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The effects of sublethal and lethal doses of ivermectin on the reproductive physiology and larval development of the dung beetle Euoniticellus intermedius (Coleoptera: Scarabaeidae)

Published online by Cambridge University Press:  10 April 2017

Imelda Martínez M.*
Affiliation:
Red de Ecoetología, Instituto de Ecología A. C., El Haya, 91070 Xalapa, Veracruz, Mexico
Jean-Pierre Lumaret
Affiliation:
Unité Mixte de Recherche (UMR) 5175 Centre d’Ecologie Fonctionnelle et Evolutive, Centre national de la recherche scientifique-Université de Montpellier-Université Paul-Valéry Montpellier III, Université Paul-Valéry, Laboratoire de Zoogéographie, 34199 Montpellier cedex 5, France
Rosario Ortiz Zayas
Affiliation:
Red de Ecoetología, Instituto de Ecología A. C., El Haya, 91070 Xalapa, Veracruz, Mexico
Nassera Kadiri
Affiliation:
Unité Mixte de Recherche (UMR) 5175 Centre d’Ecologie Fonctionnelle et Evolutive, Centre national de la recherche scientifique-Université de Montpellier-Université Paul-Valéry Montpellier III, Université Paul-Valéry, Laboratoire de Zoogéographie, 34199 Montpellier cedex 5, France
*
1Corresponding author (e-mail: imelda.martinez@inecol.mx)

Abstract

This study assesses the effects of the veterinary medical product ivermectin (IVM) in a range of concentrations on adult reproductive physiology and larval mortality of the dung beetle Euoniticellus intermedius (Reiche) (Coleoptera: Scarabaeidae). The ecotoxicological tests comprised eight treatments, including two controls and six increasing ivermectina concentrations (3.16, 10.0, 31.6, 63.2, 100, and 316 µg IVM/kg fresh dung). After 10 days of exposure, the females were dissected and the brood balls counted (fecundity). The brood balls were opened 15 days later and live larvae were counted to estimate larval mortality. Ivermectin altered the morphology of the ovary and stopped vitellogenesis, causing oocyte resorption and thus decreasing fecundity. The 30% threshold of decline in fecundity was reached at 115.9 µg IVM/kg dung, with no observed effect concentration (NOEC) and lowest observed effect concentration (LOEC) values of 10.0 and 31.6 µg IVM/kg dung, respectively. Larval sensitivity to ivermectin was higher, with a lethal concentration required to kill 50% of the population of 85.9 μg IVM/kg dung, and NOEC and LOEC of 3.16 and 10.0 µg IVM/kg dung, respectively. After cattle were treated with ivermectin at the recommended dose, the ivermectin concentration in their dung during the two first weeks after administration far exceeded the thresholds determined for E. intermedius.

Résumé

Les effets de l’ivermectine (IVM) sur la reproduction des femelles d’Euoniticellus intermedius (Reiche) (Coleoptera: Scarabaeidae) ont été évalués. La mortalité des larves a également été mesurée. Huit traitements ont été réalisés, soit deux témoins et six concentrations d’ivermectine (3,16 ; 10,0 ; 31,6 ; 63,2 ; 100 et 316 µg IVM/kg de bouse fraîche). Après 10 jours d’exposition, les femelles ont été disséquées et les pelotes fécales fabriquées ont été décomptées (fécondité). Ces boules ont été ouvertes 15 jours plus tard et les larves vivantes dénombrées (estimation de la mortalité larvaire). L’ivermectine modifie la morphologie de l’ovaire et interrompt la vitellogenèse, provoquant une résorption des ovocytes et une diminution de la fécondité. On observe 30% de baisse de fécondité à 115.9 µg IVM/kg bouse fraîche, aucun effet observable (NOEC) à 10,0 µg IVM et un début d’effet (LOEC) à 31,6 µg IVM/kg. Le seuil de sensibilité des larves est un peu plus élevé, avec une concentration létale de 50% (CL50) de 85,9 µg IVM/kg bouse fraîche et des valeurs de NOEC et LOEC de 3,16 et 10,0 µg IVM/kg, respectivement. Après le traitement du bétail, la concentration d’ivermectine dans les bouses dépasse largement les seuils établis ici pour E. intermedius.

Type
Behaviour & Ecology
Copyright
© Entomological Society of Canada 2017 

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Footnotes

Subject editor: Andrew Smith

References

Abbott, W.S. 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18: 265267.Google Scholar
Anderson, J.R., Merritt, R.W., and Loomis, E.C. 1984. The insect-free cattle dropping and its relationship to increased dung fouling of rangeland pastures. Journal of Economic Entomology, 77: 133141.Google Scholar
Beynon, S.A., Peck, M., Mann, D.J., and Lewis, O.T. 2012. Consequences of alternative and conventional endoparasite control in cattle for dung-associated invertebrates and ecosystem functioning. Agriculture, Ecosystems & Environment, 162: 3644.Google Scholar
Beynon, S.A., Wainwright, W.A., and Christie, M. 2015. The application of an ecosystem services framework to estimate the economic value of dung beetles to the U.K. cattle industry. Ecological Entomology, 40(Supplement 1): 124135.Google Scholar
Brownlee, D.J., Holden-Dye, L., and Walker, R.J. 1997. Actions of the anthelmintic ivermectin on the pharyngeal muscle of the parasitic nematode, Ascaris suum . Parasitology, 115: 553561.Google Scholar
Carne, P.B. 1951. Preservation techniques for scarabaeid and other insect larvae. Proceedings of the Linnean Society of New South Wales, 76: 2630.Google Scholar
Christensen, E.R. and Nyholm, N. 1984. Ecotoxicological assays with algae: Weibull dose response curves. Environmental Science & Technology, 18: 713718.Google Scholar
Cruz Rosales, M., Martínez, I.M., López-Collado, J., Vargas-Mendoza, M., González-Hernández, H., and Fajersson, P. 2012. Effect of ivermectin on the survival and fecundity of Euoniticellus intermedius (Coleoptera: Scarabaeidae). Revista de Biología Tropical International Journal of Tropical Biology, 60: 333345.Google Scholar
Edwards, P. 2007. Introduced dung beetles in Australia 1967–2007. Current status and future directions. Landcare Australia and The Orica Community Foundation,“Dung Beetles for Landcare Farming”, Sinnamon Park, Australia.Google Scholar
Fincher, G.T. 1986. Importation, colonization, and release of dung-burying scarabs. In Biological control of muscoid flies. Volume 61. Edited by R.S. Patterson and D.A. Rutz. Miscellaneous publications. Entomological Society of America, College Park, Maryland, United States of America. Pp. 6976.Google Scholar
Fincher, G.T. 1996. Ivermectin pour-on for cattle: effects on some dung inhabiting insects. Southwestern Entomologist, 21: 445450.Google Scholar
Floate, K.D., Wardhaugh, K.G., Boxall, A.B.A, and Sherratt, T.N. 2005. Faecal residues of veterinary pharmaceuticals: non-target effects in the pasture environment. Annual Review of Entomology, 50: 153179.Google Scholar
Flota-Bañuelos, C., López-Collado, J., Vargas-Mendoza, M., Fajersson, P., González-Hernández, H., and Martínez-M., I. 2012. Efecto de la ivermectina en la dinámica espacio-temporal de escarabajos estercoleros en Veracruz, México. Tropical and Subtropical Agroecosystems, 15: 227239.Google Scholar
Gardner, K., Meish, M., Meek, C.L., and Bivin, W.S. 1993. Effects of ivermectin in canine blood on Anopheles quadrimaculatus, Aedes albopictus and Culex salinarius . Journal of the American Mosquito Control Association, 9: 400402.Google Scholar
Halffter, G. and Edmonds, W.D. 1982. The nesting behavior of dung beetles (Scarabaeinae). An ecological and evolutive approach. Instituto de Ecología, Mexico City, Mexico.Google Scholar
Halffter, G. and Favila, M. 1993. The Scarabaeinae (Insecta: Coleoptera), an animal group for analysing, inventorying and monitoring biodiversity in tropical rainforest and modified landscapes. Biology International, 27: 1521.Google Scholar
Krüger, K. and Scholtz, C.H. 1997. Lethal and sub-lethal effects of ivermectin on the dung-breeding beetles Euoniticellus intermedius (Reiche) and Onitis alexis Klug (Coleoptera, Scarabaeidae). Agriculture, Ecosystems & Environment, 61: 123131.Google Scholar
Levene, H. 1960. Robust tests for equality of variances. In Contributions to probability and statistics: essays in honor of Harold Hotelling. Edited by I. Olkin, S.G. Ghurye, W. Hoeffding, W.G. Madow, and H.B. Mann. Stanford University Press, Palo Alto, California, United States of America. Pp 278292.Google Scholar
Lumaret, J.-P., Errouissi, F., Floate, K., Römbke, J., and Wardhaugh, K. 2012. A review on the toxicity and non-target effects of macrocyclic lactones in terrestrial and aquatic environments. Current Pharmaceutical Biotechnology, 13: 10041060.Google Scholar
Martin, R.J., Robertson, A.P., and Wolstenholme, A.J. 2002. Mode of action of the macrocyclic lactones. In Macrocyclic lactones in antiparasitic therapy. Edited by J. Vercruysse and R.S. Rew. Centre for Agriculture and Biosciences International Publishing, Wallingford, United Kingdom. Pp 125140.Google Scholar
Martínez, M.I. 1995. Observations on reproductive control in females of two species of Canthon Hoffmannsegg (Coleoptera: Scarabaeidae: Scarabaeinae). Bollettino Museo Regionale di Scienze Naturali Torino, 13: 327343.Google Scholar
Martínez, M.I. 2002. Técnicas básicas de anatomía microscópica y de morfometría para estudiar los insectos. Boletín de la Sociedad Entomológica Aragonesa, 30: 187195.Google Scholar
Martínez, M.I. and Caussanel, C. 1984. Modifications de la pars intercerebralis, corpora allata, gonades et comportement reproducteur chez Canthon cyanellus (Coleoptera, Scarabaeinae). Comptes Rendus de l’Académie des Sciences de Paris 299, série III, 14: 597602.Google Scholar
Martínez, M.I. and Cruz, R.M. 1998. Effects of nourishment on the gonadal maturation in Canthon cyanellus cyanellus LeConte (Coleoptera Scarabeidae: Scarabaeinae). The Coleopterists Bulletin, 52: 237243.Google Scholar
Martínez, M.I. and Huerta, C.C. 1997. Coordinated activity of the ovary, pars intercerebralis and corpus allatum during the prenesting and nesting cycles of Copris incertus Say (Coleoptera Scarabaeidae: Scarabaeinae). The Coleopterists Bulletin, 51: 351363.Google Scholar
Montes de Oca, E. and Halffter, G. 1998. Invasion of Mexico by two dung beetles previously introduced into the United States. Studies on Neotropical Fauna and Environment, 33: 3745.Google Scholar
Nichols, E., Spector, S., Louzada, J., Larsen, T., Amezquita, S., and Favila, M.E. 2008. The Scarabaeinae research network. 2008. Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation, 141: 14611474.Google Scholar
Nunes Alves, S., Serrão, J.E., Mocelin, G., and Lane de Melo, A. 2004. Effect of ivermectin on the life cycle and larval fat body of Culex quinquefasciatus . Brazilian Archives of Biology and Technology, 47: 433439.Google Scholar
Organisation for Economic Co-operation and Development. 2010. Test No. 122: guidance document on the determination of the toxicity of a test chemical to the dung beetle Aphodius constans. Organisation for Economic Co-operation and Development Environment, Health and Safety Publications, Series on Testing and Assessment. ENV/JM/MONO (2010)13. Organisation for Economic Co-operation and Development Publishing, Paris. France.Google Scholar
Pérez-Cogollo, L.C., Rodríguez-Vivas, R.I., Delfín-González, H., Reyes-Novelo, E., and Ojeda-Chi, M.M. 2015. Lethal and sublethal effects of ivermectin on Onthophagus landolti (Coleoptera: Scarabaeidae). Environmental Entomology, 44: 16341640.Google Scholar
Robertson, J.G. 1961. Ovariole number in Coleoptera. Canadian Journal of Zoology, 39: 245263.Google Scholar
Robertson, J.L., Russell, R.M., Preisler, H.K., and Savin, E. 2007. Bioassays with arthropods, 2nd edition, CRC Press, Boca Raton, Florida, United States of America.Google Scholar
Römbke, J., Barrett, K., Blanckenhorn, W.U., Hargreaves, T., Kadiri, N., Knäbe, S., et al. 2010. Results of an international ring test with the dung fly Musca autumnalis in support of a new OECD test guideline. Science of the Total Environment, 408: 41024106.Google Scholar
Shapiro, S.S. and Wilk, M.B. 1965. An analysis of variance test for normality (complete samples). Biometrika, 52: 591611.Google Scholar
Solís, A. and Kohlmann, B. 2012. Checklist and distribution atlas of the Scarabaeinae (Coleoptera: Scarabaeidae) of Costa Rica. Zootaxa, 3482: 132.Google Scholar
Spector, S. 2006. Scarabaeine dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae): an invertebrate focal taxon for biodiversity research and conservation. The Coleopterists Bulletin, 60: 7183.Google Scholar
Toxrat Solutions. 2015. ToxRat Professional 3.2.1. Software for the statistical analysis of biotests. Toxrat Solutions, Alsdorf, Germany.Google Scholar
Turner, M.J. and Schaeffer, J.M. 1989. Mode of action of ivermectin. In Ivermectin and abamectin. Edited by W.C. Campbell. Springer-Verlag, New York, New York, United States of America. Pp 7378.Google Scholar
Vale, G.A. and Grant, I.F. 2002. Modelled impact of insecticide-contaminated dung on the abundance and distribution of dung fauna. Bulletin of Entomological Research, 92: 251263.Google Scholar
Verdú, J.R., Cortez, V., Ortiz, A.J., González-Rodríguez, E., Pinna, J.M., Lumaret, J.-P, et al. 2015. Low doses of ivermectin cause sensory and locomotor disorders in dung beetles. Scientific Report, 5: 110. https://doi.org/10.1038/srep13912.Google Scholar
Wardhaugh, K.G., Holter, P., and Longstaff, B. 2001. The development and survival of three species of coprophagous insect after feeding on the faeces of sheep treated with controlled-release formulations of ivermectin or albendazole. Australian Veterinary Journal, 79: 125132.Google Scholar
Wardhaugh, K.G., Longstaff, B.C., and Lacey, M.J. 1998. Effects of residues of deltamethrin in cattle faeces on the development and survival of three species of dung-breeding insect. Australian Veterinary Journal, 76: 273280.Google Scholar
Waterhouse, D.F. 1974. The biological control of dung. Scientific American, 230: 100109.Google Scholar
Williams, D.A. 1971. A test for differences between treatment means when several dose levels are compared with a zero dose control. Biometrics, 27: 103117.Google Scholar
Wohde, M., Blanckenhorn, W.U., Floate, K.D., Lahr, J., Lumaret, J.-P., Römbke, J., et al. 2016. Analysis and dissipation of the antiparasitic agent ivermectin in cattle dung under different field conditions. Environmental Toxicology and Chemistry, 35: 19241933. https://doi.org/10.1002/etc.3462.Google Scholar