Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-11T05:28:36.122Z Has data issue: false hasContentIssue false
  • English
  • Français

Toxicological effect of ivermectin on the survival, reproduction, and feeding activity of four species of dung beetles (Coleoptera: Scarabaeidae and Geotrupidae) in Japan

Published online by Cambridge University Press:  13 June 2019

I. Ishikawa  and
M. Iwasa
I. Ishikawa*
Affiliation:
Laboratory of Entomology, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
M. Iwasa
Affiliation:
Laboratory of Entomology, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
*
*Author for correspondence Phone: +81 080 5389 0019 Fax: +81 155 49 5492 E-mail: s26277@st.obihiro.ac.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

We investigated the effects of the antiparasitic drug ivermectin on the dung beetles Copris acutidens Motschulsky, Onthophagus bivertex Heyden, O. lenzii Harold and Phelotrupes auratus auratus Motschulsky in Japan. Ivermectin was detected in cattle dung from 1 to 3 or 7 days post-treatment, with a peak at 3 days post-treatment in two pour-on administrations (500 µg kg−1). In C. acutidens, adult survivals and numbers of brood balls were significantly reduced in dung collected at 3 and 7 days post-treatment, and adult emergence rates were significantly decreased in dung collected at 7 and 14 days post-treatment. Feeding activity of C. acutidens was inhibited in dung collected at 3 days post-treatment, but was not significantly different from that seen in control dung at 7 and 14 days post-treatment. In O. bivertex and O. lenzii, there were no effects of ivermectin on adult survival or feeding activities, but the numbers of brood balls of O. bivertex constructed in dung collected at 3 and 7 days post-treatment were significantly lower than observed with control dung. The adult emergence rates of O. bivertex and O. lenzii were significantly reduced in dung collected at 1 to 3 and 1 to 7 days post-treatment, respectively. In P. auratus, there were no effects of ivermectin on adult survival, oviposition, feeding activity, or larval survival (until the third instar) in dung at 3 days post-treatment. The environmental risks affecting the populations of dung beetles in Japan are discussed.

Keywords

IvermectinCoprisOnthophagusPhelotrupesJapanecotoxicity
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 1 , February 2020 , pp. 106 - 114
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adler, N., Bachmann, J., Blanckenhorn, W.U., Floate, K.D., Jensen, J. & Römbke, J. (2016) Effects of ivermectin application on the diversity and function of dung and soil fauna: regulatory and scientific background information. Environmental Toxicology and Chemistry 35, 1914–1923.Google Scholar
Bang, H.S., Lee, J.H., Kwon, O.S., Na, Y.E., Jang, Y.S. & Kim, W.H. (2005) Effects of paracoprid dung beetles (Coleoptera: Scarabaeidae) on the growth of pasture herbage and on the underlying soil. Applied Soil Ecology 29, 165–171.Google Scholar
Benz, G.W. (1985) Animal health applications of ivermectin. Southwestern Entomologist 7, 2–10.Google Scholar
Bornemissza, G.E. (1970) Insectary studies on the control of dung breeding flies by the activity of the dung beetle, Onthophagus gazella F. (Coleoptera: Scarabaeinae). Australian Journal of Entomology 9, 31–41.Google Scholar
Byford, R.L., Craig, M.E. & Crosby, B.L. (1992) A review of ectoparacites and their effect on cattle production. Journal of Animal Science 70, 597–602.Google Scholar
Campbell, W.C., Fisher, M.H., Stapley, E.O., Albers-Schönberg, G. & Jacob, T.A. (1983) Ivermectin: a potent new antiparasitic agent. Science 221, 823–828.Google Scholar
Dadour, I.R., Cook, D.F. & Neesam, C. (1999) Dispersal of dung containing ivermectin in the field by Onthophagus taurus (Coleoptera: Scarabaeidae). Bulletin of Entomological Research 89, 119–123.Google Scholar
Dadour, I.R., Cook, D. & Hennessy, D. (2000) Reproduction and survival of the dung beetle Onthophagus binodis (Coleoptera: Scarabaeidae) exposed to abamectin and doramectin residues in cattle dung. Environmental Entomology 29, 1116–1122.Google Scholar
Drummond, R.O. (1985) Effectiveness of ivermectin for control of arthropod pests of livestock. Southwestern Entomologist 7, 34–42.Google Scholar
Errouissi, F., Alvinerie, M., Galtier, P., Kerboeuf, D. & Lumaret, J.P. (2001) The negative effects of the residues of ivermectin in cattle dung using a sustained-release bolus on Aphodius constans (Duft.) (Coleoptera: Aphodiidae). Veterinary Research 32, 421–427.Google Scholar
Fincher, G.T. (1992) Injectable ivermectin for cattle: effects on some dung-inhabiting insects. Environmental Entomology 21, 871–876.Google Scholar
Floate, K.D. (1998) Off-target effects of ivermectin on insects and on degradation in southern Alberta, Canada. Bulletin of Entomological Research 88, 25–35.Google Scholar
Floate, K.D., Spooner, R.W. & Colwell, D.D. (2001) Larvicidal activity of endectocides against pest flies in the dung of treated cattle. Medical and Veterinary Entomology 15, 117–120.Google Scholar
Floate, K.D., Wardhaugh, K.G., Boxall, A.B.A. & Scherratt, T.N. (2005) Fecal residues of veterinary parasiticides: nontarget effects in the pasture environment. Annual Review of Entomology 50, 153–179.Google Scholar
Geary, T.G. & Moreno, Y. (2012) Macrocyclic lactone anthelmintics: spectrum of activity and mechanism of action. Current Pharmaceutical Biotechnology 13, 866–872.Google Scholar
Hayakawa, H. (1981) A pasture-cleaning operation by means of dung beetles. The Insectarium 18, 14–23.Google Scholar
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. International Journal for Parasitology 26, 1087–1093.Google Scholar
Holter, P. & Sommer, C. (1993) Effects of ivermectin treatment on the attraction of dung beetles (Coleoptera: Scarabaeidae and Hydrophilidae) to cow pats. Bulletin of Entomological Research 83, 53–58.Google Scholar
Houlding, B., Ridsdill-Smith, T.J. & Bailey, W.J. (1991) Injectable abamectin causes a delay in scarabaeine dung beetle egg-laying in cattle dung. Australian Veterinary Journal 68, 185–186.Google Scholar
Imura, O. (2007) Diversity and functions of dung beetles in pasture. Japanese Society of Grassland Science 53, 47–51.Google Scholar
Iwasa, M., Nakamura, T., Fukaki, K. & Yamashita, N. (2005) Nontarget effects of ivermectin on coprophagous insects in Japan. Environmental Entomology 34, 1485–1492.Google Scholar
Iwasa, M., Maruo, T., Ueda, M. & Yamashita, N. (2007) Adverse effects of ivermectin on the dung beetles, Caccobius jessoensis Harold, and rare species, Copris ochus Motschulsky and Copris acutidens Motschulsky (Coleoptera: Scarabaeidae), in Japan. Bulletin of Entomological Research 97, 619–625.Google Scholar
Kawai, S., Hori, S., Kawahara, M. & Inagaki, M. (2005) Atlas of Japanese Scarabaeidae Vol. 1 coprophagous group. p. 189 in the Japanese society of Scarabaeoideans (Ed.) Roppon-Ashi Entomological Books, Tokyo.Google Scholar
Keane, J. & Avery, L. (2003) Mechanosensory inputs influence Caenorhabditis elegans pharyngeal activity via ivermectin sensitivity genes. Genetics 164, 153–162.Google Scholar
Krüger, K. & Scholtz, C.H. (1997) Lethal and sublethal effects of ivermectin on the dung-breeding beetles Euoniticellus intermedius (Reiche) and Onitis alexis Klug (Coleoptera, Scarabaeidae). Agriculture, Ecosystems, & Environment 61, 123–131.Google Scholar
Krüger, K. & Scholtz, C.H. (1998 a) Changes in the structure of dung insect communities after ivermectin usage in a grassland ecosystem. I. Impact of ivermectin under drought conditions. Acta Oecologica 19, 425–438.Google Scholar
Krüger, K. & Scholtz, C.H. (1998 b) Changes in the structure of dung insect communities after ivermectin usage in a grassland ecosystem. II. Impact of ivermectin under high rainfall. Acta Oecologica 19, 439–451.Google Scholar
Lumaret, J.P. (1996). Comparative effects of moxidectin 2% equine gel and ivermectin 1.87% equine gel on dung non-target fauna when used at the recommended dose in horse. American Cyanamid Company, Princeton, NJ. Report No. GASD. Cyanamid Websters Pty Ltd, Baulkham Hills, NSW (unpublished).Google Scholar
Lumaret, J.P., Galante, E., Lumbreras, C., Mena, J., Bertrand, M., Bernal, J.L., Cooper, J.F., Kadiri, N. & Crowe, D. (1993) Field effects of ivermectin residues on dung beetles. Journal of Applied Ecology 30, 428–436.Google Scholar
Lumaret, J.P., Errouissi, F., Floate, K., Römbke, J. & Wardhaugh, K (2012) A review on the toxicity and non-target effects of macrocyclic lactones in terrestrial and aquatic environment. Current Pharmaceutical Biotechnology 13, 1004–1060.Google Scholar
Madsen, M., Nielsen, B.O., Holter, P., Pedersen, O.C., Jespersen, J.B., Jensen, K.M.V., Nansen, P. & Grønvold, J. (1990) Treating cattle with ivermectin: effects on the fauna and decomposition of dung pats. Journal of Applied Ecology 27, 1–15.Google Scholar
Manning, P., Slade, E.M., Beynon, S.A. & Lewis, O.T. (2016) Functionally rich dung beetle assemblages are required to provide multiple ecosystem services. Agriculture, Ecosystems & Environment 218, 87–94.Google Scholar
Manning, P., Slade, E.M., Beynon, S.A. & Lewis, O.T. (2017) Effect of dung beetle species richness and chemical perturbation on multiple ecosystem functions. Ecological Entomology 42, 577–586.Google Scholar
Martínez, M.I., Lumaret, J.P., Ortiz Zayas, R. & Kadiri, N. (2016) The effects of sublethal and lethal doses of ivermectin on the reproductive physiology and larval development of the dung beetle Euoniticellus intermedius (Coleoptera: Scarabaeidae). The Canadian Entomologist 149, 461–472.Google Scholar
McCraken, D.I. (1993) The potential for avermectins to affect wildlife. Veterinary Parasitology 48, 273–280.Google Scholar
Miller, J.A., Kunz, S.E., Oehler, D.D. & Miller, R.W. (1981) Larvicidal activity of Merck MK-933, an avermectin against the horn fly, stable fly, and house fly. Journal of Economic Entomology 74, 608–611.Google Scholar
Nichols, E., Spector, S., Louzada, J., Larsen, T., Amezquita, S. & Favila, M.E. & Scarabaeinae Research Network (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetle. Biological Conservation 141, 1461–1474.Google Scholar
Ortiz, A.J., Cortez, V., Azzouz, A. & Verdú, J.R. (2017) Isolation and determination of ivermectin in post-mortem and in vivo tissues of dung beetles using a continuous solid phase extraction method followed by LC-ESI+-MS/MS. PLoS One 12, e0172202. doi: 10.1371/journal.pone.0172202.Google Scholar
Payne, L.D., Hicks, M.B. & Wehner, T.A. (1995) Determination of abamectin and/or ivermectin in cattle feces at low parts per billion levels using HPLC with fluorescence detection. Journal of Agricultural and Food Chemistry 43, 1233–1237.Google Scholar
Pérez-Cogollo, L.C., Rodríguez-Vivas, R.I., Delfín-González, H., Reyes-Novelo, E. & Ojeda-Chi, M.M. (2015) Lethal and sublethal effects of ivermectin on Onthophagus landolti (Coleoptera: Scarabaeidae). Environmental Entomology 44, 1634–1640.Google Scholar
Pérez-Cogollo, L.C., Rodríguez-Vivas, R.I., Reyes-Novelo, E., Delfín-González, H. & Muñoz-Rodríguez, D. (2017) Survival and reproduction of Onthophagus landolti (Coleoptera: Scarabaeidae) exposed to ivermectin residues in cattle dung. Bulletin of Entomological Research 107, 118–125.Google Scholar
R Development Core Team (2016) R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria. Available online at https://www/r-project.org.Google Scholar
Ridsdill-Smith, T.J. (1988) Survival and reproduction of Musca vetustissima Walker (Diptera: Muscidae) and a scarabaeine dung beetle in dung of cattle treated with avermectin B1. Journal of the Australian Entomological Society 27, 175–178.Google Scholar
Römbke, J., Coors, A., Fernández, Á.A., Förster, B., Fernández, C., Jensen, J., Lumaret, J.P., Cots, M.Á.P. & Liebig, M. (2010) Effects of the parasiticide ivermectin on the structure and function of dung and soil invertebrate communities in the field (Madrid, Spain). Applied Soil Ecology 45, 284–292.Google Scholar
Schröder, J. (1992) Chemical control of ticks on cattle. pp. 175–184 in Fivaz, B., Petnoy, T. & Horak, I. (Eds), Tick Vector Biology. Berlin, Heidelberg, Springer.Google Scholar
Sommer, C. & Nielsen, B.O. (1992) Larvae of the dung beetle Onthophagus gazella F. (Col., Scarabaeidae) exposed to lethal and sublethal ivermectin concentrations. Journal of Applied Entomology 114, 502–509.Google Scholar
Sommer, C., Grønvold, J., Holter, P., Madsen, M. & Nansen, P. (1993) Dung burial activity and development of ivermectin exposed Diastellopalpus quinquedens in a field experiment. Entomologia Experimentalis et Applicata 66, 83–89.Google Scholar
Steelman, C.D. (1976) Effects of external and internal arthropod parasites on domestic livestock production. Annual Review of Entomology 21, 155–178.Google Scholar
Verdú, J.R., Casas, J.L., Lobo, J.M. & Numa, C. (2010) Dung beetles eat acorn to increase their ovarian development and thermal tolerance. PLoS One 5, e10114. https://doi.org/10.1371/journal.pone.0010114.Google Scholar
Verdú, J.R., Cortez, V., Ortiz, A.J., González-Rodríguez, E., Martinez-Pinna, J., Lumaret, J.-P., Lobo, J.M., Numa, C. & Sánchez-Piñero, F. (2015) Low doses of ivermectin cause sensory and locomotor disorders in dung beetles. Scientific Reports 5, 13912. https://doi.org/10.1038/srep13912.Google Scholar
Verdú, J.R., Lobo, J.M., Sánchez-Piñero, F., Gallego, B., Numa, C., Lumaret, J.P., Cortez, V., Ortiz, A.J., Tonelli, M., García-Teba, J.P., Rey, A., Rodríguez, A. & Durán, J. (2018) Ivermectin residues disrupt dung beetle diversity, soil properties and ecosystem functioning: an interdisciplinary field study. Science of the Total Environment 618, 219–228.Google Scholar
Wall, R. & Strong, L. (1987) Environmental consequence of treating cattle with the antiparasitic drug ivermectin. Nature 327, 418–421.Google Scholar
Wardhaugh, K.G. & Rodriguez-Menendez, H. (1988) The effects of the antiparasitic drug, ivermectin, on the development and survival of the dung-breeding fly, Orthellia cornicina (F.) and the scarabaeine dung beetles, Copris hispanus L., Bubas bubalus (Oliver) and Onitis belial F. Journal of Applied Entomology 106, 381–389.Google Scholar
Wohde, M., Blanckenhorn, W.U., Floate, K.D., Lahr, J., Lumaret, J.-P., Römbke, J., Scheffczyk, A., Tixier, T. & Düring, R.A. (2016). Analysis and dissipation of the antiparasitic agent ivermectin in cattle dung under different field conditions. Environmental Toxicology and Chemistry 35, 1924–1933.Google Scholar
Yamashita, N., Yoshida, N., Watanabe, A. & Mikami, A. (2004) Effects of the anthelmintics on development of the dung degrading insects. Tohoku Agricultural Research 57, 119–120 (in Japanese).Google Scholar