Into the wild: developing field tests to examine the link between elasmobranch personality and laterality

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

The field of animal personality has received considerable attention in past decades, yet few studies have examined personality in the wild. This study investigated docility, a measure of boldness, in two Port Jackson shark (Heterodontus portusjacksoni) populations using field tests, and if laterality differences explained docility levels. We developed a struggle test as an assay for docility, which is particularly amenable to field studies. The struggle test was effective, and repeatable inter-individual docility differences were observed. Sex, but not population, influenced docility scores, with male sharks being less docile than females. This difference is likely due to the contrasting role each sex plays during mating. We also found individualized lateralization. However, no individual-level relationship between lateralization and docility was detected. Despite reported links between laterality and some personality traits, the relationship between laterality and boldness remains inconclusive in sharks. Further studies will prove essential to clarify the mechanisms behind personality traits in vertebrates.

Sections

References

ArchardG.A.BraithwaiteV.A. (2010). The importance of wild populations in studies of animal temperament. — J. Zool. 281: 149-160.

BercovitchF.B. (1995). Female cooperation, consortship maintenance, and male mating success in savanna baboons. — Anim. Behav. 50: 137-149.

BiroP.A.StampsJ.A. (2010). Do consistent individual differences in metabolic rate promote consistent individual differences in behavior?Trends Ecol. Evol. 25: 653-659.

BisazzaA.BrownC. (2011). Lateralization of cognitive functions in fish. — In: Fish cognition and behavior ( BrownC.LalandK.KrauseJ., eds). Wiley-Blackwell, Oxford, p.  298-324.

BisazzaA.De SantiA. (2003). Lateralization of aggression in fish. — Behav. Brain Res. 141: 131-136.

BisazzaA.CantalupoC.VallortigaraG. (1997). Lateral asymmetries during escape behavior in a species of teleost fish (Jenynsia lineata). — Physiol. Behav. 61: 31-35.

BisazzaA.CantalupoC.CapocchianoM.VallortigaraG. (2000). Population lateralisation and social behaviour: a study with 16 species of fish. — Laterality 5: 269-284.

BorgB. (1994). Androgens in teleost fishes. — Comp. Biochem. Physiol. C: Pharmacol. Toxicol. Endocrinol. 109: 219-245.

BrommerJ.E.KluenE. (2012). Exploring the genetics of nestling personality traits in a wild passerine bird: testing the phenotypic gambit. — Ecol. Evol. 2: 3032-3044.

BrownC.BibostA.-L. (2014). Laterality is linked to personality in the black-lined rainbowfish, Melanotaenia nigrans. — Behav. Ecol. Sociobiol. 68: 999-1005.

BrownC.BraithwaiteV.A. (2004). Size matters: a test of boldness in eight populations of the poeciliid Brachyraphis episcopi. — Anim. Behav. 68: 1325-1329.

BrownC.GardnerC.BraithwaiteV.A. (2004). Population variation in lateralized eye use in the poeciliid Brachyraphis episcopi. — Proc. Roy. Soc. Lond. B: Biol. Sci. 271: S455-S457.

BrownC.JonesF.BraithwaiteV.A. (2005). In situ examination of boldness–shyness traits in the tropical poeciliid, Brachyraphis episcopi. — Anim. Behav. 70: 1003-1009.

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

BrownC.WesternJ.BraithwaiteV.A. (2007b). The influence of early experience on, and inheritance of, cerebral lateralization. — Anim. Behav. 74: 231-238.

BrunnschweilerJ.M. (2006). Sharksucker–shark interaction in two carcharhinid species. — Mar. Ecol. 27: 89-94.

BsharyR.BrownC. (2014). Fish cognition. — Curr. Biol. 24: R947-R950.

BudaevS.BrownC. (2011). Personality traits and behaviour. — In: Fish cognition and behavior ( BrownC.LalandK.KrauseJ., eds). Wiley-Blackwell, Oxford, p.  135-165.

BurnhamK.P.AndersonD.R. (2003). Basic use of the information-theoretic approach. — In: Model selection and multimodel inference: a practical information-theoretic approach ( BurnhamK.P., ed.). Springer, New York, NY, p.  98-148.

CarereC.Van OersK. (2004). Shy and bold great tits (Parus major): body temperature and breath rate in response to handling stress. — Physiol. Behav. 82: 905-912.

CasperdJ.M.DunbarR.I.M. (1996). Asymmetries in the visual processing of emotional cues during agonistic interactions by gelada baboons. — Behav. Process. 37: 57-65.

DaddaM.DomenichiniA.PifferL.ArgentonF.BisazzaA. (2010). Early differences in epithalamic left–right asymmetry influence lateralization and personality of adult zebrafish. — Behav. Brain Res. 206: 208-215.

De SantiA.SovranoV.A.BisazzaA.VallortigaraG. (2001). Mosquitofish display differential left- and right-eye use during mirror image scrutiny and predator inspection responses. — Anim. Behav. 61: 305-310.

DempsterR.P.HeraldE.S. (1961). Notes on the hornshark Heterodontus francisci, with observations on mating activities. — Occas. Pap. Calif. Acad. 33: 1-7.

FairbanksL.A.FontenotM.B.Phillips-ConroyJ.E.JollyC.J.KaplanJ.R.MannJ.J. (1999). CSF monoamines, age and impulsivity in wild grivet monkeys (Cercopithecus aethiops aethiops). — Brain Behav. Evol. 53: 305-312.

FishF.E.BosticS.A.NicastroA.J.BeneskiJ.T. (2007). Death roll of the alligator: mechanics of twist feeding in water. — J. Exp. Biol. 210: 2811-2818.

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

GaulyM.MathiakH.HoffmannK.KrausM.ErhardtG. (2001). Estimating genetic variability in temperamental traits in German Angus and Simmental cattle. — Appl. Anim. Behav. Sci. 74: 109-119.

HarrisS.RamnarineI.W.SmithH.G.PetterssonL.B. (2010). Picking personalities apart: estimating the influence of predation, sex and body size on boldness in the guppy Poecilia reticulata. — Oikos 119: 1711-1718.

HenningsenA.D.MurruF.L.RasmussenL.E.L.WhitakerB.R.ViolettaG.C. (2008). Serum levels of reproductive steroid hormones in captive sand tiger sharks, Carcharias taurus (Rafinesque), and comments on their relation to sexual conflicts. — Fish Physiol. Biochem. 34: 437-446.

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.

HewsD.K.CastellanoM.HaraE. (2004). Aggression in females is also lateralized: left-eye bias during aggressive courtship rejection in lizards. — Anim. Behav. 68: 1201-1207.

IrvingE.BrownC. (2013). Examining the link between personality and laterality in a feral guppy Poecilia reticulata population. — J. Fish Biol. 83: 311-325.

JacobyD.M.P.FreemanR. (2016). Emerging network-based tools in movement ecology. — Trends Ecol. Evol. 31: 301-314.

JohnssonJ.I.CarlssonM.SundströmL.F. (2000). Habitat preference increases territorial defence in brown trout (Salmo trutta). — Behav. Ecol. Sociobiol. 48: 373-377.

KlimleyA.P. (1980). Observations of courtship and copulation in the nurse shark, Ginglymostoma cirratum. — Copeia: 878-882.

KockM.D.Du ToitR.KockN.MortonD.FogginC.PaulB. (1990). Effects of capture and translocation on biological parameters in free-ranging black rhinoceroses (Diceros bicornis) in Zimbabwe. — J. Zoo Wildl. Med.: 414-424.

Le NeindreP.TrillatG.SapaJ.MénissierF.BonnetJ.N.ChupinJ.M. (1995). Individual differences in docility in Limousin cattle. — J. Anim. Sci. 73: 2249-2253.

MatichP.HeithausM.R. (2015). Individual variation in ontogenetic niche shifts in habitat use and movement patterns of a large estuarine predator (Carcharhinus leucas). — Oecologia 178: 347-359.

MontoyaE.R.TerburgD.BosP.A.Van HonkJ. (2012). Testosterone, cortisol, and serotonin as key regulators of social aggression: a review and theoretical perspective. — Motivat. Emot. 36: 65-73.

MooreI.T.LemasterM.P.MasonR.T. (2000). Behavioural and hormonal responses to capture stress in the male red-sided garter snake, Thamnophis sirtalis parietalis. — Anim. Behav. 59: 529-534.

NakagawaS.SchielzethH. (2010). Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. — Biol. Rev. 85: 935-956.

NakanoS. (1995). Individual differences in resource use, growth and emigration under the influence of a dominance hierarchy in fluvial red-spotted masu salmon in a natural habitat. — J. Anim. Ecol. 64: 75-84.

NortonW.H.J.StumpenhorstK.Faus-KesslerT.FolchertA.RohnerN.HarrisM.P.CallebertJ.Bally-CuifL. (2011). Modulation of Fgfr1a signaling in zebrafish reveals a genetic basis for the aggression–boldness syndrome. — J. Neurosci. 31: 13796-13807.

OliveiraR.F.HirschenhauserK.CarneiroL.A.CanarioA.V.M. (2002). Social modulation of androgen levels in male teleost fish. — Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 132: 203-215.

PrattH.L.Jr.CarrierJ.C. (2001). A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. — Environ. Biol. Fish. 60: 157-188.

PurcellD.AraveC.W.WaltersJ.L. (1988). Relationship of three measures of behavior to milk production. — Appl. Anim. Behav. Sci. 21: 307-313.

RaoultV.BrownC.ZuberiA.WilliamsonJ.E. (2012). Blood cortisol concentrations predict boldness in juvenile mulloway (Argyosomus japonicus). — J. Ethol. 30: 225-232.

RaynaudJ.SchradinC. (2014). Experimental increase of testosterone increases boldness and decreases anxiety in male African striped mouse helpers. — Physiol. Behav. 129: 57-63.

RéaleD.GallantB.Y.LeblancM.Festa-BianchetM. (2000). Consistency of temperament in bighorn ewes and correlates with behaviour and life history. — Anim. Behav. 60: 589-597.

RéaleD.ReaderS.M.SolD.McdougallP.T.DingemanseN.J. (2007). Integrating animal temperament within ecology and evolution. — Biol. Rev. 82: 291-318.

ReddonA.R.HurdP.L. (2008). Aggression, sex and individual differences in cerebral lateralization in a cichlid fish. — Biol. Lett. 4: 338-340.

ReddonA.R.HurdP.L. (2009). Individual differences in cerebral lateralization are associated with shy–bold variation in the convict cichlid. — Anim. Behav. 77: 189-193.

RogersL.J. (2002). Lateralization in vertebrates: its early evolution, general pattern, and development. — Adv. Stud. Behav. 31: 107-161.

RogersL.J.AndrewR. (2002). Comparative vertebrate lateralization. — Cambridge University Press, Cambridge.

SihA.BellA.M.JohnsonJ.C.ZiembaR.E. (2004). Behavioral syndromes: an integrative overview. — Q. Rev. Biol. 79: 241-277.

TaylorR.W.BoonA.K.DantzerB.RéaleD.HumphriesM.M.BoutinS.GorrellJ.C.ColtmanD.W.McAdamA.G. (2012). Low heritabilities, but genetic and maternal correlations between red squirrel behaviours. — J. Evol. Biol. 25: 614-624.

TricasT.C.MaruskaK.P.RasmussenL.E.L. (2000). Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray. — Gen. Comp. Endocrinol. 118: 209-225.

WellsD.A.JonesD.N.BulgerD.BrownC. (2014). Male brush-turkeys attempt sexual coercion in unusual circumstances. — Behav. Process. 106: 180-186.

WilsonD.S.ColemanK.ClarkA.B.BiedermanL. (1993). Shy-bold continuum in pumpkinseed sunfish (Lepomis gibbosus): an ecological study of a psychological trait. — J. Comp. Psychol. 107: 250-260.

Figures

  • Map depicting the two study locations, Orion and Hyams reefs, in the Jervis Bay Marine Park, NSW, Australia. Brown shading illustrates rocky reef. Subtidal reef features digitized preferentially from swath bathymetry, LADS, and ADS40 aerial imagery. Map reproduced with permission from Joe Neilson (Fisheries NSW, NSW DPI). 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
  • Colour-coded docility scores for each of the 73 sharks across trials. Females (F) are depicted below the white line, and males (M) above the white line. 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
  • Proportion of sharks with a docility score of 3 in at least one trial, grouped by sex and location. Docility scores were significantly different between females and males (z=2.982, p=0.003).

    View in gallery

Information

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 15 15 9
Full Text Views 5 5 3
PDF Downloads 3 3 0
EPUB Downloads 0 0 0