it would seem prudent to recommend the use of less ecotoxic compounds and to ensure that staggered treatments are applied to the cattle population so that refugia remain in which dung-breeding insects in an area may persist.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Area-wide impact
  5. Impact amelioration
  6. Conclusions
  7. Acknowledgements
  8. References

We are grateful to Pfizer Animal Health for its support of this review and to Alice Chester-Master, School of Biological Sciences, University of Bristol, for her assistance with its preparation.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Area-wide impact
  5. Impact amelioration
  6. Conclusions
  7. Acknowledgements
  8. References