Les endectocides, ou lactones macrocycliques, sont des parasiticides vétérinaires utilisés pour enrayer les nématodes et arthropodes affectant le bétail. Les bovins traités avec ces produits excrètent dans leurs fèces des résidus qui sont toxiques pour les insectes retrouvés dans les bouses, incluant les espèces qui accélèrent la dégradation des bouses. Des inquiétudes ont été soulevées quant au fait que les endectocides puissent réduire la diversité des insectes et causer une accumulation de bouses non dégradées dans les pâturages. Cet article résume les résultats d’études effectuées pour évaluer les effets non ciblés de l’utilisation des endectocides au Canada. Les résidus diminuent l’activité des insectes dans les bouses des bovins traités pendant des semaines à des mois suite à leur application. La durée de l’effet est influencée par plusieurs facteurs, incluant les espèces d’insecte et le produit. À titre d’exemple pour la toxicité : doramectin > ivermectin ≈ eprinomectin >> moxidectin. La réduction de l’activité des insectes peut retarder la dégradation des bouses. À l’intérieur du cadre des conditions générales et des pratiques de régie, il est peu probable que l’utilisation des endectocides au Canada représente une menace significative généralisée pour l’environnement. Néanmoins, les effets non ciblés peuvent être une préoccupation dans les opérations individuelles vache-veau, particulièrement pour ceux qui traitent les animaux au printemps. Cette synthèse sur l’évaluation des effets non ciblés de l’utilisation des endectocides au Canada met en évidence l’importance de présenter les trouvailles à l’intérieur d’un contexte approprié.

Endectocides are excreted primarily in the feces of the treated animal. Hence, application to reduce numbers of internal and external parasites of livestock can also reduce numbers of insects in their dung. Reduced numbers of several species of pest flies have been reported in dung of livestock treated with various endectocides and can be viewed as an additional benefit of application. However, only a small percentage of the insect species associated with cattle dung in North America are pests, albeit some are of significant importance; for example, horn fly (Haematobia irritans [L.]) and face fly (Musca autumnalis De Geer [Diptera: Muscidae]).

The potential for endectocide residues to adversely affect nonpest species in dung has raised several concerns. Residues may be toxic to dung-dwelling insects, including species of threatened or endangered status. No such species are listed in Canada, but several rare species of dung-breeding insects have been reported for Britain (1). Reductions in the feeding and tunneling activities of dung-dwelling insects may delay dung degradation. Undegraded dung pats provide sites for pest flies to complete development, harbor nematodes parasitic in livestock, reduce available grazing area, and represent a loss of soil nitrogen in pastures (2). Reduced numbers of dung-breeding insect species can also affect other aspects of the pasture ecosystem; for instance, coprophilous insects pollinate plants and provide food for vertebrates.

Numerous studies have assessed these concerns, with variable results (3). Fecal residues typically are toxic to flies (Diptera) in the suborder Cyclorrhapha but innocuous to flies in the suborder Nematocera. Activity of beetles (Coleoptera) may be unaffected in dung of treated cattle or be suppressed in fresh dung of cattle treated weeks or even months previously. Dung of treated animals may degrade in a similar fashion, degrade more slowly, or degrade more quickly than dung of untreated animals.

The interpretation of results from these studies has occasionally been ambiguous and subject to rancorous debate. The authors of a study in Britain concluded that increased use of ivermectin by the livestock industry was likely to pose a serious threat to at least some dung-breeding species of insects and could increase the amount of pasture fouled by cattle dung (4). Scientists representing the manufacturer of ivermectin disputed these concerns, partially because they were based on use of an experimental bolus formulation of ivermectin (5,6). The formulation was subsequently registered in Britain, in 1992 (7), but is no longer marketed. A 2nd British study failed to find any effect on dung decomposition of ivermectin applied to cattle either as an injectable or a bolus formulation, which suggests that insects either had little role in dung decomposition or were relatively unaffected by fecal residues (8). These findings were criticized on several grounds, including the absence of data on insect abundance (9,10). Subsequent reviews concluded that use of avermectins would have little impact on nontarget populations of dung-breeding insects or on rates of dung degradation (11,12), although there were dissenting views (13–15). Herd (13) stated the following: “None of the published studies performed or sponsored by industry have concluded that drug residues exert a significant effect on the rate of dung degradation in temperate regions. By contrast, independent studies in Denmark, the UK, and the USA arrived at the opposite conclusion.”

Debate on the nontarget effects of endectocide use is considered by this author to have had at least 2 beneficial outcomes. First, it has spurred efforts to harmonize guidelines to assess the environmental risks associated with use of veterinary products. As part of this initiative, representatives from industry, regulatory agencies, and research institutions met in 2001 to form the group DOTTS (Dung Organism Toxicity Testing Standardisation). This official affiliate of the European Branch of the Society for Environmental Toxicology and Chemistry is developing standard protocols to assess the toxicity of veterinary parasiticides to coprophilous flies and dung-breeding beetles (3). Second, the debate has illustrated the importance of viewing results within an appropriate context. The nontarget effects of endectocide use are affected by formulation and dose, route and frequency of administration, and regional and seasonal differences in climate and dung fauna. Hence, conclusions derived from studies in a single region may be inappropriate elsewhere without consideration of regional differences.

Only recently have the nontarget effects of endectocides been studied in Canada (16–23). The absence of such previous studies reflects classification of endectocides for use in animals as “veterinary drugs,” for which environmental assessments are not needed for Canadian registration. Hence, there is no requirement for manufacturers to test for nontarget effects of endectocides in fecal residues in pastures. However, registration of new products, coupled with growing awareness of potential nontarget effects reported in other countries, prompted research in the mid-1990s to assess the nontarget effects of endectocide use in Canada. The findings and the identification of confounding factors are predicted to have heightened significance with ongoing efforts to develop and adopt international standards for the registration of veterinary products.

This article reviews the nontarget effects of endectocide application in cattle on coprophagous insects and on dung degradation in Canada. Within this broad framework there are 3 objectives.

The beef industry is concentrated in the prairie regions of Alberta, Saskatchewan, and Manitoba. This region is characterized by hot, dry summers, long, cold winters, and low levels of precipitation (25). Mean annual summer and winter temperatures, respectively, range from 14°C to 16°C and from −12.5°C to −8°C. Annual precipitation levels range from 250 mm in southwestern Saskatchewan and southeastern Alberta to almost 700 mm in southern Manitoba. Dry soil conditions are exacerbated by high winds, which accelerate water evaporation.

Climatic conditions affect parasite populations and consequent use of endectocides. Low stocking rates and periods of extreme cold or of hot, dry weather usually maintain infections of internal parasites in pastured cattle at subclinical levels. Hence, endectocides in Canada are applied most often in autumn, when cattle are moved from pastures into feedlots. Application at this time targets both external and internal parasites that are common pests of feedlot cattle during winter months. Respective examples include sucking lice (Haematopinus eurysternus [Nitzsch], Linognathus vituli [L.], and Solenopotes capillatus Enderlein) and chewing lice (Bovicola bovis [L.]) and gastrointestinal nematodes (Ostertagia and Cooperia) and cattle grub (Hypoderma spp.). Spring application of endectocides in cattle being turned out on pasture is much less common but can help reduce the buildup of nematodes in pastures and provide a measure of control against horn fly (26).

Endectocides are slightly to moderately metabolized in the treated animal and then excreted in the feces for weeks to months (29). The pattern of excretion is affected by formulation and other factors. Peak excretion usually occurs in the first week with injectable or topical formulations of ivermectin (17,30–32) and doramectin (32). Peak excretion of moxidectin occurs 1 to 2 d after application of an injectable formulation (29,33) but is delayed by 9 to 10 d after topical application (29 [Table 4.8]). The concentration of residual endectocide declines rapidly thereafter, but product can still be detected in dung up to 58 d after application (32). Use of ivermectin in a bolus formulation results in a relatively stable level of fecal excretion for up to 120 d (34). Differences in diet can cause a 4-fold difference in the peak concentration of residues in dung of cattle treated with ivermectin in an injectable formulation (31). Self-grooming by cattle treated topically can increase 10-fold the amount of ivermectin excreted in feces (35). Grooming between cattle may transfer endectocides to untreated cattle (36).

The distribution and fate of excreted residues in the environment depends on whether the treated animals are on pasture or in feedlots. Excreted residues bind tightly to the fecal material. On pasture, residues remain highly localized within the dung pat, such that their immediate effects are limited to dung-dwelling species (3). The limited data indicate that there is little degradation of residues until the dung is incorporated into the soil. Ivermectin residues in cattle dung exposed on pastures in Denmark and Tanzania showed no appreciable degradation after 45 and 14 d, respectively (30). Reported half-lives in soil are 61 to 79 d for doramectin (37), about 64 d for eprinomectin (38), and about 60 d for moxidectin (39) and in soil and soil/manure mixtures from 14 to 56 d for ivermectin (40). In feedlots, dung of treated cattle is scattered and trampled to form a relatively solid mat that accumulates during winter months. The level of degradation of fecal residues in the matted material during this time is unknown. Dung is removed from pens in the spring and composted or spread directly onto cropland. Incorporation into the soil before seeding, coupled with aerobic degradation and photo-degradation, further reduces residue concentrations (41).

Fresh dung is colonized almost immediately by adult flies, which feed, mate, and lay eggs that produce a new generation of flies in about 2 to 3 wk. Fly numbers rapidly decline after a few hours, by which time crust formation on the pat has reduced the release of odor attractants. Dung-feeding beetles arrive shortly thereafter to feed and oviposit, with peak colonization finished by the end of the 1st week after deposition. In contrast to flies, the egg-to-adult development time of dung-feeding beetles often takes weeks to months. Parasitic wasps and predaceous beetles arrive concurrently with the flies and dung-feeding beetles to feed on immature insects developing in the dung pat or to oviposit. There is very little additional colonization of dung by coprophilous insects 2 to 3 wk after deposition. Tunneling and feeding by insects accelerates pat degradation, which allows the pat to be more easily penetrated by vegetation and incorporated into the soil.

In a subsequent study (23), degradation was compared in dung from untreated cattle and dung from cattle treated 1 wk previously with a recommended topical dose of doramectin, eprinomectin, ivermectin, or moxidectin. Artificially formed pats were placed on pasture in spring and removed in autumn the same year. Degradation was measured as described for the earlier study. The experiment was repeated in each of 3 y. In 1998, reduced degradation was detected after the addition of doramectin, eprinomectin, and moxidectin. In 1999, no effect on degradation was detected. In 2000, reduced degradation was detected after the addition of moxidectin. When the data from the 3 experiments were combined, delayed degradation was detected only after the addition of eprinomectin.

Few studies have assessed the role of insects in degrading dung in North America. One such study (53) is discussed here at length because of its relevance to research in Canada, its provision of an estimated cost for undegraded dung on pastures, and its illustration of the complex and interacting factors that affect dung degradation. The investigators compared the surface areas of artificially formed control pats and similar pats to which the insecticide lindane had been added. The study was performed in the foothills of northern California, which has a dung fauna and hot, dry summers similar to those on the Canadian prairie. Pats were placed in the field during various months of the year and replicated in 4 pasture ecosystems: naturally vegetated woodland range (NW), partially cleared woodland range (PC), totally cleared woodland range (TC), and totally cleared, cultivated, and irrigated (I) pasture. Depending upon the pasture type, month, and fauna, elimination of insect activity in pats with lindane delayed total pat degradation by 4 to 21 mo in NW and PC pastures, by 4 to 30 mo in TC pastures, and by 3 to 6 mo in I pastures. Total degradation of untreated pats deposited in May required about 5 to 16 mo, compared with 9 to 40 mo for untreated pats deposited in June to September.

Undegraded dung pats smother new vegetation in subsequent years, reducing the amount of available forage. Also, the rank forage immediately adjacent to degrading pats is avoided by cattle. For a hypothetical ranch of 2024 ha supporting 455 cattle, and under the conditions at their California study site, the authors estimated that the forage lost in this manner represented a loss of 2730 kg of beef in the 1st growing season. Additional losses of 628 and 112 kg of beef were estimated for the 2nd and 3rd growing seasons after dung deposition. Calculated in $US for the year 1984, this lost production was estimated to be $3822 after the 1st year and a cumulative $4858 after 3 y. This cost would occur for each group of 455 cattle grazed per year.

Findings from studies in Canada, supported by results of studies elsewhere, show the following.

These findings can be presented within the context of the livestock industry as a whole or within the context of the individual cow–calf producer. Within an industry context, the current pattern of endectocide use in Canada is unlikely to pose a significant widespread threat to pasture environments. Most treatments are applied in autumn to cattle entering feedlots. Residues degrade during winter months before being further diluted via incorporation into cropland, where they appear to degrade readily, according to available study results. Treatments in spring or early summer have the greatest potential to adversely affect dung-dwelling insects because of peak insect activity during this time.

Within the context of individual producers, use of endectocides may be of concern. I have been contacted by dozens of ranchers in Canada and the United States concerned with perceived reductions of dung beetle numbers on their properties. These reductions may reflect factors unrelated to endectocide use. Nevertheless, concerned producers can reduce exposure of dung-dwelling insects to insecticidal residues in cattle dung by minimizing endectocide use in spring and early summer. Alternatively, they can use endectocide products that produce fecal residues less toxic to dung-dwelling insects.