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Trans-generational and within-generational effects of two macrocyclic lactones on tunneller and dweller dung beetles (Coleoptera: Scarabaeidae): a case study

Published online by Cambridge University Press:  08 August 2018

I. Martínez M. ,
N. Kadiri ,
Y. Gil Pérez  and
J.P. Lumaret
I. Martínez M.*
Affiliation:
Red de Ecoetología, Instituto de Ecología A. C., El Haya, 91070 Xalapa, Veracruz, Mexico
N. Kadiri
Affiliation:
Univ Paul Valéry Montpellier 3, Univ Montpellier, EPHE, CNRS, IRD, CEFE UMR 5175, laboratoire de Zoogéographie, F34000, Montpellier, France
Y. Gil Pérez
Affiliation:
Red de Ecoetología, Instituto de Ecología A. C., El Haya, 91070 Xalapa, Veracruz, Mexico
J.P. Lumaret
Affiliation:
Univ Paul Valéry Montpellier 3, Univ Montpellier, EPHE, CNRS, IRD, CEFE UMR 5175, laboratoire de Zoogéographie, F34000, Montpellier, France
*
1Corresponding author (e-mail: imelda.martinez@inecol.mx).
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Abstract

Two distinct experiments were carried out to assess the trans-generational and within-generational effects of the parasiticides ivermectin and moxidectin to dung beetles (Coleoptera: Scarabaeidae). In the first experiment, the fertility of Euoniticellus intermedius (Reiche) (Scarabaeinae) was assessed for individuals developing in dung containing 10 µg ivermectin/kg fresh dung, a residue concentration previously shown to be sublethal to larval development. Our results showed that the fertility of adults exposed to these residues as larvae was unaffected. In the second experiment, the fertility of Agrilinus constans (Duftschmid) (Aphodiinae) was determined after females were allowed to feed for three weeks on dung containing different concentrations of moxidectin residues (five concentrations ranging from 0.32–32.00 mg/kg dry dung). The fertility of females was not affected, regardless of the concentration to which they were exposed, even when they were exposed to high moxidectin residues that killed all the offspring. The combined findings of these two experiments emphasise that sublethal effects should be included in models that assess the nontarget effects of faecal residues to insects breeding in dung of livestock treated with veterinary medicinal products.

Résumé

Deux expériences distinctes ont été menées pour évaluer les effets trans- générationnels et inter-générationnels de l’ivermectine et la moxidectine sur les bousiers (Coleoptera: Scarabaeidae), des molécules largement utilisées dans les traitements antiparasitaires du bétail. Dans la première expérience, la fertilité d’Euoniticellus intermedius (Reiche) (Scarabaeinae) a été évaluée chez des individus se développant dans des excréments contenant 10 μg d’ivermectine / kg de bouse fraîche, une concentration de résidus précédemment démontrée comme étant sublétale pour le développement larvaire. Nos résultats ont montré que la fertilité des adultes exposés précédemment à ces résidus en tant que larves n'était pas affectée. Dans la deuxième expérience, la fertilité d’Agrilinus constans (Duftschmid) (Aphodiinae) a été déterminée après que les femelles aient été nourries pendant trois semaines avec de la bouse contenant différentes concentrations de résidus de moxidectine (cinq concentrations variant de 0,32 à 32,00 mg/kg de bouse, poids sec). Cette exposition des femelles à la moxidectine n’a pas affecté significativement leur fécondité, quelle qu’ait été le niveau de leur exposition, même à des teneurs élevées qui ont pu tuer toute leur progéniture. Les résultats combinés de ces deux expériences soulignent que les effets sublétaux devraient être inclus dans les modèles qui évaluent les effets non ciblés des résidus fécaux sur les insectes qui se reproduisent dans les déjections des animaux traités avec des médicaments vétérinaires.

Type
Behaviour & Ecology
Information
The Canadian Entomologist , Volume 150 , Issue 5 , October 2018 , pp. 610 - 621
Copyright
© Entomological Society of Canada 2018 

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References

Adler, N., Bachmann, J., and Römbke, J. 2013. New test strategy for dung beetles during the authorization process of parasiticides. Integrated Environmental Assessment and Management, 9: 524–530.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): 124–135.Google Scholar
Boxall, A.B.A., Fogg, L.A., Baird, D.J., Lewis, C., Telfer, T.C., Kolpin, D., et aal. 2006. Targeted monitoring study for veterinary medicines in the environment. Science report SC030183/SR. Environment Agency, Bristol, United Kingdom.Google Scholar
Cambefort, Y. and Hanski, I. 1991. Dung beetle population biology. In Dung beetle ecology. Edited by I. Hanski and Y. Cambefort. Princeton University Press, Princeton, New Jersey, United States of America. Pp. 36–50.Google Scholar
Chapman, J.L., Porsch, L., Vidaurre, R., Backhaus, T., Sinclair, C., Jones, G., and Boxall, A.B.A. 2017. Three methods for integration of environmental risk into the benefit-risk assessment of veterinary medicinal products. Science of the Total Environment, 605–606: 692–701.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 Biologia Tropical, 60: 333–345.Google Scholar
Doherty, W.M., Stewart, N.P., Cobb, R.M., and Keiran, P.J. 1994. In vitro comparison of the larvicidal activity of moxidectin and abamectin against Onthophagus gazella (F.) (Coleoptera: Scarabaeidae) and Haematobia irritans exigua De Meijere (Diptera: Muscidae). Journal of Australian Entomological Society, 33: 71–74.Google Scholar
Errouissi, F., Alvinerie, M., Galtier, P., Kerboeuf, D., and 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: effect of some dung inhabiting insects. Environmental Entomology, 21: 871–876.Google Scholar
Finney, D.J. 1971. Probit analysis. 3rd edition. Cambridge University Press, Cambridge, United Kingdom.Google Scholar
Floate, K.D. 2006. Endectocide use in cattle and fecal residues: environmental effects in Canada. Canadian Journal of Veterinary Research, 70: 1–10.Google Scholar
Floate, K.D. and Fox, A. 1999. Indirect effects of ivermectin residues across trophic levels: Musca domestica (Diptera: Muscidae) and Muscidifurax zaraptor (Hymenoptera: Pteromalidae). Bulletin of Entomological Research, 89: 225–229.Google Scholar
Fort Dodge Animal Health. 2001. Environmental assessment. Cydectin® (moxidectin) injectable solution for cattle. Fort Dodge Animal Health, Overland Park, Kansas, United States of America. Available from https://wayback.archive-it.org/7993/20170406081652/https://www.fda.gov/downloads/AnimalVeterinary/DevelopmentApprovalProcess/EnvironmentalAssessments/UCM303762.pdf [accessed 23 June 2018].Google Scholar
Gittings, T. and Giller, P.S. 1997. Life history traits and resource utilisation in an assemblage of north temperate Aphodius dung beetles (Coleoptera: Scarabaeidae). Ecography, 20: 55–66.Google Scholar
González Canga, A., Prieto, A.M.S., Liébana, M.J.D., Martínez, N.F., Vega, M.S., and Vieitez, J.J.G. 2009. The pharmacokinetics and metabolism of ivermectin in domestic animal species. The Veterinary Journal, 179: 25–37.Google Scholar
Halffter, G. and Edmonds, D.W. 1982. The nesting behavior of dung beetles (Scarabaeinae). An ecological and evolutive approach. Instituto de Ecología, Mexico City, Mexico.Google Scholar
Halley, B.A., Nessel, R.J., and Lu, A.Y.H. 1989. Environmental aspects of ivermectin usage in livestock: general considerations. In Ivermectin and abamectin. Edited by W.C. Campbell. Springer, New York, New York, United States of America. Pp. 162–172.Google Scholar
Hempel, H., Scheffczyk, A., Schallnass, H.J., Lumaret, J.P., Alvinerie, M., and Römbke, J. 2006. Toxicity of four veterinary parasiticides on larvae of the dung beetle Aphodius constans in the laboratory. Environmental Toxicology and Chemistry, 25: 3155–3163.Google Scholar
Herd, R.P., Sams, R.A., and 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 of Parasitology, 26: 1087–1093.Google Scholar
Iwasa, M., Maruo, T., Ueda, M., and 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
Iwasa, M., Suzuki, N., and Maruyama, M. 2008. Effects of moxidectin on coprophagous insects in cattle dung pats in Japan. Applied Entomology and Zoology, 43: 271–280.Google Scholar
Jacobs, C.T. and Scholtz, C.H. 2015. A review on the effect of macrocyclic lactones on dung dwelling insects: toxicity of macrocyclic lactones to dung beetles. Onderstepoort Journal of Veterinary Research, 82: 1–8.Google Scholar
Kadiri, N., Lumaret, J.P., and Janati-Idrissi, A. 1999. Lactones macrocycliques: leur impact sur la faune non-cible du pâturage. Annales de la Société entomologique de France (N.S.), 35(Supplement): 222–229.Google Scholar
Krüger, K. and 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
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. 278–292.Google Scholar
Lopez-Collado, J., Cruz-Rosales, M., Vilaboa-Arroniz, J., Martínez, M.I., and Gonzalez-Hernandez, H. 2017. Contribution of dung beetles to cattle productivity in the tropics: a stochastic-dynamic modeling approach. Agricultural Systems, 155: 78–87.Google Scholar
Lumaret, J.P. 1975. Etude des conditions de ponte et de développement larvaire d’Aphodius (Agrilinus) constans Duft dans la nature et au laboratoire. Vie et Milieu, Série C, 25: 267–282.Google Scholar
Lumaret, J.P. 1995. Desiccation rate of excrement: a selective pressure on dung beetles. In Time scales of biological responses to water constraints. The case of Mediterranean biota. Edited by J. Roy, J. Aronson, and F. Di Castri. SPB Academic Publishing, Amsterdam, The Netherlands. Pp. 105–118.Google Scholar
Lumaret, J.P. and Errouissi, F. 2002. Use of anthelmintics in herbivores and evaluation of risks for the non-target fauna of pastures. Veterinary Research, 33: 547–562.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: 1004–1060.Google Scholar
Manning, P., Beynon, S.A., and Lewis, O.T. 2017. Quantifying immediate and delayed effects of anthelmintic exposure on ecosystem functioning supported by a common dung beetle species. Public Library of Science One, 12: e0182730.Google Scholar
Martínez, M.I. 2001. La biologia reproductiva en Aphodiidae: síntesis de datos conocidos (Coleoptera). Bollettino della Società entomologica italiana, 133: 113–130.Google Scholar
Martínez, M.I., Lumaret, J.P., Ortiz-Zayas, R., and Kadiri, N. 2017. 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
McKellar, Q.A. and Gokbulut, C. 2012. Pharmacokinetic features of the antiparasitic macrocyclic lactones. Current Pharmaceutical Biotechnology, 13: 888–911.Google Scholar
Nervo, B., Caprio, E., Celi, L., Lonati, M., Lombardi, G. Falsone, G., et al. 2017. Ecological functions provided by dung beetles are interlinked across space and time: evidence from 15N isotope tracing. Ecology, 98: 433–446.Google Scholar
Nichols, E., Spector, S., Louzada, J., Larsen, T., Amezquita, S. Favila, M.E., et al. 2008. Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation, 141: 1461–1474.Google Scholar
Prichard, R., Ménez, C., and Lespine, A. 2012. Moxidectin and the avermectins: consanguinity but not identity. International Journal for Parasitology: Drugs and Drug Resistance, 2: 134–153.Google Scholar
Römbke, J., Hempel, H., Scheffczyk, A., Schallnass, H.-J., Alvinerie, M., and Lumaret, J.P. 2007. Environmental risk assessment of veterinary pharmaceuticals: development of standard laboratory test with the dung beetle Aphodius constans . Chemosphere, 70: 57–64.Google Scholar
Shapiro, S.S. and Wilk, M.B. 1965. An analysis of variance test for normality (complete samples). Biometrika, 52: 591–611.Google Scholar
Steel, J.W. 1993. Pharmacokinetics and metabolism of avermectins in livestock. Veterinary Parasitology, 48: 45–57.Google Scholar
Steel, J.W. 1998. Assessment of the effects of the macrocyclic lactone class of chemicals on dung beetles and dung degradation in Australia. In NRA special review of macrocyclic lactones. Edited by the National Registration Authority for Agricultural and Veterinary Chemicals, Canberra, Australia. Pp. 15–79.Google Scholar
Strong, L., Wall, R., Woolford, A., and Djeddour, D. 1996. The effect of faecally excreted ivermectin and fenbendazole on the insect colonisation of cattle dung following the oral administration of sustained-release boluses. Veterinary Parasitology, 62: 253–266.Google Scholar
Suárez, V.H., Lifschitz, A.L., Sallovitz, J.M., and Lanusse, C.E. 2009. Effects of faecal residues of moxidectin and doramectin on the activity of arthropods in cattle dung. Ecotoxicology and Environmental Safety, 72: 1551–1558.Google Scholar
ToxRat Solutions. 2015. ToxRat professional 3.2.1. Software for the statistical analysis of biotests. ToxRat Solutions GmbH, Alsdorf, Germany.Google Scholar
Verdú, J.R., Cortez, V., Ortiz, A.J., González-Rodríguez, E., Martinez-Pinna, J. Lumaret, J.P., et al. 2015. Low doses of ivermectin cause sensory and locomotor disorders in dung beetles. Scientific Reports, 5: 13912.Google Scholar
Verdú, J.R., Lobo, J.M., Sánchez-Piñero, F., Gallego, B., Numa, C. Lumaret, J.P., et al. 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
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: 273–280.Google Scholar
Wardhaugh, K.G., Mahon, R.J., Axelsen, A., Rowland, M.W., and Wanjura, W. 1993. Effects of ivermectin residues in sheep dung on the development and survival of the bush fly, Musca vetustissima Walker and a scarabaeine dung beetle, Euoniticellus fulvus Goeze. Veterinary Parasitology, 48: 139–157.Google Scholar
Wardhaugh, K.G. and Rodriguez-Menendez, H. 1988. The effects of the antiparasitic drug, ivermectin, on the development and survival of the dung-breeding fly, Orthelia cornicina (F.) and the scarabaeine dung beetles, Copris hispanus L., Bubas bubalus (Olivier) and Onitis belial (F). Journal of Applied Entomology, 106: 381–389.Google Scholar
Williams, D.A. 1971. A test for differences between treatments means when several dose levels are compared with a zero dose control. Biometrics, 27: 103–117.Google Scholar
Wratten, S.D., Mead-Briggs, M., Gettinby, G., Ericsson, G., and Baggott, D.G. 1993. An evaluation of the potential effects of ivermectin on the decomposition of cattle dung pats. The Veterinary Record, 133: 365–371.Google Scholar
Zulalian, J., Stout, S.J., daCunha, A.R., Garces, R.T., and Miller, P. 1994. Absorption, tissue distribution, metabolism and excretion of moxidectin in cattle. Journal of Agricultural and Food Chemistry, 42: 381–387.Google Scholar