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To eat or not to eat: a Garcia effect in pond snails (Lymnaea stagnalis)

Abstract

Taste aversion learning is universal. In animals, a single presentation of a novel food substance followed hours later by visceral illness causes animals to avoid that taste. This is known as bait-shyness or the Garcia effect. Humans demonstrate this by avoiding a certain food following the development of nausea after ingesting that food (‘Sauce Bearnaise effect’). Here, we show that the pond snail Lymnaea stagnalis is capable of the Garcia effect. A single ‘pairing’ of a novel taste, a carrot slurry followed hours later by a heat shock stressor (HS) is sufficient to suppress feeding response elicited by carrot for at least 24 h. Other food tastes are not suppressed. If snails had previously been exposed to carrot as their food source, the Garcia-like effect does not occur when carrot is ‘paired’ with the HS. The HS up-regulates two heat shock proteins (HSPs), HSP70 and HSP40. Blocking the up-regulation of the HSPs by a flavonoid, quercetin, before the heat shock, prevented the Garcia effect in the snails. Finally, we found that snails exhibit Garcia effect following a period of food deprivation but the long-term memory (LTM) phenotype can be observed only if the animals are tested in a food satiated state.

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Abbreviations

C:

Carrot slurry

CTA:

Conditioned taste aversion

HS:

Heat shock

HSP:

Heat shock protein

ISI:

Inter-stimulus intervals

LTM:

Long-term memory

PW:

Pond water

Q:

Quercetin

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Acknowledgements

We thank Diana Kagan and Bevin Wiley for discussions during the research. This research was supported by Regione Emilia-Romagna “L’invertebrato L. stagnalis quale modello per la Medicina Traslazionale” L.R. N. 20/2002 PROGETTI DI RICERCA SUI METODI ALTERNATIVI ALL'UTILIZZO DI ANIMALI; and FAR 2016 Department of Life Sciences, University of Modena and Reggio Emilia. Behavioural trials were performed in the University of Calgary and funding was provided by the Natural Sciences and Engineering Research Council of Canada (NSERC) to K.L.

Funding

This research was supported by Regione Emilia-Romagna “L’invertebrato L. stagnalis quale modello per la Medicina Traslazionale” L.R. N. 20/2002 PROGETTI DI RICERCA SUI METODI ALTERNATIVI ALL'UTILIZZO DI ANIMALI; and FAR 2016 Department of Life Sciences, University of Modena and Reggio Emilia. Behavioural trials were performed in the University of Calgary and funding was provided by the Natural Sciences and Engineering Research Council of Canada (NSERC) to K.L. These sources of funding had no involvement in the study design, data collection, analysis, and interpretation, writing of the report, or in the decision to submit the paper for publication.

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Conceptualization: VR, AB, KJ, MK and KL; methodology: VR, CB, and KL; data collection and analyses: VR and AB; writing—original draft: VR; writing—review and editing: AB and KL; funding acquisition: JMCB and KL; resources: JMCB and KL; supervision: KL.

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Correspondence to Ken Lukowiak.

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The authors have no conflict of interest.

Ethical approval

The pond snails used in our study, Lymnaea stagnalis are found in the Holarctic geographical region in abundant numbers and are neither an endangered nor a protected species. Experiments on pond snails are not subject to the approval of our respective animal ethics committees. Nonetheless, every effort was made to minimize the number of animals used ensuring adequate food, clean oxygenated water, and low-density conditions. The heat stress treatment used in our experiments has proven to have no long-term negative effects on the animals beyond the brief exposure period.

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Rivi, V., Batabyal, A., Juego, K. et al. To eat or not to eat: a Garcia effect in pond snails (Lymnaea stagnalis). J Comp Physiol A 207, 479–495 (2021). https://doi.org/10.1007/s00359-021-01491-5

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Keywords

  • Garcia effect
  • HSPs
  • Long-term memory
  • Taste aversion
  • Quercetin