Low doses of ivermectin cause sensory and locomotor disorders in dung beetles

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Verdú, José R ^a   Cortez, Vieyle ^a   Ortiz, Antonio J ^b   González Rodríguez, Estela ^a   Martinez Pinna, Juan ^a   Lumaret, Jean Pierre ^c   Lobo, Jorge M ^d   Numa, Catherine ^e   Sánchez Piñero, Francisco ^f  

^a UNIVERSITY OF ALICANTE   (Spain)

^b UNIVERSITY OF JAÉN   (Spain)

^c UNIV MONTPELLIER   (France)

^d MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^e UMR 5175 CEFE CNRS Université de Montpellier Université Paul Valéry Montpellier EPHE Université Paul Valéry Laboratoire Zoogéographie ^*  (Spain)

^f UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

INSECTICIDE; IVERMECTIN;

ANIMAL; ANIMAL BEHAVIOR; ANIMAL DISEASE; ANTENNA (ORGAN); BEETLE; CHEMICALLY INDUCED; DRUG EFFECTS; MUSCLE STRENGTH; NEUROMUSCULAR DISEASE; OLFACTORY BULB; PATHOPHYSIOLOGY; VETERINARY;

ANIMAL DISEASES; ANIMALS; ARTHROPOD ANTENNAE; BEETLES; BEHAVIOR, ANIMAL; INSECTICIDES; IVERMECTIN; MUSCLE STRENGTH; NEUROMUSCULAR DISEASES; OLFACTORY BULB;

EID: 84941308611     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13912     Document Type: Article

References (62)

1. Sutherland, I. H. and Campbell, W. C. Development, pharmacokinetics and mode of action of ivermectin. Act. Leidens 59, 161-168 (1990).
2. Fisher, M. H. and Mrozik, H. The chemistry and pharmacology of avermectins. Ann. Rev. Pharmacol. 32, 537-553 (1992).
3. Campbell, W. C. in Ivermectin and Abamectin (ed Campbell, W. C.) 245-259 (Springer-Verlag, 1989).
4. Benz, G. A. V., Roncalli, R. A. and Gross, S. J. in Ivermectin and Abamectin (ed Campbell, W. C.) 215-229 (Springer- Verlag, 1989).
5. Omura, S. Ivermectin: 25 years and still going strong. Int. J. Antimicrob. Ag. 31, 91-98 (2008).
6. Omura, S. and Crump, A. The life and times of ivermectin - a success story. Nat. Rev. Microbiol. 2, 984-988 (2004).
7. Albert, J., Lingle, D. H., Marder, E., ONeil, M. B. A GABA-activated chloride-conductance not blocked by picrotoxin on spiny lobster neuromuscular preparations. British J Pharmacol, 87, 771-779 (1986).
8. Duce, R. and Scott, R. H. Actions of dihydroavermectin B1a on insect muscle. Br. J. Pharmacol. 85, 395-401 (1985).
9. Keane, J. and Avery, L. Mechanosensory inputs influence Caenorhabditis elegans pharyngeal activity via ivermectin sensitivity genes. Genetics 164, 153-162 (2003).
10. Geary, T. G. and Moreno, Y. Macrocyclic Lactone Anthelmintics: Spectrum of Activity and Mechanism of Action. Curr. Pharm. Biotechnol. 13, 866-872 (2012).
11. Hoskins, S. G., Homberg, U., Kingan, T. G., Christensen, T. A. and Hildebrand, J. G. Immunocytochemistry of GABA in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res. 244, 243-252 (1986).
12. Schafer, S. and Bicker, G. Distribution of GABA-like immunoreactivity in the brain of the honeybee. J. Comp. Neurol. 246, 287-300 (1986).
13. Leitch, B. and Laurent, G. GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. J. Comp. Neurol. 372, 487-514 (1996).
14. Berg, B. G., Schachtner, J. and Homberg, U. γ -Aminobutyric acid immunostaining in the antennal lobe of the moth Heliothis virescens and its colocalization with neuropeptides. Cell. Tissue Res. 335, 593-605 (2009).
15. Pregitzer, P., Schultze, A., Raming, K., Breer, H. and Krieger, J. Expression of a GABAB - receptor in olfactory sensory neurons of sensilla trichodea on the male antenna of the moth Heliothis virescens. Int. J. Biol. Sci. 9, 707-715 (2013).
16. Puniamoorthy, N. Schafer, M. A., Rombke, J., Meier, R. and Blanckenhorn, W. U. Ivermectin sensitivity is an ancient trait affecting all Ecdysozoa but shows phylogenetic clustering among sepsid flies. Evol. Appl. doi: 10.1111/eva.12152 (2014).
17. Chiu, S.-H. L. and Lu, A. Y. H. in Ivermectin and Abamectin (ed Campbell, W. C.) 245-259 (Springer-Verlag, 1989).
18. McKellar, Q. A. and Gokbulut, C. Pharmacokinetic features of the antiparasitic macrocyclic lactones. Curr. Pharm. Biotechnol. 13, 888-911 (2012).
19. Floate, K. D., Wardhaugh, K. G., Boxall, A. B. A. and Sherratt, N. Faecal residues of veterinary parasiticides: non-target effects in the pasture environment. Ann. Rev. Entomol. 50, 153-179 (2005).
20. Kryger, U., Deschodt, C. and Scholtz, C. H. Effects of fluazuron and ivermectin treatment of cattle on the structure of dung beetle communities. Agric. Ecosys. Environ. 105, 649-656 (2005).
21. Lumaret, J. P., Errouissi, F., Floate, K., Rombke, J. and Wardhaugh, K. A Review on the Toxicity and Non-Target Effects of Macrocyclic Lactones in Terrestrial and Aquatic Environments. Curr. Pharm. Biotechnol. 13, 1004-1060 (2012).
22. Nichols, E. et al. Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biol. Conserv. 141, 1461-1474 (2008).
23. The Merck Veterinary Manual: Macrocyclic Lactones. Available at: http://www.merckmanuals.com/vet/pharmacology/ anthelmintics/macrocyclic-lactones.html/ (Accessed: 12th October 2014).
24. Wardhaugh, K. G. and Rodriguez-Menendez, H. 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). J. Appl. Entomol. 106, 381-389 (1988).
25. Wardhaugh, K. G., Mahon, R. J., Axelsen, A., Rowland, M. W. and Wanjura, W. 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. Vet. Parasitol. 48, 139-157 (1993).
26. Wardhaugh, K. G., Holter, P. and Longstaff, B. C. The development and survival of three species of coprophagous insect after feeding of the faeces of sheep treated with controlled-release formulations of ivermectin or albendazole. Aust. Vet. J. 79, 125-132 (2001).
27. Iwasa, M., Nakamura, T., Fukaki, K. and Yamashita, N. Non-target effects of ivermectin on coprophagous insects in Japan. Environ. Entomol. 35, 1485-1492 (2005).
28. Iwasa, M., Maruo, T., Ueda, M. and Yamashita, N. 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. Bull. Entomol. Res. 97, 619-625 (2007).
29. Lobl, I., Krell, F.-T. and Kral, D. in Catalogue of Palaearctic Coleoptera. Vol. 3. (eds Lobl, I. and Smetana, A.) 176-178 (Apollo Books, Stenstrup, Denmark, 2006).
30. Lobo, J. M. Decline of roller dung beetles (Scarabaeinae) populations in the Iberian Peninsula during the 20th century. Biol. Conserv. 97, 43-50 (2001).
31. Leclerc, J., Gaspar, C., Marchal, J. L., Verstraeten, C. and Wonville, C. Analyse des 1600 premieres cartes de lAtlas provisoire des insectes de Belgique, et premiere liste rouge dinsectes menace dans la faune belgue. Notes Fauniques Gembloux 4, 1-104 (1980).
32. Lumaret, J. P. and Kirk, A. A. in Dung Beetle Ecology (eds Hanski, I. and Cambefort, Y.) 97-115 (Princeton University Press, Oxford, UK, 1991).
33. Carpaneto, G. M., Mazziotta, A. and Valerio, L. Inferring species decline from collection records: roller dung beetles in Italy (Coleoptera, Scarabaeidae). Divers. Distrib. 13, 903-919 (2007).
34. Verdu, J. R., Alba-Tercedor, J. and Jimenez-Manrique, M. Evidence of different thermoregulatory mechanisms between two sympatric Scarabaeus species using infrared thermography and micro-computer tomography. PLoS ONE 7(3), e33914. doi: 10.1371/journal.pone.0033914 (2012).
35. Lobo, J. M., Sanmartin, I. and Martin-Piera, F. Diversity and spatial turnover of dung beetle (Coleoptera, Scarabaeoidea) communities in a protected area of south Europe (Donana National Park, Huelva, Spain). Elytron 11, 71-88 (1997).
36. Tribe, G. D., Burger, B. V. in Ecology and evolution of dung beetles (eds Simmons, L. W. and Ridsdill-Smith, T. J.) 87-106 (John Wiley and Sons, Ltd, Chichester, UK, 2011).
37. Pemberton, D. J., Franks, C. J., Walker, R. J. and Holden-Dye, L. Characterization of glutamate-gated chloride channels in the pharynx of wild-type and mutant Caenorhabditis elegans delineates the role of the subunit GluCl-α 2 in the function of the native receptor. Mol. Pharmacol. 59(5), 1037-1043 (2001).
38. Feng, X. P., Hayashi, J., Beech, R. N. and Prichard, R. K. Study of the nematode putative GABA type-A receptor subunits for modulation by ivermectin. J. Neurochem. 83(4), 870-878 (2002).
39. Geary, T. G. et al. Haemonchus contortus - ivermectin-induced paralysis of the pharynx. Exp. Parasitol. 77, 88-96 (1993).
40. Brownlee, D. J., Holden-Dye, L. and Walker, R. J. Actions of the anthelmintic ivermectin on the pharyngeal muscle of the parasitic nematode, Ascaris suum. Parasitol. 115, 553-561 (1997).
41. Consoli, R. A. G. B., Pereira, J. P., Silveira, J. N. and Castro, M. M. T. Suscetibilidade de adultos de Culex quinquefasciatus (Say) e Aedes fluviatilis (Lutz) (Diptera: Culicidae) a diversos inseticidas em laboratorio. Rev. Bras. Ent. 30, 79-85 (1986).
42. Tesh, R. B. and Guzman, H. Mortality and infertility in adult mosquitoes after the ingestion of blood containing ivermectin. Amer. J. Trop. Med. Hyg. 43, 229-233 (1990).
43. Gardner, K., Meish, M. V., Meek, C. L. and Bivin, W. S. Effects of ivermectin in canine blood on Anopheles quadrimaculatus, Aedes albopictus and Culex salinarius. J. Amer. Mosq. Control. Ass. 9, 400-402 (1993).
44. Panek, I., Meisner, S. and Torkkeli, P. H. Distribution and function of GABAB receptors in spider peripheral mechanosensilla. Neurophysiol. 90, 2571-2580 (2003).
45. Pfeiffer, K., Torkkeli, P. H. and French, A. S. Activation of GABAA receptors modulates all stages of mechanoreception in spider mechanosensory neurons. J Neurophysiol. 107, 196-204 (2013).
46. Lumaret, J.-P. et al. New screening test to predict the potential impact of ivermectin-contamined cattle dung on dung beetles. Vet. Res. 38, 15-24 (2007).
47. Lahr, J. et al. in SETAC Europe 24th Annual Meeting (ed. SETAC Europe) 235 (Basel, Switzerland, 2014).
48. Duce, I. R. and Scott, R. H. Actions of dihydroavermectin Bla on insect muscle. Br. J. Pharmacol. 85, 395-401 (1985).
49. Kane, N. S. et al. Drug-resistant Drosophila indicate glutamate-gated chloride channels are targets for the antiparasitics nodulisporic acid and ivermectin. P. Natl. Acad. Sci. USA 97, 13949-13954 (2000).
50. Keane, J. and Avery, L. Mechanosensory inputs influence Caenorhabditis elegans pharyngeal activity via ivermectin sensitivity genes. Genetics 164, 153-162 (2003).
51. Holden-Dye, L. and Walker, R. J. Actions of glutamate and ivermectin on the pharyngeal muscle of Ascaridia galli: a comparative study with Caenorhabditis elegans. Int. J. Parasitol. 36, 395-402 (2006).
52. Rohrer, S. P. et al. Identification of neuron-specific ivermectin binding sites in Drosophila melanogaster and Schistocerca americana. Insect Biochem. Molec. 25. 11-17 (1995
53. Errouissi, F., Alvinerie, M., Galtier, P., Kerboeuf, D. and Lumaret, J.-P. The negative effects of the residues of ivermectin in cattle dung using a sustained-release bolus on Aphodius constans (Duft.) (Coleoptera: Aphodiidae). Vet. Res. 32, 421-427 (2001).
54. Hempel, H. et al. Toxicity of four veterinary parasiticides on larvae of the dung beetle Aphodius constans in the laboratory. Environ. Toxicol. Chem. 25, 3155-3163 (2006).
55. Rombke, J. et al. Environmental risk assessment of veterinary pharmaceuticals: development of standard laboratory test with the dung beetle Aphodius constans. Chemosphere 70, 57-64 (2007).
56. Kruger, K. and Scholtz, C. H. Lethal and sublethal effects of ivermectin on the dung breeding beetles Euoniticellus intermedius (Reiche) and Onitis alexis Klug (Coleoptera, Scarabaeidae). Agric. Ecosys. Environ. 61, 123-131 (1997).
57. OHea, N., Kirwan, L., Giller, P. and Finn, J. Lethal and sub-lethal effects of ivermectin on north temperate dung beetles, Aphodius ater and Aphodius rufipes (Coleoptera: Scarabaeidae) Insect Conserv. Divers. 3, 24-33 (2010).
58. Edwards, P. B. in Workshop on the effects of parasiticides on dung beetles (eds Alexander, M. and Wardhaugh, K. G.) 12-13 (CSIRO Entomol. Tech. Rep. 89, 2001).
59. Lumaret, J.-P. Toxicite de certains helminthicides vis-a-vis des insectes coprophages et consequences sur la disparition des excrements de la surface du sol. Acta Oecol. Oecol. Appl. 7, 313-324 (1986).
60. Tyndale-Biscoe, M. Age-grading methods in adult insects: a review. Bull. Entomol. Res. 74, 341-377 (1984).
61. Min, S., Ai, M., Shin, S. A. and Suh, G. S. B. Dedicated olfactory neurons mediating attraction behavior to ammonia and amines in Drosophila. P. Natl. Acad. Sci. USA 110, 1321-1329 (2013).
62. Verdu, J. R. et al. Acorn preference by the dung beetle, Thorectes lusitanicus, under laboratory and field conditions. Anim. Behav. 74, 1697-1704 (2007).