Bioaccumulation and Elimination of Ivermectin by Eisenia foetida (Savigny 1826) Earthworms
DOI:
https://doi.org/10.47672/ajes.1426Keywords:
Earthworms, Ivermectin, Vermicompost, Accumulation and Elimination, Environmental RiskAbstract
Purpose: Bovine and equine faeces are commonly used to produce vermicompost of Eisenia foetida earthworms as a soil fertility enhancer. In animal health, ivermectin (IVM) is frequently used for parasite control. However, IVM is eliminated mainly by faeces, which raises environmental concerns. Little is known about the transfer of IVM by the earthworms´ activity. In this work the accumulation of IVM in E. foetida worms cultured in vermicompost containing IVM and the ability of the worms to release IVM to a drug-free substrate were evaluated.
Methodology: The acute toxicity test (72 h) of IVM and two bioassays, accumulation (A) and elimination (B), with E. foetida earthworms were performed in the current work. In A, the vermicompost produced was a mixture of equine and bovine faeces, the latter added with IVM 3,000 ng/g. Worms and substrates were sampled between 1 and 28 days post treatment (dpt). In B, worms obtained at 28 dpt in A were transferred to a substrate without IVM and sampled between 1 and 14 days later. Samples of worms and substrates were analysed using High Performance Liquid Chromatography (HPLC).
Findings: There was no worm mortality in the toxicity test. In assay A, E. foetida worms bio-accumulated up to 26.8% of the IVM present in the substrate. When worms from assay A, were moved to IVM-free substrate, they released 84% of the bio-accumulated IVM during the first day.
Recommendations: This study highlights that IVM bio- accumulated by earthworms and releasing in residue-free substrates represents a contamination risk, especially in farms that are minimising the use of chemical compounds.
Downloads
References
Barbaran Cruz, S.J. (2017). Reducción de Cromo en suelos contaminados por agroquÃmicos utilizando lombrices de tierra (Eisenia foetida) en el Centro Poblado Huarabi- Canta. Dissertation, Universidad Csar Vallejo
Boxall, A.B.A., Fogg, L.A, Kay P., Blackwel1, P.A., Pemberton, E.J., Croxford, A. (2004). Veterinary Medicines in the Environment. In: Ware G W (ed) Reviews of Environmental Contamination and Toxicology Vol180, Springer-Verlag, New York, pp. 1-91
Boxall, A.B.A., Sherratt, T.N., Pudner, V., Pope, L. (2007). A screening level index for assessing the impacts of veterinary medicines on dung flies. Environ. Sci. Technol., Vol 41, pp 2630-2635
Brown, G.G., Feller, C., Blanchart, E., Deleporte, P., Chernyanskii, S. (2003). With Darwin, earthworms turn intelligent and become human friends. Pedobiologia. Vol. 47, pp 924-933
Cantón, C. Cantón, L., DomÃnguez, M.P., Moreno, L., Lanusse, C., Ãlvarez, L., Ceballos, L. (2018). Field trial assessment of ivermectin pharmacokinetics and efficacy against susceptible and resistant nematode populations in cattle. Vet Parasitol. Vol 30, (256), pp 43-49. doi: 10.1016/j.vetpar.2018.05.007. Epub 2018 May 15
Capleton, A.V., Courage, C., Rumsby, O., Holmes, P., Stutt, E., Boxal, A.B.A., Levy, L.S. (2006). Prioritising veterinary medicines according to their potential indirect human exposure and toxicity profile. Toxicol. Lett. Vol 16, pp 213-223
Carbonell-Martin, G., Pro-Gonzalez, J., Aragonese-Grunert, P., Babin- Vich, M.M., Fernandez-Torija, C., Tarazona-Lafarga, J.V. (2011). Targeting the environmental assessment of veterinary drugs with the multi-species-soil system (MS·3) agricultural soil microcosms: the ivermectin case study. Span J Agric Res Vol 9(2) pp 433-443
Cuevas DÃaz, M.C., Ferrera Cerrato, R., Roldán MartÃn, A., RodrÃguez Vázquez, R. (2008). Pruebas en suelos: Ensayo de toxicidad aguda con la lombriz de tierra Eisenia andrei. In: RamÃrez Romero, P.; Mendoza Cantú, A (ed) Ensayos toxicológicos para la evaluación de sustancias quÃmicas en agua y suelo. La experiencia en Mxico, Instituto Nacional de EcologÃa, SecretarÃa de Medio Ambiente y Recursos Naturales, Mxico, pp. 211-223
De Montigny, P., Shim, J.S.K., Pivnichny, J.V.(1990). Liquid chromatographic determination of ivermectin in animal plasma with trifluoroacetic anhydride and N-methylimidazole as the derivatization reagent. J. Pharm. Biomed. Anal Vol 8, pp 507-511
Floate, K.D. (2006). Endectocide use in cattle and fecal residues: environmental effects in Canada. Can J.Vet Res.Vol.70, pp1-10
Floate, K., Fox, A. (1999). Indirect effects of ivermectin residues across trophic levels: Musca domestica (Diptera: Muscidae) and Muscidifurax zaraptor (Hymenoptera: Pteromalidae). Bull Entomol Res, Vol 89, pp 225-229
Franke, C. (1996). How meaningful is the bioconcentration factor for risk assessment? Chemosphere, Vol 32 (10), pp 1897-1905
Franke, C., Studinger, G., Berger, G., Böhling, S., Bruckmann, U., Cohors-Fresenborg, D. Jiihncke, U. (1994). The assessment of bioaccumulation. Chemosphere, Vol 29 (7), pp 1501-1514
Gagliardi, K. (1984). La crÃa intensiva de lombrices. Ed del Autor, Buenos Aires
Garg, V.K., Chand, S., Chhillar, A., Yadav, A. (2005). Growth and reproduction of Eisenia foetida in various animal wastes during vermicomposting. Appl Ecol Environ Res, Vol 3(2), pp 51-59
Grønvold, J., Henriksen, S., Larsen, M., Nansen, P., Wolstrup, J. (1996). Biological control. Aspects of biological control with special reference to arthropods, protozoans and helminths of domesticated animals. Vet Par, Vol 64, pp 47-64
Harris, M.L., Wilson, L.K., Elliott, J.E., Bishop, C.A., Tomlin, A.D., Henning, K.V. (2000). Transfer of DDT and metabolites from fruit orchard soils to American Robins (Turdus migratorius) twenty years after agricultural use of DDT in Canada. Arch Environ Contam Toxicol, Vol 39, pp 205-220
Herd, R.P., Sams, R.A., Ashcraft, S.M. (1996). Persistence of ivermectin in plasma and faeces following treatment of cows with ivermectin sustained-release, pour-on or injectable formulations. Int J Parasitol, Vol 26 (10), pp 1087-1093
Herrero, M.A., Cha, V., Carbó, L.I., Cuatrin, A., Sardi, G.M., Romero, L. (2017). Eficiencia de uso del nitrógeno por forrajeras abonadas con estircol de bovinos lecheros en la región pampeana, Argentina. Revista RIA, Vol 43 (2), pp 135-143
Iglesias, L.E, Saumell, C.A., Fus, L.A., Lutzelschwab, C.M., Steffan, P.E., Fiel, C.A (2004). Patrón primaveral de colonización y permanencia de artrópodos en masas fecales de bovinos en la zona de Tandil, Argentina. Revista RIA, Vol 33(2), pp 85-100
Iglesias, L.E., Saumell, C.A., Fernández, A.S., Fus, L.A., Lifschitz, A.L., RodrÃguez, E.M. Steffan, P.E., Fiel, C.A. (2006). Environmental impact of ivermectin excreted by cattle treated in autumn on dung fauna and degradation of faeces on pasture. Parasitol Res, Vol 100, pp 93-102
Iglesias, L.E., Fus, L.A., Lifschitz, A.L., RodrÃguez, E.M., Sagüs, M.F., Saumell, .CA. (2011). Environmental monitoring of ivermectin excreted in spring climatic conditions by treated cattle on dung fauna and degradation of faeces on pasture. Parasitol Res,Vol 108, pp 1185-1191
Iglesias, L. Junco, M., Lifschitz, A., Sallovitz, J., Saumell, C. (2022). An Environmental Concern: Uptake of Ivermectin from Growing Substrate to Plant Species. Int J Sci Res (IJSR), Vol 11(1) pp1442-1451
Krogh, K.A., Søeborg, T., Brodin, B., Sørensen, B.H. (2008). Sorption and mobility of ivermectin in different soils. J Environ Qual, Vol 37, pp 2202-2211
Lavelle, P., Bignell, D., Lepage, M., Wolters, V., Roger, P., Ineson, P., Heal, O.W., Dhillon, S. (1997) .Soil function in a changing world: the role of invertebrate ecosystem engineers Eur J. Soil Biol, Vol 33, pp 159-193
Lifschitz, A. Virkel, G., Sallovitz, J., Sutra, J.F., Galtier, P., Alvinerie, M., Lanusse, C. (2000). Comparative distribution of ivermectin and doramectin to tissues of parasite location in cattle. Vet Parasitol, Vol 87, pp 327-338
Lifschitz, A., Virkel, G., Ballent, M., Sallovitz, J., Imperiale, F., Pis, A., Lanusse, C. (2007). Ivermectin (3.15%) long-acting formulations in cattle: absorption pattern and pharmacokinetic considerations. Vet Parasitol, Vol 147, pp 303-310
Lopez Gimenez, M.A. (2000). Transformación de desechos orgánicos contaminantes, por la lombriz (Eisenia foetida sav) y caracterización de su humus. Dissertation. Universidad Veracruzana
Lowe, C.N., Butt, K.R., Sherman, R.L. (2014). Current and Potential Benefits of Mass Earthworm Culture. In: J. Morales-Ramos, M. Guadalupe-Rojas, D.I. Shapirollan (ed) Mass Production of Beneficial Organisms - Invertebrates and Entomopathogens, Elsevier (Academic Press), Cambridge, USA, pp. 683-709
Marinussen, M.P.J.C., Sjoerd, E., van der Zee, A.T.M., de Haan, F.A.M. (1997). Cu accumulation in the earthworm Dendrobaena veneta in a heavy metal (Cu, Pb, Zn) contaminated site compared to Cu accumulation in laboratory experiments. Environ Pollut, Vol 92 (2), pp 227-233
OECD (1984). Earthworm, acute toxicity test, Test Guideline No. 207, Guidelines for the testing of chemicals, OECD, Paris
O'Hea, N.M., Kirwan, L., Finn, J.A. (2010). Experimental mixtures of dung fauna affect dung decomposition through complex effects of species interactions. Oikos, Vol 119, pp 1081-1088
Palafox Alejo, A, Hernández Romero, A.H., López Luna, J., Cuevas DÃaz, M.C. (2012). Evaluación de la toxicidad de los suelos mediante bioensayos con lombrices. In: Cuevas DÃaz, M. del Cm, Espinoza Reyes, G., Ilizaliturri Hernández, C.A., Mendoza Cantú, A. (ed) Mtodos ecotoxicológicos para evaluar suelos contaminados con hidrocarburos. SecretarÃa de Medio Ambiente y Recursos Naturales (Semarnat), Instituto Nacional de EcologÃa (INE) Universidad Veracruzana, pp. 47-85.
Römbke, J., Jänsch, S., Didden, W. (2005). The use of earthworms in ecological soil classification and assessment concepts Ecotox Environ Safe, Vol 62, pp 249-265
Saint-Denis, M., Narbonneb, J., Arnaud, C., Ribera, D. (2001). Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil: effects of lead acetate. Soil Biol Biochem, Vol 33, pp 395-404
San Miguel, A., Raveton, M., Lemprière, G., Ravanel, P. (2008). Phenylpyrazoles impact on Folsomia candida (Collembola). Soil Biol Biochem, Vol 40, pp 2351-2357
Spacie, A., Hamelink, J.L. (1985). Bioaccumulation. In: Rand G M and Petrocelli SR (ed) Fundamentals of Aquatic Toxicology. Hemisphere Publishing Corp, Washington DC, Chapter 17, pp 1052-1081
Sun, Y., Diao, X., Zhang, Q., Shen, J. (2005). Bioaccumulation and elimination of avermectin B1a in the earthworms (Eisenia fetida). Chemosphere, Vol 60, pp 699-704
Tixier, T., Lumaret, J.P., Sullivan, G.T. (2015). Contribution of the timing of the successive waves of insect colonisation to dung removal in a grazed agro-ecosystem. Eur J Soil Biol, Vol 69, pp 88-93
Tuerlinckx, S.M., Morselli, T.B.G.A., Ana Huber, A.C.K. (2015). Indução de ivermectina na hormese sobre Eisenia foetida durante a vermicompostagem de esterco bovino. Rev Bras de Eng Agricola e Ambient, Vol 19 (7), pp 698-704
Valiela, I. (1974). Composition, food webs and population limitation in dung arthropod communities during invasion and succession. The American Midland Naturalist, Vol 92(2), pp 370-385
Viswanathan, R. (1994). Earthworms and assessment of ecological impact of soil xenobiotics. Chemosphere, Vol 28 (2), pp 413-420
Zapata, I.C., MartÃnez, L., EstefanÃa Posada, E., González, M.E., Saldarriaga, J.F. (2016). Efectos de la lombriz roja californiana (Eisenia foetida), sobre el crecimiento de microorganismos en suelos contaminados con mercurio de Segovia, Antioquia. Cienc Ing Neogranad, Vol 27 (1), pp 77-90. http://dx.doi.org/10.18359/rcin.1
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 LucÃa E. Iglesias, Carlos A. Saumell, Milagros Junco, Juan M. Sallovitz, Adrián L. Lifschitz
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution (CC-BY) 4.0 License that allows others to share the work with an acknowledgment of the work's authorship and initial publication in this journal.
