Journal of Ornithology

, Volume 148, Supplement 2, pp 169–178 | Cite as

Stress, corticosterone responses and avian personalities

  • John F. CockremEmail author


Birds are constantly responding to stimuli from their environment. When these stimuli are perceived as threatening, stress responses are initiated, with activation of the hypothalamo-pituitary-adrenal axis and the release of corticosterone from the adrenal gland. The basic emotion of fear is also experienced during a stress response. Corticosterone stress responses and behavioural responses to stimuli vary markedly between individual birds, raising questions about the significance of these individual differences and about the relationship between corticosterone responses and fearfulness in birds. Although fearfulness can be challenging to measure, data from several species indicate that corticosterone responses and fear behaviour responses are linked in individual birds. Consistent profiles of behavioural responses of birds to a wide range of stimuli can be identified and are called personalities. Personalities vary along a continuum, but are usually classified as proactive or reactive. Individual corticosterone and behaviour responses depend on each bird’s personality. Birds with proactive personalities have relatively active behavioural responses and relatively low corticosterone stress responses, whilst birds with reactive personalities have relatively passive behavioural responses and large corticosterone responses. Relationships between the physiological and behavioural characteristics of avian personalities can now be explored in detail to determine the significance of individual differences in stress responses and personalities in birds.


Corticosterone Stress Fear Personality Behaviour Japanese quail Great tit Chicken Adelie penguin 



Research in stress endocrinology described here has been supported by the Institute of Veterinary, Animal and Biomedical Sciences, Massey University, and by Antarctica New Zealand.


  1. Benus RF, Bohus B, Koolhaas JM, Van Oortmerssen GA (1991) Heritable variation for aggression as a reflection of individual coping strategies. Experientia 47:1008–1019PubMedCrossRefGoogle Scholar
  2. Beuving G, Jones RB, Blokhuis HJ (1989) Adrenocortical and heterophil lymphocyte responses to challenge in hens showing short or long tonic immobility reactions. Br Poult Sci 30:175–184PubMedCrossRefGoogle Scholar
  3. Beuving G, Vonder GMA (1986) Comparison of the adrenal sensitivity to ACTH of laying hens with immobilization and plasma baseline levels of corticosterone. Gen Comp Endocrinol 62:353–358PubMedCrossRefGoogle Scholar
  4. Boissy A (1995) Fear and fearfulness in animals. Quarterly Rev Biol 70:165–191CrossRefGoogle Scholar
  5. Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28PubMedCrossRefGoogle Scholar
  6. Cameron NM, Champagne FA, Fish Cpew Ozaki-Kuroda K, Meaney MJ (2005) The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci Biobehav Rev 29:843–865PubMedCrossRefGoogle Scholar
  7. Carere C, Drent PJ, Privitera L, Koolhaas JM, Groothuis TGG (2005) Personalities in great tits, Parus major: stability and consistency. Anim Behav 70:795–805CrossRefGoogle Scholar
  8. Carere C, Eens M (2005) Unravelling animal personalities: how and why individuals consistently differ. Behaviour 142:1149–1157CrossRefGoogle Scholar
  9. Carere C, Groothuis TGG, Mostl E, Daan S, Koolhaas JM (2003) Fecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress. Horm Behav 43:540–548PubMedCrossRefGoogle Scholar
  10. Carsia RV, Harvey S (2000) Adrenals. In: Whittow GC (Ed) Sturkie’s avian physiology, 5th edn. Academic, San Diego, CA, pp 489–537Google Scholar
  11. Cockrem JF (2005) Conservation and behavioral neuroendocrinology. Horm Behav 48:492–501PubMedCrossRefGoogle Scholar
  12. Cockrem JF (2007) Stress endocrinology and conservation. In: Maitra S (Ed) Hormone biotechnology. Daya, Delhi, India, pp 346–353Google Scholar
  13. Cockrem JF, Adams DC, Bennett EJ, Candy EJ, Henare SJ, Hawke EJ, Potter MA (2004) Endocrinology and the conservation of New Zealand birds. In: Gordon MS, Bartol SM (Ed) Experimental approaches to conservation biology. University of California Press, Los Angeles, CA, pp 101–121Google Scholar
  14. Cockrem JF, Silverin B (2002a) Variation within and between birds in corticosterone responses of great tits (Parus major). Gen Comp Endocrinol 125:197–206PubMedCrossRefGoogle Scholar
  15. Cockrem JF, Silverin B (2002b) Sight of a predator can stimulate a corticosterone response in the great tit (Parus major). Gen Comp Endocrinol 125:248–255PubMedCrossRefGoogle Scholar
  16. Creel S (2001) Social dominance and stress hormones. Trends Ecol Evol 16:491–497CrossRefGoogle Scholar
  17. Dawson A, Howe PD (1983) Plasma corticosterone in wild starlings (Sturnus vulgaris) immediately following capture and in relation to body weight during the annual cycle. Gen Comp Endocrinol 51:303–308PubMedCrossRefGoogle Scholar
  18. Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc Lond Ser B Biol Sci 271:847–852Google Scholar
  19. Dingemanse NJ, Both C, Van Noordwijk AJ, Rutten AL, Drent PJ (2003) Natal dispersal and personalities in great tits (Parus major). Proc R Soc Lond Ser B Biol Sci 270:741–747Google Scholar
  20. Dingemanse NJ, De Goede P (2004) The relation between dominance and exploratory behavior is context-dependent in wild great tits. Behav Ecol 15:1023–1030CrossRefGoogle Scholar
  21. Dingemanse NJ, Reale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184CrossRefGoogle Scholar
  22. Dufty AM Jr, Clobert J, Møller AP (2002) Hormones, developmental plasticity and adaptation. Trends Ecol Evol 17:190–196CrossRefGoogle Scholar
  23. Ellis BJ, Jackson JJ, Boyce WT (2006) The stress response systems: universality and adaptive individual differences. Develop Rev 26:175–212CrossRefGoogle Scholar
  24. Fraisse F, Cockrem JF (2006) Corticosterone and the measurement of stress and fear in cage housed laying chickens. Br Poultry Sci 47:1–10CrossRefGoogle Scholar
  25. Gallup GC (1977) Tonic immobility: the role of fear and predation. Psychol Rec 27:41–61Google Scholar
  26. Groothuis TGG, Carere C (2005) Avian personalities: characterization and epigenesis. Neurosci Biobehav Rev 29:137–150PubMedCrossRefGoogle Scholar
  27. Guimont FS, Wynne-Edwards KE (2006) Individual variation in cortisol responses to acute ‘on-back’ restraint in an outbred hamster. Horm Behav 50:252–260PubMedCrossRefGoogle Scholar
  28. Hayward LS, Wingfield JC (2004) Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen Comp Endocrinol 135:365–371PubMedCrossRefGoogle Scholar
  29. Hazard D, Couty M, Faure JM, Guemene D (2005) Daily and photoperiod variations of hypothalamic-pituitary-adrenal axis responsiveness in Japanese quail selected for short or long tonic immobility. Poult Sci 84:1920–1925PubMedGoogle Scholar
  30. Jones RB (1986) The tonic immobility of the domestic fowl: a review. World’s Poult Sci 42:82–96CrossRefGoogle Scholar
  31. Jones RB (1988) Repeatability of fear ranks among adult laying hens. Appl Anim Behav Sci. 19:297–304CrossRefGoogle Scholar
  32. Jones RB (1996) Fear and adaptability in poultry: insights, implications and imperatives. World’s Poultry Sci J 52:131–174CrossRefGoogle Scholar
  33. Jones RB, Beuving G, Blokhuis HJ (1988) Tonic immobility and heterophil/lymphocyte responses of the domestic fowl to corticosterone infusion. Physiol Behav 42:249–253PubMedCrossRefGoogle Scholar
  34. Jones RB, Blokhuis HJ, Beuving G (1995) Open field and tonic immobility responses in domestic chicks of 2 genetic lines differing in their propensity to feather peck. Br Poult Sci 36:525–530PubMedCrossRefGoogle Scholar
  35. Jones RB, Marin RH, Satterlee DG, Cadd GG (2002) Sociality in Japanese quail (Coturnix japonica) genetically selected for contrasting adrenocortical responsiveness. Appl Anim Behav Sci 75:337–346CrossRefGoogle Scholar
  36. Jones RB, Mills AD (1983) Estimation of fear in two lines of the domestic chick: correlations between various methods. Behav Process 8:243–253CrossRefGoogle Scholar
  37. Jones RB, Mills AD, Faure JM (1991) Genetic and experiential manipulation of fear-related behaviour in Japanese quail chicks (Coturnix coturnix japonica). J Comp Psychol 105:15–24PubMedCrossRefGoogle Scholar
  38. Jones RB, Satterlee DG, Ryder FH (1992) Open-field behaviour of Japanese quail chicks genetically selected for low or high plasma corticosterone response to immobilization stress. Poult Sci 71:1403–1407PubMedGoogle Scholar
  39. Jones RB, Mills AD, Faure JM, Williams JB (1994a) Restraint, fear, and distress in Japanese quail genetically selected for long or short tonic immobility reactions. Physiol Behav 56:529–534PubMedCrossRefGoogle Scholar
  40. Jones RB, Satterlee DG, Ryder FH (1994b) Fear of humans in Japanese quail selected for low or high adrenocortical response. Physiol Behav 56:379–383PubMedCrossRefGoogle Scholar
  41. Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935PubMedCrossRefGoogle Scholar
  42. Korte SM, Beuving G, Ruesink W, Blokhuis HJ (1997) Plasma catecholamine and corticosterone levels during manual restraint in chicks from a high and low feather pecking line of laying hens. Physiol Behav 62:437–441PubMedCrossRefGoogle Scholar
  43. Korte SM, Koolhaas JM, Wingfield JC, Mc Ewen BS (2005) The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neurosci Biobehav Rev 29:3–38PubMedCrossRefGoogle Scholar
  44. Kralj-Fiser S, Scheiber IBR, Blejec A, Moestl E, Kotrschal K (2007) Individualities in a flock of free-roaming greylag geese: behavioral and physiological consistency over time and across situations. Horm Behav 51:239–248PubMedCrossRefGoogle Scholar
  45. Labar KS, LeDoux JE (2001) Coping with danger: the neural basis of defensive behavior and fearful feelings. In: McEwen BS (Ed) Handbook of physiology (vol IV: Coping with the environment: neural and endocrine mechanisms). Oxford University Press, Oxford, Sect 7, pp 139–154Google Scholar
  46. LeDoux J (1996) The emotional brain. Simon & Schuster, New YorkGoogle Scholar
  47. Levine S (1971) Stress and behavior. Sci Am 224:26–31PubMedCrossRefGoogle Scholar
  48. Littin KE, Cockrem JF (2001) Individual variation in corticosterone secretion in laying hens. Br Poult Sci 42:536–546PubMedCrossRefGoogle Scholar
  49. Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O (2003) Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev 27:119–127PubMedCrossRefGoogle Scholar
  50. Marin RH, Satterlee DG, Cadd GG, Jones RB (2002) T-maze behavior and early egg production in Japanese quail selected for contrasting adrenocortical responsiveness. Poult Sci 81:981–986PubMedGoogle Scholar
  51. Meaney MJ (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161–1192PubMedCrossRefGoogle Scholar
  52. Mignon-Grasteau S, Roussot O, Delaby C, Faure JM, Mills A, Leterrier C, Guemene D, Constantin P, Mills M, Lepape G, Beaumont C (2003) Factorial correspondence analysis of fear-related behaviour traits in Japanese quail. Behav Process 61:69–75CrossRefGoogle Scholar
  53. Miller KA, Garner JP, Mench JA (2006) Is fearfulness a trait that can be measured with behavioural tests? A validation of four fear tests for Japanese quail. Anim Behav 71:1323–1334CrossRefGoogle Scholar
  54. Murphy LB (1978) Practical problems of recognizing and measuring fear and exploration behavior in domestic fowl. Anim Behav 26:422–431CrossRefGoogle Scholar
  55. Odeh FM, Cadd GG, Satterlee DG (2003) Genetic characterization of stress responsiveness in Japanese quail. 2. Analyses of maternal effects, additive sex linkage effects, heterosis, and heritability by diallel crosses. Poult Sci 82:31–35PubMedGoogle Scholar
  56. Postma E, Van Noordwijk AJ (2005) Genetic variation for clutch size in natural populations of birds from a reaction norm perspective. Ecology 86:2344–2357CrossRefGoogle Scholar
  57. Pravosudov VV, Kitaysky AS (2006) Effects of nutritional restrictions during post-hatching development on adrenocortical function in western scrub-jays (Aphelocoma californica). Gen Comp Endocrinol 145:25–31PubMedCrossRefGoogle Scholar
  58. Ratner SC (1967) Comparative aspects of hypnosis. In: Gordon JE (ed) Handbook of clinical and experimental hypnosis. Macmillan, New York, pp 550–587Google Scholar
  59. Reale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318PubMedCrossRefGoogle Scholar
  60. Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24PubMedCrossRefGoogle Scholar
  61. Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Physiol A Mol Integr Physiol 140:73–79Google Scholar
  62. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89PubMedCrossRefGoogle Scholar
  63. Satterlee DG, Johnson WA (1985) Metabolic traits in Japanese quail selected for high or low corticosterone response to stress. Poult Sci 64(Suppl 1):176Google Scholar
  64. Satterlee DG, Johnson WA (1988) Selection of Japanese quail for contrasting blood corticosterone response to immobilization. Poult Sci 67:25–32PubMedGoogle Scholar
  65. Satterlee DG, Jones RB, Ryder FH (1993) Short-latency stressor effects on tonic immobility fear reactions of Japanese quail divergently selected for adrenocortical responsiveness to immobilization. Poult Sci 72:1132–1136PubMedGoogle Scholar
  66. Satterlee DG, Marin RH, Jones RB (2002) Selection of Japanese quail for reduced adrenocortical responsiveness accelerates puberty in males. Poult Sci 81:1071–1076PubMedGoogle Scholar
  67. Schlichting CD (1989) Phenotypic integration and environmental change: what are the consequences of differential phenotypic plasticity of traits? Bioscience 39:460–464CrossRefGoogle Scholar
  68. Selye H (1974) Stress without distress. JB Lippincott, Philadelphia, PAGoogle Scholar
  69. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378PubMedCrossRefGoogle Scholar
  70. Silverin B (1997) The stress response and autumn dispersal behaviour in willow tits. Anim Behav 53:451–459CrossRefGoogle Scholar
  71. Silverin B (1998) Stress responses in birds. Poult Avian Biol Rev 9:153–168Google Scholar
  72. Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc Lond Ser B Biol Sci 272:2627–2634Google Scholar
  73. Steimer T, Driscoll P (2005) Inter-individual vs line/strain differences in psychogenetically selected Roman High-(RHA) and Low-(RLA) Avoidance rats: neuroendocrine and behavioural aspects. Neurosci Biobehav Rev 29:99–112PubMedCrossRefGoogle Scholar
  74. Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116CrossRefGoogle Scholar
  75. Van Noordwijk AJ (1989) Reaction norms in genetic ecology: studies of the great tit exemplify the combination of ecophysiology and quantitative genetics. Bioscience 39:453–458CrossRefGoogle Scholar
  76. Veenema AH, Meijer OC, De Kloet ER, Koolhaas JM (2003) Genetic selection for coping style predicts stressor susceptibility. J Neuroendocrinol 15:256–267PubMedCrossRefGoogle Scholar
  77. Wilson DS (1998) Adaptive individual differences within single populations. Philos Trans Roy Soc Lond B 353:199–205CrossRefGoogle Scholar
  78. Wingfield JC, O’Reilly KM, Astheimer LB (1995) Modulation of the adrenocortical response to acute stress in Arctic birds: a possible ecological basis. Am Zool 35:285–294Google Scholar
  79. Wingfield JC, Vleck CM, Moore MC (1992) Seasonal changes of the adrenocortical response to stress in birds of the Sonoran desert. J Exp Zool 264:419–428PubMedCrossRefGoogle Scholar
  80. Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584PubMedCrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2007

Authors and Affiliations

  1. 1.Institute of Veterinary, Animal and Biomedical SciencesMassey UniversityPalmerston NorthNew Zealand

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