Abstract
The grey top-shell, Gibbula cineraria is a common member of temperate to cold water kelp forest communities, but its longevity and the age structure of its populations remains unresolved. Combined measurements of shell growth rates (sclerochronology) and oxygen isotope composition allow analysis of rate and timing of shell growth. Eight specimens were analyzed from the southern North Sea (near Helgoland, German Bight). Three age groups were identified but external measurements (width, height, ornamentation patterns and number of whorls) and shell weight are not adequate for ontogenetic age discrimination. Stable oxygen isotope data is consistent with shell growth during the interval from April to December in isotopic equilibrium with seawater, and growth increments exhibit strong tidal controls with fortnightly bundles well preserved. Reliable environmental proxy data (water temperature) can be extracted from the shell aragonite using conventional stable oxygen isotope analyses, with a temporal resolution of days attainable during intervals of maximum growth, but annual extremes are not always recorded in the shell. While demonstrating the utility of G. cineraria as a environmental and potential paleoenvironmental proxy for kelp forest habitats, its longevity has been significantly overestimated.
Similar content being viewed by others
References
Alyakrinskaya IO (2005) Functional significance and weight properties of the shell in some mollusks. Biol Bull 32:397–418
Ankel WE (1936) Prosobranchia. In: Grimpe E, Wägler E (eds) Die Tierwelt der Nord- und Ostsee, Akademische Verlagsgemeinschaft, Leipzig
Arnold DC (1972) Salinity tolerances of some common prosobranchs. J Mar Biol Assoc 52:475–486
Ansell AD (1968) The rate of growth of the hard clam Mercenaria mercenaria (L) throughout the geographic range. J Cons Int Explor Mer 31:364–409
Barroso CM, Nuñez M, Richardson CE, Moreira MH (2005) The gastropod statolith: a tool for determining the age of Nassarius reticulates. Mar Biol 146:1139–1144
Berry WBN, Barker RM (1968) Fossil bivalve shells indicate longer month and year in Cretaceous than Present. Nature 217:938–939
Brand U, Veizer J (1980) Chemical diagenesis of a multicomponent carbonate system: 1. Trace elements. J Sediment Petrol 50:1219–1236
Bourget E, Crisp DJ (1975) Factors affecting deposition of the shell in Balanus balanoides (L). J Mar Biol Assoc UK 55:231–249
Buick DP, Ivany LC (2004) 100 years in the dark: extreme longevity of Eocene bivalves from Antarctica. Geology 32:921–924
Birkett DA, Maggs CA, Dring MJ, Boaden PJS, Seed R (1998) Infralittoral Reef Biotopes with Kelp Species, vol VII. An overview of dynamic and sensitivity characteristics for conservation management of marine SACs. Scottish Assoc Mar Sci (UK Marine SACs Project). Available online at: http://www.ukmarinesac.org.uk/pdfs/reefkelp.pdf
Bode A, Lombas I, Anadon N (1986) Preliminary studies on the reproduction and population dynamics of Monodonta lineata and Gibbula umbilicalis (Mollusca, Gastropoda) on the central coast of Asturias (N. Spain). Hydrobiol 142:31–39
Carré M, Bentaleb I, Blamart D, Ogle N, Cardenas F, Zevallos S, Kalin RM, Ortlieb L, Fontugne M (2005) Stable isotopes and sclerochronology of the bivalve Mesodesma donacium: potential application to Peruvian paleoceanographic reconstructions. Palaeogeog Palaeoclimatol 228:4–25
Cespuglio G, Piccinetti C, Longinelli A (1999) Oxygen and carbon isotope profiles from Nassa mutabilis shells (Gastropoda): accretion rates and biological behaviour. Mar Biol 135:627–634
Cledón M, Brey T, Penchaszadeh PE, Arntz W (2005) Individual growth and somatic production in Adelomelon brasiliana (Gastropoda; Volutidae) off Argentina. Mar Biol 147:447–452
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 63:1049–1057
Ebling FJ, Kitching JA, Purchon RD, Bassindale R (1948) The ecology of the Lough Ine Rapids with special reference to water currents. 2. The fauna of the Saccorhiza canopy. J Anim Ecol 17:223–244
Evans JW (1972) Tidal growth increments in the cockle Clinocardium nuttalli. Science 176:416–417
Franke H-D, Buchholz F, Wiltshire KH (2004) Ecological long-term research at Helgoland (German Bight, North Sea) retrospect and prospect—an introduction. Helgoland Mar Res 58:223–229
Fredriksen S (2003) Food web studies in a Norwegian kelp forest based on stable isotope (δ13C and δ15N) analysis. Mar Ecol Prog Ser 260:71–81
Gaudèncio MJ, Guerra MT (1986) Preliminary observations on Gibbula umbilicalis (da Costa, 1778) on the Portuguese coast. Hydrobiol 142:23–30
Giménez J, Brey T, Mackensen A, Penchaszadeh PE (2004) Age, growth and mortality of the prosobranch Zidona dufresnei (Donovan, 1823) in the Mar del Plata area, south-western Atlantic Ocean. Mar Biol 145:707–712
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
Graham A (1988) Molluscs: prosobranch and pyramidellid gastropods: keys and notes for the identification of the species. Leiden, Brill
Grossman EL, Ku TL (1986) Oxygen and carbon isotope fractionation in biogenic aragonite: temperature effects. Chem Geol 59:59–74
Harzhauser M, Kowalke T (2002) Sarmatian (Late Middle Miocene) gastropod assemblages of the Central Paratethys. Facies 46:57–82
Henderson JT (1929) Lethal temperatures of Lamellibranchiata. Contrib Can Biol Fish 4:399–411
Hickson JA, Johnson ALA, Heaton THE, Balson PS (1999) The shell of the Queen Scallop Aequipecten opercularis (L.) as a promising tool for palaeoenvironmental reconstruction: evidence and reasons for equilibrium stable-isotope incorporation. Palaeogeog Palaeoclimatol 154:325–337
Ilano AS, Itoa A, Fujinagac K, Nakaoa S (2004) Age determination of Buccinum isaotakii (Gastropoda: Buccinidae) from the growth striae on operculum and growth under laboratory conditions. Aquacult 242:181–195
Jones DS (1981) Annual growth increments in shells of Spisula solidissima record marine temperature variability. Science 211:165–167
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
Jones DS, Allmon WD (1995) Records of upwelling, seasonality and growth in stable-isotope profiles of Plicoene mollusk shells from Florida. Lethaia 28:61–74
Kendall MA, Lewis JR (1986) Temporal and spatial patterns in the recruitment of Gibbula umbilicalis. Hydrobiol 142:15–22
Kennish MJ, Olsson RK (1975) Effects of thermal discharges on the microstructural growth of Mercenaria mercenaria. Environ Geol (Berl) 1:41–64
Kideys AE (1996) Determination of age and growth of Buccinum undatum L. (Gastropoda) off Douglas, Isle of Man. Helgoländer Meeresunters 50:353–368
Kobashi T, Grossman EL (2003) The oxygen isotope record of seasonality in Conus shells and its application to understanding late middle Eocene (38Ma) climate. Paleont Res 7:343–355
Lewis JR, Bowman RS, Kendall MA, Williamson P (1982) Some geographical components in population dynamics: possibilities and realities in some littoral species. Netherlands J Sea Res 16:18–28
Loosanoff VL (1939) Effect of temperature upon shell movements of clams, Venus mercenaria (L.). Biol Bull (Woods Hole) 76:171–182
Lüning K (1969) Standing crop and leaf area index of the sublittoral Laminaria species near Helgoland. Mar Biol 3:282–286
Lüning K (1990) Seaweeds: their environment, biogeography, and ecophysiology. Wiley, New York, p 527
Muntz L, Ebling FJ, Kitching JA (1965) The ecology of Lough Ine. J Anim Ecol 34:315–329
Mutvei H, Westermark T, Dunca E, Carell B, Forberg S, Bignert A (1994) Methods for the study of environmental changes using the structural and chemical information in molluscan shells. Bull Mus Oceanogr Monaco 13:163–186
Nelson-Smith A (1967) Marine biology of Milford Haven: the distribution of littoral plants and animals. Field Stud 2:435–477
Ohno T (1989) Palaeotidal characteristics determined by microgrowth patterns in bivalves. Palaeontology 32:237–263
Palmer JD, Williams BG, Dowse HB (1994) The statistical analysis of tidal rhythms: tests of the relative effectiveness of five methods using model simulations and actual data. Mar Behav Physiol 24:165–182
Peck AL (1970) Aristotle. Historia animalium (Translator), Vol II, Books 4–6. Loeb Classical Library, Heinemann, London and Harvard University Press, Cambridge, MA
Pelseneer P (1933) La durée de la vie et l’âge de la maturité sexuelle chez certains mollusques. Ann Soc Roy Zool Bel 64:93–104
Pizzolla PF (2002) Gibbula cineraria. Grey top shell. Marine life information network: biology and sensitivity key information sub-programme (on-line). Plymouth: Mar Biol Ass UK (cited 03/02/2006). Available from: http://www.marlin.ac.uk/species/Gibbulacineraria.htm
Raven JA, Johnston AM, Kübler JE, Korb R, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Clayton MN, Vanderklift M, Fredriksen S, Dunton KH (2002) Seaweeds in cold seas: evolution and carbon acquisition. Ann Bot 90:525–536
Richardson CA Saurel C Barroso CM, Thain J (2005) Evaluation of the age of the red whelk Neptunea antiqua using statoliths, opercula and element ratios in the shell. J Exp Mar Biol Ecol 325:55–64
Santarelli L, Gros P (1985) Détermination de l’âge et de la croissance de Buccinum undatum L. (Gasteropoda Prosobranchia) à l’aide des isotopes stables de la coquille et de l’ornamentation operculaire. Oceanol Acta 8:221–229
Sato S (1997) Shell microgrowth patterns of bivalves reflecting seasonal change of phytoplankton abundance. Paleontol Res 1:260–266
Schöne BR, Tanabe K, Dettman DL, Sato S (2003) Environmental controls on shell growth rates and δ18O of the shallow-marine bivalve mollusk Phacosoma japonicum in Japan. Mar Biol 142:473–485
Schöne BR (2003) A ‘clam-ring’ master-chronology constructed from a short-lived bivalve mollusc from the northern Gulf of California, USA. Holocene 13:39–49
Schöne BR, Houk SD, Freyre Castro AD, Fiebig J, Kröncke I, Dreyer W, Oschmann W (2005a) Daily growth rates in shells of Arctica islandica: assessing subseasonal environmental controls on a long-lived bivalve mollusk. Palaios 20:78–92
Schöne BR, Dunca E, Fiebig J, Pfeiffer M, 2005b. Mutvei’s solution: an ideal agent for resolving microgrowth structures of biogenic carbonates. Palaeogeog Palaeoclimatol 228:149–166
Schöne BR, Rodland DL, Fiebig J, Oschmann W, Goodwin D, Flessa KW, Dettman D (2006) Reliability of multitaxon, multiproxy reconstructions: environmental conditions from accretionary biogenic skeletons. J Geol 114:267–285
Shepherd SA, Woodby D, Rumble JM, Avalos-Borja M (2000) Microstructure, chronology and growth of the Pinto abalone, Haliotis kamtschatkana, in Alaska. J Shellf Res 19:219–228
Shigemiya Y, Kato M (2001) Age distribution, growth, and lifetime copulation frequency of a freshwater snail, Clithon retropictus (Neritidae). Popul Ecol 43:133–140
Sire J-Y, Bonnet P (1984) Croissance et structure de l’opercule calcifié du gastéropode polynésien Turbo setosus (Prosobranchia: Turbinidae): détermination de l’âge individuel. Mar Biol 79:75–87
Takada Y (1995) Variation of growth rate with tidal level in the gastropod Monodonta labio on a boulder shore. Mar Ecol Prog Ser 117:103–110
Thompson I (1975) Biological clocks and shell growth in bivalves. In: Rosenberg GD, Runcorn SK (eds) Growth rhythms and the history of the earth’s rotation. Wiley, London, pp 149–161
Underwood AJ (1972) Spawning, larval development and settlement behaviour of Gibbula cineraria (Gastropoda: Prosobranchia) with a reappraisal of torsion in gastropods. Mar Biol 17:341–349
Vermeij GJ (1980) Gastropod shell growth rate, allometry, and adult size: environmental implications. In: Rhoads DC, Lutz RA (eds) Skeletal growth of aquatic organisms. Plenum, New York, pp. 379–394
Vincent B, Villancourt G (1981) Méthode de détermination de l’âge, longévité et croissance annuelle de Bithynia tentaculata L. (Gastropoda Prosobranchia) dans le Saint-Laurent (Québec). Can J Zool 59:981–985
Wehrmann A (1998) Modern cool-water carbonates on a coastal platform of Northern Brittany: carbonate production of macrophytic systems and sedimentary dynamics of bioclastic facies. Senckenbergiana maritime 28:151–166
Williams EE (1964) The growth and distribution of Gibbula umbilicalis (da Costa) on a rocky shore in Wales. J Anim Ecol 33:433–442
Williamson P, Kendall MA (1981) Population age structure and growth of the trochid Monodonta lineata determined from shell rings. J Mar Biol Assoc UK 61:1011–1026
Wiltshire KH, Manly BFJ (2004) The warming trend at Helgoland Roads, North Sea: phytoplankton response. Helgoland Mar Res 58:269–273
Witbaard R (1996) Growth variations in Arctica islandica L. (Mollusca) a reflection of hydrography-related food supply. ICES J Mar Sci 53:981–987
Zolotarev VN (1980) The life span of bivalves from the Sea of Japan and Sea of Okhotsk. Soviet J Mar Biol 6:301–308
Acknowledgments
We are indebted to Karen Wiltshire (Biologische Anstalt Helgoland) for providing instrumental temperature and salinity data. Rainer Petschick kindly conducted XRD analyses of two specimens. This study has been made possible by a German Research Foundation (DFG) grant (to the senior author) within the framework of the Emmy Noether Program for the promotion of young scientists (SCHO 793/1). DLR kindly acknowledges a research grant provided by the Alexander von Humboldt Foundation. Experiments performed in this article comply with the current laws of Germany.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by O. Kinne, Oldendorf/Luhe
Rights and permissions
About this article
Cite this article
Schöne, B.R., Rodland, D.L., Wehrmann, A. et al. 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, 1237–1252 (2007). https://doi.org/10.1007/s00227-006-0435-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-006-0435-9