, Volume 181, Issue 3, pp 865–871 | Cite as

Spatial variation in senescence rates in a bird metapopulation

  • H. HolandEmail author
  • T. Kvalnes
  • M. Gamelon
  • J. Tufto
  • H. Jensen
  • H. Pärn
  • T. H. Ringsby
  • B.-E. Sæther
Population ecology – original research


Investigating factors which affect the decline in survival with age, i.e. actuarial senescence, is important in order to understand how demographic rates vary in wild populations. Although the evidence for the occurrence of actuarial senescence in wild populations is growing, very few studies have compared actuarial senescence rates between wild populations of the same species. We used data from a long-time study of demography of house sparrows (Passer domesticus) to investigate differences in rates of actuarial senescence between habitats and sub-populations. We also investigated whether rates of actuarial senescence differed between males and females. We found that rates of actuarial senescence showed large spatial variation. We also found that the onset of actuarial senescence varied between sub-populations. However, these differences were not significantly explained by a general difference in habitat type. We also found no significant difference in actuarial senescence rates between males and females. This study shows that senescence rates in natural populations may vary significantly between sub-populations and that failing to account for such differences may give a biased estimate of senescence rates of a species.


Ageing House sparrow Metapopulation Senescence Spatial 



We would like to thank everyone involved in the House Sparrow Project for help with fieldwork. We are also grateful to everyone at Centre for Biodiversity Dynamics at the Department of Biology, NTNU, for helpful comments and help with statistics in R. This study was supported by Grants from the Research Council of Norway (FRIMEDBIO 204303 and 221956, SFF 223257), the European Research Council (ERC-2010-AdG 268562), and NTNU. The research was carried out in accordance with permits from the Norwegian Environment Agency and the Bird Ringing Centre at Stavanger Museum, Norway.

Author contribution statement

H. H wrote the manuscript. H. H, T. K, H. J, H. P, T. H. R contributed to field work and data collection. H. H, T. K, J. T conducted the analysis. H. H, T. H. R, B. E. S conceived the study. All authors contributed to the interpretation of results and revisions of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Supplementary material

442_2016_3615_MOESM1_ESM.docx (46 kb)
Supplementary material 1 (DOCX 46 kb)


  1. Altwegg R, Roulin A, Kestenholz M, Jenni L (2003) Variation and covariation in survival, dispersal, and population size in barn owls Tyto alba. J Anim Ecol 72:391–399CrossRefGoogle Scholar
  2. Anderson TR (2006) Biology of the ubiquitous house sparrow: from genes to populations. Oxford University Press, New YorkCrossRefGoogle Scholar
  3. Austad SN (1993) Retarded senescence in an insular population of Virginia opossums (Didelphis virginiana). J Zool 229:695–708CrossRefGoogle Scholar
  4. Baalsrud HT et al (2014) Effects of population characteristics and structure on estimates of effective population size in a house sparrow metapopulation. Mol Ecol 23:2653–2668CrossRefPubMedGoogle Scholar
  5. Baker JD, Thompson PM (2007) Temporal and spatial variation in age-specific survival rates of a long-lived mammal, the Hawaiian monk seal. Proc R Soc Lond B 274:407–415CrossRefGoogle Scholar
  6. Balbontin J, Møller AP (2015) Environmental conditions during early life accelerate the rate of senescence in a short-lived passerine bird. Ecology 96:948–959CrossRefPubMedGoogle Scholar
  7. Balbontin J, Møller AP, Hermosell IG, Marzal A, Reviriego M, de Lope F (2012) Geographical variation in reproductive ageing patterns and life-history strategy of a short-lived passerine bird. J Evol Biol 25:2298–2309CrossRefPubMedGoogle Scholar
  8. Bonduriansky R, Maklakov A, Zajitschek F, Brooks R (2008) Sexual selection, sexual conflict and the evolution of ageing and life span. Funct Ecol 22:443–453CrossRefGoogle Scholar
  9. Bouwhuis S, van Noordwijk AJ, Sheldon BC, Verhulst S, Visser ME (2010) Similar patterns of age-specific reproduction in an island and mainland population of great tits Parus major. J Avian Biol 41:615–620CrossRefGoogle Scholar
  10. Brooks SP, Gelman A (1998) General methods for monitoring convergence of iterative simulations. J Comput Graph Stat 7:434–455Google Scholar
  11. Brown WP, Roth RR (2009) Age-specific reproduction and survival of individually marked Wood Thrushes, Hylocichla mustelina. Ecology 90:218–229CrossRefPubMedGoogle Scholar
  12. Brunet-Rossinni AK, Austad SN (2006) Senescence in wild populations of mammals and birds. Handb Biol Aging 6:243–266Google Scholar
  13. Cartwright SJ, Nicoll MAC, Jones CG, Tatayah V, Norris K (2014) Anthropogenic natal environmental effects on life histories in a wild bird population. Curr Biol 24:536–540CrossRefPubMedPubMedCentralGoogle Scholar
  14. Caswell H (2007) Extrinsic mortality and the evolution of senescence. Trends Ecol Evol 22:173–174CrossRefPubMedGoogle Scholar
  15. Clutton-Brock TH, Isvaran K (2007) Sex differences in ageing in natural populations of vertebrates. Proc R Soc Lond B 274:3097–3104CrossRefGoogle Scholar
  16. Core Team R (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  17. Cornwallis CK, Dean R, Pizzari T (2014) Sex-specific patterns of aging in sexual ornaments and gametes. Am Nat 184:E66–E78CrossRefPubMedGoogle Scholar
  18. Dhondt AA, Kempenaers B, Clobert J (1998) Sparrowhawk Accipiter nisus predation and blue tit Parus caeruleus adult annual survival rate. Ibis 140:580–584CrossRefGoogle Scholar
  19. Festa-Bianchet M (2012) The cost of trying: weak interspecific correlations among life-history components in male ungulates. Can J Zool 90:1072–1085CrossRefGoogle Scholar
  20. Gaillard JM, Festa-Bianchet M, Yoccoz NG, Loison A, Toigo C (2000) Temporal variation in fitness components and population dynamics of large herbivores. Annu Rev Ecol Syst 31:367–393CrossRefGoogle Scholar
  21. Gamelon M et al (2014) Do age-specific survival patterns of wild boar fit current evolutionary theories of senescence? Evolution 68:3636–3643CrossRefPubMedGoogle Scholar
  22. Hamilton WD (1966) Moulding of senescence by natural selection. J Theor Biol 12:12–45CrossRefPubMedGoogle Scholar
  23. Hammers M, Richardson DS, Burke T, Komdeur J (2013) The impact of reproductive investment and early-life environmental conditions on senescence: support for the disposable soma hypothesis. J Evol Biol 26:1999–2007CrossRefPubMedGoogle Scholar
  24. Hayward AD et al (2015) Asynchrony of senescence among phenotypic traits in a wild mammal population. Exp Gerontol 71:56–68CrossRefPubMedPubMedCentralGoogle Scholar
  25. Holand H et al (2014) Lower survival probability of house sparrows severely infected by the gapeworm parasite. J Avian Biol 45:365–373CrossRefGoogle Scholar
  26. Jensen H, Steinsland I, Ringsby TH, Sæther B-E (2008) Evolutionary dynamics of a sexual ornament in the house sparrow (Passer domesticus): the role of indirect selection within and between sexes. Evolution 62:1275–1293CrossRefPubMedGoogle Scholar
  27. Jones OR et al (2008) Senescence rates are determined by ranking on the fast–slow life-history continuum. Ecol Lett 11:664–673CrossRefPubMedGoogle Scholar
  28. Kawasaki N, Brassil CE, Brooks RC, Bonduriansky R (2008) Environmental effects on the expression of life span and aging: an extreme contrast between wild and captive cohorts of Telostylinus angusticollis (Diptera: Neriidae). Am Nat 172:346–357CrossRefPubMedGoogle Scholar
  29. Kéry M, Schaub M (2011) Bayesian population analysis using WinBUGS. Academic, LondonGoogle Scholar
  30. Kirkwood TBL (1977) Evolution of aging. Nature 270:301–304CrossRefPubMedGoogle Scholar
  31. Lebreton JD, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals—a unified approach with case-studies. Ecol Monogr 62:67–118CrossRefGoogle Scholar
  32. Lemaitre JF et al (2015) Early-late life trade-offs and the evolution of ageing in the wild. Proc R Soc Lond B 282:10CrossRefGoogle Scholar
  33. Liker A, Szekely T (2005) Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59:890–897CrossRefPubMedGoogle Scholar
  34. Lunn DJ, Thomas A, Best N, Spiegelhalter D (2000) WinBUGS—a Bayesian modelling framework: concepts, structure, and extensibility. Stat Comput 10:325–337CrossRefGoogle Scholar
  35. Maklakov AA, Lummaa V (2013) Evolution of sex differences in lifespan and aging: causes and constraints. BioEssays 35:717–724CrossRefPubMedGoogle Scholar
  36. McCleery RH, Clobert J, Julliard R, Perrins CM (1996) Nest predation and delayed cost of reproduction in the great tit. J Anim Ecol 65:96–104CrossRefGoogle Scholar
  37. Medawar PB (1952) An unsolved problem of biology. Lewis, LondonGoogle Scholar
  38. Millon A, Petty SJ, Little B, Lambin X (2011) Natal conditions alter age-specific reproduction but not survival or senescence in a long-lived bird of prey. J Anim Ecol 80:968–975CrossRefPubMedGoogle Scholar
  39. Nussey DH, Kruuk LEB, Morris A, Clutton-Brock TH (2007) Environmental conditions in early life influence ageing rates in a wild population of red deer. Curr Biol 17:R1000–R1001CrossRefPubMedGoogle Scholar
  40. Nussey DH, Coulson T, Festa-Bianchet M, Gaillard JM (2008) Measuring senescence in wild animal populations: towards a longitudinal approach. Funct Ecol 22:393–406CrossRefGoogle Scholar
  41. Nussey DH, Kruuk LEB, Morris A, Clements MN, Pemberton JM, Clutton-Brock TH (2009) Inter- and intrasexual variation in aging patterns across reproductive traits in a wild red deer population. Am Nat 174:342–357CrossRefPubMedGoogle Scholar
  42. Nussey DH, Froy H, Lemaitre JF, Gaillard JM, Austad SN (2013) Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res Rev 12:214–225CrossRefPubMedGoogle Scholar
  43. Orell M, Belda EJ (2002) Delayed cost of reproduction and senescence in the willow tit Parus montanus. J Anim Ecol 71:55–64CrossRefGoogle Scholar
  44. Pardo D, Barbraud C, Weimerskirch H (2013) Females better face senescence in the wandering albatross. Oecologia 173:1283–1294CrossRefPubMedGoogle Scholar
  45. Pärn H, Jensen H, Ringsby TH, Sæther B-E (2009) Sex-specific fitness correlates of dispersal in a house sparrow metapopulation. J Anim Ecol 78:1216–1225CrossRefPubMedGoogle Scholar
  46. Pärn H, Ringsby TH, Jensen H, Sæther B-E (2012) Spatial heterogeneity in the effects of climate and density-dependence on dispersal in a house sparrow metapopulation. Proc R Soc Lond B 279:144–152CrossRefGoogle Scholar
  47. Peron G, Gimenez O, Charmantier A, Gaillard JM, Crochet PA (2010) Age at the onset of senescence in birds and mammals is predicted by early-life performance. Proc R Soc Lond B 277:2849–2856CrossRefGoogle Scholar
  48. Plummer M (2003) JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. In: Proceedings of the 3rd international workshop on distributed statistical computing, Vienna, AustriaGoogle Scholar
  49. Reed TE, Kruuk LEB, Wanless S, Frederiksen M, Cunningham EJA, Harris MP (2008) Reproductive senescence in a long-lived seabird: rates of decline in late-life performance are associated with varying costs of early reproduction. Am Nat 171:E89–E101CrossRefPubMedGoogle Scholar
  50. Regan JC, Partridge L (2013) Gender and longevity: Why do men die earlier than women? Comparative and experimental evidence. Best Pract Res Clin Endocrinol Metab 27:467–479CrossRefPubMedGoogle Scholar
  51. Reid JM, Bignal EM, Bignal S, McCracken DI, Monaghan P (2003) Age-specific reproductive performance in red-billed choughs Pyrrhocorax pyrrhocorax: patterns and processes in a natural population. J Anim Ecol 72:765–776CrossRefGoogle Scholar
  52. Ringsby TH, Sæther B-E, Solberg EJ (1998) Factors affecting juvenile survival in House Sparrow Passer domesticus. J Avian Biol 29:241–247CrossRefGoogle Scholar
  53. Ringsby TH, Sæther B-E, Altwegg R, Solberg EJ (1999) Temporal and spatial variation in survival rates of a house sparrow, Passer domesticus, metapopulation. Oikos 85:419–425CrossRefGoogle Scholar
  54. Ringsby TH, Sæther B-E, Tufto J, Jensen H, Solberg EJ (2002) Asynchronous spatiotemporal demography of a house sparrow metapopulation in a correlated environment. Ecology 83:561–569CrossRefGoogle Scholar
  55. Sæther B-E, Ringsby TH, Bakke O, Solberg EJ (1999) Spatial and temporal variation in demography of a house sparrow metapopulation. J Anim Ecol 68:628–637CrossRefGoogle Scholar
  56. Weimerskirch H (1992) Reproductive effort in long-lived birds—age-specific patterns of condition, reproduction and survival in the wandering albatross. Oikos 64:464–473CrossRefGoogle Scholar
  57. Williams GC (1957) Pleiotropy, natural-selection, and the evolution of senescence. Evolution 11:398–411CrossRefGoogle Scholar
  58. Zhang H, Rebke M, Becker PH, Bouwhuis S (2015) Fitness prospects: effects of age, sex and recruitment age on reproductive value in a long-lived seabird. J Anim Ecol 84:199–207CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • H. Holand
    • 1
    Email author
  • T. Kvalnes
    • 1
  • M. Gamelon
    • 1
  • J. Tufto
    • 2
  • H. Jensen
    • 1
  • H. Pärn
    • 1
  • T. H. Ringsby
    • 1
  • B.-E. Sæther
    • 1
  1. 1.Department of Biology, Centre for Biodiversity DynamicsNorwegian University of Science and Technology (NTNU)TrondheimNorway
  2. 2.Department of Mathematics, Centre for Biodiversity DynamicsNorwegian University of Science and Technology (NTNU)TrondheimNorway

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