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Estuaries and Coasts

, Volume 37, Issue 2, pp 436–448 | Cite as

Variability of Stable Isotope Fingerprints of the Serpulid Ficopomatus enigmaticus Within a Permanently Stratified Estuary: Implications for (Palaeo)environmental Interpretations

  • Sonja Lojen
  • Marijana Cukrov
  • Neven Cukrov
Article

Abstract

This paper examines how the mixing of freshwater and seawater, and related mixing of freshwater and marine particulate organic matter (POM) in the permanently stratified estuary of the River Krka, Croatia, are reflected in the stable isotope fingerprints of soft tissues and tubes of the serpulid Ficopomatus enigmaticus. The carbon stable isotope composition (δ13C values) of the river-borne POM is retained over long distances, causing a depletion in 13C of POM in brackish waters. A trophic depletion in 13C was recorded in serpulid soft tissues. The serpulid carbonate tubes were depleted in 13C even at locations with salinity close to that of the sea and were subject to large isotope fractionation between dissolved inorganic C (DIC) and carbonate caused by vital effects, making carbonate depleted in 13C by several per mil compared with DIC. These effects, though large in the freshwater zone, fade towards the sea. The carbonate δ18O values of tubes reflect the δ18O values of the water. The temperature-related differences in δ18O values of tubes from different sites are masked by source-related differences in the δ18O values of water arising from mixing of freshwater and seawater in the estuary. Therefore, in serpulide tubes, the terrestrial component can easily be overestimated because of vital effects during biomineralisation and trophic depletion in 13C in freshwater and brackish environments.

Keywords

Polychaete Particulate organic matter Organic carbon Carbonate Stable isotopes Estuary 

Notes

Acknowledgements

This study was funded by the Ministry of Science, Education and Sport of the Republic of Croatia (project 098-0982934-2720) and the Slovenian Research Agency (research programme P1-0134 and bilateral Slovenian–Croatian research cooperation project BI-HR 12-13/032). The authors thank Mr. Branko Jalžić from the Croatian Biospeleological Society for sampling in the cave. Sincere thanks to three anonymous reviewers for their thoughtful comments and suggestions and Dr. Anthony R. Byrne for linguistic corrections.

References

  1. Antonioli, F., A. Silenzi, and S. Frisia. 2001. Tyrrhenian Holocene palaeoclimate trends from spelean serpulids. Quaternary Science Reviews 20: 1661–1670.CrossRefGoogle Scholar
  2. Bazterrica, M.C., F. Botto, and O. Iribarne. 2012. Effects of an invasive reef-building polychaete on the biomass and composition of estuarine macroalgal assemblages. Biological Invasions 14: 765–777.CrossRefGoogle Scholar
  3. Bianchi, C.N., and C. Morri. 1996. Ficopomatus 'reefs' in the Po River Delta (Northern Adriatic): Their constructional dynamics, biology, and influences on the brackish-water biota. Marine Ecology 17: 51–66.CrossRefGoogle Scholar
  4. Bilinski, H., Ž. Kwokal, M. Plavšić, M. Wrischer, and M. Branica. 2000. Mercury distribution in the water column of the stratified Krka river estuary (Croatia): Importance of natural organic matter and of strong winds. Water Research 34: 2001–2010.CrossRefGoogle Scholar
  5. Bonacci, O., and I. Ljubenkov. 2005. New insights into the Krka river hydrology. Hrvatske vode 13: 265–281. in Croatian, with English abstract.Google Scholar
  6. Bruschetti, M., C. Bazterrica, E. Fanjul, T. Luppi, and O. Iribarne. 2011. Effect of biodeposition of an invasive polychaete on organic matter content and productivity of the sediment in a coastal lagoon. Journal of Sea Research 66: 20–28.CrossRefGoogle Scholar
  7. Buljan, M., and M. Zore-Amanda. 1979. Hydrographic properties of the Adriatic Sea in the period from 1965 through 1970. Acta Adriatica 20: 1–368.Google Scholar
  8. Burdige, D.J. 2007. Preservation of organic matter in marine sediments: Controls, mechanisms, and an imbalance in sediment organic carbon budgets? Chemical Reviews 107: 467–485.CrossRefGoogle Scholar
  9. Carabel, S., E. Godínez-Domínguez, P. Verísomo, L. Fernández, and J. Freire. 2006. An assessment of sample processing methods for stable isotope analyses of marine food webs. Journal of Experimental Marine Biology and Ecology 336: 254–261.CrossRefGoogle Scholar
  10. Cetinić, I., D. Viličić, Z. Burić, and G. Olujić. 2006. Phytoplankton seasonality in a highly stratified karstic estuary (Krka, Adriatic Sea). Hydrobiologia 555: 31–40.CrossRefGoogle Scholar
  11. Coffin, R.B., L.A. Cifuentes, and P.M. Elderidge. 1994. The use of stable carbon isotopes to study microbial processes in estuaries. In Stable Isotopes in Ecology and Environmental Science, ed. K. Lajtha and R.H. Michener, 222–240. London: Blackwell Scientific.Google Scholar
  12. Coplen, T.B. 2011. Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Communications in Mass Spectrometry 24: 2538–2560.CrossRefGoogle Scholar
  13. Cukrov, M. 2011. Biologija i ekologija vrste Ficopomatus enigmaticus (Fauvel, 1923) duž istočne obala Jadrana (Biology and ecology of the species Ficopomatus enigmaticus (Fauvel ,1923) (Annelida, Polychaeta) along the Eastern Adriatic coast). PhD Thesis (in Croatian with English abstract). Zagreb: University of Zagreb, Faculty of Science, Department of Geology.Google Scholar
  14. Davies, B.R., V. Stuart, and M. de Villiers. 1989. The filtration activity of a serpulid polychaete population (Ficopomatus enigmaticus (Fauvel)) and its effects on water quality in a coastal marina. Estuarine, Coastal and Shelf Science 29: 613–620.CrossRefGoogle Scholar
  15. Dixon, D.R. 1980. The energetics of tube production by Mecierella enigmatica (Polychaeta: Serpulidae). Journal of the Marine Biological Association of the United Kingdom 60: 655–659.CrossRefGoogle Scholar
  16. Dolenec, T., S. Lojen, Ž. Lambaša, and M. Dolenec. 2006a. Effects of fish farm loading on seagrass Posidonia oceanica at Vrgada Island (Central Adriatic): A nitrogen stable isotope study. Isotopes in Environmental and Health Studies 42: 77–85.CrossRefGoogle Scholar
  17. Dolenec, T., S. Lojen, M. Dolenec, Ž. Lambaša, M. Dobnikar, and N. Rogan. 2006b. 15N and 13C enrichment in Balanus perforatus: Tracers of municipal particulate waste in the Murter Sea (Central Adriatic, Croatia). Acta Chimica Slovenica 53: 469–476.Google Scholar
  18. Dolenec, T., S. Lojen, G. Kniewald, M. Dolenec, and N. Rogan. 2007. Nitrogen stable isotope composition as a tracer of fish farming in invertebrates Aplisina aerophoba, Balanus perforatus and Anemonia sulcata in central Adriatic. Aquaculture 262: 237–249.CrossRefGoogle Scholar
  19. Dolenec, M., P. Žvab, G. Mihelčić, Ž. Lambaša Belak, S. Lojen, G. Kniewald, T. Dolenec, and N. Rogan Šmuc. 2011. Use of stable nitrogen isotope signatures of anthropogenic organic matter in the coastal environment: A case study of the Kosirina Bay (Murter Island, Croatia). Geologia Croatica 64: 143–152.CrossRefGoogle Scholar
  20. Fagerstrom, J.A. 1987. The Evolution of Reef Communities. New York: Wiley. 600 pp.Google Scholar
  21. Fanelli, E., J.E. Cartesa, and V. Papiola. 2011. Food web structure of deep-sea macrozooplankton and micronekton off the Catalan slope: Insight from stable isotopes. Journal of Marine Systems 87: 79–89.CrossRefGoogle Scholar
  22. Fornós, J.J., V. Forteza, and A. Martínez-Taberner. 1997. Modern polychaete reefs in Western Mediterranean lagoons: Ficopomatus enigmaticus (Fauvel) in the Albufera of Menorca, Balearic Islands. Palaeogeography, Palaeoclimatology, Palaeoecology 128: 175–186.CrossRefGoogle Scholar
  23. Friebe, J.G. 1994. Serpulid-Bryozoan-Foraminiferal biostromes controlled by temperate climate and reduced salinity: Middle Miocene of the Styrian Basin, Austria. Facies 30: 51–62.CrossRefGoogle Scholar
  24. Glasby, C.J., and T. Timm. 2008. Global diversity of polychaetes (Polychaeta; Annelida) in freshwater. Hydrobiologia 595: 107–115.CrossRefGoogle Scholar
  25. Glumac, B., Berrios, L., Greer, L., and H. A. Curran. 2004. Holocene tufa-coated serpulid mounds from the Dominican Republic: Depositional and diagenetic history, with comparison to Modern serpulid aggregates from Baffin Bay, Texas, Texas. Proceedings of the 11th Symposium on the Geology of the Bahamas and Other Carbonate Regions, p. 49–65.Google Scholar
  26. Grey, J., R.I. Jones, and D. Sleep. 2000. Stable isotope analysis of the origins of zooplankton carbon in lakes of differing trophic state. Oecologia 123: 232–240.CrossRefGoogle Scholar
  27. Grey, J., S. Waldron, and R. Hutchinson. 2004. The utility of carbon and nitrogen isotope analyses to trace contributions from fish farms to the receiving communities of freshwater lakes: a pilot study in Easthwaite Water, UK. Hydrobiologia 524: 253–262.CrossRefGoogle Scholar
  28. Hammer, Ø., H.A. Nakrem, C.T.S. Little, K. Hrzyniewicz, M.R. Sandy, J.H. Hurum, P. Druckenmiller, E.M. Knutsen, and M. Høyberget. 2011. Hydrocarbon seeps from close to the Jurassic-Cretaceous boundary, Svalbard. Palaeogeography, Palaeoclimatology, Palaeoecology 306: 15–26.CrossRefGoogle Scholar
  29. Hatten, J.A., M.A. Goñi, and R.A. Wheatcroft. 2012. Chemical characteristics of particulate organic matter from a small, mountainous river system in the Oregon Coast Range, USA. Biogeochemistry 107: 43–66.CrossRefGoogle Scholar
  30. Hedges, J.I., and P.L. Parker. 1976. Land-derived organic matter in surface sediments from the Gulf of Mexico. Geochimica et Cosmochimica Acta 40: 1019–1029.CrossRefGoogle Scholar
  31. Hedges, J.I., R.G. Keil, and R. Benner. 1997. What happens to terrestrial organic matter in the ocean? Organic Geochemistry 27: 195–212.CrossRefGoogle Scholar
  32. Herlec, U. 2005. Izotopska sestava kisika in ogljika v jadranskih moluskih, iglokožcih, serpulah, otolitih, rdečih algah, briozojih, ciripednih rakih in brahiopodih = Isotope composition of oxygen and carbon in the Adriatic molluscs, echinoderms, serpulids, otoliths, red algae, bryozoans, barnacles and brachiopods, (In Slovene, with English abstract). PhD Thesis, Ljubljana: University of Ljubljana, Faculty of Natural Sciences and Engineering.Google Scholar
  33. Hill, M.B. 1967. The life cycles and salinity tolerance in the serpulid Mercierella enigmatica Fauvel and Hydroides unicata (Philippi) at Lagos, Nigeria. Journal of Animal Ecology 36: 302–332.CrossRefGoogle Scholar
  34. Hitchon, B., and H.R. Krouse. 1972. Hydrogeochemistry of the surface waters of the Mackenzie River drainage basin, Canada-III, stable isotopes of oxygen, carbon and sulphur. Geochimica et Cosmochimica Acta 36: 1337–1357.CrossRefGoogle Scholar
  35. Jímenez-López, C., E. Caballero, F.J. Huertas, and C. Romanek. 2001. Chemical, mineralogical and isotope behavior, and phase transformation during the precipitation of calcium carbonate minerals from intermediate ionic solution at 25°C. Geochimica et Cosmochimica Acta 65: 3219–3231.CrossRefGoogle Scholar
  36. Kanduč, T., D. Medaković, and B. Hamer. 2011. Mytilus galloprovincialis as a bioindicator of environmental conditions: The case of the eastern coast of the Adriatic Sea. Isotopes in Environmental and Health Studies 47: 42–61.CrossRefGoogle Scholar
  37. Lajtha, K., and R.M. Michener (eds.). 1994. Stable Isotopes in Ecology and Environmental Sciences. New York: Blackwell Science.Google Scholar
  38. Lea, D. 2003. Elemental and isotopic proxies for marine temperature. In Oceans and Marine Geochemistry, vol. 6, ed. H. Ehlenfeld, 365–390. Pergamon, Oxford: Elsevier.Google Scholar
  39. Legović, T. 1991. Exchange of water in a stratified estuary with application to Krka (Adriatic). Marine Chemistry 32: 121–135.CrossRefGoogle Scholar
  40. Legović, T., V. Žutić, Z. Gržetić, G. Cauwet, R. Precali, and D. Viličić. 1994. Eutrophication in the Krka estuary. Marine Chemistry 46: 203–215.CrossRefGoogle Scholar
  41. Lojen, S., T. Dolenec, B. Vokal, N. Cukrov, G. Mihelčić, and W. Papesch. 2004a. C and O stable isotope variability in recent freshwater carbonates (River Krka, Croatia). Sedimentology 51: 361–375.CrossRefGoogle Scholar
  42. Lojen, S., N. Ogrinc, T. Dolenec, B. Vokal, J. Szaran, G. Mihelčić, and M. Branica. 2004b. Nutrient fluxes and sulfur cycling in the organic-rich sediment of Makirina Bay (Central Dalmatia, Croatia). The Science of the Total Environment 327: 265–284.CrossRefGoogle Scholar
  43. Lojen, S., E. Spanier, A. Tsemel, T. Katz, N. Eden, and D. Angel. 2005. δ15N as a natural tracer of particulate nitrogen effluents released from marine aquaculture. Marine Biology 148: 87–96.CrossRefGoogle Scholar
  44. Lojen, S., A. Trkov, J. Ščančar, J.A. Vazquez-Navarro, and N. Cukrov. 2009. Continuous 60-year stable isotope and earth-alkali element records in a modern laminated tufa (Jaruga, river Krka, Croatia): Implications for climate reconstruction. Chemical Geology 258: 242–250.CrossRefGoogle Scholar
  45. Lojen, S., I. Sondi, and M. Juračić. 2010. Geochemical conditions for the preservation of recent aragonite-rich sediments in Mediterranean karstic marine lakes (Mljet Island, Adriatic Sea, Croatia). Marine and Freshwater Research 61: 119–128.CrossRefGoogle Scholar
  46. Minagawa, M., and E. Wada. 1984. Stepwise enrichment of 15N along food chains: Further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48: 1135–1140.CrossRefGoogle Scholar
  47. Morrison, J.O., and U. Brand. 1986. Geochemistry of recent marine invertebrates. Geoscience Canada 13: 237–254.Google Scholar
  48. Ogrinc, N., G. Fontolan, J. Faganeli, and S. Covelli. 2005. Carbon and nitrogen isotope compositions of organic matter in coastal marine sediments (Gulf of Trieste, N Adriatic Sea): Indicators of sources and preservation. Marine Chemistry 95: 163–181.CrossRefGoogle Scholar
  49. O'Leary, M.H. 1988. Carbon isotopes in photosynthesis. BioScience 38: 328–336.CrossRefGoogle Scholar
  50. O’Neil, J.R., R.N. Clayton, and T.K. Mayeda. 1969. Oxygen isotope fractionation of divalent metal carbonates. Journal of Chemical Physics 30: 5547–5558.CrossRefGoogle Scholar
  51. Peterson, B.J., and B. Fry. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology, Evolution, and Systematics 18: 293–320.CrossRefGoogle Scholar
  52. Reinhardt, E.G., D.J. Stanley, and H.P. Schwarcz. 2001. Human-induced desalinization of Manzala Lagoon, Nile Delta, Egypt: Evidence from isotope analysis of benthic Invertebrates. Journal of Coastal Research 17: 431–442.Google Scholar
  53. Romanek, C.S., E.L. Grossman, and J.W. Morse. 1992. Carbon isotope fractionation in synthetic aragonite and calcite: Effects of temperature and precipitation rate. Geochimica et Cosmochimica Acta 56: 419–430.CrossRefGoogle Scholar
  54. Rullier, F. 1946. Croissance du tube de Mercierella enigmatica (Fauvel). Bulletin du Laboratoire Maritime de Dinard 27: 11–15.Google Scholar
  55. Sampaio, L., A.M. Rodriguez, and V. Quintino. 2010. Carbon and nitrogen stable isotopes in coastal benthic populations under multiple organic enrichment sources. Marine Pollution Bulletin 60: 1790–1802.CrossRefGoogle Scholar
  56. Schwarcz, H.P. 1991. Some theoretical aspects of isotope paleodiet studies. Journal of Archaeological Science 18: 261–275.CrossRefGoogle Scholar
  57. Sondi, I., S. Lojen, M. Juračić, and E. Prohić. 2008. Mechanisms of land–sea interactions—The distribution of metals and sedimentary organic matter in sediments of a river-dominated Mediterranean karstic estuary. Estuarine, Coastal and Shelf Science 80: 12–20.CrossRefGoogle Scholar
  58. Stabili, L., R. Schirosi, M. Licciano, E. Mola, and A. Giangrande. 2010. Bioremediation of bacteria in aquaculture waste using the polychaete Sabella spallanzanii. New Biotechnology 27: 774–781.CrossRefGoogle Scholar
  59. Svensen, C., P. Viličić, P. Wassmann, E. Arashkevich, and T. Ratkova. 2007. Plankton distribution and vertical flux of biogenic matter during high summer stratification in the Krka estuary (Eastern Adriatic). Estuarine, Coastal and Shelf Science 72: 381–390.CrossRefGoogle Scholar
  60. Tebble, N. 1953. A source of danger to harbour structures—Encrustation by a tubed marine worm. Journal of the Institute of Municipal Engineers 80: 259–265.Google Scholar
  61. Turpaeva, E.P. 1961. The relation of the Black Sea Mercierella enigmatica (Fauv.) to conditions of various salinity. Trudy Instituta Okeanologii Akademii Nauk SSSR 49: 187–199.Google Scholar
  62. Videtich, P.E. 1986. Stable-isotope compositions of serpulids give insights to calcification processes in marine organisms. Palaios 1: 189–193.CrossRefGoogle Scholar
  63. Viličić, D., D. Petricioli, and N. Jasprica. 1990. Seasonal Phytoplankton Distribution in the Krka Estuary and Visovac Lake (in Croatian). In: National Park Krka, Status of Research and Problems of Ecosystem Protection. Zagreb: Croatian Ecological Society.Google Scholar
  64. Vinagre, C., C. Máguas, H.N. Cabral, and M.J. Costa. 2011. Nekton migration and feeding location in a coastal area—A stable isotope approach. Estuarine, Coastal and Shelf Science 91: 544–550.CrossRefGoogle Scholar
  65. Vinn, O., H.A. ten Hove, H. Mutvei, and K. Kirsimäe. 2008. Ultrastructure and mineral composition of serpulid tubes (Polychaeta, Annelida). Zoological Journal of the Linnean Society 154: 633–650.CrossRefGoogle Scholar
  66. Wada, E., H. Mizutani, and M. Minagawa. 1991. The use of stable isotopes for food web analysis. Critical Reviews in Food Science and Nutrition 30: 361–371.CrossRefGoogle Scholar
  67. Wada, E., Y. Kabaya, and Y. Kurihara. 1993. Stable isotope structure of aquatic ecosystems. Journal of Biosciences 18: 483–499.CrossRefGoogle Scholar
  68. Wefer, G., and W.H. Berger. 1991. Isotope paleontology: Growth and composition of extant calcareous species. Marine Geology 100: 207–248.CrossRefGoogle Scholar
  69. Woulds, C., J.J. Middelburg, and G.L. Cowie. 2012. Alteration of organic matter during infaunal polychaete gut passage and links to sediment organic geochemistry. Part I: Amino acids. Geochimica et Cosmochimica Acta 77: 396–414.Google Scholar
  70. Yoshii, K., N. Melnik, O.A. Timoshkin, N.A. Bondarenko, P.N. Anoshko, T. Yoshioka, and E. Wada. 1999. Stable isotope analyses of the pelagic food web in Lake Baikal. Limnology and Oceanography 44: 502–511.CrossRefGoogle Scholar
  71. Žutić, V., and T. Legović. 1987. A film of organic matter at the freshwater/seawater interface in an estuary. Nature 328: 612–614.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2013

Authors and Affiliations

  1. 1.Department of Environmental SciencesJožef Stefan InstituteLjubljanaSlovenia
  2. 2.Croatian Biospeleological SocietyZagrebCroatia
  3. 3.Division for Marine and Environmental ResearchRuđer Bošković InstituteZagrebCroatia

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