Individual variation in corticosterone and personality traits in the blue tit Cyanistes caeruleus

in Behaviour
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

Variation in personality traits is predicted to reflect physiology, but the extent to which variations in stress hormones derive from differences in personality and/or state-dependent factors remains unclear. To investigate this, wild blue tits (Cyanistes caeruleus) were briefly brought into captivity and scored for personality and corticosterone (Cort) concentrations. More active females had lower baseline Cort than less active individuals. Exploratory tendency and neophobia did not co-vary with baseline Cort. Stress-induced Cort concentrations were correlated negatively with exploratory tendency and haematocrit, but positively with mass gain in captivity. Therefore, baseline and stress-induced Cort concentrations in wintering blue tits were associated with state-dependent variables, sex, age and personality traits. Key to interpreting the physiology of personality traits seems to be their interactions with other traits that mediate ability to utilise resources, and thus influence an individual’s perception of its current and future energy balance.

Individual variation in corticosterone and personality traits in the blue tit Cyanistes caeruleus

in Behaviour

Sections

References

AngelierF.WingfieldJ.C.WeimerskirchH.ChastelO. (2010). Hormonal correlates of individual quality in a long-lived bird: a test of the ‘corticosterone-fitness hypothesis’. — Biol. Lett. 6: 846-849.

ApfelbeckB.RaessM. (2008). Behavioural and hormonal effects of social isolation and neophobia in a gregarious bird species, the European starling (Sturnus vulgaris). — Horm. Behav. 54: 435-441.

ArnoldK.E.RamsayS.L.GouldC.AdamA. (2007). Parental prey selection affects risk taking behaviour and spatial learning in avian offspring. — Proc. Roy. Soc. Lond. B: Biol. Sci. 274: 2563-2569.

ArnoldK.E.HerbornK.A.AdamA.AlexanderL. (2015). Individual variation in the oxidative costs of personality traits. — Funct. Ecol. 29: 522-530.

AstheimerL.B.ButtemerW.A.WingfieldJ.C. (1995). Seasonal and acute changes in adrenocortical responsiveness in an Arctic breeding bird. — Horm. Behav. 29: 442-457.

BellA.M. (2005). Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). — J. Evol. Biol. 18: 464-473.

BellA.M.SihA. (2007). Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). — Ecol. Lett. 10: 828-834.

BlasJ.BortolottiG.R.TellaJ.L.BaosR.MarchantT.A. (2007). Stress response during development predicts fitness in a wild, long lived vertebrate. — Proc. Natl. Acad. Sci. USA 104: 8880-8884.

BokonyV.LendvaiA.Z.LikerA.AngelierF.WingfieldJ.C.ChastelO. (2009). Stress response and the value of reproduction: are birds prudent parents?Am. Nat. 173: 589-598.

BonierF.MartinP.R.MooreI.T.WingfieldJ.C. (2009). Do baseline glucocorticoids predict fitness?Trends Ecol. Evol. 24: 634-642.

BothC.DingemanseN.J.DrentP.J.TinbergenJ.M. (2005). Pairs of extreme avian personalities have highest reproductive success. — J. Anim. Ecol. 74: 667-674.

BreunerC.W.GreenfieldA.L.WingfieldC.J. (1998). Noninvasive corticosterone treatment rapidly increases activity in Gambel’s white-crowned sparrows (Zonotrichia leucophrys gambelii). — Gen. Comp. Endocrinol. 111: 386-394.

BuchananK.L. (2000). Stress and the evolution of condition-dependent signals. — Trends Ecol. Evol. 15: 156-160.

ButlerS.J.WhittinghamM.J.QuinnJ.L.CresswellW. (2006). Time in captivity, individual differences and foraging behaviour in wild-caught chaffinches. — Behaviour 143: 535-548.

CarereC. (2003). Personalities as epigenetic suites of traits. — PhD thesis Groningen University Groningen.

CarereC.GroothuisT.G.G.MostlE.DaanS.KoolhaasJ.M. (2003). Fecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress. — Horm. Behav. 43: 540-548.

CarereC.CaramaschiD.FawcettT.W. (2010). Covariation between personalities and individual differences in coping with stress: converging evidence and hypotheses. — Curr. Zool. 56: 728-740.

CavigelliS.A.McClintockM.K. (2003). Fear of novelty in infant rats predicts adult corticosterone dynamics and an early death. — Proc. Natl. Acad. Sci. USA 100: 16131-16136.

CavigelliS.A.RaganC.M.MichaelK.C.KovacsicsC.E.BrlisckeA.P. (2009). Stable behavioral inhibition and glucocorticoid production as predictors of longevity. — Physiol. Behav. 98: 205-214.

CockremJ.F. (2007). Stress, corticosterone responses and avian personalities. — J. Ornithol. 148: S169-S178.

CockremJ.F.SilverinB. (2002a). Sight of a predator can stimulate a corticosterone response in the great tit (Parus major). — Gen. Comp. Endocrinol. 125: 248-255.

CockremJ.F.SilverinB. (2002b). Variation within and between birds in corticosterone responses of great tits (Parus major). — Gen. Comp. Endocrinol. 125: 197-206.

CockremJ.F.BarrettD.P.CandyE.J.PotterM.A. (2009). Corticosterone responses in birds: Individual variation and repeatability in Adelie penguins (Pygoscelis adeliae) and other species, and the use of power analysis to determine sample sizes. — Gen. Comp. Endocrinol. 163: 158-168.

DaisleyJ.N.BromundtV.MostlE.KotrschalK. (2005). Enhanced yolk testosterone influences behavioral phenotype independent of sex in Japanese quail chicks Coturnix japonica. — Horm. Behav. 47: 185-194.

DickensM.J.EarleK.A.RomeroL.M. (2009). Initial transference of wild birds to captivity alters stress physiology. — Gen. Comp. Endocrinol. 160: 76-83.

DingemanseN.J.WrightJ.KazemA.J.N.ThomasD.K.HicklingR.DawnayN. (2007). Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. — J. Anim. Ecol. 76: 1128-1138.

DingemanseN.J.EdelaarP.KempenaersB. (2010). Why is there variation in baseline glucocorticoid levels?Trends Ecol. Evol. 25: 261-262.

DrentP.J.van OersK.van NoordwijkA.J. (2003). Realized heritability of personalities in the great tit (Parus major). — Proc. Roy. Soc. Lond. B: Biol. Sci. 270: 45-51.

FazioE.FerlazzoA. (2003). Evaluation of stress during transport. — Vet. Res. Commun. 27: 519-524.

GentleL.K.GoslerA.G. (2001). The effects of altering perceived predation risk on the fat reserves of wild great tits, Parus major. — Proc. Roy. Soc. Lond. B: Biol. Sci. 268: 487-491.

GoslerA.G. (1996). Environmental and social determinants of winter fat storage in the great tit Parus major. — J. Anim. Ecol. 65: 1-17.

GoslingS.D. (2001). From mice to men: what can we learn about personality from animal research?Psychol. Bull. 127: 45-86.

GoutteA.AngelierF.WelckerJ.MoeB.Clement-ChastelC.GabrielsenG.W.BechC.ChastelO. (2010). Long-term survival effect of corticosterone manipulation in Black-legged kittiwakes. — Gen. Comp. Endocrinol. 167: 246-251.

GriecoF.van NoordwijkA.J.VisserM.E. (2002). Evidence for the effect of learning on timing of reproduction in blue tits. — Science 296: 136-138.

HauM.GoymannW. (2015). Endocrine mechanisms, behavioral phenotypes and plasticity: known relationships and open questions. — Front. Zool. 12: 1-15.

HendersonL.J.HeidingerB.J.EvansN.P.ArnoldK.E. (2013). Ultraviolet crown coloration in female blue tits predicts reproductive success and baseline corticosterone. — Behav. Ecol. 24: 1299-1305.

HendersonL.J.EvansN.P.HeidingerB.J.AdamsA.ArnoldK.E. (2014). Maternal condition but not corticosterone is linked to offspring sex ratio in a passerine bird. — PloS One 9: e110858.

HerbornK.CoffeyJ.LarcombeS.AlexanderL.ArnoldK.E. (2011). Oxidative profile varies with personality in European greenfinches. — J. Exp. Biol. 214: 1732-1739.

HerbornK.A.MacleodR.MilesW.T.S.SchofieldA.N.B.AlexanderL.ArnoldK.E. (2010). Personality in captivity reflects personality in the wild. — Anim. Behav. 79: 835-843.

HuntingfordF.A. (1976). Relationship between anti-predator behavior and aggression among conspecifics in 3-spined stickleback, Gasterosteus aculeatus. — Anim. Behav. 24: 245-260.

Jenni-EiermannS.GlausE.GrüeblerM.SchwablH.JenniL. (2008). Glucocorticoid response to food availability in breeding barn swallows (Hirundo rustica). — Gen. Comp. Endocrinol. 155: 558-565.

KoolhaasJ.M.de BoerS.F.BuwaldaB.van ReenenK. (2007). Individual variation in coping with stress: a multidimensional approach of ultimate and proximate mechanisms. — Brain Behav. Evol. 70: 218-226.

KoolhaasJ.M.de BoerS.F.CoppensC.M.BuwaldaB. (2010). Neuroendocrinology of coping styles: towards understanding the biology of individual variation. — Front. Neuroendocrinol. 31: 307-321.

LandysM.M.RamenofskyM.GuglielmoC.G.WingfieldJ.C. (2004). The low-affinity glucocorticoid receptor regulates feeding and lipid breakdown in the migratory Gambel’s white-crowned sparrow Zonotrichia leucophrys gambelii. — J. Exp. Biol. 207: 143-154.

Le MahoY.KarmannH.BriotD.HandrichY.RobinJ.P.MioskowskiE.CherelY.FarniJ. (1992). Stress in birds due to routine handling and a technique to avoid it. — Am. J. Physiol. 263: R775-R781.

Le VinA.L.MableB.K.TaborskyM.HegD.ArnoldK.E. (2011). Individual variation in helping in a cooperative breeder: relatedness versus behavioural type. — Anim. Behav. 82: 467-477.

LessellsC.M.BoagA.M. (1987). Unrepeatable repeatabilities: a common mistake. — Auk 104: 116-121.

LohmusM.SandbergR.HolbertonR.L.MooreF.R. (2003). Corticosterone levels in relation to migratory readiness in red-eyed vireos (Vireo olivaceus). — Behav. Ecol. Sociobiol. 54: 233-239.

LongJ.A.HolbertonR.L. (2004). Corticosterone secretion, energetic condition, and a test of the migration modulation hypothesis in the hermit thrush (Catharus guttatus), a short-distance migrant. — Auk 121: 1094-1102.

MartinJ.G.A.RealeD. (2008). Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. — Anim. Behav. 75: 309-318.

MartinL.B. (2009). Stress and immunity in wild vertebrates: timing is everything. — Gen. Comp. Endocrinol. 163: 70-76.

MartinsT.L.F.RobertsM.L.GiblinI.HuxhamR.EvansM.R. (2007). Speed of exploration and risk-taking behavior are linked to corticosterone titres in zebra finches. — Horm. Behav. 52: 445-453.

Mettke-HofmannC.WinklerH.LeislerB. (2002). The significance of ecological factors for exploration and neophobia in parrots. — Ethology 108: 249-272.

Mettke-HofmannC.LorentzenS.SchlichtE.SchneiderJ.WernerF. (2009). Spatial neophilia and spatial neophobia in resident and migratory warblers (Sylvia). — Ethology 115: 482-492.

MonaghanP. (2008). Review. Early growth conditions, phenotypic development and environmental change. — Phil. Trans. Roy. Soc. Lond. B: Biol. Sci. 363: 1635-1645.

MullerC.Jenni-EiermannS.BlondelJ.PerretP.CaroS.P.LambrechtsM.JenniL. (2006). Effect of human presence and handling on circulating corticosterone levels in breeding blue tits (Parus caeruleus). — Gen. Comp. Endocrinol. 148: 163-171.

PiersmaT.ReneerkensJ.RamenofskyM. (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.

PravosudovV.V.KitayskyA.S.WingfieldJ.C.ClaytonN.S. (2001). Long-term unpredictable foraging conditions and physiological stress response in mountain chickadees (Poecile gambeli). — Gen. Comp. Endocrinol. 123: 324-331.

Raja-ahoS.SuorsaP.VainioM.NikinmaaM.LehikoinenE.EevaT. (2010). Body condition is associated with adrenocortical response in the barn swallow (Hirundo rustica L.) during early stages of autumn migration. — Oecologia 163: 323-332.

RomeroL.M.ReedJ.M. (2005). Collecting baseline corticosterone samples in the field: is under 3 min good enough?Comp. Biochem. Physiol. A 140: 73-79.

RomeroL.M.ReedJ.M.WingfieldJ.C. (2000). Effects of weather on corticosterone responses in wild free-living passerine birds. — Gen. Comp. Endocrinol. 118: 113-122.

RubensteinD.R. (2007). Stress hormones and sociality: integrating social and environmental stressors. — Proc. Roy. Soc. Lond. B: Biol. Sci. 274: 967-975.

Ruiz-GomezM.D.KittilsenS.HoglundE.HuntingfordF.A.SorensenC.PottingerT.G.BakkenM.WinbergS.KorzanW.J.OverliO. (2008). Behavioral plasticity in rainbow trout (Oncorhynchus mykiss) with divergent coping styles: when doves become hawks. — Horm. Behav. 54: 534-538.

ScheidC.NoëR. (2010). The performance of rooks in a cooperative task depends on their temperament. — Anim. Cogn. 13: 545-553.

SchoechS.J.RenselM.A.BridgeE.S.BoughtonR.K.WilcoxenT.E. (2009). Environment, glucocorticoids, and the timing of reproduction. — Gen. Comp. Endocrinol. 163: 201-207.

SihA.KatsL.B.MooreR.D. (1992). Effects of predatory sunfish on the density, drift, and refuge use of stream salamander larvae. — Ecology 73: 1418-1430.

StampsJ.GroothuisT.G.G. (2010). The development of animal personality: relevance, concepts and perspectives. — Biol. Rev. 85: 301-325.

SvenssonL. (1992). Identification guide to European passerines. — BTOThetford.

ToblerM.SandellM.I. (2007). Yolk testosterone modulates persistence of neophobic responses in adult zebra finches, Taeniopygia guttata. — Horm. Behav. 52: 640-645.

van OersK.DrentP.J.de GoedeP.van NoordwijkA.J. (2004). Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. — Proc. Roy. Soc. Lond. B: Biol. Sci. 271: 65-73.

van OersK.de JongG.van NoordwijkA.J.KempenaersB.DrentP.J. (2005a). Contribution of genetics to the study of animal personalities: a review of case studies. — Behaviour 142: 1185-1206.

van OersK.KlunderM.DrentP.J. (2005b). Context dependence of personalities: risk-taking behavior in a social and a nonsocial situation. — Behav. Ecol. 16: 716-723.

VerbeekM.E.M.DrentP.J.WiepkemaP.R. (1994). Consistent individual-differences in early exploratory-behavior of male great tits. — Anim. Behav. 48: 1113-1121.

VerbeekM.E.M.BoonA.DrentP.J. (1996). Exploration, aggressive behavior and dominance in pair-wise confrontations of juvenile male great tits. — Behaviour 133: 945-963.

WilsonD.S.ClarkA.B.ColemanK.DearstyneT. (1994). Shyness and boldness in humans and other animals. — Trends Ecol. Evol. 9: 442-446.

WingfieldJ.C. (1994). Modulation of the adrenocortical response to stress in birds. — In: Perspectives in comparative endocrinology ( DaveyK.G.PeterR.E.TobeS.S. eds). National Research Council of CanadaOttawa, ON p.  520-528.

WingfieldJ.C.KitayskyaA.S. (2002). Endocrine responses to unpredictable environmental events: stress or anti-stress hormones?Integr. Comp. Biol. 42: 600-609.

WingfieldJ.C.VelckC.M.MooreM.C. (1992). Seasonal changes of the adrenocortical response to stress in birds of the Sonoran desert. — J. Exp. Zool. 264: 419-428.

Figures

  • View in gallery

    Relationships between personality traits and plasma Cort concentrations. Baseline Cort concentrations were related to (a) activity level in females (crosses, solid line, N=6), but not in males (circles, dashed line, N=31); and unrelated to (b) exploratory tendency (N=37); and (c) neophobia (N=35). Stress-induced Cort concentrations were (d) unrelated to activity levels (N=29); (e) marginally related to neophobia (N=24); and (f) significantly related to exploratory tendency (N=29).

  • View in gallery

    Relationships between change in mass over two days of captivity (mass at blood sampling on day 2–mass at capture from wild) and baseline plasma Cort concentrations for juveniles (circles, dashed line, N=13) and adults (stars, solid line, N=23).

  • View in gallery

    Relationships between stress-induced plasma Cort concentrations and (a) change in mass over two days of captivity (mass at blood sampling on day 2–mass at capture from wild) (N=30); and (b) mean haematocrit level (N=30).

  • View in gallery

    Apparatus used during the captive exploration trials (a) Photo of cage set up. (d) Schematic of cage set up; the food was removed 1 h and water bowl 30 min before the start of the trial, via the door. This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/journals/1568539x.

  • View in gallery

    The apparatus used for neophobia trial. (a) A photo of the novel objects used in the neophobia trial: A, half a purple rubber ball; B, a plastic pink frog. (b) A photo of a blue tit approaching the novel object in a food bowl (photo credits: Katherine Herborn). This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/journals/1568539x.

Index Card

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 17 17 9
Full Text Views 24 24 24
PDF Downloads 4 4 4
EPUB Downloads 0 0 0