Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Predicting reproductive success from hormone concentrations in the common tern (Sterna hirundo) while considering food abundance

Abstract

In birds, reproductive success is mainly a function of skill or environmental conditions, but it can also be linked to hormone concentrations due to their effect on behavior and individual decisions made during reproduction. For example, a high prolactin concentration is required to express parental behaviors such as incubation or guarding and feeding the young. Corticosterone level, on the other hand, is related to energy allocation or stress and foraging or provisioning effort. In this study, we measured individual baseline prolactin and corticosterone between 2006 and 2012 in breeding common terns (Sterna hirundo) using blood-sucking bugs. Reproductive parameters as well as prey abundance on a local and a wider scale were also determined during this period. Baseline prolactin and corticosterone varied significantly between years, as did breeding success. At the individual level, prolactin was positively and corticosterone was negatively linked to herring and sprat abundance. At the population level, we also found a negative link between corticosterone and prey abundance, probably reflecting overall foraging conditions. High prolactin during incubation was mainly predictive of increased hatching success, potentially by supporting more constant incubation and nest-guarding behavior. It was also positively linked to a lesser extent with fledging success, which could indicate a high feeding rate of young. Corticosterone concentration was positively related to high breeding success, which may be due to increased foraging activity and feeding of young. In general, our study shows that baseline prolactin and corticosterone levels during incubation can predict reproductive success, despite the presence of an interval between sampling and hatching or fledging of young.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Angelier F, Chastel O (2009) Stress, prolactin and parental investment in birds: a review. Gen Comp Endocrinol 163:142–148

  2. Angelier F, Barbraud C, Lormée H, Prud’Homme F, Chastel O (2006) Kidnapping of chicks in emperor penguins: a hormonal by-product? J Exp Biol 209:1413–1420

  3. Angelier F, Shaffer SA, Weimerskirch H, Trouvé C, Chastel O (2007a) Corticosterone and foraging behavior in a pelagic seabird. Physiol Biochem Zool 80:283–293

  4. Angelier F, Clément-Chastel C, Gabrielsen GW, Chastel O (2007b) Corticosterone and time-activity budget: an experiment with black-legged kittiwakes. Horm Behav 52:482–491

  5. Angelier F, Clément-Chastel C, Welcker Y, Gabrielsen GW, Chastel O (2009) How does corticosterone affect parental behaviour and reproductive success? A study of prolactin in black-legged kittiwakes. Funct Ecol 23:784–793

  6. 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

  7. Angelier F, Wingfield JC, Trouvé C, de Grissac S, Chastel O (2013) Modulation of the prolactin and corticosterone stress responses: do they tell the same story in a long-lived bird, the Cape petrel? Gen Comp Endocrinol 182:7–15

  8. Arnold JM, Oswald SA, Voigt CC, Palme R, Braasch A, Bauch C, Becker PH (2008) Taking the stress out of blood collection: comparison of field blood-sampling techniques for analysis of baseline corticosterone. J Avian Biol 39:588–592

  9. Astheimer LB, Buttemer WA, Wingfield JC (1992) Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scand 23:355–365

  10. Becker PH (1998) Long-term trends of breeding success in Common Terns Sterna hirundo in the Wadden Sea. Vogelwelt 119:223–234

  11. Becker PH, Ludwigs J-D (2004) Sterna hirundo, common tern. BWP Update 6:91–137

  12. Becker PH, Wendeln H (1997) A new application for transponders in population ecology of the common tern. Condor 99:534–538

  13. Becker PH, Wink M (2002) Geschlechtsabhängige Größenunterschiede von Flügglingen der Flussseeschwalbe (Sterna hirundo). J Ornithol 143:51–56

  14. Becker PH, Frank D, Walter U (1987) Geographische und jährliche Variation der Ernährung der Flussseeschwalbe (Sterna hirundo) an der Nordseeküste. J Ornithol 128:457–475

  15. Becker PH, Frank D, Sudmann SR (1993) Temporal and spatial patterns of common tern (Sterna hirundo) foraging in the Wadden Sea. Oecologia 93:389–393

  16. Becker PH, Voigt CC, Arnold JM, Nagel R (2006) A non-invasive technique to bleed incubating birds without trapping: a blood-sucking bug in a hollow egg. J Ornithol 147:115–118

  17. Bonier F, Martin PR, Moore IT, Wingfield JC (2009a) Do baseline glucocorticoids predict fitness? TREE 24:634–642

  18. Bonier F, Moore IT, Martin PR, Robertson RJ (2009b) The relationship between fitness and baseline glucocorticoids in a passerine bird. Gen Comp Endocrinol 163:208–213

  19. Bonier F, Moore IT, Robertson RJ (2013) The stress of parenthood? Increased glucocorticoids in birds with experimentally enlarged broods. Biol Lett. doi:10.1098/rsbl.2011.0391

  20. Buck CL, O’Reilly KM, Kildaw SD (2007) Interannual variability of black-legged kittiwake productivity is reflected in baseline plasma corticosterone. Gen Comp Endocrinol 150:430–436

  21. Buntin JD (1996) Neural and hormonal control of parental behaviour in birds. In: Rosenblatt JS, Snowdown CT (eds) Advances in the study of behaviour. Academic, New York, pp 161–213

  22. Buntin JD, Becker GM, Ruzycki E (1991) Facilitation of parental behavior in ring doves by systemic or intracranial injections of prolactin. Horm Behav 25:424–444

  23. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

  24. Chastel O, Lacroix A, Weimerskirch H, Gabrielsen GW (2005) Modulation of prolactin but not corticosterone response to stress in relation to parental effort in a long-lived bird. Horm Behav 47:459–467

  25. Criscuolo F, Chastel O, Gabrielsen GW, Lacroix A, Le Maho Y (2002) Factors affecting plasma concentration of prolactin in the common eider Somateria mollissima. Gen Comp Endocrinol 125:399–409

  26. Criscuolo F, Chastel O, Gabrielsen GW, Lacroix A, MahoY Le (2003) Relationship between nutritional status and prolactin levels in the common eider, a capital incubator. In: Huiskes AHL, Gieskes WWC, Rozena J, Schorno RML, van der Vies SM, Wolff WJ (eds) Antarctic biology in a global context. Backhuys, Leyden, pp 193–197

  27. Crossin G, Trathan PN, Phillips RA, Gorman KB, Dawson A, Sakamoto KQ, Williams TD (2012) Corticosterone predicts foraging behavior and parental care in Macaroni penguins. Am Nat 180:E31–E41

  28. Dänhardt A (2013) Erfassung der Fischfauna an der Jade mittels Hamenkutter vor dem Hintergrund der Meeresstrategie-Rahmenrichtlinie.

  29. Dänhardt A, Becker PH (2008) Die Bedeutung Umweltbedingter Verteilungsmuster von Schwarmfischen für Seevögel im Ökosystem Niedersächsiches Wattenmeer. Abschlussbericht des Projektes 53-NWS-41/04 der Niedersächsischen Wattenmeerstiftung.

  30. Dänhardt A, Becker PH (2011a) Herring and sprat abundance indices predict chick growth and reproductive performance in common terns breeding in the Wadden Sea. Ecosystems 14:791–803

  31. Dänhardt A, Becker PH (2011b) Does small scale vertical distribution of juvenile schooling fish affect prey availability to surface-feeding seabirds in the Wadden Sea? J Sea Res 65:247–255

  32. Delehanty DJ, Oring LW, Fivizzani AJ, El Halawani ME (1997) Circulating prolactin of incubating male Wilson’s Phalaropes corresponds to clutch size and environmental stress. Condor 99:397–405

  33. Doody LM, Wilhelm SI, McKay DW, Walsh CJ, Storey AE (2008) The effects of variable foraging conditions on common murre (Uria aalge) corticosterone concentrations and parental provisioning. Horm Behav 53:140–148

  34. Duckworth RA, Badyaev AV, Parlow AF (2003) Elaborately ornamented males avoid costly parental care in the house finch (Carpodacus mexicanus): a proximate perspective. Behav Ecol Sociobiol 55:176–183

  35. El Halawani ME, Silsby JL, Rozenboim I, Pitts GR (1995) Increased egg production by active immunization against vasoactive intestinal peptide in the turkey (Meleagris gallopova). Biol Repro 52:179–183

  36. Golet GH, Schmutz JA, Irons DB, Estes JA (2004) Determinants of reproductive costs in the long-lived black-legged kittiwake: a multiyear experiment. Ecol Monogr 74:353–372

  37. ICES (2013) Report of the Herring Assessment Working Group for the area south of 62 N (HAWG), 12–21 March 2013. ICES Headquarters, Copenhagen

  38. Jaatinen K, Seltman MW, Hollmén T, Atkinson S, Mashburn K, Öst M (2013) Context dependency of baseline glucocorticoids as indicators of individual quality in a capital breeder. Gen Comp Endocrinol. doi:10.1016/j.ygcen2013.06.022

  39. Kitaysky AS, Wingfield JC, Piatt JF (1999) Dynamics of food availability, body condition and physiological stress response in breeding black-legged Kittiwakes. Funct Ecol 13:577–584

  40. Kitaysky AS, Piatt JF, Wingfield JC (2007) Stress hormones link food availability and population processes in seabirds. Mar Ecol Prog Ser 352:245–258

  41. Kitaysky AS, Piatt JF, Hatch SA, Kitaiskaia 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 24:625–637

  42. 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

  43. Limmer B, Becker PH (2010) Improvement of reproductive performance with age and breeding experience depends on recruitment age in a long-lived seabird. Oikos 117:60–68

  44. Lormée H, Jouventin P, Trouvé C, Chastel O (2003) Sex-specific patterns in baseline corticosterone and body condition changes in breeding Red-footed Boobies Sula sula. Ibis 145:212–219

  45. McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15

  46. McNamara JM, Buchanan KL (2005) Stress, resource allocation and mortality. Behav Ecol 16:1008–1017

  47. O’Dwyer TW, Buttermer WA, Priddel DM, Downing JA (2006) Prolactin, body condition and the cost of good parenting: an interyear study in a long-lived seabird, Gould’s Petrel (Pterodrom leucoptera). Funct Ecol 20:806–811

  48. Ouyang J, Sharp PJ, Dawson A, Quetting M, Hau M (2011) Hormone levels predict individual differences in reproductive success in a passerine bird. Proc R Soc B 278:2537–2545

  49. Quillfeldt P (2001) Variation in breeding success in Wilson’s storm petrels: influence of environmental factors. Antarct Sci 13:400–409

  50. Rebke M, Coulson T, Becker PH, Vaupel WP (2010) Reproductive improvement and senescence in a long-lived bird. Proc Natl Acad Sci USA 107:7841–7846

  51. Riechert J, Chastel O, Becker PH (2012) Why do experienced birds reproduce better? Possible endocrine mechanisms in a long-lived seabird, the common tern. Gen Comp Endocrinol 178:391–399

  52. Riechert J, Chastel O, Becker PH (2014) Regulation of breeding behavior: do energy-demanding periods induce a change in prolactin or corticosterone baseline levels in the common tern (Sterna hirundo)? Physiol Biochem Zool 87(3):420–431

  53. Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Physiol A 140:73–79

  54. Romero LM, Romero RC (2002) Corticosterone responses in wild birds: the importance of rapid initial sampling. Condor 104:129–135

  55. Romero LM, Wikelski M (2001) Corticosterone levels predict survival probabilities of Galápagos marine iguanas during El Niño events. Proc Natl Acad Sci USA 98:7366–7370

  56. Romero LM, Reed JM, Wingfield JC (2000) Effect of weather on corticosterone responses in wild free-living passerine birds. Gen Comp Endocrinol 118:113–122

  57. Satterthwaite WJ, Kitaysky AS, Mangel M (2012) Linking climate variability, productivity and stress to demography in a long-lived seabird. Mar Ecol Proc Ser 454:221–235

  58. Sharp PJ, Sterling RJ, Talbot RP, Huskisson NS (1989) The role of the hypothalamic vasoactive intestinal polypeptide in the maintenance of prolactin secretion in incubating bantam hens: observations using passive immunization, radioimmunoassay, and immunocytochemistry. J Endocrinol 122:5–13

  59. Shultner J, Kitaysky AS, Welcker Y, Hatch S (2013a) Fat or lean: adjustment of endogenous energy stores to predictable and unpredictable changes in allostatic load. Funct Ecol 27:45–55

  60. Shultner J, Kitaysky AS, Gabrielsen GW, Hatch SA, Bech C (2013b) Differential reproductive responses to stress reveal the role of life-history strategies within a species. Proc R Soc B 280(1771):20132090. doi:10.1098/rspb.2013.2090

  61. Sinervo B, Svennson E (1998) Mechanistic and selective causes of life-history trade-offs and plasticity. Oikos 83:432–442

  62. Spee M, Beaulieu M, Dervaux A, Chastel O, Le Maho Y, Raclot T (2010) Should I stay or should I go? Hormonal control of nest abandonment in a long-lived bird, the Adélie penguin. Horm Behav 58:762–768

  63. Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

  64. Szostek KL, Becker PH (2012) Terns in trouble: demographic consequences of low breeding success and recruitment on a common tern population in the German Wadden Sea. J Ornithol 153:313–326

  65. Wagener M (1998) Praktische Hinweise für brutbiologische Untersuchungen an der Flussseeschwalbe Sterna hirundo. Vogelwelt 119:279–286

  66. Wang Q, Buntin JD (1999) The roles of stimuli from young, previous breeding experience, and plasma prolactin in regulating parental behaviour in ring doves (Streptopelia risoria). Horm Behav 35:241–253

  67. Welcker Y, Harding AMA, Kitaysky AS, Speakman JR, Gabrielsen GW (2009) Daily energy expenditure increases in response to low nutritional stress in an Arctic-breeding seabird with no effect on mortality. Funct Ecol 23:1081–1090

  68. Wendeln H (1997) Body mass of female common terns (Sterna hirundo) during courtship: relationships to male quality, egg mass, diet, laying date and age. Colon Waterbirds 20:235–243

  69. Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how? J Neuroendocrinol 15:711–724

  70. Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone–behavior interactions: the “emergency life history stage”. Am Zool 38:191–206

  71. Youngren OM, El Halawani ME, Silsby JL, Phillips RE (1991) Intracranial prolactin perfusion induced incubation behavior in turkey hens. Biol Reprod 44:425–431

Download references

Acknowledgments

We are very grateful for assistance of C. Bauch, N. Eckstein, J. Erber, J. Krauss, S. Kreutzer, L. Peters, J. Spieker, K. Weißenfels, and C. Wolters in taking blood samples, and we wish to thank many field assistants for their help in collecting field data, especially G. Wagenknecht. At the CEBC, we thank S. Danó, A. Lacroix, C. Parenteau, and C. Trouvé for their excellent technical work in hormone assays. We thank Dr. A. F. Parlow for supplying chicken prolactin and antibodies. Many thanks to G.A. Schaub from the University of Bochum for providing the bugs and to J. Trauernicht as well as R. Nagel for technical support. L. Szostek and O. Vedder helped to improve the manuscript. This study was performed under the license of Bezirksregierung Weser-Ems and Stadt Wilhelmshaven and was supported by the Deutsche Forschungsgemeinschaft (BE916/8 and 9). The authors declare that there is no conflict of interest.

Author information

Correspondence to Juliane Riechert.

Additional information

Communicated by Indrikis Krams.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Riechert, J., Becker, P.H. & Chastel, O. Predicting reproductive success from hormone concentrations in the common tern (Sterna hirundo) while considering food abundance. Oecologia 176, 715–727 (2014). https://doi.org/10.1007/s00442-014-3040-5

Download citation

Keywords

  • Prolactin
  • Corticosterone
  • Breeding success
  • Year effect
  • Food abundance