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

  • Physiological ecology - Original research
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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.

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References

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

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

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

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

    Article  Google Scholar 

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

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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

    Article  PubMed  Google Scholar 

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

  • 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.

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

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

  • 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

    PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • 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

    Article  Google Scholar 

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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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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.

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  1. Institute of Avian Research “Vogelwarte Helgoland”, An der Vogelwarte 21, 26386, Wilhelmshaven, Germany

    Juliane Riechert & Peter H. Becker

  2. Centre d’Etudes Biologiques de Chizé, CNRS, 79360, Villiers En Bois, France

    Olivier Chastel

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  1. Juliane Riechert
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  2. Peter H. Becker
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Correspondence to Juliane Riechert.

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Communicated by Indrikis Krams.

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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

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