Skip to main content
Log in

New insights into oyster high-resolution hinge growth patterns

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

Abstract

While oyster shells are one of the most common mollusks used for the analysis of (paleo)environmental and (paleo)climatic records based on geochemical proxies, high-resolution growth rate changes still need to be determined. Promising previous works are restricted to small portions of shell sections due to difficulties in continuous growth increment revelation. Based on a mark and recapture experiment of Magallana gigas specimens reared in an intertidal area of Normandy (France) for 22 months, and a sclerochronological approach using cathodoluminescence microscopy, this study provides the longest high-resolution record of growth increments in oyster shells to date. Different growth patterns were identified likely related to the oyster age. After age 1 year, the formation of growth increments follows an expected tide-related model, leading to the mineralization of ~ 2 calcitic increments per day, together with growth rate changes at lunar and semi-lunar periodicities, and a seasonal trend with occasional growth breaks during winter when temperatures fall below ~ 6 °C. However, for oysters younger than 1 year, i.e., before reaching their sexual maturity, the growth increment analysis reveals unconventional patterns. In this case, oysters’ growth is associated with either a large number (~ 5) or less than one increment per day depending on the period. This pattern is also associated with frequent growth cessations, although the growth rate of the shell is high at this period. Our results illustrate that the high-resolution sclerochronological approach is required for accurate paleoenvironmental reconstructions based on oyster shells.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Audouin J (1962) Hydrologie de l’étang de Thau. Rev Trav Inst Pech Marit 26(2):5–104

    Google Scholar 

  • Barbin V (2013) Application of cathodoluminescence microscopy to recent and past biological materials: a decade of progress. Mineral Petrol 107(3):353–362

    Article  CAS  Google Scholar 

  • Barbin V, Schvoerer M (1997) Cathodoluminescence and geosciences. C R Acad Sci Paris 325:157–169

    Article  CAS  Google Scholar 

  • Barbin V, Ramseyer K, Elfman M (2008) Biological record of added manganese in seawater: a new efficient tool to mark in vivo growth lines in the oyster species Crassostrea gigas. Int J Earth Sci 97(1):193–199

    Article  CAS  Google Scholar 

  • Bayne BL, Newell RIE (1983) Physiological energetics of marine molluscs. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca: physiology, part 1. Academic Press, Cambridge, pp 407–415

    Google Scholar 

  • Belley R, Snelgrove PV, Archambault P, Juniper SK (2016) Environmental drivers of benthic flux variation and ecosystem functioning in Salish Sea and Northeast Pacific sediments. PloS 11(3):e0151110

    Article  Google Scholar 

  • Berthome JP, Prou J, Bodoy A (1986) Performances de croissance de l’huître creuse, Crassostrea gigas (Thunberg) dans le bassin d’élevage de Marennes-Oléron entre 1979 & 1982. Haliotis 15:183–192

    Google Scholar 

  • Bougeois L, de Rafelis M, Reichart GJ, de Nooijer LJ, Nicollin F, Dupont-Nivet G (2014) A high resolution study of trace elements and stable isotopes in oyster shells to estimate Central Asian Middle Eocene seasonality. Chem Geol 363:200–212

    Article  CAS  Google Scholar 

  • Bouin MN, Caniaux G, Traulle O, Legain D, Le Moigne P (2012) Long-term heat exchanges over a Mediterranean lagoon. J Geophys R Atmospheres 117(D23):1–18

    Google Scholar 

  • Brown JR (1988) Multivariate analyses of the role of environmental factors in seasonal and site-related growth variation in the Pacific oyster Crassostrea gigas. Mar Ecol Prog Ser 45(3):225–236

    Article  Google Scholar 

  • Brown JR, Hartwick EB (1988) Influences of temperature, salinity and available food upon suspended culture of the Pacific oyster, Crassostrea gigas: I Absolute and allometric growth. Aquaculture 70(3):231–251

    Article  Google Scholar 

  • Butler PG, Wanamaker AD Jr, Scourse JD, Richardson CA, Reynolds DJ (2013) Variability of marine climate on the North Icelandic Shelf in a 1357-year proxy archive based on growth increments in bivalve Arctica islandica. Palaeogeogr Palaeoclimatol Palaeoecol 373:141–151

    Article  Google Scholar 

  • Carter JG (1980) Guide to bivalve shell microstructures. In: Rhoads DC, Lutz RA (eds) Skeletal growth of aquatic organisms. Plenum Press, New York, pp 645–673

    Google Scholar 

  • Chauvaud L, Thouzeau G, Paulet YM (1998) Effects of environmental factors on the daily growth rate of Pecten maximus juveniles in the Bay of Brest (France). J Exp Mar Biol Ecol 227(1):83–111

    Article  Google Scholar 

  • Chauvaud L, Lorrain A, Dunbar RB, Paulet YM, Thouzeau G, Jean F, Guarini JM, Mucciarone D (2005) Shell of the Great Scallop Pecten maximus as a high frequency archive of paleoenvironmental change. Geochem Geophys Geosyst 6:1–34

    Article  Google Scholar 

  • Clark GR (2005) Daily growth lines in some living Pectens (Mollusca: Bivalvia), and some applications in a fossil relative: time and tide will tell. Palaeogeogr Palaeoclimatol Palaeoecol 228(1):26–42

    Article  Google Scholar 

  • Cloern JE (1991) Tidal stirring and phytoplankton bloom dynamics in an estuary. J Mar Res 49(1):203–221

    Article  Google Scholar 

  • de Rafelis M, Renard M, Emmanuel L, Durlet C (2000) Apport de la cathodoluminescence à la connaissance de la spéciation du manganèse dans les carbonates pélagiques. C R Acad Sci Paris 330:391–398

    Article  Google Scholar 

  • Dettman DL, Flessa KW, Roopnarine PD, Schöne BR, Goodwin DH (2004) The use of oxygen isotope variation in shells of estuarine mollusks as a quantitative record of seasonal and annual Colorado River discharge. Geochim Cosmochim Acta 68:1253–1263

    Article  CAS  Google Scholar 

  • Doldan MS, de Rafelis M, Kroeck MA, Pascual MS, Morsan EM (2018) Age estimation of the oyster Ostrea puelchana determined from the hinge internal growth pattern. Mar Biol 165:119

    Article  Google Scholar 

  • El Ali A, Barbin V, Calas G, Cervelle B, Ramseyer K, Bouroulec J (1993) Mn2+ activated luminescence in dolomite, calcite and magnesite: quantitative determination of manganese site distribution by EPR and CL spectroscopy. Chem Geol 104:189–202

    Article  CAS  Google Scholar 

  • Evans JW (1972) Tidal growth increments in the cockle Clinocardium nuttalli. Science 176:416–417

    Article  CAS  Google Scholar 

  • Füllenbach CS, Schöne BR, Shirai K, Takahata N, Ishida A, Sano Y (2017) Minute co-variations of Sr/Ca ratios and microstructures in the aragonitic shell of Cerastoderma edule (Bivalvia)—are geochemical variations at the ultra-scale masking potential environmental signals? Geochim Cosmochim Acta 205:256–271

    Article  Google Scholar 

  • Gangnery A, Chabirand J-M, Lagarde F, Le Gall P, Oheix J, Bacher C, Buestel D (2003) Growth model of the Pacific oyster, Crassostrea gigas, cultured in Thau Lagoon (Méditerranée, France). Aquaculture 2015:267–290

    Article  Google Scholar 

  • Ghil M, Allen RM, Dettinger MD, Ide K, Kondrashov D, Mann ME, Robertson A, Saunders A, Tian Y, Varadi F, Yiou P (2002) Advanced spectral methods for climatic time series. Rev Geophys 40:31–341

    Article  Google Scholar 

  • Goodwin DH, Flessa KW, Schöne BR, Dettman DL (2001) Cross-calibration of daily growth increments, stable isotope variation, and temperature in the gulf of California bivalve mollusk Chione cortezi: implications for paleoenvironmental analysis. Palaios 16:387–398

    Article  Google Scholar 

  • Goodwin DH, Schöne BR, Dettman DL (2003) Resolution and fidelity of oxygen isotopes as paleotemperature proxies in bivalves mollusk shells: models and observations. Palaios 18:110–125

    Article  Google Scholar 

  • Gröcke DR, Gillikin DP (2008) Advances in mollusc sclerochronology and sclerochemistry: tools for understanding climate and environment. Geo-Marine Lett 28:265–268

    Article  Google Scholar 

  • Hall S (1984) A multiple regression model of oyster growth. Fish Res 2:167–175

    Article  Google Scholar 

  • Harzhauser M, Piller WE, Müllegger S, Grunert P, Micheels A (2011) Changing seasonality patterns in Central Europe from Miocene Climate Optimum to Miocene Climate Transition deduced from the Crassostrea isotope archive. Glob Planet Change 76:77–84. https://doi.org/10.1016/j.gloplacha.2010.12.003

    Article  Google Scholar 

  • Higuera-Ruiz R, Elorza J (2009) Biometric, microstructural, and high-resolution trace element studies in Crassostrea gigas of Cantabria (Bay of Biscay, Spain): Anthropogenic and seasonal influences. Estuar Coast Shelf Sci 82(2):201–213

    Article  CAS  Google Scholar 

  • Hudson JH, Shinn EA, Halley RB, Lidz B (1976) Sclerochronology: a tool for interpreting past environments. Geology 4:361–364

    Article  Google Scholar 

  • Huyghe D, Lartaud F, Emmanuel L, Merle D, Renard M (2015) Palaeogene climate evolution in the Paris Basin from oxygen stable isotope (δ18O) compositions of marine molluscs. J Geol Soc 172(5):576–587

    Article  Google Scholar 

  • Ivany LC, Lohmann KC, Hasiuk F, Blacke DB, Glass A, Aronson RB, Moody RM (2008) Eocene climate record of a high southern latitude continental shelf: Seymour Island, Antarctica. Geol Soc Am Bull 120:659–678

    Article  CAS  Google Scholar 

  • Kirby MX, Soniat TM, Spero HJ (1998) Stable isotope sclerochronology of Pleistocene and Recent oyster shells (Crassostrea virginica). Palaios 13:560–569

    Article  Google Scholar 

  • Krantz DE, Williams DF, Jones DS (1987) Ecological and paleoenvironmental information using stable isotope profiles from living and fossil molluscs. Palaeogeogr Palaeoclimatol Palaeoecol 58(3–4):249–266

    Article  CAS  Google Scholar 

  • Langlet D, Alunno-Bruscia M, Rafélis M, Renard M, Roux M, Schein E, Buestel D (2006) Experimental and natural cathodoluminescence in the shell of Crassostrea gigas from Thau lagoon (France): ecological and environmental implications. Mar Ecol Prog Ser 317:143–156

    Article  Google Scholar 

  • Lartaud F, Langlet D, De Rafelis M, Emmanuel L, Renard M (2006) Description of seasonal rhythmicity in fossil oyster shells Crassostrea aginensis Tournouer, 1914 (Aquitanian) and Ostrea bellovacina Lamarck, 1806 (Thanetian). Cathodoluminescence and sclerochronological approaches. Geobios 39(6):845–852

    Article  Google Scholar 

  • Lartaud F, Chauvaud L, Richard J, Toulot A, Bollinger C, Testut L, Paulet YM (2010a) Experimental growth pattern calibration of Antarctic scallop shells (Adamussium colbecki, Smith 1902) to provide a biogenic archive of high-resolution records of environmental and climatic changes. J Exp Mar Bio Ecol 393(1):158–167

    Article  Google Scholar 

  • Lartaud F, de Rafélis M, Ropert M, Emmanuel L, Geairon P, Renard M (2010b) Mn labelling of living oysters: artificial and natural cathodoluminescence analyses as a tool for age and growth rate determination of C. gigas (Thunberg, 1793) shells. Aquaculture 300(1):206–217

    Article  Google Scholar 

  • Lartaud F, Emmanuel L, de Rafelis M, Ropert M, Labourdette N, Richardson CA, Renard M (2010c) A latitudinal gradient of seasonal temperature variation recorded in oyster shells from the coastal waters of France and The Netherlands. Facies 56:13–25

    Article  Google Scholar 

  • Le Guitton M, Soetaert K, Damsté JS, Middelburg JJ (2015) Biogeochemical consequences of vertical and lateral transport of particulate organic matter in the southern North Sea: a multiproxy approach. Estuar Coast Shelf Sci 165:117–127

    Article  Google Scholar 

  • Lietard C, Pierre C (2008) High-resolution isotopic records (δ18O and δ13C) and cathodoluminescence study of lucinid shells from methane seeps of the Eastern Mediterranean. Geo-Mar Lett 28(4):195–203

    Article  CAS  Google Scholar 

  • Lutz RA, Rhoads DC (1977) Anaerobiosis and a theory of growth line formation. Science 198(4323):1222–1227

    Article  CAS  Google Scholar 

  • Machel HG, Mason RA, Mariano AN, Mucci A (1991) Causes and emission of luminescence in calcite and dolomite, and their applications for studies of carbonates diagenesis. In: Barker CE, Kopp OC (eds) Luminescence microscopy: quantitative and qualitative aspects. SEPM 25: 9–25

  • Mahé K, Bellamy E, Lartaud F, de Rafélis M (2010) Calcein and manganese experiments for marking the shell of the common cockle (Cerastoderma edule): tidal rhythm validation of increments formation. Aquat Living Resour 23(3):239–245

    Article  Google Scholar 

  • Mary C, Pien S, Ropert M, Blin JL (2006) Rapport REMONOR, Résultats 2005. Issy-les-Moulineaux, Ifremer, p 67

    Google Scholar 

  • Meibom A, Mostefaoui S, Cuif JP, Dauphin Y, Houlbreque F, Dunbar R, Constantz B (2007) Biological forcing controls the chemistry of reef-building coral skeleton. Geophys Res Lett 34(2):1–5

    Article  Google Scholar 

  • Mitchell IM, Crawford CM, Rushton MJ (2000) Flat oyster (Ostrea angasi) growth and survival rates at Georges Bay, Tasmania (Australia). Aquaculture 191(4):309–321

    Article  Google Scholar 

  • Mouchi V, de Rafélis M, Lartaud F, Fialin M, Verrecchia E (2013) Chemical labelling of oyster shells used for time-calibrated high-resolution Mg/Ca ratios: a tool for estimation of past seasonal temperature variations. Palaeogeogr Palaeoclimatol Palaeoecol 373:66–74

    Article  Google Scholar 

  • Mouchi V, Briard J, Gaillot S, Argant T, Forest V, Emmanuel L (2018) Reconstructing environments of collection site from archaeological bivalve shells: case study from oysters (Lyon, France). J Archaeol Sci: Reports 21:1225–1235. https://doi.org/10.1016/j.jasrep.2017.10.025

    Article  Google Scholar 

  • Nedoncelle K, Lartaud F, de Rafélis M, Boulila S, Le Bris N (2013) A new method for high-resolution bivalve growth rate studies in hydrothermal environments. Mar Biol 160(6):1427–1439

    Article  CAS  Google Scholar 

  • Nedoncelle K, Lartaud F, Contreira Pereira L, Yücel M, Thurnherr AM, Mullineaux L, Le Bris N (2015) Bathymodiolus growth dynamics in relation to environmental fluctuations in vent habitats. Deep Sea Res I Oceanogr Res Pap 106:183–193

    Article  Google Scholar 

  • Ohno T (1989) Palaeotidal characteristics determined by micro-growth patterns in bivalves. Palaeontology 32(2):237–263

    Google Scholar 

  • Quayle DB (1988) Pacific oyster culture in British Columbia. Can Bull Fish Aquat Sci 218:241

    Google Scholar 

  • Richardson CA (1989) An analysis of the microgrowth bands in the shell of the common mussel Mytilus edulis. J Mar Biol Assoc UK 69(2):477–491

    Article  Google Scholar 

  • Richardson CA, Collis SA, Ekaratne K, Dare P, Key D (1993) The age determination and growth rate of the European flat oyster, Ostrea edulis, in British waters determined from acetate peels of umbo growth lines. ICES J Mar Sci 50(4):493–500

    Article  Google Scholar 

  • Rodland DL, Schöne BR, Helema S, Nielsen JK, Baier S (2006) A clockwork mollusc: ultradian rhythms in bivalve activity revealed by digital photography. J Exp Mar Bio Ecol 334:316–323

    Article  Google Scholar 

  • Ropert M, Pien S, Mary C, Bouchaud B (2007) Rapport REMONOR, Résultats 2006. Issy-les-Moulineaux, Ifremer, p 70

    Google Scholar 

  • Salvi D, Mariottini P (2017) Molecular taxonomy in 2D: a novel ITS2 rRNA sequence–structure approach guides the description of the oysters’ subfamily Saccostreinae and the genus Magallana (Bivalvia: Ostreidae). Zool J Linnean Soc 179:263–276

    Google Scholar 

  • Schöne BR (2008) The curse of physiology—challenges and opportunities in the interpretation of geochemical data from mollusk shells. Geo-Mar Lett 28(5):269–285

    Article  Google Scholar 

  • Schöne B (2013) Arctica islandica (Bivalvia): a unique paleoenvironmental archive of the northern North Atlantic Ocean. Global Planet Change 111:199–225

    Article  Google Scholar 

  • Schöne BR, Giere O (2005) Growth increments and stable isotope variation in shells of the deep-sea hydrothermal vent bivalve mollusk Bathymodiolus brevior from the North Fiji Basin. Pacific Deep Sea Res 1 Oceanogr Res Pap 52(10):1896–1910

    Article  Google Scholar 

  • Schöne BR, Surge D (2005) Looking back over skeletal diaries -high-resolution environmental reconstructions from accretionary hard parts of aquatic organisms. Palaeogeogr Palaeoclimatol Palaeoecol 228:1–191

    Article  Google Scholar 

  • Schöne BR, Lega J, Flessa KW, Goodwin DH, Dettman DL (2002a) Reconstructing daily temperatures from growth rates of the intertidal bivalve mollusk Chione cortezi (northern Gulf of California, Mexico). Palaeogeogr Palaeoclimatol Palaeoecol 184(1):131–146

    Article  Google Scholar 

  • Schöne BR, Goodwin DH, Flessa KW, Dettman DL, Roopnarine PD (2002b) Sclerochronology and growth of the bivalve molluscs Chione (Chionista) fluctifraga and Chione (Chionista) cortezi in the northern Gulf of California, Mexico. Veliger 45:45–54

    Google Scholar 

  • Schöne BR, Oschmann W, Rössler J, Freyre Castro AD, Houk SD, Kröncke I, Dreyer W, Janssen R, Rumohr H, Dunca E (2003) North Atlantic oscillation dynamics recorded in shells of a long-lived bivalve mollusk. Geology 31:1237–1240

    Article  Google Scholar 

  • Schwartzmann C, Durrieu G, Sow M, Ciret P, Lazareth CE, Massabuau JC (2011) In situ clam growth rate behavior in relation to temperature: a one-year coupled study of high-frequency noninvasive valvometry and sclerochronology. Limnol Oceanogr 56:1940–1951

    Article  Google Scholar 

  • Scourse J, Richardson C, Forsythe G, Harris I, Heinemeier J, Fraser N, Briffa K, Jones P (2006) First cross-matched floating chronology from the marine fossil record: data from growth lines of the long-lived bivalve mollusc Arctica islandica. Holocene 16:967–974

    Article  Google Scholar 

  • Soletchnik P, Geairon P, Razet D, Goulletquer P (1996) Physiologie de la maturation et de la ponte chez l’huître creuse Crassostrea gigas. Rapport Ifremer, Issy-les-Moulineaux, pp 2–34

    Google Scholar 

  • Surge D, Lohmann KC (2008) Evaluating Mg/Ca ratios as a temperature proxy in the estuarine oyster, Crassostrea virginica. J Geophys Res Biogeosci 113(G2):1–9

    Article  Google Scholar 

  • Surge D, Lohmann KC, Dettman DL (2001) Controls on isotopic chemistry of the American oyster, Crassostrea virginica: implications for growth patterns. Palaeogeogr Palaeoclimatol Palaeoecol 172:283–296

    Article  Google Scholar 

  • Thomson DJ (1982) Spectrum estimation and harmonic analysis. Proc IEEE 70(9):1055–1096

    Article  Google Scholar 

  • Tran D, Nadau A, Durrieu G, Ciret P, Parisot JP, Massabuau JC (2011) Field chronobiology of a molluscan bivalve: how the moon and sun cycles interact to drive oyster activity rhythms. Chronobiol Int 28(4):307–317

    Article  Google Scholar 

  • Tynan S, Dutton A, Eggins S, Opdyke B (2014) Oxygen isotope records of the Australian flat oyster (Ostrea angasi) as a potential temperature archive. Mar Geol 357:195–209

    Article  CAS  Google Scholar 

  • Tynan S, Opdyke BN, Walczak M, Eggins S, Dutton A (2017) Assessment of Mg/Ca in Saccostrea glomerata (the Sydney rock oyster) shell as a potential temperature record. Palaeogeogr Palaeoclimatol Palaeoecol 484:79–88

    Article  Google Scholar 

  • Ullmann CV, Wiechert U, Korte C (2010) Oxygen isotope fluctuations in a modern North Sea oyster (Crassostrea gigas) compared with annual variations in seawater temperature: Implications for palaeoclimate studies. Chem Geol 277(1):160–166

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the ANR Amor ‘Data Model Reconstruction of the Cenozoic Climate’ and the BQR project from Sorbonne Université, ‘High frequency to very high frequency recordings of environmental changes to climate by biomineralization.’ Special thanks may be due to Brian Mitchell for improving the English of the manuscript. Thoughtful comments by Editor A. Checa and two anonymous reviewers helped to improve the original version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Franck Lartaud.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huyghe, D., de Rafelis, M., Ropert, M. et al. New insights into oyster high-resolution hinge growth patterns. Mar Biol 166, 48 (2019). https://doi.org/10.1007/s00227-019-3496-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-019-3496-2

Navigation