SpringerLink
Log in

Significance of otolith calcium carbonate crystal structure diversity to microchemistry studies

  • Reviews
  • Published:
Reviews in Fish Biology and Fisheries Aims and scope Submit manuscript

Abstract

Otoliths, calcium carbonate (CaCO3) ear stones of fish, contain a wealth of information about fish life and environmental history yet the CaCO3 polymorph form the otolith is made of is a critical, but seldom considered, piece of information during otolith analysis. Otolith trace element chemistry data increasingly informs management decisions, but recent work has shown that CaCO3 polymorphs—aragonite, vaterite, and calcite—can bear on incorporation of trace elements in a non-trivial way. Most fishes are thought to have otoliths of the aragonite CaCO3 form, but this construct is potentially outdated with many recent literature reports showing otherwise. Our study used previously unpublished neutron diffraction data and reports from published literature to address three objectives: (1) summarize the relative effects of otolith CaCO3 polymorphism on otolith microchemistry, (2) summarize reports of otolith polymorphs to gain a better understanding of the extent of non-aragonite otoliths among fishes, (3) outline future research needed to align interpretations of microchemistry with our current understanding of otolith polymorph diversity. We found that while aragonite otoliths are the most common, so are exceptions. For example, the ostensibly rare (among species) CaCO3 form vaterite was reported in at least some otoliths of 40% of the species surveyed. Our work suggests that examination of the CaCO3 polymorph composition of otoliths should become more common particularly in studies where results will or may be used to inform management decisions. Future research should work to attribute controls on otolith CaCO3 polymorph expression using a combination of -omics and material characterization approaches to enrich the life history and environmental information output from otoliths and increase our understanding of the assumptions made in otolith trace element chemistry studies.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

References

  • Becker BJ, Fodrie FJ, McMillan PA, Levin LA (2005) Spatial and temporal variation in trace elemental fingerprints of mytilid mussel shells: a precursor to invertebrate larval tracking. Limnol Oceanogr 50:48–61

    Article  CAS  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2009) GenBank. Nucleic Acids Res 37(Database issue):D26–D31 Epub 2008 Oct 21

    Article  CAS  PubMed  Google Scholar 

  • Borelli G, Guibbolini ME, Mayer-Gostan N, Priouzeau F, De Pontual H, Allemand D, Puverel S, Tambutte E, Payan P (2003) Daily variations of endolymph composition: relationship with the otolith calcification process in trout. J Exp Biol 206:2685–2692

    Article  CAS  PubMed  Google Scholar 

  • Bowen CA, Bronte CR, Argyle RL, Adams JV, Johnson JE (1999) Vateritic sagitta in wild and stocked lake trout: applicability to stock origin. Trans Am Fish Soc 128:929–938

    Article  Google Scholar 

  • Brandenberger E, Schintz HR (1945) Vtber die Natur der Verkalkungen bei Mensch und Tier und das Verhalten der anorganischen Knochensubstanz im Falle der haupt-sachlichen menschlichen Knochenkrankheiten. Helv Med Acta Suppl 16:1–63

    Google Scholar 

  • Brophy D, Jeffries TE, Danilowicz BS (2004) Elevated manganese concentrations at the cores of clupeid otoliths: possible environmental, physiological, or structural origins. Mar Biol 144:779–786

    Article  CAS  Google Scholar 

  • Brown RJ, Severin KP (2009) Otolith chemistry analyses indicate that water Sr: Ca is the primary factor influencing otolith Sr: Ca for freshwater and diadromous fish but not for marine fish. Can J Fish Aquat Sci 66(10):1790–1808

    Article  CAS  Google Scholar 

  • Brown AD, Sisneros JA, Jurasin T, Nguyen C, Coffin AB (2013) Differences in lateral line morphology between hatchery-and wild-origin steelhead. PLoS ONE 8:e59162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campana SE (1983) Feeding periodicity and the production of daily growth increments in otoliths of steelhead trout (Salmo gairdneri) and starry flounder (Platichthys stellatus). Can J Zool 61:1591–1597

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Carlström D (1963) A crystallographic study of vertebrate otoliths. Biol Bull 125:441–463

    Article  Google Scholar 

  • Casselman JM (1990) Growth and relative size of calcified structures of fish. Trans Am Fish Soc 119:673–688

    Article  Google Scholar 

  • Chakoumakos BC, Pracheil BM, Koenigs RP, Bruch RM, Feygenson M (2016) Empirically testing vaterite structural models using neutron diffraction and thermal analysis. Sci Rep 6:36799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chesney EJ, McKee BM, Blanchard T, Chan LH (1998) Chemistry of otoliths from juvenile menhaden Brevoortia patronus: evaluating strontium, strontium: calcium and strontium isotope ratios as environmental indicators. Mar Ecol Prog Ser 171:261–273

    Article  CAS  Google Scholar 

  • Ciccarelli FD, Doerks T, Von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287

    Article  CAS  PubMed  Google Scholar 

  • David AW, Grimes CB, Isely JJ (1994) Vaterite sagittal otoliths in hatchery-reared juvenile red drums. Prog Fish Cult 56:301–303

    Article  Google Scholar 

  • de Vries MC, Gillanders BM, Elsdon TS (2005) Facilitation of barium uptake into fish otoliths: influence of strontium concentration and salinity. Geochim Cosmochim Acta 69:4061–4072

    Article  CAS  Google Scholar 

  • Degens ET, Deuser WG, Haedrich RL (1969) Molecular structure and composition of fish otoliths. Mar Biol 2:105–113

    Article  CAS  Google Scholar 

  • Espino-Barr E, Gallardo-Cabello M, Cabral-Solís EG, Garcia-Boa A, Puente-Gómez M (2015) Analysis of the otoliths sagitta, asteriscus and lapillus of Yellowfin Mojarra Gerres cinereus (Perciformes: Gerreidae) in the coast of Colima and Jalisco, Mexico. Open J Ocean Coast Sci 2:18–33

    Article  Google Scholar 

  • Falini G, Fermani S, Vanzo S, Miletic M, Zaffino G (2005) Influence on the formation of aragonite or vaterite by otolith macromolecules. Eur J Inorg Chem 2005:162–167

    Article  CAS  Google Scholar 

  • Falini G, Fermani S, Reggi M, Džakula BN, Kralj D (2014) Evidence of structural variability among synthetic and biogenic vaterite. ChemComm 50:15370–15373

    CAS  Google Scholar 

  • Federhen S (2011) The NCBI taxonomy database. Nucleic Acids Res 40:D136–D143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gauldie RW (1986) Vaterite otoliths from chinook salmon (Oncorhynchus tshawytscha). New Zeal J Fresh 20:209–217

    Article  CAS  Google Scholar 

  • Gauldie RW (1990) Vaterite otoliths from the opah, Lampris immaculatus, and two species of sunfish, Mola mola and M. ramsayi. Acta Zool 71:193–199

    Article  Google Scholar 

  • Gauldie RW (1993) Polymorphic crystalline structure of fish otoliths. J Morphol 218:1–28

    Article  CAS  PubMed  Google Scholar 

  • Gauldie RW (1996) Effects of temperature and vaterite replacement on the chemistry of metal ions in the otoliths of Oncorhynchus tshawytscha. Can J Fish Aquat Sci 53:2015–2026

    Article  CAS  Google Scholar 

  • Gauldie RW, Dunlop D, Tse J (1986) The remarkable lungfish otolith. New Zeal J Fresh 20:81–92

    Article  Google Scholar 

  • Gauldie RW, Sharma SK, Volk E (1997) Micro-Raman spectral study of vaterite and aragonite otoliths of the coho salmon, Oncorhynchus kisutch. Comp Biochem Physiol Part A Physiol 118:753–757

    Article  Google Scholar 

  • Halden NM, Friedrich LA (2008) Trace-element distributions in fish otoliths: natural markers of life histories, environmental conditions and exposure to tailings effluence. Mineral Mag 72:593–605

    Article  CAS  Google Scholar 

  • Hsu CC, Chang CW, Iizuka Y, Tzeng WN (2009) A growth check deposited at estuarine arrival in otoliths of juvenile flathead mullet (Mugil cephalus L.). Zool Stud 48:315–324

    Google Scholar 

  • Immerman F (1908) Beitrage zur Altersbestimmung der Fische II Die innere Struktur der Schollenotolithen. Wiss Meeresuntersuch Abt Helgoland N F 8:129–176

    Google Scholar 

  • Irie T (1955) The crystal texture of the otolith of a marine teleost. Pseudosciaena J Fac Fish Anim Husb Hiroshima Univ 1:1–8

    CAS  Google Scholar 

  • Jessop BM, Shiao JC, Iizuka Y, Tzeng WN (2002) Migratory behaviour and habitat use by American eels Anguilla rostrata as revealed by otolith microchemistry. Mar Ecol Prog Ser 233:217–229

    Article  Google Scholar 

  • Johansson G (1966) Contribution to the biology of the dab (Limanda limanda L.) in Icelandic waters. Rit Fiskideildar 4:18–23

    Google Scholar 

  • Larson AC, Von Dreele RB (2000) Report LAUR 86-748 Los Alamos National Laboratory, New Mexico, USA

  • Lenaz D, Miletic M, Pizzul E, Vanzo S, Adami G (2006) Mineralogy and geochemistry of otoliths in freshwater fish from Northern Italy. Eur J Mineral 18:143–148

    Article  CAS  Google Scholar 

  • Limburg KE, Elfman M (2017) Insights from two-dimensional map** of otolith chemistry. J Fish Biol 90:480–491

    Article  CAS  PubMed  Google Scholar 

  • Limburg KE, Wuenschel MJ, Hüssy K, Heimbrand Y, Samson M (2018) Making the otolith magnesium chemical calendar-clock tick: plausible mechanism and empirical evidence. Rev Fish Sci Aquac 26:479–493

    Article  Google Scholar 

  • Loeppky AR, Chakoumakos BC, Pracheil BM, Anderson WG (2019) Otoliths of sub-adult Lake Sturgeon, Acipenser fulvescens, contain aragonite and vaterite calcium carbonate polymorphs. Fish Biol. https://doi.org/10.1111/jfb.13951

    Article  Google Scholar 

  • Long JM, Grabowski TB (2017) Otoliths. In: Quist MC, Isermann D (eds) Age and growth of fishes: principles and techniques. American Fisheries Society, Bethesda, pp 189–219

    Google Scholar 

  • Macdonald JI, McNeil DG, Crook DA (2012) Asteriscus v. lapillus: comparing the chemistry of two otolith types and their ability to delineate riverine populations of common carp Cyprinus carpio. J Fish Biol 81:1715–1729

    Article  CAS  PubMed  Google Scholar 

  • Maisey JG (1987) Notes on the structure and phylogeny of vertebrate otoliths. Copeia 1987:495–499

    Article  Google Scholar 

  • Melancon S, Fryer BJ, Ludsin SA, Gagnon JE, Yang Z (2005) Effects of crystal structure on the uptake of metals by lake trout (Salvelinus namaycush) otoliths. Can J Fish Aquat Sci 62:2609–2619

    Article  CAS  Google Scholar 

  • Melancon S, Fryer BJ, Markham JL (2009) Chemical analysis of endolymph and the growing otolith: fractionation of metals in freshwater fish species. Environ Toxicol Chem 28:1279–1287

    Article  CAS  PubMed  Google Scholar 

  • Morales-Nin BYO (1987) The influence of environmental factors on microstructure of otoliths of three demersal fish species caught off Namibia. S Afr J Mar Sci 5(1):255–262

    Article  Google Scholar 

  • Morat F, Betoulle S, Robert M, Thailly AF, Biagianti-Risbourg S, Lecomte-Finiger R (2008) What can otolith examination tell us about the level of perturbations of Salmonid fish from the Kerguelen Islands? Ecol Freshw Fish 17:617–627

    Article  Google Scholar 

  • Morris RW, Kittleman LR (1967) Piezoelectric property of otoliths. Science 158:368–370

    Article  CAS  PubMed  Google Scholar 

  • Morrongiello JR, Thresher RE, Smith DC (2012) Aquatic biochronologies and climate change. Nat Clim Change 2:849–857

    Article  Google Scholar 

  • Mugiya Y (1972) On aberrant sagittas of teleostan fishes. Jpn J Ichthyol 19:11–14

    Google Scholar 

  • Murray CB (1994) A method for preparing Chinook salmon otoliths for age determination, and evidence of its validity. Trans Am Fish Soc 123:358–367

    Article  Google Scholar 

  • Nolf D (1985) In: Schultze HP (ed) Otolith piscium, vol 10. Handbook of paleoichthyology. G. Fischer Verlag, Deutsch, pp 1–145

    Google Scholar 

  • Oliveira AM, Farina M, Ludka IP, Kachar B (1996) Vaterite, calcite, and aragonite in the otoliths of three species of piranha. Naturwissenschaften 83:133–135

    Article  CAS  Google Scholar 

  • Oxman DS, Barnett-Johnson R, Smith ME, Coffin A, Miller DL, Josephson R, Popper AN (2007) The effect of vaterite deposition on sound reception, otolith morphology, and inner ear sensory epithelia in hatchery-reared Chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 64:1469–1478

    Article  Google Scholar 

  • Palmork KH, Taylor MEU, Coates R (1963) Crystal structure of aberrant otoliths. Acta Chem Scand 17:1457

    Article  CAS  Google Scholar 

  • Paquette J, Reeder RJ (1995) Relationship between surface structure, growth mechanism, and trace element incorporation in calcite. Geochim Cosmochim Acta 59:735–749

    Article  CAS  Google Scholar 

  • Parmentier E, Cloots R, Warin R, Henrist C (2007) Otolith crystals (in Carapidae): growth and habit. J Struct Biol 159:462–473

    Article  CAS  PubMed  Google Scholar 

  • Pracheil BM, Hogan JD, Lyons J, McIntyre PB (2014) Using hard-part microchemistry to advance conservation and management of North American freshwater fishes. Fisheries 39:451–465

    Article  Google Scholar 

  • Pracheil BM, Chakoumakos BC, Feygenson M, Whitledge GW, Koenigs RP, Bruch RM (2017) Sturgeon and paddlefish (Acipenseridae) sagittal otoliths are composed of the calcium carbonate polymorphs vaterite and calcite. J Fish Biol 90(2):549–558

    Article  CAS  PubMed  Google Scholar 

  • Pracheil BM, Lyons J, Hamann EJ, Short PH, McIntyre PB (2019) Lifelong population connectivity between large rivers and their tributaries: a case study of shovelnose sturgeon from the Mississippi and Wisconsin rivers. Ecol Freshw Fish 28(1):20–32

    Article  Google Scholar 

  • Reimer T, Dempster T, Warren-Myers F, Jensen AJ, Swearer SE (2016) High prevalence of vaterite in sagittal otoliths causes hearing impairment in farmed fish. Sci Rep 6:25249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reimer T, Dempster T, Wargelius A, Fjelldal PG, Hansen T, Glover KA, Solberg MF, Swearer SE (2017) Rapid growth causes abnormal vaterite formation in farmed fish otoliths. J Exp Biol 220:2965–2969

    Article  PubMed  Google Scholar 

  • Ren D, Feng Q, Bourrat X (2013) The co-effect of organic matrix from carp otolith and microenvironment on calcium carbonate mineralization. Mater Sci Eng C 33:3440–3449

    Article  CAS  Google Scholar 

  • Rietveld H (1969) A profile refinement method for nuclear and magnetic structures. J Appl Crystallogr 2:65–71

    Article  CAS  Google Scholar 

  • Sasaki H, Miyata J (1954) Experimental study on otoliths. Yonago Acta Med 1:49

    CAS  Google Scholar 

  • Sayers EW, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Edgar R, Federhen S, Feolo M, Geer LY, Helmberg W, Kapustin Y, Landsman D, Lipman DJ, Madden TL, Maglott DR, Miller V, Mizrachi I, Ostell J, Pruitt KD, Schuler GD, Sequeira E, Sherry ST, Shumway M, Sirotkin K, Souvorov A, Starchenko G, Tatusova TA, Wagner L, Yaschenko E, Ye J (2009) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 37:D5–D15

    Article  CAS  PubMed  Google Scholar 

  • Schultze HP (1988) Notes on the structure and phylogeny of vertebrate otoliths. Copeia 1988:257–259

    Article  Google Scholar 

  • Schulz-Mirbach T, Ladich F, Plath M, Heß M (2018) Enigmatic ear stones: what we know about the functional role and evolution of fish otoliths. Biol Rev 94(2):457–482

    Article  PubMed  Google Scholar 

  • Secor DH, Dean JM, Laban EH (1992) Otolith removal and preparation for microstructural analysis. In: Stevenson DK, Campana SE (eds) Otolith micro-structure examination and analysis, vol 117. Canadian special publication of fisheries and aquatic sciences. Department of Fisheries and Oceans, Ottawa, pp 19–57

    Google Scholar 

  • Söllner C, Burghammer M, Busch-Nentwich E, Berger J, Schwarz H, Riekel C, Nicolson T (2003) Control of crystal size and lattice formation by starmaker in otolith biomineralization. Science 302:282–286

    Article  CAS  PubMed  Google Scholar 

  • Starrs D, Ebner BC, Fulton CJ (2016) All in the ears: unlocking the early life history biology and spatial ecology of fishes. Biol Rev 91:86–105

    Article  PubMed  Google Scholar 

  • Strong MB, Neilson JD, Hunt JJ (1986) Aberrant crystallization of pollock (Pollachius virens) otoliths. Can J Fish Aquat Sci 43:1457–1463

    Article  Google Scholar 

  • Sweeting RM, Beamish RJ, Noakes DJ, Neville CM (2003) Replacement of wild coho salmon by hatchery-reared coho salmon in the Strait of Georgia over the past three decades. N Am J Fish Manag 23:492–502

    Article  Google Scholar 

  • Sweeting RM, Beamish RJ, Neville CM (2004) Crystalline otoliths in teleosts: comparisons between hatchery and wild coho salmon (Oncorhynchus kisutch) in the Strait of Georgia. Rev Fish Biol Fish 14:361–369

    Article  Google Scholar 

  • Tabouret H, Bareille G, Claverie F, Pécheyran C, Prouzet P, Donard OFX (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

    Article  CAS  PubMed  Google Scholar 

  • Thomas OR, Swearer SE, Kapp EA, Peng P, Tonkin-Hill GQ, Papenfuss A, Roberts A, Bernard P, Roberts BR (2019) The inner ear proteome of fish. FEBS J286:66–81

    Article  CAS  Google Scholar 

  • Toby BH (2001) EXPGUI, a graphical user interface for GSAS. J Appl Crystallogr 34:210–213

    Article  CAS  Google Scholar 

  • Tohse H, Saruwatari K, Kogure T, Nagasawa H, Takagi Y (2009) Control of polymorphism and morphology of calcium carbonate crystals by a matrix protein aggregate in fish otoliths. Cryst Growth Des 9:4897–4901

    Article  CAS  Google Scholar 

  • Tomás J, Geffen AJ (2003) Morphometry and composition of aragonite and vaterite otoliths of deformed laboratory reared juvenile herring from two populations. J Fish Biol 63:1383–1401

    Article  Google Scholar 

  • Tzeng WN, Chang CW, Wang CH, Shiao JC, Iizuka Y, Yang YJ, Ložys L (2007) Misidentification of the migratory history of anguillid eels by Sr/Ca ratios of vaterite otoliths. Mar Ecol Prog Ser 348:285–295

    Article  CAS  Google Scholar 

  • Veinott GI, Porter TR, Nasdala L (2009) Using Mg as a proxy for crystal structure and Sr as an indicator of marine growth in vaterite and aragonite otoliths of aquaculture rainbow trout. Trans Am Fish Soc 138:1157–1165

    Article  CAS  Google Scholar 

  • Wang J, Becker U (2009) Structure and carbonate orientation of vaterite (CaCO3). Am Mineral 94:380–386

    Article  CAS  Google Scholar 

  • Watson JE (1964) Determining the age of young herring from their otoliths. Trans Am Fish Soc 93:11–20

    Article  Google Scholar 

  • Wilson RR Jr (1985) Depth-related changes in sagitta morphology in six macrourid fishes of the Pacific and Atlantic Oceans. Copeia 1985:1011–1017

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dan Daugherty for providing alligator gar otoliths, Allison Fortner for providing early manuscript comments, and Tony Lanzirotti and Matt Newville for providing beamline support for data generated at the Advanced Photon Source used in Fig. 3. This research used resources at the High Flux Isotope Reactor and Spallation Neutron Source, DOE Office of Science User Facilities operated by the Oak Ridge National Laboratory. Use of the Advanced Photon Source was supported by the U. S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under Contract No. DE-AC02-06CH11357. Funding was provided by a Laboratory Directed Research and Development Seed Award.

Author information

Authors and Affiliations

  1. Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA

    Brenda M. Pracheil & Robert George

  2. School of Informatics, Computing, and Cyber Systems, Northern Arizona University, Flagstaff, AZ, USA

    Robert George

  3. Neutron Scattering Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA

    Bryan C. Chakoumakos

Authors
  1. Brenda M. Pracheil
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert George
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bryan C. Chakoumakos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brenda M. Pracheil.

Additional information

Publisher's Note

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

Copyright Notice

This manuscript has been authored by employees of UT-Battelle, LLC, under contract DE-AC05-00OR22725 with the U.S. Department of Energy. Accordingly, the United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a non-exclusive, paid-up, irrevocable, world-wide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 10 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pracheil, B.M., George, R. & Chakoumakos, B.C. Significance of otolith calcium carbonate crystal structure diversity to microchemistry studies. Rev Fish Biol Fisheries 29, 569–588 (2019). https://doi.org/10.1007/s11160-019-09561-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11160-019-09561-3

Keywords

Search

Navigation