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Keywords:

  • Biodiversity;
  • breakdown;
  • dung fauna;
  • habitat;
  • invertebrate diversity;
  • ivermectin

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  1. Ivermectin is a broad-spectrum antiparasitic drug, routinely administered to livestock worldwide, and concerns have been raised about its impacts on non-target dung fauna and pasture systems. This study reports the effect of sward structure (long sward, short sward, or bare ground) on ivermectin persistence and cowpat colonisation by invertebrates, during an on-farm experiment in the United Kingdom.
  2. The levels of ivermectin in cowpats were high [21 899 μg kg−1 (dry weight) 1 day after treatment with a pour-on formulation] and remained detectable throughout the 47-day trial. Residue breakdown occurred, but levels persisted above those lethal to some invertebrates. Sward structure had no significant effect on ivermectin levels.
  3. Ivermectin residues affected cowpat colonisation. Diptera were present in significantly lower numbers in treated cowpats. Coprophagous Coleoptera were less affected by ivermectin residues, although some species were present in significantly higher numbers in treated cowpats in the long sward environments.
  4. The non-target effects of pesticides are currently of concern to policy makers. The results of this research add further weight to these concerns, particularly with regard to the duration for which ivermectin persists in situ in UK pasture, and because of the preferential attraction to treated cowpats exhibited by coprophagous Coleoptera.

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Ivermectin, a macrocylic lactone belonging to the avermectin group of chemicals, is a broad-spectrum antiparasitic drug, which is routinely administered to livestock throughout the world. Although it offers an efficient and economical method for treating and controlling parasitic diseases, concerns have been raised about its possible impact on biodiversity in farmland systems (Wall & Strong, 1987; Floate et al., 2005). In particular, the long-term effects on non-target dung fauna and pasture systems remain unclear (Lumaret & Errouissi, 2002; Suarez et al., 2003; Floate et al., 2005), especially in temperate climates (O'Hea et al., 2010).

After administration, the breakdown of ivermectin by metabolism is generally moderate, and between 62% and 98% of the ivermectin used in treatment may be excreted unaltered in the faeces (Floate et al., 2005; Kryger et al., 2005). While few studies have quantified ivermectin levels in faeces, it is evident that ivermectin does not rapidly degrade, and remains at concentrations considered harmful to coprophagous fauna for long periods. Suarez et al. (2003) detected residues of up to 109 μg kg−1 (dry weight) in cowpats after 180 days in an Argentinian field, and Sommer and Steffansen (1993) reported that 84% of the ivermectin initially excreted remained in cowpats after 45 days in a Danish pasture.

Residues of ivermectin are known to affect dung colonisation by Coleoptera and Diptera, but relatively few studies have investigated this effect (O'Hea et al., 2010), and research to date has produced conflicting results (Floate, 2007). It has been demonstrated that certain insects may avoid dung from treated cattle (Wall & Strong, 1987; Holter et al., 1993; Floate, 1998b, 2007; Suarez et al., 2003; Webb et al., 2010), whereas others may preferentially colonise it (Wardhaugh & Mahon, 1991; Holter et al., 1993; Lumaret et al., 1993; Floate, 1998b, 2007), both of which have implications for dung breakdown, insect survival, and long-term pasture health.

Ivermectin has been shown to have a significant effect on temperate dung beetles. O'Hea et al. (2010) found that ivermectin residues significantly slowed the development of Aphodius species, with ivermectin levels as low as 200 μg kg−1 (wet weight) reducing the percentage of A. ater developing beyond larvae instar III to just 15%. Ivermectin has also been shown to cause mortality of A. constans, with the LC50 for first instar larvae being determined at between 420 and 692 μg kg−1 (dry weight) by Lumaret et al. (2007), and between 880 and 980 μg kg−1 (dry weight) by Hempel et al. (2006).

Diptera of the Suborder Cyclorrhaphan are particularly sensitive to ivermectin, and concentrations as low as 1 μg kg−1 (wet weight) are toxic to common species such as the yellow dung fly (Scathophaga stercoraria) (Strong & James, 1993). West and Tracy (2009) reported a significant reduction in S. stercoraria pupation in cowpats containing ivermectin, with only 28% of flies pupating when ivermectin levels were 0.2 μg kg−1 (wet weight). The median effective concentration (EC50) for 50% egg-to-adult mortality for S. stercoraria was determined by Römbke et al. (2009) as 20.9 ± 19.1 μg kg−1 (wet weight).

Researchers have highlighted the need for studies into the effects of ivermectin under a wider variety of conditions (Suarez et al., 2003). Studies in the United Kingdom are particularly important, as there has been limited research in temperate climates, with the majority of recently published literature relating to tropical countries and tropical species, as noted by O'Hea et al. (2010) and Webb et al. (2010). There has also been a call for greater understanding of the effects that landscape features such as field size, boundary type, and sward height have on the persistence and impact of avermectins in the environment (Webb et al., 2007). Pastures are non-uniform environments, varying in terms of vegetation height and cover – factors that alter microclimate and insect activity, survival, and reproduction (Vessby, 2001; Hutton & Giller, 2003), and possibly the persistence and breakdown of ivermectin (Halley et al., 1989b). Despite this, no studies have been carried out to determine the effect of sward structure on ivermectin persistence or cowpat colonisation.

The overall objective of this study was to assess ivermectin persistence, and how it affects cowpat colonisation, in three different sward structures commonly found in and around temperate pasture ecosystems in the United Kingdom.

Method

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Study area

The experiment was carried out on a small mixed beef and dairy farm in Shustoke, east of Birmingham, England (SP 230901, 52o30′N, 01o39′W), between the 22nd April and 10th June 2005. The farm was selected as it was representative of a typical livestock farm which routinely administers ivermectin pour-on formulas for the treatment of internal and external parasites.

Livestock treatment and cowpat preparation

On the 22nd April 2005, 10 young beef calves (continental cross – Limousin with Friesian) aged between 12 and 24 months were treated with 500 μg kg−1 of body weight with an ivermectin pour-on formula (Noromectin, produced by Norbrook, UK, which contains ivermectin 0.5% w/v), while 10 separately housed calves remained untreated as the control group. Treatment occurred when local farmers were administering antiparasitic drugs to their cattle, to coincide with the time that cattle are turned out to grazing at the end of April or beginning of May (Webb et al., 2007). The calves' diet from early April was grass pasture.

Approximately 60 litres of dung was collected from each treatment group the day after treatment (day zero). The dung collected from each group was carried to the field site where it was homogenised by group, on a large plastic sheet, to minimise the variation that would otherwise occur between animals within each treatment. For each treatment group, the dung was then made into 60 experimental cowpats, each with a wet weight of 1 kg and diameter of 20 cm. A 20 g sample of untreated and treated dung was collected and stored at −20 °C for later analysis to determine the ivermectin level on day 0.

Experimental design

Three areas within a single pasture, bordered by hedges on all four sides, were selected to represent typical long sward, short sward, and bare ground areas commonly found in pastures. In each sward type, two replicate plots of 3 m by 7 m were marked out using string and pegs, thus giving a total of six plots.

Within each plot, 10 cowpats from untreated dung and 10 from treated dung (i.e. 20 cowpats in total) were spaced in an alternating sequence, 1 m apart, across three rows. This layout was used to intersperse treatments in space, as cowpat colonisation by various insects is not uniform, and because Barth (1993) recommends that cowpats of the same treatment should not be placed in groups, but rather varied to minimise effects of location.

The experimental cowpats were collected from the field, 1, 4, 10, 24, and 47 days after deposition day (day 0). These collection dates were chosen on the basis that more intensive sampling should be conducted during the early stages of the experiment because insect activity is greatest during this period (Skidmore, 1991). The experiment was terminated at day 47 because after 45 days in temperate pastures it is unlikely that coprophilous invertebrates will colonise any remaining dung (Skidmore, 1991).

On each collection date, two randomly selected cowpats from treated dung containing ivermectin and two from untreated dung (four pats in total) were removed from each replicate of each sward plot (2 replicates × 3 sward types = 6 plots) and hence 24 cowpats were collected on each visit. Approximately 20 g of dung was immediately removed from the centre of each cowpat, sealed in a small air tight polythene bag and stored at −20 °C to enable the later determination of drug residues. The remainder of each cowpat was transferred to the laboratory in a large polythene bag where it was stored at 5 °C overnight until analysed.

Invertebrates in the cowpats were hand sorted in a white tray and individuals were stored in a fridge until they could be counted. Sorting of invertebrates was restricted to beetles (order Coleoptera), flies (order Diptera), spiders (order Araneae), slugs (order Gastropoda), earwigs (order Dermaptera), millipedes (class Diplopoda), and centipedes (class Chilopoda). In the case of Coprophagous Coleoptera, only adults were recovered and these were retained for identification to species level. Coprophagous Diptera larvae were also abundant, but these could not be identified to species level, so were grouped prior to analysis.

High-performance liquid chromatography (HPLC) was used to determine ivermectin levels in the dung, based on the method developed by Payne et al. (1995) and Asbakk et al. (1999). Initial ivermectin levels were determined using dung collected on the day the experiment was set up (day zero), and mean levels at time points thereafter were calculated using the four cowpats retrieved from each treatment and sward structure on the subsequent collection days.

Several physical parameters were monitored in the field as they influence dung degradation and insect activity. On each collection day, sward height, and temperature and humidity 1 cm above the ground were measured at three randomly determined points in each sward structure plot to capture the microclimatic conditions at the cowpat.

Statistical analyses

Sward height, air temperature, and humidity measurements on each collection date were compared across sward structures using one-way anova followed by Tukey's multiple comparison test.

Ivermectin residue levels were calculated as concentrations per 10 g dry weight to remove the variability in the dung water content. Split plot analysis was carried out to determine the effect of sward type (main plots) and time (sub plots) on ivermectin levels.

The large number of zero values in the insect count data prevented a parametric assessment due to lack of normality in the data. Thus, to determine whether there was an attractive or repellent effect of ivermectin on each species of coprophagous Coleoptera, and on total Diptera recorded, we used a split plot analysis based on cowpats (sub plots) within sward type (main plots), but basing significance on the results of 1000 Monte Carlo simulations. Only the significance of ivermectin and of the ivermectin × sward type interaction is reported. Species with low numbers of individuals were not analysed.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Sward structure

The average sward height, air temperature, and humidity recorded in each sward structure, on each collection day, are presented in Table 1. As expected, sward height varied significantly between the three sward structures (< 0.01). Temperature also varied significantly between sward structures (< 0.01), with the long sward habitat being significantly warmer than the short sward and bare ground habitats. Humidity also varied significantly between sward structures (< 0.01), with the bare ground habitat being significantly less humid than the long and short sward habitat.

Table 1. Mean (and range) sward height, and temperature and humidity 1 cm above ground level, on each collection day (n = 6)
Sward structureDaySward height (cm)Temperature (oC)Humidity (%)
Long sward112.5 (10.0–14.0)13.4 (12.9–13.6)66.4 (66.1–66.6)
410.0 (7.0–12.0)11.4 (10.9–12.0)92.2 (88.9–95.2)
109.3 (4.0–12.0)19.1 (17.6–20.5)58.5 (49.0–65.0)
2412.8 (8.0–21.0)17.8 (17.2–18.2)60.4 (59.3–61.2)
4710.8 (8.0–15.0)11.4 (11.1–11.7)86.4 (85.8–86.2)
Short sward12.5 (2.0–3.0)12.4 (12.0–12.9)71.7 (71.4–72.0)
42.0 (0.0–3.2)11.4 (10.9–11.7)88.6 (87.9–88.9)
103.3 (2.5–4.2)16.1 (15.7–16.5)63.1 (55.0–64.9)
243.5 (2.8–4.0)18.5 (17.8–19.4)53.7 (52.9–54.9)
472.9 (2.0–4.0)11.8 (11.5–12.1)80.6 (79.2–81.8)
Bare ground1011.7 (11.4–12.0)72.2 (71.8–72.5)
4010.9 (10.6–11.1)85.0 (84.7–85.3)
10016.5 (15.9–17.5)61.3 (60.4–62.0)
24018.6 (18.4–18.7)52.6 (51.9–53.1)
47011.6 (11.5–11.7)74.5 (72.0–75.9)

Ivermectin residues

The ivermectin level in the faeces from treated cattle 1 day after treatment with Noromectin, averaged 21 899 μg kg−1 (dry weight) (Fig. 1). There was no significant difference between sward structures on ivermectin levels (F2,3 = 2.38; P > 0.05). Ivermectin levels reduced significantly through time (F4,36 = 16.73; P < 0.001), and there was no significant interaction with sward structure (F8,36 = 0.84; P > 0.05).

image

Figure 1. Mean ivermectin concentrations in cowpats (μg kg−1 dry weight) (n = 4).

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The control cowpats, collected from the untreated cattle, contained no ivermectin residues [0 μg kg−1 (dry weight)] throughout the trial.

Invertebrate presence

Non-dipteran invertebrates were found in higher numbers in treated cowpats at the majority of collection dates (Fig. 2), and Diptera larvae were found in greater numbers in untreated cowpats in all sward structures (Fig. 3).

image

Figure 2. Total number of non-dipteran invertebrates collected from untreated cowpats (white bars) and treated cowpats (black bars) in the three sward structures after 1, 4, 10, 24, and 47 days in the field.

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image

Figure 3. Total number of Diptera larvae collected from untreated cowpats (white bars) and treated cowpats (black bars) in the three sward structures after 1, 4, 10, 24, and 47 days in the field.

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Coprophagous invertebrates

The coprophagous coleopteran species collected from cowpats are presented in Table 2.

Table 2. Total coprophagous Coleoptera and diptera larvae recovered from cowpats from untreated (U) and treated (T) cattle in each sward structure (n = 20)
 Long swardShort swardBare ground P
UTEffectUTEffectUTEffectIvermectinIvermectin × Sward
  1. Arrows indicate whether ivermectin treatment increased or decreased insect abundance in each sward structure.

Hydrophilidae
Cercyon atomarius 08[UPWARDS ARROW]82[DOWNWARDS ARROW]80[DOWNWARDS ARROW]0.5230.008
Cercyon haemorrhoidalis 210[UPWARDS ARROW]23[UPWARDS ARROW]330.2070.275
Cercyon melanocephalus 10 10 01 NotTested
Cercyon pygmaeus 03 10 10 NotTested
Sphaeridium scarabaeoides 110[UPWARDS ARROW]96[DOWNWARDS ARROW]62[DOWNWARDS ARROW]0.8920.043
Scarabaeidae
Aphodius ater  1377[UPWARDS ARROW]460824[UPWARDS ARROW]388481[UPWARDS ARROW]0.2300.663
Aphodius erraticus 5114[UPWARDS ARROW]18150[UPWARDS ARROW]20231[UPWARDS ARROW]<0.0010.990
Aphodius fimetarius 05[UPWARDS ARROW]822[UPWARDS ARROW]1015[UPWARDS ARROW]0.1640.745
Aphodius fossor  10 02 00 NotTested
Aphodius prodromus 39311[UPWARDS ARROW]204556[UPWARDS ARROW]185209[UPWARDS ARROW]0.0640.513
Aphodius sphacelatus 03[UPWARDS ARROW]00 3547[UPWARDS ARROW]0.9731.000
Diptera larvae1860165[DOWNWARDS ARROW]120774[DOWNWARDS ARROW]33380[DOWNWARDS ARROW]<0.0010.865

A total of 11 coprophagous Coleoptera species were present in this study. All species found were in imago form, and no larvae were recovered from cowpats. With the exception of one species (Aphodius fossor), represented by a singleton in long swards, species of Scarabaeidae were present in consistently higher numbers in cowpats from ivermectin-treated cattle in all sward structures. This relationship was only significant for A. erraticus (< 0.001), but marginally significant (= 0.064) for A. prodromus.

Members of the Hydrophilidae family were generally present in higher numbers in treated cowpats in the long sward habitat, but tended to be found in higher numbers in untreated cowpats in the short sward and bare ground habitats. A significant interaction term for Cercyon atomarius (= 0.008) and Sphaeridium scarabaeoides (P = 0.043) confirms a preference for treated cowpats in the long sward habitat, but for untreated cowpats in the short sward and bare ground habitats.

There were significantly (< 0.001) more Diptera larvae in the untreated cowpats, across the three sward structures.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

The initial mean ivermectin concentration measured in faeces collected from treated cattle 1 day after treatment (day zero) was 21 899 μg kg−1 (dry weight). Similarly, high concentrations have been reported following treatment with comparable pour-on ivermectin formulas; Herd et al. (1996) detected a peak excretion of 18 500 μg kg−1 (dry weight) in dung collected from cattle 2 days after treatment. Once cowpats were placed in the field, the peak ivermectin residues observed at day 0 decreased through time, and followed a similar pattern of breakdown to that reported by Iglesias et al. (2006), with an initial rapid decrease in residues over the first 3 weeks, after which the concentration remained fairly constant.

Despite reductions in ivermectin concentrations, by the end of the 47-day trial, residues remained at relatively high concentrations in cowpats. This demonstrates that ivermectin can persist in temperate environments for more than 6 weeks, and is supported by similar research in other temperate environments, e.g. O'Hea et al. (2010) and Sommer and Steffansen (1993). Indeed Suarez et al. (2003) reported concentrations of up to 109 μg kg−1 (dry weight) after 180 days in a temperate Argentinian pasture.

The persistence of ivermectin implies that residues have the potential to affect the dung community for the entire period that cowpats are utilisable by dung fauna in temperate climates (Skidmore, 1991; Hempel et al., 2006). Suarez et al. (2003) also reached this conclusion, stating that drug residues remained at levels high enough to adversely affect dung-colonising fauna throughout their entire 180-day trial. If farmers also adhere to the treatment regime recommended by manufacturers, whereby ivermectin administration is carried out three times, at five weekly intervals, then pastures in the United Kingdom would probably contain relatively high levels of ivermectin residues throughout the entire grazing season, between April and September (Floate, 1998a).

Sward structure did not have a significant effect on the ivermectin levels in cowpats. This is somewhat surprising as the three sward structures differed significantly in terms of mean sward heights, which resulted in significantly higher temperatures in the long sward habitat, and significantly lower humidity in the bare ground habitat. These relatively small differences were obviously not sufficient to differentially affect ivermectin breakdown because higher temperatures are known to increase ivermectin breakdown rates (Halley et al., 1989a). It is anticipated that more extreme environments within grazing areas, for example those shaded by trees in wood pastures, may have a greater effect, as exposure to sunlight is one of the most important factors influencing the breakdown of ivermectin (Halley et al., 1989b).

Ivermectin residues had a clear effect on the presence of invertebrates in cowpats. Diptera larvae were consistently present in higher numbers in cowpats from untreated cattle, and non-dipteran invertebrates were generally present in higher numbers in cowpats from treated cattle. Similar findings have been reported in other studies (Lumaret et al., 1993; Floate, 1998b). In particular, Floate (2007) reported that dung containing chemically similar doramectin residues attracted coleopteran species 3, 7, and 14 days after treatment of cattle, and Wardhaugh and Mahon (1991) reported that the attractive effect of ivermectin continued to occur in faeces produced up to 25 days after treatment.

Diptera larvae were not identified beyond order, so individuals were grouped. This provides a crude indication of the impact of ivermectin on Diptera, as over 170 species of Diptera are associated with dung pats in Northern Europe (Hanski, 1991). Results should be interpreted with caution, as preferences and sensitivities of individual species could have been masked (Floate, 1998a). Nevertheless, there is strong reason to believe that at least some of the larvae recovered belonged to the yellow dung fly (S. stercoraria), as adults of this species were observed breeding in large numbers on pats in the field.

Diptera larvae were present in significantly higher numbers in untreated cowpats across sward structures. This finding is supported by many researchers (Lumaret et al., 1993; Suarez et al., 2003; Floate, 2007; Römbke et al., 2010), with some studies reporting that ivermectin residues eliminate certain dung-dwelling Diptera (Madsen et al., 1990; Strong & Wall, 1994). It is possible that the low number of Diptera larvae recovered from treated cowpats was a consequence of mortality, as Diptera larvae of the suborder Cyclorrhapha are highly sensitive to ivermectin residues (Lumaret & Errouissi, 2002; Floate et al., 2005), although species of the suborder Nematocera are largely unaffected (Floate et al., 2005). This has implications for the common species S. stercoraria which is reportedly unable to detect even lethally high levels of ivermectin, meaning that ovipositing females cannot avoid it (Römbke et al., 2009), although conversely, data in Floate (2007) indicates that S. stercoraria do avoid dung from cattle treated with ivermectin.

The EC50 of ivermectin for egg-to-adult mortality of S. stercoraria was determined as 20.9 ± 19.1 μg kg−1 (wet weight) (Römbke et al., 2009), and concentrations as low as 0.2 μg kg−1 (wet weight) have been found to reduce pupation to just 28% (West & Tracy, 2009). These effects occurred at ivermectin levels which were much lower than those detected at any time during this experiment, and this has significant implications for survival and cohort size, particularly because S. stercoraria colonise cowpats immediately at deposition and are therefore likely to be exposed to very high levels of ivermectin (Skidmore, 1991).

The 11 species of coprophagous Coleoptera present in this study are typical of those found in temperate environments, and North European dung beetle assemblages, which are dominated by Aphodius species (Hanski, 1991). The six species of Aphodius, four species of Cercyon, and one species of Sphaeridium found in this study are common and generally abundant in England (Skidmore, 1991). Coprophagous Coleoptera were present in higher numbers in treated cowpats in the majority of cases, based on cumulative data over the entire 47-day trial. It is, however, worth noting that the majority of the individuals were collected early in the experiment, on days 4 and 10, and this reflects cowpat succession in temperate environments, as described by Skidmore (1991).

All species of coprophagus Coleoptera found were in imago form, and no larvae were present in any of the cowpats. Because the development of beetle eggs may take weeks to months, the presence of Aphodius larvae would be expected between the first week and 4 months after cowpat deposition (Putman, 1983). The absence of larvae on all collection dates suggests that no beetles were breeding in cowpats during this study, although it is possible that larvae were subject to predation, or developed and pupated in the soil beneath the cowpat between collection dates.

All species of Scarabaeidae, except one (which was represented by a singleton in long swards), were present in consistently higher numbers in cowpats from treated cattle in all sward structures. Of the species sufficiently abundant for data analysis, this relationship was only significant in one case (A. erraticus) and marginally significant in one other (A. prodromus). Other studies have also reported increased numbers of Coleoptera in cowpats from treated cattle (Wardhaugh & Mahon, 1991; Lumaret et al., 1993), and Floate (2007) reported that ivermectin had an attractive effect on some Aphodius species, including A. erraticus, A. fimetarius, and A. fossor, which were recorded during this study.

Despite these findings, it has also been demonstrated that certain insects may avoid dung from treated cattle (Wall & Strong, 1987; Holter et al., 1993; Floate, 1998b, 2007; Suarez et al., 2003; Webb et al., 2010). Interestingly, Floate (1998b) found A. prodromus and A. fimetarius to demonstrate the opposite preference in Canada following a comparable pour-on treatment, and similarly, in Denmark, Holter et al. (1993) recovered significantly more A. ater and A. prodromus from dung produced by untreated cattle compared with the dung from those following an ivermectin injection.

Although the adults of many Hydrophilidae species were present in greater numbers in untreated cowpats, Cercyon atomarius, C. haemorrhoidalis, and Sphaeridium scarabaeoides were found in higher numbers in treated cowpats in the long sward habitat. This contradicts published findings, which have reported ivermectin to cause significant reductions in the adult populations of Hydrophilidae (Holter et al., 1993; Floate, 1998b), and the complete absence of their larvae (Strong et al., 1996). While C. atomarius and S. scarabaeoides showed a preference for the treated dung in the long sward habitat, conversely, they also exhibited a preference for the untreated dung in the short sward and bare ground habitats.

The reason for the attractive effect of ivermectin is thought to be a result of the presence of volatile metabolites of the avermectin administered, or possibly a result of changes in the gut flora of the cattle as a consequence of treatment (Wardhaugh & Mahon, 1991; Lumaret et al., 1993). This is supported by Floate (2007), who suggests that it is unlikely that insects respond directly to the presence of parent compounds which bond tightly with particulate matter within the dung. The larger numbers of Scarabaeidae and Hydrophilidae recovered from the treated cowpats in the long sward habitat suggest that this sward structure was accentuating the attractive effect of ivermectin.

The influence of sward structure means that ivermectin could have a greater impact on coprophagous Coleoptera in long sward structures, such as the areas typically found in field margins and meadows. Further studies are needed to determine whether ivermectin consistently increases the attractiveness of cowpats in these sward structures. If ivermectin is found to increase the attractiveness of cowpats in meadows, then the use of ivermectin may need to be restricted or prohibited in these sward structures in the United Kingdom, as they tend to be small and fragmented – characteristics that increase the risk of species extinctions (JNCC, 2006).

The increased attraction to cowpats containing ivermectin has significant implications for the survival of coprophagous Coleoptera because drug residues have been shown to inhibit the development of Aphodius larvae (Hempel et al., 2006; O'Hea et al., 2010), reduce adult emergence (Floate, 1998a), and cause mortality (Hempel et al., 2006). The ivermectin levels recorded in this study, even at the end of the 47-day trial, remained higher than the LC50 determined for A. constans, which was reported as 880 to 980 μg kg−1 (dry weight) by Hempel et al. (2006), and 470 to 692 μg kg−1 (dry weight) by Lumaret et al. (2007). If other species have similar LC50s, then this has severe implications for Aphodius populations. This is supported by O'Hea et al. (2010) who concluded that ivermectin caused significant reductions in cohort size which were sufficient to affect the next generation of beetles.

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

The impact of ivermectin on farmland biodiversity is currently of real concern to policy makers in the United Kingdom, to the extent that the question ‘What are the impacts on biodiversity of prophylactic treatment of farm livestock with antibiotics, anti-fungal and anti-helmintic compounds?’ was identified as one of 100 questions of relevance following a workshop of policy makers, advisers, lobbyists, and members of the research community (Sutherland et al., 2006).

These findings help further our understanding of how ivermectin impacts on invertebrates in an in situ farm environment and thus improve the knowledge base from which to develop grounded policy recommendations for conserving on-farm biodiversity in the United Kingdom. Of particular note from this research is the fact that ivermectin was able to persist at levels well above those reported toxic to dung fauna, even after 47 days in the field. This suggests that pastures will contain ivermectin at biologically significant levels for the entire grazing season, especially if the treatment regimes recommended by manufacturers are adhered to. Practical options for the reduction in ivermectin use include the application of targeted treatments in preference to broad-spectrum chemicals, or the selection of less toxic macrocyclic lactones such as moxidectin (Floate, 2006; Suarez et al., 2009).

Also of importance from this research is the finding that ivermectin residues can significantly alter cowpat colonisation. Coprophagous Coleoptera were consistently present in higher numbers in cowpats from treated cattle and in the case of Aphodius erraticus this attraction was significant. This means that species such as A. erraticus could be continually exposed to ivermectin as a result of their cowpat selection, and this has implications for beetle presence and cohort size. Moreover, these impacts will be compounded if some dung beetle species are preferentially attracted to farms using ivermectin. This has potential implications for current UK government schemes such as Environmental Stewardship (ES), which incentivise the conservation of on-farm invertebrate diversity, particularly where ES farms are located in close proximity to conventional farms. Although it has been demonstrated that Aphodius species can distinguish between dung from treated and untreated cattle separated by distances of 3–5 m (Floate, 1998b, 2007), further research is required to determine the distances at which Aphodius species can detect ivermectin, and the spatial scales at which their resource selection occurs.

Although ivermectins were found to have a significant impact on Diptera abundance in treated cowpats, this is less likely to have short-term conservation implications for UK farmland due to the continued availability of ivermectin-free cattle dung in most areas. For example, it is likely that some ivermectin-free dung will be present within the local landscape, as famers often graze untreated milking cows with the young treated cattle (Webb et al., 2010).

Above all, the current research highlights the potential for on-farm field experiments to improve understanding of the effects of ivermectin compounds on invertebrates, and the need for further field investigations in temperate environments to determine the long-term impacts on non-target dung fauna.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

We thank Dr Tim Sparks for assistance with statistical analysis, and for comments on an earlier draft. We also thank two anonymous reviewers for their advice and guidance.

References

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  3. Introduction
  4. Method
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
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