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J. Appl. Ent. 127, 481–488 (2003)Ó 2003 Blackwell Verlag, BerlinISSN 0931-2048 Effects of ivermectin and doramectin faecal residueson the invertebrate colonization of cattle dung V. H. Suarez1, A. L. Lifschitz2, J. M. Sallovitz2 and C. E. Lanusse2 1Estacio´n Experimental Agropecuaria Anguil, INTA, Anguil, La Pampa, Argentina; 2Laboratorio deFarmacologı´a, Dpto. Fisiopatologı´a, Facultad de Ciencias Veterinarias, UNCPBA, Campus Universitario,Tandil, Argentina Ms. received: May 10, 2002; accepted: January 14, 2003 Abstract: The effects of avermectin [ivermectin (IVM) and doramectin (DRM)] faecal residues on dung colonizationand degradation by invertebrates were evaluated during late spring in the east of La Pampa province, Argentina. Thestudy was conducted after collection of faecal material from animals (10 steers per group) allocated to the followinggroups: untreated control group (CG) and groups treated subcutaneously (200 lg/kg) with either DRM (DG) or along-acting formulation of IVM (IG). Fifty pats (550 g each) per group were collected, prepared and deposited on thefield on days 3, 7, 16 and 29 post-treatment (pt). Eight pats per group were recovered after 7, 14, 21, 42, 100 and180 days post-deposition (pd) on the field. The weight, percentage of dry matter, number of arthropods and nematodesfrom faeces were determined. The faecal concentrations of IVM and DRM were measured by high performance liquidchromatography (HPLC) throughout the trial period to correlate the pattern of drug degradation in dung with pd time.
The total number of arthropods in dungs from CG was higher (P < 0.05) than those counted between days 3 and 29 ptin IG and DG. A decrease in the number of Coleoptera larvae (P < 0.05) between days 21 and 42 days pd wasobserved in both treated groups. Diptera larvae counts in CG pats were significantly higher (P < 0.05) than thoseobtained in treated groups in the 7- and 14-day-old pats. A lower number (P < 0.05) of Collembola, compared withpats from CG, was recovered from IG and DG pats deposited at days 3 and 7 pt and exposed from day 42. The countsof Acari in pats from treated animals were lower (P < 0.05) than those observed in CG pats at 3, 8 and 16 days pt.
There were no differences neither in adult Scarabaeidae recovered nor in the proportions of dung buried and destroyedby great dung beetles. Dung specific nematodes were reduced (P < 0.05) in IG and DG pats from 3 and 7 days ptcompared with those of CG pats. The comparative results shown here demonstrate that the negative effects of bothIVM and DRM on dung colonization are similar. The pattern of drug degradation in the environment was very slow.
High residual concentrations of both active parent compounds were recovered in dungs exposed in the field for up to180 days pd. Concentrations as high as 13 ng/g (IVM) and 101 ng/g (DRM) were measured in faeces obtained frompats deposited on day 27 pt and exposed to the environment during 180 days. The results show a decrease ininvertebrate colonization of dung recovered from IVM- and DRM-treated cattle, which is in agreement with the largedrug residual concentrations measured in faeces.
Key words: cattle-Nematoda, doramectin, dung-fauna, environmental toxicity, faecal residues, ivermectin treated animal and excreted in large concentrations asunchanged parent drugs in faeces (Lifschitz et al., The endectocide drugs are 16-membered macrocyclic 2000). There are differences on the pharmacokinetic lactones with a broad-spectrum antiparasitic activity behaviour, pattern of faecal excretion and efficacy of against a wide range of nematodes and arthropods.
endectocide compounds in cattle according to the type The macrocyclic lactones available on the market for of formulation and route of administration used (Herd, use in cattle include the avermectins [ivermectin (IVM), abamectin, doramectin (DRM) and eprinomectin), and Cattle productive assessments in the Pampeana milbemycins (moxidectin). These compounds cause region of Argentina have demonstrated that parasitic paralysis or several sublethal metabolic disorders and losses can be important in bovine grazing systems eventually death of invertebrates that ingest or tran- (Suarez et al., 1991, 1999) and that parasite control is scuticulally absorb them (Campbell and Benz, 1984).
very profitable. In this area, as in many other regions Endectocides are potent parasiticide molecules with of the southern hemisphere, a great proportion of high efficacy patterns at extremely low dosages. They current parasite control programmes are based on the are extensively distributed to different tissues in the U. S. Copyright Clearance Center Code Statement: use of endectocides, taking advantage of their persist- ence effect on a broad range of target parasites.
At deposition day, weight, dry matter and parasitological Early studies have reported high effect on target- measurements from fresh faeces were determined. Ten pest insect in the dung pats, such as Haematobia grams wet weight of the samples from each group was irritans (Miller et al., 1981). These led to further collected for estimating faecal moisture by drying samples investigations into the adverse effects of these drugs for 48 h at 100°C and expressed as percentage of dry upon non-target fauna of the dung (Wall and Strong, weight. Nematode eggs were counted according to the 1987). Currently, there is some information from method of Roberts and O’Sullivan (1949) and specific Europe, Australia and North America (Madsen et al., infective larvae (L3) differentiated after culture of faecal Herd, 1995; Wardhaugh and Beckmann, 1996) on the non-specific effects of IVM, which can kill or Eight pats per group were recovered and examined after 7, 14, 21, 42, 100 and 180 days on the field. Collected pats were disrupt the development of a wide variety of insect- transferred to polyethylene bags and taken to the laboratory.
colonizing dung pats. This decomposing dung fauna Each pat sample was weighed and the dry weight was help to maintain the ecosystem by returning nutrients determined. The dung fauna was enumerated and identified.
to the soil; thus, the long-term consequences of Arthropods were recovered using the Berlese method (Ber- endectocide utilization remain unknown (Strong, lese, 1904), while a 5-g dung subsample was processed through Baermann modified method (Suarez, 1997) to isolate Current knowledge of the environmental impact of endectocide-based control strategies in countries with avery intensive use, such as in Argentina, is scarce.
2.4 Measurement of faecal drug residue concentrations Some preliminary information has shown the adverseeffect of IVM on the level of invertebrate colonization Faecal samples (10 g) of IVM- and DRM-treated animals and faecal dispersion in dung pats during autumn were collected, kept in labelled vials and stored at )20°C until analysed by high-performance liquid chromatography Suarez, 2001). However, no information is available on the ecotoxic effects of these types of drugs during (HPLC). The extraction of IVM and DRM from faecalsamples was carried out following the technique described by other seasonal periods and in other ecological regions.
et al. (2000), using abamectin (ABM) as internal Additionally, scarce information of ecotoxic effects of standard. The solid phase extraction was carried out using an DRM is available worldwide (Dadour et al., 2000).
Aspec XL autosampler (Gilson, Villiers Le Bell, France). The This field study was conducted to evaluate the derivatization to convert IVM and DRM in fluorescent comparative effects of IVM and DRM faecal residues molecules was done as described by De Montigny et al.
on cattle dung-colonizing fauna and on dung mass (1990). IVM and DRM faecal concentrations were deter- mined by HPLC with fluorescence detection using a Shim-adzu 10 A HPLC system (Shimadzu Corporation, Kyoto,Japan) following the technique described by Lifschitz et al.
(1999, 2000). The IVM or DRM/ABM peak area ratios were used to estimate the IVM and DRM concentrations in spiked(validation of the analytical method) and experimental faecal samples. The solvents (Baker, Phillipsburg, NJ) used duringthe extraction process and drug analysis were of HPLC The experiment was carried out at the Agricultural Research Station (EEA) of Anguil in the Western Pampeana region of A complete validation of the analytical procedures used for Argentina. On 9 November 1998, 30 steers aged 18 months extraction and quantification of IVM and DRM was and weighing 378 ± 18 kg were randomly allocated to three performed before starting the analysis of experimental groups of donor animals. These animals were representative samples. Calibration curves were prepared in a range of the grazing fattening system of the region and were between 0.5 and 100 ng/g using least squares linear regres- naturally infected with prevalent gastrointestinal nematodes sion analysis. Correlation coefficients (r) were >0.99. Drug (Suarez, 1990). Steers received a injectable treatment with recovery from faeces at different concentrations was 72.3% either a generic long-acting IVM (IG) formulation (Feno- (IVM) and 73.6% (DRM). The intra-assay precision max; Hoechst Roussel Vet., Av. Int. Tomkinson 2054 (1642), expressed as coefficient of variation was 3.31% (IVM) and San Isidro, Province of Buenos Aires, Argentina) or DRM (Dectomax; Pfizer S.A.C.I., Virrey Loreto 2477 (1426),Buenos Aires, Argentina) (DG), both given at 200 lg/kg.
Group CG was the untreated control.
Daily rainfall, evaporation, relative humidity and daily 2.2 Faecal collection and pat preparation temperatures were recorded from the Department of Mete-orology of INTA, Anguil, near the experimental site.
At days 3 (12 November), 7 (16 November), 16 (25November) and 29 (8 December) after treatment, faecesvoided in the previous 18–22 h were collected separately from each cattle group for deposition on the field, using separate Data on the counts of arthropods and nematodes recovered equipment. The dung from each group was then mixed per 100 g of dry dung matter, weight and dry matter thoroughly and weighed into 550 g wet weight aliquots percentages from replicated pats were analysed by analysis fashioned into 50 experimental pats of 15 cm diameter. These of variance with treatment and duration of field exposure as 50 artificially formed pat replicates per group were placed in alternating 2 m sequence in three rows on bare-scraped soil SAS, 1988). The arthropod data were rank trans- Iman and Canover, 1979) for analysis.
Effects of avermectins on dung colonization The annual rainfall in this region ranged between 700and 800 mm and the highest incidence was fromOctober (spring) to April (autumn). However, at thebeginning of the study rainfall decreased by 30%below the 45-year mean and late spring and earlysummer period experienced severe drought.
The great variety of species collected were divided intolarge arthropods, mainly Coleoptera and Dipteralarvae, and microarthropods such as Collembola and Fig. 1. Total cumulative number of Coleoptera larvae Acari. The total number of arthropods recovered from from day 3, 7, 16 and 29 post-treatment, recovered in IG and DG pats was significantly (P < 0.05) lower 100 g of dry weight of pats exposed after 7, 14, 21, 42, than in control pats. Differences were recorded in all 100, 180 days on the field. Dung pats were obtained from pat data depositions from the 3rd to the 29th day post- treatment (table 1). There was a significant (P < 0.01) doramectin (DG) or untreated controls (CG) interaction between treatment groups and time in thefield.
number of larvae after 7 and 14 days of exposure in the field. Only larvae of the Sarcophagidae, Muscidae andSphaeroceridae families were observed. Control pats The majority of families of Coleoptera present in the contained the highest counts (P < 0.05) in the 7- and pats were Scarabaeidae and Aphodiidae. The largest 14-day-old pats from the 3rd and 7th post-treatment dung beetles found were Sulcophanaeus menelas, faecal extraction. Total mean Diptera counts for all Onthophagus hirculus and Canthidium breve, but the post-treatment depositions is presented in fig. 2.
most frequent family recovered by the Berlese methodwere mainly Aphodiidae and other families speciessuch as Histeridae and Staphylinidae. No significant differences were observed between the adult Scara- Collembola specimens numbers showed significant baeidae, Aphodiidae, Histeridae and Staphylinidae (P < 0.05) differences between treated and non- treated groups at days 3 and 7 post-treatment.
The number of Coleoptera larvae (mainly Aphodii- Numbers of Collembola from faeces from injected dae) collected per 100 g of pat dry weight is shown in animals were smaller after 42–180 days in the field fig. 1. In general, larval counts in the dung pats from compared with controls. Mean total Collembola treated animal groups were significantly (P < 0.05) numbers recovered from 100 g of dry faeces from lower than those from the control group. However, day 3 and 7 post-treatment were 2.0, 2.3 and 3.7 for while the control dung showed the highest differencesin larval numbers between groups at 21 and 42 days,no statistical differences were seen up to 14 days in the Diptera larvae occurred in low numbers and were distributed very irregularly. Pats contained the highest Table 1. Mean total arthropod number recovered in 100 g of dry weight of pats deposited 3, 7, 16 and 29 days after treatment. Dung pats were from cattlegroups injected withivermectin (IG), doramectin (DG) Fig. 2. Mean number of Diptera larvae recovered in 100 g of dry weight of pats deposited 3, 7, 16, and 29 days after treatment. Dung pats were obtained from Column mean values with different scripts are significantly dif- doramectin (DG) or untreated controls (CG) The appearance between treated and control group pats was not different throughout this study. There were very low numbers of pats destroyed by the great dung beetles (Sulcophanaeus and Onthophagus) and there were no differences between treatments in the proportions of dung buried. Most of them rest 78.9 ± 20.05% of mean dry weight during the whole trial. There were no significant differences in wet and dry weight (moisture content) of pats among the threegroups at any time.
Fig. 3. Total cumulative number of Acari from day 3, 7, Statistical analysis comparing dung fauna numbers 16 and 29 post-treatment, recovered in 100 g of dry showed that the effects of the IVM and DRM were not weight of pats exposed after 7, 14, 21, 42, 100, 180 days significantly different. All figures and tables of arthro- on the field. Dung pats were obtained from cattle groups pods recovered showed similar numbers of inverte- treated witheither ivermectin (IG), doramectin (DG) brates collected from pats from both drug-treated IG, DG and CG, respectively. There was a significantinteraction between treatment and exposition in the Large concentrations of IVM and DRM were meas- field. Collembola counts from pats during the first ured in all the dung pat samples evaluated from 42 days in the field were negligible in all groups.
treated groups. Faecal IVM concentrations were Numbers of Acari recovered from the control group 1150 ng/g (at day 3 post-treatment) and 22.8 ng/g (at pats were significantly (P < 0.05) higher than those of day 29 post-treatment). DRM faecal concentrations treated groups from day 14 in the field and from obtained at the same days post-treatment varied depositions collected from day 3, 7 and 16 post- between 1122 and 135 ng/g, respectively. Long per- sistence of both molecules was observed in the patsexposed in the field during different periods. TheIVM and DRM concentration levels measured in dung pats obtained at different days post-treatment and The infective larval genera of gastrointestinal nema- after the different post-deposition periods are sum- todes recovered from the control cattle pats were marized in tables 2 and 3. The long persistence of the Ostertagia, Haemonchus, Cooperia, Trichostrongylus active parent compounds in the environment was and Oesophagostomum. No infective nematode larvae corroborated by the large faecal concentrations meas- were detected in pats of treated groups.
ured in dung pats up to 180 days after their deposition About dung-specific nematodes recovered, only in 3 and 7 days after treatment, total counts occurred insignificant (P < 0.05) reduced numbers in pats fromtreated cattle compared with controls. The mean number of dung-specific nematodes recovered from5 g of dung dry matter during the study was 87.2, 68.9 Residues of both IVM and DRM induced a marked and 123.0, respectively, for IG, DG and CG. This drug adverse effect on different dung-colonizing inverte- adverse effect was noted in treated cattle pats until brates. These results are in agreement with previously reported data suggesting the toxicity of IVM faecal concentrations (ng/g dryweight) in cattle dung pats pt, post-treatment; pd, post-deposition; ND, not determined.
Effects of avermectins on dung colonization posed in the field for differentperiods (from 7 to 180 days) pt, post-treatment; pd, post-deposition; ND, not determined.
residues on non-target dung arthropods (Strong, 1993; abamectin were toxic to dung beetles larvae for Herd, 1995; Wardhaugh and Beckmann, 1996). How- 2–4 weeks post-treatment (Wardhaugh and Mahon, ever, there were no differences on adult Coleoptera 1991; Ridsdill-Smith, 1993). In Brazil, Iglesias (1998) counts in any pats regardless of the treatment, and it reported a minor number of Coleoptera larvae after seems that there was no repellent effect in pats 30 days of deposition in faeces of IVM-treated ani- collected from IVM-treated animals. In addition, these results seem to show non-lethal toxic effect on adult Dipteran larvae, present in low numbers in this dung colonizing Coleoptera. However, the methodo- trial, aerate dung, making them attractive to other logy used in this work was unable to measure precisely invertebrates. According to previous results (Suarez, the probable residue toxicity to the reproductive 2001) fly larvae were reduced in treated cattle faeces, performance of colonizing Coleoptera. A recent work but the low number of fly larvae limited statistical (Wardhaugh et al., 2001) documented IVM- and epri- analysis. In the subtropical region of Brazil, where the nomectin-induced reproductive deficiencies in dung trials were carried out in July during the drought beetles. Other studies (Wardhaugh and Rodriguez season, very high numbers of fly larvae were collec- ´ndez, 1988; Ridsdill-Smith, 1993) have also shown ted. In this scenario, significant reduced number of that some species of newly emerged adult beetles are Diptera larvae in IVM-treated cattle faeces from 3 to affected by IVM faecal residues, but with few days 28 days post-treatment after 10, 30 and 60 days in the older they can survive. About the impact of DRM field were reported (Iglesias, 1998). Another trial residues, Dadour et al. (2000) indicated that this drug showed that in faeces from IVM-treated cattle, the affects the mortality and reproductive potential on development of Musca domestica was not observed newly emerged adults of Onthophagus binodis between (or neglegible), for H. irritans it was prevented for up to 35 days post-treatment, while Stomoxys calcitrans Although this study was not designed to obtain development was less affected (Miller et al., 1981). In quantitative data on the largest dung-burying beetles addition, no target flies were affected by avermectin such as Sulcophanaeus and Onthophagus, these beetle faecal residues for 10 and 30–35 days post-treatment species were those recovered at the largest counts.
These beetles destroy and bury the dung pats during (Madsen et al., 1990; Wardhaugh and Mahon, 1998).
the first days after deposition. Pitfall traps must be Biological assays indicated that avermectin residues necessary to quantify their presence and other meth- varied according to the formulation and route of odology to study their nesting and larval stages.
administration of the drug, and oral formulation Contrary to previous autumn observations (Suarez, (0.2 mg/kg) for sheep or horses adversely affected fly 2001) where numbers of adult Staphylinidae of treated larvae only for 3–4 days after administration (Herd, groups were lower up to 16 days post-treatment, in this trial with different climatic conditions, there were Microarthropods were also affected by IVM and similar numbers of this predator insect family. Simi- DRM treatments. In Collembola, numbers were only larly, Strong et al. (1996), under England weather reduced in treated groups during 7 days after treat- conditions, obtained no Staphylinidae differences ment, while in a previous autumn trial, numbers were negatively affected for 28 days after treatment (Suarez, The Coleoptera larvae (mainly Aphodiidae) were 2001). These differences may be due to the reduced present in the DRM and IVM pats in lower numbers density observed in the present study or other inter- than in control pats from 21 or 42 days in the field.
acting factors related to a drought period in late These data evidenced that drug residues could be implicated in adverse effect on Coleoptera immature Data of Acari collected in the current assay are in stages at least during 29 days after treatment under our agreement with those obtained from the autumn trial regional conditions. Previous studies in Europe (Som- (Suarez, 2001), where mites of treated groups were et al., 1993; Strong et al., 1996) confirm these significantly fewer than those of control group during findings, showing that IVM affects reproductive per- 3, 8 and 16 days post-treatment. There are few reports formance of adults, feeding activity and development about microarthropods. In agreement with the present of larvae. Injectable formulations of both IVM and results, Iglesias (1998), in Brazil, reported that mites of several suborders (Gamasida, Oribatida and Acaridi- with a more rapid rate of excretion, and as a da) were reduced in the dung from IVM-treated cattle consequence, is likely to be less harmful to the during 3, 14 and 28 days after treatment. Endectocide environment. Drug formulation, dosage and admin- concentrations in faeces directly account for the istration route are important factors in determining deleterious effect on Acari. However, the presence of drug profile elimination and persistence of dung drug residues in nematodes and Diptera eggs eaten by residues (Herd et al., 1996). Comparative studies some Acari species, may also contribute to reduction in indicate that moxidectin has no detectable effects on Acari. The food source of some Acari and Collembola non-target arthropods and hence it is environmentally are based in bacteria and saprophytic fungi (Moore safer than IVM (Fincher and Wang, 1993; Strong and and DeRuiter, 1993). The consequences of the endect- Wall, 1994). Comparisons between pour-on formu- ocide residues on these invertebrates and their inter- lations of eprinomectin and moxidectin showed that actions with the dung food web need to be elucidated.
cattle faeces voided after treatment with eprinomectin Suarez (1990) reported infective larvae of gastroin- were associated with high Onthophagus juvenile mor- testinal nematode genera recovered from the control tality during the first 1–2 weeks post-treatment, while cattle pats. There were very few studies on dung- moxidectin had no detectable effects (Wardhaugh specific nematodes, many of which are fungivorous and help reduce fungal populations. Data from this Large IVM and DRM faecal concentrations were trial confirm the initial autumn observation of Suarez measured in dung pats throughout the experimental (2001) where dung pats from treated cattle had low period. The concentrations of DRM in faeces were nematode numbers. However, in that report the higher than those measured for IVM, which is highly persistence of adverse effect was prolonged until consistent with the previously reported patterns of 2 weeks after injection, while in the present trial the tissue distribution and excretion profile for these effect was noted only in the first week post-treatment.
molecules in cattle (Lifschitz et al., 2000). A pro- In Germany, Barth et al. (1993) pointed out that only longed persistence of both active parent compounds some dung-specific nematodes species occurred in (IVM and DRM) permitted their detection in faeces reduced numbers in pats of the IVM bolus-treated from pats exposed for up to 180 days in the field (tables 2 and 3). Remaining drug concentrations in The similar rate of pat degradation for the groups dung deposited after 27 days post-treatment and reported in this trial differ from previous data obtained exposed to environmental conditions for 180 days during early autumn. Autumn results (Suarez, 2001) represented between 56% (IVM) and 75% (DRM) of showed significant delays in the rate of degradation of the concentrations measured immediately after their those pats from cattle injected with IVM and DRM, deposition. Hence, this scarce effect of field exposure utilizing reduced pat weight as indicator. Dung fauna on IVM and DRM faecal concentrations determined diversity recovered in late autumn trial was not that enough drug to adversely affecting dung-colon- different from those of the actual trial, but was more izing fauna was present throughout the entire trial abundant and the number of pats dispersed was also period. These concentrations were far above those higher. These contradictory results agree with other determined as lethal (Sommer et al., 1992) or suble- controversial results obtained under different experi- thal (Strong, 1992; Dadour et al., 2000) for dung fauna. Altogether, these results indicate that expo- (Strong, 1992) and Denmark (Madsen et al., 1990) sure to field conditions will not prevent the deleteri- showed significant delays in dung disappearance in ous effects of faecal residual concentrations of pats from IVM-treated cattle, while others obtained no endectocide molecules on dung fauna. These effects delay differences (McKeand et al., 1988; Wratten et al., will be exerted for a long time until dung pats are no 1993). These differences may have been influenced by more suitable for feeding and colonization of beetles.
several factors, such as the methodologies used for pat A more pronounced effect can be expected when dispersal measurements, dung fauna regional species, administering IVM as an intraruminal long-acting the influences of climate and season fauna variation bolus. The administration of an intraruminal IVM (Herd, 1995). Seasonal peaks of insect activity are bolus showed a long-lasting deleterious effect as high likely to produce greater degradation effects (Strong, concentrations (38 ng/g) are achieved in faeces for up 1993). In the present study, drought conditions seem to be the cause of reduced arthropod number and pat The results reported here for this geographical In accordance with a similar previous field trial region demonstrate that cattle faecal residues of both during autumn (Suarez, 2001), there were similar IVM and DRM adversely affect the invertebrate effects between the two injectable avermectins under colonization of dung in late spring. Both drugs appear late spring field conditions of the La Pampa region.
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Source: ftp://ftp.visi.com/disk3/neurotic/Suarez-Ivermectin%20Faecal%20residues.pdf