, Volume 173, Issue 1, pp 151–160 | Cite as

Temporal variation of juvenile survival in a long-lived species: the role of parasites and body condition

  • Guillaume Souchay
  • Gilles Gauthier
  • Roger Pradel
Population ecology - Original research


Studies of population dynamics of long-lived species have generally focused on adult survival because population growth should be most sensitive to this parameter. However, actual variations in population size can often be driven by other demographic parameters, such as juvenile survival, when they show high temporal variability. We used capture–recapture data from a long-term study of a hunted, migratory species, the greater snow goose (Chen caerulescens atlantica), to assess temporal variability in first-year survival and the relative importance of natural and hunting mortality. We also conducted a parasite-removal experiment to determine the effect of internal parasites and body condition on temporal variation in juvenile survival. We found that juvenile survival showed a higher temporal variability than adult survival and that natural mortality was more important than hunting mortality, unlike in adults. Parasite removal increased first-year survival and reduced its annual variability in females only. Body condition at fledging was also positively correlated with first-year survival in treated females. With reduced parasite load, females, which are thought to invest more in their immune system than males according to Bateman’s principle, could probably reallocate more energy to growth than males, leading to a higher survival. Treated birds also had a higher survival than control ones during their second year, suggesting a developmental effect that manifested later in life. Our study shows that natural factors such as internal parasites may be a major source of variation in juvenile survival of a long-lived, migratory bird, which has implications for its population dynamics.


Elasticity Mortality Cestodes Body mass Geese 



Funding was provided by the Natural Sciences and Engineering Research Council of Canada, the Arctic Goose Joint Venture (Canadian Wildlife Service), the Centre d’Étude Nordiques, the Department of Indian and Northern Affairs Canada and by the International Research Group Dynamics of Biodiversity and Life-History traits. Logistic support in the Arctic was generously provided by the Polar Continental Shelf Project (Natural Resources Canada) and assistance in the field by Parks Canada and the Hunter and Trappers Association of Pond Inlet. Droncit, the anthelmintic drug, was provided by Bayer Canada. Finally, we are grateful to the numerous field assistants that helped with goose banding and especially Gérald Picard, to hunters who reported the banded birds that they shot and to Marie-Christine Cadieux for managing the database and for assistance in the field.

Supplementary material

442_2013_2613_MOESM1_ESM.docx (21 kb)
Supplementary material 1 (DOCX 21 kb)


  1. Alisauskas RT, Drake KL, Slattery SM, Kellett DK (2006) Neckbands, harvest, and survival of Ross’s geese from Canada’s Central Arctic. J Wildl Manage 70:89–100CrossRefGoogle Scholar
  2. Amundson CL, Arnold TW (2010) Anthelmintics increase survival of American coot (Fulica americana) chicks. Auk 127:653–659. doi: 10.1525/auk.2010.09162 CrossRefGoogle Scholar
  3. Anderson MG, Lindberg MS, Emery RB (2001) Probability of survival and breeding for juvenile female canvasbacks. J Wildl Manage 65:385–397CrossRefGoogle Scholar
  4. Arlettaz R, Schaad M, Reichlin TS, Schaub M (2010) Impact of weather and climate variation on hoopoe reproductive ecology and population growth. J Ornithol 151:889–899. doi: 10.1007/s10336-010-0527-7 CrossRefGoogle Scholar
  5. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368. doi: 10.1038/hdy.1948.21 PubMedCrossRefGoogle Scholar
  6. Benton TG, Plaistow SJ, Coulson TN (2006) Complex population dynamics and complex causation: devils, details and demography. Proc R Soc B Biol Sci 273:1173–1181. doi: 10.1098/rspb.2006.3495 CrossRefGoogle Scholar
  7. Bogdanova MI, Nager RG, Monaghan P (2007) Age of the incubating parents affects nestling survival: an experimental study of the herring gull Larus argentatus. J Avian Biol 38:83–93CrossRefGoogle Scholar
  8. Braasch A, Schauroth C, Becker PH (2009) Post-fledging body mass as a determinant of subadult survival in common terns Sterna hirundo. J Ornithol p 150. doi: 10.1007/s10336-008-0362-2
  9. Bradley JS, Wooler RD (1991) Philopatry and age of first-breeding in long-lived birds. Acta XX Congr Int Ornithol 1657–1665Google Scholar
  10. Brown CR, Brown MB (2004) Group size and ectoparasitism affect daily survival probability in a colonial bird. Behav Ecol Sociobiol 56:498–511. doi: 10.1007/s00265-004-0813-6 Google Scholar
  11. Burnham KP, Anderson DA (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  12. Calvert AM, Gauthier G (2005) Effects of exceptional conservation measures on survival and seasonal hunting mortality in greater snow geese. J Appl Ecol 42:442–452. doi: 10.1111/j.1365-2664.2005.01042.x CrossRefGoogle Scholar
  13. Cam E, Aubry L (2011) Early development, recruitment and life history trajectory in long-lived birds. J Ornithol 152:187–201. doi: 10.1007/s10336-011-0707-0 CrossRefGoogle Scholar
  14. Cattadori IM, Haydon DT, Hudson PJ (2005) Parasites and climate synchronize red grouse populations. Nature 433:737–741. doi: 10.1038/nature03276 PubMedCrossRefGoogle Scholar
  15. Choquet R, Lebreton JD, Gimenez O, Reboulet AM, Pradel R (2009a) U-CARE: utilities for performing goodness of fit tests and manipulating CApture-REcapture data. Ecography 32:1071–1074. doi: 10.1111/j.1600-0587.2009.05968.x CrossRefGoogle Scholar
  16. Choquet R, Rouan L, Pradel R (2009b) Program E-Surge: a software application for fitting multievent models. In: Thomson DL, Cooch EG, Conroy MJ (eds) Modeling demographic processes in marked populations, vol 3. Springer, New York, pp 845–865. doi: 10.1007/978-0-387-78151-8_39
  17. Clobert J, Lebreton JD (1991) Estimation of demographic parameters in birds population. In: Perrins CM, Lebreton J-D, Hirons GJM (eds) Oxford University Press, Oxford, pp 75–104Google Scholar
  18. Cooch EG (2002) Fledging size and survival in snow geese: timing is everything (or is it?). J Appl Stat 29:143–162CrossRefGoogle Scholar
  19. Coulson T, Gaillard JM, Festa-Bianchet M (2005) Decomposing the variation in population growth into contributions from multiple demographic rates. J Anim Ecol 74:789–801. doi: 10.1111/j.1365-2656.2005.00975.x CrossRefGoogle Scholar
  20. Croxall JP, Rothery P (1991) Population regulation of seabirds: implications of their demography for conservation. In: Perrins CM, Lebreton J-D, Hirons GJM (eds) Bird population studies. Oxford University Press, Oxford, pp 272–296Google Scholar
  21. de Kroon H, Van Groenendael J, Ehrlen J (2000) Elasticities: a review of methods and model limitations. Ecology 81:607–618CrossRefGoogle Scholar
  22. Dickey MH, Gauthier G, Cadieux MC (2008) Climatic effects on the breeding phenology and reproductive success of an arctic-nesting goose species. Glob Change Biol 14:1973–1985. doi: 10.1111/j.1365-2486.2008.01622.x CrossRefGoogle Scholar
  23. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622. doi: 10.1086/285346 CrossRefGoogle Scholar
  24. Francis CM, Richards MH, Cooke F, Rockwell RF (1992) Long-term changes in survival rates of lesser snow geese. Ecology 73:1346–1362. doi: 10.2307/1940681 CrossRefGoogle Scholar
  25. Frederiksen M, Bregnballe T (2000) Diagnosing a decline in return rate of 1-year-old cormorants: mortality, emigration or delayed return? J Anim Ecol 69:753–761CrossRefGoogle Scholar
  26. Gaillard JM, Yoccoz NG (2003) Temporal variation in survivals in mammals: a case of environment canalization? Ecology 84:3294–3306CrossRefGoogle Scholar
  27. Gaillard JM, Festa-Bianchet M, Yoccoz NG (1998) Population dynamics of large herbivores: variable recruitment with constant adult survival. Trends Ecol Evol 13:58–63PubMedCrossRefGoogle Scholar
  28. Gaillard JM, Festa-Bianchet M, Yoccoz NG, Loison A, Toïgo C (2000) Temporal variation in fitness components and population dynamics of large herbivores. Annu Rev Ecol Syst 31:367–393CrossRefGoogle Scholar
  29. Gauthier G, Brault S (1998) Population model of the greater snow goose: projected impacts of reduction in survival on population growth rate. In: Batt BDJ (ed) The greater snow goose: report of the Arctic Goose Habitat Working Group. Arctic Goose Joint Venture special publication. U.S. Fish and Wildlife Service, Washington and Canadian Wildlife Service, Ottawa, pp 65–80Google Scholar
  30. Gauthier G, Lebreton JD (2008) Analysis of band-recovery data in a multistate capture-recapture framework. Can J Zool 36:59–73Google Scholar
  31. Gauthier G, Giroux JF, Reed A, Béchet A, Belanger L (2005) Interactions between land use, habitat use, and population increase in greater snow geese: what are the consequences for natural wetlands? Glob Change Biol 11:856–868. doi: 10.1111/j.1365-2486.2005.00944.x CrossRefGoogle Scholar
  32. Gauthier G, Fournier F, Larochelle J (2006) The effect of environmental conditions on early growth in geese. Acta Zool Sin 52(Supplement):670–674Google Scholar
  33. Gibson G, Wagner G (2000) Canalization in evolutionary genetics: a stabilizing theory? BioEssays 22:372–380PubMedCrossRefGoogle Scholar
  34. Giroux JF, Batt B, Brault S, Costanzo G, Filion B, Gauthier G, Luszcz D, Reed A (1998) Conclusions and management recommendations. In: Batt B (ed) The greater snow goose, report of the Arctic Goose Habitat Working Group. U.S. Fish and Wildlife Service, Washington, D.C. and Canadian Wildlife Service, Ottawa, Ontario, pp 81–88Google Scholar
  35. Harris MP, Frederiksen M, Wanless S (2007) Within- and between-year variation in the juvenile survival of common guillemots Uria aalge. Ibis 149:472–481CrossRefGoogle Scholar
  36. Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258. doi: 10.1126/science.282.5397.2256 PubMedCrossRefGoogle Scholar
  37. Jenouvrier S, Barbraud C, Weimerskirch H (2005) Long-term contrasted responses to climate of two Antarctic seabird species. Ecology 86:2889–2903CrossRefGoogle Scholar
  38. Juillet C, Choquet R, Gauthier G, Pradel R (2012) Carry-over effects of spring hunt and climate on recruitment to the natal colony in a migratory species. J Appl Ecol 49:1237–1246. doi: 10.1111/j.1365-2664.2012.02199.x Google Scholar
  39. Le Galliard JF, Marquis O, Massot M (2010) Cohort variation, climate effects and population dynamics in a short-lived lizard. J Anim Ecol 79:1296–1307. doi: 10.1111/j.1365-2656.2010.01732.x PubMedCrossRefGoogle Scholar
  40. Lebreton JD, Pradel R (2002) Multistate recapture models: modelling incomplete individual histories. J Appl Stat 29:353–369CrossRefGoogle Scholar
  41. Lebreton JD, Nichols JD, Barker RJ, Pradel R, Spendelow JA (2009) Modeling individual animal histories with multistate capture–recapture models. Adv Ecol Res 41:87–173. doi: 10.1016/s0065-2504(09)00403-6 CrossRefGoogle Scholar
  42. Legendre P (2011) Package lmodel2: model II regressionGoogle Scholar
  43. Lepage D, Gauthier G, Reed A (1998) Seasonal variation in growth of greater snow goose goslings: the role of food supply. Oecologia 114:226–235CrossRefGoogle Scholar
  44. Lesage L, Gauthier G (1997) Growth and organ development in greater snow goose goslings. Auk 114:229–241CrossRefGoogle Scholar
  45. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348PubMedCrossRefGoogle Scholar
  46. McLaughlin JD, McGurk BP (1987) An analysis of gizzard worm infections in fall migrant ducks at Delta, Manitoba, Canada. Can J Zool 65:1470–1477CrossRefGoogle Scholar
  47. Menu S, Gauthier G, Reed A (2002) Changes in survival rates and population dynamics of greater snow geese over a 30-year period: implications for hunting regulations. J Appl Ecol 39:91–102CrossRefGoogle Scholar
  48. Menu S, Gauthier G, Reed A (2005) Survival of young greater snow geese (Chen caerulescens atlantica) during fall migration. Auk 122:479–496CrossRefGoogle Scholar
  49. Monticelli D, Ramos JA, Hines JE, Nichols JD, Spendelow JA (2008) Juvenile survival in a tropical population of roseate terns: interannual variation and effect of tick parasitism. Mar Ecol Prog Ser 365:277–287. doi: 10.3354/meps07508 CrossRefGoogle Scholar
  50. Morris WF, Doak DF (2004) Buffering of life histories against environmental stochasticity: accounting for a spurious correlation between the variabilities of vital rates and their contributions to fitness. Am Nat 163:579–590PubMedCrossRefGoogle Scholar
  51. Morrison RIG, Davidson NC, Wilson JR (2007) Survival of the fattest: body stores on migration and survival in red knots Calidris canutus islandica. J Avian Biol 38:479–487. doi: 10.1111/j.2007.0908-8857.03934.x Google Scholar
  52. Naef-Daenzer B, Widmer F, Nuber M (2001) Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. J Anim Ecol 70:730–738CrossRefGoogle Scholar
  53. Newborn D, Foster R (2002) Control of parasite burdens in wild red grouse Lagopus lagopus scoticus through the indirect application of anthelmintics. J Appl Ecol 39:909–914CrossRefGoogle Scholar
  54. Nunn CL, Lindenfors P, Pursall ER, Rolff J (2009) On sexual dimorphism in immune function. Philos Trans R Soc B Biol Sci 364:61–69. doi: 10.1098/rstb.2008.0148 CrossRefGoogle Scholar
  55. O’Neal DM, Kiley RP, Ketterson ED (2011) The effect of winter sex ratio on immune function and condition in a differential migrant. Physiol Behav 102:406–413. doi: 10.1016/j.physbeh.2010.11.034 PubMedCrossRefGoogle Scholar
  56. Pedersen AB, Greives TJ (2008) The interaction of parasites and resources cause crashes in a wild mouse population. J Anim Ecol 77:370–377. doi: 10.1111/j.1365-2656.2007.01321.x PubMedCrossRefGoogle Scholar
  57. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891. doi: 10.1111/j.1600-0706.2009.17643.x CrossRefGoogle Scholar
  58. Pfister CA (1998) Patterns of variance in stage-structured populations: evolutionary predictions and ecological implications. Proc Natl Acad Sci USA 95:213–218PubMedCrossRefGoogle Scholar
  59. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  60. Redpath SM, Mougeot F, Leckie FM, Elston DA, Hudson PJ (2006) Testing the role of parasites in driving the cyclic population dynamics of a gamebird. Ecol Lett 9:410–418. doi: 10.1111/j.1461-0248.2006.00895.x PubMedCrossRefGoogle Scholar
  61. Reed ET, Gauthier G, Pradel R (2005) Effects of neck bands on reproduction and survival of female greater snow geese. J Wildl Manage 69:91–100CrossRefGoogle Scholar
  62. Righi M, Gauthier G (2002) Natural infection by intestinal cestodes: variability and effect on growth in greater snow goose goslings (Chen caerulescens atlantica). Can J Zool 80:1077–1083CrossRefGoogle Scholar
  63. Rolff J (2002) Bateman’s principle and immunity. Proc R Soc London Ser B Biol Sci 269:867–872. doi: 10.1098/rspb.2002.1959 CrossRefGoogle Scholar
  64. Roth O, Scharsack JP, Keller I, Reusch TBH (2011) Bateman’s principle and immunity in a sex-role reversed pipefish. J Evol Biol 24:1410–1420. doi: 10.1111/j.1420-9101.2011.02273.x PubMedCrossRefGoogle Scholar
  65. Saether BE, Bakke O (2000) Avian life history variation and contribution of demographic traits to the population growth rate. Ecology 81:642–653Google Scholar
  66. Schmutz JA (1993) Survival and pre-fledging body-mass in juvenile emperor geese. Condor 95:222–225. doi: 10.2307/1369404 CrossRefGoogle Scholar
  67. Schmutz JA, Ely CR (1999) Survival of greater white-fronted geese: effects of year, season, sex, and body condition. J Wildl Manage 63:1239–1249CrossRefGoogle Scholar
  68. Sedinger JS, Nicolai CA (2011) Recent trends in first-year survival for black brant breeding in Southwestern Alaska. Condor 113:511–517. doi: 10.1525/cond.2011.100218 CrossRefGoogle Scholar
  69. Sedinger JS, Flint PL, Lindberg MS (1995) Environmental Influence on life-history traits—growth, survival, and fecundity in black brant (Brant bernicla). Ecology 76:2404–2414. doi: 10.2307/2265816 CrossRefGoogle Scholar
  70. Sedinger JS, Herzog MP, Ward DH (2004) Early environment and recruitment of black brant (Branta bernicla nigricans) into the breeding population. Auk 121:68–73. doi:10.1642/0004-8038(2004)121[0068:eearob];2Google Scholar
  71. Shutler D, Alisauskas RT, Daniel McLaughlin J (2012) Associations between body composition and helminths of lesser snow geese during winter and spring migration. Int J Parasitol 42:755–760. doi: 10.1016/j.ijpara.2012.05.008 PubMedCrossRefGoogle Scholar
  72. Slattery SM (2000) Factors affecting first-year survival in Ross’ Geese. University of SaskatchewanGoogle Scholar
  73. Slattery SM, Alisauskas RT (2002) Use of the Barker model in an experiment examining covariate effects on first-year survival in Ross’s Geese (Chen rossii): a case study. J Appl Stat 29:497–508CrossRefGoogle Scholar
  74. Taber RD (1971) Criteria of sex and age. In: Giles RH Jr (ed) Wildlife management techniques. The Wildlife Society, Washington, DC, pp 325–402Google Scholar
  75. Toïgo C, Gaillard JM (2003) Causes of sex-biased adult survival in ungulates: sexual size dimorphism, mating tactic or environment harshness? Oikos 101:376–384CrossRefGoogle Scholar
  76. van de Pol M, Vindenes Y, Saether BE, Engen S, Ens BJ, Oosterbeek K, Tinbergen JM (2010) Effects of climate change and variability on population dynamics in a long-lived shorebird. Ecology 91:1192–1204PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Guillaume Souchay
    • 1
    • 2
  • Gilles Gauthier
    • 1
  • Roger Pradel
    • 2
  1. 1.Département de Biologie & Centre d’Études NordiquesUniversité LavalQuébecCanada
  2. 2.Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175Montpellier Cedex 05France

Personalised recommendations