Advertisement

Animal Cognition

, Volume 21, Issue 4, pp 513–529 | Cite as

Spatio-temporal organization during group formation in rats

  • Omri Weiss
  • Anat Levi
  • Elad Segev
  • Margarita Simbirsky
  • David EilamEmail author
Original Paper

Abstract

In the present study, the dynamic process of group formation in eight unfamiliar rats was followed in order to reveal how the group becomes oriented together in time and space, in light of the complexity that accompanies grouping. The focus was on who, where, and when joined together. We found that rats preferred to be in companionship over remaining alone, with all the rats gradually shifting to share the same location as a resting place. Group formation can be viewed as a tri-phasic process, with some rats gradually becoming more social than others, and thus playing a key role in group formation. Starting with seemingly independent traveling, the rats gradually converged to share the same location as a terminal (home base) for roundtrips in the arena. Because such a terminal is considered as the organizer of an individual’s spatial behavior, the shared home-base location may be viewed as the organizer of spatial behavior of the entire group. Despite huddling together, the rats continued to travel alone or in duos throughout the 3 h of testing. We suggest that resting together and traveling alone or in duos enabled the maintenance of communal relationship while reducing the complexity involved in traveling in relatively large groups. Taken together, the present results demonstrate the dynamic process during which unfamiliar rats shift from independent to group spatial behavior.

Keywords

Spatial representation Exploration Social environment Social cognition Group formation 

Notes

Acknowledgements

This study was supported by the Israel Science Foundation grant 230/13 to DE. We are grateful to Naomi Paz for language editing.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study and the maintenance conditions for the rats were carried out under the regulations and approval of the Institutional Committee for Animal Experimentation at Tel-Aviv University (permit # 04-15-061).

Supplementary material

10071_2018_1185_MOESM1_ESM.docx (421 kb)
Online Resource 1. Supplemental data for: (i) The social networks of each octet of rats which are averaged in Figure 5; (ii) A reference group of eight rats that were tested for one hour and pooled into one virtual group; and (iii) A reference group made of simulated traveling of eight virtual rats. These data show that the results described in the octets were a product of the social environment and not a mere product of random traveling (DOCX 421 KB)

Online Resource 2. Group formation. This phase comprised two stages. During the first stage (first half hour) the rats begin by exploring the arena for a few minutes, briefly encountering their mates and immediately continuing to travel. After about 5 minutes, the rats start to interact more with one another, but are not yet establishing stable groups and frequently exchange partners. In the second stage (30-60 minutes), the same trends of a decrease in traveling and increased duration of resting with more and more partners continue (MP4 5636 KB)

Online Resource 3. Group stabilization. The second hour (time intervals 60-90 and 90-120) is the period in which the group had already been stabilized. The major changes that occurred in the first hour led to the formation of relatively large resting groups. However, there are still many rats in motion (alone or with one partner) despite their occasionally resting in the larger groups. This is also the time when most of the rats are sharing the same home base (MP4 3194 KB)

Online Resource 4. Group performance. The third hour (120-180 min) is the period when the dynamic processes levels off. Activity decrease further, the rats are resting together in one place, and every now and then a few rats, typically alone or with a partner, are taking roundtrips into the arena (WMV 9987 KB)

References

  1. Alberts JR (1978a) Huddling by rat pups: Multisensory control of contact behavior. J Comp Physiol Psychol 92:220–230.  https://doi.org/10.1037/h0077458 CrossRefPubMedGoogle Scholar
  2. Alberts JR (1978b) Huddling by rat pups: Group behavioral mechanisms of temperature regulation and energy conservation. J Comp Physiol Psychol 92:231–245.  https://doi.org/10.1037/h0077459 CrossRefPubMedGoogle Scholar
  3. Alberts JR (2007) Huddling by rat pups: ontogeny of individual and group behavior. Dev Psychobiol 49:22–32.  https://doi.org/10.1002/dev.20190 CrossRefPubMedGoogle Scholar
  4. Barclay RMR (1982) Night roosting behavior of the little brown bat, Myotis lucifugus. J Mammal 63:464–474.  https://doi.org/10.2307/1380444 CrossRefGoogle Scholar
  5. Bar-Yam Y (1997) Dynamics of complex systems. Addison-Wesley, Reading, MAGoogle Scholar
  6. Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. In: Proceedings of International AAAI Conference on Web and Social Media, pp 361−362Google Scholar
  7. Ben-Yehoshua D, Yaski O, Eilam D (2011) Spatial behavior: the impact of global and local geometry. Anim Cogn 14:341–350.  https://doi.org/10.1007/s10071-010-0368-z CrossRefPubMedGoogle Scholar
  8. Bijleveld AI, Egas M, van Gils JA, Piersma T (2010) Beyond the information centre hypothesis: communal roosting for information on food, predators, travel companions and mates? Oikos 119:277–285.  https://doi.org/10.1111/j.1600-0706.2009.17892.x CrossRefGoogle Scholar
  9. Blumenfeld-Lieberthal E, Eilam D (2016) Physical, behavioral and spatiotemporal perspectives of home in humans and other animals. In: Portugali J, Stolk E (eds) Springer International Publishing, pp 127–149Google Scholar
  10. Bonuti R, Morato S (2017) Proximity as a predictor of social behavior in rats. J Neurosci Methods 293:37–44.  https://doi.org/10.1016/j.jneumeth.2017.08.027 CrossRefPubMedGoogle Scholar
  11. Broom DM, Dick WJA, Johnson CE et al (1976) Pied wagtail roosting and feeding behaviour. Bird Study 23:267–279.  https://doi.org/10.1080/00063657609476513 CrossRefGoogle Scholar
  12. Brown MF (2011) Social influences on rat spatial choice. Comp Cogn Behav Rev 6:5–23.  https://doi.org/10.3819/ccbr.2011.6002 CrossRefGoogle Scholar
  13. Buckley NJ (1996) Food finding and the influence of information, local enhancement, and communal roosting on foraging success of north american vultures. Auk 113:473–488.  https://doi.org/10.2307/4088913 CrossRefGoogle Scholar
  14. Caccamise DF, Morrison DW (1986) Avian communal roosting: implications of diurnal activity centers. Am Nat 128:191–198.  https://doi.org/10.1086/284553 CrossRefGoogle Scholar
  15. Chidambaram L, Bostrom R (1997) Group development (I): a review and synthesis of development models. Gr Decis Negot 6:159–187.  https://doi.org/10.1023/A:1008603328241 CrossRefGoogle Scholar
  16. Couzin ID, Krause J, James R et al (2002) Collective memory and spatial sorting in animal groups. J Theor Biol 218:1–11.  https://doi.org/10.1006/jtbi.2002.3065 CrossRefPubMedGoogle Scholar
  17. Delm M (1990) Vigilance for predators: detection and dilution effects. Behav Ecol Sociobiol 26:337–342.  https://doi.org/10.1007/BF00171099 CrossRefGoogle Scholar
  18. Dorfman A, Nielbo KL, Eilam D (2016) Traveling companions add complexity and hinder performance in the spatial behavior of rats. PLoS One 11:e0146137.  https://doi.org/10.1371/journal.pone.0146137 CrossRefPubMedPubMedCentralGoogle Scholar
  19. du Plessis MA, Weathers WW, Koenig WD (1994) Energetic benefits of communal roosting by Acorn Woodpeckers during the nonbreeding season. Condor 96:631–637.  https://doi.org/10.2307/1369466 CrossRefGoogle Scholar
  20. Eichenbaum H (2015) The hippocampus as a cognitive map … of social space. Neuron 87:9–11.  https://doi.org/10.1016/j.neuron.2015.06.013 CrossRefPubMedGoogle Scholar
  21. Eilam D (2003) Open-field behavior withstands drastic changes in arena size. Behav Brain Res 142:53–62CrossRefPubMedGoogle Scholar
  22. Eilam D (2010) Is it safe? Voles in an unfamiliar dark open-field divert from optimal security by abandoning a familiar shelter and not visiting a central start point. Behav Brain Res 206:88–92CrossRefPubMedGoogle Scholar
  23. Eilam D, Golani I (1989) Home base behavior of rats (Rattus norvegicus) exploring a novel environment. Behav Brain Res 34:199–211.  https://doi.org/10.1016/S0166-4328(89)80102-0 CrossRefPubMedGoogle Scholar
  24. Eiserer LA (1984) Communal roosting in birds. Bird Behav 5:61–80Google Scholar
  25. Fortin D, Fortin M-E, Beyer HL et al (2009) Group-size-mediated habitat selection and group fusion–fission dynamics of bison under predation risk. Ecology 90:2480–2490.  https://doi.org/10.1890/08-0345.1 CrossRefPubMedGoogle Scholar
  26. Galef BGJ, White DJ (1997) Socially acquired information reduces Norway rats’ latencies to find food. Anim Behav 54:705–714.  https://doi.org/10.1006/anbe.1997.0475 CrossRefGoogle Scholar
  27. Golani I, Benjamini Y, Eilam D (1993) Stopping behavior: constraints on exploration in rats (Rattus norvegicus). Behav Brain Res 53:21–33CrossRefPubMedGoogle Scholar
  28. Grand T, Dill L (1999) The effect of group size on the foraging behaviour of juvenile coho salmon: reduction of predation risk or increased competition? Anim Behav 58:443–451.  https://doi.org/10.1006/anbe.1999.1174 CrossRefPubMedGoogle Scholar
  29. Hafting T, Fyhn M, Molden S et al (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806.  https://doi.org/10.1038/nature03721 CrossRefPubMedGoogle Scholar
  30. Hines DJ, Whishaw IQ (2005) Home bases formed to visual cues but not to self-movement (dead reckoning) cues in exploring hippocampectomized rats. Eur J Neurosci 22:2363–2375.  https://doi.org/10.1111/j.1460-9568.2005.04412.x CrossRefPubMedGoogle Scholar
  31. Ilany A, Barocas A, Koren L et al (2013) Structural balance in the social networks of a wild mammal. Anim Behav 85:1397–1405.  https://doi.org/10.1016/j.anbehav.2013.03.032 CrossRefGoogle Scholar
  32. Keller MR, Brown MF (2011) Social effects on rat spatial choice in an open field task. Learn Motiv 42:123–132.  https://doi.org/10.1016/j.lmot.2010.12.004 CrossRefGoogle Scholar
  33. Kerth G, Reckardt K (2003) Information transfer about roosts in female Bechstein’s bats: an experimental field study. Proceedings Biol Sci 270:511–515.  https://doi.org/10.1098/rspb.2002.2267
  34. Krause J (1993) The relationship between foraging and shoal position in a mixed shoal of roach (Rutilus rutilus) and chub (Leuciscus cephalus): a field study. Oecologia 93:356–359.  https://doi.org/10.1007/BF00317878 CrossRefPubMedGoogle Scholar
  35. Krause J (1994) Differential fitness returns in relation to spatial position in groups. Biol Rev 69:187–206.  https://doi.org/10.1111/j.1469-185X.1994.tb01505.x CrossRefPubMedGoogle Scholar
  36. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  37. Kropff E, Carmichael JE, Moser M-B, Moser EI (2015) Speed cells in the medial entorhinal cortex. Nature 523:419–424.  https://doi.org/10.1038/nature14622 CrossRefPubMedGoogle Scholar
  38. Loewen I, Wallace DG, Whishaw IQ (2005) The development of spatial capacity in piloting and dead reckoning by infant rats: use of the huddle as a home base for spatial navigation. Dev Psychobiol 46:350–361.  https://doi.org/10.1002/dev.20063 CrossRefPubMedGoogle Scholar
  39. Maaswinkel H, Gispen WH, Spruijt BM (1997) Executive function of the hippocampus in social behavior in the rat. Behav Neurosci 111:777–784.  https://doi.org/10.1037/0735-7044.111.4.777 CrossRefPubMedGoogle Scholar
  40. Mintz M, Russig H, Lacroix L, Feldon J (2005) Sharing of the home base: a social test in rats. Behav Pharmacol 16:227–236CrossRefPubMedGoogle Scholar
  41. Nemati F, Whishaw IQ (2007) The point of entry contributes to the organization of exploratory behavior of rats on an open field: an example of spontaneous episodic memory. Behav Brain Res 182:119–128.  https://doi.org/10.1016/j.bbr.2007.05.016 CrossRefPubMedGoogle Scholar
  42. O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–175.  https://doi.org/10.1016/0006-8993(71)90358-1 CrossRefPubMedGoogle Scholar
  43. O’Keefe J, Nadel L (1978) The Hippocampus as a cognitive map, vol 3. Clarendon Press, OxfordGoogle Scholar
  44. Ohayon S, Avni O, Taylor AL et al (2013) Automated multi-day tracking of marked mice for the analysis of social behaviour. J Neurosci Methods 219:10–19.  https://doi.org/10.1016/j.jneumeth.2013.05.013 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Partridge BL, Pitcher TJ, Gables C (1980) The sensory basis of fish schools: relative roles of lateral line and vision. J Comp Psychol 135:315–325Google Scholar
  46. Poysa H (1992) Group foraging in patchy environments: the importance of coarse-level local enhancement. Ornis Scand 23:159–166.  https://doi.org/10.2307/3676444 CrossRefGoogle Scholar
  47. Schank JC, Alberts JR (1997) Self-organized huddles of rat pups modeled by simple rules of individual behavior. J Theor Biol 189:11–25.  https://doi.org/10.1006/jtbi.1997.0488 CrossRefPubMedGoogle Scholar
  48. Shemesh Y, Sztainberg Y, Forkosh O et al (2013) High-order social interactions in groups of mice. Elife 2:1–19.  https://doi.org/10.7554/eLife.00759 CrossRefGoogle Scholar
  49. Shi Q, Ishii H, Kinoshita S et al (2013) Modulation of rat behaviour by using a rat-like robot. Bioinspir Biomim 8:1–10.  https://doi.org/10.1088/1748-3182/8/4/046002 CrossRefGoogle Scholar
  50. Shi Q, Ishii H, Tanaka K et al (2015) Behavior modulation of rats to a robotic rat in multi-rat interaction. Bioinspir Biomim 10:56011.  https://doi.org/10.1088/1748-3190/10/5/056011 CrossRefGoogle Scholar
  51. Siegfried WR (1971) Communal roosting of the cattle egret. Trans R Soc South Africa 39:419–443.  https://doi.org/10.1080/00359197109519131 CrossRefGoogle Scholar
  52. Solstad T, Boccara CN, Kropff E et al (2008) Representation of geometric borders in the entorhinal cortex. Science 322:1865–1868.  https://doi.org/10.1126/science.1166466 CrossRefPubMedGoogle Scholar
  53. Stacey PB (1986) Group size and foraging efficiency in yellow baboons. Behav Ecol Sociobiol 18:175–187.  https://doi.org/10.1007/BF00290821 CrossRefGoogle Scholar
  54. Swingland IR (1977) The social and spatial organization of winter communal roosting in Rooks (Corvus frugilegus). J Zool 182:509–528.  https://doi.org/10.1111/j.1469-7998.1977.tb04167.x CrossRefGoogle Scholar
  55. Szechtman H, Sulis W, Eilam D (1998) Quinpirole induces compulsive checking behavior in rats: a potential animal model of Obsessive–Compulsive Disorder (OCD). Behav Neurosci 112:1475–1485.  https://doi.org/10.1037/0735-7044.112.6.1475 CrossRefPubMedGoogle Scholar
  56. Taube JS, Muller RU, Ranck JB (1990a) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10:420–435CrossRefPubMedGoogle Scholar
  57. Taube JS, Muller RU, Ranck JB (1990b) Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci 10:436–447CrossRefPubMedGoogle Scholar
  58. Tavares RM, Mendelsohn A, Grossman Y et al (2015) A map for social navigation in the human brain. Neuron 87:231–243.  https://doi.org/10.1016/j.neuron.2015.06.011 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Tchernichovski O, Golani I (1995) A phase plane representation of rat exploratory behavior. J Neurosci Methods 62:21–27CrossRefPubMedGoogle Scholar
  60. Thomas DW, Fenton MB (1978) Notes on the dry season roosting and foraging behaviour of Epomophorus gambianus and Rousettus aegyptiacus (Chiroptera pteropodidae). J Zool 186:403–406.  https://doi.org/10.1111/j.1469-7998.1978.tb03929.x CrossRefGoogle Scholar
  61. Tolman EC (1932) Purposive behavior in animals and men. University of California Press, Los Angeles, CAGoogle Scholar
  62. Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189–208.  https://doi.org/10.1037/h0061626 CrossRefPubMedGoogle Scholar
  63. Valle FP (1971) Rats’ performance on repeated tests in the open field as a function of age. Psychon Sci 23:333–334.  https://doi.org/10.3758/bf03336137 CrossRefGoogle Scholar
  64. Varela FJ, Thompson E, Rosch E (1991) The embodied mind: cognitive science and human experience. MIT Press, CambridgeGoogle Scholar
  65. Wallace DG, Hamilton DA, Whishaw IQ (2006) Movement characteristics support a role for dead reckoning in organizing exploratory behavior. Anim Cogn 9:219–228.  https://doi.org/10.1007/s10071-006-0023-x CrossRefPubMedGoogle Scholar
  66. Walsh RN, Cummins R (1976) The open-field test: a critical review. Psychol Bull 83:482–504CrossRefPubMedGoogle Scholar
  67. Wang M-Y, Brennan CH, Lachlan RF, Chittka L (2015) Speed–accuracy trade-offs and individually consistent decision making by individuals and dyads of zebrafish in a colour discrimination task. Anim Behav.  https://doi.org/10.1016/j.anbehav.2015.01.022 CrossRefGoogle Scholar
  68. Ward P (1965) Feeding ecology of the black-faced dioch Quelea quelea in Nigeria. Ibis (Lond 1859) 107:173–214.  https://doi.org/10.1111/j.1474-919X.1965.tb07296.x CrossRefGoogle Scholar
  69. Ward AJW (2011) Social facilitation of exploration in mosquitofish (Gambusia holbrooki). Behav Ecol Sociobiol 66:223–230.  https://doi.org/10.1007/s00265-011-1270-7 CrossRefGoogle Scholar
  70. Ward P, Zahavi A (1973) The importance of certain assemblages of birds as “information-centers for food-finding. Ibis (Lond 1859) 115:517–534.  https://doi.org/10.1111/j.1474-919X.1973.tb01990.x CrossRefGoogle Scholar
  71. Weatherhead PJ (1983) Two principal strategies in avian communal roosts. Am Nat 121:237–243.  https://doi.org/10.1086/284053 CrossRefGoogle Scholar
  72. Weiss S, Yaski O, Eilam D et al (2012) Network analysis of rat spatial cognition: behaviorally-established symmetry in a physically asymmetrical environment. PLoS One 7:e40760.  https://doi.org/10.1371/journal.pone.0040760 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Weiss O, Segev E, Eilam D (2015) “Shall two walk together except they be agreed?” Spatial behavior in rat dyads. Anim Cogn 18:39–51.  https://doi.org/10.1007/s10071-014-0775-7 CrossRefPubMedGoogle Scholar
  74. Weiss O, Dorfman A, Ram T et al (2017a) Rats do not eat alone in public: food-deprived rats socialize rather than competing for baits. PLoS One.  https://doi.org/10.1371/journal.pone.0173302 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Weiss O, Segev E, Eilam D (2017b) Social spatial cognition in rat tetrads: how they select their partners and their gathering places. Anim Cogn 20:409–418.  https://doi.org/10.1007/s10071-016-1063-5 CrossRefPubMedGoogle Scholar
  76. Weissbrod A, Shapiro A, Vasserman G et al (2013) Automated long-term tracking and social behavioural phenotyping of animal colonies within a semi-natural environment. Nat Commun 4:1–10.  https://doi.org/10.1038/ncomms3018 CrossRefGoogle Scholar
  77. Wey T, Blumstein DT, Shen W, Jordán F (2008) Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim Behav 75:333–344.  https://doi.org/10.1016/j.anbehav.2007.06.020 CrossRefGoogle Scholar
  78. Whishaw IQ, Gharbawie OA, Clark BJ, Lehmann H (2006) The exploratory behavior of rats in an open environment optimizes security. Behav Brain Res 171:230–239CrossRefPubMedGoogle Scholar
  79. Yaski O, Eilam D (2008) How do global and local geometries shape exploratory behavior in rats? Behav Brain Res 187:334–342.  https://doi.org/10.1016/j.bbr.2007.09.027 CrossRefPubMedGoogle Scholar
  80. Yom-Tov Y, Imber A, Otterman J (1977) The microclimate of winter roosts of the starling Sturnus vulgaris. Ibis (Lond 1859) 119:366–368.  https://doi.org/10.1111/j.1474-919X.1977.tb08258.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Omri Weiss
    • 1
  • Anat Levi
    • 1
  • Elad Segev
    • 2
  • Margarita Simbirsky
    • 2
  • David Eilam
    • 1
    Email author
  1. 1.Department of Zoology, School of ZoologyTel-Aviv UniversityTel-AvivIsrael
  2. 2.Department of Applied MathematicsHolon Institute of TechnologyHolonIsrael

Personalised recommendations