Conditioned food aversion mediated by odour cue and microencapsulated levamisole to avoid predation by canids
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.
KeywordsLearned 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.
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.
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.
- Batsell WR, Paschall GY (2009) Mechanisms of compound conditioning in flavor-aversion conditioning. In: Reilly S, Schachtman TR (eds) Conditioned taste aversion: behavioral and neural processes. Oxford University Press, Oxford, pp 159–178Google Scholar
- Conover MR (1989) Potential compounds for establishing conditioned food aversions in raccoons. Wildl Soc Bull 17:430–435Google Scholar
- Cowan DP, Reynolds JC, Gill EL (2000) Reducing predation through conditioned taste aversion. In: Gosling LM, Sutherland WJ (eds) Behaviour and conservation. Cambridge University Press, New York, pp 281–299Google Scholar
- European Commission (2007) Commission recommendation of 18 June 2007 on guidelines for the accommodation and care of animals used for experimental and other scientific purposes. Off J Eur Union L197:1–89Google Scholar
- Gokce HI, Gunes V, ERrdogan HM, Citil M, Akca A, Yuksek N (2004) The effects of levamisole poisoning on the haematological and biochemical parameters in dogs. Dtsch tierärztl Wschr 111:81–85Google Scholar
- Lindstrom MJ, Bates DM (1988) Newton-Raphson and EM algorithms for linear mixed effects models for repeated–measures data. J Am Stat Assoc 83:1014–1022Google Scholar
- R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria http://www.r-projectorg/. Accessed 22 May 2018
- Ray JC, Hunter L, Zigouris J (2005) Setting conservation and research priorities for larger African carnivores. WCS Working Paper No. 24. Wildlife Conservation Society, New YorkGoogle Scholar
- Rescorla RA, Wagne AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In: Black AH, Prokasy WF (eds) Classical conditioning II: current research and theories. Appleton-Century-Crofts, New York, pp 64–99Google Scholar
- Smith ME, Linnell JD, Odden J, Swenson JE (2000) Review of methods to reduce livestock depredation II. Aversive conditioning, deterrents and repellents. Acta Agric Scand A Anim Sci 50:304–315Google Scholar