Improved performance, within-individual consistency and between-individual differences in the righting behaviour of the Caribbean sea star, Oreaster reticulatus

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

Individuals cope differently to challenging and stressful situations. Being inverted is challenging and stressful for animals, as the position leaves them vulnerable to predators and desiccation. Although sea star self-righting was first studied in the 19th century, efforts to quantify patterns of within-individual consistency and among-individual differences are limited. Here we examined the performance and repeatability of righting behaviour in the Caribbean sea star (Oreaster reticulatus). Oreaster reticulatus were wild caught and transported to a nearby facility where they were inverted up to five times. Most animals improved their righting times and exhibited within-individual consistency and among individual differences in righting method. We posit that it may be favourable to employ a consistent righting method to effectively achieve an upright position. Predation pressure and stress physiology are hypothesized to shape individual differences in righting behaviour. Moreover, these results provide preliminary evidence of personality in sea stars.

Sections

References

AbjörnssonK.HanssonL.-A.BrönmarkC. (2004). Responses of prey from habitats with different predator regimes: local adaptation and heritability. — Ecology 85: 1859-1866.

BellA.M.HankisonS.J.LaskowskiK.L. (2009). The repeatability of behaviour: a meta-analysis. — Anim. Behav. 77: 771-783.

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

BlakeD.B. (1981). The new Jurassic sea star genus Eokainaster and comments on life habits and the origins of the modern Asteroidea. — J. Paleontol. 55: 33-46.

BonnetX.LagardeF.HenenB.T.CorbinJ.NagyK.A.NaulleauG.BalhoulK.ChastelO.LegrandA.CambagR. (2001). Sexual dimorphism in steppe tortoises (Testudo horsfieldii): influence of the environment and sexual selection on body shape and mobility. — Biol. J. Linn. Soc. 72: 357-372.

BriffaM.GreenawayJ. (2011). High in situ repeatability of behaviour indicates animal personality in the beadlet anemone Actinia equina (Cnidaria). — PloS One 6: e21963.

BriffaM.BridgerD.BiroP.A. (2013). How does temperature affect behaviour? Multilevel analysis of plasticity, personality and predictability in hermit crabs. — Anim. Behav. 86: 47-54.

CarewT.J.SahleyC.L. (1986). Invertebrate learning and memory: from behavior to molecules. — Annu. Rev. Neurosci. 9: 435-487.

ClarkA.M.DowneyM.E. (1992). Starfishes of the Atlantic. — Chapman & Hall, London.

DalesmanS.RundleS.D.ColemanR.A.CottonP.A. (2006). Cue association and antipredator behaviour in a pulmonate snail, Lymnaea stagnalis. — Anim. Behav. 71: 789-797.

FlammangP.MichelA.CauwenbergeA.V.AlexandreH.JangouxM. (1998). A study of the temporary adhesion of the podia in the sea star Asterias rubens (Echinodermata, Asteroidea) through their footprints. — J. Exp. Biol. 201: 2383-2395.

GarmA.NilssonD.-E. (2014). Visual navigation in starfish: first evidence for the use of vision and eyes in starfish. — Proc. Roy. Soc. Lond. B: Biol. Sci. 281: 20133011.

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

HeldM.B.E.HarleyC.D.G. (2009). Responses to low salinity by the sea star Pisaster ochraceus from high — and low-salinity populations. — Invertebr. Biol. 128: 381-390.

HennebertE.WattiezR.DemeuldreM.LadurnerP.HwangD.S.WaiteJ.H.FlammangP. (2014). Sea star tenacity mediated by a protein that fragments, then aggregates. — Proc. Natl. Acad. Sci. USA 111: 6317-6322.

HiroseM. (2011). Orientation and righting behavior of the sand-dwelling bryozoan Conescharellina catella. — Invertebr. Biol. 130: 282-290.

JenningsH.S. (1907). Behavior of the starfish Asterias forreri de Loriol. — Univ. Calif. Publ. Zool. 4: 53-185.

KleitmanN. (1941). The effect of temperature on the righting of echinoderms. — Biol. Bull. 80: 292-298.

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. Behav. Rev. 23: 925-935.

KuriharaT. (1999). Effects of sediment type and food abundance on the vertical distribution of the starfish Asterina pectinifera. — Mar. Ecol. Prog. Ser. 181: 269-277.

LamingS.R.JenkinsS.R.McCarthyI.D. (2013). Repeatability of escape response performance in the queen scallop, Aequipecten opercularis. — J. Exp. Biol. 216: 3264-3272.

LawrenceJ.M.CowellB.C. (1996). The righting response as an indication of stress in Stichaster striatus (Echinodermata, Asteroidea). — Mar. Freshw. Behav. Physiol. 27: 239-248.

MahC.L.BlakeD.B. (2012). Global diversity and phylogeny of the Asteroidea (Echinodermata). — PloS One 7: e35644.

MatherJ.A.LogueD.M. (eds) (2013). The bold and the spineless: invertebrate personalities. — The University of Chicago Press, Chicago, IL, USA.

MetaxasA.ScheiblingR.E.RobinsonM.C.YoungC.M. (2008). Larval development, settlement, and early post-settlement behavior of the tropical sea star Oreaster reticulatus. — Bull. Mar. Sci. 83: 471-480.

MigitaM. (2012). Complexity in the righting behavior of the starfish Asterina pectinifera. — In: Echinoderms in a changing world: Proceedings of the 13th International Echinoderm Conference, January 5–9, 2009, University of Tasmania, Hobart Tasmania, Australia. CRC Press, Boca Raton, FL, p.  235.

MigitaM.MizukamiE.GunjiY.-P. (2005). Flexibility in starfish behavior by multi-layered mechanism of self-organization. — Biosystems 82: 107-115.

MontgomeryE.M. (2014). Predicting crawling speed relative to mass in sea stars. — J. Exp. Mar. Biol. Ecol. 458: 27-33.

MontgomeryE.M.PalmerA.R. (2012). Effects of body size and shape on locomotion in the bat star (Patiria miniata). — Biol. Bull. 222: 222-232.

MotokawaT. (ed.) (1985). Catch connective tissue: the connective tissue with adjustable mechanical properties. — In: Echinodermata. Balkema, Rotterdam, p.  69-73.

MotokawaT. (1988). Catch connective tissue: a key character for echinoderms’ success. — In: Echinoderm biology, p.  39-54.

MotokawaT.WainwrightS.A. (1991). Stiffness of starfish arm and involvement of catch connective tissue in the stiffness change. — Comp. Biochem. Physiol. A Physiol. 100: 393-397.

MotokawaT.SatoE.UmeyamaK. (2012). Energy expenditure associated with softening and stiffening of echinoderm connective tissue. — Biol. Bull. 222: 150-157.

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

NeumannC. (2000). Evidence of predation on Cretaceous sea stars from north-west Germany. — Lethaia 33: 65-70.

PennD.BrockmannJ. (1995). Age-biased stranding and righting in male horseshoe crabs, Limulus polyphemus. — Anim. Behav. 49: 1531-1539.

PinheiroJ.BatesD.DebRoyS.SarkarD. & R Core Team (2014). nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 3:118. — R Foundation for Statistical Computing, Vienna.

PollisI.GonorJ. (1975). Behavioral aspects of righting in two asteroids from the Pacific coast of North America. — Biol. Bull. 148: 68-84.

R Core Team (2016). R: a language and environment for statistical computing. — R Foundation for Statistical Computing, Vienna.

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

RochetteR.ArsenaultD.J.JustomeB.HimmelmanJ.H. (1998). Chemically-mediated predator-recognition learning in a marine gastropod. — Ecoscience 5: 353-360.

RudinF.S.BriffaM. (2012). Is boldness a resource-holding potential trait? Fighting prowess and changes in startle response in the sea anemone, Actinia equina. — Proc. Roy. Soc. Lond. B: Biol. Sci. 279: 1904-1910.

SchielzethH.NakagawaS. (2011). rptR: Repeatability for Gaussian and non-Gaussian data. R Package Version 06 404: r36. — R Foundation for Statistical Computing, Vienna.

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

SinnD.L.GoslingS.D.MoltschaniwskyjN.A. (2008). Development of shy/bold behaviour in squid: context-specific phenotypes associated with developmental plasticity. — Anim. Behav. 75: 433-442.

SteyermarkA.C.SpotilaJ.R. (2001). Body temperature and maternal identity affect snapping turtle (Chelydra serpentina) righting response. — Copeia: 1050-1057.

ToscanoB.J.GattoJ.GriffenB.D. (2013). Effect of predation threat on repeatability of individual crab behavior revealed by mark-recapture. — Behav. Ecol. Sociobiol. 68: 519-527.

TurnerA.M.TurnerS.E.LappiH.M. (2006). Learning, memory and predator avoidance by freshwater snails: effects of experience on predator recognition and defensive strategy. — Anim. Behav. 72: 1443-1450.

WattsS.A.LawrenceJ.M. (1990). The effect of temperature and salinity interactions on righting, feeding and growth in the sea star Luidia clathrata (Say). — Mar. Behav. Physiol. 17: 159-165.

WickhamH. (2009). ggplot2: elegant graphics for data analysis. — Springer, New York, NY.

WolfM.WeissingF.J. (2010). Animal personalities: consequences for ecology and evolution. — Trends Ecol. Evol. 27: 452-461.

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

Figures

  • Righting methods 1 (A) and 2 (B) used by the Caribbean sea star O. reticulatus. In method 1, the animal reaches aborally with 4 arms whereas in method 2 all five arms reach orally before the animal tips over. 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
  • Righting duration (minutes) across consecutive trials for individual O. reticulatus. Trends are illustrated by locally weighted regression curves.

    View in gallery
  • Fitted values (± 95% CI) from a linear mixed model for the righting duration of a typical O. reticulatus across five trials. Estimates were generated by holding body size and water temperature at their means (x¯bodysize=14.8cm; x¯Temp=25.4°C).

    View in gallery

Information

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 17 17 11
Full Text Views 3 3 3
PDF Downloads 1 1 1
EPUB Downloads 0 0 0