Do female Norway rats form social bonds?

Abstract

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.

Significance statement

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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References

  1. Adams N, Boice R (1983) A longitudinal study of dominance in an outdoor colony of domestic rats. J Comp Psychol 97:24–33

    Article  Google Scholar 

  2. 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

    Google Scholar 

  3. 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

    CAS  Article  Google Scholar 

  4. Barnett SA (1963) The rat—a study in behavior. Aldine, Chicago

    Google Scholar 

  5. Barrett L, Henzi SP (2001) Constraints on relationship formation among female primates. Behaviour 139:263–289

    Article  Google Scholar 

  6. Bates DM, Maechler M, Bolker BM, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  7. Beauchamp G (1998) The effect of group size on mean food intake rate in birds. Biol Rev 73:449–472

    Article  Google Scholar 

  8. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 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

    CAS  Article  Google Scholar 

  10. Braun A, Bugnyar T (2012) Social bonds and rank acquisition in raven nonbreeder aggregations. Anim Behav 84:1507–1515

    Article  PubMed  PubMed Central  Google Scholar 

  11. Calhoun JB (1962) The ecology and sociology of the Norway rat. US Public Health Service Publication no. 1008. US Government Printing Office, Washington DC

  12. 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

    CAS  Google Scholar 

  13. Côté IM, Poulinb R (1994) Parasitism and group size in social animals: a meta-analysis. Behav Ecol 6:159–165

    Article  Google Scholar 

  14. Crawley MJ (2007) The R book. John Wiley & Sons Ltd, Chichester

    Google Scholar 

  15. 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

    Google Scholar 

  16. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Davis DE (1953) The characteristics of rat populations. Q Rev Biol 28:373–401

    CAS  Article  PubMed  Google Scholar 

  18. 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 

  19. 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

    Article  Google Scholar 

  20. Dolivo V, Rutte C, Taborsky M (2016) Ultimate and proximate mechanisms of reciprocal altruism in rats. Learn Behav 44:223

    Article  PubMed  Google Scholar 

  21. Durrell JL, Sneddon IA, O’Connell NE, Whitehead H (2004) Do pigs form preferential associations? Appl Anim Behav Sci 89:41–52

    Article  Google Scholar 

  22. Fang J, Clemens LG (1999) Contextual determinants of female-female mounting in laboratory rats. Anim Behav 57:545–555

    CAS  Article  PubMed  Google Scholar 

  23. 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

    Google Scholar 

  24. 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  26. 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

    CAS  Article  PubMed  Google Scholar 

  27. Hardy DF (1972) Sexual behavior in continuously cycling rats. Behaviour 41:288–297

    CAS  Article  PubMed  Google Scholar 

  28. Hemelrijk CK (1990) Models of, and tests for, reciprocity, unidirectionality and other social interaction patterns at a group level. Anim Behav 39:1013–1029

    Article  Google Scholar 

  29. 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

    Article  Google Scholar 

  30. 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

    Article  Google Scholar 

  31. Hinde RA (1976) Interactions, relationships and social structure. Man 11:1–17

    Article  Google Scholar 

  32. 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

    Article  Google Scholar 

  33. 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

    Google Scholar 

  34. 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

    Google Scholar 

  35. Janson CH (1988) Food competition in brown capuchin monkeys (Cebus apella): quantitative effects of group size and tree productivity. Behaviour 105:53–76

    Article  Google Scholar 

  36. Kappeler PM (1997) Determinants of primate social organization: comparative evidence and new insights from Malagasy lemurs. Biol Rev 72:111–151

    CAS  Article  PubMed  Google Scholar 

  37. Koenig WD, Dickinson JL (2016) Cooperative breeding in vertebrates: studies of ecology, evolution, and behavior. Cambridge University Press, Cambridge

    Google Scholar 

  38. 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

    Article  Google Scholar 

  39. 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

    Article  Google Scholar 

  40. Massen JJM, Sterck EHM, de Vos H (2010) Close social associations in animals and humans: functions and mechanisms of friendship. Behaviour 147:1379–1412

    Article  Google Scholar 

  41. Melis AP, Hare B, Tomasello M (2006a) Chimpanzees recruit the best collaborators. Science 311:1297–1300

    CAS  Article  PubMed  Google Scholar 

  42. Melis AP, Hare B, Tomasello M (2006b) Engineering cooperation in chimpanzees: tolerance constraints on cooperation. Anim Behav 72:275–286

    Article  Google Scholar 

  43. Norton S, Culver B, Mullenix P (1975) Development of nocturnal behavior in albino rats. Behav Biol 15:317–331

    CAS  Article  PubMed  Google Scholar 

  44. 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

  45. 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

    Article  Google Scholar 

  46. Schino G (2001) Grooming, competition and social rank among female primates: a meta-analysis. Anim Behav 62:265–271

    Article  Google Scholar 

  47. Schino G, Aureli F (2016) Reciprocity in group-living animals: partner control versus partner choice. Biol Rev:1–8

  48. 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 

  49. Schuster R, Perelberg A (2004) Why cooperate? An economic perspective is not enough. Behav Process 66:261–277

    Article  Google Scholar 

  50. Schweinfurth MK, Stieger B, Taborsky M (2017) Experimental evidence for reciprocity in allogrooming among wild-type Norway rats. Sci Rep

  51. Seyfarth RM, Cheney DL (2012) The evolutionary origins of friendship. Annu Rev Psychol 63:153–177

    Article  PubMed  Google Scholar 

  52. 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

    CAS  Google Scholar 

  53. Silk JB (2002) Using the “f”-word in primatology. Behaviour 139:421–446

    Article  Google Scholar 

  54. 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

    Article  Google Scholar 

  55. 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

    Article  Google Scholar 

  56. 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

    Article  PubMed  PubMed Central  Google Scholar 

  57. 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

  58. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H. Freeman & Company, New York

    Google Scholar 

  59. Taborsky M, Frommen JG, Riehl C (2016) Correlated pay-offs are key to cooperation. Philos Trans R Soc B 371:20150084

    Article  Google Scholar 

  60. Tan L, Hackenberg TD (2016) Functional analysis of mutual behavior in laboratory rats. J Comp Psychol 130:1–11

    Article  Google Scholar 

  61. Telle H (1966) Beitrag zur Erkenntnis der Verhaltensweise von Ratten, vergleichend dargestellt bei Rattus norvegicus und Rattus rattus. Z Angew Zool 53:129–196

    Google Scholar 

  62. 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

    Article  Google Scholar 

  63. Wagner RH (1992) The pursuit of extra-pair copulations by monogamous female razorbills: how do females benefit? Behav Ecol Sociobiol 29:455–464

    Article  Google Scholar 

  64. Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm limited females. Trends Ecol Evol 17:313–320

  65. 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

    Article  Google Scholar 

  66. Weingrill T (2000) Infanticide and the value of male-female relationships in mountain chacma baboons. Behaviour 137:337–359

    Article  Google Scholar 

  67. 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 

  68. 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

    CAS  Article  PubMed  Google Scholar 

  69. 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

    CAS  Article  PubMed  Google Scholar 

  70. Ziporyn T, McClintock MK (1991) Passing as an indicator of social dominance among female wild and domestic Norway rats. Behaviour 118:26–41

    Article  Google Scholar 

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Acknowledgments

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.

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Contributions

MKS and MT conceived and designed the study and wrote the manuscript. JN, KS, AKR and MG collected the data. MKS and LE planned the statistical analyses, which were conducted by MKS. LE wrote the R-code for all Mantel tests. All authors read and commented on the final version of the manuscript.

Corresponding author

Correspondence to M. K. Schweinfurth.

Ethics declarations

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.

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The authors declare that they have no conflict of interest.

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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.

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All data generated or analysed during this study are included in the supplementary information files.

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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

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Keywords

  • Norway rats
  • Social bonds
  • Hierarchy
  • Peer relationship