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.
Social transmission of food preference (STFP) Foraging Behavioral syndromes Information sharing Exploration Rat
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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.
All authors designed the experiment. CD ran the experiment, CD and NM analyzed the data, and all authors wrote the manuscript.
This work was supported by a National Science and Engineering Research Council of Canada (NSERC) Grant No. RGPIN-2016-06138 (to NM).
Compliance and ethical standards
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.
Choleris E, Kavaliers M (1999) Social learning in animals: sex differences and neurobiological analysis. Pharmacol Biochem Behav 64(4):767–776CrossRefGoogle Scholar
Conradt L, Roper TJ (2000) Activity synchrony and social cohesion: a fission-fusion model. Proc R Soc B 267(1458):2213–2218CrossRefGoogle Scholar
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):350–358CrossRefGoogle Scholar
Crawley JN (1985) Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 9(1):37–44CrossRefGoogle Scholar
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):2343–2349CrossRefGoogle Scholar
Eilam D, Golani I (1989) Home base behavior of rats (Rattus norvegicus) exploring a novel environment. Behav Brain Res 34(3):199–211CrossRefGoogle Scholar
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):171–180CrossRefGoogle Scholar
Fonio E, Benjamini Y, Golani I (2012) Short and long term measures of anxiety exhibit opposite results. PLoS One 7(10):e48414CrossRefGoogle Scholar
Galef BG (1981) Development of olfactory control of feeding-site selection in rat pups. J Comp Physiol Psychol 95(4):615CrossRefGoogle Scholar
Galef BG Jr (1989) Enduring social enhancement of rats’ preferences for the palatable and the piquant. Appetite 13(2):81–92CrossRefGoogle Scholar
Galef BG (2002) Social learning of food preferences is rodents: rapid appetitive learning. Curr Protoc Neurosci 8(8):5DGoogle Scholar
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 803–818Google Scholar
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 75:341–357CrossRefGoogle Scholar
Galef BG, Giraldeau LA (2001) Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim Behav 61(1):3–15CrossRefGoogle Scholar
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 108:266–273CrossRefGoogle Scholar
Galef BG Jr, Whiskin EE (2001) Interaction of social and individual learning in food preferences of Norway rats. Anim Behav 62:41–46CrossRefGoogle Scholar
Galef BG, Whiskin EE (2003) Socially transmitted food preferences can be used to study long-term memory in rats. Anim Learn Behav 31(2):160–164CrossRefGoogle Scholar
Galef BG, Wigmore SW (1983) Transfer of information concerning distant foods: a laboratory investigation of the ‘information-centre’ hypothesis. Anim Behav 31(3):748–758CrossRefGoogle Scholar
Galef BG, Kennett DJ, Wigmore SW (1984) Transfer of information concerning distant foods in rats: a robust phenomenon. Learn Behav 12(3):292–296CrossRefGoogle Scholar
Galef BG Jr, Attenborough KS, Whiskin EE (1990a) Responses of observer rats to complex, diet-related signals emitted by demonstrator rats. J Comp Psychol 104:11–19CrossRefGoogle Scholar
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 18:199–205CrossRefGoogle Scholar
Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psych Bull 127(1):45CrossRefGoogle Scholar
Harcourt JL, Ang TZ, Sweetman G, Johnstone RA, Manica A (2009) Leadership, personality and social feedback. Commun Integr Biol 2(4):335–336CrossRefGoogle Scholar
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):175–190CrossRefGoogle Scholar
Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
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):447–453CrossRefGoogle Scholar
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):829–837CrossRefGoogle Scholar
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 277:601–608CrossRefGoogle Scholar
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 34:194–198CrossRefGoogle Scholar
Montgomery KC (1955) The relation between fear induced by novel stimulation and exploratory drive. J Comp Physiol Psychol 48(4):254CrossRefGoogle Scholar
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):287–302CrossRefGoogle Scholar
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):e43747CrossRefGoogle Scholar
Palanza P, Gioiosa L, Parmigiani S (2001) Social stress in mice: gender differences and effects of estrous cycle and social dominance. Physiol Behav 73:411–420CrossRefGoogle Scholar
Posadas-Andrews A, Roper TJ (1983) Social transmission of food-preferences in adult rats. Anim Behav 31(1):265–271CrossRefGoogle Scholar
Real LA (1992) Information processing and the evolutionary ecology of cognitive architecture. Am Nat 140:S108–S145CrossRefGoogle Scholar
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82(2):291–318CrossRefGoogle Scholar
Rook AJ, Penning PD (1991) Synchronisation of eating, ruminating and idling activity by grazing sheep. Appl Anim Behav Sci 32(2):157–166CrossRefGoogle Scholar
Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19(7):372–378CrossRefGoogle Scholar
Smotherman WP (1982) In utero chemosensory experience alters taste preferences and corticosterone responsiveness. Behav Neural Biol 36(1):61–68CrossRefGoogle Scholar
Steiniger F (1950) Beiträge zur soziologie und sonstigen biologie der wanderratte. Ethology 7(3):356–379Google Scholar
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):6948–6953CrossRefGoogle Scholar