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Oecologia

, Volume 183, Issue 2, pp 353–365 | Cite as

Effectiveness of baseline corticosterone as a monitoring tool for fitness: a meta-analysis in seabirds

  • Graham H. Sorenson
  • Cody J. Dey
  • Christine L. Madliger
  • Oliver P. Love
Physiological ecology - Original research

Abstract

Many ecosystems have experienced anthropogenically induced changes in biodiversity, yet predicting these patterns has been difficult. Recently, individual behavioural and physiological measures have been proposed as more rapid links between environmental variation and fitness compared to demographics. Glucocorticoid hormones have received much attention given that they mediate energetic demands, metabolism, and foraging behaviour. However, it is currently unclear whether glucocorticoids can reliably predict environmental and fitness-related traits and whether they may be useful in specific groups of taxa. In particular, seabirds are a well-studied avian group often employed as biomonitoring tools for environmental change given their wide distribution and reliance on large oceanic patterns. Despite the increase in studies attempting to link variation in baseline corticosterone (the primary avian glucocorticoid) to variation in fitness-related traits in seabirds, there has been no comprehensive review of the relationship in this taxon. We present a phylogenetically controlled systematic review and meta-analysis of correlative and experimental studies examining baseline corticosterone as a predictor of fitness-related traits relevant to predicting seabird population health. Our results suggest that, while variation in baseline corticosterone may be a useful predictor of larger-scale environmental traits such as overall food availability and fitness-related traits such as reproductive success, this hormone may not be sensitive enough to detect variation in body condition, foraging effort, and breeding effort. Overall, our results support recent work suggesting that the use of baseline glucocorticoids as conservation biomarkers is complex and highly context dependent, and we suggest caution in their use and interpretation as simplified, direct biomarkers of fitness.

Keywords

Glucocorticoids Systematic review Cort-fitness Biomarker Food availability Seabirds 

Notes

Author contribution statement

GHS and OPL conceived and designed the search methodology. GHS searched the literature, collected the data, and calculated effect sizes. GHS and CJD analysed the data. GHS, CJD, and CLM wrote the manuscript with additional edits from OPL.

Supplementary material

442_2016_3774_MOESM1_ESM.pdf (546 kb)
Supplementary material 1 (PDF 545 kb)

References

  1. Adams DC (2008) Phylogenetic meta-analysis. Evolution 62:567–572. doi: 10.1111/j.1558-5646.2007.00314.x CrossRefPubMedGoogle Scholar
  2. Angelier F, Clement-Chastel C, Gabrielsen GW, Chastel O (2007a) Corticosterone and time-activity budget: an experiment with Black-legged kittiwakes. Horm Behav 52:482–491. doi: 10.1016/j.yhbeh.2007.07.003 CrossRefPubMedGoogle Scholar
  3. Angelier F, Moe B, Clement-Chastel C et al (2007b) Corticosterone levels in relation to change of mate in Black-legged kittiwakes. Condor 109:668–674. doi: 10.1242/jeb.089763 CrossRefGoogle Scholar
  4. Angelier F, Shaffer SA, Weimerskirch H et al (2007c) Corticosterone and foraging behavior in a pelagic seabird. Physiol Biochem Zool 80:283–292. doi: 10.1086/512585 CrossRefPubMedGoogle Scholar
  5. Angelier F, Bost C-A, Giraudeau M et al (2008) Corticosterone and foraging behavior in a diving seabird: the Adelie penguin, Pygoscelis adeliae. Gen Comp Endocrinol 156:134–144. doi: 10.1016/j.ygcen.2007.12.001 CrossRefPubMedGoogle Scholar
  6. Angelier F, Giraudeau M, Bost C-AC-A et al (2009) Are stress hormone levels a good proxy of foraging success? An experiment with King Penguins, Aptenodytes patagonicus. J Exp Biol 212:2824–2829. doi: 10.1242/jeb.027722 CrossRefPubMedGoogle Scholar
  7. Angelier F, Wingfield JC, Weimerskirch H, Chastel O (2010) Hormonal correlates of individual quality in a long-lived bird: a test of the “corticosterone-fitness hypothesis”. Biol Lett 6:846–849. doi: 10.1098/rsbl.2010.0376 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Angelier F, Wingfield JC, Parenteau C et al (2015) Does short-term fasting lead to stressed-out parents? A study of incubation commitment and the hormonal stress responses and recoveries in snow petrels. Horm Behav 67:28–37. doi: 10.1016/j.yhbeh.2014.11.009 CrossRefPubMedGoogle Scholar
  9. Arlettaz R, Nussle S, Baltic M et al (2015) Disturbance of wildlife by outdoor winter recreation: allostatic stress response and altered activity-energy budgets. Ecol Appl 25:1197–1212. doi: 10.1890/14-1141.1.sm CrossRefPubMedGoogle Scholar
  10. Astheimer LB, Buttemer WA, Wingfield JC (1992) Interactions of corticosterone with feeding, activity and metabolism in Passerine birds. Ornis Scand 23:355–365. doi: 10.2307/3676661 CrossRefGoogle Scholar
  11. Balbontín J, Møller AP, Hermosell IG et al (2012) Lifetime individual plasticity in body condition of a migratory bird. Biol J Linn Soc 105:420–434. doi: 10.1111/j.1095-8312.2011.01800.x CrossRefGoogle Scholar
  12. Benowitz-Fredericks ZM, Shultz MT, Kitaysky AS (2008) Stress hormones suggest opposite trends of food availability for planktivorous and piscivorous seabirds in 2 years. Deep Res Part II Top Stud Oceanogr 55:1868–1876. doi: 10.1016/j.dsr2.2008.04.007 CrossRefGoogle Scholar
  13. Berger-Tal O, Polak T, Oron A et al (2011) Integrating animal behavior and conservation biology: a conceptual framework. Behav Ecol 22:236–239. doi: 10.1093/beheco/arq224 CrossRefGoogle Scholar
  14. Bodey TW, Jessopp MJ, Votier SC et al (2014) Seabird movement reveals the ecological footprint of fishing vessels. Curr Biol 24:R514–R515. doi: 10.1016/j.cub.2014.04.041 CrossRefPubMedGoogle Scholar
  15. Boncoraglio G, Saino N (2007) Habitat structure and the evolution of bird song: a meta-analysis of the evidence for the acoustic adaptation hypothesis. Funct Ecol 21:134–142. doi: 10.1111/j.1365-2435.2006.01207.x CrossRefGoogle Scholar
  16. Bonier F, Martin PR, Moore IT, Wingfield JC (2009) Do baseline glucocorticoids predict fitness? Trends Ecol Evol 24:634–642. doi: 10.1016/j.tree.2009.04.013 CrossRefPubMedGoogle Scholar
  17. Bonier F, Moore IT, Robertson RJ (2011) The stress of parenthood? Increased glucocorticoids in birds with experimentally enlarged broods. Biol Lett 7:944–946. doi: 10.1098/rsbl.2011.0391 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Breuner CW, Patterson SH, Hahn TP (2008) In search of relationships between the acute adrenocortical response and fitness. Gen Comp Endocrinol 157:288–295. doi: 10.1016/j.ygcen.2008.05.017 CrossRefPubMedGoogle Scholar
  19. Brooks S, Gelman A (1998) General methods for monitoring convergence of iterative simulations. J Comput Graph Stat 7:434–455. doi: 10.2307/1390675 Google Scholar
  20. Bukacinska M, Bukacinski D, Spaans AL (2016) Attendance and diet in relation to breeding success in herring gulls (Larus argentatus). Auk 113:300–309Google Scholar
  21. Busch DS, Hayward LS (2009) Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biol Conserv 142:2844–2853. doi: 10.1016/j.biocon.2009.08.013 CrossRefGoogle Scholar
  22. Chastel O, Lacroix A, Weimerskirch H, Gabrielsen GW (2005) Modulation of prolactin but not corticosterone responses to stress in relation to parental effort in a long-lived bird. Horm Behav 47:459–466. doi: 10.1016/j.yhbeh.2004.10.009 CrossRefPubMedGoogle Scholar
  23. Chown SL, Gaston KJ (2015) Macrophysiology—progress and prospects. Funct Ecol 30:330–344. doi: 10.1111/1365-2435.12510 CrossRefGoogle Scholar
  24. Cooke SJ, O’Connor CM (2010) Making conservation physiology relevant to policy makers and conservation practitioners. Conserv Lett 3:159–166. doi: 10.1111/j.1755-263X.2010.00109.x CrossRefGoogle Scholar
  25. Cooke SJ, Sack L, Franklin CE et al (2013) What is conservation physiology? Perspectives on an increasingly integrated and essential science. Conserv Physiol 1:1–23. doi: 10.1093/conphys/cot001 CrossRefGoogle Scholar
  26. Cooke SJ, Blumstein DT, Buchholz R et al (2014) Physiology, behavior, and conservation. Physiol Biochem Zool 87:1–14. doi: 10.1086/671165 CrossRefPubMedGoogle Scholar
  27. Cooper H, Hedges LV, Valentine JC (2009) Handbook of research synthesis and meta-analysis. Russell Sage Foundation, New YorkGoogle Scholar
  28. Croll DA, Gaston AJ, Noble DG (1991) Adaptive loss of mass in thick-billed murres. Condor 93:496–502. doi: 10.2307/1368181 CrossRefGoogle Scholar
  29. Crossin GT, Phillips RA, Lattin CR et al (2013) Corticosterone mediated costs of reproduction link current to future breeding. Gen Comp Endocrinol 193:112–120. doi: 10.1016/j.ygcen.2013.07.011 CrossRefPubMedGoogle Scholar
  30. Crossin GT, Love OP, Cooke SJ, Williams TD (2016a) Glucocorticoid manipulations in free-living animals: considerations of dose delivery, life-history context and reproductive state. Funct Ecol 30:116–125. doi: 10.1111/1365-2435.12482 CrossRefGoogle Scholar
  31. Crossin GT, Phillips RA, Lattin CR et al (2016b) Physiological costs of reproduction and carryover effects in annually versus biennially breeding albatrosses (Thalassarche spp.). Antarct SciGoogle Scholar
  32. Croxall JP, Butchart SHM, Lascelles B et al (2012) Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv Int 22:1–34. doi: 10.1017/S0959270912000020 CrossRefGoogle Scholar
  33. Dantzer B, Fletcher QE, Boonstra R, Sheriff MJ (2014) Measures of physiological stress: a transparent or opaque window into the status, management and conservation of species? Conserv Physiol 2:1–18. doi: 10.1093/conphys/cou023 CrossRefGoogle Scholar
  34. Descamps SS, Strøm H, Steen H et al (2013) Decline of an arctic top predator: synchrony in colony size fluctuations, risk of extinction and the subpolar gyre. Oecologia 173:1271–1282. doi: 10.1007/s00442-013-2701-0 CrossRefPubMedGoogle Scholar
  35. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. doi: 10.1093/molbev/mss075 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Egger M, Smith GD (1997) Bias in meta-analysis detected by a simple, graphical test. Br Med J 315:629–634CrossRefGoogle Scholar
  37. Elliott KH, Welcker J, Gaston AJ et al (2013) Thyroid hormones correlate with resting metabolic rate, not daily energy expenditure, in two charadriiform seabirds. Biol Open 2:580–586. doi: 10.1242/bio.20134358 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev Camb Philos Soc 81:117–142. doi: 10.1017/S1464793105006949 CrossRefPubMedGoogle Scholar
  39. Fokidis HB, Des Roziers MB, Sparr R et al (2012) Unpredictable food availability induces metabolic and hormonal changes independent of food intake in a sedentary songbird. J Exp Biol 215:2920–2930. doi: 10.1242/jeb.071043 CrossRefPubMedGoogle Scholar
  40. Frederiksen M, Mavor RA, Wanless S (2007) Seabirds as environmental indicators: the advantages of combining data sets. Mar Ecol Prog Ser 352:205–211. doi: 10.3354/meps07071 CrossRefGoogle Scholar
  41. Gaston AJ, Mallory ML, Gilchrist HG (2012) Populations and trends of Canadian Arctic seabirds. Polar Biol 35:1221–1232. doi: 10.1007/s00300-012-1168-5 CrossRefGoogle Scholar
  42. Gaston AJ, Elliott KH, Ropert-Coudert Y et al (2013) Modeling foraging range for breeding colonies of thick-billed murres Uria lomvia in the Eastern Canadian Arctic and potential overlap with industrial development. Biol Conserv 168:134–143. doi: 10.1016/j.biocon.2013.09.018 CrossRefGoogle Scholar
  43. Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, CambridgeGoogle Scholar
  44. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–472CrossRefGoogle Scholar
  45. Guglielmo CG, Hara PDO, Williams TD (2002) Extrinsic and intrinsic sources of variation in plasma lipid metabolites of free-living western sandpipers (Calidris mauri). Auk 119:437–445. doi:10.1642/0004-8038(2002)119[0437:EAISOV]2.0.CO;2Google Scholar
  46. Hackett SJ, Kimball RT, Reddy S et al (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768. doi: 10.1126/science.1157704 CrossRefPubMedGoogle Scholar
  47. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22. doi: 10.1002/ana.22635 CrossRefGoogle Scholar
  48. Halpern BS, Walbridge S, Selkoe KA et al (2008) A global map of human impact on marine ecosystems. Science 319:948–953. doi: 10.1126/science.1149345 CrossRefPubMedGoogle Scholar
  49. Harding AMA, Piatt JF, Schmutz JA (2007) Seabird behavior as an indicator of food supplies: sensitivity across the breeding season. Mar Ecol Prog Ser 352:269–274. doi: 10.3354/meps07072 CrossRefGoogle Scholar
  50. Hau M, Ricklefs RE, Wikelski M et al (2010) Corticosterone, testosterone and life-history strategies of birds. Proc R Soc B-Biol Sci 277:3203–3212. doi: 10.1098/rspb.2010.0673 CrossRefGoogle Scholar
  51. Hayward LS, Bowles AE, Ha JC, Wasser SK (2011) Impacts of acute and long-term vehicle exposure on physiology and reproductive success of the northern spotted owl. Ecosphere 2:1–20. doi: 10.1890/ES10-00199.1 CrossRefGoogle Scholar
  52. Hennin HL, Wells-Berlin AM, Love OP (2016) Baseline glucocorticoids are drivers of body mass gain in a diving seabird. Ecol Evol 6:1702–1711. doi: 10.1002/ece3.1999 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Herring G, Cook MI, Gawlik DE, Call EM (2011) Food availability is expressed through physiological stress indicators in nestling white ibis: a food supplementation experiment. Funct Ecol 25:682–690. doi: 10.1111/j.1365-2435.2010.01792.x CrossRefGoogle Scholar
  54. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528. doi: 10.1126/science.1189930 CrossRefPubMedGoogle Scholar
  55. Horvathova T, Nakagawa S, Uller T (2011) Strategic female reproductive investment in response to male attractiveness in birds. Proc R Soc B Biol Sci 279:163–170. doi: 10.1098/rspb.2011.0663 CrossRefGoogle Scholar
  56. Hussey NE, Kessel ST, Aarestrup K et al (2015) Aquatic animal telemetry: a panoramic window into the underwater world. Science 348:1255642–1–1255642–10. doi: 10.1126/science.1255642 CrossRefGoogle Scholar
  57. Jacobs SR, Elliott KH, Gaston AJ (2013) Parents are a Drag: long-lived birds share the cost of increased foraging effort with their offspring, but males pass on more of the costs than females. PLoS One 8:e54594. doi: 10.1371/journal.pone.0054594 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Jenni-Eiermann S, Glaus E, Grüebler M et al (2008) Glucocorticoid response to food availability in breeding barn swallows (Hirundo rustica). Gen Comp Endocrinol 155:558–565. doi: 10.1016/j.ygcen.2007.08.011 CrossRefPubMedGoogle Scholar
  59. Jetz W, Thomas GH, Joy JB et al (2012) The global diversity of birds in space and time. Nature 491:444–448. doi: 10.1038/nature11631 CrossRefPubMedGoogle Scholar
  60. Kitaysky AS, Wingfield JCC, Piatt JFF (1999) Dynamics of food availability, body condition and physiological stress response in breeding Black-legged kittiwakes. Funct Ecol 13:577–584. doi: 10.1046/j.1365-2435.1999.00352.x CrossRefGoogle Scholar
  61. Kitaysky AS, Piatt JF, Wingfield JC (2007) Stress hormones link food availability and population processes in seabirds. Mar Ecol Prog Ser 352:245–258. doi: 10.3354/meps07074 CrossRefGoogle Scholar
  62. Kitaysky AS, Piatt JF, Hatch SA et al (2010) Food availability and population processes: severity of nutritional stress during reproduction predicts survival of long-lived seabirds. Funct Ecol 24:625–637. doi: 10.1111/j.1365-2435.2009.01679.x CrossRefGoogle Scholar
  63. Lanctot RB, Hatch SA, Gill VA, Eens M (2003) Are corticosterone levels a good indicator of food availability and reproductive performance in a kittiwake colony? Horm Behav 43:489–502. doi: 10.1016/S0018-506X(03)00030-8 CrossRefPubMedGoogle Scholar
  64. 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 148:132–149. doi: 10.1016/j.ygcen.2006.02.013 CrossRefPubMedGoogle Scholar
  65. Leclaire S, Bourret V, Wagner RH et al (2011) Behavioral and physiological responses to male handicap in chick-rearing black-legged kittiwakes. Behav Ecol 22:1156–1165. doi: 10.1093/beheco/arr149 CrossRefGoogle Scholar
  66. Love OP, Breuner CW, Vézina F, Williams TD (2004) Mediation of a corticosterone-induced reproductive conflict. Horm Behav 46:59–65. doi: 10.1016/j.yhbeh.2004.02.001 CrossRefPubMedGoogle Scholar
  67. Love OP, Madliger CL, Bourgeon S et al (2014) Evidence for baseline glucocorticoids as mediators of reproductive investment in a wild bird. Gen Comp Endocrinol 199:65–69. doi: 10.1016/j.ygcen.2014.01.001 CrossRefPubMedGoogle Scholar
  68. Lynn SE, Stamplis TB, Barrington WT et al (2010) Food, stress, and reproduction: short-term fasting alters endocrine physiology and reproductive behavior in the zebra finch. Horm Behav 58:214–222. doi: 10.1016/j.yhbeh.2010.03.015 CrossRefPubMedGoogle Scholar
  69. Madliger CL, Love OP (2014) The need for a predictive, context-dependent approach to the application of stress hormones in conservation. Conserv Biol 28:283–287. doi: 10.1111/cobi.12185 CrossRefPubMedGoogle Scholar
  70. Madliger CL, Love OP (2015) The power of physiology in changing landscapes: considerations for the continued integration of conservation and physiology. Integr Comp Biol 55:1–9CrossRefGoogle Scholar
  71. Madliger CL, Love OP (2016) Do baseline glucocorticoids simultaneously represent fitness and environmental quality in an aerial insectivore? Oikos. doi: 10.1111/oik.03354 Google Scholar
  72. Madliger CL, Semeniuk CAD, Harris CM, Love OP (2015) Assessing baseline stress physiology as an integrator of environmental quality in a wild avian population: implications for use as a conservation biomarker. Biol Conserv 192:409–417. doi: 10.1016/j.biocon.2015.10.021 CrossRefGoogle Scholar
  73. Madliger CL, Cooke SJ, Crespi EJ et al (2016) Success stories and emerging themes in conservation physiology. Conserv Physiol 4:1–17. doi: 10.1093/conphys/cov057 CrossRefGoogle Scholar
  74. Mark MM, Rubenstein DR (2013) Physiological costs and carry-over effects of avian interspecific brood parasitism influence reproductive tradeoffs. Horm Behav 63:717–722. doi: 10.1016/j.yhbeh.2013.03.008 CrossRefPubMedGoogle Scholar
  75. McEwen BS, Wingfield JC (2010) What is in a name? Integrating homeostasis, allostasis and stress. Horm Behav 57:105–111. doi: 10.1016/j.yhbeh.2009.09.011 CrossRefPubMedGoogle Scholar
  76. Moody AT, Hobson KA, Gaston AJ (2012) High-arctic seabird trophic variation revealed through long-term isotopic monitoring. J Ornithol 153:1067–1078. doi: 10.1007/s10336-012-0836-0 CrossRefGoogle Scholar
  77. Nakagawa S, Santos ESA (2012) Methodological issues and advances in biological meta-analysis. Evol Ecol 26:1253–1274. doi: 10.1007/s10682-012-9555-5 CrossRefGoogle Scholar
  78. O’Connor CM, Gilmour KM, Arlinghaus R et al (2010) Seasonal carryover effects following the administration of cortisol to a wild teleost fish. Physiol Biochem Zool 83:950–957. doi: 10.1086/656286 CrossRefPubMedGoogle Scholar
  79. Orians GH, Pearson NE (1979) On the theory of central place foraging. In: Horn DJ, Mitchell RD, Stairs GR (eds) Analysis of ecological systems. Ohio State University Press, Columbus, pp 154–177Google Scholar
  80. Ouyang JQ, Sharp PJ, Dawson A et al (2011) Hormone levels predict individual differences in reproductive success in a passerine bird. Proc R Soc B Biol Sci 278:2537–2545. doi: 10.1098/rspb.2010.2490 CrossRefGoogle Scholar
  81. Ouyang JQ, Sharp P, Quetting M, Hau M (2013) Endocrine phenotype, reproductive success and survival in the great tit, Parus major. J Evol Biol 26:1988–1998. doi: 10.1111/jeb.12202 CrossRefPubMedGoogle Scholar
  82. Ozgul A, Childs DZ, Oli MK et al (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature 466:482–485. doi: 10.1038/nature09210 CrossRefPubMedGoogle Scholar
  83. Paleczny M, Hammill E, Karpouzi V, Pauly D (2015) Population trend of the world’s monitored seabirds, 1950–2010. PLoS One 10:e0129342. doi: 10.1371/journal.pone.0129342 CrossRefPubMedPubMedCentralGoogle Scholar
  84. Parsons M, Mitchell I, Butler A et al (2008) Seabirds as indicators of the marine environment. ICES J Mar Sci 65:1520–1526. doi: 10.1093/icesjms/fsn155 CrossRefGoogle Scholar
  85. Piatt JF, Harding AMA (2007) Population ecology of seabirds in cook inlet. In: Spies R (ed) Long-term ecological change in the Northern Gulf of Alaska. pp 335–352Google Scholar
  86. Piatt JF, Sydeman WJ (2007) Theme Section: seabirds as indicators of marine ecosystems. Mar Ecol Prog Ser 352:199–309. doi: 10.3354/meps07070 CrossRefGoogle Scholar
  87. Piatt JF, Harding AM, Shultz M et al (2007) Seabirds as indicators of marine food supplies: cairns revisited. Mar Ecol Prog Ser 352:221–234. doi: 10.3354/meps07078 CrossRefGoogle Scholar
  88. Plummer M, Best N, Cowles K, Vines K (2006) CODA: convergence diagnosis and output analysis for MCMC. R News 6:7–11. doi: 10.1159/000323281 Google Scholar
  89. Ponchon A, Grémillet D, Christensen-Dalsgaard S et al (2014) When things go wrong: intra-season dynamics of breeding failure in a seabird. Ecosphere 5:1–19. doi: 10.1890/ES13-00233.1 CrossRefGoogle Scholar
  90. Prokop ZM, Michalczyk Ł, Drobniak SM et al (2012) Meta-analysis suggests choosy females get sexy sons more than “Good genes”. Evolution (N Y) 66:2665–2673. doi: 10.1111/j.1558-5646.2012.01654.x Google Scholar
  91. Ramos R, Garnier R, Gonzalez-Solis J, Boulinier T (2014) Long antibody persistence and transgenerational transfer of immunity in a long-lived vertebrate. Am Nat 184:764–776. doi: 10.1086/678400 CrossRefPubMedGoogle Scholar
  92. Ricklefs RE, WIlkelski M (2002) The physiology/life history nexus. Trends Ecol Evol 17:462–469CrossRefGoogle Scholar
  93. Riechert J, Becker PH, Chastel O (2014) Predicting reproductive success from hormone concentrations in the common tern (Sterna hirundo) while considering food abundance. Oecologia 176:715–727. doi: 10.1007/s00442-014-3040-5 CrossRefPubMedGoogle Scholar
  94. Sanderson JL, Young AJ, Hodge SJ et al (2014) Hormonal mediation of a carry-over effect in a wild cooperative mammal. Funct Ecol 28:1377–1386. doi: 10.1111/1365-2435.12307 CrossRefGoogle Scholar
  95. Satterthwaite WH, Kitaysky AS, Mangel M (2012) Linking climate variability, productivity and stress to demography in a long-lived seabird. Mar Ecol Prog Ser 454:221–235. doi: 10.3354/meps09539 CrossRefGoogle Scholar
  96. Schultner J, Moe B, Chastel O et al (2014) Corticosterone mediates carry-over effects between breeding and migration in the kittiwake Rissa tridactyla. Mar Ecol Prog Ser 496:125–133. doi: 10.3354/meps10603 CrossRefGoogle Scholar
  97. Strasser EH, Heath JA (2013) Reproductive failure of a human-tolerant species, the American kestrel, is associated with stress and human disturbance. J Appl Ecol 50:912–919. doi: 10.1111/1365-2664.12103 CrossRefGoogle Scholar
  98. Thierry A-M, Brajon S, Spee M et al (2014) Differential effects of increased corticosterone on behavior at the nest and reproductive output of chick-rearing Adelie penguins. Behav Ecol Sociobiol 68:721–732. doi: 10.1007/s00265-014-1685-z CrossRefGoogle Scholar
  99. Weimerskirch H, Barbraud C, Lys P (2000) Sex differences in parental investment and chick growth in Wandering albatrosses: fitness consequences. Ecology 81:309–318CrossRefGoogle Scholar
  100. Weimerskirch H, Cherel Y, Delord K et al (2014) Lifetime foraging patterns of the wandering albatross: life on the move! J Exp Mar Bio Ecol 450:68–78. doi: 10.1016/j.jembe.2013.10.021 CrossRefGoogle Scholar
  101. Wendeln H, Becker PH (1999) Effects of parental quality and effort on the reproduction of common terns. J Anim Ecol 68:205–214. doi: 10.1046/j.1365-2656.1999.00276.x CrossRefGoogle Scholar
  102. Williams CT, Kitaysky AS, Kettle AB, Buck CL (2008) Corticosterone levels of tufted puffins vary with breeding stage, body condition index, and reproductive performance. Gen Comp Endocrinol 158:29–35. doi: 10.1016/j.ygcen.2008.04.018 CrossRefPubMedGoogle Scholar
  103. Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711–724. doi: 10.1046/j.1365-2826.2003.01033.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Graham H. Sorenson
    • 1
  • Cody J. Dey
    • 2
  • Christine L. Madliger
    • 1
    • 2
  • Oliver P. Love
    • 1
    • 2
  1. 1.Department of Biological SciencesUniversity of WindsorWindsorCanada
  2. 2.Great Lakes Institute for Environmental ResearchUniversity of WindsorWindsorCanada

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