Environ. Sci. Technol. 2007, 41, 2630-2635
A Screening Level Index for Assessing the Impacts of Veterinary Medicines on Dung Flies A L I S T A I R B . A . B O X A L L , * ,†,‡ TOM N. SHERRATT,§ VICTORIA PUDNER,† AND LOUISE J. POPE† Environment Department, University of York, Heslington, York, UK, YO10 5DD, Central Science Laboratory, Sand Hutton, York, UK, YO41 1LZ, and Carleton University, Ottawa, Canada, K1S 5B6
Veterinary parasiticides are administered to livestock to control a wide range of parasites. Following excretion, these substances may persist in the environment and impact nontarget organisms. This paper describes a simple screeningbased index for predicting the effects of veterinary parasiticides on dung flies using data on parasiticide toxicity, animal husbandry, and parasiticide use. The utility of the index has been assessed, at the farm scale for a number of dipteran species, using data from a survey of farms in England and insect ecology and ecotoxicological data. The results indicate that a large proportion (35%) of parasiticide treatments in England will have no impact on dung fly populations. In terms of individual parasiticides, the macrocyclic lactone doramectin was predicted to have the highest impact on English dipteran populations with a maximum reduction in the population of horn flies on one farm of 28%. Ivermectin pour-on had the next highest impact (6.8%), followed by eprinomectin (6.4%), and ivermectin injection (4.1%). Due to a lack of data, it was not possible to assess the effects of the benzimidazole parasiticides (oxfendazole and fenbendazole), morantel and permethrin. The approach is simple, nondata-intensive and has the potential to be a valuable tool for use in environmental risk assessment or management of new and existing veterinary parasiticides.
Introduction There is increasing concern over the potential impacts of veterinary pharmaceuticals on the environment (1, 2). Veterinary parasiticides are administered to livestock to control a wide range of parasites including gastrointestinal worms, liver fluke, lung worm, lice, blow-flies, keds, ticks, and scab mite (3). The compounds may be applied as oral drenches, topically (e.g., in dips or in pour-ons), via intraruminal boluses, or in injectable formulations. For compounds administered orally or by injection, after administration, the substances may be partially or totally metabolized in the animal before being released, along with metabolites, in the faeces or urine (4). For substances applied topically, the * Corresponding author phone: +44 (0)1904 462142; fax +44 (0)1904 462438; e-mail:
[email protected]. † University of York. ‡ Central Science Laboratory. § Carleton University. 2630
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substance may be absorbed and subsequently metabolized or there may be the potential for the active substances to be “washed-off” onto the soil or dung or into surface waters. Once in the dung, the substances may persist for a period of time, and consequently, dung-inhabiting invertebrates may be exposed to them (5, 6). Such exposures may lead to toxic effects. As many of the dung-associated invertebrates are important in the diets of various insectivorous vertebrates, including common farmland birds and rarer species such as horseshoe bats, the substances may also cause effects at higher trophic levels (7). The risks of selected parasiticides associated with dung (e.g., ivermectin) to selected invertebrate groups have been well-assessed in laboratory and single-pasture studies (e.g., refs 5, 8-11). However, only a few studies have addressed the possible local or wider population consequences of livestock parasiticides for dung-associated invertebrates or for vertebrates preying on them (e.g., refs 12, 13). Moreover, there is limited information on the risks to certain groups (e.g., aquatic invertebrates) and on certain individual classes of parasiticide. One approach to assess the local or wider population consequences of the use of parasiticides is to use population modeling. A number of models have been proposed (e.g., refs 14-17). All of these models have investigated the impacts of treatment at a single-farm scale. The majority of the models developed to date are detailed, and hence, they require a large number of input data that, in many cases, is not available. A more simplistic screening level index might, therefore, be useful that provides a “worst case” assessment of effects on insect populations based on a limited dataset. Such an index might assist decision makers in identifying chemicals or scenarios of concern that warrant further investigation or higher level modeling. In this paper, we describe a simple screening-level index for assessing the risks of parasiticides to dung fly populations. The application of the index is illustrated using data for the English pasture situation.
Materials and Methods Index Description. The screening index uses a simple stepwise approach to predict the potential effect of parasiticides on the population size of dung insects over a year, this is described below. First, the time over which the life stages of interest are likely to occur in dung is determined. For dung flies, laboratory ecotoxicity tests typically involve the addition of eggs to dung and the endpoint assessed is adult emergence so the life stages of interest are, therefore, those occurring from egg-to-adult. The period(s) over which dung containing residues of parasiticide is excreted is then determined (this will be dependent on the rate at which the compound and its active metabolites are excreted). The proportion of time (q) when the life stage(s) come into contact with dung containing residues is then determined using eq 1.
q ) [(t1 + t2 +... tn)]/T
(1)
Where T is the time over which the life stages of interest are present in dung; t1, t2, to tn are the times (maximum n) over which dung excreted onto the field contains residue of a parasiticide. If (i) toxicity does not change over the period-of-timedung is attractive to the colonists, (ii) the life stages of interest do not move between pats, (iii) the organism exhibits relatively quick development, so that dung colonized in 10.1021/es0618705 CCC: $37.00
2007 American Chemical Society Published on Web 02/28/2007
FIGURE 1. Frequency of use of parasiticide active ingredients on cattle farms in the United Kingdom. periods t1, t2, t3, etc. are capable of supporting the life stage, and (iv) the density of the sensitive life stage is evenly distributed over the period it is available, then a crude estimate of the impact of the parasiticide (expressed as the percentage reduction in population size per annum) can be derived using eq 2.
impact ) 100 p q v
(2)
Where p is the maximum proportion of cattle treated at any one time, and v is the proportion of the life stage killed from laboratory bioassay results. Where bioassay data are available on the toxicity of dung over time, a time weighted average value can be used for v. For flies, assumptions i-iii listed above are reasonable as insects will typically colonise fresh dung that will support complete development and the life stages of interest (eggto-adult) will not move between pats. Application of Modeling Approach. To explore the utility of the screening-level index, it was applied to explore the potential impacts of parasiticides, in use in England, on the population size of three species of pest flies; i.e., horn fly, stable fly, and house fly. Data were obtained or generated on the ecology and ecotoxicology of dung fauna and on parasiticide usage characteristics. Review of Dung Organism Ecology and Ecotoxicology. In order to assess the effects of the substances on dung productivity, it is necessary to have a detailed understanding of the biology of the dung organisms. Information pertinent to the model (e.g., insect life history and reported susceptibility to faecal residues of various parasiticides) was obtained from the published literature. Survey of Parasiticide Use in the United Kingdom. A survey was sent out to an equal number of beef and dairy farms in each county of England. Contact details were obtained from online telephone directories. The survey included questions on the type and formulation of the parasiticide, administration method, number of the herd treated, timing of treatment, whether treated and untreated individuals were kept together, the length of time treated animals were kept inside after treatment, and area of pasture on which the treated animals were kept. A number of further questions were asked to assist other studies in the same field. Telephone interviews were conducted with a sample of farmers to ensure the questions were answerable and made sense. The survey was sent with an explanatory letter and a pre-paid return envelope. Responses from the survey were analyzed to identify the frequency of parasiticide use (by
active ingredient), method of application, frequency, timing of application and the proportion of a herd treated. In total, surveys were sent to 300 farmers. Impact Assessment. The effect of parasiticide use on each of the three species of pest flies was assessed using data provided by the respondents. This meant that potentially there was more than one model output per farm as frequently more than one parasiticide was used on each farm. Effects on populations were estimated at the farm scale using data on the proportion of treated animals calculated from the survey responses for the whole farm. Time-weighted average toxicity values were used in the modeling and these were derived using a combination of laboratory bioassay data and information on withholding periodssit was assumed that animals will excrete residues of a parasiticide for the entire length of the withholding period. Withholding periods were taken from the NOAH compendium (18), in instances where more than one withdrawal period was available for a particular parasiticide and administration route, the longest was selected. The results from the modeling were then used to develop impact distributions for cattle farms in England.
Results and Discussion Seventy farmers responded to the survey accounting for approximately 0.1% of cattle holdings in England. Sixty of these were suitable for analysis, the remaining ten had critical information missing. Included in the analysis were 32 beef farms, 18 dairy farms, and 10 mixed beef and dairy farms. Altogether over all farms, there were 76 parasiticide records. The survey showed that parasiticide products containing ivermectin were the most frequently used followed by products containing oxfendazole, eprinomectin, doramectin, and fenbendazole (Figure 1). Morantel, moxidectin, and permethrin were only used on 1-2 dairy farms. As well as being the most widely used parasiticide, ivermectin is also the most studied active ingredient in terms of environmental impacts and the risks are well-known. In terms of method of application, pour-on formulations were the most frequently used followed by bolus, drench, and injection administrations. The mode of application can have a significant effect in the impact of a medicine. For example, long-term lethal effects on dung fauna have previously been noted with bolus use, due to the continuous release of the drug for prolonged periods of time (17, 19). The proportion of cattle treated on the farms ranged from 8-100% although it was rare that an entire herd was treated at one time. The majority of farmers (75%) also separated VOL. 41, NO. 7, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 2. Temporal distribution of larval activity, periods of animal housing and medicine use on English cattle farms.
TABLE 1. Drug Withholding Periods and Measured Percentage Survival and Time-weighted Average Survival of Horn Fly, House Fly and Stable Fly in Dung of Cattle before Treatment and up to Four Weeks after Treatmenta withholding pretreatment week 1 survival week 2 survival week 4 survival time weighted period (d) fly species survival (%) (% of control) (% of control) (% of control) average survival (%) doramectin pour-on
42
eprinomectin pour-on
15
ivermectin pour-on
28
ivermectin injection moxidectin pour on
35 14
a
horn fly house fly stable fly horn fly house fly stable fly horn fly house fly stable fly horn fly horn fly house fly stable fly
42.5 85.2 63.5 70 80.4 72.4 7.1 99 58.3 20-41 49.2 88 75.2
0 0.23 0 0 16.9 31.8 0 4 41.2 0 74 86.8 98.4
0 31 15.3 0 96 84.1 0 81.4 137 0 101 98.2 98.9
0 81.9 68.0 33 103 78.7 11.3 100 48.7 139 57.7 91.1 71.9
0 65 50.4 8.3 78 70 2.8 66.7 91 55.6 87.5 92.5 98.7
Data from refs 5, 18, and 23.
treated and untreated cattle when they were released to pasture. Therefore, while single fields could be affected significantly by the drug residues, the impact of a parasiticide on insect populations at the farm scale is likely to be lower due to a dilution effect of the untreated dung (6). The majority of medicines were administered during the spring and summer months (Figure 2). A large body of data is available on the ecology of dung and dung organisms (20, 21). Horn flies (Haemotobia irritans) deposit their eggs almost exclusively in fresh cow dung, normally within 10 min of dropping. The eggs hatch in 18 h to the first stage larva or maggot. The maggot feeds in the dung developing through three instars in 3-5 days. Pupation normally requires 3-5 days. When adults emerge form the pupal case, it takes 3 days for the complete maturation of the reproductive organs for egg production. The total life cycle from egg to egg-laying adult takes from 10 to 14 days. Female flies can lay 14-17 eggs at one time and up to 200 eggs during their lifetime. Adult Horn flies rarely leave the host on which they feed except to deposit the eggs on dung. Most of the adult life is spent on the host or migrating to new animals. Stable flies (Stomoxys calcitrans) lay their eggs in a variety of decaying animal and plant waste, but are rarely found in 2632
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fresh dung. Fly larvae (three larval stages) develop in excrement mixed with straw, soil, silage, or grain, but are also found in wet straw, hay, grass clippings, post-harvest refuse, and poorly managed compost piles. Larval development requires 11-21 days under warm, favorable conditions to 63 days under less favorable conditions. Mature larvae then crawl to drier areas to pupate. The pupal period varies from 6 to 26 days depending on temperature. The entire life cycle from egg to adult is generally completed in 3 to 6 weeks. House fly (Musca domesticus) females lay their eggs in moist decaying organic material. Eggs hatch within 40 h, depending on temperature. Larvae feed on yeast, bacteria, and decomposition products within their developmental site. Larval development through three stages takes from 3 to 8 days. Larvae crawl to drier areas to pupate when feeding is completed. The pupal stage lasts from 3 to 10 days, again depending primarily on temperature. Adults emerge and begin feeding within 24 h. Males are ready to mate shortly after emergence and females by the second or third day. The entire life cycle from egg to adult can be completed in 10 to 14 days during warm weather. It is generally recognized that the larval life stage is the most sensitive life stage to parasitcides. In the UK, horn fly
FIGURE 3. Frequency distribution of impacts of (a) doramectin pour-on (b) ivermectin pour-on (c) eprinomectin pour-on on Horn fly (Haematobia irritans), stable fly (Stomoxys calcitrans), and house fly (Musca domestica) larval populations on cattle farms in England. larvae are active from March to September, stable fly larvae are active from May to October, and House fly larvae are active from April to September (Figure 2). The periods of larval activity for these fly species, therefore, coincide with the times when selected parasiticides are being used and excreted to the pasture environment (Figure 2). However, comparison of information on usage and ecological data indicated that 35% of all treatments would have no impact on dung fly populations size, due to either treatments taking place during winter housing or due to the fact cattle were
kept in after treatment for long enough that all of the drug would have been excreted. Keeping livestock housed after parasiticide treatment has been one method suggested to minimize the nontarget impacts (22). Appropriate toxicity data for deriving the index were available for ivermectin, doramectin, and eprinomectin to three pest fly species: horn flies, stable flies, and house flies (5, 23; Table 1). In general, the rank order in terms of effect on larval mortality in the laboratory was doramectin pouron > ivermectin pour-on > eprinomectin pour-on > iverVOL. 41, NO. 7, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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mectin injection > moxidectin. The horn flies were the most sensitive species to all of parasiticides where data were available (Table 1). The simple index was, therefore, calculated to assess the effects of ivermectin-, doramectin-, eprinomectin-, and moxidectin-based treatments on the population size of dung fly species over a 1-year period. Input data and predicted impacts for individual farms are provided in the Supporting Information. Due to a lack of suitable toxicity data, it was not possible to utilize the assessment index for any of the farms using medicines containing the active ingredients oxfendazole, permethrin, fenbendazole, and morantel. The results demonstrated that doramectin pour-on had the highest predicted maximum effect on the population size of all three species for which data were held (maximum reduction in population size of 28% on horn fly; mean reduction of 2.8, 6.9, and 3.2% for house, horn, and stable flies, respectively), ahead of ivermectin pour-on (maximum reduction in population size 6.8% on horn fly; mean reduction of 0.7, 1.7, and 0.2% for house, horn, and stable flies, respectively), ahead of eprinomectin pour-on (maximum reduction in population size 6.4% on horn fly; mean reduction of 1.3, 1.5, and 1.4% for house, horn and stable flies, respectively)) (Figure 3a, b, and c) and ivermectin injection (maximum population size reduction 4.1%, mean population size reduction on horn fly of 1.37%). Only one farm used moxidectin and this farm housed animals during and after treatment so no effect on population size was predicted. Additionally, no impact was predicted for eprinomectin and doramectin for 50% of the farms represented (Figure 3a and b). No impact of ivermectin pour on and ivermectin injection was predicted on 53 and 67% of the farms represented, respectively. Doramectin is more toxic in laboratory dung organism assays than ivermectin and eprinomectin (3, 23) and also has a longer withholding period so, assuming the withdrawal period provides an indication of excretion rate from the animal, the length of time drug residues are expected to remain in the dung is longer for doramectin. Doramectin has been found to be metabolized less than the other macocyclic lactones, so more of the pure form is excreted for longer (3). It should be noted here that, despite this high impact, doramectin pour-on only accounted for 10.5% of medicine use records in the survey results and so may not be a major issue nationally. The results were generally similar to those of Sherratt et al. (15). Their simulation model rarely predicted greater than 25% mortality when considering the effect of macrocyclic lactones on dung invertebrate populations. In terms of effects on population size, the simple index used in this study may well over-estimate impacts. For example, it was assumed that all cows in the herd produced the same amount of dung. This is unlikely as calves produce less dung and are also generally the most treated of the herd (24). The model also assumed that the toxicity of dung will remain constant during the time over which the dung is attractive to insect colonists. For many veterinary medicines this will not be the case as concentrations in dung in the field will reduce as a result of biotic and abiotic degradation processes. Differences in food source may also be important. For example, the excretion of ivermectin varies depending on what the cattle have been fed on, with five times higher levels of ivermectin excreted by grain fed cattle in comparison to pasture fed cattle (25). The basic index could, however, be easily refined to reflect changes in the age of treated animals, dung production and drug persistence. The use of frequency distribution instead of point estimates as inputs could also be considered. The index also only considers lethal effects and did not consider other potential non-lethal effects. Differences in sensitivity of different sub-orders of diptera and coleoptera have been reported (3). Moreover, a range of non-lethal effects 2634
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of parasitcides on dung invertebrates have been observed following parasiticide exposure including reduced fecundity, larval stages remaining as permanent larvae, and morphological abnormalities (11, 26). These non-lethal effects are all important factors that may have the potential to further reduce future dung fly populations (27, 28). The complex food-web associated with the cow-dung community (3) was also not considered. Dung inveretebrates are an important food source for predators (e.g., ref 29). A predaceous species may suffer if there was not adequate food to sustain it, and the drug residues could potentially reduce the number of that species’ prey. Finally, while the index allows for repeated generations, it does not consider density dependent effectss a more sophisticated model would be required for this. Despite these limitations, we believe that the simple index provides a useful tool for predicting the relative impacts of different parasiticide substances and parasite management regimes on pasture invertebrate populations over large scales and long time periods. Compared to existing modeling approaches, which are detailed and require a large number of input data, the index is simple, transparent, and non-data intensive. In the current study, we have used real world usage data to support it. We therefore believe it is a useful tool that could be readily used by decision makers to extrapolate from simple laboratory studies (e.g., those being developed by the SETAC DOTTS group (30)) to effects on the wider population. While the application of the index has been illustrated for only three fly species, if data were available on the effects and ecology of other species (e.g., rare flies and beetles), it would be simple to apply the model to also predict impacts on these. We would, however, advocate the use of largescale multidisciplinary studies, alongside model development studies of this type, to develop a better understanding of the chronic effects of parasiticides on pasture ecology and to determine how model outputs relate to these chronic impacts. The study supports the conclusions of previous work (e.g., ref 31) and demonstrates that the impact of a parasiticide is not only determined by the toxicity of the drug but by a combination of drug usage pattern, animal husbandy characteristics, and dung insect ecology. It is essential that all of these factors are considered in the risk assessment process, and the only feasible way of investigating all of the possible treatment regimes and timing and ecological information is with the use of an index or a model.
Acknowledgments This work was partly funded by English Nature and the European Commission Framework Programme VI project ERAPHARM (contract no. 511135). We thank Dr Alastair Burn (Natural England) for his input to the project.
Supporting Information Available Input data and predicted impacts for individual farms. This material is available free of charge via the Internet at http:// pubs.acs.org.
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(18) National Office of Animal Health. NOAH Compendium of Animal Medicines; http://www.noahcompendium.co.uk/compendium/ overview/. Date accessed: 1 March 2006. (19) Errouissi, F.; Alvinerie, M.; Galtier, P.; Kerbouef, D.; Lumaret, J. P. The negative effects of residues of ivermectin in cattle dung using a sustained-release bolus on Aphodius constans (Duft)(Coleoptera: Aphodiidae). Vet. Res. 2001, 32(5), 421-427. (20) Cooper, C.; Sherratt, T.; Boxall, A. Modelling the impact of residues of ectoparasiticides and endoparasiticides in livestock dung on populations of dung flora and fauna: Phase 1; Report to English Nature: Peterborough, England, 2002. (21) Skidmore, P. Insects of the British Cow-Dung Community; Field Studies Council: Shewsbury, England, 1991. (22) Lumaret, J.; Errouissi, F.; Galtier, P.; Alvinerie, M. Pour-on formulation of eprinomectin for cattle: fecal elimination profile and effects on the development of the dung-inhabiting diptera Neomycia cornicina (L.) (Muscidae). Environ. Toxicol. Chem. 2005, 24 (2), 797-801. (23) Floate, K. D.; Spooner, R. W.; Colwell, D. D. Larvicidal activity of endectocides against pest flies in the dung of treated cattle. Med. Vet. Entomol. 2001, 15, 117-120. (24) Wratten, S. D.; Forbes, A. B. Environmental assessment of veterinary avermectins in temperate pastoral ecosystems. Annu. Appl. Biol. 1996, 128, 329-348. (25) Cook, D. F.; Dadour, I. R.; Ali, D. N. Effect of diet on excretion profile of ivermectin in cattle faeces. Int. J. Parasitol. 1996, 26 (3), 291-295. (26) Strong, L. Avermectins: a review of their impact on insects of cattle dung. Bull. Entomol. Res. 1992, 82, 265-274. (27) Strong, L. Overview: the impact of avermectins on pastureland ecology. Vet. Parasitol. 1993, 48, 3-17. (28) Lumaret, J.; Errouissi, F. Use of anthelmintics in herbivores and evaluation of risks for the non target fauna of pastures. Vet. Res. 2002, 33, 547-562. (29) McAney, C. M.; Fairley, J. S. Analysis of the diet of the lesser Horseshoe bat Rhinolophus hipposideros in the west of Ireland. J. Zool. 1989, 217, 491-498. (30) SETAC Professional Interest Groups: Dung Organisms Toxicity Testing. http://www.setc.org/htdocs/who_intgrp_dotts.html. Date accessed: 13 April 2006. (31) Forbes, A. B. Review of regional and temporal use of avermectins in cattle and horses worldwide. Vet. Parasitol. 1993, 48 (1-4), 19-28.
Received for review August 4, 2006. Revised manuscript received January 13, 2007. Accepted January 25, 2007. ES0618705
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