Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Costs and benefits of social relationships in the collective motion of bird flocks

Abstract

Current understanding of collective behaviour in nature is based largely on models that assume that identical agents obey the same interaction rules, but in reality interactions may be influenced by social relationships among group members. Here, we show that social relationships transform local interactions and collective dynamics. We tracked individuals’ three-dimensional trajectories within flocks of jackdaws, a species that forms lifelong pair-bonds. Reflecting this social system, we find that flocks contain internal sub-structure, with discrete pairs of individuals tied together by spring-like effective forces. Within flocks, paired birds interacted with fewer neighbours than unpaired birds and flapped their wings more slowly, which may result in energy savings. However, flocks with more paired birds had shorter correlation lengths, which is likely to inhibit efficient information transfer through the flock. Similar changes to group properties emerge naturally from a generic self-propelled particle model. These results reveal a critical tension between individual- and group-level benefits during collective behaviour in species with differentiated social relationships, and have major evolutionary and cognitive implications.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Flock morphology and evidence of pairing.
Fig. 2: Pairing causes variations in local interaction.
Fig. 3: Effect of pairing on the power consumption of individuals.
Fig. 4: Pairing reduces group correlation length.

Similar content being viewed by others

Data availability

Supplementary Figs. 1–12 and Supplementary Tables 1–3 are available in the Supplementary Information. Raw images captured by one of the four cameras and the reconstructed birds’ 3D movement trajectories are provided in Supplementary Videos 1–6. Plain text files, each including bird ID number, position, time, velocity, acceleration and wingbeat frequency at every time step, are provided in Supplementary Data 1–7. A plain text file that includes mean wingbeat frequency, flight speed and local density (approximated by the number of neighbours within a distance of 5 m from the focal bird) for paired and unpaired birds in six flocks, as well as for birds flying alone, is provided in Supplementary Data 8. All data required to reproduce the results in this study are included in Supplementary Data 1–8. Supplementary Data and Supplementary Videos are available at https://figshare.com/s/c55eb82bab800571d25d.

References

  1. Biro, D., Sasaki, T. & Portugal, S. J. Bringing a time–depth perspective to collective animal behaviour. Trends Ecol. Evol. 31, 550–562 (2016).

    Article  Google Scholar 

  2. Sumpter, D. J. T. The principles of collective animal behaviour. Philos. Trans. R. Soc. B 361, 5–22 (2006).

    Article  CAS  Google Scholar 

  3. Vicsek, T., Czirók, A., Ben-Jacob, E., Cohen, I. & Shochet, O. Novel type of phase transition in a system of self-driven particles. Phys. Rev. Lett. 75, 1226–1229 (1995).

    Article  CAS  Google Scholar 

  4. Vicsek, T. & Zafeiris, A. Collective motion. Phys. Rep. 517, 71–140 (2012).

    Article  Google Scholar 

  5. Croft, D., James, R. & Krause, J. Exploring Animal Social Networks (Princeton University Press, 2008).

  6. del Mar Delgado, M. et al. The importance of individual variation in the dynamics of animal collective movements. Philos. Trans. R. Soc. B 373, 20170008 (2018).

    Article  Google Scholar 

  7. King, A. J., Fehlmann, G., Biro, D., Ward, A. J. & Fürtbauer, I. Re-wilding collective behaviour: an ecological perspective. Trends Ecol. Evol. 33, 347–357 (2018).

    Article  Google Scholar 

  8. Farine, D. R., Strandburg-Peshkin, A., Couzin, I. D., Berger-Wolf, T. Y. & Crofoot, M. C. Individual variation in local interaction rules can explain emergent patterns of spatial organization in wild baboons. Proc. R. Soc. B 284, 20162243 (2017).

    Article  Google Scholar 

  9. Bode, N. W. F., Wood, A. J. & Franks, D. W. Social networks and models for collective motion in animals. Behav. Ecol. Sociobiol. 65, 117–130 (2011).

    Article  Google Scholar 

  10. Krause, J., James, R., Franks, D. & Croft, D. Animal Social Networks (Oxford University Press, 2015).

  11. Jolles, J. W., King, A. J., Manica, A. & Thornton, A. Heterogeneous structure in mixed-species corvid flocks in flight. Anim. Behav. 85, 743–750 (2013).

    Article  Google Scholar 

  12. King, A. J., Sueur, C., Huchard, E. & Cowlishaw, G. A rule-of-thumb based on social affiliation explains collective movements in desert baboons. Anim. Behav. 82, 1337–1345 (2011).

    Article  Google Scholar 

  13. Moussaïd, M., Perozo, N., Garnier, S., Helbing, D. & Theraulaz, G. The walking behaviour of pedestrian social groups and its impact on crowd dynamics. PLoS ONE 5, 1–7 (2010).

    Article  Google Scholar 

  14. Hemelrijk, C. K. & Kunz, H. Density distribution and size sorting in fish schools: an individual-based model. Behav. Ecol. 16, 178–187 (2005).

    Article  Google Scholar 

  15. Sueur, C., Petit, O. & Deneubourg, J. L. Short-term group fission processes in macaques: a social networking approach. J. Exp. Biol. 213, 1338–1346 (2010).

    Article  CAS  Google Scholar 

  16. Bode, N. W. F., Wood, A. J. & Franks, D. W. The impact of social networks on animal collective motion. Anim. Behav. 82, 29–38 (2011).

    Article  Google Scholar 

  17. Miguel, M. C., Parley, J. T. & Pastor-Satorras, R. Effects of heterogeneous social interactions on flocking dynamics. Phys. Rev. Lett. 120, 068303 (2018).

    Article  CAS  Google Scholar 

  18. Farine, D. R. et al. Both nearest neighbours and long-term affiliates predict individual locations during collective movement in wild baboons. Sci. Rep. 6, 1–10 (2016).

    Article  Google Scholar 

  19. Black, J. Partnerships in Birds: The Study of Monogamy (Oxford University Press, 1996).

  20. Hemelrijk, C. K. & Hildenbrandt, H. Scale-free correlations, influential neighbours and speed control in flocks of birds. J. Stat. Phys. 158, 563–578 (2014).

    Article  Google Scholar 

  21. Hemelrijk, C. K. & Hildenbrandt, H. Some causes of the variable shape of flocks of birds. PLoS ONE 6, e22479 (2011).

    Article  CAS  Google Scholar 

  22. Ballerini, M. et al. Interaction ruling animal collective behavior depends on topological rather than metric distance: evidence from a field study. Proc. Natl Acad. Sci. USA 105, 1232–1237 (2008).

    Article  CAS  Google Scholar 

  23. Cavagna, A. et al. Scale-free correlations in starling flocks. Proc. Natl Acad. Sci. USA 107, 11865–11870 (2010).

    Article  CAS  Google Scholar 

  24. Emery, N. J., Seed, A. M., Von Bayern, A. M. P. & Clayton, N. S. Cognitive adaptations of social bonding in birds. Philos. Trans. R. Soc. B 362, 489–505 (2007).

    Article  Google Scholar 

  25. Kubitza, R. J., Bugnyar, T. & Schwab, C. Pair bond characteristics and maintenance in free-flying jackdaws Corvus monedula: effects of social context and season. J. Avian Biol. 46, 206–215 (2015).

    Article  Google Scholar 

  26. Röell, A. Social behaviour of the jackdaw, Corvus monedula, in relation to its niche. Behaviour 64, 1–124 (1978).

    Article  Google Scholar 

  27. Valletta, J. J., Torney, C., Kings, M., Thornton, A. & Madden, J. Applications of machine learning in animal behaviour studies. Anim. Behav. 124, 203–220 (2017).

    Article  Google Scholar 

  28. Kings, M. Foraging Tactics and Social Networks in Wild Jackdaws. PhD thesis, University of Exeter (2018).

  29. Ling, H. et al. Simultaneous measurements of three-dimensional trajectories and wingbeat frequencies of birds in the field. J. R. Soc. Interface 15, 20180653 (2018).

    Article  Google Scholar 

  30. Katz, Y., Tunstrom, K., Ioannou, C. C., Huepe, C. & Couzin, I. D. Inferring the structure and dynamics of interactions in schooling fish. Proc. Natl Acad. Sci. USA 108, 18720–18725 (2011).

    Article  CAS  Google Scholar 

  31. Usherwood, J. R., Stavrou, M., Lowe, J. C., Roskilly, K. & Wilson, A. M. Flying in a flock comes at a cost in pigeons. Nature 474, 494–497 (2011).

    Article  CAS  Google Scholar 

  32. Tobalske, B. W., Hedrick, T. L., Dial, K. P. & Biewener, A. A. Comparative power curves in bird flight. Nature 421, 363–366 (2003).

    Article  CAS  Google Scholar 

  33. Chen, X., Dong, X., Be’Er, A., Swinney, H. L. & Zhang, H. P. Scale-invariant correlations in dynamic bacterial clusters. Phys. Rev. Lett. 108, 148101 (2012).

    Article  Google Scholar 

  34. Cavagna, A., Giardina, I. & Grigera, T. S. The physics of flocking: correlation as a compass from experiments to theory. Phys. Rep. 728, 1–62 (2018).

    Article  Google Scholar 

  35. Couzin, I. D., Krause, J., Franks, N. R. & Levin, S. A. Effective leadership and decision-making in animal groups on the move. Nature 433, 513–516 (2005).

    Article  CAS  Google Scholar 

  36. Woods, R. D., Kings, M., McIvor, G. E. & Thornton, A. Caller characteristics influence recruitment to collective anti-predator events in jackdaws. Sci. Rep. 8, 1–8 (2018).

    Article  Google Scholar 

  37. Kondo, N., Izawa, E.-I. & Watanabe, S. Crows cross-modally recognize group members but not non-group members. Proc. R. Soc. B 279, 1937–1942 (2012).

    Article  Google Scholar 

  38. Henderson, I. G., Hart, P. J. B. & Burke, T. Strict monogamy in a semi-colonial passerine: the jackdaw Corvus monedula. J. Avian Biol. 31, 177–182 (2000).

    Article  Google Scholar 

  39. Henderson, I. G. & Hart, P. J. B. Provisioning, parental investment and reproductive success in jackdaws Corvus monedula. Ornis Scand. 24, 142–148 (1993).

    Article  Google Scholar 

  40. Coombs, C. J. F. Rookeries and roosts of the rook and jackdaw in south-west Cornwall. Bird Study 8, 55–70 (1961).

    Article  Google Scholar 

  41. Zandberg, L., Jolles, J. W., Boogert, N. J. & Thornton, A. Jackdaw nestlings can discriminate between conspecific calls but do not beg specifically to their parents. Behav. Ecol. 25, 565–573 (2014).

    Article  Google Scholar 

  42. Aubin, T. & Jouventin, P. Cocktail party effect in king penguin colonies. Proc. R. Soc. B 265, 1665–1673 (1998).

    Article  Google Scholar 

  43. Hartley, R. & Zisserman, A. Multiple View Geometry in Computer Vision 2nd edn (Cambridge University Press, 2004).

  44. Theriault, D. H. et al. A protocol and calibration method for accurate multi-camera field videography. J. Exp. Biol. 217, 1843–1848 (2014).

    Article  Google Scholar 

  45. Furukawa, Y. & Ponce, J. Accurate camera calibration from multi-view stereo and bundle adjustment. Int. J. Comput. Vis. 84, 257–268 (2009).

    Article  Google Scholar 

  46. Ouellette, N. T., Xu, H. & Bodenschatz, E. A quantitative study of three-dimensional lagrangian particle tracking algorithms. Exp. Fluids 40, 301–313 (2006).

    Article  Google Scholar 

  47. Ouellette, N. T., Xu, H., Bourgoin, M. & Bodenschatz, E. An experimental study of turbulent relative dispersion models. New J. Phys. 8, 109 (2006).

    Article  Google Scholar 

  48. Kelley, D. H. & Ouellette, N. T. Emergent dynamics of laboratory insect swarms. Sci. Rep. 3, 1073 (2013).

    Article  CAS  Google Scholar 

  49. Mordant, N., Crawford, A. M. & Bodenschatz, E. Experimental lagrangian acceleration probability density function measurement. Physica D 193, 245–251 (2004).

    Article  Google Scholar 

  50. Puckett, J. G., Ni, R. & Ouellette, N. T. Time-frequency analysis reveals pairwise interactions in insect swarms. Phys. Rev. Lett. 114, 258103 (2015).

    Article  Google Scholar 

  51. Cavagna, A., Queiros, S. M. D., Giardina, I., Stefanini, F. & Viale, M. Diffusion of individual birds in starling flocks. Proc. R. Soc. B 280, 20122484 (2013).

    Article  CAS  Google Scholar 

  52. Attanasi, A. et al. Collective behaviour without collective order in wild swarms of midges. PLoS Comput. Biol. 10, e1003697 (2014).

    Article  Google Scholar 

  53. Couzin, I. D., Krause, J., James, R., Ruxton, G. D. & Franks, N. R. Collective memory and spatial sorting in animal groups. J. Theor. Biol. 218, 1–11 (2002).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a Human Frontier Science Program grant (No. RG0049/2017) to A.T., N.T.O. and R.T.V. We are grateful to P. Dunstan, R. Stone and the Gluyas family for permission to work on their land, and to V. Lee, B. Hooper, A. Hall, P. Petts, C. Peterson and J. Westley for their assistance in the field.

Author information

Authors and Affiliations

Authors

Contributions

H.L., N.T.O., A.T. and R.T.V. conceived the ideas. H.L. and N.T.O. designed the methodology. G.M. and A.T. collected the data. H.L., K.V. and N.T.O. analysed the data. G.M., H.L. and A.T. performed statistical analysis. All authors led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Corresponding authors

Correspondence to Alex Thornton or Nicholas T. Ouellette.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–12, Supplementary Tables 1–3.

Reporting Summary

Supplementary Video 1

Original images captured by one of the four cameras and the reconstructed birds’ 3D movement trajectories for flock No. 1.

Supplementary Video 2

Original images captured by one of the four cameras and the reconstructed birds’ 3D movement trajectories for flock No. 2.

Supplementary Video 3

Original images captured by one of the four cameras and the reconstructed birds’ 3D movement trajectories for flock No. 3.

Supplementary Video 4

Original images captured by one of the four cameras and the reconstructed birds’ 3D movement trajectories for flock No. 4.

Supplementary Video 5

Original images captured by one of the four cameras and the reconstructed birds’ 3D movement trajectories for flock No. 5.

Supplementary Video 6

Original images captured by one of the four cameras and the reconstructed birds’ 3D movement trajectories for flock No. 6.

Supplementary Data 1

Bird ID number, position, time, velocity, acceleration and wingbeat frequency at every time step for flock No. 1.

Supplementary Data 2

Bird ID number, position, time, velocity, acceleration and wingbeat frequency at every time step for flock No. 2.

Supplementary Data 3

Bird ID number, position, time, velocity, acceleration and wingbeat frequency at every time step for flock No. 3.

Supplementary Data 4

Bird ID number, position, time, velocity, acceleration and wingbeat frequency at every time step for flock No. 4.

Supplementary Data 5

Bird ID number, position, time, velocity, acceleration and wingbeat frequency at every time step for flock No. 5.

Supplementary Data 6

Bird ID number, position, time, velocity, acceleration and wingbeat frequency at every time step for flock No. 6.

Supplementary Data 7

Bird ID number, position, time, velocity, acceleration and wingbeat frequency at every time step for 305 isolated pairs (birds with id 1 & 2, 3 & 4, 5 & 6 and so on are from a single pair).

Supplementary Data 8

Text file that includes mean wingbeat frequency, flight speed and local density (approximated by the number of neighbours within a distance of 5 m of the focal bird) for paired and unpaired birds in six flocks, as well as for birds flying alone.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ling, H., Mclvor, G.E., van der Vaart, K. et al. Costs and benefits of social relationships in the collective motion of bird flocks. Nat Ecol Evol 3, 943–948 (2019). https://doi.org/10.1038/s41559-019-0891-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-019-0891-5

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing