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Revista de Biología Tropical ISSN: 0034-7744 ISSN: 2215-2075 Universidad de Costa Rica Rodríguez-Vivas, Roger Iván; Basto-Estrella, Gertrudis del Socorro; Reyes-Novelo, Enrique; Pérez-Cogollo, Luis Carlos; Arcila-Fuentes, William; Ojeda-Chi, Melina; Martínez-M., Imelda Onthophagus landolti and Canthon indigaceus chevrolati (Coleoptera: Scarabaeinae) are attracted to the feces of ivermectin-treated cattle in the Mexican tropics Revista de Biología Tropical, vol. 67, no. 1, 2019, pp. 254-265 Universidad de Costa Rica DOI: 10.15517/RBT.V67I1.32917 Available in: http://www.redalyc.org/articulo.oa?id=44962136021 How to cite Complete issue Scientific Information System Redalyc More information about this article Network of Scientific Journals from Latin America and the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Project academic non-profit, developed under the open access initiative Onthophagus landolti and Canthon indigaceus chevrolati (Coleoptera: Scarabaeinae) are attracted to the feces of ivermectin-treated cattle in the Mexican tropics Roger Iván Rodríguez-Vivas1, Gertrudis del Socorro Basto-Estrella1, Enrique Reyes-Novelo2, Luis Carlos Pérez-Cogollo3, William Arcila-Fuentes1, Melina Ojeda-Chi1 & Imelda Martínez-M.4 1. Facultad de Medicina Veterinaria and Zootecnia, Universidad Autónoma de Yucatán, Carretera Mérida-Xmatkuil Km. 15.5, 97100 Mérida, Yucatán, México; [email protected], [email protected], [email protected], [email protected] 2. Centro de Investigaciones Regionales “Dr Hideyo Noguchi”, Av. Itzaes No. 490 × 59, Col. Centro, 97000 Mérida, Yucatán, México; [email protected] 3. Departamento de Ciencias Pecuarias, Facultad de Medicina Veterinaria and Zootecnia, Universidad de Córdoba, Ciudad Universitaria, Carrera 6 No. 76-103, 354, Montería, Colombia; [email protected] 4. Instituto de Ecología A.C., Carretera Antigua a Coatepec 351, El Haya, 91070 Xalapa, Veracruz, México; [email protected] Received 09-IV-2018. Corrected 08-VIII-2018. Accepted 03-XII-2018. Abstract: Ivermectin (IVM) is widely used for parasite control in livestock in the tropics. Residual IVM in feces conserves its insecticide activity for weeks and can harm dung beetle (DB) species. Attraction to the feces of IVM-treated cattle was tested using the DB species Onthophagus landolti (Harold) and Canthon indigaceus chevrolati (Harold) as models. Experiments were done under controlled laboratory conditions, semi-controlled field conditions and uncontrolled field conditions. Olfactometers were used in the controlled and semi-controlled trials. The control treatment was baited IVM-free feces, and the experimental treatments were the feces of cattle treated with 1 % IVM (subcutaneous administration; single, 0.2 mg/kg bw dosage) and collected at 5, 14, 21 and 28 days post-treatment. The uncontrolled field trial involved pitfall traps baited with IVM-free feces or feces from IVM-treated cattle collected five days post-treatment. Under controlled and semi-controlled conditions, the feces of IVM-treated cattle (at 5, 14, 21 or 28 days post-treatment) attracted more O. landolti and C. i. chevrolati individuals than IVM-free feces (P < 0.05). The same response occurred under uncontrolled conditions. This clear attraction for IVM-containing cattle feces by the studied DB species highlights that incorrect IVM use may pose a risk to DB communities in cattle production systems. Key words: Ivermectin; cattle feces; dung beetles; attraction; controlled conditions; field conditions; olfactometer. Rodríguez-Vivas, R. I., Basto-Estrella, G. S., Reyes-Novelo, E., Pérez-Cogollo, L. C., Arcila- Fuentes, W., Ojeda-Chi, M. & Martínez-M., I. (2019). Onthophagus landolti and Canthon indigaceus chevrolati (Coleoptera: Scarabaeinae) are attracted to the feces of ivermectin- treated cattle in the Mexican tropics. Revista de Biología Tropical, 67(1), 254-265. In temperate and tropical areas of the nutrients into the soil, contributing to the main- world, dung beetles belonging to the subfamily tenance of grassland productivity, and control- Scarabaeinae (Floate, 2011) perform a large ling natural animal pests (Nichols et al., 2008). part of the dung removal from the ground. This Macrocyclic lactones (ML) are the most function accelerates the incorporation of dung widely used deparasitizing treatment in cattle 254 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(1): 254-265, March 2019 for control of endo- and ectoparasites (Rodrí- cattle system sustainability (Dadour, Cook, & guez-Vivas et al., 2010; Davey, Pound, Miller, Neesam, 1999; Lee & Wall, 2006; Steinfeld et & Klavons, 2010). Of the ML, ivermectin al., 2006). Indeed, the ecological services of (IVM) is currently the most popular compound DB species in cattle grassland ecosystems is in tropical cattle ranching (Rodríguez-Vivas so important they are used as a research taxon et al., 2010). Its high liposolubility, means 90 in applied biodiversity conservation research. % of the IVM applied in cattle is eliminated Scarabaeinae DB assemblages are trustworthy in the feces, with insecticide activity intact indicators of ecological disturbance and cli- (Rodríguez-Vivas et al., 2010). Maximum con- mate change (Nichols & Gardner, 2011). centration of excreted IVM occurs in feces pro- Many studies have addressed IVM’s lethal duced three days post-treatment (dpt), although and sublethal effects in different DB species in detectable concentrations remain in feces up response to ingesting the feces of treated ani- to 28 dpt (Pérez-Cogollo, Rodríguez-Vivas, mals. These effects may be exacerbated if the Reyes-Novelo, Delfín-González, & Muñoz- feces are more attractive to the beetles (Floate, Rodríguez, 2017). 2007; Errouissi & Lumaret, 2010). Some stud- Dung beetles (DB) use animal feces as ies involving field experiments using pitfall a resource in their feeding and reproduction traps have documented that, within the same cycles. Ingestion with IVM can cause lethal coprophagous insect community, IVM excreted and sublethal effects in DB (reduction of in feces can have an attraction effect on some DB egg production and larval development) taxa and a repellant effect on others (Lumaret (Errouissi & Lumaret, 2010; Webb, Beaumont, et al., 1993; Holter, Sommer, & Grønvold, Nager, & McCracken, 2010; Floate, 2011; Wall 1993a; Floate, 1998a; Sutton, Bennett, & Bate- & Beynon, 2012; Pérez-Cogollo, Rodríguez- man, 2014). Distinguishing which species in a Vivas, Delfín-González, Reyes-Novelo, & Oje- community experience attraction is important da-Chi, 2015; González-Tokman et al., 2017; because if these are the dominant species it Martínez, Lumaret, Ortiz Zayas, & Nassera can seriously impact excrement recycling in Kadiri, 2017a). Administration of IVM to live- ranching areas. stock herds in a region can lead to drastic Considering this situation and in an effort decreases in DB population densities and even to generate baseline data to contribute to reduction in the number of DB species (Mar- responsible ML management in cattle produc- tínez, Ramírez-Hernández, & Lumaret, 2017b; tion systems, the aims of the present study Verdú et al., 2017). This is especially the case were to use field and laboratory experiments if IVM treatment coincides with DB reproduc- to evaluate the attractive effect of feces from tion periods when stages more sensitive to IVM IVM-treated cattle to the DB species Onthoph- (e.g. eggs and larvae) can come into contact agus landolti (Harold, 1880) and Canthon with and/or consume feces containing IVM indigaceus chevrolati (Harold, 1868). residues (Errouissi & Lumaret, 2010; Basto- Estrella, Rodríguez-Vivas, Delfín-González, MATERIALS AND METHODS & Reyes-Novelo, 2014; Pérez-Cogollo et al., 2015; Martínez et al., 2017a). Study site: Due to their dominance in DB Reductions in DB species diversity and communities in the study region, the species O. population sizes can have long-term effects on landolti and C. indigaceus chevrolati were used the elimination processes of cattle feces from as models to measure feces attraction (Basto- the surface of grasses (Floate, Wardhaugh, Estrella, Rodríguez-Vivas, Delfín-González, & Boxall, & Sherratt, 2005; Verdú el al., 2017). Reyes-Novelo, 2012). Among other effects, this can reduce and even From January to August 2017 individuals delay grass growth, altering the ecological of these two species were collected direct- services of these insects, which are so vital to ly from cattle dung on a ranch in Tizimin Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(1): 254-265, March 2019 255 municipality, in the state of Yucatan, Mexico months prior to the experiment. Each was sub- (21°15’8.44’’ N - 88°6’ 4.65’’ W). The pro- cutaneously injected with 1 % IVM (Ivomec®, duction system was semi-intensive with the Merial, Lot 8D164/16, Exp. 05/2019) at the main feed grasses being Brachiaria brizantha manufacturer recommended dosage of 0.2 mg/ (Hochst. ex A. Rich.) and Panicum maximun kg (Rodríguez-Vivas et al., 2010). Then, the (Jacq.) (Simon BK & Jacobs SWL). Macrocy- animals moved to a semi-enclosed corral with a clic lactones had never been used for parasite cement floor. The floor was cleaned prior to the control at this ranch. cattle being placed there and every day during Regional climate was warm subhumid all the experiment period. Feces were collected with 1 000 mm average annual rainfall and on day 0 (control, prior to IVM treatment), 25.8 ºC annual average temperature (Orella- and then