Marine Biology

, Volume 159, Issue 3, pp 601–611 | Cite as

Isotopic fractionation between seawater and the shell of Scrobicularia plana (Bivalvia) and its application for age validation

  • Sílvia SantosEmail author
  • Joana F. M. F. Cardoso
  • Valeska Borges
  • Rob Witbaard
  • Pieternella C. Luttikhuizen
  • Henk W. van der Veer
Original Paper


This study analyzed the isotopic profiles of four aragonitic shells of Scrobicularia plana in conjunction with measured seawater temperatures and salinities. Comparison of δ18OSHELL with expected values revealed fractionation of δ18O in near equilibrium with the ambient environment. Growth cessation occurred between November and March. Carbonate deposition stopped when temperatures were <12°C. Analysis of δ13CSHELL values suggested that carbon in the shell does not reflect the DIC in ambient water, likely due to the incorporation of metabolic carbon. An ontogenetic trend of increasing δ13C values over time was observed, likely related to changes in metabolic activity. Annual growth patterns were inferred from δ18OSHELL profiles and compared with internal and external growth lines. Estimations of age based on external lines were unreliable, resulting in overestimation of age and underestimation of growth rates, likely due to the disturbance lines being wrongly identified as annual. Analysis of internal lines may lead to over- or underestimation of age and was more reliable in recent portions of the shell.


Bivalve Dissolve Inorganic Carbon Seawater Temperature Growth Line External Line 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study was co-financed by the Portuguese Foundation for Science and Technology (FCT) and Fundo Social Europeu (POPH/FSE) through grants awarded to Sílvia Santos (SFRH/BD/28370/2006) and Joana Cardoso (SFRH/BPD/34773/2007). Thanks are due to Dr. Hubert Vonhof and Ralph Groen from Vrije Universiteit (VU) Amsterdam for assistance with the analysis of δ18O of water samples. The authors also thank Gerard Nieuwland, Michiel Kienhuis, and Evaline van Weerlee, at NIOZ, for all the help with the analysis of the isotopic profiles of shell carbonates and water DIC. Furthermore, we thank Hans Witte for helping with the experimental setup and Catarina Cruzeiro, Célia Carvalho, Sofia Saraiva, and Vânia Freitas for assistance during the monthly measurements. Finally, we also thank Jeanine Olsen, Carlo Heip and 2 anonymous reviewers for comments on earlier versions of the paper.

Supplementary material

227_2011_1838_MOESM1_ESM.tif (25.1 mb)
Fig. S1 Cross-section of S. plana stained with Feigl’s solution. Black color is indicative that aragonite is shell’s main component. (TIFF 25690 kb)
227_2011_1838_MOESM2_ESM.eps (495 kb)
Fig. S2 Mean monthly water temperature, mean monthly salinity, δ18OWATER and δ13CWATER values for 2008–2009, measured near experimental site (Marsdiep, western Dutch Wadden Sea). (EPS 494 kb)
227_2011_1838_MOESM3_ESM.eps (908 kb)
Fig. S3 Daily seawater temperatures (open circles) measured close to experimental site. Estimated water temperatures based on δ18OSHELL and δ18OWATER are represented for shells 1291 (open circles), 1317 (open triangles), and 1338 (open squares). (EPS 907 kb)
227_2011_1838_MOESM4_ESM.eps (485 kb)
Fig. S4 Covariation of δ18OSHELL and δ13CSHELL values of four S. plana shells. Correlation was determined by linear regression (shell 1243: r2 = 0.24, F1,30 = 9.69, p = 0.004; shell 1291: r2 = 0.01, F1,45 = 0.31, p = 0.58; shell 1317: r2 = 0.05, F1,39 = 1.96, p = 0.17; shell 1317: r2 = 0.01, F1,25 = 0.31, p = 0.58). (EPS 485 kb)
227_2011_1838_MOESM5_ESM.eps (456 kb)
Fig. S5 Shell growth of S. plana during experimental period. Only animals measured monthly that survived first winter, in a total of 25 animals, were considered. (EPS 456 kb)


  1. Bachelet G (1980) Growth and recruitment of the tellinid bivalve Macoma balthica at the southern limit of its geographical distribution, the Gironde estuary (SW France). Mar Biol 59:105–117CrossRefGoogle Scholar
  2. Bachelet G (1981) Application de l’équation de von Bertalanffy à la croissance du bivalve Scrobicularia plana. Cah Biol Mar 22:291–311Google Scholar
  3. Bocher P, Piersma T, Dekinga A, Kraan C, Yates MG, Guyot T, Folmer EO, Radenac G (2007) Site- and species-specific distribution patterns of molluscs at five intertidal soft-sediment areas in northwest Europe during a single winter. Mar Biol 151:577–594CrossRefGoogle Scholar
  4. Brey T, Mackensen A (1997) Stable isotopes prove shell growth bands in the Antarctic bivalve Laternula elliptica to be formed annually. Polar Biol 17:465–468CrossRefGoogle Scholar
  5. Bucci JP, Showers WJ, Genna B, Levine JF (2009) Stable oxygen and carbon isotope profiles in an invasive bivalve (Corbicula fluminea) in North Carolina watersheds. Geochim Cosmochim Acta 73:3234–3247CrossRefGoogle Scholar
  6. Carriker MR, Swann CP, Prezant RS, Counts CL (1991) Chemical elements in the aragonitic and calcitic microstructural groups of shell of the oyster Crassostrea virginica: a proton probe study. Mar Biol 109:287–297CrossRefGoogle Scholar
  7. Casagranda C, Boudouresque CF (2005) Abundance, population structure and production of Scrobicularia plana and Abra tenuis (Bivalvia: Scrobicularidae) in a Mediterranean brackish lagoon, Lake Ichkeul, Tunisia. Int Rev Hydrobiol 90:376–391CrossRefGoogle Scholar
  8. Dettman DL, Lohmann KC (1993) Seasonal change in Paleogene surface water δ18O: Fresh-water bivalves of western North America. In: Swart PK, Lohmann KC, McKenzie J, Savin S (eds) Climate change in continental isotopic records, vol 78. AGU Monograph, Washington, pp 153–163CrossRefGoogle Scholar
  9. Dettman DL, Reische AK, Lohmann KC (1999) Controls on the stable isotope composition of seasonal growth bands in aragonitic fresh-water bivalves (Unionidae). Geochim Cosmochim Acta 63:1049–1057CrossRefGoogle Scholar
  10. Epstein S, Buchsbaum R, Lowenstam H, Urey HC (1953) Revised carbonate-water isotopic temperature scale. Geol Soc Am Bull 64:1315–1325CrossRefGoogle Scholar
  11. Feigl F (1937) Qualitative analysis by spot tests: inorganic and organic applications. Nordemann Publishing Company, New YorkGoogle Scholar
  12. Freitas V, Campos J, Fonds M, Van der Veer HW (2007) Potential impact of temperature change on epibenthic predator-bivalve prey interactions in temperate estuaries. J Therm Biol 32:328–340CrossRefGoogle Scholar
  13. Geist J, Auerswald K, Boom A (2005) Stable carbon isotopes in freshwater mussel shells: environmental record or marker for metabolic activity? Geochim Cosmochim Acta 69:3545–3554CrossRefGoogle Scholar
  14. Gillikin DP, De Ridder F, Ulens H, Elskens M, Keppens E, Baeyens W, Dehairs F (2005) Assessing the reproducibility and reliability of estuarine bivalve shells (Saxidomus giganteus) for sea surface temperature reconstruction: implications for paleoclimate studies. Palaeogeogr Palaeoclimatol Palaeoecol 228:70–85CrossRefGoogle Scholar
  15. Gillikin DP, Lorrain A, Bouillon S, Willenz P, Dehairs F (2006) Stable carbon isotopic composition of Mytilus edulis shells: relation to metabolism, salinity, δ13CDIC and phytoplankton. Org Geochem 37:1371–1382CrossRefGoogle Scholar
  16. Goewert A, Surge D, Carpenter SJ, Downing J (2007) Oxygen and carbon isotope ratios of Lampsilis cardium (Unionidae) from two streams in agricultural watersheds of Iowa, USA. Palaeogeogr Palaeoclimatol Palaeoecol 252:637–648CrossRefGoogle Scholar
  17. Gonfiantini R, Stichler W, Rozanski K (1995) Standards and intercomparison materials distributed by the International Atomic Energy Agency for stable isotope measurements. I.A.E.A. Reference and intercomparison materials for stable isotopes of light elements. Techdoc 825Google Scholar
  18. Goodwin DH, Paul P, Wissink CL (2009) MoGroFunGen: a numerical model for reconstructing intra-annual growth rates of bivalve molluscs. Palaeogeogr Palaeoclimatol Palaeoecol 276:47–55CrossRefGoogle Scholar
  19. Gosling EM (2003) Bivalve molluscs: biology, ecology and culture. Blackwell Publishing, Oxford, UKGoogle Scholar
  20. Green J (1957) The growth of Scrobicularia plana (Da Costa) in the Gwendraeth estuary. J Mar Biol Assoc UK 36:41–47CrossRefGoogle Scholar
  21. Grossman EL, Ku TL (1986) Oxygen and carbon isotope fractionation in biogenic aragonite: temperature effects. Chem Geol (Isot Geosci Sect) 59:59–74CrossRefGoogle Scholar
  22. Guerreiro J (1998) Growth and production of the bivalve Scrobicularia plana in two southern European estuaries. Vie Milieu 48:121–131Google Scholar
  23. Haag WR, Commens-Carson AM (2008) Testing the assumption of annual shell ring deposition in freshwater mussels. Can J Fish Aquat Sci 65:493–508CrossRefGoogle Scholar
  24. Hallmann N, Schöne BR, Strom A, Fiebig J (2008) An intractable climate archive: sclerochronological and shell oxygen isotope analyses of the Pacific geoduck, Panopea abrupta (bivalve mollusk) from Protection Island (Washington State, USA). Palaeogeogr Palaeoclimatol Palaeoecol 269:115–126CrossRefGoogle Scholar
  25. Hughes RN (1970) Population dynamics of bivalve Scrobicularia plana (Da Costa) on an intertidal mud-flat in North Wales. J Anim Ecol 39:333–356CrossRefGoogle Scholar
  26. Ingram BL, Conrad ME, Ingle JC (1996) Stable isotope and salinity systematics in estuarine waters and carbonates: San Francisco Bay. Geochim Cosmochim Acta 60:455–467CrossRefGoogle Scholar
  27. Jones DS (1980) Annual cycle of shell growth increment formation in two continental shelf bivalves and its paleoecologic significance. Paleobiology 6:331–340Google Scholar
  28. Keegan BF (1986) The COST 647 project on coastal benthic ecology: a perspective. Hydrobiologia 142:IX–XIICrossRefGoogle Scholar
  29. Kesler D, Downing J (1997) Internal shell annuli yield inaccurate growth estimates in the freshwater mussels Elliptio complanata and Lampsilis radiata. Freshwat Biol 37:325–332CrossRefGoogle Scholar
  30. Kirby MX, Soniat TM, Spero HJ (1998) Stable isotope sclerochronology of Pleistocene and recent oyster shells (Crassostrea virginica). Palaios 13:560–569CrossRefGoogle Scholar
  31. Klein RT, Lohmann KC, Thayer CW (1996) Sr/Ca and 13C/12C ratios in skeletal calcite of Mytilus trossulus: Covariation with metabolic rate, salinity, and carbon isotopic composition of seawater. Geochim Cosmochim Acta 60:4207–4221CrossRefGoogle Scholar
  32. Krantz DE, Williams DF, Jones DS (1987) Ecological and paleoenvironmental information using stable isotope profiles from living and fossil molluscs. Palaeogeogr Palaeoclimatol Palaeoecol 58:249–266CrossRefGoogle Scholar
  33. Langston WJ, Burt GR, Chesman BS (2007) Feminisation of male clams Scrobicularia plana from estuaries in Southwest UK and its induction by endocrine-disrupting chemicals. Mar Ecol Prog Ser 333:173–184CrossRefGoogle Scholar
  34. Lartaud F, Emmanuel L, De Rafelis M, Pouvreau S, Renard M (2010) Influence of food supply on the δ13C signature of mollusc shells: implications for palaeoenvironmental reconstitutions. Geo-Mar Lett 30:23–34CrossRefGoogle Scholar
  35. Lorrain A, Paulet YM, Chauvaud L, Dunbar R, Mucciarone D, Fontugne M (2004) δ13C variation in scallop shells: increasing metabolic carbon contribution with body size? Geochim Cosmochim Acta 68:3509–3519CrossRefGoogle Scholar
  36. MacDonald BA, Thomas MLH (1980) Age determination of the soft-shell clam Mya arenaria using shell internal growth lines. Mar Biol 58:105–109CrossRefGoogle Scholar
  37. McConnaughey T (1989) 13C and 18O isotopic disequilibrium in biological carbonates: I. Patterns. Geochim Cosmochim Acta 53:151–162CrossRefGoogle Scholar
  38. McConnaughey TA, Gillikin DP (2008) Carbon isotopes in mollusk shell carbonates. Geo-Mar Lett 28:287–299CrossRefGoogle Scholar
  39. Moura P, Gaspar MB, Monteiro CC (2009) Age determination and growth rate of a Callista chione population from the southwestern coast of Portugal. Aquat Biol 5:97–106CrossRefGoogle Scholar
  40. Philippart CJM, van Iperen JM, Cadée GC, Zuur AF (2010) Long-term field observations on seasonality in chlorophyll-a concentrations in a shallow coastal marine ecosystem, the Wadden Sea. Estuar Coast 33:286–294CrossRefGoogle Scholar
  41. Poulain C, Lorrain A, Mas R, Gillikin DP, Dehairs F, Robert R, Paulet YM (2010) Experimental shift of diet and DIC stable carbon isotopes: Influence on shell δ13C values in the Manila clam Ruditapes philippinarum. Chem Geol 272:75–82CrossRefGoogle Scholar
  42. Richardson CA (2001) Molluscs as archives of environmental change. Oceanogr Mar Biol Annu Rev 39:103–164Google Scholar
  43. Richardson CA, Walker P (1991) The age structure of a population of the hard-shell clam, Mercenaria mercenaria from Southampton Water, England, derived from acetate peel replicas of shell sections. ICES J Mar Sci 48:229–236CrossRefGoogle Scholar
  44. Rohling EJ, Cooke S (1999) Stable oxygen and carbon isotopes in foraminiferal carbonate shells. In: Sen Gupta BK (ed) Modern foraminifera. Kluwer, The Netherland, pp 239–258Google Scholar
  45. Romanek CS, Grossman EL, Morse JW (1992) Carbon isotopic fractionation in synthetic aragonite and calcite: effects of temperature and precipitation rate. Geochim Cosmochim Acta 56:419–430CrossRefGoogle Scholar
  46. Ropes JW (1985) Modern methods used to age oceanic bivalves. Nautilus 99:53–57Google Scholar
  47. Rosenberg GD (1980) An ontogenetic approach to the environmental significance of bivalve shell chemistry. In: Rhoads DC, Lutz RA (eds) Skeletal growth of aquatic organisms. Plenum Press, New York, pp 133–168Google Scholar
  48. Santos S, Cardoso JFMF, Carvalho C, Luttikhuizen PC, van der Veer HW (2011a) Seasonal variability in somatic and reproductive investment of the bivalve Scrobicularia plana (da Costa, 1778) along a latitudinal gradient. Estuar Coast Shelf Sci 92:19–26CrossRefGoogle Scholar
  49. Santos S, Luttikhuizen PC, Campos J, Heip CHR, der Veer HW (2011b) Spatial distribution patterns of the peppery furrow shell Scrobicularia plana (da Costa, 1778) along the European coast: a review. J Sea Res 66:238–247CrossRefGoogle Scholar
  50. Schöne BR, Rodland DL, Wehrmann A, Heidel B, Oschmann W, Zhang Z, Fiebig J, Beck L (2007) Combined sclerochronologic and oxygen isotope analysis of gastropod shells (Gibbula cineraria, North Sea): life-history traits and utility as a high-resolution environmental archive for kelp forests. Mar Biol 150:1237–1252CrossRefGoogle Scholar
  51. Sola JC (1997) Reproduction, population dynamics, growth and production of Scrobicularia plana Da Costa (Pelecypoda) in the Bidasoa estuary, Spain. Netherlands J Aquat Ecol 30:283–296CrossRefGoogle Scholar
  52. Surge D, Lohmann KC, Dettman DL (2001) Controls on isotopic chemistry of the American oyster, Crassostrea virginica: implications for growth patterns. Palaeogeogr Palaeoclimatol Palaeoecol 172:283–296CrossRefGoogle Scholar
  53. Tebble N (1976) British bivalve seashells: a handbook for identification. H.M.S.O., EdinburghGoogle Scholar
  54. van Aken HM (2001) 140 years of daily observations in a tidal inlet (Marsdiep). In: ICES Marine Science Symposia, pp 359–361Google Scholar
  55. Verdelhos T, Neto JM, Marques JC, Pardal MA (2005) The effect of eutrophication abatement on the bivalve Scrobicularia plana. Estuar Coast Shelf Sci 63:261–268CrossRefGoogle Scholar
  56. Versteegh EAA, Troelstra SR, Vonhof HB, Kroon D (2009) Oxygen isotope composition of bivalve seasonal growth increments and ambient water in the rivers Rhine and Meuse. Palaios 24:497–504CrossRefGoogle Scholar
  57. Witbaard R, Jenness MI, Van Der Borg K, Ganssen G (1994) Verification of annual growth increments in Arctica islandica L. from the North Sea by means of oxygen and carbon isotopes. Neth J Sea Res 33:91–101CrossRefGoogle Scholar
  58. Zwarts L (1991) Seasonal variation in body weight of the bivalves Macoma balthica, Scrobicularia plana, Mya arenaria and Cerastoderma edule in the Dutch Wadden Sea. Neth J Sea Res 28:231–245CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Sílvia Santos
    • 1
    Email author
  • Joana F. M. F. Cardoso
    • 1
    • 2
  • Valeska Borges
    • 1
  • Rob Witbaard
    • 1
  • Pieternella C. Luttikhuizen
    • 1
  • Henk W. van der Veer
    • 1
  1. 1.NIOZ, Royal Netherlands Institute for Sea ResearchDen Burg TexelThe Netherlands
  2. 2.CIMAR/CIIMAR, Centro Interdisciplinar de Investigação Marinha e Ambiental, Universidade do PortoPortoPortugal

Personalised recommendations