Hostname: page-component-76dd75c94c-h9cmj Total loading time: 0 Render date: 2024-04-30T09:21:50.265Z Has data issue: false hasContentIssue false
  • English
  • Français

Survival and reproduction of Onthophagus landolti (Coleoptera: Scarabaeidae) exposed to ivermectin residues in cattle dung

Published online by Cambridge University Press:  09 September 2016

L.C. Pérez-Cogollo ,
R.I. Rodríguez-Vivas ,
E. Reyes-Novelo ,
H. Delfín-González  and
D. Muñoz-Rodríguez
L.C. Pérez-Cogollo
Affiliation:
Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Km. 15.5 carretera Mérida-Xmatkuil. C.P. 97100, Yucatán, México
R.I. Rodríguez-Vivas*
Affiliation:
Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Km. 15.5 carretera Mérida-Xmatkuil. C.P. 97100, Yucatán, México
E. Reyes-Novelo
Affiliation:
Centro de Investigaciones Regionales “Dr Hideyo Noguchi”. Av. Itzaes No. 490 × 59 Col. Centro. C.P. 97000, Yucatán, México
H. Delfín-González
Affiliation:
Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Km. 15.5 carretera Mérida-Xmatkuil. C.P. 97100, Yucatán, México
D. Muñoz-Rodríguez
Affiliation:
Facultad de Ingeniería Química, Universidad Autónoma de Yucatán, Periférico Norte Km. 33.5, Tablaje catastral 13615, Colonia Chuburná de Hidalgo Inn. C.P. 97203, Yucatán, México
*
*Address for correspondence Phone: +52 9999 42 32 00 Fax: +52 9999 42 32 05 E-mail: rvivas@correo.uady.mx
Get access Rights & Permissions [Opens in a new window]

Abstract

Two bioassays were conducted in parallel to assess the effects of cattle treated with either 1% ivermectin (IVM) or 3.15% IVM (dosed at 0.2 and 0.63 mg kg−1, respectively) on reproduction and survival of Onthophagus landolti Harold. Adult beetles were exposed 10 days to faeces of treated cattle starting at: one day before treatment (controls), 3, 6, 14, 28 and 35 days post-treatment. Adult survival of O. landolti was not affected by either of the two treatments. Faecal residues of 1% IVM almost completely suppressed fecundity of beetles at 3, 6 and 14 days post-treatment (dPT), and reduced fecundity of O. landolti at 28 dPT ( 38.3%), relative to controls. Meanwhile, IVM residues after treatment with 3.15% IVM almost completely suppressed fecundity of beetles at 3, 6, 14 and 28 dPT, and reduced fecundity of O. landolti at 35 dPT (80.9%), relative to controls. Larval survival was significantly reduced only at 3 dPT with 1% IVM. Meanwhile, treatment with 3.15% IVM significantly reduced larval survival at 6, 14 and 28 dPT. Larval mortality was recorded only in L-I and L-II instars. Moreover, in both bioassays, most of the L-I and L-II specimens that survived showed signs of toxicity. In conclusion, residual IVM in cattle faeces after treatment with injectable IVM has a detrimental effect on the fecundity of adult O. landolti up to 4 weeks post-treatment and on the subsequent larval survival.

Keywords

dung beetlemacrocyclic lactonetoxicity testnon-target effect
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 1 , February 2017 , pp. 118 - 125
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Alegria-Lopez, M.A., Rodriguez-Vivas, R.I., Torres-Acosta, J.F.J., Ojeda-Chi, M.M. & Rosado-Aguilar, J.A. (2015) Use of ivermectin as endoparasiticide in tropical cattle herds generates resistance in gastrointestinal nematodes and the tick Rhipicephalus microplus (Acari: Ixodidae). Journal of Medical Entomology 52, 214–221.Google Scholar
Alonso-Díaz, M.A., Arnaud-Ochoa, R.A., Becerra-Nava, R., Torres-Acosta, J.F.J., Rodriguez-Vivas, R.I. & Quiroz-Romero, R.H. (2015) Frequency of cattle farms with ivermectin resistant gastrointestinal nematodes in Veracruz, Mexico. Veterinary Parasitology 212, 439–443.CrossRefGoogle ScholarPubMed
Andresen, E. (2005) Effects of season and vegetation type on community organization of dung beetles in a tropical dry forest. Biotropica 37, 291–300.Google Scholar
Basto-Estrella, G., Rodríguez-Vivas, R.I., Delfín-González, H. & Reyes-Novelo, E. (2014) Dung beetle (Coleoptera: Scarabaeinae) diversity and seasonality in response to use of macrocyclic lactones at cattle ranches in the Mexican neotropics. Insect Conservation and Diversity 7, 73–81.Google Scholar
Blanckenhorn, W.U., Puniamoorthy, N., Schäfer, M.A., Scheffczyk, A. & Römbke, J. (2013) Standardized laboratory tests with 21 species of temperate and tropical sepsid flies confirm their suitability as bioassays of pharmaceutical residues (ivermectin) in cattle dung. Ecotoxicology and Environmental Safety 89, 21–28.Google Scholar
Bull, D.L., Ivie, G.W., MacConnell, J.G., Gruber, V.F., Ku, C.C., Arison, B.H., Stevenson, J.M. & VandenHeuvel, W.J. (1984) Fate of avermectin B1a in soil and plants. Journal of Agricultural and Food Chemistry 32, 94–102.Google Scholar
Canul-Ku, H.L., Rodriguez-Vivas, R.I., Torres-Acosta, J.F., Aguilar-Caballero, A.J., Perez-Cogollo, L.C. & Ojeda-Chi, M.M. (2012) Prevalence of cattle herds with ivermectin resistant nematodes in the hot sub-humid tropics of Mexico. Veterinary Parasitology 183, 292–298.Google Scholar
Cruz, B.C., Lopes, W.D.Z., Maciel, W.G., Felippelli, G., Fávero, F.C., Teixeira, W.F.P., Carvalho, R.S., Ruivo, M.A., Colli, M.H.A., Sakamoto Massamitsu, C.A., da Costa, A.J. & De Oliveira, G.P. (2015) Susceptibility of Rhipicephalus (Boophilus) microplus to ivermectin (200, 500 and 630 µg kg−1) in field studies in Brazil. Veterinary Parasitology 207, 309–317.Google Scholar
Dadour, I., 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.CrossRefGoogle Scholar
Davey, R.B., Pound, J.M., Miller, J.A. & Klavons, J.A. (2010) Therapeutic and persistent efficacy of a long-acting (LA) formulation of ivermectin against Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) and sera concentration through time in treated cattle. Veterinary Parasitology 169, 149–156.Google Scholar
Delgado, L. & Márquez, J. (2006) Estado del conocimiento y conservación de los coleópteros Scarabaoidea (Insecta) del estado de Hidalgo, México. Acta Zoológica Mexicana 22, 57–108.CrossRefGoogle Scholar
Escobar, F. (1997) Estudio de la comunidad de coleópteros coprófagos (Scarabaeidae) en un remanente de bosque seco al norte del Tolima, Colombia. Caldasia 19, 419–430.Google Scholar
Fernández, C., San Andres, M., Porcel, M.A., Rodriguez, C., Alonso, A. & Tarazona, J.V. (2009) Pharmacokinetic profile of ivermectin in cattle dung excretion, and its associated environmental hazard. Soil and Sediment Contamination 18, 564–575.CrossRefGoogle Scholar
Floate, K., Wardhaugh, K., Boxall, A.B.A. & Sherratt, T.N. (2005) Fecal residues of veterinary parasiticides: nontarget effects in the pasture environment. Annual Review of Entomology 50, 153–179.Google Scholar
González, C.A., Sahagún, P.A.M., Diez, L.M.J., Fernández, M.N., Sierra, V.M. & García’, V.J.J. (2009) The pharmacokinetics and metabolism of ivermectin in domestic animal species. Veterinary Journal 179, 25–37.Google Scholar
Halley, B.A., VandenHeuvel, W.J.A. & Wislocki, P.G. (1993) Environmental effects of the usage of avermectins in livestock. Veterinary Parasitology 48, 109–125.Google Scholar
Hempel, H., Scheffczyk, A., Schallnaß, H.-J., Lumaret, J.P., Alvinerie, M. & 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
Hernández, B., Maes, J.M., Harvey, C.A., Vílchez, S., Medina, A. & Sánchez, D. (2003) Abundancia y diversidad de escarabajos coprófagos y mariposas diurnas en un paisaje ganadero en el departamento de Rivas, Nicaragua. Agroforestería de las Américas 10, 93–102.Google Scholar
Holter, P. & Scholtz, C.H. (2007) What do dung beetles eat? Ecological Entomology 32, 690–697.CrossRefGoogle Scholar
Iwasa, M., Nakamura, T., Fukaki, K. & Yamashita, N. (2005) Nontarget effects of ivermectin on coprophagous insects in Japan. Environmental Entomology 34, 1485–1492.CrossRefGoogle 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
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 and Enviroment 61, 123–131.Google Scholar
Lanusse, C., Lifschitz, A., Virkel, G., Alvarez, L., Sánchez, S., Sutra, J.F., Galtier, P. & Alvinerie, M. (1997) Comparative plasma disposition kinetics of ivermectin, moxidectin and doramectin in cattle. Journal of Veterinary Pharmacology and Therapeutics 20, 91–99.CrossRefGoogle ScholarPubMed
Lifschitz, A., Virkel, G., Pis, A., Imperiale, F., Sánchez, S., Alvarez, L., Kujanek, R. & Lanusse, C. (1999) Ivermectin disposition kinetics after subcutaneous and intramuscular administration of an oilbased formulation to cattle. Veterinary Parasitology 86, 203–215.Google Scholar
Lifschitz, A., Virkel, G., Sallovitz, J., Sutra, J., Galtier, P., Alvinerie, M. & Lanusse, C. (2000) Comparative distribution of ivermectin and doramectin to parasite location tissues in cattle. Veterinary Parasitology 87, 327–338.Google Scholar
Lifschitz, A., Virkel, G., Ballent, M., Sallovitz, J.M., Imperiale, F., Pis, A. & Lanusse, C. (2007) Ivermectin (3.15%) long-acting formulations in cattle: absorption pattern and pharmacokinetic considerations. Veterinary Parasitology 147, 303–310.Google Scholar
Lumaret, J.P., Alvinerie, M., Hempel, H., ScallanaB, H.-J., Claret, D. & Römbke, J. (2007) New screening test to predict the potential impact of ivermectin-contaminated cattle dung on dung beetles. Veterinary Research 38, 15–24.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 environments. Current Pharmaceutical Biotechnology 13, 1004–1060.CrossRefGoogle ScholarPubMed
Neita-Moreno, J.C. & Morón, M.A. (2008) Estados inmaduros de Ancognatha ustulata (Coleoptera: Melolonthidae: Dynastinae: Cyclocephalini). Revista Mexicana de Biodiversidad 79, 355–361.Google Scholar
O'Hea, N.M., Kirwan, L., Giller, P.A. & Finn, J.A. (2010) Lethal and sub-lethal effects of ivermectin on north temperate dung beetles, Aphodius ater and Aphodius rufipes (Coleoptera: Scarabaeidae). Insect Conservation and Diversity 3, 24–33.CrossRefGoogle Scholar
Perez-Cogollo, L.C., Rodriguez-Vivas, R.I., Ramírez-Cruz, G.T. & Rosado-Aguilar, J.A. (2010) Survey of Rhipicephalus microplus resistance to ivermectin at cattle farms with history of macrocyclic lactones use in Yucatan, Mexico. Veterinary Parasitology 172, 109–113.Google Scholar
Pérez-Cogollo, L.C., Rodríguez-Vivas, R.I., Delfín-González, H., Reyes-Novelo, E. & Ojeda-Chi, M.M. (2015 a) 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., Delfín-González, H., Reyes-Novelo, E. & Morón, M.A. (2015 b) Life history of Onthophagus landolti Harold, 1880 (Coleoptera: Scarabaeidae), with descriptions of the preimaginal stages. Coleopterists Bulletin 69, 255–263.Google Scholar
Rodríguez-Vivas, R.I., Pérez-Cogollo, L.C., Rosado-Aguilar, J.A., Ojeda-Chi, M.M., Trinidad-Martinez, I., Miller, R.J., Li, A.Y., Pérez de León, A., Guerrero, F. & Klafke, G. (2014) Rhipicephalus (Boophilus) microplus resistant to acaricides and ivermectin in cattle farms of Mexico. Brazilian Journal of Veterinary Parasitology 23, 113–122.Google Scholar
SAS Institute. (2004) SAS/STAT 9.2 User’s Guide. SAS Instiute, Cary, NC.Google Scholar
Sommer, C. & Steffansen, B. (1993) Changes with time after treatment in the concentrations of ivermectin in fresh cow dung and in cow pats aged in the field. Veterinary Parasitology 48, 67–73.Google Scholar
Sommer, C., Grønvold, J., Holter, P. & Nansen, P. (1993) Effects of ivermectin on two afrotropical dung beetles, Onthophagus gazella and Diastellopalpus quinquedens (Coleoptera: Scarabaeidae). Veterinary Parasitology 48, 171–179.Google Scholar
Strong, L. & Wall, R. (1994) Effects of ivermectin and moxidectin on the insects of cattle dung. Bulletin of Entomological Research 84, 403–409w.CrossRefGoogle Scholar
Sun, Y., Diao, X., Zhang, Q. & Shen, J. (2005) Bioaccumulation and elimination of avermectin B1a in the earthworms (Eisenia fetida). Chemosphere 60, 699–704.CrossRefGoogle ScholarPubMed
Verdú, J.R., Moreno, C.E., Sánchez-Rojas, G., Numa, C., Galante, E. & Halffter, G. (2007) Grazing promotes dung beetle diversity in the xeric landscape of a Mexican Biosphere Reserve. Biological Conservation 140, 308–317.Google Scholar
Wardhaugh, K. & 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 (Oliver) and Onitis belial F. Journal of Applied Entomology 106, 381–389.Google Scholar
Wardhaugh, K., Mahon, R.J., Axelsen, A., Rowland, M.W. & Wanjura, W. (1993) Effects of ivermectin residues in sheep dung on the development and survival of the bushfly, Musca vetustissima Walker and a scarabaeine dung beetle, Euoniticellus fulvus Goeze. Veterinary Parasitology 48, 139–157.Google Scholar
Wardhaugh, K., Longstaff, B.C. & Morton, R. (2001) A comparison of the development and survival of the dung beetle, Onthophagus taurus (Schreb.) when fed on the faeces of cattle treated with pour-on formulations of eprinomectin or moxidectin. Veterinary Parasitology 99, 155–168.Google Scholar