An assessment of metal contamination along the Irish coast using the seaweed Ascophyllum nodosum (Fucales, Phaeophyceae)

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Abstract

The relative abundance and variation of Cr, Co, Cd and Pb in Ascophyllum nodosum and intertidal surface sediments from six locations around the coast were assessed over six seasons. Higher Cd and Pb levels in Galway Docks and Cork Harbour were attributed to localised inputs of these metals from municipal and domestic waste, while at a reference site (Ballyconneely), high algal Cr concentrations were considered a function of geological setting rather than anthropogenic loading. Little seasonal variation was observed, with the exception of higher Co levels in plants in winter, associated with growth dynamics and increased fluvial inputs. In comparison with previously published data for metals in A. nodosum from the North Atlantic, with the exception of localised hot spots, the Irish coastline is still a relatively pristine environment. A. nodosum may be successfully and easily used as a biomonitor of metal contamination in coastal waters.

Introduction

Metal contamination in the marine environment is a widespread occurrence, and coastal regions, rather than the open ocean, are the main impacted areas (Bryan and Langston, 1992, Millward and Turner, 2001). Metal concentrations in seawater reflect both anthropogenic and natural sources (Cobelo-García et al., 2004), while the majority of the anthropogenic load is derived from municipal developments along rivers and estuaries (Ridgway et al., 2003). In recent years, Ireland has witnessed an increase in population and industrial activity, with most towns on the coastline having undergone rapid expansion. This demographic and urban pressure has led to increased discharges of waste into coastal waters, often without adequate treatment, but little research on its environmental impact has been carried out. This highlights the need for monitoring programmes to establish spatial and temporal trends in contaminant abundance and bioavailability. Biomonitors, organisms which accumulate contaminants in their tissues, can be used to assess the relative quality of coastal environments, including the presence, levels and changes of contaminants (Phillips and Rainbow, 1993, Langston and Spence, 1995, Rainbow, 1995, Amado Filho et al., 1997, Amado Filho et al., 1999). Metal content and accumulation in the brown seaweed Ascophyllum nodosum (L.) Le Jol, has been extensively studied in relation to spatial (e.g. Riget et al., 1997, Phaneuf et al., 1999, Stengel and Dring, 2000, Stengel et al., 2004) and temporal patterns (e.g. Molloy and Hills, 1996, Riget et al., 1997), accumulation and release, through transplantation studies (e.g. Myklestad et al., 1979, Eide et al., 1980), concentrations in different-aged thallus regions (Julshamn, 1981a, Stengel et al., 2005), effects on fertilisation and germination (Toth and Pavia, 2003) and relationship with phenol content (Pedersen, 1984, Toth and Pavia, 2000).

Also, sediments are widely recognised and increasingly employed in assessing the degree of contamination in marine systems (Bryan and Langston, 1992) as they act as both an important reservoir and an ultimate sink for trace metals (Mountouris et al., 2002). Metals, however, have an affinity for the finer grained, clay mineral and authigenic fraction, so that finer textured sediments contain relatively high natural metal levels (Loring, 1982, Ackermann et al., 1983, Cauwet, 1987, Arujo et al., 1988, Horowitz, 1991, Loring and Rantala, 1992). Therefore, to adequately assess the extent of metal contamination in sediments in monitoring studies, it is necessary to correct for variations in sediment mineralogy, geochemistry and grain size between locations, by normalising the metal concentration to a constituent of the sediment, which are predominately associated with one fraction only. Aluminium, Li and Fe have been considered suitable normalisers because of their association with smaller grained particles which can adsorb greater amounts of metals (Loring, 1990, Loring, 1991, Bothner et al., 1998).

A well established list of attributes by which ‘biomonitors’ are selected has been in place for many years (Butler et al., 1971, Haug et al., 1974a, Phillips, 1994, Langston and Spence, 1995), with A. nodosum fulfilling most of these. In Ireland this seaweed is the commercially most valuable species, with extracted alginates widely used in the pharmaceutical and food industry (Guiry, 1997). Despite this, little data are available on the content of potentially toxic metals in A. nodosum from Ireland; to date only two studies (Cullinane and Whelan, 1982, Stengel and Dring, 2000) have assessed metal concentrations in A. nodosum, both of which refer to localised sites only. This is the first study to analyse A. nodosum from a range of Irish coastal sites over a period of six seasons. In biomonitoring studies it is of paramount importance that each sample analysed constitutes the same tissue region, as different regions within a thallus possess different accumulation characteristics which may be related to their growth, and also to their alginate (Haug et al., 1974b) and phenol content (Pedersen, 1984). Many metals may be essential micronutrients for various metabolic processes (Whitton and Say, 1975), but may be toxic to organisms at higher concentrations (Rai et al., 1981). The metals analysed in this study (Co, Cr, Cd and Pb) are included in the Dangerous Substances Directive (76/464/EEC), a list of substances originally published by the EEC in 1976, which were considered to be of particular concern in aquatic environments, due to their production volumes, persistence, bioaccumulation properties and toxicity (Phillips and Rainbow, 1993, Crathorne et al., 2001).

The aims of this study were to assess the brown seaweed A. nodosum as a biomonitor of Cr, Co, Cd and Pb in the Irish marine environment by the examination of spatial and temporal trends (over six seasons) in the concentration of these contaminants in this species. The study sites along the Irish coastline (Fig. 1) were selected on the basis of potentially reflecting a wide range of heavy metal concentrations. All of these locations were expected to represent different levels of industrial and human activity which should be reflected in the metal content of A. nodosum tissue from these regions. The sampling locations are categorised in Table 1, based on both hydrographic conditions (reflecting the varying intertidal habitats along the Irish coastline) and suspected contamination levels. These locations constitute areas of active seaweed harvesting (Ballyconneely) and areas near industrial and municipal centres. The inclusions of sediments in this study provided supplementary information for evaluating the degree of contamination at the study sites.

Section snippets

Description of the study sites

Algae and sediment samples were collected from six sites (see details in Table 1) around Ireland (Fig. 1) over six seasons between February 1999 and July 2000. Ballyconneely (53° N 24.694′ 010°W 02.767′), where A. nodosum is currently harvested, is considered an almost pristine environment, characterised by only small and scattered residential settlements. Galway Docks (53° N 16.216′ 009°W 02.510′) were used in the past as a loading facility for base metal ores from mining activities at Tynagh

Metal concentrations in Ascophyllum nodosum

Concentrations of Cr, Co, Cd and Pb (μg g−1 D.W.) in A. nodosum over six seasons are shown in Fig. 2a–d. Tukey's post-hoc tests followed two-way ANOVAs examining the effect of site and season on the individual metals. Post-hoc differences between locations for each metal are presented as a matrix of probabilities in Table 4. Seasonal differences were few and inconsistent. The mean concentrations of the metals measured in the algae were in the order Pb > Cr > Co > Cd.

Discussion

Spatial and temporal variations in the elemental composition of seaweeds may be attributed to a number of factors, including environmental and biological factors, and their interactions (Phillips, 1977, Phillips, 1994, Zolotukhina, 1991, Struck et al., 1997). When using the Cr, Co, Cd and Pb content of A. nodosum from the selected locations along the Irish coast to assess environmental quality and establish potential ‘hot spots’, site-specific environmental parameters that may affect seaweed

Conclusions

When using A. nodosum to assess metal contamination on the Irish coast it is important to consider that elemental concentrations in this species reflect the respective bioavailable concentration patterns at different times. However, ambient environmental conditions affect metal accumulation by A. nodosum, as well as factors enhancing or reducing accumulation, such as temperature, light, nutrients and salinity. Also, as riverine inputs are strongly influenced by the rock-type of their catchment,

Acknowledgements

This work was supported by funding from the Irish Higher Education Authority's Programme for Research in Third Level Institutions Cycle II for the Environmental Change Institute, NUI Galway. The authors are grateful to Mr. Harry O Donnell (Department of Earth and Ocean Sciences, NUI Galway) and Mr. Martin Gilligan (Public Analysts Laboratory, University College Hospital Galway) for technical assistance and to Arramara Teoranta (Kilkieran, Connemara, Co. Galway).

References (89)

  • S. Haritonidis et al.

    Bioaccumulations of metals by the green alga Ulva rigida from Thermaikos Gulf, Greece

    Environmental Pollution

    (1999)
  • A. Haug et al.

    Estimation of heavy metal pollution in two Norwegian fjord areas by analysis of the brown alga Ascophyllum nodosum

    Environmental Pollution

    (1974)
  • X. Hou et al.

    Study on the concentration and seasonal variation of inorganic elements in 35 species of marine algae

    The Science of the Total Environment

    (1998)
  • M. Kilemade et al.

    An assessment of the pollutant status of surficial sediment in Cork Harbour in the South East of Ireland with particular reference to polycyclic aromatic hydrocarbons

    Marine Pollution Bulletin

    (2004)
  • D.H. Loring

    Lithium – a new approach for the granulometric normalization of trace metal data

    Marine Chemistry

    (1990)
  • D.H. Loring et al.

    Manual for the geochemical analysis of marine sediments and suspended particulate matter

    Earth Science Reviews

    (1992)
  • A. Melhuus et al.

    A preliminary study of the use of benthic algae as biological indicators of heavy metal pollution in Sorfjorden, Norway

    Environmental Pollution

    (1978)
  • G.E. Millward et al.

    Metal pollution

  • A. Mountouris et al.

    Bioconcentration of heavy metals in aquatic environments: the importance of bioavailability

    Marine Pollution Bulletin

    (2002)
  • G. Nickless et al.

    Distribution of Cd, Pb and Zn in the Bristol Channel

    Marine Pollution Bulletin

    (1972)
  • D. Phaneuf et al.

    Evaluation of the contamination of marine algae (seaweed) from the St. Lawrence River and likely to be consumed by humans

    Environmental Research Section A

    (1999)
  • D.J.H. Phillips

    The use of biological indicator organisms to monitor trace metal pollution in marine and estuarine environments – a review

    Environmental Pollution

    (1977)
  • D.J.H. Phillips

    Trace metals in the common mussel Mytilus edulis (L.) and in the alga Fucus vesiculosus (L.) from the region of the Sound (Öresund)

    Environmental Pollution

    (1979)
  • D.J.H. Phillips

    The chemistries and environmental fates of trace metals and organochlorines in aquatic ecosystems

    Marine Pollution Bulletin

    (1995)
  • P.S. Rainbow

    Biomonitoring of heavy metal availability in the marine environment

    Marine Pollution Bulletin

    (1995)
  • P.S. Rainbow et al.

    Cosmopolitan biomonitors of trace metals

    Marine Pollution Bulletin

    (1993)
  • D.L. Rice et al.

    Experimental outdoor studies with Ulva fasciata Delile. II. Trace metal chemistry

    Journal of Experimental Marine Biology and Ecology

    (1981)
  • J. Ridgway et al.

    Distinguishing between natural and anthropogenic sources of metals entering the Irish Sea

    Applied Geochemistry

    (2003)
  • F. Riget et al.

    Natural seasonal variation of cadmium, copper, lead and zinc in brown seaweed (Fucus vesiculosus)

    Marine Pollution Bulletin

    (1995)
  • F. Riget et al.

    Baseline levels and natural variability of elements in three seaweed species from West Greenland

    Marine Pollution Bulletin

    (1997)
  • D.B. Stengel et al.

    Copper and iron concentrations in Ascophyllum nodosum (Fucales, Phaeophyta) from different sites in Ireland and after culture experiments in relation to thallus age and epiphytism

    Journal of Experimental Marine Biology and Ecology

    (2000)
  • D.B. Stengel et al.

    Zinc concentrations in marine macroalgae and a lichen from western Ireland in relation to phylogenetic grouping, habitat and morphology

    Marine Pollution Bulletin

    (2004)
  • D.B. Stengel et al.

    Tissue, Cu, Fe and Mn concentrations in different-aged and different functional thallus regions of three brown algae from western Ireland. Estuarine

    Coastal and Shelf Science

    (2005)
  • B.D. Struck et al.

    Statistical evaluation of ecosystem properties influencing the uptake of As, Cd, Co, Cu, Hg, Mn, Ni, Pb and Zn in seaweed (Fucus vesiculosus) and common mussel (Mytilus edulis)

    The Science of the Total Environment

    (1997)
  • G. Veinott et al.

    Baseline metal concentrations in coastal Labrador sediments

    Marine Pollution Bulletin

    (2001)
  • R. Villares et al.

    Seasonal and background levels of heavy metals in two green seaweeds

    Environmental Pollution

    (2002)
  • P. Wright et al.

    Spatial and seasonal variation in heavy metals in the sediments and biota of two adjacent estuaries, the Orwell and the Stour, in eastern England

    The Science of the Total Environment

    (1999)
  • F. Ackermann et al.

    Monitoring of heavy metals in coastal and estuarine sediments – a question of grain size: 20 μm versus <60 μm

    Environmental Technology Letters

    (1983)
  • M. Arujo et al.

    Heavy metal contamination in sediments from the Belgian Coast and Schildt Estuary

    Marine Pollution Bulletin

    (1988)
  • Boelens, R.G.V., Maloney, D.M., Parsons, A.P., Walsh, A.R., 1999. Ireland's marine and coastal areas and adjacent seas:...
  • G.W. Bryan

    The absorption of zinc and other metals by the brown seaweed Laminaria digitata

    Journal of the Marine Biological Association of the United Kingdom

    (1969)
  • G.W. Bryan et al.

    A guide to the assessment of heavy metal contamination in estuaries using biological indicators

    Occasional Publication of the Marine Biological Association of the United Kingdom

    (1985)
  • P.A. Butler et al.

    Methods of detection, measurement and monitoring of pollutants in the marine environment

  • V.A. Catsiki et al.

    The use of the chlorophyte Ulva lactuca (L.) as an indicator organism of metal pollution (Cost-48) Symposium of Sub Group III

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