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When deciding to cooperate by direct reciprocity, Norway rats sometimes benefit from olfactory competence and seem not impaired by insufficient cognitive abilities

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Abstract

Direct reciprocity requires the ability to recognize and memorize social partners, and to remember their previous actions. ‘Insufficient cognitive abilities’ have been assumed to potentially impair the ability to cooperate by direct reciprocity. Here we compare the propensity of rats to use direct reciprocity with their ability to memorize and recognize sensory cues in a non-social task. Female rats enriched in one of three sensory modalities (visual, olfactory or auditory) performed better in a learning task when they were tested with the specific sensory modality in which they have been enriched. For the cooperation test, during three subsequent reciprocity experiments the rats could provide two partners differing in their previous helpfulness with food. Individuals performing better in the non-social learning task that involved olfactory cues applied direct reciprocity more successfully in one experiment. However, in the experiment preventing visual cues and physical contact, rats applied direct reciprocity rules irrespective of their performance in the learning task with olfactory cues. This indicates that an enhanced olfactory recognition ability, despite being beneficial, is not a prerequisite for the rats’ ability to cooperate by direct reciprocity. This might suggest that when rats have all types of information about their social partner, individuals may apply other criteria than the reciprocity decision rule when determining how much help to provide, as for instance coercion. Interestingly, when all individuals are constrained to mostly rely on olfactory memory, individuals apply direct reciprocity independently of their ability to memorize olfactory cues in a non-social context. ‘Insufficient cognitive abilities’ may thus not be the true reason when direct reciprocity is not observed.

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References

  • Andrist CA (2008) Behavioural syndromes in Norway rats (Rattus norvegicus), Master thesis, University of Bern

  • Barnett SA (1957) An analysis of social behaviour in wild rats. Proc Zool Soc Lond 130:107–152

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.0-6. http://CRAN.R-project.org/package=lme4

  • Boeckle M, Bugnyar T (2012) Long-term memory for affiliates in ravens. Curr Biol 22:801–806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breen AJ, Lovie KE, Guerard C, Edwards SC, Cooper J, Healy SD, Guillette LM (2020) Juvenile socio-ecological environment shapes material technology in nest-building birds. Behav Ecol 31(4):892–901

    Article  Google Scholar 

  • Brown RE (1979) Mammalian social odors: a critical review. Adv Stud Behav 10:103–162

    Article  Google Scholar 

  • Brudzynski SM (2009) Communication of adult rats by ultrasonic vocalization: biological, sociobiological, and neuroscience approaches. ILAR J 50(1):43–50

    Article  CAS  PubMed  Google Scholar 

  • Brudzynski SM, Pniak A (2002) Social contacts and production of 50-kHz short ultrasonic calls in 584 adult rats. J Comp Psychol 116(1):73–82

    Article  PubMed  Google Scholar 

  • Burn CC (2008) What is it like to be a rat? Rat sensory perception and its implications for experimental design and rat welfare. Appl Anim Behav Sci 112:1–32

    Article  Google Scholar 

  • Cai R, Guo F, Zhang JP, Xu JH, Cui YL, Sun XD (2009) Environmental enrichment improves behavioral performance and auditory spatial representation of primary auditory cortical neurons in rat. Neurobiol Learn Mem 91:366–376

    Article  PubMed  Google Scholar 

  • Calhoun JB (1979) The ecology and sociobiology of the Norway rat. U.S. Dept. of Health, Education, and Welfare, Public Health Service, Bethesda

    Google Scholar 

  • Carter G (2014) The reciprocity controversy. Anim Behav Cogn 1(3):368–386

    Article  Google Scholar 

  • Carter GG, Wilkinson GS (2013) Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment. Proc R Soc B Biol Sci 280(1753):20122573

    Article  Google Scholar 

  • Carter GG, Wilkinson GS (2015) Social benefits of non-kin food sharing by female vampire bats. Proc R Soc B 282:20152524

    Article  PubMed  PubMed Central  Google Scholar 

  • Carter GG, Farine DR, Wilkinson GS (2017a) Social bet-hedging in vampire bats. Biol Lett 13(5):20170112

    Article  PubMed  PubMed Central  Google Scholar 

  • Carter GG, Wilkinson GS, Page RA (2017b) Food-sharing vampire bats are more nepotistic under conditions of perceived risk. Behav Ecol 28(2):565–569

    Article  Google Scholar 

  • Carter GG, Farine DR, Crisp RJ, Vrtilek JK, Ripperger SP, Page RA (2020) Development of new food-sharing relationships in vampire bats. Curr Biol 30(7):1275–1279

    Article  CAS  PubMed  Google Scholar 

  • Cheney DL (2011) Extent and limits of cooperation in animals. PNAS 108(suppl. 2):10902–10909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clutton-Brock T (2009) Cooperation between non-kin in animal societies. Nature 462:51–57

    Article  CAS  PubMed  Google Scholar 

  • Delmas GE, Lew SE, Zanutto BS (2019) High mutual cooperation rates in rats learning reciprocal altruism: The role of payoff matrix. PLoS ONE 14(1):e0204837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dolivo V, Taborsky M (2015a) Norway rats reciprocate help according to the quality of help they received. Biol Lett 11:20140959

    Article  PubMed  PubMed Central  Google Scholar 

  • Dolivo V, Taborsky M (2015b) Cooperation among Norway rats: the importance of visual cues for reciprocal cooperation and the role of coercion. Ethology 121:1071–1080

  • Dolivo V, Taborsky M (2017) Environmental enrichment of young adult rats (Rattus norvegicus) in different sensory modalities has long-lasting effects on their ability to learn via specific sensory channels. J Comp Psychol 131:79–88 https://doi.org/10.1037/com0000063

    Article  PubMed  Google Scholar 

  • Dolivo V, Rutte C, Taborsky M (2016) Ultimate and proximate mechanisms of reciprocal altruism in rats. Learn Behav 4:223–226 https://doi.org/10.3758/s13420-016-0236-z

    Article  Google Scholar 

  • Ducouret P, Romano A, Dreiss AN, Marmaroli P, Falourd X, Bincteux M, Roulin A (2020) Elder barn owl nestlings flexibly redistribute parental food according to siblings’ need or in return for allopreening. Am Nat 196(2):257–269

    Article  PubMed  Google Scholar 

  • Engelhardt SC, Taborsky M (2022) Food-exchanging Norway rats apply the direct reciprocity decision rule rather than copying by imitation. Anim Behav 194:265–274. https://doi.org/10.1016/j.anbehav.2022.09.005

    Article  Google Scholar 

  • Gerber N, Schweinfurth MK, Taborsky M (2020) The smell of cooperation: rats increase helpful behaviour when receiving odour cues of a conspecific performing a cooperative task. Proc R Soc B 287:20202327

    Article  PubMed  PubMed Central  Google Scholar 

  • Gfrerer N, Taborsky M (2017) Working dogs cooperate among one another by generalized reciprocity. Sci Rep 7(1):1–6

    Article  Google Scholar 

  • Gheusi G, Goodall G, Dantzer R (1997) Individually distinctive odours represent individual conspecifics in rats. Anim Behav 53:935–944

    Article  Google Scholar 

  • Hammerstein P, Noë R (2016) Biological trade and markets. Phil Trans R Soc B 371:20150101

    Article  PubMed  PubMed Central  Google Scholar 

  • Hammerstein P (2003) Genetic and cultural evolution of cooperation. Book series: Dahlem workshop reports: environmental sciences research report 83–93

  • Jeffery KJ (2007) Do discrimination tasks discourage multi-dimensional stimulus processing? Evidence from a cross-modal object discrimination in rats. Behav Brain Res 183:213–221

    Article  PubMed  Google Scholar 

  • Kettler N, Schweinfurth MK, Taborsky M (2021) Rats show direct reciprocity when interacting with multiple partners. Sci Rep 11(1):1–8

    Article  Google Scholar 

  • Kotrschal A, Taborsky B (2010) Environmental change enhances cognitive abilities in fish. PLoS Biol 8:e1000351

    Article  PubMed  PubMed Central  Google Scholar 

  • Landers MS, Knott GW, Lipp HP, Poletaeva I, Welker E (2011) Synapse formation in adult barrel cortex following naturalistic environmental enrichment. Neuroscience 199:143–152

    Article  CAS  PubMed  Google Scholar 

  • Lehmann L, Keller L (2006) The evolution of cooperation and altruism – a general framework and a classification of models. J Evol Biol 19(5):1365–1376

    Article  CAS  PubMed  Google Scholar 

  • Melis AP, Hare B, Tomasello M (2006) Engineering cooperation in chimpanzees: tolerance constraints on cooperation. Anim Behav 30:381–392

    Google Scholar 

  • Paulsson NI, Taborsky M (2021) Reaching out for inaccessible food is a potential begging signal in cooperating wild-type Norway rats, Rattus norvegicus. Front Psychol 12:712333

    Article  PubMed  PubMed Central  Google Scholar 

  • Paulsson NI, Taborsky M (2022) Norway rats help social partners in need in response to ultrasonic begging signals. Ethology 128(12):724–733

    Article  Google Scholar 

  • Quinones AE, van Doorn GS, Pen I, Weissing FJ, Taborsky M (2016) Negotiation and appeasement can be more effective drivers of sociality than kin selection. Philos Trans R Soc B Biol Sci 371:20150089

    Article  Google Scholar 

  • R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, Tsien JZ (2000) Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat Neurosci 3:238–244

    Article  CAS  PubMed  Google Scholar 

  • Rochefort C, Gheusi G, Vincent JD, Lledo PM (2002) Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22:2679–2689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roulin A, des Monstiers B, Ifrid E, Da Silva A, Genzoni E, Dreiss AN (2015) Reciprocal preening and food sharing in colour-polymorphic nestling barn owls. J Evol Biol 29:380–394. https://doi.org/10.1111/jeb.12793

    Article  PubMed  Google Scholar 

  • Rutte C, Taborsky M (2007) Generalized reciprocity in rats. PLoS Biol 5:1421–1425

    Article  CAS  Google Scholar 

  • Rutte C, Taborsky M (2008) The influence of social experience on cooperative behavior of rats (Rattus norvegicus): direct vs generalized reciprocity. Behav Ecol Sociobiol 62:499–505

    Article  Google Scholar 

  • Salvanes AGV, Moberg O, Ebbesson LO, Nilsen TO, Jensen KH, Braithwaite VA (2013) Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proc R Soc B Biol Sci 280(1767):20131331

    Article  Google Scholar 

  • Schneeberger K, Dietz M, Taborsky M (2012) Reciprocal cooperation between unrelated rats depends on cost to donor and benefit to recipient. BMC Evol Biol 12:41

    Article  PubMed  PubMed Central  Google Scholar 

  • Schneeberger K, Röder G, Taborsky M (2020) The smell of hunger: Norway rats provision social partners based on odour cues of need. PLoS Biol 18(3):e3000628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schweinfurth MK, Taborsky M (2018a) Norway rats (Rattus norvegicus) communicate need, which elicits donation of food. J Comp Psychol 132:119–129

    Article  PubMed  Google Scholar 

  • Schweinfurth MK, Taborsky M (2018b) Relatedness decreases and reciprocity increases cooperation in Norway rats. Proc R Soc B Biol Sci 285(1874):20180035

    Article  Google Scholar 

  • Schweinfurth MK, Taborsky M (2020) Rats play tit-for-tat instead of integrating social experience over multiple interactions. Proc R Soc B 287(1918):20192423

    Article  PubMed  PubMed Central  Google Scholar 

  • Schweinfurth MK, Aeschbacher J, Santi M, Taborsky M (2019) Male Norway rats cooperate according to direct but not generalized reciprocity rules. Anim Behav 152:93–101

    Article  Google Scholar 

  • Stevens JR, Hauser MD (2004) Why be nice? Psychological constraints on the evolution of cooperation. Trends Cogn Sci 8(2):60–65

    Article  PubMed  Google Scholar 

  • Stevens JR, Cushman FA, Hauser MD (2004) Evolving the psychological mechanisms for cooperation. Annu Rev Ecol Evol Syst 36:499–518

    Article  Google Scholar 

  • Szipl G, Boeckle M, Wascher CAF, Spreafico M, Bugnyar T (2015) With whom to dine? Ravens’ responses to food-associated calls depend on individual characteristics of the caller. Anim Behav 99:33–42

    Article  PubMed  PubMed Central  Google Scholar 

  • Taborsky M, Frommen JG, Riehl C (2016) The evolution of cooperation based on direct fitness benefits. Phil Trans R Soc B 371:20150472

    Article  PubMed  PubMed Central  Google Scholar 

  • Taborsky M, Cant MA, Komdeur J (2021) The evolution of social behaviour. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Trivers RL (1971) The evolution of reciprocal altruism. Q Rev Biol 46:35–57

    Article  Google Scholar 

  • Veyrac A, Sacquet J, Nguyen V, Marien M, Jourdan F, Didier A (2009) Novelty determines the effects of olfactory enrichment on memory and neurogenesis through noradrenergic mechanisms. Neuropsychopharmacology 34:786–795

    Article  CAS  PubMed  Google Scholar 

  • Wood RI, Kim JY, Li GR (2016) Cooperation in rats playing the iterated Prisoner’s Dilemma game. Anim Behav 114:27–35

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu JH, Yu LP, Cai R, Zhang JP, Sun XD (2009) Early auditory enrichment with music enhances auditory discrimination learning and alters NR2B protein expression in rat auditory cortex. Behav Brain Res 196:49–54

    Article  PubMed  Google Scholar 

  • Yokoyama S, Radlwimmer FB (1998) The “five-sites” rule and the evolution of red and green color vision in mammals. Mol Biol Evol 15:560–567

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We acknowledge financial support of the SNF (project grant 310030B_138660 to Michael Taborsky) and of the SAV (grant to Vassilissa Dolivo).

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Dolivo, V., Engqvist, L. & Taborsky, M. When deciding to cooperate by direct reciprocity, Norway rats sometimes benefit from olfactory competence and seem not impaired by insufficient cognitive abilities. Anim Cogn 26, 1119–1130 (2023). https://doi.org/10.1007/s10071-023-01754-5

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