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.

Ageing red deer alter their spatial behaviour and become less social

Nature Ecology & Evolution volume 6, pages 1231–1238 (2022)Cite this article

Subjects

Abstract

Social relationships are important to many aspects of animals’ lives, and an individual’s connections may change over the course of their lifespan. Currently, it is unclear whether social connectedness declines within individuals as they age, and what the underlying mechanisms might be, so the role of age in structuring animal social systems remains unresolved, particularly in non-primates. Here we describe senescent declines in social connectedness using 46 years of data in a wild, individually monitored population of a long-lived mammal (European red deer, Cervus elaphus). Applying a series of spatial and social network analyses, we demonstrate that these declines occur because of within-individual changes in social behaviour, with correlated changes in spatial behaviour (smaller home ranges and movements to lower-density, lower-quality areas). These findings demonstrate that within-individual socio-spatial behavioural changes can lead older animals in fission–fusion societies to become less socially connected, shedding light on the ecological and evolutionary processes structuring wild animal populations.

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

Learn more

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

Fig. 1: Ageing was associated with reduction in social connectedness.
Fig. 2: The spatial distributions of age of mature females and grazing quality within the study area.
Fig. 3: Ageing was associated with changes in a range of socio-spatial behaviours.

Data availability

All data are available at https://github.com/gfalbery/Lonely-Old-Deers.

Code availability

All code are available at https://github.com/gfalbery/Lonely-Old-Deers.

References

  1. White, L. A., Forester, J. D. & Craft, M. E. Using contact networks to explore mechanisms of parasite transmission in wildlife. Biol. Rev. 92, 389–409 (2017).

    Article  PubMed  Google Scholar 

  2. Silk, M. J. et al. Using social network measures in wildlife disease ecology, epidemiology, and management. Bioscience 67, 245–257 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Albery, G. F., Kirkpatrick, L., Firth, J. A. & Bansal, S. Unifying spatial and social network analysis in disease ecology. J. Anim. Ecol. 90, 1–17 (2021).

    Article  Google Scholar 

  4. Evans, J. C., Silk, M. J., Boogert, N. J. & Hodgson, D. J. Infected or informed? Social structure and the simultaneous transmission of information and infectious disease. Oikos 129, 1271–1288 (2020).

    Article  Google Scholar 

  5. Aplin, L. M., Sheldon, B. C. & Morand-Ferron, J. Milk bottles revisited: social learning and individual variation in the blue tit, Cyanistes caeruleus. Anim. Behav. 85, 1225–1232 (2013).

    Article  Google Scholar 

  6. Silk, J. B. The adaptive value of sociality in mammalian groups. Phil. Trans. R. Soc. Lond. B 362, 539–559 (2007).

    Article  Google Scholar 

  7. Snyder-Mackler, N. et al. Social determinants of health and survival in humans and other animals. Science 368, eaax9553 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Machanda, Z. P. & Rosati, A. G. Shifting sociality during primate ageing. Phil. Trans. R. Soc. B 375, 20190620 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Nussey, D. H., Coulson, T., Festa-Bianchet, M. & Gaillard, J. M. Measuring senescence in wild animal populations: towards a longitudinal approach. Funct. Ecol. 22, 393–406 (2008).

    Article  Google Scholar 

  10. van de Pol, M. & Verhulst, S. Age-dependent traits: a new statistical model to separate within- and between-individual effects. Am. Nat. 167, 766–773 (2006).

    Article  PubMed  Google Scholar 

  11. Froy, H. et al. Declining home range area predicts reduced late-life survival in two wild ungulate populations. Ecol. Lett. 21, 1001–1009 (2018).

    Article  PubMed  Google Scholar 

  12. Rosati, A. G. et al. Social selectivity in aging wild chimpanzees. Science 370, 473–476 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kim, S.-Y., Torres, R., Rodriguez, C. & Drummond, H. Effects of breeding success, mate fidelity and senescence on breeding dispersal of male and female blue-footed boobies. J. Anim. Ecol. 76, 471–479 (2007).

    Article  PubMed  Google Scholar 

  14. Webber, Q. M. R. & Vander Wal, E. An evolutionary framework outlining the integration of individual social and spatial ecology. J. Anim. Ecol. 87, 113–127 (2018).

    Article  PubMed  Google Scholar 

  15. Webber, Q. M. R. & Vander Wal, E. Trends and perspectives on the use of animal social network analysis in behavioural ecology: a bibliometric approach. Anim. Behav. 149, 77–87 (2019).

    Article  Google Scholar 

  16. Siracusa, E. R., Higham, J. P., Snyder-mackler, N. & Brent, L. J. N. Social ageing: exploring the drivers of late-life changes in social behaviour in mammals. Biol. Lett. 18, 20210643 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Elliott, K. H. et al. Ageing gracefully: physiology but not behaviour declines with age in a diving seabird. Funct. Ecol. 29, 219–228 (2015).

    Article  Google Scholar 

  18. Aartsen, M. J., Van Tilburg, T., Smits, C. H. M. & Knipscheer, K. C. P. M. A longitudinal study of the impact of physical and cognitive decline on the personal network in old age. J. Soc. Pers. Relat. 21, 249–266 (2004).

    Article  Google Scholar 

  19. Brent, L. J. N., Ruiz-Lambides, A. & Platt, M. L. Family network size and survival across the lifespan of female macaques. Proc. R. Soc. B 284, 20170515 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Turner, J. W., Robitaille, A. L., Bills, P. S. & Holekamp, K. E. Early-life relationships matter: social position during early life predicts fitness among female spotted hyenas. J. Anim. Ecol. 90, 183–196 (2021).

    Article  PubMed  Google Scholar 

  21. Almeling, L., Hammerschmidt, K., Sennhenn-Reulen, H., Freund, A. M. & Fischer, J. Motivational shifts in aging monkeys and the origins of social selectivity. Curr. Biol. 26, 1744–1749 (2016).

    Article  CAS  PubMed  Google Scholar 

  22. Albery, G. F. et al. Multiple spatial behaviours govern social network positions in a wild ungulate. Ecol. Lett. 24, 676–686 (2021).

    Article  PubMed  Google Scholar 

  23. Sanchez, J. N. & Hudgens, B. R. Interactions between density, home range behaviors, and contact rates in the Channel Island fox (Urocyon littoralis). Ecol. Evol. 5, 2466–2477 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Shizuka, D. & Johnson, A. E. How demographic processes shape animal social networks. Behav. Ecol. https://doi.org/10.1093/beheco/arz083 (2019).

  25. Krause, J., James, R., Franks, D. W. & Croft, D. P. Animal Social Networks (Oxford Univ. Press, 2015).

  26. Firth, J. A. et al. Wild birds respond to flockmate loss by increasing their social network associations to others. Proc. R. Soc. B 284, 20170299 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Evans, J. C., Liechti, J. I., Boatman, B. & König, B. A natural catastrophic turnover event: individual sociality matters despite community resilience in wild house mice. Proc. R. Soc. B 287, 20192880 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Rathke, E. & Fischer, J. Social aging in male and female Barbary macaques. Am. J. Primatol. https://doi.org/10.1002/ajp.23272 (2021).

  29. Kroeger, S. B., Blumstein, D. T. & Martin, J. G. A. A. How social behaviour and life-history traits change with age and in the year prior to death in female yellow-bellied marmots. Phil. Trans. R. Soc. B 376, 20190745 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Brambilla, A., von Hardenberg, A., Sueur, C., Canedoli, C. & Stanley, C. Long term analysis of social structure: evidence of age-based consistent associations in Alpine ibex. bioRxiv 1–42 (2021).

  31. González, N. T. et al. Age-related change in adult chimpanzee social network integration. Evol. Med. Public Health 9, 448–459 (2021).

    Article  Google Scholar 

  32. Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. Red Deer: Behavior and Ecology of Two Sexes. Vol. 15 (Univ. Chicago Press, 1982).

  33. Nussey, D. H., Kruuk, L. E. B., Donald, A., Fowlie, M. & Clutton-Brock, T. H. The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecol. Lett. 9, 1342–1350 (2006).

    Article  PubMed  Google Scholar 

  34. Croft, D. P., James, R. & Krause, J. Exploring Animal Social Networks (Princeton Univ. Press, 2008).

  35. Tobler, W. R. A computer movie simulating urban growth in the Detroit region. Econ. Geogr. 46, 234 (1970).

    Article  Google Scholar 

  36. Firth, J. A. & Sheldon, B. C. Social carry-over effects underpin trans-seasonally linked structure in a wild bird population. Ecol. Lett. 19, 1324–1332 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Spiegel, O., Leu, S. T., Sih, A. & Bull, C. M. Socially interacting or indifferent neighbours? Randomization of movement paths to tease apart social preference and spatial constraints. Methods Ecol. Evol. https://doi.org/10.1111/2041-210X.12553 (2016).

  38. Nussey, D. H. et al. The relationship between tooth wear, habitat quality and late-life reproduction in a wild red deer population. J. Anim. Ecol. 76, 402–412 (2007).

    Article  PubMed  Google Scholar 

  39. Loe, L. E., Mysterud, A., Langvatn, R. & Stenseth, N. C. Decelerating and sex-dependent tooth wear in Norwegian red deer. Oecologia 135, 346–353 (2003).

    Article  PubMed  Google Scholar 

  40. Peignier, M. et al. Space use and social association in a gregarious ungulate: testing the conspecific attraction and resource dispersion hypotheses. Ecol. Evol. 9, 5133–5145 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Franks, D. W., Ruxton, G. D. & James, R. Sampling animal association networks with the gambit of the group. Behav. Ecol. Sociobiol. 64, 493–503 (2010).

    Article  Google Scholar 

  42. Patterson, S. K., Strum, S. C. & Silk, J. B. Resource competition shapes female–female aggression in olive baboons, Papio anubis. Anim. Behav. 176, 23–41 (2021).

    Article  Google Scholar 

  43. Kays, R., Crofoot, M. C., Jetz, W. & Wikelski, M. Terrestrial animal tracking as an eye on life and planet. Science 348, aaa2478 (2015).

    Article  PubMed  CAS  Google Scholar 

  44. Gilbertson, M. L. J., White, L. A. & Craft, M. E. Trade‐offs with telemetry‐derived contact networks for infectious disease studies in wildlife. Methods Ecol. Evol. https://doi.org/10.1111/2041-210X.13355 (2020).

  45. Froy, H. et al. Senescence in immunity against helminth parasites predicts adult mortality in a wild mammal. Science 365, 1296–1298 (2019).

    Article  CAS  PubMed  Google Scholar 

  46. Siracusa, E. R. et al. Familiar neighbors, but not relatives, enhance fitness in a territorial mammal. Curr. Biol. 31, 438–445.e3 (2021).

    Article  CAS  PubMed  Google Scholar 

  47. Nussey, D. H., Kruuk, L. E. B., Morris, A. & Clutton-Brock, T. H. Environmental conditions in early life influence ageing rates in a wild population of red deer. Curr. Biol. 17, 1000–1001 (2007).

    Article  CAS  Google Scholar 

  48. Castles, M. et al. Social networks created with different techniques are not comparable. Anim. Behav. 96, 59–67 (2014).

    Article  Google Scholar 

  49. Froy, H., Walling, C. A., Pemberton, J. M., Clutton-brock, T. H. & Kruuk, L. E. B. Relative costs of offspring sex and offspring survival in a polygynous mammal. Biol. Lett. 12, 20160417 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E. Fitness costs of gestation and lactation in wild mammals. Nature 337, 260–262 (1989).

    Article  CAS  PubMed  Google Scholar 

  51. Cairns, S. J. & Schwager, S. J. A comparison of association indices. Anim. Behav. 35, 1454–1469 (1987).

    Article  Google Scholar 

  52. Brent, L. J. N. Friends of friends: are indirect connections in social networks important to animal behaviour? Anim. Behav. 103, 211–222 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Whitehead, H. Analyzing Animal Societies: Quantitative Methods for Vertebrate Social Analysis (Univ. Chicago Press, 2008).

  54. Calenge, C. Home range estimation in R: the adehabitatHR package. https://cran.r-project.org/web/packages/adehabitatHR/index.html (2011).

  55. Lindgren, F. & Rue, H. Bayesian spatial modelling with R-INLA. J. Stat. Softw. 63, 1–25 (2015).

    Article  Google Scholar 

  56. Rue, H. & Martino, S. Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. Stat. Methodol. 71, 319–392 (2009).

    Article  Google Scholar 

  57. Bakka, H. et al. Spatial modelling with R-INLA: a review. WIREs Comput. Stat. 10, e1443 (2018).

    Article  Google Scholar 

  58. Lindgren, F., Rue, H. & Lindstrom, J. An explicit link between Gaussian fields and Gaussian Markov random fields: the stochastic partial differential equation approach. J. R. Stat. Soc. B 73, 423–498 (2011).

    Article  Google Scholar 

Download references

Acknowledgements

We thank NatureScot and its predecessors for permission to work on the Isle of Rum NNR. The field project has been supported by grants mainly from the UK NERC with some additional funding from BBSRC, the Royal Society and ERC. We thank all who have contributed to the maintenance of the project over time, especially L. Kruuk. We thank multiple dedicated field workers who have contributed to field data collection, especially F. Guinness, who collected the first 20 years of census data. G.F.A. was funded by NSF grant number 1414296, and by a Bruce McEwen Career Development Fellowship from the NIH Animal Models for the Social Dimensions of Health and Aging Research Network (NIH/NIH R24 AG065172). J.A.F. was supported by BBSRC (BB/S009752/1) and funding from NERC (NE/S010335/1).

Author information

Authors and Affiliations

  1. Department of Biology, Georgetown University, Washington DC, USA

    Gregory F. Albery

  2. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, UK

    Gregory F. Albery, Alison Morris, Sean Morris, Josephine M. Pemberton & Daniel H. Nussey

  3. Wissenschaftskolleg zu Berlin, Berlin, Germany

    Gregory F. Albery

  4. Department of Zoology, University of Cambridge, Cambridge, UK

    Tim H. Clutton-Brock

  5. Department of Zoology, University of Oxford, Oxford, UK

    Josh A. Firth

  6. Merton College, University of Oxford, Oxford, UK

    Josh A. Firth

Authors
  1. Gregory F. Albery
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tim H. Clutton-Brock
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alison Morris
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sean Morris
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Josephine M. Pemberton
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Daniel H. Nussey
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Josh A. Firth
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

G.F.A., D.H.N. and J.A.F. devised the analysis; G.F.A. carried out the analysis and wrote the manuscript. A.M. and S.M. collected behavioural data. T.H.C.-B., J.M.P., D.H.N. and J.A.F. commented on the manuscript. T.H.C.-B. and J.M.P. oversaw wider running of the project.

Corresponding author

Correspondence to Gregory F. Albery.

Ethics declarations

Competing interests

We declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks the anonymous reviewers for their contribution to the peer review of this work.

Additional information

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

Extended data

Extended Data Fig. 1 Model effect estimates investigating how selective disappearance drives age-related changes in spatial behaviour (Model Set 5).

Each panel displays the model effect estimates for age and longevity for each spatial metric, demonstrating that selective disappearance was not responsible for the age-related changes in spatial behaviour, except in the case of density (a). Dots represent the mean of the posterior effect estimate distribution; error bars denote the 95% credibility intervals of the effect. The y axis is in units of standard deviations. NB density and centroid distance did not have an SPDE effect fitted to control for spatial autocorrelation because they are deterministically distributed in space, such that the SPDE effect would be uninformative.

Extended Data Fig. 2 Model estimates describing associations between spatial behaviours and social behaviours, and age-related declines in social behaviour when these variables were accounted for (Model Set 6).

Dots represent the mean of the posterior effect estimate distribution; error bars denote the 95% credibility intervals of the effect. These estimates are displayed both for the base model (a) and the SPDE model (b). HRA = home range area.

Extended Data Fig. 3 Model estimates for age effects on sociality in our longevity models (blue colours; Model Set 2); and in the same models with spatial behaviours accounted for (red colours; Model set 6).

Dots represent the mean of the posterior effect estimate distribution; error bars denote the 95% credibility intervals of the effect. Panel a displays the effects without an SPDE effect fitted; panel B displays the same effects with SPDE fitted.

Extended Data Fig. 4 Pairwise correlations among social (A) and spatial (B) behavioural metrics.

Panels that are more blue are more negative; panels that are more red are more positive.

Supplementary information

Supplementary Information

Tables of model effect estimates.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Albery, G.F., Clutton-Brock, T.H., Morris, A. et al. Ageing red deer alter their spatial behaviour and become less social. Nat Ecol Evol 6, 1231–1238 (2022). https://doi.org/10.1038/s41559-022-01817-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-022-01817-9

This article is cited by

Search

Advanced 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