Sex differences in the long-term repeatability of the acute stress response in long-lived, free-living Florida scrub-jays (Aphelocoma coerulescens)

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 185, Issue 1, 2015, Pages 119-133

  Small, Thomas W ^a   Schoech, Stephan J ^a  

^a University of Memphis   (United States)

Author keywords

Florida scrub jay; Glucocorticoids; Personality; Plasticity; Repeatability; Stress response

Indexed keywords

CORTICOSTERONE; HYDROCORTISONE;

AGE; ANIMAL; BLOOD; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; LONGITUDINAL STUDY; MALE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RADIOIMMUNOASSAY; SEXUAL DEVELOPMENT; SONGBIRD; UNITED STATES;

AGE FACTORS; ANIMALS; CORTICOSTERONE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLORIDA; HYDROCORTISONE; LONGITUDINAL STUDIES; MALE; PASSERIFORMES; RADIOIMMUNOASSAY; SEX CHARACTERISTICS; STRESS, PHYSIOLOGICAL;

EID: 84945283738     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-014-0866-4     Document Type: Article

References (123)

1. Almasi B, Roulin A, Jenni-Eiermann S, Breuner CW, Jenni L (2009) Regulation of free corticosterone and CBG capacity under different environmental conditions in altricial nestlings. Gen Comp Endocrinol 164:117–124
2. Angelier F, Chastel O (2009) Stress, prolactin and parental investment in birds: a review. Gen Comp Endocrinol 163:142–148
3. Angelier F, Holberton RL, Marra PP (2009) Does stress response predict return rate in a migratory bird species? A study of American redstarts and their non-breeding habitat. Proc R Soc B 276:3545–3551
4. 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
5. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manage 74:1175–1178
6. Bauer CM, Skaff NK, Bernard AB, Trevino JM, Ho JM, Romero LM, Ebensperger LA, Hayes LD (2013) Habitat type influences endocrine stress response in the degu (Octodon degus). Gen Comp Endocrinol 186:136–144
7. Baugh AT, Schaper SV, Hau M, Cockrem JF, de Goede P, van Oers K (2012) Corticosterone responses differ between lines of great tits (Parus major) selected for divergent personalities. Gen Comp Endocrinol 175:488–494
8. Baugh AT, van Oers K, Naguib M, Hau M (2013) Initial reactivity and magnitude of the acute stress response associated with personality in wild great tits (Parus major). Gen Comp Endocrinol 189:96–104
9. Bebus SE, Small TW, Elderbrock EK, Heiss RS, Schoech SJ (2012) Corticosterone responsiveness at nutritional independence predicts behavior nine months later in the Florida scrub-yay (Aphelocoma coerulescens). Integr Comp Biol 52:E11
10. Blas J, Bortolotti GR, Tella JL, Baos R, Marchant TA (2007) Stress response during development predicts fitness in a wild, long lived vertebrate. Proc Natl Acad Sci U S A 104:8880–8884
11. Bonier F, Martin PR, Moore IT, Wingfield JC (2009) Do baseline glucocorticoids predict fitness? Trends Ecol Evol 24:634–642
12. Boonstra R (2005) Equipped for life: The adaptive role of the stress axis in male mammals. J Mammal 86:236–247
13. Bouwhuis S, Quinn JL, Sheldon BC, Verhulst S (2014) Personality and basal metabolic rate in a wild bird population. Oikos 123:56–62
14. Breininger DR (1999) Florida Scrub-Jay demography and dispersal in a fragmented landscape. Auk 116:520–527
15. Breininger DR, Nichols JD, Carter GM, Oddy DM (2009) Habitat-specific breeder survival of Florida Scrub-Jays: inferences from multistate models. Ecology 90:3180–3189
16. Breuner CW, Hahn TP (2003) Integrating stress physiology, environmental change, and behavior in free-living sparrows. Horm Behav 43:115–123
17. Breuner CW, Orchinik M (2001) Seasonal regulation of membrane and intracellular corticosteroid receptors in the house sparrow brain. J Neuroendocrinol 13:412–420
18. Breuner CW, Wingfield JC, Romero LM (1999) Diel rhythms of basal and stress-induced corticosterone in a wild, seasonal vertebrate, Gambel’s white-crowned sparrow. J Exp Zool 284:334–342
19. Breuner CW, Orchinik M, Hahn TP, Meddle SL, Moore IT, Owen-Ashley NT, Sperry TS, Wingfield JC (2003) Differential mechanisms for regulation of the stress response across latitudinal gradients. Am J Physiol Regul Integr Comp Physiol 285:R594–R600
20. Breuner CW, Patterson SH, Hahn TP (2008) In search of relationships between the acute adrenocortical response and fitness. Gen Comp Endocrinol 157:288–295
21. Careau V, Garland T (2012) Performance, personality, and energetics: correlation, causation, and mechanism. Physiol Biochem Zool 85:543–571
22. Careau V, Réale D, Humphries MM, Thomas DW (2010) The pace of life under artificial selection: personality, energy expenditure, and longevity are correlated in domestic dogs. Am Nat 175:753–758
23. Cavigelli SA, McClintock MK (2003) Fear of novelty in infant rats predicts adult corticosterone dynamics and an early death. Proc Natl Acad Sci U S A 100:16131–16136
24. Claessens SEF, Daskalakis NP, van der Veen R, Oitzl MS, de Kloet ER, Champagne DL (2011) Development of individual differences in stress responsiveness: an overview of factors mediating the outcome of early life experiences. Psychopharmacology 214:141–154
25. Clinchy M, Sheriff MJ, Zanette LY (2013) Predator-induced stress and the ecology of fear. Funct Ecol 27:56–65
26. Cockrem JF (2013a) Individual variation in glucocorticoid stress responses in animals. Gen Comp Endocrinol 181:45–58
27. Cockrem JF (2013b) Corticosterone responses and personality in birds: Individual variation and the ability to cope with environmental changes due to climate change. Gen Comp Endocrinol 190:156–163
28. Cockrem JF, Silverin B (2002) Variation within and between birds in corticosterone responses of great tits (Parus major). Gen Comp Endocrinol 125:197–206
29. Cockrem JF, Barrett DP, Candy EJ, Potter MA (2009) Corticosterone responses in birds: individual variation and repeatability in Adelie penguins (Pygoscelisadeliae) and other species, and the use of power analysis to determine sample sizes. Gen Comp Endocrinol 163:158–168
30. Cook KV, McConnachie SH, Gilmour KM, Hinch SG, Cooke SJ (2011a) Fitness and behavioral correlates of pre-stress and stress-induced plasma cortisol titers in pink salmon (Oncorhynchus gorbuscha) upon arrival at spawning grounds. Horm Behav 60:489–497
31. Cook KV, O’Connor CM, Gilmour KM, Cooke SJ (2011b) The glucocorticoid stress response is repeatable between years in a wild teleost fish. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 197:1189–1196
32. Cook KV, O’Connor CM, McConnachie SH, Gilmour KM, Cooke SJ (2012) Condition dependent intra-individual repeatability of stress-induced cortisol in a freshwater fish. Comp Biochem Physiol A: Mol Integr Physiol 161:337–343
33. Creel S, Dantzer B, Goymann W, Rubenstein DR (2013) The ecology of stress: effects of the social environment. Funct Ecol 27:66–80
34. Crossin GT, 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
35. Del Giudice M, Hinnant JB, Ellis BJ, El-Sheikh M (2012) Adaptive patterns of stress responsivity: a preliminary investigation. Dev Psychol 48:775–790
36. Dingemanse NJ, Réale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184
37. Dingemanse NJ, Edelaar P, Kempenaers B (2010) Why is there variation in baseline glucocorticoid levels? Trends Ecol Evol 25:261–262
38. Fleshner M, Deak T, Spencer RL, Laudenslager ML, Watkins LR, Maier SF (1995) A long-term increase in basal levels of corticosterone and a decrease in corticosteroid-binding globulin after acute stressor exposure. Endocrinology 136:5336–5342
39. Fokidis HB, Orchinik M, Deviche P (2009) Corticosterone and corticosteroid binding globulin in birds: relation to urbanization in a desert city. Gen Comp Endocrinol 160:259–270
40. Furlonger AA, Huynh L, Luloff TW, Schmidt KL, MacDougall-Shackleton SA (2012) Effects of supplementation with preferred foods on the reproductive axis of American Goldfinches (Spinus tristis). Can J Zool 90:203–209
41. Garvin MC, Tarvin KA, Stark LM, Woolfenden GE, Fitzpatrick JW, Day JF (2004) Arboviral infection in two species of wild jays (Aves: Corvidae): evidence for population impacts. J Med Entomol 41:215–225
42. Hau M, Ricklefs RE, Wikelski M, Lee KA, Brawn JD (2010) Corticosterone, testosterone and life-history strategies of birds. Proc R Soc B 277:3203–3212
43. Heidinger BJ, Chastel O, Nisbet ICT, Ketterson ED (2010) Mellowing with age: older parents are less responsive to a stressor in a long-lived seabird. Funct Ecol 24:1037–1044
44. Holberton RL, Wingfield JC (2003) Modulating the corticosterone stress response: a mechanism for balancing individual risk and reproductive success in arctic-breeding sparrows? Auk 120:1140–1150
45. Hruschka DJ, Kohrt BA, Worthman CM (2005) Estimating between- and within-individual variation in cortisol levels using multilevel models. Psychoneuroendocrinology 30:698–714
46. Husak JF, Moore IT (2008) Stress hormones and mate choice. Trends Ecol Evol 23:532–534
47. Jones BC, Bebus SE, Small TW, Bateman PW, Schoech SJ (2013) Corticosterone responsiveness and behavioral phenotype reveal learned antipredator behavior is sex specific in Florida scrub-jays (Aphelocoma coerulescens). Integr Comp Biol 53:E104
48. Klukowski M (2011) Effects of breeding season, testosterone and ACTH on the corticosterone response of free-ranging male fence lizards (Sceloporus undulatus). Gen Comp Endocrinol 173:295–302
49. Klukowski LA, Cawthorn JM, Ketterson ED, Nolan Jr V (1997) Effects of experimentally elevated testosterone on plasma corticosterone and corticosteroid-binding globulin in dark-eyed juncos (Junco hyemalis). Gen Comp Endocrinol 108:141–151
50. Knol MJ, Pestman WR, Grobbee DE (2011) The (mis)use of overlap of confidence intervals to assess effect modification. Eur J Epidemiol 26:253–254
51. Koolhaas JM (2008) Coping style and immunity in animals: making sense of individual variation. Brain Behav Immun 22:662–667
52. Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MA, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935
53. La Fleur SE (2006) The effects of glucocorticoids on feeding behavior in rats. Physiol Behav 89:110–114
54. 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
55. Landys MM, Goymann W, Schwabl I, Trapschuh M, Slagsvold T (2010) Impact of season and social challenge on testosterone and corticosterone levels in a year-round territorial bird. Horm Behav 58:317–325
56. Lattin CR, Romero LM (2013) Seasonal variation in corticosterone receptor binding in brain, hippocampus, and gonads in House Sparrows (Passer domesticus). Auk 130:591–598
57. Lattin CR, Bauer CM, de Bruijn R, Romero LM (2012) Hypothalamus-pituitary-adrenal axis activity and the subsequent response to chronic stress differ depending upon life history stage. Gen Comp Endocrinol 178:494–501
58. Lema S, Kitano J (2013) Hormones and phenotypic plasticity: Implications for the evolution of integrated adaptive phenotypes. Curr Zool 59:506–525
59. Lendvai AZ, Giraudeau M, Chastel O (2007) Reproduction and modulation of the stress response: an experimental test in the house sparrow. Proc R Soc B 274:391–397
60. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121
61. Li D, Wu J, Zhang X, Ma X, Wingfield JC, Lei F, Wang G, Wu Y (2011) Comparison of adrenocortical responses to acute stress in lowland and highland Eurasian tree sparrows (Passer montanus): similar patterns during the breeding, but different during the prebasic molt. J Exp Zool A Ecol Genet Physiol 315:512–519
62. Littin KE, Cockrem JF (2001) Individual variation in corticosterone secretion in laying hens. Br Poult Sci 42:536–546
63. Lo MJ, Kau MM, Cho WL, Wang PS (2000) Aging effects on the secretion of corticosterone in male rats. J Investig Med 48:335–342
64. Lo MJ, Kau MM, Wang PS (2006) Effect of aging on corticosterone secretion in diestrous rats. J Cell Biochem 97:351–358
65. Love OP, Breuner CW, Vézina F, Williams TD (2004) Mediation of a corticosterone-induced reproductive conflict. Horm Behav 46:59–65
66. Lynn SE, Prince LE, Phillips MM (2010) A single exposure to an acute stressor has lasting consequences for the hypothalamo-pituitary-adrenal response to stress in free-living birds. Gen Comp Endocrinol 165:337–344
67. MacDougall-Shackleton SA, Schmidt KL, Furlonger AA, MacDougall-Shackleton EA (2013) HPA axis regulation, survival, and reproduction in free-living sparrows: Functional relationships or developmental correlations? Gen Comp Endocrinol 190:188–193
68. Maher C, Lott D (2000) A review of ecological determinants of territoriality within vertebrate species. Am Midl Nat 143:1–29
69. Malisch JL, Satterlee DG, Cockrem JF, Wada H, Breuner CW (2010) How acute is the acute stress response? Baseline corticosterone and corticosteroid-binding globulin levels change 24 h after an acute stressor in Japanese quail. Gen Comp Endocrinol 165:345–350
70. Martin LB (2009) Stress and immunity in wild vertebrates: timing is everything. Gen Comp Endocrinol 163:70–76
71. Martins TLF, Roberts ML, Giblin I, Huxham R, Evans MR (2007) Speed of exploration and risk-taking behavior are linked to corticosterone titres in zebra finches. Horm Behav 52:445–453
72. Miles DB, Calsbeek R, Sinervo B (2007) Corticosterone, locomotor performance, and metabolism in side-blotched lizards (Uta stansburiana). Horm Behav 51:548–554
73. Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc Lond B Biol Sci 363:1635–1645
74. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev Camb Philos Soc 85:935–956
75. Narayan EJ, Cockrem JF, Hero JM (2013) Repeatability of baseline corticosterone and short-term corticosterone stress responses, and their correlation with testosterone and body condition in a terrestrial breeding anuran (Platymantis vitiana). Comp Biochem Physiol A: Mol Integr Physiol 165:304–312
76. Orchinik M, Murray T, Moore F (1991) A corticosteroid receptor in neuronal membranes. Science 252:1848–1851
77. Ouyang JQ, Hau M, Bonier F (2011) Within seasons and among years: When are corticosterone levels repeatable? Horm Behav 60:559–564
78. Palacios MG, Sparkman AM, Bronikowski AM (2012) Corticosterone and pace of life in two life-history ecotypes of the garter snake Thamnophis elegans. Gen Comp Endocrinol 175:443–448
79. Patterson SH, Hahn TP, Cornelius JM, Breuner CW (2014) Natural selection and glucocorticoid physiology. J Evol Biol 27:259–274
80. Payton ME, Greenstone MH, Schenker N (2003) Overlapping confidence intervals or standard error intervals: what do they mean in terms of statistical significance? J Insect Sci 3:34
81. Pitk M, Tilgar V, Kilgas P, Mänd R (2012) Acute stress affects the corticosterone level in bird eggs: a case study with great tits (Parus major). Horm Behav 62:475–479
82. Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio P-O (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos Trans R Soc Lond B Biol Sci 365:4051–4063
83. Rensel MA, Schoech SJ (2011) Repeatability of baseline and stress-induced corticosterone levels across early life stages in the Florida scrub-jay (Aphelocoma coerulescens). Horm Behav 59:497–502
84. Rensel MA, Boughton RK, Schoech SJ (2010) Development of the adrenal stress response in the Florida scrub-jay (Aphelocoma coerulescens). Gen Comp Endocrinol 165:255–261
85. Rensel MA, Comito D, Kosarussavadi S, Schlinger BA (2014) Region-specific neural corticosterone patterns differ from plasma in a male songbird. Endocrinology 155:3572–3581
86. Reul JM, van den Bosch FR, de Kloet ER (1987) Relative occupation of type-I and type-II corticosteroid receptors in rat brain following stress and dexamethasone treatment: functional implications. J Endocrinol 115:459–467
87. Richards SA, Whittingham MJ, Stephens PA (2010) Model selection and model averaging in behavioural ecology: the utility of the IT-AIC framework. Behav Ecol Sociobiol 65:77–89
88. Rodríguez-Prieto I, Martín J, Fernández-Juricic E (2010) Habituation to low-risk predators improves body condition in lizards. Behav Ecol Sociobiol 64:1937–1945
89. Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24
90. 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 140:73–79
91. Romero LM, Reed JM (2008) Repeatability of baseline corticosterone concentrations. Gen Comp Endocrinol 156:27–33
92. Ruiz M, French SS, Demas GE, Martins EP (2010) Food supplementation and testosterone interact to influence reproductive behavior and immune function in Sceloporus graciosus. Horm Behav 57:134–139
93. Saino N, Romano M, Ferrari RP, Martinelli R, Møller AP (2005) Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring. J Exp Zool A Comp Exp Biol 303:998–1006
94. 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
95. Schoech SJ, Mumme R, Moore M (1991) Reproductive endocrinology and mechanisms of breeding inhibition in cooperatively breeding Florida scrub jays (Aphelocoma c. coerulescens). Condor 93:354–364
96. Schoech SJ, Ketterson ED, Nolan V (1999) Exogenous testosterone and the adrenocortical response in dark-eyed juncos. Auk 116:64–72
97. Schoech SJ, Bowman R, Reynolds SJ (2004) Food supplementation and possible mechanisms underlying early breeding in the Florida Scrub-Jay (Aphelocoma coerulescens). Horm Behav 46:565–573
98. Schoech SJ, Bowman R, Bridge ES, Boughton RK (2007) Baseline and acute levels of corticosterone in Florida Scrub-Jays (Aphelocoma coerulescens): effects of food supplementation, suburban habitat, and year. Gen Comp Endocrinol 154:150–160
99. Schoech SJ, Rensel MA, Bridge ES, Boughton RK, Wilcoxen TE (2009) Environment, glucocorticoids, and the timing of reproduction. Gen Comp Endocrinol 163:201–207
100. Schoech SJ, Rensel MA, Heiss RS (2011) Short- and long-term effects of developmental corticosterone exposure on avian physiology, behavioral phenotype, cognition, and fitness: A review. Curr Zool 57:514–530
101. Schoech SJ, Rensel MA, Wilcoxen TE (2012) Here today, not gone tomorrow: long-term effects of corticosterone. J Ornithol 153:217–226
102. Sih A (2011) Effects of early stress on behavioral syndromes: an integrated adaptive perspective. Neurosci Biobehav Rev 35:1452–1465
103. Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289
104. Smith BR, Blumstein DT (2007) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455
105. Stöwe M, Rosivall B, Drent PJ, Möstl E (2010) Selection for fast and slow exploration affects baseline and stress-induced corticosterone excretion in Great tit nestlings, Parus major. Horm Behav 58:864–871
106. Stranahan AM, Lee K, Mattson MP (2008) Central mechanisms of HPA axis regulation by voluntary exercise. Neuromolecular Med 10:118–127
107. Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21
108. Tarlow EM, Hau M, Anderson DJ, Wikelski M (2003) Diel changes in plasma melatonin and corticosterone concentrations in tropical Nazca boobies (Sula granti) in relation to moon phase and age. Gen Comp Endocrinol 133:297–304
109. Thaker M, Vanak AT, Lima SL, Hews DK (2010) Stress and aversive learning in a wild vertebrate: the role of corticosterone in mediating escape from a novel stressor. Am Nat 175:50–60
110. 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 141:451–467
111. Vitousek MN, Romero LM (2013) Stress responsiveness predicts individual variation in mate selectivity. Gen Comp Endocrinol 187:32–38
112. Wada H, Salvante KG, Stables C, Wagner E, Williams TD, Breuner CW (2008) Adrenocortical responses in zebra finches (Taeniopygia guttata): individual variation, repeatability, and relationship to phenotypic quality. Horm Behav 53:472–480
113. Wilcoxen TE, Boughton RK, Schoech SJ (2010) Selection on innate immunity and body condition in Florida scrub-jays throughout an epidemic. Biol Lett 6:552–554
114. Wilcoxen TE, Boughton RK, Bridge ES, Rensel MA, Schoech SJ, Reynolds SJ (2011) Age-related differences in baseline and stress-induced corticosterone in Florida scrub-jays. Gen Comp Endocrinol 173:461–466
115. Wingfield JC (2005) The concept of allostasis: coping with a capricious environment. J Mammal 86:248–254
116. Wingfield JC, Hunt KE (2002) Arctic spring: hormone-behavior interactions in a severe environment. Comp Biochem Physiol Part B Biochem Mol Biol 132:275–286
117. Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711–724
118. Wingfield JC, Vleck CM, Moore MC (1992) Seasonal changes of the adrenocortical response to stress in birds of the Sonoran Desert. J Exp Zool 264:419–428
119. Wingfield JC, O’Reilly KM, Astheimer LB (1995) Modulation of the adrenocortical responses to acute stress in arctic birds: a possible ecological basis. Am Zool 35:285–294
120. 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”. Integr Comp Biol 38:191–206
121. Woolfenden GE, Fitzpatrick JW (1984) The Florida scrub-jay: demography of a cooperative-breeding bird. Princeton University Press, Princeton
122. Woolfenden GE, Fitzpatrick JW (1990) Florida scrub jays: a synopsis after 18 years of study. In: Stacy PB, Koenig WD (eds) Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge University Press, pp 241–266
123. Zimmer C, Boogert NJ, Spencer KA (2013) Developmental programming: Cumulative effects of increased pre-hatching corticosterone levels and post-hatching unpredictable food availability on physiology and behaviour in adulthood. Horm Behav 64:494–500