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Survival and growth of Lumbricus terrestris (Lumbricidae) fed on dung from cattle given sustained-release boluses of ivermectin or fenbendazole
European Journal of Soil Biology 38 (2002) 319−322 www.elsevier.com/locate/ejsobi
Survival and growth of Lumbricus terrestris (Lumbricidae) fed on dung from cattle given sustained-release boluses of ivermectin or fenbendazole Tina S. Svendsen a,*, Christian Sommer a, Peter Holter b, Jørn Grønvold a a
Section of Zoology, Department of Ecology, The Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark b Department of Terrestrial Ecology, Zoological Institute, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark Received 14 August 2000; accepted 23 May 2001
Abstract The effects of faecally excreted ivermectin and fenbendazole, and their metabolites, on the survival and growth of the common pastureland earthworm Lumbricus terrestris, have been studied in the laboratory. Hatchlings were fed dung voided by untreated cattle or cattle given sustained-release boluses of the antiparasitic agents ivermectin or fenbendazole. Hatchling survival and growth rates were followed until maturity. The survival of worms fed untreated dung was 100% whereas survival in ivermectin and fenbendazole groups was 97 and 91%, respectively. The first worms became mature 16 weeks after hatching, irrespective of dung type, and all worms were mature 24 weeks after hatching. The growth rate of the worms fed dung from cattle given ivermectin boluses was 2.6 mg higher day–1 than that recoded for the control group, whereas the growth rate of worms fed on dung from cattle given fenbendazole boluses did not differ significantly from the control group. It may be concluded that ivermectin, fenbendazole and their metabolites had no adverse effects on the survival and growth of L. terrestris when exposed through dung under laboratory conditions. © 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Lumbricus terrestris; Ivermectin; Fenbendazole; Sustained-release bolus; Growth; Dung
1. Introduction The effect of the broad-spectrum anthelmintic ivermectin on non-target dung-degrading insect fauna has been studied several times, e.g. [9,14,16,17,18]. Ivermectin and its metabolites are excreted in dung [3] in concentrations dependent on formulation and route of administration [5,14]. Ivermectin administered in a sustained-release bolus is potentially more harmful to dung-inhabiting fauna than ivermectin given topically or by injection. This is due to the extended period of drug release in the rumen and high concentrations of the parent drug in the dung [5,13,16,17].
* Corresponding author. Fax: +45-35-28-26-70. E-mail address: [email protected] (T.S. Svendsen).
The anthelmintic benzimidazole, fenbendazole is also formulated as a sustained-release bolus. Residues and metabolites of fenbendazole are also excreted in dung [12], but Strong et al. [16] found no toxic effects on dung-inhabiting insects in studies on dung from cattle given fenbendazole boluses. However, other benzimidazoles are used as fungicides and some of these compounds have negative effects on earthworms in toxicity tests [15]. Although earthworms play the major role in the disappearance of dung pats in north temperate countries like Denmark [6], studies on the effect of veterinary medicines on earthworms are scarce [4]. Reports are mainly concerned with short-term effects of residues and metabolites of ivermectin on earthworm numbers in the field, e.g. [9,14,17]. The few laboratory studies performed on earthworms have been set up with the epigeic earthworm Eisenia
© 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. PII: S 1 1 6 4 - 5 5 6 3 ( 0 2 ) 0 1 1 6 7 - 6
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fetida exposed to ivermectin mixed into soil [2,3]. However, E. fetida is normally not associated with cow dung and may therefore be of limited relevance. Furthermore, tests of drugs at concentrations occurring in the field, and exposure through ingestion of dung rather than by contact with contaminated soil are of more relevance in studies of the effects of veterinary medicines on earthworms. In the present work we study the effect, under laboratory conditions, of ivermectin, fenbendazole and their metabolites on survival and growth of the anecic earthworm Lumbricus terrestris fed on dung from cattle given bolus formulations of these drugs.
2. Materials and methods 2.1. Test substrate Artificial soil was prepared according to the OECD guideline for the testing of chemicals [11]; 10% sphagnum peat, 20% kaolin clay and 70% sand (particle size 0.3–0.6 mm). Tap water was added to maintain a moisture content of 25.2 ± 2.3% (wet mass ± SD) and pH was adjusted to 6.7 ± 0.3 by addition of calcium carbonate. 2.2. Dung In May 1999, 14 heifers (weighing 366 ± 24 kg) were given fenbendazole sustained-release boluses (12 g Panacurt bolus, Hoechst Roussel), and eight heifers (415 ± 26 kg) received ivermectin boluses (1.72 g Ivomect bolus, MSD Agvet). The two groups of heifers grazed on separate pastures. Dung from a third group of four grazing heifers (500 ± 66 kg) served as untreated control. Fresh dung pats from each group were collected from the pastures and their water content was adjusted 85–86% wet mass. The dung was stored at –18 °C and used from July to December 1999. In December 1999, a new batch of dung was collected from three groups of four stabled cattle each, fed new ensiled grass only. The three groups (weighing 181 ± 18 kg, 180 ±16 kg and 239 ± 32 kg) were given fenbendazole or ivermectin boluses, or remained untreated. The water content in the dung was 87–88% wet mass. This dung was used in the experiment from December 1999 to June 2000. 2.3. Culturing of L. terrestris Hatchlings were taken from cocoons produced in the laboratory from field collected mature L. terrestris that were held at 15 °C in artificial soil. Cocoons were kept in 12-well tissue culturing plates with moist filter paper and one cocoon in each well. The plates were placed at 15 °C and cocoons were inspected weekly until hatching.
2.4. Survival and growth Each hatchling was transferred to a 300 ml jar with 100 g of artificial soil. The hatchlings were randomly allocated to three groups until there was a total of 32 worms in each group. The hatchlings were fed 10 g of either untreated control dung or dung from fenbendazole or ivermectin treated heifers. The dung was placed on the soil surface and both dung and soil were renewed every 4 weeks when worms were weighed. After 8 weeks, the amount of soil was increased to 200 g and the worms were fed 25 g of dung for the next 8 weeks. Subsequently the amount of dung was raised to 50 g per 4 weeks until worms reached maturity. 2.4.1. Statistics The age of worms when first fully clitellated was compared between groups with a χ2-test. The mass of the control group at maturity was compared with corresponding values of the two treated groups by the GLM procedure in the SAS statistical software system, as were the mass and the growth rate of hatchlings.
3. Results The initial mean mass of hatchlings in the control, ivermectin and fenbendazole group were 0.056 ± 0.002 g, 0.058 ± 0.002 g and 0.059 ± 0.002 g, respectively. There were no significant differences between groups (P > 0.05). In all groups, the survivorship until maturity was high (Table 1). The first worms became mature (fully clitellated) after 16 weeks irrespective of dung type. The majority became fully clitellated after 20 weeks and some took 24 weeks, but this did not result in any significantly differences between groups (P > 0.05) (Table 1). The mean growth rate from hatching to maturity was significantly higher in the ivermectin group than in the control group (P < 0.05), whereas the latter did not differ significantly from the fenbendazole group (Table 1).
4. Discussion There was no direct toxic effect of either ivermectin or fenbendazole, or their metabolites in cattle dung on L. terrestris. The mean age and weight when the worms reached maturity were unaffected. The growth rate was slightly higher (2.6 mg day–1) when worms were fed on dung from cattle given ivermectin than on dung from untreated cattle (Table 1). However, the growth rates and the age of maturity recorded for all earthworm groups in the current study are intermediate between those observed in other studies of L. terrestris [1,7], suggesting that our rearing conditions were close to optimal.
T.S. Svendsen et al. / Eur. J. Soil Biol. 38 (2002) 319–322
321
Table 1 Mean growth rate, age and mass when first fully clitellated and mortality of L. terrestris fed on dung from untreated grazing cattle (control) or from grazing cattle given ivermectin or fenbendazole sustained-release boluses Age at maturity (weeks) 16 Dung treatment
Growth rate (mg day–1)
Control 29.5 Ivermectin 32.1 Fenbendazole 31.1
20
24
Dead
Number (% of total)
Mean mass ± SE
Number (% of total)
Mean mass ± SE
Number (% of total)
Mean mass ± SE
Number (% of total)
6 (19) 5 (16) 7 (22)
3.75 ± 0.19 3.32 ± 0.13 3.82 ± 0.10
20 (63) 23 (72) 14 (44)
4.26 ± 0.14 4.69 ± 0.12 4.45 ± 0.19
6 (19) 3 (9) 8 (25)
4.19 ± 0.26 5.11 ± 0.53 4.82 ± 0.20
0 1 (3) 3 (9)
Our results, which indicate that neither ivermectin nor fenbendazole have any adverse effects on the survival or growth rates of L. terrestris, agree with those of Madsen et al. [8] who found no effect on the weight of Aporrectodea longa and A. tuberculata fed on dung from cattle treated with a range of anthelmintics, including ivermectin and fenbendazole, under semi-field conditions. Gunn and Sadd [2] found a similar response of E. fetida at ivermectin concentrations up to 8 mg kg–1 soil, but reported reduced earthworm growth and increased mortality at higher drug concentrations. Halley et al. [3] found no correlation between ivermectin concentrations in soil and weight changes in E. fetida, but observed increased mortality at concentrations higher than 25 mg ivermectin kg–1 soil. In the present study, as in Madsen et al. [8], the concentrations of the drugs and their metabolites in the dung were not known. We used 1.72 g ivermectin boluses constructed to release 12 mg ivermectin per day and 12 g fenbendazole boluses releasing 67–103 mg fenbendazole per day [10]. Herd et al. [5] found ivermectin concentrations of 0.4–0.5 mg kg–1 dung (wet mass) from cows (weighing approx. 400 kg) treated with similar sustained-release ivermectin boluses, and that more than 80% of the daily bolus release of ivermectin was excreted in the dung. The concentration of fenbendazole in cow dung following sustained-release administration has not been reported. However, it seems likely that the concentration of the drugs and their metabolites in this study were much lower but more realistic than the concentrations tested by Gunn and Sadd [2] and Halley et al. [3]. Moreover, the effect of the drugs and their metabolites ingested by feeding on dung of treated livestock may be different to those elicited by exposure to pure drugs mixed into the soil. Different species of earthworms might also respond differently. In consequence, further studies involving a wider range of relevant earthworm species at drug concentration that are known to occur under field conditions seem highly desirable. From our study we conclude that ivermectin and fenbendazole and their metabolites in cow dung have no adverse effects on the survival and growth of the dungfeeding earthworm L. terrestris under laboratory conditions.
Acknowledgements We are grateful to Karen Freiesleben, Torben Olsen, Lise and Jørgen Due for providing cattle for this experiment. Thanks to Hanne L. Kristiansen and Hanne Rawat for technical assistance and to Keith Wardhaugh for comments on the manuscript.
References [1]
[2]
[3]
[4] [5]
[6]
[7]
[8]
[9]
K.R. Butt, J. Frederickson, R.M. Morris, The life cycle of the earthworm Lumbricus terrestris L. (Oligochaeta: Lumbricidae) in laboratory culture, Eur. J. Soil Biol. 30 (1994) 49–54. A. Gunn, J.W. Sadd, The effect of ivermectin on the survival, behaviour and cocoon production of the earthworm Eisenia fetida, Pedobiologia 38 (1994) 327–333. B.A. Halley, T.A. Jacob, A.Y.H. Lu, The environmental impact of the use of ivermectin: Environmental effects and fate, Chemosphere 18 (1989) 1543–1563. R. Herd, Endectocidal drugs: ecological risks and countermeasures, Int. J. Parasit. 25 (1995) 875–885. R.P. Herd, R.A. Sams, M. Ashcraft, Persistence of ivermectin in plasma and faeces following treatment of cows with ivermectin sustained-release, pour-on or injectable formulations, Int. J. Parasit. 26 (1996) 1087–1093. P. Holter, Effect of earthworms on the disappearance rate of cattle droppings, in: J.E. Satchell (Ed.), Earthworm Ecology, Chapman and Hall, London, 1983, pp. 49–57. A. Lofs-Holmin, Reproduction and growth of common arable land and pasture species of earthworms (Lumbricidae) in laboratory studies, Swedish J. Agric. Res. 13 (1982) 31–37. M. Madsen, J. Grønvold, P. Nansen, P. Holter, Effects of treatment of cattle with some anthelmintics on the subsequent degradation of their dung, Acta vet. Scand. 29 (1988) 515–517. M. Madsen, B. Overgaard Nielsen, P. Holter, O.C. Pedersen, J. Brøchner Jespersen, K.M. Vagn Jensen, P. Nansen, J. Grønvold, Treating cattle with ivermectin: Effects on the fauna and decomposition of dung pats, J. Appl. Ecol. 27 (1990) 1–15.
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[10] Q.A. McKellar, Ecotoxicology and residues of anthelmintic compounds, Vet. Parasitol. 72 (1997) 413–435. [11] OECD, Guideline for the testing of chemicals. Earthworm, acute toxicity tests, OECD 207 (1984). [12] C.R. Short, S.A. Barker, L.C. Hsieh, S.P. Ou, T. McDowell, L.E. Davis, C.A. Neff-Davis, G. Koritz, R.F. Bevill, I.J. Munsiff, Disposition of fenbendazole in cattle, Am. J. Vet. Res. 48 (1987) 958–961. [13] C. Sommer, B. Overgaard Nielsen, Larvae of the dung beetle Onthophagus gazella F, (Col., Scarabaeidae) exposed to lethal and sublethal ivermectin concentrations, J. Appl. Entomol. 114 (1992) 502–509. [14] C. Sommer, B. Steffansen, B. Overgaard Nielsen, J. Grønvold, K.M. Vagn Jensen, J. Brøchner Jespersen, J. Springborg, P. Nansen, Ivermectin excreted in cattle dung after subcutaneous injection or pour-on treatment: concentrations and impact on dung fauna, Bull. Entomol. Res. 82 (1992) 257–264.
[15] A. Stringer, M.A. Wright, The toxicity of benomyl and some related 2-substituted benzimidazoles to the earthworm Lumbricus terrestris, Pestic. Sci. 7 (1976) 459–464. [16] L. Strong, R. Wall, A. Woolford, D. Djeddour, The effect of faecally excreted ivermectin and fenbendazole on the insect colonisation of cattle dung following the oral administration of sustained-release boluses, Vet. Parasitol. 62 (1996) 253–266. [17] R. Wall, L. Strong, Environmental consequences of treating cattle with the antiparasitic drug ivermectin, Nature 327 (1987) 418–421. [18] K.G. Wardhaugh, R.J. Mahon, Avermectin residues in sheep and cattle dung and their effects on dung-beetle (Coleoptera: Scarabaeidae) colonisation and dung burial, Bull. Entomol. Res. 81 (1991) 333–339.
Survival and growth of Lumbricus terrestris (Lumbricidae) fed on dung from cattle given sustained-release boluses of ivermectin or fenbendazole Tina S. Svendsen a,*, Christian Sommer a, Peter Holter b, Jørn Grønvold a a
Section of Zoology, Department of Ecology, The Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark b Department of Terrestrial Ecology, Zoological Institute, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark Received 14 August 2000; accepted 23 May 2001
Abstract The effects of faecally excreted ivermectin and fenbendazole, and their metabolites, on the survival and growth of the common pastureland earthworm Lumbricus terrestris, have been studied in the laboratory. Hatchlings were fed dung voided by untreated cattle or cattle given sustained-release boluses of the antiparasitic agents ivermectin or fenbendazole. Hatchling survival and growth rates were followed until maturity. The survival of worms fed untreated dung was 100% whereas survival in ivermectin and fenbendazole groups was 97 and 91%, respectively. The first worms became mature 16 weeks after hatching, irrespective of dung type, and all worms were mature 24 weeks after hatching. The growth rate of the worms fed dung from cattle given ivermectin boluses was 2.6 mg higher day–1 than that recoded for the control group, whereas the growth rate of worms fed on dung from cattle given fenbendazole boluses did not differ significantly from the control group. It may be concluded that ivermectin, fenbendazole and their metabolites had no adverse effects on the survival and growth of L. terrestris when exposed through dung under laboratory conditions. © 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Lumbricus terrestris; Ivermectin; Fenbendazole; Sustained-release bolus; Growth; Dung
1. Introduction The effect of the broad-spectrum anthelmintic ivermectin on non-target dung-degrading insect fauna has been studied several times, e.g. [9,14,16,17,18]. Ivermectin and its metabolites are excreted in dung [3] in concentrations dependent on formulation and route of administration [5,14]. Ivermectin administered in a sustained-release bolus is potentially more harmful to dung-inhabiting fauna than ivermectin given topically or by injection. This is due to the extended period of drug release in the rumen and high concentrations of the parent drug in the dung [5,13,16,17].
* Corresponding author. Fax: +45-35-28-26-70. E-mail address: [email protected] (T.S. Svendsen).
The anthelmintic benzimidazole, fenbendazole is also formulated as a sustained-release bolus. Residues and metabolites of fenbendazole are also excreted in dung [12], but Strong et al. [16] found no toxic effects on dung-inhabiting insects in studies on dung from cattle given fenbendazole boluses. However, other benzimidazoles are used as fungicides and some of these compounds have negative effects on earthworms in toxicity tests [15]. Although earthworms play the major role in the disappearance of dung pats in north temperate countries like Denmark [6], studies on the effect of veterinary medicines on earthworms are scarce [4]. Reports are mainly concerned with short-term effects of residues and metabolites of ivermectin on earthworm numbers in the field, e.g. [9,14,17]. The few laboratory studies performed on earthworms have been set up with the epigeic earthworm Eisenia
© 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. PII: S 1 1 6 4 - 5 5 6 3 ( 0 2 ) 0 1 1 6 7 - 6
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T.S. Svendsen et al. / Eur. J. Soil Biol. 38 (2002) 319–322
fetida exposed to ivermectin mixed into soil [2,3]. However, E. fetida is normally not associated with cow dung and may therefore be of limited relevance. Furthermore, tests of drugs at concentrations occurring in the field, and exposure through ingestion of dung rather than by contact with contaminated soil are of more relevance in studies of the effects of veterinary medicines on earthworms. In the present work we study the effect, under laboratory conditions, of ivermectin, fenbendazole and their metabolites on survival and growth of the anecic earthworm Lumbricus terrestris fed on dung from cattle given bolus formulations of these drugs.
2. Materials and methods 2.1. Test substrate Artificial soil was prepared according to the OECD guideline for the testing of chemicals [11]; 10% sphagnum peat, 20% kaolin clay and 70% sand (particle size 0.3–0.6 mm). Tap water was added to maintain a moisture content of 25.2 ± 2.3% (wet mass ± SD) and pH was adjusted to 6.7 ± 0.3 by addition of calcium carbonate. 2.2. Dung In May 1999, 14 heifers (weighing 366 ± 24 kg) were given fenbendazole sustained-release boluses (12 g Panacurt bolus, Hoechst Roussel), and eight heifers (415 ± 26 kg) received ivermectin boluses (1.72 g Ivomect bolus, MSD Agvet). The two groups of heifers grazed on separate pastures. Dung from a third group of four grazing heifers (500 ± 66 kg) served as untreated control. Fresh dung pats from each group were collected from the pastures and their water content was adjusted 85–86% wet mass. The dung was stored at –18 °C and used from July to December 1999. In December 1999, a new batch of dung was collected from three groups of four stabled cattle each, fed new ensiled grass only. The three groups (weighing 181 ± 18 kg, 180 ±16 kg and 239 ± 32 kg) were given fenbendazole or ivermectin boluses, or remained untreated. The water content in the dung was 87–88% wet mass. This dung was used in the experiment from December 1999 to June 2000. 2.3. Culturing of L. terrestris Hatchlings were taken from cocoons produced in the laboratory from field collected mature L. terrestris that were held at 15 °C in artificial soil. Cocoons were kept in 12-well tissue culturing plates with moist filter paper and one cocoon in each well. The plates were placed at 15 °C and cocoons were inspected weekly until hatching.
2.4. Survival and growth Each hatchling was transferred to a 300 ml jar with 100 g of artificial soil. The hatchlings were randomly allocated to three groups until there was a total of 32 worms in each group. The hatchlings were fed 10 g of either untreated control dung or dung from fenbendazole or ivermectin treated heifers. The dung was placed on the soil surface and both dung and soil were renewed every 4 weeks when worms were weighed. After 8 weeks, the amount of soil was increased to 200 g and the worms were fed 25 g of dung for the next 8 weeks. Subsequently the amount of dung was raised to 50 g per 4 weeks until worms reached maturity. 2.4.1. Statistics The age of worms when first fully clitellated was compared between groups with a χ2-test. The mass of the control group at maturity was compared with corresponding values of the two treated groups by the GLM procedure in the SAS statistical software system, as were the mass and the growth rate of hatchlings.
3. Results The initial mean mass of hatchlings in the control, ivermectin and fenbendazole group were 0.056 ± 0.002 g, 0.058 ± 0.002 g and 0.059 ± 0.002 g, respectively. There were no significant differences between groups (P > 0.05). In all groups, the survivorship until maturity was high (Table 1). The first worms became mature (fully clitellated) after 16 weeks irrespective of dung type. The majority became fully clitellated after 20 weeks and some took 24 weeks, but this did not result in any significantly differences between groups (P > 0.05) (Table 1). The mean growth rate from hatching to maturity was significantly higher in the ivermectin group than in the control group (P < 0.05), whereas the latter did not differ significantly from the fenbendazole group (Table 1).
4. Discussion There was no direct toxic effect of either ivermectin or fenbendazole, or their metabolites in cattle dung on L. terrestris. The mean age and weight when the worms reached maturity were unaffected. The growth rate was slightly higher (2.6 mg day–1) when worms were fed on dung from cattle given ivermectin than on dung from untreated cattle (Table 1). However, the growth rates and the age of maturity recorded for all earthworm groups in the current study are intermediate between those observed in other studies of L. terrestris [1,7], suggesting that our rearing conditions were close to optimal.
T.S. Svendsen et al. / Eur. J. Soil Biol. 38 (2002) 319–322
321
Table 1 Mean growth rate, age and mass when first fully clitellated and mortality of L. terrestris fed on dung from untreated grazing cattle (control) or from grazing cattle given ivermectin or fenbendazole sustained-release boluses Age at maturity (weeks) 16 Dung treatment
Growth rate (mg day–1)
Control 29.5 Ivermectin 32.1 Fenbendazole 31.1
20
24
Dead
Number (% of total)
Mean mass ± SE
Number (% of total)
Mean mass ± SE
Number (% of total)
Mean mass ± SE
Number (% of total)
6 (19) 5 (16) 7 (22)
3.75 ± 0.19 3.32 ± 0.13 3.82 ± 0.10
20 (63) 23 (72) 14 (44)
4.26 ± 0.14 4.69 ± 0.12 4.45 ± 0.19
6 (19) 3 (9) 8 (25)
4.19 ± 0.26 5.11 ± 0.53 4.82 ± 0.20
0 1 (3) 3 (9)
Our results, which indicate that neither ivermectin nor fenbendazole have any adverse effects on the survival or growth rates of L. terrestris, agree with those of Madsen et al. [8] who found no effect on the weight of Aporrectodea longa and A. tuberculata fed on dung from cattle treated with a range of anthelmintics, including ivermectin and fenbendazole, under semi-field conditions. Gunn and Sadd [2] found a similar response of E. fetida at ivermectin concentrations up to 8 mg kg–1 soil, but reported reduced earthworm growth and increased mortality at higher drug concentrations. Halley et al. [3] found no correlation between ivermectin concentrations in soil and weight changes in E. fetida, but observed increased mortality at concentrations higher than 25 mg ivermectin kg–1 soil. In the present study, as in Madsen et al. [8], the concentrations of the drugs and their metabolites in the dung were not known. We used 1.72 g ivermectin boluses constructed to release 12 mg ivermectin per day and 12 g fenbendazole boluses releasing 67–103 mg fenbendazole per day [10]. Herd et al. [5] found ivermectin concentrations of 0.4–0.5 mg kg–1 dung (wet mass) from cows (weighing approx. 400 kg) treated with similar sustained-release ivermectin boluses, and that more than 80% of the daily bolus release of ivermectin was excreted in the dung. The concentration of fenbendazole in cow dung following sustained-release administration has not been reported. However, it seems likely that the concentration of the drugs and their metabolites in this study were much lower but more realistic than the concentrations tested by Gunn and Sadd [2] and Halley et al. [3]. Moreover, the effect of the drugs and their metabolites ingested by feeding on dung of treated livestock may be different to those elicited by exposure to pure drugs mixed into the soil. Different species of earthworms might also respond differently. In consequence, further studies involving a wider range of relevant earthworm species at drug concentration that are known to occur under field conditions seem highly desirable. From our study we conclude that ivermectin and fenbendazole and their metabolites in cow dung have no adverse effects on the survival and growth of the dungfeeding earthworm L. terrestris under laboratory conditions.
Acknowledgements We are grateful to Karen Freiesleben, Torben Olsen, Lise and Jørgen Due for providing cattle for this experiment. Thanks to Hanne L. Kristiansen and Hanne Rawat for technical assistance and to Keith Wardhaugh for comments on the manuscript.
References [1]
[2]
[3]
[4] [5]
[6]
[7]
[8]
[9]
K.R. Butt, J. Frederickson, R.M. Morris, The life cycle of the earthworm Lumbricus terrestris L. (Oligochaeta: Lumbricidae) in laboratory culture, Eur. J. Soil Biol. 30 (1994) 49–54. A. Gunn, J.W. Sadd, The effect of ivermectin on the survival, behaviour and cocoon production of the earthworm Eisenia fetida, Pedobiologia 38 (1994) 327–333. B.A. Halley, T.A. Jacob, A.Y.H. Lu, The environmental impact of the use of ivermectin: Environmental effects and fate, Chemosphere 18 (1989) 1543–1563. R. Herd, Endectocidal drugs: ecological risks and countermeasures, Int. J. Parasit. 25 (1995) 875–885. R.P. Herd, R.A. Sams, M. Ashcraft, Persistence of ivermectin in plasma and faeces following treatment of cows with ivermectin sustained-release, pour-on or injectable formulations, Int. J. Parasit. 26 (1996) 1087–1093. P. Holter, Effect of earthworms on the disappearance rate of cattle droppings, in: J.E. Satchell (Ed.), Earthworm Ecology, Chapman and Hall, London, 1983, pp. 49–57. A. Lofs-Holmin, Reproduction and growth of common arable land and pasture species of earthworms (Lumbricidae) in laboratory studies, Swedish J. Agric. Res. 13 (1982) 31–37. M. Madsen, J. Grønvold, P. Nansen, P. Holter, Effects of treatment of cattle with some anthelmintics on the subsequent degradation of their dung, Acta vet. Scand. 29 (1988) 515–517. M. Madsen, B. Overgaard Nielsen, P. Holter, O.C. Pedersen, J. Brøchner Jespersen, K.M. Vagn Jensen, P. Nansen, J. Grønvold, Treating cattle with ivermectin: Effects on the fauna and decomposition of dung pats, J. Appl. Ecol. 27 (1990) 1–15.
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