Skip to main content

Advertisement

SpringerLink
Log in

Utility of statolith elemental chemistry as a proxy for temperature to elucidate the movements of the Irukandji jellyfish species Alatina alata

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Movements undertaken by marine organisms occur for varying reasons and knowledge surrounding them is critically important for understanding population structures, ecology and for effective management and conservation of species. The objective of this study was to test a hypothesis that the cubozoan jellyfish Alatina alata spends a large part of its life at great depths by utilising the recently validated technique of statolith elemental chemistry. The approach was to ground-truth estimates of temperature based on a previous manipulative laboratory-based experiment, determine Sr:Ca and Ba:Ca ratios in the statoliths of A. alata at different life-history stages and use elemental chemistry as an environmental marker to estimate their life-time movements. High Sr:Ca values in the core and edge of the statoliths were found which corresponded with the time jellyfish were in shallow waters. Ambient water temperatures estimated for the end period of the jellyfish’s lives closely matched known sea surface temperatures in Hawaii, hence supporting a correlation between statolith Sr:Ca and temperature. For the middle section of the statoliths, strong evidence from both Sr:Ca and Ba:Ca ratios suggested that the jellyfish reached depths of at least 200–400 m. Ba:Sr maxima further supported this as Ba concentrations are usually higher below the thermocline. Individual Sr:Ca tracks also suggested that individuals moved over a depth range of tens to hundreds of meters through undertaking regular vertical movements. This study demonstrates that the use of elemental chemistry within cubozoan statoliths has the potential to determine vertical and horizontal movements where temperature gradients are strong.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Arkhipkin AI, Campana SE, FitzGerald J, Thorrold SR (2004) Spatial and temporal variation in elemental signatures of statoliths from the Patagonian longfin squid (Loligo gahi). Can J Fish Aquat Sci 61:1212–1224

    Google Scholar 

  • Beck JW, Edwards RL, Ito E, Taylor FW, Recy J, Rougerie F, Joannot P, Henin C (1992) Sea-surface temperature from coral skeletal strontium/calcium ratios. Science 257:644–647

    CAS  PubMed  Google Scholar 

  • Bruland K, Lohan M (2006) Controls of trace metals in seawater. Oceans Mar Geochem 6:23–47

    Google Scholar 

  • Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297

    CAS  Google Scholar 

  • Campana SE, Thorrold SR (2001) Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? Can J Fish Aquat Sci 58:30–38

    Google Scholar 

  • Chiaverano LM, Holland BS, Crow GL, Blair L, Yanagihara AA (2013) Long-term fluctuations in circalunar beach aggregations of the box jellyfish Alatina moseri in Hawaii, with links to environmental variability. PLoS ONE 8:e77039

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Villiers S, Shen GT, Nelson BK (1994) The SrCa–temperature relationship in coralline aragonite: influence of variability in (SrCa) seawater and skeletal growth parameters. Geochim Cosmochim Acta 58:197–208

    Google Scholar 

  • Elsdon TS, Gillanders BM (2003) Reconstructing migratory patterns of fish based on environmental influences on otolith chemistry. Re Fish Biol Fish 13:217–235

    Google Scholar 

  • Elsdon TS, Wells BK, Campana SE, Gillanders BM, Jones CM, Limburg KE, Secor DH, Thorrold SR, Walther BD (2008) Otolith chemistry to describe movements and life-history parameters of fishes: hypotheses, assumptions, limitations and inferences. Oceanography and marine biology. CRC Press, Boca Raton, pp 303–336

    Google Scholar 

  • Fowler AJ, Campana SE, Thorrold SR, Jones CM (1995) Experimental assessment of the effect of temperature and salinity on elemental composition of otoliths using laser ablation ICPMS. Can J Fish Aquat Sci 52:1431–1441

    Google Scholar 

  • Frank KT, Page FH, McRuer JK (1989) Hydrographic effects on the vertical distribution of haddock (Melanogrammus aeglefinus) eggs and larvae on the southwestern Scotian Shelf. Can J Fish Aquat Sci 46:s82–s92

    Google Scholar 

  • Garm A, Bielecki J, Petie R, Nilsson D-E (2012) Opposite patterns of diurnal activity in the box jellyfish Tripedalia cystophora and Copula sivickisi. Biol Bull 222:35–45

    CAS  PubMed  Google Scholar 

  • Gershwin L-A, Richardson AJ, Winkel KD, Fenner PJ, Lippmann J, Hore R, Avila-Soria G, Brewer D, Kloser RJ, Steven A (2013) Biology and ecology of Irukandji jellyfish (Cnidaria: Cubozoa). Advances in marine biology. Elsevier, Amsterdam, pp 1–85

    Google Scholar 

  • Gibson R, Barnes M, Atkinson R (2001) Selective tidal-stream transport of marine animals. Oceanogr Mar Biol Annu Rev 39:305–353

    Google Scholar 

  • Gillanders BM, Able KW, Brown JA, Eggleston DB, Sheridan PF (2003) Evidence of connectivity between juvenile and adult habitats for mobile marine fauna: an important component of nurseries. Mar Ecol Prog Ser 247:281–295

    Google Scholar 

  • Gordon M, Seymour J (2012) Growth, development and temporal variation in the onset of six Chironex fleckeri medusae seasons: a contribution to understanding jellyfish ecology. PLoS ONE 7:e31277

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon M, Hatcher C, Seymour J (2004) Growth and age determination of the tropical Australian cubozoan Chiropsalmus sp. Hydrobiologia 530:339–345

    Google Scholar 

  • Harris RP (1988) Interactions between diel vertical migratory behavior of marine zooplankton and the subsurface chlorophyll maximum. Bull Mar Sci 43:663–674

    Google Scholar 

  • Hays GC (2003) A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Migrations and dispersal of marine organisms. Springer, Berlin, pp 163–170

    Google Scholar 

  • Heath M, Henderson E, Baird D (1988) Vertical distribution of herring larvae in relation to physical mixing and illumination. Mar Ecol Prog Ser 47:211–228

    Google Scholar 

  • Horner TJ, Kinsley CW, Nielsen SG (2015) Barium-isotopic fractionation in seawater mediated by barite cycling and oceanic circulation. Earth Planet Sci Lett 430:511–522

    CAS  Google Scholar 

  • Ikeda Y, Arai N, Sakamoto W, Kodokoro H, Yoshida K (1998) Microchemistry of the statoliths of the Japanese common squid Todarodes pacificus with special reference to its relation to the vertical temperature profiles of squid habitat. Fish Sci 64:179–184

    CAS  Google Scholar 

  • Jacquet S, Dehairs F, Rintoul S (2004) A high resolution transect of dissolved barium in the Southern Ocean. Geophys Res Lett. https://doi.org/10.1029/2004GL020016

    Article  Google Scholar 

  • Karl DM, Lukas R (1996) The Hawaii Ocean Time-series (HOT) program: background, rationale and field implementation. Deep Sea Res (2 Top Stud Oceangr) 43:129–156

    CAS  Google Scholar 

  • Kawamura M, Ueno S, Iwanaga S, Oshiro N, Kubota S (2003) The relationship between fine rings in the statolith and growth of the cubomedusa Chiropsalmus quadrigatus (Cnidaria: Cubozoa) from Okinawa Island, Japan. Plankton Biol Ecol 50:37–42

    Google Scholar 

  • Kingsford MJ, Mooney CJ (2014) The ecology of box jellyfishes (Cubozoa). Jellyfish blooms. Springer, Berlin, pp 267–302

    Google Scholar 

  • Kingsford MJ, Leis JM, Shanks A, Lindeman KC, Morgan SG, Pineda J (2002) Sensory environments, larval abilities and local self-recruitment. Bull Mar Sci 70:309–340

    Google Scholar 

  • Lawley JW, Ames CL, Bentlage B, Yanagihara A, Goodwill R, Kayal E, Hurwitz K, Collins AG (2016) Box jellyfish Alatina alata has a circumtropical distribution. Biol Bull 231:152–169

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis C, Bentlage B, Yanagihara A, Gillan W, Van Blerk J, Keil DP, Bely AE, Collins AG (2013) Redescription of Alatina alata (Reynaud, 1830) (Cnidaria: Cubozoa) from Bonaire, Dutch Caribbean. Zootaxa 3737:473

    PubMed  PubMed Central  Google Scholar 

  • Little M, Pereira P, Carrette T, Seymour J (2006) Jellyfish responsible for Irukandji syndrome. J Assoc Phys 99:425–427

    CAS  Google Scholar 

  • Lobel P, Robinson A (1986) Transport and entrapment of fish larvae by ocean mesoscale eddies and currents in Hawaiian waters. Deep Sea Res Pt A 33:483–500

    Google Scholar 

  • Lobel PS, Robinson AR (1988) Larval fishes and zooplankton in a cyclonic eddy in Hawaiian waters. J Plankton Res 10:1209–1223

    Google Scholar 

  • McCulloch MT, Gagan MK, Mortimer GE, Chivas AR, Isdale PJ (1994) A high-resolution Sr/Ca and δ18O coral record from the Great Barrier Reef, Australia, and the 1982–1983 El Niño. Geochim Cosmochim Acta 58:2747–2754

    CAS  Google Scholar 

  • McCulloch M, Cappo M, Aumend J, Müller W (2005) Tracing the life history of individual barramundi using laser ablation MC-ICP-MS Sr-isotopic and Sr/Ba ratios in otoliths. Mar Freshw Res 56:637–644

    CAS  Google Scholar 

  • Menéndez MC, Piccolo MC, Hoffmeyer MS (2012) Short-term variability on mesozooplankton community in a shallow mixed estuary (Bahía Blanca, Argentina): influence of tidal cycles and local winds. Estuar Coast Shelf Sci 112:11–22

    Google Scholar 

  • Mooney C, Kingsford M (2012) Sources and movements of Chironex fleckeri medusae using statolith elemental chemistry. Jellyfish blooms IV. Springer, Berlin, pp 269–277

    Google Scholar 

  • Mooney CJ, Kingsford MJ (2016) The influence of salinity on box jellyfish (Chironex fleckeri, Cubozoa) statolith elemental chemistry. Mar Biol 163:103

    Google Scholar 

  • Morrissey SJ, Schlaefer JA, Kingsford MJ (2020) Experimental validation of the relationships between cubozoan statolith elemental chemistry and salinity and temperature. J Exp Mar Biol Ecol 527:151375

    Google Scholar 

  • Seymour JE, Carrette TJ, Sutherland PA (2004) Do box jellyfish sleep at night? Med J Aust 181:706

    Google Scholar 

  • Shen C-C, Lee T, Chen C-Y, Wang C-H, Dai C-F, Li L-A (1996) The calibration of D [Sr/Ca] versus sea surface temperature relationship for Porites corals. Geochim Cosmochim Acta 60:3849–3858

    CAS  Google Scholar 

  • Sih TL, Cappo M, Kingsford M (2017) Deep-reef fish assemblages of the Great Barrier Reef shelf-break (Australia). Sci Rep 7:10886

    PubMed  PubMed Central  Google Scholar 

  • Sinclair M, Iles T (1989) Population regulation and speciation in the oceans. ICES J Mar Sci 45:165–175

    Google Scholar 

  • Sinclair DJ, McCulloch MT (2004) Corals record low mobile barium concentrations in the Burdekin River during the 1974 flood: evidence for limited Ba supply to rivers? Palaeogeogr Palaeoclimatol Palaeoecol 214:155–174

    Google Scholar 

  • Stern SJ (2009) Migration and movement patterns. Encyclopedia of marine mammals. Elsevier, Amsterdam, pp 726–730

    Google Scholar 

  • Strzelecki J, Koslow J, Waite A (2007) Comparison of mesozooplankton communities from a pair of warm-and cold-core eddies off the coast of Western Australia. Deep Sea Res (2 Top Stud Oceaogr) 54:1103–1112

    Google Scholar 

  • Tabouret H, Bareille G, Claverie F, Pécheyran C, Prouzet P, Donard O (2010) Simultaneous use of strontium: calcium and barium: calcium ratios in otoliths as markers of habitat: application to the European eel (Anguilla anguilla) in the Adour basin, South West France. Mar Environ Res 70:35–45

    CAS  PubMed  Google Scholar 

  • Thorrold SR, Jones GP, Hellberg ME, Burton RS, Swearer SE, Neigel JE, Morgan SG, Warner RR (2002) Quantifying larval retention and connectivity in marine populations with artificial and natural markers. Bull Mar Sci 70:291–308

    Google Scholar 

  • Ueno S, Imai C, Mitsutani A (1995) Fine growth rings found in statolith of a cubomedusa Carybdea rastoni. J Plankton Res 17:1381–1384

    Google Scholar 

  • Underwood AJ, Underwood AJ, Wnderwood A (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. CUP, Cambridge

    Google Scholar 

  • Walther B, Limburg K (2012) The use of otolith chemistry to characterize diadromous migrations. J Fish Biol 81:796–825

    CAS  PubMed  Google Scholar 

  • Walther BD, Kingsford MJ, McCulloch MT (2013) Environmental records from Great Barrier Reef corals: Inshore versus offshore drivers. PLoS ONE 8:e77091

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wolanski E, Delesalle B (1995) Upwelling by internal waves, Tahiti, French Polynesia. Cont Shelf Res 15:357–368

    Google Scholar 

  • Woodhead JD, Hellstrom J, Hergt JM, Greig A, Maas R (2007) Isotopic and elemental imaging of geological materials by laser ablation inductively coupled plasma-mass spectrometry. Geostand Geoanal Res 31:331–343

    CAS  Google Scholar 

  • Yoshimoto CM, Yanagihara AA (2002) Cnidarian (coelenterate) envenomations in Hawai'i improve following heat application. Trans R Soc Trop Med Hyg 96:300–303

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Yi Hu at AAC for assistance with LA-ICPMS and Mark O’Callaghan for added assistance. The authors also thank the reviewers for commenting on drafts of this manuscript. This project was supported by funding from the ARC Centre of Excellence for Coral Reef Studies to MJK.

Author information

Authors and Affiliations

  1. College of Science and Engineering, James Cook University, Townsville, QLD, 4811, Australia

    Scott J. Morrissey & Michael J. Kingsford

  2. Department of Tropical Medicine, Medical Microbiology and Pharmacology, John A. Burns School of Medicine, University of Hawaii at Mānoa, Honolulu, HI, 96822, USA

    Angel A. Yanagihara

  3. ARC Centre of Excellence for Coral Reef Studies, Townsville, QLD, 4811, Australia

    Michael J. Kingsford

Authors
  1. Scott J. Morrissey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angel A. Yanagihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael J. Kingsford
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Scott J. Morrissey.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interests.

Human and animals rights statement

All applicable international, national and/or institutional guidelines for sampling, care and experimental use of organisms for the study have been followed and all necessary approvals have been obtained.

Additional information

Responsible Editor: A. Checa.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Reviewed by undisclosed experts.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morrissey, S.J., Yanagihara, A.A. & Kingsford, M.J. Utility of statolith elemental chemistry as a proxy for temperature to elucidate the movements of the Irukandji jellyfish species Alatina alata. Mar Biol 167, 134 (2020). https://doi.org/10.1007/s00227-020-03752-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-020-03752-4

Search

Navigation