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.
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.