Conditioned food aversion mediated by odour cue and microencapsulated levamisole to avoid predation by canids

  • Jorge TobajasEmail author
  • Pilar Gómez-Ramírez
  • Pedro María-Mojica
  • Isabel Navas
  • Antonio Juan García-Fernández
  • Pablo Ferreras
  • Rafael Mateo
Original Article


Worldwide, predators and humans are in conflict for resources such as game species or livestock, especially in the case of wild canids. One non-lethal method to reduce predation is conditioned food aversion (CFA), in which animals learn to avoid a food due to the illness after ingestion, caused by the addition of an undetected chemical compound. CFA can be enhanced by adding an artificial odour cue, in a process known as taste-potentiated odour aversion (TPOA). We tested CFA and TPOA with three experimental groups of penned dogs. Food was offered with a combination of microencapsulated levamisole + vanilla odour (ODO), microencapsulated levamisole (LEV), or plain food as a control. The aims were (a) to test whether dogs detected the microencapsulated levamisole, (b) to analyse the strength and extinction time of CFA induced by microencapsulated levamisole, and (c) to analyse the strength and extinction time of TPOA. Two-choice tests were carried out during 11 post-conditioning months, and two reinforcements with microencapsulated levamisole were performed during the first post-conditioning month. In the first post-conditioning test, ODO and LEV groups ate significantly less untreated food than control group. After reinforcement, the dogs in LEV group resumed eating the food. Three of four dogs in ODO group showed long-lasting CFA until the 11th month. These results show that TPOA could be used to induce odour aversion on canids and that the odour cue overshadows the slight bitter taste of microencapsulated levamisole. These results show TPOA as a promising tool to reduce predation by wild canids.


Learned aversion Conditioned taste aversion Dog Predation conflict Non-lethal predation control Wildlife management 



We thank Nuria García and José J. Cerón for the welfare and analytical support, respectively. Thanks to Josep Ramon Ticó from the Service of Development of Medicines (Pharmacy Faculty, University of Barcelona) for developing the levamisole microencapsulation. Thanks to the anonymous referees for improving the manuscript.

Funding information

This study is a result of CGL2013–40975-R project, from I + D + I National Plan funded by the Spanish Ministry of Economy and Competitiveness. Jorge Tobajas benefitted from a FPI PhD scholarship (BES-2014-068987) funded by the Spanish Ministry of Economy and Competitiveness.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Supplementary material

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ESM 1 (DOCX 26 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Instituto de Investigación en Recursos Cinegéticos (IREC)CSIC-UCLM-JCCMCiudad RealSpain
  2. 2.Toxicology Area, Department of Health Sciences, Faculty of VeterinaryUniversity of MurciaMurciaSpain
  3. 3.Toxicology and Risk Assessment Group, Biomedical Research Institute of Murcia (IMIB-Arrixaca)University of MurciaMurciaSpain

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