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Arrival date and territorial behavior are associated with corticosterone metabolite levels in a migratory bird

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Abstract

Glucocorticoids promote the mobilization of energy stores and they may facilitate the expression of energetically expensive functions. Early arrival on the breeding grounds in migratory species and territorial competition are energetically demanding activities that may be supported by elevated baseline glucocorticoid levels. Here, we evaluated the associations between the baseline levels of excreted corticosterone (CORT) metabolites of male Pied Flycatchers (Ficedula hypoleuca) just after arriving on their breeding area and timing of arrival, considering ornamental traits indicative of social status, like forehead patch size and black plumage coloration, as well as heat shock protein levels (HSP60). We observed a positive association of CORT metabolites with HSP60 levels, which are synthesized under several environmental challenges affecting cell homeostasis. Our data showed a negative association between arrival date and CORT metabolite levels, possibly as a result of the higher energetic demands imposed by the hard environmental conditions experienced at the time of an early arrival after migration. We observed a negative relationship of forehead patch dimensions and CORT metabolite levels, suggesting that dominance is associated with low baseline CORT metabolites. Also, males that expressed a higher degree of territorial behaviour when exposed to a playback song of a conspecific at their nest-box showed higher CORT metabolites upon arrival than males that expressed a lower degree of territorial behavior. This may indicate that elevated baseline CORT metabolite levels may facilitate an intense territorial competition in males. Thus, male–male competition may be a factor affecting observed baseline glucocorticoid levels in migratory birds.

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References

  • Alatalo R, Lundberg A, Sundberg J (1990) Can female preference explain sexual dichromatism in the pied flycatcher Ficedula hypoleuca? Anim Behav 39:244–252

    Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Barr CS, Dokas LA (1999) Glucocorticoids regulate the synthesis of HSP27 in rat brain slices. Brain Res 13:9–17

    Google Scholar 

  • Becker JB, Breedlove SM (2002) Introduction to behavioral endocrinology. In: Becker JB, Breedlove SM, Crews D, McCarthy MM (eds) Behavioral endocrinology, 2nd edn. MIT Press, Cambridge

    Google Scholar 

  • Belthoff JR, Dufty AM Jr (1994) Plumage variation, plasma steroids and social dominance in male house finches. Condor 96:614–625

    Google Scholar 

  • Berger S, Martin LB II, Wikelski M, Romero M, Kalko EKV, Vitousek MN, Rödl T (2005) Corticosterone suppresses immune activity in territorial Galápagos marine iguanas during reproduction. Horm Behav 47:419–429

    CAS  PubMed  Google Scholar 

  • Bourgeon S, Martínez J, Criscuolo F, Le Maho Y, Raclot T (2006) Fasting-induced changes of immunological and stress indicators in breeding female eiders. Gen Comp Endocrinol 147:336–342

    CAS  PubMed  Google Scholar 

  • Breuner CW, Hahn TP (2003) Integrating stress physiology, environmental change, and behavior in free-living sparrows. Horm Behav 43:115–123

    PubMed  Google Scholar 

  • Brown CR, Brown MB (2000) Weather-mediated natural selection on arrival time in cliff swallows (Petrochelidon pyrrhonota). Behav Ecol Sociobiol 47:339–345

    Google Scholar 

  • Cherel Y, Robin JP, Walch O, Karmann H, Netchitailo P, Le Maho Y (1988) Fasting in king penguin. I. Hormonal and metabolic changes during breeding. Am J Physiol Regul Integr Comp Physiol 254:170–177

    Google Scholar 

  • Creel S (2001) Social dominance and stress hormones. Trends Ecol Evol 16:491–497

    Google Scholar 

  • Dale S, Slagsvold T, Lampe HM, Saetre GP (1999) Population divergence in sexual ornaments: the white forehead patch of Norwegian pied flycatchers is small and unsexy. Evolution 53:1235–1246

    PubMed  Google Scholar 

  • Darwin C (1871) The descent of man, and selection in relation to sex. Murray, London

    Google Scholar 

  • Davies NB (1980) The economics of territorial behaviour in birds. Ardea 68:63–74

    Google Scholar 

  • Ding Q, Vaynman S, Souda P, Whitelegge JP, Gomez-Pinilla F (2006) Exercise affects energy metabolism and neural plasticity-related proteins in the hippocampus as revealed by proteomic analyses. Eur J Neurosci 24:1265–1276

    PubMed  Google Scholar 

  • Drost R (1936) Über das Brutkleid männlicher Trauerfliegenschnäpper Muscicapa hypoleuca. Vogelzug 6:179–186

    Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    CAS  PubMed  Google Scholar 

  • Feige U, Polla BS (1994) HSP70—a multigene, multistructure, multifunction with potential clinical applications. Experientia 50:979–986

    CAS  PubMed  Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. Clarendon, Oxford

    Google Scholar 

  • Fleshner M, Campisi J, Amiri J, Diamond DM (2004) Cat exposure induces both intra- and extracellular Hsp72: the role of adrenal hormones. Psychoneuroendocrinol 29:1142–1152

    CAS  Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, brigth males and the immunocompetence handicap. Am Nat 139:603–622

    Google Scholar 

  • Garamszegi LZ, Merino S, Török J, Eens M, Martínez J (2006) Indicators of physiological stress and the elaboration of sexual traits in the collared flycatcher. Behav Ecol 17:399–404

    Google Scholar 

  • Gil D, Gahr M (2002) The honesty of bird song: multiple constraints for multiple traits. Trends Ecol Evol 17:133–141

    Google Scholar 

  • Gottlander K (1987) Variation in the song rate of the male pied flycatcher Ficedula hypoleuca: causes and consequences. Anim Behav 35:1037–1043

    Google Scholar 

  • Goymann W (2005) Noninvasive monitoring of hormones in bird droppings: physiological validation, sampling, extraction, sex differences and the influence of diet on hormone metabolite levels. Ann N Y Acad Sci 1046:35–53

    CAS  PubMed  Google Scholar 

  • Goymann W, Wingfield JC (2004) Allostatic load, social status and stress hormones: the cost of social status matter. Anim Behav 67:591–602

    Google Scholar 

  • Gustafsson L, Qvarnström A, Sheldon BC (1995) Trade-offs between life-history traits and a secondary sexual character in male collared flycatchers. Nature 375:311–313

    CAS  Google Scholar 

  • Haller J, Albert I, Makara GB (1997) Acute effects of corticosterone lack specificity but showed marked context dependency. J Neuroendocrinol 9:515–518

    CAS  PubMed  Google Scholar 

  • Hayden-Hixson DM, Ferris CF (1991) Cortisol exerts site-, context- and dose-dependent effects on agonistic responding in hamsters. J Neuroendocrinol 3:613–622

    CAS  PubMed  Google Scholar 

  • Herring G, Gawlik DE (2007) The role of stress proteins in the study of allostatic overload in birds: use and applicability to current studies in avian ecology. ScientificWorld J 28:1596–1602

    Google Scholar 

  • Holberton RL (1999) Changes in patterns of corticosterone secretion concurrent with migratory fattening in a Neotropical migratory bird. Gen Comp Endocrinol 116:49–58

    CAS  PubMed  Google Scholar 

  • Holberton RL, Able KP, Wingfield JC (1989) Status signaling in dark-eyed juncos, Junco hyemalis: plumage manipulations and hormonal correlates of dominance. Anim Behav 37:681–689

    Google Scholar 

  • Holberton RL, Parrish JD, Wingfield JC (1996) Modulation of the adrenocortical stress response in neotropical migrans during autumn migration. Auk 113:558–564

    Google Scholar 

  • Husak JF, Moore IT (2008) Stress hormones and mate choice. Trends Ecol Evol 23:532–534

    PubMed  Google Scholar 

  • Järvi T, Røskaft E, Bakken M, Zumsteg B (1987) Evolution of variation in male secondary sexual characteristics. A test of eight hypotheses applied to pied flycatchers. Behav Ecol Sociobiol 20:161–169

    Google Scholar 

  • Kilpimaa J, Alatalo RV, Siitari H (2004) Trade-offs between sexual advertisement and immune function in the pied flycatcher (Ficedula hypoleuca). Proc R Soc Lond B 271:245–250

    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

    Google Scholar 

  • Kokko H (1999) Competition for early arrival in migratory birds. J Anim Ecol 68:940–950

    Google Scholar 

  • Krebs JR (1980) Optimal foraging, predation risk and territory defence. Ardea 68:83–90

    Google Scholar 

  • Kroodsma DE, Byers BE, Goodale E, Johnson S, Liu W (2001) Pseudoreplication in playback experiments, revisited a decade later. Anim Behav 61:1029–1033

    Google Scholar 

  • Landys MM, Wingfield JC, Ramenosfky M (2004) Plasma corticosterone increases during migratory restlessness in the captive white-crowned sparrow Zonotrichia leucophrys gambelli. Horm Behav 46:574–581

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Landys MM, Goymann W, Raess M, Slagsvold T (2007) Hormonal responses to male-male social challenge in the blue tit Cyanistes caeruleus: single-broodedness as an explanatory variable. Physiol Biochem Zool 80:228–240

    CAS  PubMed  Google Scholar 

  • Landys-Ciannelli MM, Ramenosfky M, Piersma T, Group CastricumRinging, Wingfield JC (2002) Baseline and stress-induced plasma corticosterone during long-distance migration in the bar-tailed godwit, Limosa lapponica. Physiol Biochem Zool 75:101–110

    CAS  PubMed  Google Scholar 

  • Lobato E, Merino S, Moreno J, Morales J, Tomás G, Martínez-de la Puente J, Osorno JL, Kuchar A, Möstl E (2008) Corticosterone metabolites in blue tits and pied flycatcher droppings: effects of brood size, ectoraparasites and temperature. Horm Behav 53:295–305

    CAS  PubMed  Google Scholar 

  • Lormée H, Jouventin P, Trouve 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

    Google Scholar 

  • Lundberg A, Alatalo RV (1992) The pied flycatcher. Academic, London

    Google Scholar 

  • Marra PP, Holberton RL (1998) Corticosterone levels as indicators of habitat quality: effects of habitat segregation in a migratory bird during the non-breeding season. Oecologia 116:284–292

    PubMed  Google Scholar 

  • Martínez J, Pérez-Serrano J, Bernadina WE, Rodriguez-Caabeiro F (2001) Stress response to cold in Trichinella species. Cryobiology 43:293–302

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Merino S, Martínez J, Barbosa A, Møller AP, De Lope F, Pérez J, Rodríguez-Caabeiro F (1998) Increase in a heat shock protein from blood cells in response to parasitism of nestling house martins (Delichon urbica): an experimental approach. Oecologia 116:343–347

    CAS  PubMed  Google Scholar 

  • Merino S, Martínez J, Møller AP, Barbosa A, de Lope F, Rodríguez-Caabeiro F (2002) Blood stress protein levels in relation to sex and parasitism of barn swallows (Hirundo rustica). Ecoscience 9:300–305

    Google Scholar 

  • Mikics E, Kruk MR, Haller J (2004) Genomic and non-genomic effects of glucocorticoids on aggressive behavior in male rats. Psychoneuroendocrinology 29:618–635

    CAS  PubMed  Google Scholar 

  • Mikics E, Barsi B, Haller J (2007) The effect glucocorticoids on aggressiveness in established colonies of rats. Psychoneuroendocrinology 32:160–170

    CAS  PubMed  Google Scholar 

  • Millspaugh JJ, Washburn BE (2004) Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. Gen Comp Endocrinol 138:189–199

    CAS  PubMed  Google Scholar 

  • Møller AP (1994) Phenotype-dependent arrival time and its cosequences in migratory birds. Behav Ecol Sociobiol 35:115–122

    Google Scholar 

  • Moore MC, Jessop TS (2003) Stress, reproduction and adrenocortical modulation in amphibians and reptiles. Horm Behav 43:39–47

    CAS  PubMed  Google Scholar 

  • Moreno J, Potti J, Yorio P, García-Borboroglu P (2001) Sex differences in cell-mediated immunity in the magellanic penguin Spheniscus magellanicus. Ann Zool Fenn 38:111–116

    Google Scholar 

  • Moreno J, Merino S, Martínez J, Sanz JJ, Arriero E (2002) Heterophil/lymphocyte ratios and the heat-shock protein levels are related to growth in nestling birds. Ecoscience 9:434–439

    Google Scholar 

  • Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12:3788–3796

    CAS  PubMed  Google Scholar 

  • Möstl E, Maggs JL, Schrötter G, Besenfelder U, Palme R (2002) Measurement of cortisol metabolites in faeces of ruminants. Vet Res Commun 26:127–139

    PubMed  Google Scholar 

  • Newton I (2007) Weather-related mass-mortality events in migrants. Ibis 149:453–467

    Google Scholar 

  • Olanrewaju HA, Wongpichet S, Thaxton JP, Dozier WA III, Branton SL (2006) Stress and acid-base balance in chickens. Poult Sci 85:1266–1274

    CAS  PubMed  Google Scholar 

  • Osorno JL, Morales J, Moreno J, Merino S, Tomás G, Vásquez RA (2006) Evidence for differential maternal allocation to eggs in relation to manipulated male attractiveness in the pied flycatcher (Ficedula hypoleuca). J Ornithol 147:605–611

    Google Scholar 

  • Palme R, Rettenbacher S, Touma C, El-Bahr SM, Möstl E (2005) Stress hormones in mammals and birds. Comparative aspects regarding metabolism excretion and noninvasive measurement in fecal samples. Ann N Y Acad Sci 1049:162–171

    Google Scholar 

  • Pärt T, Qvarnström A (1997) Badge size in collared flycatchers predict outcome of male competition over territories. Anim Behav 54:893–899

    Google Scholar 

  • Piersma T, Reneerkens J, Ramenosfky M (2000) Baseline corticosterone peaks in shorebirds with maximal energy stores for migration: a general preparatory mechanism for rapid behavioral and metabolic transitions? Gen Comp Endocrinol 120:118–126

    CAS  PubMed  Google Scholar 

  • Poisbleau M, Fritz H, Guillon N, Chastel O (2005) Linear social dominance hierarchy and corticosterone responses in male mallard and pintails. Horm Behav 47:485–492

    CAS  PubMed  Google Scholar 

  • Potti J, Montalvo S (1991a) a male arrival and female mate choice in pied flycatchers Ficedula hypoleuca in Central Spain. Ornis Scand 22:45–55

    Google Scholar 

  • Potti J, Montalvo S (1991b) Male colour variation in Spanish pied flycatchers Ficedula hypoleuca. Ibis 133:293–299

    Google Scholar 

  • Pravosudov VV, Mendoza SP, Clayton NS (2003) The relationship between dominance, corticosterone, memory, and food caching in mountain chickadees (Poecile gambeli). Horm Behav 44:93–102

    CAS  Google Scholar 

  • Qvarnström A, Pärt T, Sheldon B (2000) Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature 405:344–347

    PubMed  Google Scholar 

  • Råberg L, Grahn M, Hasselquist D, Svensson E (1998) On the adaptive significance of stress-induced immunosupression. Proc R Soc Lond B 265:1637–1641

    Google Scholar 

  • Rettenbacher S, Möstl E, Hackl R, Ghareeb K, Palme R (2004) Measurement of corticosterone metabolites in chicken droppings. Br Poult Sci 45:704–711

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Romero LM, Ramenofsky M, Wingfield JC (1997) Season and migration alters the corticosterone response to capture and handling in an artic migrant, the white-crowned sparrow (Zonotrichia leucophrys gambelli). Comp Biochem Physiol C 116:171–177

    CAS  PubMed  Google Scholar 

  • Saetre GP, Dale S, Slagvold T (1994) Female pied flycatchers prefer brightly coloured males. Anim Behav 48:1407–1416

    Google Scholar 

  • Saino N, Møller AP (1995) Sexual ornamentation and immunocompetence in the barn swallow. Behav Ecol 7:227–232

    Google Scholar 

  • Saino N, Galeotti P, Sacchi R, Møller AP (1996) Song and immunological condition in male barn swallows (Hirundo rustica). Behav Ecol 8:364–371

    Google Scholar 

  • Sanz JJ, Potti J, Moreno J, Merino S, Frías O (2003) Climate change and fitness components of a migratory bird breeding in the Mediterranean region. Glob Change Biol 9:461–472

    Google Scholar 

  • Sapolsky RM (2000) Stress hormones: good and bad. Neurobiol Dis 7:540–542

    CAS  PubMed  Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89

    CAS  PubMed  Google Scholar 

  • Schäfler AE, Kirmanoglou K, Pecher P, Hannekum A, Schumacher B (2002) Overexpression of heat shock protein 60/10 in myocardium of patiens with chronic atrial fibrillation. Ann Thorac Surg 74:767–770

    PubMed  Google Scholar 

  • Schlesinger MJ (1990) Heat shock proteins. J Biol Chem 265:12111–12114

    CAS  PubMed  Google Scholar 

  • Schwabl H, Ramenosfsky M, Schwabl-Benzinger I, Farner DS, Wingfield JC (1988) Social status, circulating levels of hormones, and competition for food in winter flocks of the white-throated sparrow. Behaviour 107:107–121

    Google Scholar 

  • Smith RJ, Moore FR (2005) Arrival timing and seasonal reproductive performance in longdistace migratory landbird. Behav Ecol Sociobiol 57:231–239

    Google Scholar 

  • Sørensen JG, Kristensen TN, Loeschke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037

    Google Scholar 

  • Sorenson LG, Nolan PM, Brown AM, Derrickson SR, Monfort SL (1997) Hormonal dynamics during mate choice in the northern pintail: a test of the challenge hypothesis. Anim Behav 54:1117–1133

    CAS  PubMed  Google Scholar 

  • Svensson L (1984) Identification guide to European passerines. Ugga, Stockholm

    Google Scholar 

  • Thambirajah AA, Sleigh K, Stiver HG, Chow AW (2008) Differential heat shock protein responses to strenuous standardized exercise in chronic fatigue syndrome patients and matched healthy controls. Clin Invest Med 31:319–327

    Google Scholar 

  • Tomás G, Martínez J, Merino S (2004) Collection and analysis of blood samples to detect stress proteins in wild birds. J Field Ornithol 75:281–287

    Google Scholar 

  • Tomás G, Merino S, Martínez J, Moreno J, Sanz JJ (2005) Stress protein levels and blood parasite infection in blue tits (Parus caeruleus): a medication field experiment. Ann Zool Fenn 42:45–56

    Google Scholar 

  • Van Duyse E, Pinxten R, Darras VM, Arckens L, Eens M (2004) Opposite changes in plasma testosterone and corticosterone levels following a simulated territorial challenge in male great tits. Behaviour 141:451–567

    Google Scholar 

  • Washburn BS, Moreland JJ, Slaughter AM, Werner I, Hinton DE, Sanders BM (2002) Effects of handling on heat shock protein expression in rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 21:557–560

    CAS  PubMed  Google Scholar 

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Acknowledgments

This paper is dedicated to the memory of José Luis Osorno who planned this study during a sabbatical leave in Madrid in 2002–2003. The study has received financial support from projects CGL2004-00787/BOS and CGL2007-61251 to J. Moreno and BOS2003-05724 and CGL2006-14129-C02-01/BOS to S.M. (DGI-Ministerio de Ciencia e Innovación). All procedures conform to the requirements of animal welfare and conservation of Spanish laws. J. Morales and G.T. were supported by grants from MEC and Comunidad de Madrid respectively. E.L. was supported by a FPU grant from MEC. R.A.V. acknowledges support from a grant CSIC-Universidad de Chile 2003-04-09, ICM,-P05-002, and PFB-23-CONICYT-Chile. Consuelo Corral and Tonantzin Calvo helped in the field. We thank Chris Guglielmo and an anonymous reviewer for their constructive comments on a previous version of this manuscript. We were authorized by Javier Donés, Director of the Montes de Valsaín reserve, to work in the study area. Dirección General del Medio Natural-Junta de Castilla y León authorized the capture, ringing, and blood sampling of birds. This paper is a contribution from the El Ventorrillo field station.

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Correspondence to Elisa Lobato.

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Communicated by C. G. Guglielmo.

J. L. Osorno: Deceased.

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Lobato, E., Moreno, J., Merino, S. et al. Arrival date and territorial behavior are associated with corticosterone metabolite levels in a migratory bird. J Ornithol 151, 587–597 (2010). https://doi.org/10.1007/s10336-009-0488-x

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