HPI reactivity does not reflect changes in personality among trout introduced to bold or shy social groups

in Behaviour
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Physiological stress responses often correlate with personalities (e.g., boldness). However, this relationship can become decoupled, although the mechanisms underlying changes in this relationship are poorly understood. Here we quantify (1) how an individual’s boldness (response to novel objects) in rainbow trout, Oncorhynchus mykiss, changes in response to interactions with a population of either bold or shy conspecifics and we (2) measured associated post-stress cortisol levels. Initially-bold trout became shyer regardless of group composition, whereas shy trout remained shy demonstrating that bold individuals are more plastic. Stress-induced plasma cortisol reflected the original personality of fish but not the personality induced by the treatment, irrespective of population personality. Change in boldness of bold trout may indicate preference towards initially subordinate behaviour when joining a new population. However, here we provide further evidence that behavioural and physiological parameters of coping styles may become uncoupled whereby behavioural changes are not correlated with stress responsiveness.

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References

AdriaenssensB.JohnssonJ.I. (2012). Natural selection, plasticity and the emergence of a behavioural syndrome in the wild. — Ecol. Lett. 16: 47-55.

BackströmT.SchjoldenJ.ØverliØ.ThörnqvistP.-O.WinbergS. (2011). Stress effects on AVT and CRF systems in two strains of rainbow trout (Oncorhynchus mykiss) divergent in stress responsiveness. — Horm. Behav. 59: 180-186.

BarnardC.J.BurkT. (1979). Dominance hierarchies and the evolution of “individual recognition”. — J. Theor. Biol. 81: 65-73.

BatesD.MaechlerM.BolkerB.WalkerS. (2015). Fitting linear mixed-effects models using lme4. — J. Stat. Softw. 67: 1-48.

BeitingerT.L. (1990). Behavioral reactions for the assessment of stress in fishes. — J. Great Lakes Res. 16: 495-528.

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

BernierN.J.CraigP.M. (2005). CRF-related peptides contribute to stress response and regulation of appetite in hypoxic rainbow trout. — Am. J. Physiol. 289: R982-R990.

BoultonK.CoutoE.GrimmerA.J.EarleyR.L.CanarioA.V.M.WilsonA.J.WallingC.A. (2015). How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model. — Ecol. Evol. 5: 618-633.

BrownC.BurgessF.BraithwaiteV.A. (2007). Heritable and experiential effects on boldness in a tropical poeciliid. — Behav. Ecol. Sociobiol. 62: 237-243.

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

CastanheiraM.F.CerqueiraM.MillotS.GonçalvesR.A.OliveiraC.C.V.ConceiçãoL.E.C.MartinsC.I.M. (2016). Are personality traits consistent in fish? — The influence of social context. — Appl. Anim. Behav. Sci. 178: 96-101.

ClementsS.SchreckC.B.LarsenD.A.DickhoffW.W. (2002). Central administration of corticotropin-releasing hormone stimulates locomotor activity in juvenile chinook salmon. — Gen. Comp. Endocrinol. 125: 319-327.

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

DeverillJ.I.AdamsC.E.BeanC.W. (1999). Prior residence, aggression and territory acquisition in hatchery-reared and wild brown trout. — J. Fish Biol. 55: 868-875.

DeWittT.J.SihA.WilsonD.S. (1998). Costs and limits of phenotypic plasticity. — Trends Ecol. Evol. 13: 77-81.

DinanT.G. (1996). Serotonin and the regulation of hypothalamic-pituitary-adrenal axis function. — Life Sci. 58: 1683-1694.

DingemanseN.J.KazemA.J.N.RéaleD.WrightJ. (2010). Behavioural reaction norms: where animal personality meets individual plasticity. — Trends Ecol. Evol. 25: 81-89.

FavatiA.LeimarO.RadesäterT.LøvlieH. (2014). Social status and personality: stability in social state can promote consistency of behavioural responses. — Proc. R. Soc. Lond. B Biol. 281: 20132531.

FrostA.J.Winrow-GiffenA.AshleyP.J.SneddonL.U. (2007). Plasticity in animal personality traits: does prior experience alter the degree of boldness?Proc. R. Soc. Lond. B Biol. 274: 333-339.

GilmourK.M.DiBattistaJ.D.ThomasJ.B. (2005). Physiological causes and consequences of social status in salmonid fish. — Integrat. Comp. Biol. 45: 263-273.

HarcourtJ.L.SweetmanG.JohnstoneR.A.ManicaA. (2009). Personality counts: the effect of boldness on shoal choice in three-spined sticklebacks. — Anim. Behav. 77: 1501-1505.

HöjesjöJ.JohnssonJ.I.PeterssonE.JärviT. (1998). The importance of being familiar: individual recognition and social behavior in sea trout (Salmo trutta). — Behav. Ecol. 9: 445-451.

HuntingfordF.A. (1976). The relationship between anti-predator behaviour and aggression among conspecifics in the three-spined stickleback, Gasterosteus aculeatus. — Anim. Behav. 24: 245-260.

HuntingfordF.AdamsC. (2005). Behavioural syndromes in farmed fish: implications for production and welfare. — Behaviour 142: 1207-1221.

JohnssonJ.I. (1997). Individual recognition affects aggression and dominance relations in rainbow trout, Oncorhynchus mykiss. — Ethology 103: 267-282.

JohnssonJ.I.SernlandE.BlixtM. (2001). Sex-specific aggression and antipredator behaviour in young brown trout. — Ethology 107: 587-599.

JönssonE.JohnssonJ.I.BjörnssonB.T. (1996). Growth hormone increases predation exposure of rainbow trout. — Proc. R. Soc. Lond. B Biol. 263: 647-651.

KimT.ZukM. (2000). The effects of age and previous experience on social rank in female red junglefowl, Gallus gallus spadiceus. — Anim. Behav. 60: 239-244.

KoolhaasJ.M.KorteS.M.De BoerS.F.Van der VegtB.J.Van ReenenC.G.HopsterH.De JongI.C.RuisM.A.W.BlokhuisH.J. (1999). Coping styles in animals: current status in behavior and stress-physiology. — Neurosci. Biobehav. Rev. 23: 925-935.

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.

KrauseJ.RuxtonG.D. (2002). Living in groups. — Oxford University Press, Oxford.

KrekeN.DietrichD.R. (2008). Physiological endpoints for potential SSRI interactions in fish. — Crit. Rev. Toxicol. 37: 215-247.

LeBlondC.ReebsS.G. (2006). Individual leadership and boldness in shoals of golden shiners (Notemigonus crysoleucas). — Behaviour 143: 1263-1280.

LePageO.LarsonE.T.MayerI.WinbergS. (2005). Serotonin, but not melatonin, plays a role in shaping dominant-subordinate relationships and aggression in rainbow trout. — Horm. Behav. 48: 233-242.

LimaS.L.DillL.M. (1990). Behavioral decisions made under the risk of predation: a review and prospectus. — Can. J. Zool. 68: 619-640.

MagnhagenC. (2012). Personalities in a crowd: what shapes the behaviour of Eurasian perch and other shoaling fishes?Curr. Zool. 58: 35-44.

MagnhagenC.BunnefeldN. (2009). Express your personality or go along with the group: what determines the behaviour of shoaling perch?Proc. Roy. Soc. Lond. B: Biol. Sci. 276: 3369-3374.

MagnhagenC.StaffanF. (2003). Social learning in young-of-the-year perch encountering a novel food type. — J. Fish Biol. 63: 824-829.

MoreiraP.S.A.PulmanK.G.T.PottingerT.G. (2004). Extinction of a conditioned response in rainbow trout selected for high or low responsiveness to stress. — Horm. Behav. 46: 450-457.

OlsenE.M.VøllestadL.A. (2001). An evaluation of visible implant elastomer for marking age-0 brown trout. — N. Am. J. Fish. Managem. 21: 967-970.

ØverliØ.KorzanW.J.LarsonE.T.WinbergS.LePageO.PottingerT.G.RennerK.J.SummersC.H. (2004). Behavioral and neuroendocrine correlates of displaced aggression in trout. — Horm. Behav. 45: 324-329.

ØverliØ.WinbergS.PottingerT.G. (2005). Behavioral and neuroendocrine correlates of selection for stress responsiveness in rainbow trout — a review. — Integr. Comp. Biol. 45: 463-474.

ØverliØ.SørensenC.PulmanK.G.T.PottingerT.G.KorzanW.SummersC.H.NilssonG.E. (2007). Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. — Neurosci. Biobehav. Rev. 31: 396-412.

PickeringA.D.PottingerT.G. (1983). Seasonal and diel changes in plasma cortisol levels of the brown trout, Salmo trutta L.Gen. Comp. Endocrinol. 49: 232-239.

PickeringA.D.PottingerT.G. (1989). Stress responses and disease resistance in salmonid fish — effects of chronic elevation of plasma-cortisol. — Fish Physiol. Biochem. 7: 253-258.

PinheiroJ.BatesD.DebRoyS.SarkarD. & R Core Team (2016). Linear and nonlinear mixed effects models. — R package version 3.1-128. R Foundation for Statistical Computing, Vienna. Available online at https://cran.r-project.org/web/packages/nlme/index.html.

PottingerT.G.CarrickT.R. (2001). Stress responsiveness affects dominant-subordinate relationships in rainbow trout. — Horm. Behav. 40: 419-427.

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

Ruiz-GomezM.D.L.HuntingfordF.A.ØverliØ.ThornqvistP.-O.HöglundE. (2011). Response to environmental change in rainbow trout selected for divergent stress coping styles. — Physiol. Behav. 102: 317-322.

SchjoldenJ.BackströmT.PulmanK.G.T.PottingerT.G.WinbergS. (2005). Divergence in behavioural responses to stress in two strains of rainbow trout (Oncorhynchus mykiss) with contrasting stress responsiveness. — Horm. Behav. 48: 537-544.

SihA.WattersJ.V. (2005). The mix matters: behavioural types and group dynamics in water striders. — Behaviour 142: 1417-1431.

SihA.BellA.JohnsonJ.C. (2004). Behavioral syndromes: an ecological and evolutionary overview. — Trends Ecol. Evol. 19: 372-378.

SneddonL.U. (2003). The bold and the shy: individual differences in rainbow trout. — J. Fish Biol. 62: 971-975.

SneddonL.U.BraithwaiteV.A.GentleM.J. (2003). Novel object test: examining nociception and fear in the rainbow trout. — J. Pain 4: 431-440.

SneddonL.U.MargaretoJ.CossinsA.R. (2005). The use of transcriptomics to address questions in behaviour: production of a suppression subtractive hybridisation library from dominance hierarchies of rainbow trout. — Physiol. Biochem. Zool. 75: 695-705.

SundströmL.F.PeterssonE.HöjesjöJ.JohnssonJ.I.JärviT. (2004). Hatchery selection promotes boldness in newly hatched brown trout (Salmo trutta): implications for dominance. — Behav. Ecol. 15: 192-198.

ThomsonJ.S.WattsP.C.PottingerT.G.SneddonL.U. (2011). Physiological and genetic correlates of boldness: characterising the mechanisms of behavioural variation in rainbow trout, Oncorhynchus mykiss. — Horm. Behav. 59: 67-74.

ThomsonJ.S.WattsP.C.PottingerT.G.SneddonL.U. (2012). Plasticity of boldness in rainbow trout, Oncorhynchus mykiss: do hunger and predation influence risk-taking behaviour?Horm. Behav. 61: 750-757.

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

Vaz-SerranoJ.Ruiz-GomezM.D.L.GjøenH.-M.SkovP.V.HuntingfordF.A.ØverliØ.HöglundE. (2011). Consistent boldness behaviour in early emerging fry of domesticated Atlantic salmon (Salmo salar): decoupling of behavioural and physiological traits of the proactive stress coping style. — Physiol. Behav. 103: 359-364.

WinbergS.LePageO. (1998). Elevation of brain 5-HT activity, POMC expression, and plasma cortisol in socially subordinate rainbow trout. — Am. J. Physiol. 274: 645-654.

ZuurA.F.IenoE.N.WalkerN.J.SavelievA.A.SmithG.M. (2009). Mixed effects models and extensions in ecology with R. — Springer, New York, NY.

Figures

  • Schematic of the experimental procedure, indicating the experimental set-up and the time-scale of experiments. Dotted lines indicate dividers within the Population Tanks which housed two fish populations simultaneously (see Section 2.3 for details).

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  • Behaviour of rainbow trout, Oncorhynchus mykiss, before (white boxes) and after (grey boxes) a week spent with a population of either bold or shy trout (where boldness was measured as latency to approach within 5 cm of a novel object, and where bold fish approached in <180 s and shy fish approached in >300 s or not at all). Figures indicate different measures of behaviour: (a) latency to approach to within 5 cm of a novel object (s) for bold and shy focal fish; (b) duration of passive behaviour (s) of bold and shy focal fish; and frequency of changing between passive and active behaviour (see text for details) between (c) bold and shy focal fish and (d) comparisons of all focal fish compared between populations. For all boxes: line = median, box = interquartile range, whiskers indicate extent of data < 1.5 × IQR, dots = outliers (greater than 1.5 × IQR outside the box).

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  • Mean (± SE) plasma cortisol concentrations in bold (white) and shy (grey) rainbow trout, Oncorhynchus mykiss, 15 min after an emersion stress. Individual trout were placed into a group of either nine bold (Bold Population) or nine shy conspecifics (Shy Population) for one week before sampling. Groups which do not share a common lower case letter were significantly different (p<0.05). N=5,8 for bold trout and N=11,10 for shy trout in a bold and shy population respectively.

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  • Mean (± SE) specific growth rate (G) of bold (white) and shy (grey) rainbow trout, Oncorhynchus mykiss, placed for one week into a population of 9 bold or shy trout. n=5,8 for bold trout and n=10,10 for shy trout in a bold and shy population, respectively.

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