Skip to main content

Advertisement

SpringerLink
Log in

The use of the marine gastropod, Cellana tramoserica, as a biomonitor of metal contamination in near shore environments

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

The use of the marine gastropod, Cellana tramoserica, as a biomonitor of metal exposure was investigated. The factors influencing metal concentrations, such as mass, gender, substrate, shoreline position and temporal variation were examined. Tissue metal concentrations were mostly found to be independent of mass and gender. When metal concentrations were significantly correlated with mass, correlations were low and explained little variability. The underlying substrate and position in the littoral zone had only a small influence on metal concentrations. Variation between individuals, inherent variability due to genetic variability, was the most significant contribution to the overall variation in metal concentrations, resulting in positive skewing of population distributions. The mean metal concentrations varied temporally; metal masses were relatively constant with fluctuations in metal concentrations related to fluctuations in metal body burdens. The populations from a metal-contaminated site had significantly higher tissue Cu, Zn, As and Pb concentrations than the populations from relatively uncontaminated locations. C. tramoserica therefore can be considered to be a net accumulator of metals. A sample number of >10 is required to detect changes of 25 % from the mean concentrations at uncontaminated locations. This species meets the requirements of a suitable biomonitor for metal contaminants in the environment i.e. hardy, sessile, widespread, sufficient tissue mass and a metal accumulator. As the measurement of metal concentrations in C. tramesoria were influenced by substrate and shore position and, sometimes, mass, sites with similar substrates and organisms of similar mass and shoreline position should be chosen for comparison. When comparing metal concentrations in gastropods from different locations, they should be collected over the same period to minimise variability due to mass differences, spawning and other seasonal/temporal effects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • ABS. (1996). Australian Bureau of Statistics-Census Data http://www.abs.gov.au/census.

  • Ahn, I.-Y., Kim, K.-W., & Choi, J. (2002). A baseline study on metal concentrations in the Antarctic limpet Nacella concinna (Gastropoda: Patellidae) on King George Island: variations with sex and body parts. Marine Pollution Bulletin, 44, 421–431.

    Article  Google Scholar 

  • Baldwin, S., Deaker, M., & Maher, W. (1994). Low-volume microwave digestion of marine biological tissues for the measurement of trace elements. Analyst, 119, 1701–1704.

    Article  CAS  Google Scholar 

  • Blackmore, G. (2001). Interspecific variation in heavy metal body concentrations in Hong Kong marine invertebrates. Environmental PollutIon, 114, 303–311.

    Article  CAS  Google Scholar 

  • Boyden, C. R. (1977). Effect of size upon metal content of shellfish. Journal of the Marine Biology Association of UK, 57, 675–714.

    Article  CAS  Google Scholar 

  • Brown, M. T., & Depledge, M. H. (1998) Determinants of trace metal concentrations in marine organisms. Chpt 7. In W. J. Langstone, & M. J. Bebianno (eds), Metal metabolism in Aquatic Environments (pp 185–217). Chapman and Hall London.

  • Bryan, G. W., Potts, G. W., & Forster, G. R. (1977). Indicators of heavy-metal contamination in the Looe Estuary (Cornwall) with particular regard to silver and lead. Journal of the Marine Biological Association UK, 57, 370–390.

    Google Scholar 

  • Brzoska, M. M., & Moniuszko-Jakoniuk, J. (2001). Interactions between cadmium and zinc in the organism. Food and Chemical Toxicology, 39, 967–980.

    Article  CAS  Google Scholar 

  • Burt, A., Maher, W., Roach, A., Krikowa, F., Honkoop, P., & Bayne, B. L. (2007). The accumulation of Zn, Se, Cd and Pb and physiological condition of Anadara trapezia transplanted to a contamination gradient in Lake Macquarie, New South Wales, Australia. Marine Environmental Research, 64(1), 54–78.

    Article  CAS  Google Scholar 

  • Chapman, P. M. (1985). Effects of gut sediment contents on measurements of metal levels in benthic invertebrates—a cautionary note. Bulletin of Environmental Contamination and Toxicology, 35, 345–347.

    Article  CAS  Google Scholar 

  • Chelazzi, G., De Pirro, M., & Willims, G. A. (2004). Different cardiac response to copper in limpets from metal polluted and clean shores of Hong Kong. Marine Environmental Research, 58, 83–93.

    Article  CAS  Google Scholar 

  • Cossa, D., Bourget, E., & Piuze, J. (1979). Sexual maturation as a source of variation in the relationship between cadmium concentration and body weight of Mytilus edulis L. Marine Pollution Bulletin, 10, 174–176.

    Article  Google Scholar 

  • Creese, R. G., & Ballantine, W. J. (1983). An assessment of breeding in the intertidal limpet Cellana radians (Gmelin). Journal of Experimental Marine Biology and Ecology, 67, 43–59.

    Article  Google Scholar 

  • Creese, R. G., & Underwood, A. J. (1982). Analysis of inter- and intra-specific competition amongst intertidal limpets with different methods of feeding. Oecologia, 53, 337–346.

    Article  Google Scholar 

  • Cubadda, F., Conti, M. E., & Campanella, L. (2001). Size-dependent concentrations of trace metals in four Mediterranean gastropods. Chemosphere, 45, 561–569.

    Article  CAS  Google Scholar 

  • Daka, E. R., & Hawkins, S. J. (2006). Interactive effects of copper, cadmium and lead on zinc accumulation in the gastropod mollusc Littorina saxatilis. Water, Air, and Soil Pollution, 171, 19–28.

    Article  CAS  Google Scholar 

  • Edgar, G. J. (2008). Australian marine life (2nd ed.), (p 272). Australia: Reed New Holland Publishers.

  • Fairweather, P. G., & Underwood, A. J. (1991). Experimental removal of a rocky intertidal predator: variations within two habitats in the effects on prey. Journal of Experimental Marine Biology and Ecology, 154, 29–75.

    Article  Google Scholar 

  • Felstein, T., Kashman, Y., Abelson, A., Fishelson, L., Mokady, O., Bresler, V., & Erel, Y. (2003). Marine molluscs in environmental monitoring. III. Trace metals and organic pollutants in animal tissues and sediments. Marine Research, 57, 212–219.

    Google Scholar 

  • Fletcher, W. J. (1984a). Interspecific variation in population dynamics and growth of the limpet, Cellana tramoserica. Oecologia, 63, 110–121.

    Article  Google Scholar 

  • Fletcher, W. J. (1984b). Variability in the reproductive effort of the limpet, Cellana tramoserica. Oecologia, 61, 259–264.

    Article  Google Scholar 

  • Fletcher, W. J., & Creese, R. G. (1985). Competitive interactions between co-occurring herbivorous gastropods. Marine Biology, 86, 183–191.

    Article  Google Scholar 

  • Frazier, J. M. (1976). The dynamics of metals in the American oyster, Crassostrea virginica. II. Environmental effects. Chesapeake Science, 17(3), 188–197.

    Article  CAS  Google Scholar 

  • Gay, D., & Maher, W. A. (2003). Natural variation of copper, zinc, cadmium and selenium concentrations in Bembicium namum and their potential use as a biomonitor of trace metals. Water Research, 37, 2173–2185.

    Article  CAS  Google Scholar 

  • He, Z., & Morrison, R. J. (2001). Changes in the marine environment of Port Kembla Harbour, NSW, Australia, 1975–1995: a review. Marine Pollution Bulletin, 42, 193–201.

    Article  CAS  Google Scholar 

  • Herut, B., Kress, N., Shefer, E., & Hornung, H. (1999). Trace elements levels in mollusks form clean and polluted coastal marine sites in the Mediterranean, Red and North Seas. Marine Research, 53, 154–162.

    Google Scholar 

  • Hung, T.-C., Meng, P.-J., Han, B.-C., Chuang, A., & Huang, C.-C. (2001). Trace metals in different species of molluscs, water and sediments form Taiwan coastal area. Chemosphere, 44, 833–841.

    Article  CAS  Google Scholar 

  • Ireland, M. P., & Wootton, R. J. (1977). Distribution of lead, zinc, copper and manganese in the marine gastropods, Thais lapillus and Littorina littorea, around the coast of Wales. Environmental Pollution, 12, 27–41.

    Article  CAS  Google Scholar 

  • Kang, S. G., Wright, D. A., et al. (2000). Baseline metal concentration in the Asian periwinkle Littorina brevicula employed as a biomonitor to assess metal pollution in Korean coastal water. Science of the Total Environment, 263, 143–153.

    Article  CAS  Google Scholar 

  • Langston, W. J., & Spence, S. K. (1995). Biological factors involved in metal concentrations observed in aquatic organisms. In A. Tessier & D. R. Turner (Eds.), Metal speciation and bioavailability (pp. 407–478). New York: John Wiley.

    Google Scholar 

  • Leung, K. M. Y., Morgan, I. J., Wu, R. S. S., Lau, T. C., Svavarsson, J., & Furness, R. W. (2001). Growth rate as a factor confounding the use of the dogwhelk Nucella lapillus as biomonitor of heavy metal contamination. Marine Ecology-Progress Series, 221, 145–159.

    Article  CAS  Google Scholar 

  • Lobel, P. B., & Wright, D. A. (1982). Gonadal and nongonadal zinc concentrations in mussels. Marine Pollution Bulletin, 13, 320–323.

    Article  CAS  Google Scholar 

  • Lobel, P. B., Mogie, P., Wright, D. A., & Wu, B. L. (1982). Metal accumulation in four molluscs. Marine Pollution Bulletin, 13, 170–174.

    Article  CAS  Google Scholar 

  • Maher, W., Forster, S., Krikowa, F., Snitch, P., Chapple, G., & Craig, P. (2001). Measurement of trace elements and phosphorus in marine animal and plant tissues by low-volume microwave digestion and ICP-MS. Atomic Spectroscopy, 22(5), 361–370.

    CAS  Google Scholar 

  • Martley, E., Gulson, B. L., & Pfeifer, H. R. (2004). Metal concentrations in soils around the copper smelter and surrounding industrial complex of Port Kembla, NSW, Australia. Science of the Total Environment, 325, 113–127.

    Article  CAS  Google Scholar 

  • Moran, P. J. (1984). Water quality control and its effect on the concentration of heavy metals in Port Kembla Harbour, N.S.W. Marine Pollution Bulletin, 15, 294–297.

    Article  CAS  Google Scholar 

  • Parry, G. D. (1978). Effects of growth and temperature acclimation on metabolic rate in the limpet, Cellana tramoserica (Gastropoda: Patellidae). Journal of Animal Ecology, 47, 351–368.

    Article  Google Scholar 

  • Phillips, D. J. H. (1977). The use of biological indicator organisms to monitor trace metal pollution in marine and estuarine environments-a review. Environmental Pollution, 13, 281–311.

    Article  CAS  Google Scholar 

  • Phillips, D. J. H. (1990). Use of macroalgae and invertebrates as monitors of metal levels in estuaries and coastal waters Ch. 6. In R. W. Furness & P. S. Rainbow (Eds.), Heavy metals in the marine environment (pp. 81–99). Florida: CRC Press.

    Google Scholar 

  • Phillips, D. J. H., & Rainbow, P. S. (1993). The biomonitoring of trace metals and radionuclides Ch 5. In Biomonitoring of trace aquatic contaminants (pp. 79–132). Oxford: Elsevier Science Publishers Ltd.

    Google Scholar 

  • Phillips, D. J. H., & Segar, D. A. (1986). Use of bio-indicators in monitoring conservative contaminants: programme design imperatives. Marine Pollution Bulletin, 17, 10–17.

    Article  Google Scholar 

  • Rainbow, P. S. (1995). Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin, 31, 183–192.

    Article  CAS  Google Scholar 

  • Robinson, W. A., Maher, W. A., Krikowa, F., Nell, J. A., & Hand, R. (2005). The use of the oyster Saccostrea glomerata as a biomonitor of trace metal contamination: intra-sample, local scale and temporal variability and its implications for biomonitoring. Journal of Environmental Monitoring, 7(3), 208–223.

    Article  CAS  Google Scholar 

  • SAS®. (1988). SAS/STAT user’s guide, release 6.03 edition. Cary: The SAS Institute Inc.

    Google Scholar 

  • Schmitz, H. A., Maher, W. A., Taylor, A. M., & Krikowa, F. (2015). Effects of cadmium accumulation from suspended sediments and phytoplankton on the oyster Saccostrea glomerata. Aquatic Toxicology, 160, 22–30.

    Article  CAS  Google Scholar 

  • Simpson, R. D. (1979). Uptake and loss of zinc and lead by mussels (Mytilus edulis) and relationship with body weight and reproductive cycle. Marine Pollution Bulletin, 10, 74–78.

    Article  CAS  Google Scholar 

  • Spooner, D. R., Maher, W., & Otway, N. (2003). Trace metal concentrations in sediments and oysters of Botany Bay, NSW, Australia. Archives of Environmental Contamination and Toxicology, 45, 92–101.

    Article  CAS  Google Scholar 

  • Swerdlow, R. D., Ebert, R. F., Lee, P., Bonaventura, C., & Miller, K. I. (1996). Keyhole limpet hemocyanin: structural and functional characterization of two different subunits and multimers. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 113, 537–548.

    Article  CAS  Google Scholar 

  • Taylor, A., & Maher, W. (2003). The use of two marine gastropods, Austrocochlea constricta and Bembicum auratum as biomonitors of zinc, cadmium and copper exposure. 1. Effects of mass within and between site variability and net accumulation relative to environmental exposure. Journal of Coastal Science, 19, 541–549.

    Google Scholar 

  • Taylor, A., & Maher, W. (2006). The use of two marine gastropods, Austrocochlea constricta and Bembicum auratum as biomonitors of zinc, cadmium and copper exposure. 2. Effect of tissue distribution, gender, reproductive state and temporal variation. Journal of Coastal Science, 22, 298–306.

    Article  Google Scholar 

  • Taylor, A. M., & Maher, W. A. (2012a). Exposure-dose-response of Anadara trapezia to metal contaminated estuarine sediments. 1. Cadmium spiked sediments. Aquatic Toxicology, 109, 234–242.

    Article  CAS  Google Scholar 

  • Taylor, A. M., & Maher, W. A. (2012b). Exposure-dose-response of Anadara trapezia to metal contaminated estuarine sediments. 2. Lead spiked sediments. Aquatic Toxicology, 116–117, 79–89.

    Article  Google Scholar 

  • Taylor, A. M., & Maher, W. A. (2012c). Exposure-dose-response of Anadara trapezia to metal contaminated estuarine sediments. 3. Selenium spiked sediments. Aquatic Toxicology, 124–125, 152–162.

    Article  Google Scholar 

  • Taylor, A. M., & Maher, W. A. (2013). Exposure-dose-response of Tellina deltoidalis to metal-contaminated estuarine sediments 1. Cadmium spiked sediments. Comparative Biochemistry and Physiology Part C, 158, 44–55.

    CAS  Google Scholar 

  • Taylor, A. M., & Maher, W. A. (2014a). Exposure-dose-response of Tellina deltoidalis to metal contaminated estuarine sediments 2. Lead spiked sediments. Comparative Biochemistry and Physiology, Part C, 159, 52–61.

    CAS  Google Scholar 

  • Taylor, A. M., & Maher, W. A. (2014b). Exposure-dose-response of Tellina deltoidalis to contaminated estuarine sediments 3. Selenium spiked sediments. Comparative Biochemistry and Physiology, Part C, 166, 34–43.

    CAS  Google Scholar 

  • Taylor, A. M., & Maher, W. A. (2015). Developing a sentinel mollusc species for toxicity assessment: metal exposure, dose and response—laboratory v. field exposures and resident organisms. Environmental Chemistry, 13, 434–446.

    Google Scholar 

  • Underwood, A. J. (1974). The reproductive cycles and geographical distribution of some common Eastern Australian prosobranchs (Molluscs: Gastropoda). Australian Journal of Marine and Freshwater Research, 25, 63–88.

    Article  Google Scholar 

  • Underwood, A. J. (1984). Microalgal food and the growth of the intertidal gastropods Nerita atramentosa (Reeve) and Bembicium nanum (Lamark) at four heights on shore. Journal of Experimental Biology and Ecology, 79, 277–291.

    Article  Google Scholar 

  • Underwood, A. J., & Atkinson, M. H. (1975). Rocky intertidal and subtidal habitats. In G. Cho, A. Georges, & A. Stoutjesdijk (Eds.), Jervis Bay. A place of cultural, scientific and educational value (pp. 123–132). Canberra: Australian National Parks and Wildlife Service.

    Google Scholar 

  • Underwood, A. J., & Jerkanoff, P. (1981). Effects on interactions between algae and grazing gastropods on the structure of a lowshore algal community. Oecologia, 48, 221–233.

    Article  Google Scholar 

  • Wang, W., & Dei, R. C. H. (1999). Kinetic measurements of metal accumulation in two marine microalgae. Marine Biology, 135, 11–23.

    Article  Google Scholar 

  • Waring, J. S., Maher, W. A., & Krikowa, F. (2006). Trace metal bioaccumulation in eight common coastal Australian polychaeta. Journal of Environmental Monitoring, 8, 1149–1157.

    Article  CAS  Google Scholar 

  • White, S. L., & Rainbow, P. S. (1985). On the metabolic requirements for copper and zinc in molluscs and crustaceans. Marine Environmental Research, 16, 215–229.

    Article  CAS  Google Scholar 

  • Zar, J. H. (1984). Biostatistical analysis (2nd ed.), (pp. 134–137). New Jersey: Prentice-Hall International Inc.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Ecochemistry Laboratory, University of Canberra, Canberra, ACT, 2601, Australia

    W. Maher, N Maher, A. Taylor, F. Krikowa & R. Ubrihien

  2. Climate Change Research Centre Faculty of Science, University of NSW, Randwick, NSW, 2522, Australia

    N Maher

  3. Centre for Sustainable Ecosystem Solutions, School of Biological Sciences, University of Wollongong, Wollongong, NSW, 2522, Australia

    K. M. Mikac

Authors
  1. W. Maher
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N Maher
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Krikowa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. Ubrihien
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. K. M. Mikac
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to W. Maher.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maher, W., Maher, N., Taylor, A. et al. The use of the marine gastropod, Cellana tramoserica, as a biomonitor of metal contamination in near shore environments. Environ Monit Assess 188, 391 (2016). https://doi.org/10.1007/s10661-016-5380-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-016-5380-6

Keywords

Search

Navigation