Abstract
Traditional isotope sclerochronology employing isotope ratio mass spectrometry has been used for decades to determine the periodicity of growth increment formation in marine organisms with accretionary growth. Despite its well-demonstrated capabilities, it is not without limitation. The most significant of these being the volume of carbonate powder required for analysis with conventional drill-sampling techniques, which limit sampling to early in ontogeny when growth is fast or to species that reach relatively large sizes. In species like Astarte borealis (Schumacher, 1817), a common component of Arctic boreal seas, traditional methods of increment analysis are difficult, because the species is typically long-lived, slow growing, and forms extremely narrowly spaced growth increments. Here, we use Secondary Ion Mass Spectrometry (SIMS) to analyze δ18O in 10-μm-diameter spots and resolve the seasonal timing of growth increment formation in Astarte borealis in the southeastern Baltic Sea. In the individaul sampled here, dark growth increments can form in either the fall, winter, or spring. Furthermore, growth increment data from two populations (RFP3S = 54.7967° N, 12.38787° E; WA = 54.86775° N, 14.09832° E) indicate that in the Baltic Sea, A. borealis is moderately long-lived (at least 43 years) and slow growing (von Bertalanffy k values 0.08 and 0.06). Our results demonstrate the potential of A. borealis to be a recorder of Baltic Sea seasonality over the past century using both live- and dead-collected shells, and also the ability of SIMS analysis to broaden the spectrum of bivalves used in sclerocrhonological work.
Similar content being viewed by others
Availability of data and materials
The datasets generated during and/or analyzed during the current study will be made available in the Center for Open Science repository (http://osf.io).
Code availablility.
Not applicable.
References
Ballesta-Artero I, Witbaard R, Carroll ML, van der Meer J (2017) Environmental factors regulating gaping activity of the bivalve Arctica islandica in Northern Norway. Mar Bio 164:116. https://doi.org/10.1007/s00227-017-3144-7
Barker RM (1964) Microtextural variation in pelecypod shells. Malacologia 2:69–86
Black HD, Andrus CFT, Lambert WJ, Rick TC, Gillikin DP (2017) δ15N values in Crassostrea virginica shells provides early direct evidence for nitrogen loading to Chesapeake Bay. Sci Rep 7:3–10. https://doi.org/10.1038/srep44241
Boening DW (1999) An evaluation of bivalves as biomonitors of heavy metals pollution in marine waters. Environ Monit Assess 55:459–470
Clark GR (1974) Growth lines in invertebrate skeletons. Annu Rev Earth Planet Sci 2:77–99. https://doi.org/10.1146/annurev.ea.02.050174.000453
Coplen TB, Kendall C, Hopple J (1983) Comparison of stable isotope reference samples. Nature 302:236–238
Dunca E, Schöne BR, Mutvei H (2005) Freshwater bivalves tell of past climates: but how clearly do shells from polluted rivers speak? Palaeogeogr Palaeoclimatol Palaeoecol 228:43–57. https://doi.org/10.1016/j.palaeo.2005.03.050
Dunca E, Mutvei H, Göransson P, Morth CM, Schöne BR, Whitehouse MJ, Elfman M, Baden SP (2009) Using ocean quahog (Arctica islandica) shells to reconstruct palaeoenvironment in Öresund, Kattegat and Skagerrak, Sweden. Int J Earth Sci (geol Rundsch) 98:3–17
Elliot M, deMenocal PB, Linsley BK, Howe SS (2003) Environmental controls on the stable isotopic composition of Mercenaria mercenaria: potential application to paleoenvironmental studies. Geochem Geophys 4:1–16. https://doi.org/10.1029/2002GC000425
Gagayev S (1989) Growth and production of mass species of bivalves in Chaun Bay (East Siberian Sea). Oceanology 29:504–507
Gillikin DP, Dehairs F, Baeyens W, Navez J, Lorrain A, André L (2005) Inter- and intra-annual variations of Pb/Ca ratios in clam shells (Mercenaria mercenaria): a record of anthropogenic lead pollution? Mar Pollut Bull 50:1530–1540. https://doi.org/10.1016/j.marpolbul.2005.06.020
Goodwin DH, Flessa KW, Schöne BR, Dettman DL, Schöne BR (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. https://doi.org/10.1669/0883-1351(2001)016
Gusev AA, Rudinskaya LV (2014) Shell form, growth, and production of Astarte borealis (Schumacher, 1817) (Astartidae, Bivalvia) in the southeastern Baltic Sea. Oceanology 54:458–464. https://doi.org/10.1134/S0001437014040043
Helser T, Kastelle C, Crowell A, Ushikubo T, Orland IJ, Kozdon R, Valley JW (2018a) A 200-year archaeozoological record of Pacific cod (Gadus macrocephalus) life history as revealed through ion microprobe oxygen isotope ratios in otoliths. J Archaeol Sci Rep 21:1236–1246. https://doi.org/10.1016/j.jasrep.2017.06.037
Helser TE, Kastelle CR, McKay JL, Orland IJ, Kozond R, Valley JW (2018b) Evaluation of micromilling/conventional isotope ratio mass spectrometry and secondary ion mass spectrometry of δ18O values in fish otoliths for sclerochronology. Rapid Commun Mass Spectrom 32:1781–1790. https://doi.org/10.1002/rcm.8231
Hendozko E, Szefer P, Warzocha J (2010) Ecotoxicology and environmental safety heavy metals in Macoma balthica and extractable metals in sediments from the southern Baltic Sea. Ecotoxicol Environ Saf 73:152–163. https://doi.org/10.1016/j.ecoenv.2009.09.006
Hendy CH (1971) The isotopic geochemistry of speleothems—I. The calculation of the effects of different modes of formation on the isotopic composition of speleothems and their applicability as paleoclimate indicators. Geochim Cosmochim Acta 35:801–824
Henry KM, Cerrato RM (2007) The annual macroscopic growth pattern of the northern quahog [=hard clam, Mercenaria mercenaria (L.)], in Narragansett Bay, Rhode Island. J Shellfish Res 26:985–993. https://doi.org/10.2983/0730-8000(2007)26[985:tamgpo]2.0.co;2
Jones DS, Quitmyer IR (1996) Marking time with bivalve shells: oxygen isotopes and season of annual increment formation. Palaios 11:340. https://doi.org/10.2307/3515244
Jones DS, Williams DF, Arthur MA (1983) Growth history and ecology of the Atlantic Surf Clam, Spisula solidissima (Dillwyn), as revealed by stable isotopes and annual shell increments. J Exp Mar Biol Ecol 73:225–242. https://doi.org/10.1016/0022-0981(83)90049-7
Jones DS, Arthur MA, Allard DJ (1989) Sclerochronological records of temperature and growth from shells of Mercenaria mercenaria from Narragansett Bay, Rhode Island. Mar Biol 102:225–234. https://doi.org/10.1007/BF00428284
Killam DE, Clapham ME (2018) Identifying the ticks of bivalve shell clocks: seasonal growth in relation to temperature and food supply. Palaios 33:228–236. https://doi.org/10.2110/palo.2017.072
Kozdon R, Ushikubo T, Kita NT, Spicuzza MJ, Valley JW (2009) Intratest oxygen isotope variability in the planktonic foraminifer N. pachyderma: real vs. apparent vital effects by ion microprobe. Chem Geol 258(34):327–337
Krantz DE, Jones DS, Williams DF (1984) Growth rates of the sea scallop, Placopecten magellanicus, determined from the 18O/16O record in shell calcite. Biol Bull 167:186–199
Liehr G, Zettler ML, Leipe T, Witt G (2005) The ocean quahog Arctica islandica L.—a bioindicator for contaminated sediments. Mar Biol 147:671–679
Linzmeier BJ, Kozdon R, Peters SE, Valley JW (2016) Oxygen isotope variability within Nautilus shell growth bands. PLoS ONE 11(4):e0153890. https://doi.org/10.1371/journal.pone.0153890
Linzmeier ABJ, Landman NH, Peters SE, Kozdon R, Kitajima K (2018) Ion microprobe—measured stable isotope evidence for ammonite habitat and life mode during early ontogeny. Paleobiology 44:684–708. https://doi.org/10.1017/pab.2018.21
Lutz RA, Rhoads DC (1980) Growth patterns within the molluscan shell. In: Rhoads DC, Lutz RA (eds) Skeletal growth of aquatic organisms. Plenum Press, New York, pp 203–254
Matta ME, Orland IJ, Ushikubo T, Helser TE, Black BA, Valley JW (2013) Otolith oxygen isotopes measured by high-precision secondary ion mass spectrometry reflect life history of a yellow fin sole (Limanda aspera). Rapid Commun Mass Spectrom 27:691–699. https://doi.org/10.1002/rcm.6502
Moss DK, Ivany LC, Judd EJ, Cummings PW, Bearden CE, Kim WJ, Artruc EG, Driscoll JR (2016) Lifespan, growth rate, and body size across latitude in marine Bivalvia, with implications for Phanerozoic evolution. Proc R Soc B Biol Sci 283:20161364. https://doi.org/10.1098/rspb.2016.1364
Moss DK, Surge D, Khaitov V (2018) Lifespan and growth of Astarte borealis (Bivalvia) from Kandalaksha Gulf, White Sea, Russia. Polar Biol 41:1359–1369. https://doi.org/10.1007/s00300-018-2290-9
Olson IC, Kozdon R, Valley JW, Gilbert PUPA (2012) Mollusk shell nacre ultrastructure correlates with environmental temperature and pressure. J Am Chem Soc 134:7351–7358
Orland IJ, Kozdon R, Linzmeier B, Wycech J, Sliwinski M, Kitajima K, Kita N, Valley JW (2015) Enhancing the accuracy of carbonate δ18O and δ13C measurements by SIMS. American Geophysical Union, Fall Meeting, December 18, 2015. Presentation PP52B-03. https://agu.confex.com/agu/fm15/meetingapp.cgi/Paper/67486. Accessed 12 Apr 2021
Pannella G (1976) Tidal growth patterns in recent and fossil mollusc bivalve shells. Sci Nat Heidelberg 63:539–543
Pannella G, MacClintock C (1968) Biological and environmental rhythms reflected in molluscan shell growth. Paleontol Soc Mem 2:64–80
Protasowicki M, Dural M, Jaremek J (2008) Trace metals in the shells of blue mussels (Mytilus edulis) from the Poland coast of Baltic sea. Environ Monit Assess 141:329–337. https://doi.org/10.1007/s10661-007-9899-4
Quitmyer IR, Jones DS, Arnold WS (1997) The sclerochronology of hard clams, Mercenaria spp., from the South-Eastern USA: a method of elucidating the zooarchaeological records of seasonal resource procurement and seasonality in prehistoric shell middens. J Archaeol Sci 24:825–840. https://doi.org/10.1006/jasc.1996.0163
Rainbow PS, Fialkowski W, Sokolowski A, Smith BD, Wolowicz M (2004) Geographical and seasonal variation of trace metal bioavailabilities in the Gulf of Gdansk, Baltic Sea using mussels (Mytilus trossulus) and barnacles (Balanus improvisus) as biomonitors. Mar Biol 144:271–286. https://doi.org/10.1007/s00227-003-1197-2
Reed AJ, Godbold JA, Grange LJ, Solan M (2021) Growth of marine ectotherms is regionally constrained and asymmetric with latitude. Global Ecol Biogeogr. https://doi.org/10.1111/geb.13245
Richardson CA (2001) Molluscs as archives of environmental change. Oceanogr Mar Biol 39:103–164
Saleuddin ASM (1965) The mode of life and functional anatomy of Astarte spp. (Eulamellibranchia). J Molluscan Stud 36:229–257. https://doi.org/10.1093/oxfordjournals.mollus.a064952
Sato S (1995) Spawning periodicity and shell microgrowth patterns of the venerid bivalve Phacosoma japonicum (Reeve, 1850). Veliger 38:61–72
Schöne BR (2013) Arctica islandica (Bivalvia): A unique paleoenvironmental archive of the northern North Atlantic Ocean. Glob Planet Chang 111:199–225. https://doi.org/10.1016/j.gloplacha.2013.09.013
Schöne BR, Surge D (2012) Bivalve sclerochronology and geochemistry. In: Seldon P, Hardesty J, Carter JG, coordinator (eds) Part N, Bivalvia, Revised, Volume 1 Treatise Online 46:14, 1–24. University of Kansas, Paleontological Institute, Lawrence, Kansas
Schöne BR, Fiebig J, Pfeiffer M, Gleß R, Hickson J, Johnson ALA, Dreyer W, Oschmann W (2005a) Climate records from a bivalved Methuselah (Arctica islandica, Mollusca; Iceland). Palaeogeogr Palaeoclimatol Palaeoecol 228:130–148. https://doi.org/10.1016/j.palaeo.2005.03.049
Schöne BR, Houk SD, Freyre Castro AD, Fiebig J, Oschmann W, Kröncke I, Dreyer W, Gosselck F (2005b) Daily growth rates in shells of Arctica islandica: assessing sub-seasonal environmental controls on a long-lived bivalve mollusk. Palaios 20:78–92
Schöne BR, Huang X, Zettler ML, Zhao L, Mertz R, Jochum KP, Walliser EO (2021) Mn/Ca in shells of Arctica islandica (Baltic Sea)—a potential proxy for ocean hypoxia? Est Coast Shelf Sci 251:107257
Schumacher CF (1817) Essai d’un nouveau système des habitations des vers testacès. Schultz, Copenhagen
Selin NI (2007) Shell form, growth and life span of Astarte arctica and A. borealis (Mollusca: Bivalvia) from the subtidal zone of northeastern Sakhalin. Russ J Mar Biol 33:232–237. https://doi.org/10.1134/S1063074007040050
Selin NI (2010) The growth and life span of bivalve mollusks at the northeastern coast of Sakhalin Island. Russ J Mar Biol 36:258–269. https://doi.org/10.1134/S1063074010040048
Surge D, Walker KJ (2006) Geochemical variation in microstructural shell layers of the southern quahog (Mercenaria campechiensis): implications for reconstructing seasonality. Palaeogeogr Palaeoclimatol Palaeoecol 237:182–190. https://doi.org/10.1016/j.palaeo.2005.11.016
Surge D, Kelly G, Arnold WS, Geiger SP, Gowert AE (2007) Isotope sclerochronology of Mercenaria mercenaria, M. campechiensis, and their natural hybrid form: Does genotype matter? Palaios 23:559–565. https://doi.org/10.2110/palo.2007.p07-056r
Surge D, Wang T, Gutiérrez-Zugasti I, Kelley PH (2013) Isotope sclerochronology and season of annual growth line formation in limpet shells (Patella vulgata) from warm- and cold-temperate zones in the eastern North Atlantic. Palaios 28:386–393. https://doi.org/10.2110/palo.2012.p12-038r
Szefer P (2002) Metal pollutants and radionuclides in the Baltic Sea—an overview. Oceanologia 44:129–178
Szefer P, Szefer K (1990) Metals in molluscs and associated bottom sediments of the southern Baltic. Helgol Meeresunters 44:411–424
Torres ME, Zima D, Falkner KK, Macdonald RW, O’Brien M, Schöne BR, Siferd T (2011) Hydrographic changes in Nares Strait (Canadian Arctic Archipelago) in recent decades based on δ18O profiles of bivalve shells. Arctic 64:45–58. https://doi.org/10.1016/j.jmb.2005.01.031
Vihtakari M, Renaud PE, Clarke LJ, Whitehouse MJ, Hop H, Carroll ML, Ambrose WG Jr (2016) Decoding the oxygen isotope signal for seasonal growth patterns in Arctic bivalves. Palaeogeogr Palaeoclimatol Palaeoecol 446:263–283
von Bertalanffy L (1938) A quantitative theory of organic growth (Inquires on growth laws. II). Hum Biol 10:181–213
von Oertzen J-A (1972) Cycles and rates of reproduction of six Baltic Sea bivalves of different zoogeographical origin. Mar Biol 14:143–149
von Oertzen J-A (1973) Abiotic potency and physiological resistance of shallow and deep water bivalves. Oikos Suppl 15:261–266
Weidman CR, Jones GA, Kyger (1994) The long-lived mollusc Arctica islandica: a new paleoceanographic tool for the reconstruction of bottom temperatures for the continental shelves of the northern North Atlantic Ocean. J Geophys Res 99:18305. https://doi.org/10.1029/94JC01882
Wycech JB, Kelly DC, Kozdon R, Orland IJ, Spero HJ, Valley JW (2018) Comparison of δ18O analyses on individual planktic foraminifer (Orbulina universa) shells by SIMS and gas-source mass spectrometry. Chem Geol 483:119–130. https://doi.org/10.1016/j.chemgeo.2018.02.028
Zettler M (2001) Recent geographical distribution of the Astarte borealis species complex, its nomenclature and bibliography (Bivalvia: Astartidae). Schr Malakozool 18:1–14
Zettler ML (2002) Ecological and morphological features of the bivalve Astarte borealis (Scumacher, 1817) in the Baltic Sea near its geographical range. J Shellfish Res 21:33–40
Acknowledgements
We thank Garrett Braniecki for drafting the map figure. Comments from two anonymous reviewers improved the manuscript. Funding for this study was provided by the US National Science Foundation (NSF) to Surge (Grant #EAR-1656974). The WiscSIMS Laboratory is supported by the US NSF (Grant # EAR-1355590 and EAR-1658823).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors are not aware of any conflicts of interest which may arise as a result of this work.
Additional information
Responsible Editor: A. G. Checa.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewers: undisclosed experts.
Rights and permissions
About this article
Cite this article
Moss, D.K., Surge, D., Zettler, M.L. et al. Age and growth of Astarte borealis (Bivalvia) from the southwestern Baltic Sea using secondary ion mass spectrometry. Mar Biol 168, 133 (2021). https://doi.org/10.1007/s00227-021-03935-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-021-03935-7