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Oecologia

, Volume 177, Issue 1, pp 235–243 | Cite as

Pre-breeding energetic management in a mixed-strategy breeder

  • Holly L. Hennin
  • Pierre Legagneux
  • Joël Bêty
  • Tony D. Williams
  • H. Grant Gilchrist
  • Tyne M. Baker
  • Oliver P. Love
Physiological ecology - Original research

Abstract

Integrative biologists have long appreciated that the effective acquisition and management of energy prior to breeding should strongly influence fitness-related reproductive decisions (timing of breeding and reproductive investment). However, because of the difficulty in capturing pre-breeding individuals, and the tendency towards abandonment of reproduction after capture, we know little about the underlying mechanisms of these life-history decisions. Over 10 years, we captured free-living, arctic-breeding common eiders (Somateria mollissima) up to 3 weeks before investment in reproduction. We examined and characterized physiological parameters predicted to influence energetic management by sampling baseline plasma glucocorticoids (i.e., corticosterone), very-low-density lipoprotein (VLDL), and vitellogenin (VTG) for their respective roles in mediating energetic balance, rate of condition gain (physiological fattening rate) and reproductive investment. Baseline corticosterone increased significantly from arrival to the initiation of reproductive investment (period of rapid follicular growth; RFG), and showed a positive relationship with body mass, indicating that this hormone may stimulate foraging behaviour to facilitate both fat deposition and investment in egg production. In support of this, we found that VLDL increased throughout the pre-breeding period, peaking as predicted during RFG. Female eiders exhibited unprecedentedly high levels of VTG well before their theoretical RFG period, a potential strategy for pre-emptively depositing available protein stores into follicles while females are simultaneously fattening. This study provides some of the first data examining the temporal dynamics and interaction of the energetic mechanisms thought to be at the heart of individual variation in reproductive decisions and success in many vertebrate species.

Keywords

Energetic management Corticosterone Energetic metabolites Breeding threshold Mixed-strategy breeder 

Notes

Acknowledgments

We would like to thank the 2003–2013 East Bay field crew for data collection, I. Butler and R. Kelly for data organization, and two anonymous reviewers for their helpful comments. This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada, Environment Canada, Nunavut Wildlife Management Board, Greenland Institute of Nature, Polar Continental Shelf, Fonds Québécois de la Recherche sur la Nature et les Technologies, Canadian Network of Centres of Excellence ArcticNet, and the Department of Indian Affairs and Northern Canada.

Supplementary material

442_2014_3145_MOESM1_ESM.docx (35 kb)
Supplementary material 1 (DOCX 35 kb)

References

  1. Alisauskas RT, Ankney CD (1992) The cost of egg laying and its relationship to nutrient reserves in waterfowl. In: Batt BDJ, Afton AD, Anderson MG, Ankney CD, Johnson DH, Kadlec JA, Krapu GL (eds) Ecology and management of breeding waterfowl. University of Minnesota Press, Minneapolis, pp 30–61Google Scholar
  2. Angelier F, Bost C-A, Giraudeau M, Bouteloup G, Dano S, Chastel O (2008) Corticosterone and foraging behaviour in a diving seabird: the Adélie penguin, Pygoscelis adeliae. Gen Comp Endocrinol 156:134–144PubMedCrossRefGoogle Scholar
  3. Anteau MJ, Afton AD (2008) Using plasma-lipid metabolites to index changes in lipid reserves of free-living lesser scaup (Aythya affinis). Auk 125:354–357CrossRefGoogle Scholar
  4. Astheimer LB, Buttemer WA, Wingfield JC (1992) Interactions of corticosterone with feeding, activity, and metabolism in passerine birds. Ornis Scand 23:355–365CrossRefGoogle Scholar
  5. Bêty J, Gauthier G, Giroux J-F (2003) Body condition, migration, and the timing of reproduction in snow geese: a test of the condition-dependent model of optimal clutch size. Am Nat 162:110–121PubMedCrossRefGoogle Scholar
  6. Bottitta GE, Nol E, Gilchrist HG (2003) Effects or experimental manipulation of incubation length on behaviour and body mass of common eiders in the Canadian arctic. Waterbirds 26:100–107CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  8. Calenge C (2012) Package “adehabitatLT” for the R software: analysis of animal movementsGoogle Scholar
  9. Cerasale DJ, Guglielmo CG (2006) Dietary effects on prediction of body mass changes in birds by plasma metabolites. Auk 123:836–846CrossRefGoogle Scholar
  10. Challenger WO, Williams TD, Christians JK, Vézina F (2001) Follicular development and plasma yolk precursor dynamics through the laying cycle in the European starling (Sturnus vulgaris). Phys Biochem Zool 74:356–365CrossRefGoogle Scholar
  11. Crespi EJ, Williams TD, Jessop TS, Delehanty B (2013) Life history ecology of stress: how do glucocorticoid hormones influence life-history variation in animals? Funct Ecol 27:93–106CrossRefGoogle Scholar
  12. Crossin GT, Trathan PN, Phillips RA, Dawson A, Le Bouard F, Williams TD (2010) A carry-over effect of migration underlies individual variation in reproductive readiness and extreme egg size dimorphism in macaroni penguins. Am Nat 176:357–366PubMedCrossRefGoogle Scholar
  13. Crossin GT, Dawson A, Phillips RA, Trathan PN, Gorman KB, Adlard S, Williams TD (2012) Seasonal patterns of prolactin and corticosterone secretion in an Antarctic seabird that moults during reproduction. Gen Comp Endocrinol 175:74–81PubMedCrossRefGoogle Scholar
  14. Dallman MF, Strack AM, Akana SF, Bradbury MJ, Hanson ES, Scribner KA, Smith M (1993) Feast and famine: critical role of glucocorticoids with insulin in daily energy flow. Front Neuroend 14:303–347CrossRefGoogle Scholar
  15. Descamps S, Yoccoz NG, Gaillard J-M, Gilchrist HG, Erikstad KE, Hanssen SA, Cazelles B, Forbes MR, Bêty J (2010) Detecting population heterogeneity in effects of North Atlantic oscillations on seabird body condition: get into the rhythm. Oikos 119:1526–1536CrossRefGoogle Scholar
  16. Descamps S, Bêty J, Love OP, Gilchrist HG (2011) Individual optimization of reproduction in a long-lived migratory bird: a test of the condition-dependent model of laying date and clutch size. Funct Ecol 25:671–681CrossRefGoogle Scholar
  17. Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252Google Scholar
  18. Gibbons GF, Wiggins D, Brown AM, Hebbachi AM (2004) Synthesis and function of hepatic very-low-density lipoprotein. Biochem Soc Trans 32:59–64PubMedCrossRefGoogle Scholar
  19. Gorman KB, Esler D, Walzem RL, Williams TD (2009) Plasma yolk precursor dynamics during egg production by female greater scaup (Aythya marila): characterization and indices of reproductive state. Phys Biochem Zool 82:372–381CrossRefGoogle Scholar
  20. Hennin HL, Bêty J, Gilchirst HG, Love OP (2012) Do state-mediated hormones predict reproductive decisions in Arctic-nesting common eiders? Integr Comp Biol 52:E76Google Scholar
  21. Holberton RL (1999) Changes in patterns of corticosterone secretion concurrent with migratory fattening in a neotropical migratory bird. Gen Comp Endocrinol 116:49–58PubMedCrossRefGoogle Scholar
  22. Holberton RL, Wilson CM, Hunter MJ, Cash WB, Sims CG (2007) The role of corticosterone in suppressing migratory lipogenesis in the dark-eyed junco, Junco hyemalis: a model for central and peripheral regulation. Phys Biochem Zool 80:125–137CrossRefGoogle Scholar
  23. Kisdi É, Meszéna G, Pásztor L (1998) Individual optimization: mechanisms shaping the optimal reaction norm. Evol Ecol 12:211–221CrossRefGoogle Scholar
  24. Kitaysky AS, Wingfield JC, Piatt JF (1999) Dynamics of food availability, body condition and physiological stress response in breeding black-legged kittiwakes. Funct Ecol 13:577–584CrossRefGoogle Scholar
  25. Kitaysky AS, Piatt JF, Hatch SA, Kitaiskia EV, Benowitz-Fredericks ZM, Shultz MT, Wingfield JC (2010) Food availability and population processes: severity of nutritional stress during reproduction predicts survival of long-lived seabirds. Funct Ecol 24:625–637CrossRefGoogle Scholar
  26. Korschgen CE (1977) Breeding stress of female eiders in Maine. J Wildl Manag 41:360–373CrossRefGoogle Scholar
  27. Landys MM, Ramenofsky M, Wingfield JC (2006) Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen Comp Endocrinol 148:132–149PubMedCrossRefGoogle Scholar
  28. Lavielle M (1999) Detection of multiple changes in a sequence of dependent variables. Stoch Proc Appl 83:79–102CrossRefGoogle Scholar
  29. Lepage D, Gauthier G, Menu S (2000) Reproductive consequences of egg-laying decisions in snow geese. J Anim Ecol 69:414–427CrossRefGoogle Scholar
  30. Love OP, Williams TD (2008) Plasticity in the adrenocortical response of a free-living vertebrate: the role of pre- and post-natal developmental stress. Horm Behav 54:496–505PubMedCrossRefGoogle Scholar
  31. Love OP, Gilchrist HG, Descamps S, Semeniuk CAD, Bêty J (2010) Pre-laying climatic cues can time reproduction to optimally hatch offspring hatching and ice condition in an Arctic marine bird. Oecologia 164:277–286PubMedCrossRefGoogle Scholar
  32. Love OP, McGowan OP, Sheriff MJ (2013) Maternal adversity and ecological stressors in natural populations: the role of stress axis programming in individuals, with implications for populations and communities. Funct Ecol 27:81–92CrossRefGoogle Scholar
  33. Love OP, Bourgeon S, Madliger CL, Semeniuk CAD, Williams TD (2014) Evidence for baseline glucocorticoids as mediators of reproductive investment in a wild bird. Gen Comp Endocrinol 199:65–69PubMedCrossRefGoogle Scholar
  34. Lynn SE, Stamplis TN, Barrington WT, Weida N, Hudak CA (2010) Food, stress, and reproduction: short-term fasting alters endocrine physiology and reproductive behavior in the zebra finch. Horm Behav 58:214–222PubMedCrossRefGoogle Scholar
  35. Mallory ML, Gaston AJ, Gilchrist HG, Robertson GJ, Braune BM (2010) Effects of climate change, altered sea ice distribution and seasonal phenology on marine birds. In: Ferguson SF, Loseto LL, Mallory ML (eds) A little less Arctic: top predators in the world’s largest Northern inland sea, Hudson Bay. Springer, New York, pp 179–195CrossRefGoogle Scholar
  36. McNamara JM, Houston AI (1996) State-dependent life histories. Nature 380:215–221PubMedCrossRefGoogle Scholar
  37. Mitchell MA, Carlisle AJ (1991) Plasma zinc as an index of vitellogenin production and reproductive status in the domestic fowl. Comp Biochem Physiol A 100:719–724PubMedCrossRefGoogle Scholar
  38. Mosbech A, Gilchrist HG, Merkel F, Sonne C, Flagstad A, Nyegaard H (2006) Year-round movements of Northern common eiders Somateria mollissima borealis breeding in Arctic Canada and West Greenland followed by satellite telemetry. Ardea 94:651–665Google Scholar
  39. Muggeo VMR (2003) Estimating regression models with unknown break-points. Stat Med 22:3055–3071PubMedCrossRefGoogle Scholar
  40. Palm EC (2012) Trophic, energetic, and physiological responses of wintering white-winged scoters (Melanitta fusca) to habitat variation. MSc thesis, Simon Fraser University, BurnabyGoogle Scholar
  41. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  42. Rigou Y, Guillemette M (2010) Foraging effort and pre-laying strategy in breeding common eiders. Waterbirds 33:314–322CrossRefGoogle Scholar
  43. Robertson GJ (1995) Annual variation in common eider egg size: effects of temperature, clutch size, date, and laying sequence. Can J Zool 73:1579–1587CrossRefGoogle Scholar
  44. Robinson R (2008) For mammals, loss of yolk and gain of milk went hand in hand. PLoS Biol 6:e77PubMedCentralPubMedCrossRefGoogle Scholar
  45. Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24PubMedCrossRefGoogle Scholar
  46. Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Phys A 140:73–79CrossRefGoogle Scholar
  47. Rowe L, Ludwig D, Schluter D (1994) Time, condition, and the seasonal decline of avian clutch size. Am Nat 143:698–722CrossRefGoogle Scholar
  48. Salvante KG, Williams TD (2002) Vitellogenin dynamics during egg-laying: daily variation, repeatability and relationship with egg size. J Avian Biol 33:391–398CrossRefGoogle Scholar
  49. Seaman DA, Guglielmo CG, Williams TD (2005) Effects of physiological state, mass change and diet on plasma metabolite profiles in the western sandpiper Calidris mauri. J Exp Biol 208:761–769PubMedCrossRefGoogle Scholar
  50. Sénéchal E, Bêty J, Gilchrist HG, Hobson KA, Jamieson SE (2011) Do purely capital layers exist among flying birds? Evidence of exogenous contribution to arctic-nesting common eider eggs. Oecologia 165:593–604PubMedCrossRefGoogle Scholar
  51. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  52. Stephens PA, Boyd IL, McNamara JM, Houston AI (2009) Capital breeding and income breeding: their meaning, measurement, and worth. Ecology 90:2057–2067PubMedCrossRefGoogle Scholar
  53. Vanderkist BA, Williams TD, Bertram DF, Lougheed LW, Ryder JL (2000) Indirect, physiological assessment of reproductive state and breeding chronology in free-living birds: an example in the marbled murrelet (Brachyramphus marmoratus). Funct Ecol 14:758–765CrossRefGoogle Scholar
  54. Walzem RL, Hansen RJ, Williams DL, Hamilton RL (1999) Estrogen induction of VLDLy assembly in egg-laying hens. J Nutr 129(2S suppl.):467S–472SPubMedGoogle Scholar
  55. Watson MD, Robertson GJ, Cooke F (1993) Egg-laying time and laying interval in the common eider. Condor 95:869–878CrossRefGoogle Scholar
  56. Williams TD (2005) Mechanisms underlying the costs of egg production. BioSci 55:39–48CrossRefGoogle Scholar
  57. Williams TD (2012a) Chapter 2: The hormonal and physiological control of egg production. Physiological adaptations for breeding birds. Princeton University Press, Princeton, pp 8–51Google Scholar
  58. Williams TD (2012b) Hormones, life-history, and phenotypic variation: opportunities in evolutionary avian endocrinology. Gen Comp Endocrinol 176:286–295PubMedCrossRefGoogle Scholar
  59. Williams TD, Warnock N, Takekawa JY, Bishop MA (2007) Flyway-scale variation in plasma triglyceride levels as an index of refuelling rate in spring-migrating western sandpipers (Calidris mauri). Auk 124:886–897CrossRefGoogle Scholar
  60. Wingfield JC, Smith JP, Farner DS (1982) Endocrine responses of white-crowned sparrows to environmental stress. Condor 84:399–409CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Holly L. Hennin
    • 1
  • Pierre Legagneux
    • 2
  • Joël Bêty
    • 2
  • Tony D. Williams
    • 3
  • H. Grant Gilchrist
    • 4
  • Tyne M. Baker
    • 1
  • Oliver P. Love
    • 1
  1. 1.Department of Biological SciencesUniversity of WindsorWindsorCanada
  2. 2.Département de Biologie, chimie et géographie and Centre d’études nordiquesUniversité du Québec à RimouskiRimouskiCanada
  3. 3.Biological SciencesSimon Fraser UniversityBurnabyCanada
  4. 4.Environment Canada, National Wildlife Research CentreCarleton UniversityOttawaCanada

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