Social bonds reflect specific and enduring relationships among conspecifics. In some group-living animals, they have been found to generate immediate and long-term fitness benefits. It is currently unclear how important and how widespread social bonds are in animals other than primates. It has been hypothesized that social bonds may help in establishing stable levels of reciprocal cooperation. Norway rats (Rattus norvegicus) reciprocate received help to an unrelated social partner. It is hitherto unknown, however, whether this cooperative behaviour is based on the establishment of social bonds among involved individuals. Norway rats live in social groups that can be very large; hence, without bonds, it may be difficult to keep track of other individuals and their previous behaviour, which is a precondition for generating evolutionarily stable levels of cooperation based on direct reciprocity. Here we tested whether wild-type female rats form bonds among each other, which are stable both over time and across different contexts. In addition, we scrutinized the potential influence of social rank on the establishment of bonds. Despite the fact that the hierarchy structure within groups remained stable over the study period, no stable social bonds were formed between group members. Apparently, social information from consecutive encounters with the same social partner is not accumulated. The lack of long-term social bonds might explain why rats base their decisions to cooperate primarily on the last encounter with a social partner, which may differ from other animals where cooperation is based on the existence of long-term social bonds.
Social bonds have been hypothesized to favour reciprocal cooperation. Norway rats reciprocate help received from a social partner, but it is hitherto unclear whether they form social bonds that might further such cooperative behaviour. Here we tested whether female Norway rats engage in social relationships with a same-sex partner, which are stable over time and across contexts. In contrast to the hypothesized existence of bonds among long-term group members, our results provide no evidence that rats form specific social relationships. Rather than accumulating social information into social bonds, rats apparently base their decision to cooperate merely on the outcome of recent encounters.
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Adams N, Boice R (1983) A longitudinal study of dominance in an outdoor colony of domestic rats. J Comp Psychol 97:24–33
Archie EA, Moss CJ, Alberts SC (2001) Friends and relations: kinship and the nature of female elephant social relationships. In: Moss CJ, Croze H, Lee PC (eds) The Amboseli elephants: a long-term perspective on a long-lived mammal. The University of Chicago Press, Chicago, pp 238–245
Archie EA, Moss CJ, Alberts SC (2006) The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proc R Soc Lond B 273:513–522
Barnett SA (1963) The rat—a study in behavior. Aldine, Chicago
Barrett L, Henzi SP (2001) Constraints on relationship formation among female primates. Behaviour 139:263–289
Bates DM, Maechler M, Bolker BM, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Beauchamp G (1998) The effect of group size on mean food intake rate in birds. Biol Rev 73:449–472
Beery AK, Routman DM, Zucker I (2009) Same-sex social behavior in meadow voles: multiple and rapid formation of attachments. Physiol Behav 97:52–57
Blanchard CD, Fukunaga-Stinson C, Takahashi LK, Flannelly KJ, Blanchard RJ (1984) Dominance and aggression in social groups of male and female rats. Behav Process 9:31–48
Braun A, Bugnyar T (2012) Social bonds and rank acquisition in raven nonbreeder aggregations. Anim Behav 84:1507–1515
Calhoun JB (1962) The ecology and sociology of the Norway rat. US Public Health Service Publication no. 1008. US Government Printing Office, Washington DC
Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. Proc R Soc Lond B 106:13850–13853
Côté IM, Poulinb R (1994) Parasitism and group size in social animals: a meta-analysis. Behav Ecol 6:159–165
Crawley MJ (2007) The R book. John Wiley & Sons Ltd, Chichester
Crockett CM, Janson CH (2000) Infanticide in red howlers: female group size, group composition and a possible link to folivory. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 75–98
Crockford C, Wittig RM, Langergarber KE, Ziegler TE, Zuberbühler K, Deschner T (2013) Urinary oxytocin and social bonding in related and unrelated wild chimpanzees. Proc R Soc B 280:20122765
Davis DE (1953) The characteristics of rat populations. Q Rev Biol 28:373–401
Dolivo V, Taborsky M (2015a) Norway rats reciprocate help according to the quality of help they received. Biol Lett 11:20140959
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, Rutte C, Taborsky M (2016) Ultimate and proximate mechanisms of reciprocal altruism in rats. Learn Behav 44:223
Durrell JL, Sneddon IA, O’Connell NE, Whitehead H (2004) Do pigs form preferential associations? Appl Anim Behav Sci 89:41–52
Fang J, Clemens LG (1999) Contextual determinants of female-female mounting in laboratory rats. Anim Behav 57:545–555
Forbes D, Blom H, Kostmitsopoulus N, Moore G, Perretta G (2007) Euroguide on the accommodation and care of animals used for experimental and other scientific purposes. Federation of European Laboratory Animal Science Associations, London
Foster WA, Treherne JE (1981) Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 293:466–467
Gheusi G, Goodall G, Dantzer R (1997) Individually distinctive odours represent individual conspecifics in rats. Anim Behav 53:935–944
Gilbert C, Robertson G, Le Maho Y, Naito Y, Ance A (2006) Huddling behavior in emperor penguins: dynamics of huddling. Physiol Behav 88:479–488
Hardy DF (1972) Sexual behavior in continuously cycling rats. Behaviour 41:288–297
Hemelrijk CK (1990) Models of, and tests for, reciprocity, unidirectionality and other social interaction patterns at a group level. Anim Behav 39:1013–1029
Henzi SP, Lusseau D, Weingrill T, van Schaik CP, Barrett L (2009) Cyclicity in the structure of female baboon social networks. Behav Ecol Sociobiol 63:1015–1021
Herskin J, Steffensen JF (1998) Energy savings in sea bass swimming in a school: measurements of tail beat frequency and oxygen consumption at different swimming speeds. J Fish Biol 53:366–376
Hinde RA (1976) Interactions, relationships and social structure. Man 11:1–17
Holekamp KE, Cooper SM, Katona CI, Berry NA, Frank LG, Smale L (1997) Patterns of association among female spotted hyenas (Crocuta crocuta). J Mammal 78:55–64
Hurst JL, Barnard CJ, Nevison CM, West CD (1997) Housing and welfare in laboratory rats: welfare implications of isolation and social contact among caged males. Anim Welf 6:329–347
Hurst JL, Barnard CJ, Nevison CM, West CD (1998) Housing and welfare in laboratory rats: the welfare implications of social isolation and social contact among females. Anim Welf 7:121–136
Janson CH (1988) Food competition in brown capuchin monkeys (Cebus apella): quantitative effects of group size and tree productivity. Behaviour 105:53–76
Kappeler PM (1997) Determinants of primate social organization: comparative evidence and new insights from Malagasy lemurs. Biol Rev 72:111–151
Koenig WD, Dickinson JL (2016) Cooperative breeding in vertebrates: studies of ecology, evolution, and behavior. Cambridge University Press, Cambridge
Krafft B, Colin C, Peignot P (1994) Diving-for-food: a new model to assess social roles in a group of laboratory rats. Ethology 96:11–23
Lusseau D, Schneider K, Boisseau OJ, Haase P, Slooten E, Dawson SM (2003) The bottlenose dolphin community of doubtful sound features a large proportion of long-lasting associations: can geographic isolation explain this unique trait? Behav Ecol Sociobiol 54:396–405
Massen JJM, Sterck EHM, de Vos H (2010) Close social associations in animals and humans: functions and mechanisms of friendship. Behaviour 147:1379–1412
Melis AP, Hare B, Tomasello M (2006a) Chimpanzees recruit the best collaborators. Science 311:1297–1300
Melis AP, Hare B, Tomasello M (2006b) Engineering cooperation in chimpanzees: tolerance constraints on cooperation. Anim Behav 72:275–286
Norton S, Culver B, Mullenix P (1975) Development of nocturnal behavior in albino rats. Behav Biol 15:317–331
Perony N, König B, Schweitzer F (2010) A stochastic model of social interaction in wild house mice. In: Proceedings of the European Conference on Complex Systems 2010. https://www.sg.ethz.ch/media/publication_files/paper_eccs.pdf
Rutte C, Taborsky M (2008) The influence of social experience on cooperative behaviour of rats (Rattus norvegicus): direct vs generalised reciprocity. Behav Ecol Sociobiol 62:499–505
Schino G (2001) Grooming, competition and social rank among female primates: a meta-analysis. Anim Behav 62:265–271
Schino G, Aureli F (2016) Reciprocity in group-living animals: partner control versus partner choice. Biol Rev:1–8
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
Schuster R, Perelberg A (2004) Why cooperate? An economic perspective is not enough. Behav Process 66:261–277
Schweinfurth MK, Stieger B, Taborsky M (2017) Experimental evidence for reciprocity in allogrooming among wild-type Norway rats. Sci Rep
Seyfarth RM, Cheney DL (2012) The evolutionary origins of friendship. Annu Rev Psychol 63:153–177
Sharp J, Zammit T, Azar T, Lawson D (2003) Stress-like responses to common procedures in individually and group-housed female rats. J Am Assoc Lab Anim Sci 42:9–18
Silk JB (2002) Using the “f”-word in primatology. Behaviour 139:421–446
Silk JB, Altmann J, Alberts SC (2006) Social relationships among adult female baboons (Papio cynocephalus) I. Variation in the strength of social bonds. Behav Ecol Sociobiol 61:183–195
Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc R Soc Lond B 276:3099–3104
Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2010) Female chacma baboons form strong, equitable, and enduring social bonds. Behav Ecol Sociobiol 64:1733–1747
Simpson GL, Bates DM, Oksanen J (2016) Permute: functions for generating restricted permutations of data. Available at https://cran.r-project.org/web/packages/permute/index.html
Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H. Freeman & Company, New York
Taborsky M, Frommen JG, Riehl C (2016) Correlated pay-offs are key to cooperation. Philos Trans R Soc B 371:20150084
Tan L, Hackenberg TD (2016) Functional analysis of mutual behavior in laboratory rats. J Comp Psychol 130:1–11
Telle H (1966) Beitrag zur Erkenntnis der Verhaltensweise von Ratten, vergleichend dargestellt bei Rattus norvegicus und Rattus rattus. Z Angew Zool 53:129–196
Val-Laillet D, Guesdon V, von Keyserlingk MAG, de Passillé AM, Rushen J (2009) Allogrooming in cattle: relationships between social preferences, feeding displacements and social dominance. Appl Anim Behav Sci 116:141–149
Wagner RH (1992) The pursuit of extra-pair copulations by monogamous female razorbills: how do females benefit? Behav Ecol Sociobiol 29:455–464
Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm limited females. Trends Ecol Evol 17:313–320
Weidt A, Hofmann SE, König B (2008) Not only mate choice matters: fitness consequences of social partner choice in female house mice. Anim Behav 75:801–808
Weingrill T (2000) Infanticide and the value of male-female relationships in mountain chacma baboons. Behaviour 137:337–359
Wood RI, Kim JY, Li GR (2016) Cooperation in rats playing the iterated Prisoner’s dilemma game. Anim Behav 114:27–35
Yee JR, Cavigelli SA, Delgado B, McClintock MK (2008) Reciprocal affiliation among adolescent rats during a mild group stressor predicts mammary tumors and lifespan. Psychosom Med 70:1050–1059
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
Ziporyn T, McClintock MK (1991) Passing as an indicator of social dominance among female wild and domestic Norway rats. Behaviour 118:26–41
We thank Evi Zwygart for the help with animal care, Valentina Balzarini and Michelle Gygax for the drawings and Joachim G. Frommen for the comments on the manuscript. This study was funded by the SNF-grant 31003A_156152 provided to MT.
In accordance with the animal welfare regulations of Switzerland (Tierschutzverordnung Schweiz 04/2008) the rats (weight category 300–400 g) were housed in enriched cages (80/50/37.5 cm). Enrichment included a wooden house and board, a channel, a piece of wood to nibble, a loo roll to play, digging-material (wood shavings), nest-building material (hay) and a salt block. Food (conventional rat pellets and corn mix alternating with fresh vegetables or fruits) and water were provided ad libitum according to recommendations of the Federation of Laboratory Animal Science Associations (Forbes et al. 2007). We established small groups with five individuals per cage (Sharp et al. 2003). All rats experienced a handling procedure from early age onwards, so they were well habituated to humans and not stressed while being transported to the experimental cage or by the presence of an observer. No injuries occurred in the experiments. Approval and research permission was granted by Swiss Federal Veterinary Office under licence BE25/14.
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. This article does not contain any studies with human participants performed by any of the authors.
All data generated or analysed during this study are included in the supplementary information files.
Communicated by A. I. Schulte-Hostedde
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Schweinfurth, M.K., Neuenschwander, J., Engqvist, L. et al. Do female Norway rats form social bonds?. Behav Ecol Sociobiol 71, 98 (2017). https://doi.org/10.1007/s00265-017-2324-2
- Norway rats
- Social bonds
- Peer relationship