Pair foraging degrades socially transmitted food preferences in rats

Abstract

Following presentation of a novel food odor on the breath of a conspecific, naïve rats will exhibit a preference for that food, a form of learning called social transmission of food preference (STFP). When tested in isolation, STFPs are robust, persisting for up to a month and overcoming prior aversions. This testing protocol, however, does not account for rats’ ecology. Rats and other rodents forage in small groups, rather than alone. We allowed rats to forage in pairs and found that, following social foraging, they no longer displayed a food preference, i.e., that STFPs degrade during social foraging. Non-foraging rats exposed to the same foods for the same amount of time in isolation maintained their preferences. We also examined whether individual differences between rats affect STFP. Neither boldness nor sociability predicted initial STFP strength, but bolder rats’ preferences degraded more following social foraging. Shyer rats were more likely to eat at the same time as their partner. By tracking rats’ interactions during social foraging, we show that they use complex rules to combine their own preferences with socially acquired information about foods in their environment. These results situate STFP within the behavioral ecology of foraging and suggest that individual traits and the interactions between them modulate how social learning is maintained, modified, or lost.

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References

  1. Barnett SA (1963) The rat: A study in behavior. Transaction Publishers, New York

    Google Scholar 

  2. Beauchamp G (2013) Social predation: how group living benefits predators and prey. Academic Press, London

    Google Scholar 

  3. Bourin M, Hascoët M (2003) The mouse light/dark box test. Eur J Pharmacol 463(1):55–65

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Choleris E, Kavaliers M (1999) Social learning in animals: sex differences and neurobiological analysis. Pharmacol Biochem Behav 64(4):767–776

    CAS  PubMed  Google Scholar 

  5. Conradt L, Roper TJ (2000) Activity synchrony and social cohesion: a fission-fusion model. Proc R Soc B 267(1458):2213–2218

    CAS  PubMed  Google Scholar 

  6. Countryman RA, Gold PE (2007) Rapid forgetting of social transmission of food preferences in aged rats: relationship to hippocampal CREB activation. Learn Mem 14(5):350–358

    PubMed  PubMed Central  Google Scholar 

  7. Crawley JN (1985) Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 9(1):37–44

    CAS  PubMed  Google Scholar 

  8. Dochtermann NA, Jenkins SH (2007) Behavioural syndromes in Merriam’s kangaroo rats (Dipodomys merriami): a test of competing hypotheses. Proc R Soc B 274(1623):2343–2349

    PubMed  Google Scholar 

  9. Eilam D, Golani I (1989) Home base behavior of rats (Rattus norvegicus) exploring a novel environment. Behav Brain Res 34(3):199–211

    CAS  PubMed  Google Scholar 

  10. Everitt BS (1981) A Monte Carlo investigation of the likelihood ratio test for the number of components in a mixture of normal distributions. Multivar Behav Res 16(2):171–180

    CAS  Google Scholar 

  11. Fonio E, Benjamini Y, Golani I (2012) Short and long term measures of anxiety exhibit opposite results. PLoS One 7(10):e48414

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Galef BG (1981) Development of olfactory control of feeding-site selection in rat pups. J Comp Physiol Psychol 95(4):615

    PubMed  Google Scholar 

  13. Galef BG Jr (1989) Enduring social enhancement of rats’ preferences for the palatable and the piquant. Appetite 13(2):81–92

    PubMed  Google Scholar 

  14. Galef BG (2002) Social learning of food preferences is rodents: rapid appetitive learning. Curr Protoc Neurosci 8(8):5D

    Google Scholar 

  15. Galef BG (2012) Social learning in rats: historical context and experimental findings. In: Zentall T, Wasserman E (eds) Oxford handbook of comparative cognition. Oxford University Press, Oxford, pp 803–818

    Google Scholar 

  16. Galef BG Jr, Clark MM (1971) Social factors in the poison avoidance and feeding behavior of wild and domesticated rat pups. J Comp Physiol Psychol 75:341–357

    PubMed  Google Scholar 

  17. Galef BG, Giraldeau LA (2001) Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim Behav 61(1):3–15

    PubMed  Google Scholar 

  18. Galef BG Jr, Iliffe CP (1994) Social enhancement of odor preference in rats: is there something special about odors associated with foods? J Comp Psychol 108:266–273

    PubMed  Google Scholar 

  19. Galef BG Jr, Whiskin EE (2001) Interaction of social and individual learning in food preferences of Norway rats. Anim Behav 62:41–46

    Google Scholar 

  20. Galef BG, Whiskin EE (2003) Socially transmitted food preferences can be used to study long-term memory in rats. Anim Learn Behav 31(2):160–164

    Google Scholar 

  21. Galef BG, Wigmore SW (1983) Transfer of information concerning distant foods: a laboratory investigation of the ‘information-centre’ hypothesis. Anim Behav 31(3):748–758

    Google Scholar 

  22. Galef BG, Kennett DJ, Wigmore SW (1984) Transfer of information concerning distant foods in rats: a robust phenomenon. Learn Behav 12(3):292–296

    Google Scholar 

  23. Galef BG Jr, Attenborough KS, Whiskin EE (1990a) Responses of observer rats to complex, diet-related signals emitted by demonstrator rats. J Comp Psychol 104:11–19

    PubMed  Google Scholar 

  24. Galef BG Jr, McQuoid LM, Whiskin EE (1990b) Further evidence that Norway rats do not socially transmit learned aversions to toxic baits. Anim Learn Behav 18:199–205

    Google Scholar 

  25. Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psych Bull 127(1):45

    CAS  Google Scholar 

  26. Harcourt JL, Ang TZ, Sweetman G, Johnstone RA, Manica A (2009) Leadership, personality and social feedback. Commun Integr Biol 2(4):335–336

    PubMed  PubMed Central  Google Scholar 

  27. Inglis IR, Shepherd DS, Smith P, Haynes PJ, Bull DS, Cowan DP, Whitehead D (1996) Foraging behaviour of wild rats (Rattus norvegicus) towards new foods and bait containers. Appl Anim Behav Sci 47(3–4):175–190

    Google Scholar 

  28. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford

    Google Scholar 

  29. Kurvers RH, Eijkelenkamp B, van Oers K, van Lith B, van Wieren SE, Ydenberg RC, Prins HH (2009) Personality differences explain leadership in barnacle geese. Anim Behav 78(2):447–453

    Google Scholar 

  30. Kurvers RH, van Oers K, Nolet BA, Jonker RM, van Wieren SE, Prins HH, Ydenberg RC (2010a) Personality predicts the use of social information. Ecol Lett 13(7):829–837

    PubMed  Google Scholar 

  31. Kurvers RHJM, Prins HHT, van Wieren SE, van Oers K, Nolet BA, Ydenberg RC (2010b) The effect of personality on social foraging: shy barnacle geese scrounge more. Proc R Soc B 277:601–608

    PubMed  Google Scholar 

  32. Marler P, Dufty A, Pickert R (1986) Vocal communication in the domestic chicken: II. Is a sender sensitive to the presence and nature of a receiver? Anim Behav 34:194–198

    Google Scholar 

  33. Montgomery KC (1955) The relation between fear induced by novel stimulation and exploratory drive. J Comp Physiol Psychol 48(4):254

    CAS  PubMed  Google Scholar 

  34. Moy SS, Nadler JJ, Perez A, Barbaro RP, Johns JM, Magnuson TR, Piven J, Crawley JN (2004) Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav 3(5):287–302

    CAS  PubMed  Google Scholar 

  35. Nakayama S, Johnstone RA, Manica A (2012) Temperament and hunger interact to determine the emergence of leaders in pairs of foraging fish. PLoS One 7(8):e43747

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Palanza P, Gioiosa L, Parmigiani S (2001) Social stress in mice: gender differences and effects of estrous cycle and social dominance. Physiol Behav 73:411–420

    CAS  PubMed  Google Scholar 

  37. Posadas-Andrews A, Roper TJ (1983) Social transmission of food-preferences in adult rats. Anim Behav 31(1):265–271

    Google Scholar 

  38. Real LA (1992) Information processing and the evolutionary ecology of cognitive architecture. Am Nat 140:S108–S145

    Google Scholar 

  39. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82(2):291–318

    PubMed  Google Scholar 

  40. Rook AJ, Penning PD (1991) Synchronisation of eating, ruminating and idling activity by grazing sheep. Appl Anim Behav Sci 32(2):157–166

    Google Scholar 

  41. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19(7):372–378

    PubMed  Google Scholar 

  42. Smotherman WP (1982) In utero chemosensory experience alters taste preferences and corticosterone responsiveness. Behav Neural Biol 36(1):61–68

    CAS  PubMed  Google Scholar 

  43. Steiniger F (1950) Beiträge zur soziologie und sonstigen biologie der wanderratte. Ethology 7(3):356–379

    Google Scholar 

  44. Ward AJ, Sumpter DJ, Couzin ID, Hart PJ, Krause J (2008) Quorum decision-making facilitates information transfer in fish shoals. Proc Nat Acad Sci 105(19):6948–6953

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Eden Kleinhandler, Mackenzie Schultz, and members of the Collective Cognition Lab for assistance in running the experiment, David White for helpful comments and discussion, and Kelley Putzu for animal care.

Funding

This work was supported by a National Science and Engineering Research Council of Canada (NSERC) Grant No. RGPIN-2016-06138 (to NM).

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Contributions

All authors designed the experiment. CD ran the experiment, CD and NM analyzed the data, and all authors wrote the manuscript.

Corresponding author

Correspondence to Chelsey C. Damphousse.

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Conflict of interest

Chelsey C. Damphousse declares that she has no conflict of interest. Diano F. Marrone declares that he has no conflict of interest. Noam Miller declares that he has no conflict of interest.

Statement on welfare of animals

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The procedures used followed the Canadian Council on Animal Care guidelines and were approved by the Wilfrid Laurier University Animal Care Committee.

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Damphousse, C.C., Marrone, D.F. & Miller, N. Pair foraging degrades socially transmitted food preferences in rats. Anim Cogn 22, 1027–1037 (2019). https://doi.org/10.1007/s10071-019-01294-x

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Keywords

  • Social transmission of food preference (STFP)
  • Foraging
  • Behavioral syndromes
  • Information sharing
  • Exploration
  • Rat