Tracing timing of growth in cultured molluscs using strontium spiking

Introduction Growth experiments present a powerful tool for determining the effect of environmental parameters on growth and carbonate composition in biogenic calcifiers. For successful proxy calibration and biomineralization studies, it is vital to identify volumes of carbonate precipitated by these organisms at precise intervals during the experiment. Here, we investigate the use of strontium labelling in mollusc growth experiments. Methods Three bivalve species (Cerastoderma edule, Mytilus edulis and Ostrea edulis) were grown under monitored field conditions. The bivalves were regularly exposed to seawater with elevated concentrations of dissolved strontium chloride (SrCl2). In addition, the size of their shells was determined at various stages during the experiment using calliper measurements and digital photography. Trace element profiles were measured in cross sections through the shells of these molluscs using laser ablation ICPMS and XRF techniques. Results Our results show that doses of dissolved strontium equivalent to 7-8 times the background marine value (~0.6 mmol/L) are sufficient to cause reproducible peaks in shell-incorporated strontium in C. edule and M. edulis shells. No negative effects were observed on shell calcification rates. Lower doses (3-5 times background values) resulted in less clearly identifiable peaks, especially in M. edulis. Strontium spiking labels in shells of O. edulis are more difficult to detect, likely due to their irregular growth. Discussion Strontium spiking is a useful technique for creating time marks in cultured shells and a reproducible way to monitor shell size during the growing season while limiting physical disturbance of the animals. However, accurate reconstructions of growth rates at high temporal resolution require frequent spiking with high doses of strontium.

[1]  M. Ziegler,et al.  Temperature Dependence of Clumped Isotopes (∆47) in Aragonite , 2022, Geophysical research letters.

[2]  G. Haug,et al.  Enhanced ocean oxygenation during Cenozoic warm periods , 2022, Nature.

[3]  R. Posenato,et al.  Microstructures and sclerochronology of exquisitely preserved lower Jurassic lithiotid bivalves: Paleobiological and paleoclimatic significance , 2022, Palaeogeography, Palaeoclimatology, Palaeoecology.

[4]  G. Reichart,et al.  New Calcium Carbonate Nano‐particulate Pressed Powder Pellet (NFHS‐2‐NP) for LA‐ICP‐OES, LA‐(MC)‐ICP‐MS and µXRF , 2022, Geostandards and Geoanalytical Research.

[5]  J. Jagt,et al.  A new age model and chemostratigraphic framework for the Maastrichtian type area (southeastern Netherlands, northeastern Belgium) , 2022, Newsletters on Stratigraphy.

[6]  M. Ziegler,et al.  Warm deep-sea temperatures across Eocene Thermal Maximum 2 from clumped isotope thermometry , 2022, Communications Earth & Environment.

[7]  J. Thébault,et al.  Ba/Ca profiles in shells of Pecten maximus – A proxy for specific primary producers rather than bulk phytoplankton , 2022, Chemical Geology.

[8]  J. Middelburg,et al.  High precipitation rates characterize biomineralization in the benthic foraminifer Ammonia beccarii , 2021, Geochimica et Cosmochimica Acta.

[9]  M. Ziegler,et al.  Multi-isotopic and trace element evidence against different formation pathways for oyster microstructures , 2021 .

[10]  Douglas S. Jones,et al.  Fossil bivalves and the sclerochronological reawakening , 2021, Paleobiology.

[11]  P. Boudry,et al.  Sustainable large‐scale production of European flat oyster ( Ostrea edulis ) seed for ecological restoration and aquaculture: a review , 2021, Reviews in Aquaculture.

[12]  G. Engelhard,et al.  Ostrea edulis beds in the central North Sea: delineation, ecology, and restoration , 2020 .

[13]  P. Reimus,et al.  Mobility of Radionuclides in Fractured Carbonate Rocks: Lessons from a Field-Scale Transport Experiment , 2020, Environmental science & technology.

[14]  D. Sumner,et al.  Structure and distribution of chalky deposits in the Pacific oyster using x-ray computed tomography (CT) , 2020, Scientific Reports.

[15]  C. Powell,et al.  Effective Attenuation Lengths for Different Quantitative Applications of X-ray Photoelectron Spectroscopy , 2020, Journal of Physical and Chemical Reference Data.

[16]  Gabriel V. Markov,et al.  Biological rhythms in the deep-sea hydrothermal mussel Bathymodiolus azoricus , 2020, Nature Communications.

[17]  K. Maruyama,et al.  Incorporation of Incompatible Strontium and Barium Ions into Calcite (CaCO3) through Amorphous Calcium Carbonate , 2020, Minerals.

[18]  H. Synal,et al.  Unravelling 5 decades of anthropogenic 236U discharge from nuclear reprocessing plants. , 2020, The Science of the total environment.

[19]  S. Verheyden,et al.  Benchtop μXRF as a tool for speleothem trace elemental analysis: Validation, limitations and application on an Eemian to early Weichselian (125–97 ka) stalagmite from Belgium , 2020, Palaeogeography, Palaeoclimatology, Palaeoecology.

[20]  G. Haug,et al.  Nano‐Powdered Calcium Carbonate Reference Materials: Significant Progress for Microanalysis? , 2019, Geostandards and Geoanalytical Research.

[21]  D. Nikolayev,et al.  Experimental neutron pole figures of minerals composing the bivalve mollusc shells , 2019, SN Applied Sciences.

[22]  M. Renard,et al.  New insights into oyster high-resolution hinge growth patterns , 2019, Marine Biology.

[23]  D. Arizteguí,et al.  High-resolution palaeohydrological reconstruction of central Italy during the Holocene , 2019, The Holocene.

[24]  B. Schöne,et al.  Environmental and biological factors influencing trace elemental and microstructural properties of Arctica islandica shells. , 2018, The Science of the total environment.

[25]  Alison R. Taylor,et al.  Calcein Staining as a Tool to Investigate Coccolithophore Calcification , 2018, Front. Mar. Sci..

[26]  J. Erez,et al.  Insights on the interaction of calcein with calcium carbonate and its implications in biomineralization studies , 2018, 2001.03037.

[27]  Sharon L. Grim,et al.  Environmental and Biological Influences on Carbonate Precipitation Within Hot Spring Microbial Mats in Little Hot Creek, CA , 2018, Front. Microbiol..

[28]  B. Passey,et al.  Temperature evolution and the oxygen isotope composition of Phanerozoic oceans from carbonate clumped isotope thermometry , 2018 .

[29]  B. Schöne,et al.  Determining seasonality of mussel collection from an early historic Inuit site, Labrador, Canada: Comparing thin-sections with high-resolution stable oxygen isotope analysis , 2018, Journal of Archaeological Science: Reports.

[30]  D. Benavente,et al.  Impact of salt and frost weathering on the physical and durability properties of travertines and carbonate tufas used as building material , 2018, Environmental Earth Sciences.

[31]  A. Jamieson,et al.  Life history of abyssal and hadal fishes from otolith growth zones and oxygen isotopic compositions , 2017 .

[32]  F. Vanhaecke,et al.  Tropical seasonality in the late Campanian (late Cretaceous): Comparison between multiproxy records from three bivalve taxa from Oman , 2017 .

[33]  B. Schöne,et al.  Reproducibility of trace element time-series (Na/Ca, Mg/Ca, Mn/Ca, Sr/Ca, and Ba/Ca) within and between specimens of the bivalve Arctica islandica - A LA-ICP-MS line scan study , 2017 .

[34]  Kenji Kawamura,et al.  A global multiproxy database for temperature reconstructions of the Common Era , 2017, Scientific Data.

[35]  P. Claeys,et al.  Trace element analyses of carbonates using portable and micro-X-ray fluorescence: performance and optimization of measurement parameters and strategies , 2017 .

[36]  Shanshan Zhou,et al.  Experimental evaluation of fluorescent (alizarin red S and calcein) and clip-tag markers for stock assessment of ark shell, Anadara broughtonii , 2017, Chinese Journal of Oceanology and Limnology.

[37]  P. Claeys,et al.  Micro X‐ray fluorescence (μXRF) line scanning on Cretaceous rudist bivalves: A new method for reproducible trace element profiles in bivalve calcite , 2017 .

[38]  D. Hoffmann,et al.  Determination of aragonite trace element distribution coefficients from speleothem calcite–aragonite transitions , 2016 .

[39]  B. Schöne,et al.  Strontium/lithium ratio in aragonitic shells of Cerastoderma edule (Bivalvia) — A new potential temperature proxy for brackish environments , 2015 .

[40]  S. Eggins,et al.  Optimizing LA-ICP-MS analytical procedures for elemental depth profiling of foraminifera shells , 2015 .

[41]  D. Merle,et al.  Palaeogene climate evolution in the Paris Basin from oxygen stable isotope (δ18O) compositions of marine molluscs , 2015, Journal of the Geological Society.

[42]  D. Garbe‐Schönberg,et al.  Nano-particulate pressed powder tablets for LA-ICP-MS , 2014 .

[43]  Haiou Qiu,et al.  Paleo-redox conditions across the Permian-Triassic boundary in shallow carbonate platform of the Nanpanjiang Basin, South China , 2014, Science China Earth Sciences.

[44]  J. Banner,et al.  Oxygen isotope variations in rainfall, drip-water and speleothem calcite from a well-ventilated cave in Texas, USA: Assessing a new speleothem temperature proxy , 2014 .

[45]  Christopher C. Day,et al.  Controls on trace-element partitioning in cave-analogue calcite , 2013 .

[46]  G. Nehrke,et al.  A new model for biomineralization and trace-element signatures of Foraminifera tests , 2013 .

[47]  C. Korte,et al.  The Giant Pacific Oyster (Crassostrea gigas) as a modern analog for fossil ostreoids: Isotopic (Ca, O, C) and elemental (Mg/Ca, Sr/Ca, Mn/Ca) proxies , 2013 .

[48]  É. Verrecchia,et al.  Chemical labelling of oyster shells used for time-calibrated high-resolution Mg/Ca ratios: A tool for estimation of past seasonal temperature variations , 2013 .

[49]  R. Witbaard,et al.  Exploring the calcium isotope signature of Arctica islandica as an environmental proxy using laboratory- and field-cultured specimens , 2013 .

[50]  D. Pleissner,et al.  Effect of Salinity on Growth of Mussels, Mytilus edulis, with Special Reference to Great Belt (Denmark) , 2012 .

[51]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[52]  K. Shirai,et al.  Past daily light cycle recorded in the strontium/calcium ratios of giant clam shells , 2012, Nature Communications.

[53]  D. Günther,et al.  Determination of Reference Values for NIST SRM 610–617 Glasses Following ISO Guidelines , 2011 .

[54]  Igor Gutiérrez-Zugasti Coastal resource intensification across the Pleistocene–Holocene transition in Northern Spain: Evidence from shell size and age distributions of marine gastropods , 2011 .

[55]  C. Kraan,et al.  Now an empty mudflat: past and present benthic abundances in the western Dutch Wadden Sea , 2011, Helgoland Marine Research.

[56]  M. Rafélis,et al.  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. , 2010 .

[57]  H. Kitazato,et al.  Foraminifera promote calcification by elevating their intracellular pH , 2009, Proceedings of the National Academy of Sciences.

[58]  J. Chappell,et al.  Profiles of trace elements and stable isotopes derived from giant long-lived Tridacna gigas bivalves: Potential applications in paleoclimate studies , 2009 .

[59]  H. Kennedy,et al.  Ion microprobe assessment of the heterogeneity of Mg/Ca, Sr/Ca and Mn/Ca ratios in Pecten maximus and Mytilus edulis (bivalvia) shell calcite precipitated at constant temperature , 2009 .

[60]  F. Houlbrèque,et al.  Strontium‐86 labeling experiments show spatially heterogeneous skeletal formation in the scleractinian coral Porites porites , 2008 .

[61]  R. Zenobi,et al.  Aerobic microbial dolomite at the nanometer scale : Implications for the geologic record , 2008 .

[62]  H. Kennedy,et al.  Inter- and intra-specimen variability masks reliable temperature control on shell Mg/Ca ratios in laboratory- and field-cultured Mytilus edulis and Pecten maximus (bivalvia) , 2008 .

[63]  Henri Bertin,et al.  CO2 injection into saline carbonate aquifer formations I: laboratory investigation , 2008 .

[64]  M. Carré,et al.  Calcification rate influence on trace element concentrations in aragonitic bivalve shells: Evidences and mechanisms , 2006 .

[65]  Bernd R. Schöne,et al.  Reliability of Multitaxon, Multiproxy Reconstructions of Environmental Conditions from Accretionary Biogenic Skeletons , 2006, The Journal of Geology.

[66]  Yakov Kuzyakov,et al.  Carbonate re-crystallization in soil revealed by 14C labeling: Experiment, model and significance for paleo-environmental reconstructions , 2006 .

[67]  K. Jochum,et al.  Chemical Characterisation of the USGS Reference Glasses GSA‐1G, GSC‐1G, GSD‐1G, GSE‐1G, BCR‐2G, BHVO‐2G and BIR‐1G Using EPMA, ID‐TIMS, ID‐ICP‐MS and LA‐ICP‐MS , 2005 .

[68]  D. Dettman,et al.  Paleosalinity in a brackish lake during the Holocene based on stable oxygen and carbon isotopes of shell carbonate in Nakaumi Lagoon, southwest Japan , 2005 .

[69]  P. Dove,et al.  Nanoscale effects of strontium on calcite growth : An in situ AFM study in the absence of vital effects , 2005 .

[70]  A. Lorrain,et al.  Strong biological controls on Sr/Ca ratios in aragonitic marine bivalve shells , 2005 .

[71]  H. Kawahata,et al.  Concentrations of Trace Elements in Carbonate Reference Materials Coral JCp‐1 and Giant Clam JCt‐1 by Inductively Coupled Plasma‐Mass Spectrometry , 2004 .

[72]  F. Bashey A Comparison of the Suitability of Alizarin Red S and Calcein for Inducing a Nonlethally Detectable Mark in Juvenile Guppies , 2004 .

[73]  H. Elderfield,et al.  A Cenozoic seawater Sr/Ca record from benthic foraminiferal calcite and its application in determining global weathering fluxes , 2003 .

[74]  I. Probert,et al.  Calcification rate and temperature effects on Sr partitioning in coccoliths of multiple species of coccolithophorids in culture , 2002 .

[75]  C. H. Weijden Pitfalls of normalization of marine geochemical data using a common divisor , 2002 .

[76]  H. Kawahata,et al.  Preparation of a New Geological Survey of Japan Geochemical Reference Material: Coral JCp-1 , 2002 .

[77]  D. Dettman,et al.  Controls on isotopic chemistry of the American oyster, Crassostrea virginica: implications for growth patterns , 2001 .

[78]  F. H. Rodd,et al.  The Suitability of Calcein to Mark Poeciliid Fish and a New Method of Detection , 2001 .

[79]  D. Schrag,et al.  Sr/Ca variations in Cretaceous carbonates: relation to productivity and sea level changes , 2001 .

[80]  J. Beukema,et al.  Synchronized reproductive success of the main bivalve species in the Wadden Sea: causes and consequences , 2001 .

[81]  A. Smaal,et al.  Regulation and monitoring of marine aquaculture in The Netherlands , 2000 .

[82]  Barnes,et al.  Environmental controls on growth of the massive coral Porites. , 2000, Journal of experimental marine biology and ecology.

[83]  P. Carbonel,et al.  A quantitative method of palaeolake-level reconstruction using ostracod assemblages: an example from the Bolivian Altiplano , 1994, Hydrobiologia.

[84]  B. L. Henke,et al.  X-Ray Interactions: Photoabsorption, Scattering, Transmission, and Reflection at E = 50-30,000 eV, Z = 1-92 , 1993 .

[85]  P. Sheehan,et al.  The Evolution of Reef Communities , 1987 .

[86]  H. M. Page,et al.  Temporal and spatial patterns of growth in mussels Mytilus edulis on an offshore platform: relationships to water temperature and food availability , 1987 .

[87]  John H. Wilson Environmental parameters controlling growth of Ostrea edulis L. and Pecten maximus L. in suspended culture , 1987 .

[88]  T. J. Hilbish,et al.  Growth trajectories of shell and soft tissue in bivalves: Seasonal variation in Mytilus edulis L. , 1986 .

[89]  S. Hagiwara,et al.  The calcium channel , 1983, Trends in Neurosciences.

[90]  M. Quinby-Hunt,et al.  Distribution of elements in sea water , 1983 .

[91]  C. Richardson,et al.  The use of tidal growth bands in the shell of Cerastoderma edule to measure seasonal growth rates under cool temperate and sub-arctic conditions , 1980, Journal of the Marine Biological Association of the United Kingdom.

[92]  B. Hanshaw,et al.  Major geochemical processes in the evolution of carbonate—Aquifer systems , 1979 .

[93]  J. Evans,et al.  Tidal Growth Increments in the Cockle Clinocardium nuttalli , 1972, Science.

[94]  B. Schöne,et al.  Changes of shell microstructural characteristics of Cerastoderma edule (Bivalvia) — A novel proxy for water temperature , 2017 .

[95]  A. Haour,et al.  Tracking the Cowrie Shell: Excavations in the Maldives, 2016 , 2016 .

[96]  H. Nováková,et al.  Possibilities of LA-ICP-MS technique for the spatial elemental analysis of the recent fish scales: Line scan vs. depth profiling , 2011 .

[97]  C. Heinrich,et al.  SILLS: A MATLAB-based program for the reduction of laser ablation ICP-MS data of homogeneous materials and inclusions , 2008 .

[98]  B. Valchev ON THE POTENTIAL OF SMALL BENTHIC FORAMINIFERA AS PALEOECOLOGICAL INDICATORS: RECENT ADVANCES , 2003 .

[99]  R. Day,et al.  A comparison of fluorochromes for marking abalone shells , 1995 .

[100]  C. Richardson,et al.  The age determination and growth rate of the European flat oyster, Ostrea edulis , in British waters determined from acetate peels of umbo growth lines , 1993 .

[101]  B. Bayne,et al.  Growth and Production of Mussels Mytilus edulis from Two Populations , 1980 .

[102]  R. Palmer,et al.  Interaction of mineral elements in sea water and shell of oysters (Crassostrea virginica (Gmelin)) cultured in controlled and natural systems , 1980 .

[103]  R. Markuszewski Structure, fluorescence, and chelating properties of Calcein , 1976 .

[104]  J. Dodd Magnesium and strontium in calcareous skeletons; a review , 1967 .