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Oecologia

, Volume 183, Issue 3, pp 653–666 | Cite as

Linking pre-laying energy allocation and timing of breeding in a migratory arctic raptor

  • Vincent Lamarre
  • Alastair Franke
  • Oliver P. Love
  • Pierre Legagneux
  • Joël Bêty
Physiological ecology - original research

Abstract

For migratory species, acquisition and allocation of energy after arrival on the breeding grounds largely determine reproductive decisions. Few studies have investigated underlying physiological mechanisms driving variation in breeding phenology so far. We linked physiological state to individual timing of breeding in pre-laying arctic-nesting female peregrine falcons (Falco peregrinus tundrius). We captured females from two populations 2–20 days before egg-laying to assess plasma concentration of β-hydroxybutyric acid (BUTY) and triglyceride (TRIG), two metabolites known to reflect short-term changes in fasting and fattening rate, respectively. We also assessed baseline corticosterone (CORTb), a hormone that mediates energy allocation, and the scaled mass index (SMI) as an indicator of somatic body reserves. Plasma BUTY was slightly higher during the pre-recruiting period compared to the period of rapid follicular growth, indicating a reduction in catabolism of lipid reserves before investment in follicle development. Conversely, TRIG levels increased in pre-recruiting females, and best-predicted individual variation in pre-laying interval and lay date. A marked increase in CORTb occurred concomitantly with the onset of rapid follicle growth. SMI was highly variable possibly reflecting variation in food availability or individuals at different stages. Results suggest that (1) lower rates of pre-laying fattening and/or lower mobilization rate of lipoproteins to ovarian follicles delayed laying, and (2) an elevation in pre-laying CORTb may result from, or be required to compensate for, the energetic costs of egg production. Results of this study illustrate how variation in the allocation of energy before laying can influence individual fitness-related reproductive decisions.

Keywords

Energy allocation β-Hydroxybutyric acid Triglyceride Corticosterone Peregrine falcon 

Notes

Acknowledgements

All work was conducted under the following permits: Nunavut Wildlife Research Permit (WL 2011-038, WL 2012-042, WL 2013-034, WL 2014-034); Canadian Wildlife Service Banding Permit (10833); University of Alberta Animal Use Protocol (AUP00000042). We are especially grateful to Erik Hedlin, Andy Aliyak and Mark Prostor for their invaluable help with fieldwork. We also thank (alphabetical order): Matt Fredlund, Philippe Galipeau, Mikaël Jaffré, Pascal Pettigrew, Mike Qrunnut, Barry Robinson and Mathieu Tétreault for their contribution to field work. We thank Chris Harris for running the physiological assays. We are extremely grateful for the help and support that we received from the Government of Nunavut, Department of Environment, especially Chris Hotson, Drikus Gissing, and Mitch Campbell. We are indebted to personal at Agnico Eagle Mines Limited (AEM), in particular Stéphane Robert, Ryan Vanengen, Philip Roy, Alexandre Gauthier and Marcel Dumais. We thank the members of Kangiqliniq and Igloolik hunters and Trappers Organizations for their approval and ongoing support for this project. We would also like to thank Michael Shouldice and Dorothy Tootoo from the Arctic College, as well as the residents of Rankin Inlet and Igloolik. We would like to thank Guy Fitzgerald from the Union québécoise de réhabilitation des oiseaux de proie and Josée Tremblay from the Zoo sauvage de St-Félicien. Finally, we would like to thank Emma Vatka and an anonymous reviewer for their constructive suggestions and comments. This project was funded by ArcticNet (AF), the Government of Nunavut (AF), the Canadian Circumpolar Institute (AF), Aboriginal and Northern Affairs Canada (VL), and the Peregrine Fund (AF). Finally, VL was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC), the Fond de Recherche du Québec, Nature et Technologies (FRQNT), the Garfield Weston Foundation and Mitacs Accelerate (AF; AEM industry partner) and analyses in OPL’s lab were supported by funding from NSERC Discovery and the Canada Research Chairs program.

Author contribution statement

JB and AF orginally formulated the idea. VL, JB and AF developed methodology. OPL advised on the choice of relevant physiological parameters and supervised laboratory analyses. AF and VL conducted fieldwork. VL, JB and PL performed statistical analyses. VL wrote the manuscript with the input of all co-authors.

References

  1. Anctil A, Franke A, Bêty J (2013) Heavy rainfall increases nestling mortality of an arctic top predator : experimental evidence and long-term trend in peregrine falcons. Oecologia 174:1033–1043CrossRefPubMedPubMedCentralGoogle Scholar
  2. Angelier F, Shaffer SA, Weimerskirch H, Trouvé C, Chastel O (2007) Corticosterone and foraging behavior in a pelagic seabird. Physiol Biochem Zool 80:283–292CrossRefPubMedGoogle Scholar
  3. Angelier F, Bost C-A, Giraudeau M, Bouteloup G, Dano S, Chastel O (2008) Corticosterone and foraging behavior in a diving seabird: the Adélie penguin, Pygoscelis adeliae. Gen Comp Endocrinol 156:134–144CrossRefPubMedGoogle Scholar
  4. 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
  5. Bêty J, Gauthier G, Giroux J-F (2003) Body condition, migration, and timing of reproduction in snow geese: a test of the condition-dependant model of optimal clutch size. Am Nat 162:110–121CrossRefPubMedGoogle Scholar
  6. Boismenu C, Gauthier G, Larochelle J (1992) Physiology of prolonged fasting in greater snow geese (Chen caerulescens atlantica). Auk 109:511–521Google Scholar
  7. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer Science & Business Media, New YorkGoogle Scholar
  8. Bradley M, Oliphant LW (1991) The diet of Peregrine Falcons in Rankin Inlet, Northwest Territories: an unusually high proportion of mammalian prey. Condor 93:193-197CrossRefGoogle Scholar
  9. Cade TJ (1960) Ecology of the peregrine and gyrfalcon populations in Alaska. University of California Press, CaliforniaGoogle Scholar
  10. Carlier P, Gallo A (1995) What motivates the food bringing behaviour of the peregrine falcon throughout breeding? Behav Process 33:247–256CrossRefGoogle Scholar
  11. Cerasale DJ, Guglielmo CG (2006) Dietary effects on prediction of body mass changes in birds by plasma metabolites. Auk 123:836–846CrossRefGoogle Scholar
  12. Challenger WO, Williams TD, Christians JK, Vézina F (2001) Development and plasma yolk precursor dynamics through the laying cycle in the European starling (Sturnus vulgaris). Physiol Biochem Zool 74:356–365CrossRefPubMedGoogle Scholar
  13. Cherel Y, Robin J-P, Le Maho Y (1988) Physiology and biochemistry of long-term fasting in birds. Can J Zool 66:159–166CrossRefGoogle Scholar
  14. Court GS, Gates CC, Boag DA (1988) Natural history of the peregrine falcon in the Keewatin district of the Northwest Territories. Arctic 41:17–30CrossRefGoogle Scholar
  15. Crossin GT, Trathan PN, Phillips RA, Gorman KB, Dawson A, Sakamoto KQ, Williams TD (2012) Corticosterone predicts foraging behaviour and parental care in macaroni penguins. Am Nat 180:E31–E41CrossRefPubMedGoogle 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-dependant model of laying date and clutch size. Funct Ecol 25:671–681CrossRefGoogle Scholar
  17. Devries JH, Brook RW, Howerter DW, Anderson MG (2008) Effects of spring body condition and age on reproduction in mallards (Anas platyrhynchos). Auk 125:618–628CrossRefGoogle Scholar
  18. Drent RH (2006) The timing of birds’ breeding seasons: the Perrins hypothesis revisited especially for migrants. Ardea 94:305–322Google Scholar
  19. Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252Google Scholar
  20. Einum S, Fleming IA (2000) Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54:628–639CrossRefPubMedGoogle Scholar
  21. Franke A, Setterington M, Court G, Birkholz D (2010) Long-term trends of persistent organochlorine pollutants, occupancy and reproductive success in peregrine falcons (Falco peregrinus tundrius) breeding near Rankin Inlet, Nunavut, Canada. Arctic 63:442–450CrossRefGoogle Scholar
  22. Gorman KB, Esler D, Flint PL, Williams TD (2008) Nutrient-reserve dynamics during egg production by female greater scaup (Aythya marila): relationships with timing of reproduction. Auk 125:384–394CrossRefGoogle Scholar
  23. 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. Physiol Biochem Zool 82:372–381CrossRefPubMedGoogle Scholar
  24. Goutte A, Angelier F, Clément-Chastel C, Trouvé C, Moe B, Bech C, Gabrielsen GW, Chastel O (2010) Stress and the timing of breeding: glucocorticoid-luteinizing hormones relationships in an arctic seabird. Gen Comp Endocrinol 169:108–116CrossRefPubMedGoogle Scholar
  25. Goutte A, Clément-Chastel C, Moe B, Bech C, Gabrielsen GW, Chastel O (2011) Experimentally reduced corticosterone release promotes early breeding in black-legged kittiwakes. J Exp Biol 214:2005–2013CrossRefPubMedGoogle Scholar
  26. Goutte A, Angelier F, Bech C, Clément-Chastel C, Dell’Omo G, Gabrielsen GW, Lendvai ÁZ, Moe B, Noreen E, Pinaud D, Tartu S, Chastel O (2014) Annual variation in the timing of breeding, pre-breeding foraging areas and corticosterone levels in an Arctic population of black-legged kittiwakes. Mar Ecol Prog Ser 496:233–247CrossRefGoogle Scholar
  27. Hennin HL, Legagneux P, Bêty J, Williams TD, Gilchrist G, Baker TM, Love OP (2015) Pre-breeding energetic management in a mixed-strategy breeder. Oecologia 177:235–243CrossRefPubMedGoogle Scholar
  28. Hennin HL, Legagneux P, Bêty J, Gilchrist HG, Williams TD, Love OP (2016) Energetic physiology mediates individual optimization of breeding phenology in a migratory Arctic seabird. Am Nat (in press) Google Scholar
  29. Jaffré M, Franke A, Anctil A, Galipeau P, Hedlin E, Lamarre V, L’Hérault V, Nikolaiczuk L, Peck K, Robinson B, Bêty J (2015) Écologie de la reproduction du faucon pèlerin au Nunavut. Nat Can 139:54–64Google Scholar
  30. Jenni-Eiermann S, Jenni L (1994) Plasma metabolite levels predict individual body-mass changes in a small long-distance migrant, the garden warbler. Auk 111:888–899CrossRefGoogle Scholar
  31. Jenni-Eiermann S, Jenni L (1998) What can plasma metabolites tell us about the metabolism, physiological state and condition of individual birds? An overview. Biol Conser Fauna 102:312–319Google Scholar
  32. Kitaysky AS, Wingfield JC, Piatt JF (2001) Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behav Ecol 12:619–625CrossRefGoogle Scholar
  33. 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 148:132–149CrossRefPubMedGoogle Scholar
  34. Legagneux P, Hennin H, Williams TD, Gilchrist HG, Love OP, Bêty J (2016) Food shortage reduces breeding propensity regardless of pre-laying physiological investment in a partial capital breeder. J Avian Biol (in press) Google Scholar
  35. L'Hérault V, Franke A, Lecomte N, Alogut A, Bêty J (2013) Landscape heterogeneity drives intra‐population niche variation and reproduction in an arctic top predator. Ecol Evol 3:2867-2879Google Scholar
  36. Love OP, Breuner CW, Vézina F, Williams TD (2004) Mediation of a corticosterone-induced reproductive conflict. Horm Behav 46(1):59–65CrossRefPubMedGoogle Scholar
  37. Love OP, Chin EH, Wynne-Edwards KE, Williams TD (2005) Stress hormones: a link between maternal condition and sex-biased reproductive investment. Am Nat 166:751–766PubMedGoogle Scholar
  38. Love OP, Madliger CL, Bourgeon S, Semeniuk CAD, Williams TD (2014) Evidence for baseline glucocorticoids as mediators of reproductive investment in a wild bird. Gen Comp Endocrinol 199:65–69CrossRefPubMedGoogle Scholar
  39. McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15CrossRefPubMedGoogle Scholar
  40. Meijer T, Masma D, Daan S (1989) Energetics of reproduction in female kestrels. Auk 106:549–559Google Scholar
  41. Meijer T, Daan S, Hall M (1990) Family planning in the Kestrel (Falco tinnunculus): the proximate control of covariation of laying date and clutch size. Behaviour 114:117–136CrossRefGoogle Scholar
  42. Muggeo VMR (2003) Estimating regression models with unknown break-points. Stat Med 22:3055–3071CrossRefPubMedGoogle Scholar
  43. Nager RG (2006) The challenge of making eggs. Ardea 94:323–346Google Scholar
  44. Newton I (2006) Can conditions experienced during migration limit the population levels of birds? J Ornithol 147:146–166CrossRefGoogle Scholar
  45. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891CrossRefGoogle Scholar
  46. Pietiäinen H, Kolunen H (1993) Female body condition and breeding in the Ural owl Strix uralensis. Funct Ecol 7:726–735CrossRefGoogle Scholar
  47. Core Team R (2014) R: a language and environment for statistical computing. Austria, ViennaGoogle Scholar
  48. Ratcliffe D (1980) The Peregrine Falcon. Buteo Books, South DakotaGoogle Scholar
  49. Robinson BG, Franke A, Derocher AE (2014) The influence of weather and lemmings on spatiotemporal variation in the abundance of multiple avian guilds in the Arctic. PLoS One 9:e101495CrossRefPubMedPubMedCentralGoogle Scholar
  50. Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24CrossRefPubMedGoogle Scholar
  51. Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Physiol Part A Mol Integr Physiol 140:73–79CrossRefGoogle Scholar
  52. Rowe L, Ludwig D, Schluter D (1994) Time, condition, and the seasonal decline of avian clutch size. Am Nat 143:698–722CrossRefGoogle Scholar
  53. Sénéchal É, 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 165:593–604CrossRefPubMedGoogle Scholar
  54. Sonerud GA (1986) Effect of snow cover on seasonal changes in diet, habitat, and regional distribution of raptors that prey on small mammals in boreal zones of Fennoscandia. Holarct Ecol 9:33–47Google Scholar
  55. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  56. Stephens PA, Boyd IL, McNamara JM, Houston AI (2009) Capital breeding and income breeding: their meaning, measurement, and worth. Ecology 90:2057–2067CrossRefPubMedGoogle Scholar
  57. Swain SD (1992) Energy substrate profiles during fasting in horned larks (Eremophila alpestris). Physiol Zool 65:568–582CrossRefGoogle Scholar
  58. Totzke U, Fenske M, Hüppop O, Raabe H, Schach N (1999) The influence of fasting on blood and plasma composition of herring gulls (Larus argentatus). Physiol Biochem Zool 72:426–437CrossRefPubMedGoogle Scholar
  59. Vézina F, Salvante KG (2010) Behavioral and physiological flexibility are used by birds to manage energy and support investment in the early stages of reproduction. Curr Zool 56:767–792Google Scholar
  60. Wagner DN, Green DJ, Pavlik M, Cooper J, Williams TD (2014) Physiological assessment of the effects of changing water levels associated with reservoir management on fattening rates of neotropical migrants at a stopover site. Conserv Physiol 2:cou017CrossRefPubMedPubMedCentralGoogle Scholar
  61. Walzem RL, Hansen RJ, Williams DL, Hamilton RL (1999) Estrogen induction of VLDLy assembly in egg-laying hens. J Nutr 129:467S–472SPubMedGoogle Scholar
  62. White CM, Clum NJ, Cade TJ, Hunt WG (2002) Peregrine falcon (Falco peregrinus). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology; retrieved from the Birds of North America Online, Ithaca. http://bna.birds.cornell.edu/bna/species/660
  63. Williams TD (2005) Mechanisms underlying the costs of egg production. Bioscience 55:39–48CrossRefGoogle Scholar
  64. Williams TD (2012) Physiological adaptations for breeding in birds. Princeton University Press, New JerseyGoogle Scholar
  65. Williams TD, Guglielmo CG, Egeler O, Martyniuk CJ (1999) Plasma lipid metabolites provide information on mass change over several days in captive Western Sandpipers. Auk 116(4):994–1000CrossRefGoogle Scholar
  66. Williams TD, Warnock N, Takekawa JY, Bishop MA (2007) Flyway-scale variation in plasma triglyceride levels as an index of refueling rate in spring-migrating Western Sandpipers (Calidris mauri). Auk 124:886–897CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Département de biologie, chimie et géographie et Centre d’études nordiquesUniversité du Québec à RimouskiRimouskiCanada
  2. 2.Arctic Raptors ProjectRankin InletCanada
  3. 3.Department of Biological Sciences and Great Lakes Institute for Environmental ResearchUniversity of WindsorWindsorCanada

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