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Long Term Trends in Trace Metals in Biota in the Forth Estuary, Scotland, 1981–1999
Volume 40/Number 12/December 2000
results suggest that there is little sign of any declining trend in concentrations of these chlorohydrocarbon pesticides, including DDT, following its ban in China in 1983 (Connell et al., 1998b), even in our western waters where trans-boundary transport may be expected to be substantial as a result of in¯uence from the Pearl River. This research was supported by funding from the Agriculture, Fisheries and Conservation Department of the Hong Kong SAR Government, a Central Allocation Grant (8730011) awarded by the Hong Kong Research Grant Council, and a Strategic Research Grant (7001030) of the City University of Hong Kong. We would like to thank Dr. Dave Phillips for his constructive comments which improved the ®nal version of the manuscript. Aspinwall Clouston (1997) Development of a Comprehensive Conservation Strategy and Management Plan in Relation to the Listing of Mai Po and Inner Deep Bay as a Wetland of International Importance under the Ramsar Convention. Agreement No. CE 47/ 95, Agriculture and Fisheries Department, Hong Kong Government. Connell, D. W., Wu, R. S. S., Richardson, B. J., Leung, K., Lam, P. K. S. and Connell, P. A. (1998a) Fate and risk evaluation of persistent organic contaminants and related compounds in Victoria Harbour, Hong Kong. Chemosphere 36, 2019±2030. Connell, D. W., Wu, R. S. S., Richardson, B. J., Leung, K., Lam, P. K. S. and Connell, P. A. (1998b) Occurrence of persistent organic contaminants and related substances in Hong Kong marine areas: an overview. Marine Pollution Bulletin 36, 376±384. Hills, P., Zhang, L. and Liu, J. (1998) Transboundary pollution between Guangdong Province and Hong Kong: threats to water quality in the Pearl River estuary and their implications for environmental policy and planning. Journal of Environmental Planning and Management 41, 375±396. Hong, H. S., Xu, L., Zhang, L., Chen, J. C., Wong, Y. S. and Wan, T. S. M. (1995) Environmental fate and chemistry of organic pollutants in the sediment of Xiamen and Victoria harbours. Marine Pollution Bulletin 31, 229±236. Ip, H. M. H. (1983) Breast milk contaminants in Hong Kong. Bulletin of the Hong Kong Medical Association 35, 1±16. Kennish, M. J. (1996) Practical Handbook of Estuarine and Marine Pollution. CRC Press, New Jersey. Lam, P. K. S. (1996) Development of a Comprehensive Conservation Strategy and a Management Plan in Relation to the Listing of Mai
Marine Pollution Bulletin Vol. 40, No. 12, pp. 1214±1220, 2000 Ó 2000 Elsevier Science Ltd. All rights reserved. Printed in Great Britain 0025-326X/00 $ - see front matter
PII: S0025-326X(00)00189-2
Long Term Trends in Trace Metals in Biota in the Forth Estuary, Scotland, 1981±1999 JUDITH DOBSON Scottish Environment Protection Agency East Region, Heriot-Watt Research Park, Riccarton, Edinburgh EH14 4AP, UK The Forth is an industrialized estuary in south-east Scotland (Fig. 1). The industrial nature of the catchment 1214
Po and Inner Deep Bay as a Wetland of International Importance under the Ramsar Convention. Technical Note No. 3: Invertebrate Survey. Agriculture and Fisheries Department, Hong Kong Government. Lee, S. Y. (1993) Invertebrate species new to science recorded from the Mai Po Marshes, Hong Kong. In The Marine Biology of South China Sea, ed. B. Morton, pp. 199±209. Hong Kong University Press, Hong Kong. Neller, R. J. and Lam, K. C. (1994) The environment. In Guangdong: Survey of a Province Undergoing Rapid Change, eds. Y. M. Yeung and D. K. Y. Chu, pp. 401±428. The Chinese University Press, Hong Kong. Peking University (1994) Environmental Impact Assessment Study on Shenzhen River Regulation Project. Shenzhen River Regulation Oce of Municipal Government. Phillips, D. J. H. (1985) Organochlorines and trace metals in greenlipped mussels Perna viridis from Hong Kong waters: a test of indicator ability. Marine Ecology Progress Series 21, 251±258. Phillips, D. J. H. (1989) Trace metals and organochlorines in the coastal waters of Hong Kong. Marine Pollution Bulletin 20, 319± 327. Pruell, R. J., Lake, J. L., Davis, W. R. and Quinn, J. G. (1986) Uptake and depuration of organic contaminants by blue mussels (Mytilus edulis) exposed to environmentally contaminated sediment. Marine Biology 91, 497±507. Richardson, B. J. and Zheng, G. J. (1999) Chlorinated hydrocarbon contaminants in Hong Kong sur®cial sediments. Chemosphere 39, 61±71. Richardson, B. J., Zheng, G.J. and Tse, E.S.C. (2000) A comparison of mussels and SPMDs for monitoring organochlorine pesticides and total petroleum hydrocarbons in Hong Kong waters. In Fish Physiology, Toxicology and Water Quality. Proceedings of the Fifth International Symposium, Hong Kong, 9±13 November 1998, ed. V. Thurston, pp. 169±178. USEPA. Xu, L., Zheng, G. J., Lam, P. K. S. and Richardson, B. (1999) Relationship between tissue concentrations of polycyclic aromatic hydrocarbons and DNA adducts in green-lipped mussels (Perna viridis). Ecotoxicology 8, 73±82. Young, L. and Melville, D. S. (1993) Conservation of the Deep Bay environment. In The Marine Biology of South China Sea, ed. B. Morton, pp. 211±229. Hong Kong University Press, Hong Kong. Zheng, G. J. and Richardson, B. J. (1999) Petroleum hydrocarbons and PAHs in marine sediments of Hong Kong. Chemosphere 38, 2625±2632. Zheng, J. and Quinn, J. G. (1988) Analytical procedures to classify organic pollutants in natural waters, sediments, and benthic organisms. Acta Oceanologica Sinica 7, 226±236.
and the relatively small freshwater ¯ow (63 m3 secÿ1 annual average) result in direct discharges of domestic and industrial wastewaters comprising 10% of the average volume of freshwater discharge to the estuary (Leatherland, 1987). Point source discharges are regulated by the statutory regulatory authority (currently the Scottish Environment Protection Agency, SEPA; formerly the Forth River Puri®cation Board, FRPB) to attempt to ensure that numerical Environmental Quality Standards (EQS) set in response to the Dangerous Substances Directive (76/464/EEC) of the European Union are not exceeded. EQS are based on the toxicity of the substance in solution. However, the partitioning of trace metals can lead to the accumulation of these substances in both sediments and biota. Long-term monitoring programmes undertaken by SEPA, therefore, include the analysis of trace metals in sediments and biota, so as to highlight trends and any potential problems.
Marine Pollution Bulletin
Fig. 1 Location of the Forth Estuary and Firth of Forth and sampling sites: 1 ± Largo, 2 ± Levenmouth, 3 ± Inverkeithing, 4 ± Limekilns, 5 ± Ironmill, 6 ± Culross, 7 ± Skin¯ats, 8 ± Grangemouth, 9 ± Carriden, 10 ± Blackness, 11 ± Port Edgar, 12 ± Granton, 13 ± Leith, 14 ± Joppa, 15 ± Cockenzie, 16 ± Ferny Ness, 17 ± Tynemouth.
The measurement of long-term trends in the contamination of sediments is complicated by their mobility and structure, and does not indicate directly the bioavailable fraction (Phillips, 1997). Biota which accumulate trace contaminants can be used to assess spatial and temporal variations in the bioavailable concentrations of contaminants in estuarine and coastal waters. Such organisms are generally referred to as biomonitors. Ecient biomonitors do not regulate their trace metal concentrations and, therefore, passively re¯ect ambient contaminant levels. Rainbow and Phillips (1993) recommended the use of more than one indicator organism, to re¯ect dierent pathways of uptake. The blue mussel Mytilus edulis and the brown seaweed Fucus vesiculosus have been extensively used as biomonitors (e.g. Bryan and Hummerstone, 1973; Luoma et al., 1982; Barnet and Ashcroft, 1985; O'Connor, 1998). Both organisms ful®l the criteria for proposed biomonitors and are poor regulators of trace metals (Phillips, 1995). M. edulis is a suspension feeder, so obtains metals from particulate matter during the feeding process as well as from solution, whereas F. vesiculosus takes up trace metals passively from solution (Phillips, 1997; Rainbow, 1995). The FRPB began annual monitoring of trace metals in M. edulis in 1981 and in F. vesiculosus in 1982. The discharge of trace metals to the Forth Estuary from point sources decreased substantially during the following 18 years, in response to improvements in production processes and wastewater treatment. This paper presents bioaccumulation data collected over this period, which illustrate changes in tissue concentrations related to reductions in inputs. Samples of both mussels and algae were collected annually from suitable sites around the Forth Estuary and the Firth of Forth during late February or early March. Continuous data are available from 17 sites (Fig. 1) in the study area. Sampling was timed to avoid the changes in metal concentrations and body burdens associated with spawning and to minimize seasonal variations (Phillips, 1980). At least 20 individual mussels in the size range 40±45 mm were collected from mid-shore at each site. The mussels were depurated for 24 h and stored deep-
frozen. The ¯esh from 20 defrosted and drained individuals was pooled and freeze-dried. The algae were washed with deionised water to remove adhering sediment and the bladders and tips were removed by tearing. The main part of the thallus was retained and freezedried. The freeze-dried samples of mussels and seaweed were then ground in a pestle and mortar, and a subsample was digested in nitric acid. Prior to 1990, samples were digested in an open ¯ask on a hotplate, but digestion in sealed vessels in a microwave oven has been employed since 1990. The change in digestion procedure has not aected the results obtained for a certi®ed reference material of dog®sh muscle (DORM-1) which was analysed with each batch of samples. The results for metals in this material (Table 1) generally show good agreement between the certi®ed and measured values. Since 1991, additional quality control has been provided by interlaboratory testing schemes (QUASIMEME/ NMAQC) for trace metals in biota (Pedersen et al., 1997; Gardner et al., 1997). Point source and riverine inputs of metal contaminants to the tidal waters of the Forth have been monitored and quanti®ed since 1990 as part of a programme to evaluate inputs to the North Sea. Point source discharges of metals show a continuing decline, particularly where discharges have been eliminated or regulation has resulted in substitution, recycling or improved euent treatment. Reductions in the discharge of selected metals over this period are summarized in Table 2. The relative contributions of metals from rivers and point source discharges from domestic and industrial sources TABLE 1 Analytical results for the certi®ed reference material DORM-1.
Cadmium Chromium Lead Copper Mercury Nickel Zinc
Certi®ed values (mg kgÿ1 dry weight)
Results (mg kgÿ1 dry weight)
0:086 0:012 3:6 0:40 0:41 0:12 5:22 0:33 0:798 0:074 1:2 0:3 21:3 1:0
0:088 0:009 3:42 0:63 0:62 0:42 4:96 0:49 0:75 0:136 1:2 0:6 29:9 7:7
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Volume 40/Number 12/December 2000 TABLE 2 Inputs of selected metals in wastewaters and rivers to tidal waters of the Forth.a
Cadmium (kg yrÿ1 ) Mercury (kg yrÿ1 ) Chromium (t yrÿ1 ) Copper (t yrÿ1 ) Lead (t yrÿ1 ) Zinc (t yrÿ1 )
1985
1994
1997
3700 300 57 66 28 116
240±390 48 13 33 14 93
100±306 42 11 22 7 71
a A range is given, where concentrations are below the limit of detection, the maximum assumes the concentration is at the LOD, the minimum assumes a concentration of 0.
are shown in Fig. 2. The discharge from industry has decreased for all metals, but the most substantial decreases are for mercury, cadmium and chromium. The largest point source discharge of mercury was to the Forth Estuary. The environmental impact of this discharge has been well documented (Elliot and Grif®ths, 1986). The same discharge was the main source of chromium and also results in local increases in levels of dissolved copper (Balls et al., 1997a). The biggest point source discharge of cadmium was located in the Firth and resulted in local contamination of the biota. Diuse riverine inputs and discharges from sewers are now the major sources of metals to both the Estuary and the Firth. Spatial surveys have identi®ed a general decrease in trace metal concentrations from the furthest upstream sites in the Forth Estuary to the outer sites in the Firth of Forth, in both the mussel and seaweed data. This is interrupted by occasional increases in metal levels in the vicinity of major discharges to the Firth of Forth (Fig. 3). Data from the Forth are based on the analysis of one pool of 20 mussels at a site. Recent guidelines issued by the Oslo and Paris Commission (OSPAR, 1997) for monitoring contaminants in biota for the Joint Assessment and Monitoring Programme (JAMP), recommend analysing three pools of 20 mussels from a site. Replicate analyses are recommended to better describe the natural variability and facilitate the detection of tem-
Fig. 3 Average (1991±1998) concentrations of mercury (mg kgÿ1 dry weight) in mussels in the Forth Estuary and Firth.
poral trends. In order to reduce variability in the data, annual average concentrations for metals in biota have been calculated using data from eight sites (Limekilns, Ironmill Bay, Culross, Skin¯ats, Grangemouth, Carriden, Blackness, Port Edgar) in the Forth Estuary. This averaging technique eliminates the between-site variability in the estuary but may enhance the interannual variability, thus permitting temporal trends to be observed. Annual data are available for M. edulis (Table 3), but data for the period 1991±1995 are missing for F. vesiculosus (Table 4). A simple regression between year and concentration of metal has been employed to establish trends in the data. There are less data available for sites in the Firth and the sites are more dispersed, which invalidates the use of averaged data in that instance. Data are presented in Table 5 for cadmium at a clean (Tynemouth) and contaminated (Leith) site in the Firth. These data show a reduction in cadmium concentrations to background levels at the contaminated site as the discharge reduced and ®nally ceased in 1991. The strongest temporal trends in the Forth Estuary data are for cadmium and mercury in mussels (Table 3) and chromium and mercury in seaweed (Table 4). Inputs of these metals have all reduced substantially over this period, as a result of reductions in point source discharges. The trend in the discharge of mercury is compared with trends in mercury concentrations of mussels
Fig. 2 Comparison of inputs to the Forth from rivers, sewers and trade discharges in the 1980s and 1990s.
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Marine Pollution Bulletin TABLE 3 Trace metal concentrations (mg kgÿ1 dry weight) in mussels from the Forth Estuary.a Year
Cadmium
Zinc
Lead
Nickel
Copper
Chromium
Mercury
1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 r2
nd 2.26 2.49 2.24 2.36 3.29 2.36 1.98 2.14 2.42 1.37 1.93 1.53 1.66 1.64 1.96 1.66 1.27 1.53 0.51
253.4 102.6 141.4 166.5 188.6 212.0 197.5 173.3 222.9 212.5 186.0 279.8 188.6 193.6 172.9 155.5 155.9 150.1 158.0 0
21.1 10.0 9.8 14.5 12.3 23.1 17.4 13.8 15.8 18.6 11.7 17.8 18.0 13.5 10.5 12.5 11.5 10.4 9.3 0.07
2.73 7.61 1.34 2.56 2.16 3.41 2.18 2.25 2.46 4.82 5.67 3.68 2.80 3.75 3.34 4.00 1.99 3.67 2.22 0
13.1 13.8 14.8 14.8 11.3 nd nd 11.0 13.9 14.6 9.8 12.0 14.5 13.0 11.5 11.7 11.1 10.3 10.4 0.25
11.7 15.5 3.9 7.8 14.5 13.9 8.9 5.8 8.2 13.3 5.6 8.8 9.7 8.2 4.5 6.0 5.3 3.5 3.0 0.31
nd 1.85 3.23 2.45 1.26 1.82 1.06 0.54 0.77 0.67 1.03 1.28 0.83 0.63 0.50 0.36 0.39 0.47 0.36 0.62
a
nd: no data.
TABLE 4 Trace metals (mg kgÿ1 dry weight) in F. vesiculosus from the Forth Estuary.a Year
Cadmium
Zinc
Lead
Nickel
Copper
Chromium
Mercury
1982 1983 1984 1985 1986 1987 1988 1989 1990 1996 1997 1998 1999 r2
nd 0.42 0.99 1.23 1.07 1.20 0.75 0.70 0.89 0.86 0.84 0.77 0.66 0.01
129.2 181.8 196.2 197.0 147.7 158.7 196.5 201.8 174.8 131.6 121.8 118.5 119.0 0.2
3.16 2.15 4.15 4.98 5.13 1.91 3.34 3.77 3.33 nd 3.06 2.52 1.67 0.05
5.01 5.39 8.45 9.01 5.63 7.70 8.33 5.99 nd 10.78 6.19 8.32 7.71 0.15
18.3 17.3 30.7 36.2 32.4 33.4 28.4 20.1 23.5 15.8 28.5 21.6 13.3 0.02
4.68 6.44 6.58 13.30 8.11 6.80 8.15 6.79 5.29 1.26 1.47 1.24 0.87 0.4
0.29 0.33 0.34 0.17 0.19 0.07 0.08 0.21 0.21 0.13 0.11 0.10 nd 0.46
a
nd: no data.
TABLE 5 Concentrations of cadmium (mg kgÿ1 dry weight) in mussels in the Firth of Forth. Year 1981 1982 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998
Tynemouth
1.67 1.89 0.93 1.46 1.37 1.16 1.29 0.95 1.78 1.01 0.80
Leith 11.1 16.5 31.2 29 15.9 9.23 6.74 3.55 2.11 1.91 1.22 1.67 1.57 1.56 1.64 0.86
and seaweed in Fig. 4. The mercury concentrations in both mussels and seaweed have declined, but not nearly to the same extent as the levels of the element discharged. Fig. 5 compares temporal trends in chromium concentrations of biota with the discharge of chromium to the Forth. Concentrations of chromium in the seaweed have decreased more rapidly in response to the changes in the discharge, compared to those in the mussels. It may be noted that contamination of the biota of the Forth Estuary was already established when routine monitoring began. Davies (1987) described the Forth Estuary as one of the most contaminated sea areas around Scotland, on the basis of the relatively high concentrations of lead, cadmium, mercury, copper and zinc in mussels. Contaminants which remain in solution are ¯ushed out of the Estuary over a relatively short timescale, so 1217
Volume 40/Number 12/December 2000
Fig. 4 Temporal trends in mercury in biota and in mercury discharged to the Forth.
Fig. 5 Temporal trends in chromium in biota and in chromium discharged to the Forth Estuary.
there is a rapid response to reductions in the level of inputs. By contrast, particle-reactive contaminants are retained within the sediments over relatively long timescales (years) and the sediments will take longer to recover as discharges are reduced. The Forth is a turbid estuary, and particle-reactive metals are removed from solution eectively with the result that dissolved metal concentrations in the estuary are relatively low, but the concentrations of contaminants in the sediments are relatively high (Balls et al., 1997a). This is particularly well illustrated by the partitioning of mercury in the Forth Estuary. Elliot and Griths, 1986 estimated that 97% of the mercury discharged was retained within the sediments. The concentration of dissolved mercury in the water column remained well below the EQS of 300 ng lÿ1 (dissolved, annual average) at 7 3 ng lÿ1 in 1982 and rapidly decreased to become undetectable (i.e. less than 3 ng lÿ1 ) in response to the decrease in the discharge. 1218
Annual monitoring of mercury in the sediments downstream of the major discharge of this element has shown a high degree of variability in the data. Variability due to sediment structure has been largely removed by analysis of the < 63 lm fraction and normalizing to 1% carbon. Fig. 6 shows the normalized data, which indicate an initial decrease in the mercury content of the sediments, followed by an increase between 1983 and 1991 and no clear change since then. This illustrates the slow response of the sediments to reductions in the discharge of the element. The sediments migrate up and down the estuary in response to ¯uctuations in river ¯ows and tidal range. The annual ¯ux of mercury out of the estuary on particulate matter has been estimated to be in the region of 4 kg dayÿ1 (Davies et al., 1986). This is greater than the discharge of mercury from industry has been since 1985. Between 1982 and 1998 the estimated export of mercury exceeded the input from industry by a total of 16813 kg.
Marine Pollution Bulletin
Fig. 6 Temporal trends in mercury concentrations in the sediments of the Forth Estuary.
However, the concentration in the sediments has not evidently decreased during this period, which suggests that the rate of ¯ux of mercury out of the estuary may have decreased in response to the reduction in input. The mussels give an indication of the bioavailable mercury, and it is encouraging that their concentrations of mercury have decreased relatively quickly in response to reductions in the discharge of the element. The partitioning of chromium in the Forth Estuary has not been as well studied as that of mercury. This is partly due to the greater background concentration of chromium in the sediments, and to the technical diculties of analysis. Annual monitoring of the sediments of the Forth is based on a partial digestion technique, which quanti®es the fraction extracted with concentrated nitric acid. Quanti®cation of the total concentration of chromium present requires a total digestion procedure, to extract chromium present in the clay mineral lattice. Neither technique quanti®es bioavailable chromium. The concentration of dissolved chromium in the Forth Estuary is low (< 1 lg lÿ1 ) which suggests chromium is particle-reactive and is largely removed from solution into the sediments. The sediments of the Forth are enriched with chromium (Balls et al., 1997b), and annual monitoring appears to indicate that the concentration of this element in the sediments is increasing (Fig. 7) which is in direct contrast to the measured reduction in discharges. The concentrations of chromium in Forth Estuary mussels and seaweed are enhanced relative to the `national background' concentrations proposed by ADRIS (1995) of 2 and 1 mg kgÿ1 dry weight, respectively. Chromium concentrations in both mussels and seaweed have decreased over time in the estuary, although the inter-annual variability in mussels was greater than in seaweed. It is concluded that reductions in point source discharges of metals in the Forth catchment have led to rapid reductions in the concentrations of metals in the dissolved phase. However, in a turbid estuary such as the Forth, particle-reactive metals are largely retained within the sediments. Contaminants retained in the sediments are eectively trapped within the estuary (at least for some time) and are available to ®lter-feeding deposit and
Fig. 7 Temporal trends in chromium concentrations in the sediments of the Forth Estuary.
feeding organisms. Biomonitors integrate both the eects of reductions in inputs of metals and their partitioning between sediments and waters, and also provide an indication of the levels of bioavailable metal. Both mussels and seaweed should be included in the monitoring programme, as these constitute eective biomonitors for a range of determinants and respond dierently to metals in the dissolved and particulate phases. The author would like to thank colleagues in SEPA East who have contributed to the production of this paper. In particular I wish to thank Jennifer Fozzard and Una Thom for their analytical work; Tom Leatherland and Anton Edwards for helpful comments; and sta in the General Chemistry section for the discharge information. ADRIS (1995) ADRIS Estuary Classi®cation Scheme. Association of Directors and River Inspectors in Scotland Marine and Estuary Sub-group, Perth, Scotland. Balls, P. W., Owens, R. E. and Muller, F. L. L. (1997a) Dissolved trace metals in the Clyde, Forth and Tay estuaries ± a synopsis and comparison with other UK estuaries. Coastal Zone Topics 3, 46±56. Balls, P. W., Hull, S., Miller, B. S., Pirie, J. M. and Proctor, W. (1997b) Trace metals in Scottish estuarine and coastal sediments. Marine Pollution Bulletin 34, 42±50. Barnet, B. E. and Ashcroft, C. R. (1985) Heavy metals in Fucus vesiculosus in the Humber Estuary. Environmental Pollution (Series B) 9, 193±213. Bryan, G. W. and Hummerstone, L. G. (1973) Brown Seaweed as an indicator of heavy metals in estuaries in South-West England. Journal of the Marine Biological Association of the United Kingdom 53, 705±720. Davies, I. M. (1987) Trace metals and organohalogen compounds in the Forth, Scotland. In Proceedings of the Royal Society of Edinburgh 93B, 315±326. Davies, I. M., Griths, A. H., Leatherland, T. M. and Metcalfe, A. P. (1986) Particulate mercury ¯uxes in the Forth Estuary, Scotland. Rapports et Proces-Verbaux des Reunions du Conseil International pour l'Exploration de la Mer 186, 301±305. Elliot, M. and Griths, A. H. (1986) Mercury contamination in components of an estuarine ecosystem. Water Science and Technology 18, 161±170. Gardner, M. J., Dobson, J. E., Griths, A. H., Jessep, M. A. and Ravenscroft, J. E. (1997) An overview of the UK National marine analytical quality control (NMAQC) scheme and its links with QUASIMEME. Marine Pollution Bulletin 35, 125±132. Leatherland, T. M. (1987) The estuary and Firth of Forth, Scotland: uses and aims. Proceedings of the Royal Society of Edinburgh 93B, 285±297. Luoma, S. N., Bryan, G. W. and Langston, W. J. (1982) Scavenging of heavy metals from particulates by brown seaweed. Marine Pollution Bulletin 13, 394±396.
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Volume 40/Number 12/December 2000 O'Connor, T. P. (1998) Mussel watch results from 1986 to 1996. Marine Pollution Bulletin 37 14±19. OSPAR (1997) JAMP guidelines for monitoring contaminants in biota. Oslo and Paris Commissions Joint Assessment and Monitoring Programme 9 June, 1997. Pedersen, B., Co®no, W. and Davies, I. (1997) The 1993±1995 QUASIMEME laboratory performance study: trace metals in sediment and biota. Marine Pollution Bulletin 35, 42±51. 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±317.
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Phillips, D. J. H. (1980) Quantitative Aquatic Biological Indicators ± Their Use to Monitor Trace Metal and Organochlorine Pollution. Applied Science Publishers, Barking. Phillips, D. J. H. (1995) The chemistries and environmental fates of trace metals and organochlorines in aquatic ecosystems. Marine Pollution Bulletin 31, 193±200. Rainbow, P. S. (1995) Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin 31, 183±192. Rainbow, P. S. and Phillips, D. J. H. (1993) Cosmopolitan biomonitors of trace metals. Marine Pollution Bulletin 26, 593±601.
results suggest that there is little sign of any declining trend in concentrations of these chlorohydrocarbon pesticides, including DDT, following its ban in China in 1983 (Connell et al., 1998b), even in our western waters where trans-boundary transport may be expected to be substantial as a result of in¯uence from the Pearl River. This research was supported by funding from the Agriculture, Fisheries and Conservation Department of the Hong Kong SAR Government, a Central Allocation Grant (8730011) awarded by the Hong Kong Research Grant Council, and a Strategic Research Grant (7001030) of the City University of Hong Kong. We would like to thank Dr. Dave Phillips for his constructive comments which improved the ®nal version of the manuscript. Aspinwall Clouston (1997) Development of a Comprehensive Conservation Strategy and Management Plan in Relation to the Listing of Mai Po and Inner Deep Bay as a Wetland of International Importance under the Ramsar Convention. Agreement No. CE 47/ 95, Agriculture and Fisheries Department, Hong Kong Government. Connell, D. W., Wu, R. S. S., Richardson, B. J., Leung, K., Lam, P. K. S. and Connell, P. A. (1998a) Fate and risk evaluation of persistent organic contaminants and related compounds in Victoria Harbour, Hong Kong. Chemosphere 36, 2019±2030. Connell, D. W., Wu, R. S. S., Richardson, B. J., Leung, K., Lam, P. K. S. and Connell, P. A. (1998b) Occurrence of persistent organic contaminants and related substances in Hong Kong marine areas: an overview. Marine Pollution Bulletin 36, 376±384. Hills, P., Zhang, L. and Liu, J. (1998) Transboundary pollution between Guangdong Province and Hong Kong: threats to water quality in the Pearl River estuary and their implications for environmental policy and planning. Journal of Environmental Planning and Management 41, 375±396. Hong, H. S., Xu, L., Zhang, L., Chen, J. C., Wong, Y. S. and Wan, T. S. M. (1995) Environmental fate and chemistry of organic pollutants in the sediment of Xiamen and Victoria harbours. Marine Pollution Bulletin 31, 229±236. Ip, H. M. H. (1983) Breast milk contaminants in Hong Kong. Bulletin of the Hong Kong Medical Association 35, 1±16. Kennish, M. J. (1996) Practical Handbook of Estuarine and Marine Pollution. CRC Press, New Jersey. Lam, P. K. S. (1996) Development of a Comprehensive Conservation Strategy and a Management Plan in Relation to the Listing of Mai
Marine Pollution Bulletin Vol. 40, No. 12, pp. 1214±1220, 2000 Ó 2000 Elsevier Science Ltd. All rights reserved. Printed in Great Britain 0025-326X/00 $ - see front matter
PII: S0025-326X(00)00189-2
Long Term Trends in Trace Metals in Biota in the Forth Estuary, Scotland, 1981±1999 JUDITH DOBSON Scottish Environment Protection Agency East Region, Heriot-Watt Research Park, Riccarton, Edinburgh EH14 4AP, UK The Forth is an industrialized estuary in south-east Scotland (Fig. 1). The industrial nature of the catchment 1214
Po and Inner Deep Bay as a Wetland of International Importance under the Ramsar Convention. Technical Note No. 3: Invertebrate Survey. Agriculture and Fisheries Department, Hong Kong Government. Lee, S. Y. (1993) Invertebrate species new to science recorded from the Mai Po Marshes, Hong Kong. In The Marine Biology of South China Sea, ed. B. Morton, pp. 199±209. Hong Kong University Press, Hong Kong. Neller, R. J. and Lam, K. C. (1994) The environment. In Guangdong: Survey of a Province Undergoing Rapid Change, eds. Y. M. Yeung and D. K. Y. Chu, pp. 401±428. The Chinese University Press, Hong Kong. Peking University (1994) Environmental Impact Assessment Study on Shenzhen River Regulation Project. Shenzhen River Regulation Oce of Municipal Government. Phillips, D. J. H. (1985) Organochlorines and trace metals in greenlipped mussels Perna viridis from Hong Kong waters: a test of indicator ability. Marine Ecology Progress Series 21, 251±258. Phillips, D. J. H. (1989) Trace metals and organochlorines in the coastal waters of Hong Kong. Marine Pollution Bulletin 20, 319± 327. Pruell, R. J., Lake, J. L., Davis, W. R. and Quinn, J. G. (1986) Uptake and depuration of organic contaminants by blue mussels (Mytilus edulis) exposed to environmentally contaminated sediment. Marine Biology 91, 497±507. Richardson, B. J. and Zheng, G. J. (1999) Chlorinated hydrocarbon contaminants in Hong Kong sur®cial sediments. Chemosphere 39, 61±71. Richardson, B. J., Zheng, G.J. and Tse, E.S.C. (2000) A comparison of mussels and SPMDs for monitoring organochlorine pesticides and total petroleum hydrocarbons in Hong Kong waters. In Fish Physiology, Toxicology and Water Quality. Proceedings of the Fifth International Symposium, Hong Kong, 9±13 November 1998, ed. V. Thurston, pp. 169±178. USEPA. Xu, L., Zheng, G. J., Lam, P. K. S. and Richardson, B. (1999) Relationship between tissue concentrations of polycyclic aromatic hydrocarbons and DNA adducts in green-lipped mussels (Perna viridis). Ecotoxicology 8, 73±82. Young, L. and Melville, D. S. (1993) Conservation of the Deep Bay environment. In The Marine Biology of South China Sea, ed. B. Morton, pp. 211±229. Hong Kong University Press, Hong Kong. Zheng, G. J. and Richardson, B. J. (1999) Petroleum hydrocarbons and PAHs in marine sediments of Hong Kong. Chemosphere 38, 2625±2632. Zheng, J. and Quinn, J. G. (1988) Analytical procedures to classify organic pollutants in natural waters, sediments, and benthic organisms. Acta Oceanologica Sinica 7, 226±236.
and the relatively small freshwater ¯ow (63 m3 secÿ1 annual average) result in direct discharges of domestic and industrial wastewaters comprising 10% of the average volume of freshwater discharge to the estuary (Leatherland, 1987). Point source discharges are regulated by the statutory regulatory authority (currently the Scottish Environment Protection Agency, SEPA; formerly the Forth River Puri®cation Board, FRPB) to attempt to ensure that numerical Environmental Quality Standards (EQS) set in response to the Dangerous Substances Directive (76/464/EEC) of the European Union are not exceeded. EQS are based on the toxicity of the substance in solution. However, the partitioning of trace metals can lead to the accumulation of these substances in both sediments and biota. Long-term monitoring programmes undertaken by SEPA, therefore, include the analysis of trace metals in sediments and biota, so as to highlight trends and any potential problems.
Marine Pollution Bulletin
Fig. 1 Location of the Forth Estuary and Firth of Forth and sampling sites: 1 ± Largo, 2 ± Levenmouth, 3 ± Inverkeithing, 4 ± Limekilns, 5 ± Ironmill, 6 ± Culross, 7 ± Skin¯ats, 8 ± Grangemouth, 9 ± Carriden, 10 ± Blackness, 11 ± Port Edgar, 12 ± Granton, 13 ± Leith, 14 ± Joppa, 15 ± Cockenzie, 16 ± Ferny Ness, 17 ± Tynemouth.
The measurement of long-term trends in the contamination of sediments is complicated by their mobility and structure, and does not indicate directly the bioavailable fraction (Phillips, 1997). Biota which accumulate trace contaminants can be used to assess spatial and temporal variations in the bioavailable concentrations of contaminants in estuarine and coastal waters. Such organisms are generally referred to as biomonitors. Ecient biomonitors do not regulate their trace metal concentrations and, therefore, passively re¯ect ambient contaminant levels. Rainbow and Phillips (1993) recommended the use of more than one indicator organism, to re¯ect dierent pathways of uptake. The blue mussel Mytilus edulis and the brown seaweed Fucus vesiculosus have been extensively used as biomonitors (e.g. Bryan and Hummerstone, 1973; Luoma et al., 1982; Barnet and Ashcroft, 1985; O'Connor, 1998). Both organisms ful®l the criteria for proposed biomonitors and are poor regulators of trace metals (Phillips, 1995). M. edulis is a suspension feeder, so obtains metals from particulate matter during the feeding process as well as from solution, whereas F. vesiculosus takes up trace metals passively from solution (Phillips, 1997; Rainbow, 1995). The FRPB began annual monitoring of trace metals in M. edulis in 1981 and in F. vesiculosus in 1982. The discharge of trace metals to the Forth Estuary from point sources decreased substantially during the following 18 years, in response to improvements in production processes and wastewater treatment. This paper presents bioaccumulation data collected over this period, which illustrate changes in tissue concentrations related to reductions in inputs. Samples of both mussels and algae were collected annually from suitable sites around the Forth Estuary and the Firth of Forth during late February or early March. Continuous data are available from 17 sites (Fig. 1) in the study area. Sampling was timed to avoid the changes in metal concentrations and body burdens associated with spawning and to minimize seasonal variations (Phillips, 1980). At least 20 individual mussels in the size range 40±45 mm were collected from mid-shore at each site. The mussels were depurated for 24 h and stored deep-
frozen. The ¯esh from 20 defrosted and drained individuals was pooled and freeze-dried. The algae were washed with deionised water to remove adhering sediment and the bladders and tips were removed by tearing. The main part of the thallus was retained and freezedried. The freeze-dried samples of mussels and seaweed were then ground in a pestle and mortar, and a subsample was digested in nitric acid. Prior to 1990, samples were digested in an open ¯ask on a hotplate, but digestion in sealed vessels in a microwave oven has been employed since 1990. The change in digestion procedure has not aected the results obtained for a certi®ed reference material of dog®sh muscle (DORM-1) which was analysed with each batch of samples. The results for metals in this material (Table 1) generally show good agreement between the certi®ed and measured values. Since 1991, additional quality control has been provided by interlaboratory testing schemes (QUASIMEME/ NMAQC) for trace metals in biota (Pedersen et al., 1997; Gardner et al., 1997). Point source and riverine inputs of metal contaminants to the tidal waters of the Forth have been monitored and quanti®ed since 1990 as part of a programme to evaluate inputs to the North Sea. Point source discharges of metals show a continuing decline, particularly where discharges have been eliminated or regulation has resulted in substitution, recycling or improved euent treatment. Reductions in the discharge of selected metals over this period are summarized in Table 2. The relative contributions of metals from rivers and point source discharges from domestic and industrial sources TABLE 1 Analytical results for the certi®ed reference material DORM-1.
Cadmium Chromium Lead Copper Mercury Nickel Zinc
Certi®ed values (mg kgÿ1 dry weight)
Results (mg kgÿ1 dry weight)
0:086 0:012 3:6 0:40 0:41 0:12 5:22 0:33 0:798 0:074 1:2 0:3 21:3 1:0
0:088 0:009 3:42 0:63 0:62 0:42 4:96 0:49 0:75 0:136 1:2 0:6 29:9 7:7
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Volume 40/Number 12/December 2000 TABLE 2 Inputs of selected metals in wastewaters and rivers to tidal waters of the Forth.a
Cadmium (kg yrÿ1 ) Mercury (kg yrÿ1 ) Chromium (t yrÿ1 ) Copper (t yrÿ1 ) Lead (t yrÿ1 ) Zinc (t yrÿ1 )
1985
1994
1997
3700 300 57 66 28 116
240±390 48 13 33 14 93
100±306 42 11 22 7 71
a A range is given, where concentrations are below the limit of detection, the maximum assumes the concentration is at the LOD, the minimum assumes a concentration of 0.
are shown in Fig. 2. The discharge from industry has decreased for all metals, but the most substantial decreases are for mercury, cadmium and chromium. The largest point source discharge of mercury was to the Forth Estuary. The environmental impact of this discharge has been well documented (Elliot and Grif®ths, 1986). The same discharge was the main source of chromium and also results in local increases in levels of dissolved copper (Balls et al., 1997a). The biggest point source discharge of cadmium was located in the Firth and resulted in local contamination of the biota. Diuse riverine inputs and discharges from sewers are now the major sources of metals to both the Estuary and the Firth. Spatial surveys have identi®ed a general decrease in trace metal concentrations from the furthest upstream sites in the Forth Estuary to the outer sites in the Firth of Forth, in both the mussel and seaweed data. This is interrupted by occasional increases in metal levels in the vicinity of major discharges to the Firth of Forth (Fig. 3). Data from the Forth are based on the analysis of one pool of 20 mussels at a site. Recent guidelines issued by the Oslo and Paris Commission (OSPAR, 1997) for monitoring contaminants in biota for the Joint Assessment and Monitoring Programme (JAMP), recommend analysing three pools of 20 mussels from a site. Replicate analyses are recommended to better describe the natural variability and facilitate the detection of tem-
Fig. 3 Average (1991±1998) concentrations of mercury (mg kgÿ1 dry weight) in mussels in the Forth Estuary and Firth.
poral trends. In order to reduce variability in the data, annual average concentrations for metals in biota have been calculated using data from eight sites (Limekilns, Ironmill Bay, Culross, Skin¯ats, Grangemouth, Carriden, Blackness, Port Edgar) in the Forth Estuary. This averaging technique eliminates the between-site variability in the estuary but may enhance the interannual variability, thus permitting temporal trends to be observed. Annual data are available for M. edulis (Table 3), but data for the period 1991±1995 are missing for F. vesiculosus (Table 4). A simple regression between year and concentration of metal has been employed to establish trends in the data. There are less data available for sites in the Firth and the sites are more dispersed, which invalidates the use of averaged data in that instance. Data are presented in Table 5 for cadmium at a clean (Tynemouth) and contaminated (Leith) site in the Firth. These data show a reduction in cadmium concentrations to background levels at the contaminated site as the discharge reduced and ®nally ceased in 1991. The strongest temporal trends in the Forth Estuary data are for cadmium and mercury in mussels (Table 3) and chromium and mercury in seaweed (Table 4). Inputs of these metals have all reduced substantially over this period, as a result of reductions in point source discharges. The trend in the discharge of mercury is compared with trends in mercury concentrations of mussels
Fig. 2 Comparison of inputs to the Forth from rivers, sewers and trade discharges in the 1980s and 1990s.
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Marine Pollution Bulletin TABLE 3 Trace metal concentrations (mg kgÿ1 dry weight) in mussels from the Forth Estuary.a Year
Cadmium
Zinc
Lead
Nickel
Copper
Chromium
Mercury
1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 r2
nd 2.26 2.49 2.24 2.36 3.29 2.36 1.98 2.14 2.42 1.37 1.93 1.53 1.66 1.64 1.96 1.66 1.27 1.53 0.51
253.4 102.6 141.4 166.5 188.6 212.0 197.5 173.3 222.9 212.5 186.0 279.8 188.6 193.6 172.9 155.5 155.9 150.1 158.0 0
21.1 10.0 9.8 14.5 12.3 23.1 17.4 13.8 15.8 18.6 11.7 17.8 18.0 13.5 10.5 12.5 11.5 10.4 9.3 0.07
2.73 7.61 1.34 2.56 2.16 3.41 2.18 2.25 2.46 4.82 5.67 3.68 2.80 3.75 3.34 4.00 1.99 3.67 2.22 0
13.1 13.8 14.8 14.8 11.3 nd nd 11.0 13.9 14.6 9.8 12.0 14.5 13.0 11.5 11.7 11.1 10.3 10.4 0.25
11.7 15.5 3.9 7.8 14.5 13.9 8.9 5.8 8.2 13.3 5.6 8.8 9.7 8.2 4.5 6.0 5.3 3.5 3.0 0.31
nd 1.85 3.23 2.45 1.26 1.82 1.06 0.54 0.77 0.67 1.03 1.28 0.83 0.63 0.50 0.36 0.39 0.47 0.36 0.62
a
nd: no data.
TABLE 4 Trace metals (mg kgÿ1 dry weight) in F. vesiculosus from the Forth Estuary.a Year
Cadmium
Zinc
Lead
Nickel
Copper
Chromium
Mercury
1982 1983 1984 1985 1986 1987 1988 1989 1990 1996 1997 1998 1999 r2
nd 0.42 0.99 1.23 1.07 1.20 0.75 0.70 0.89 0.86 0.84 0.77 0.66 0.01
129.2 181.8 196.2 197.0 147.7 158.7 196.5 201.8 174.8 131.6 121.8 118.5 119.0 0.2
3.16 2.15 4.15 4.98 5.13 1.91 3.34 3.77 3.33 nd 3.06 2.52 1.67 0.05
5.01 5.39 8.45 9.01 5.63 7.70 8.33 5.99 nd 10.78 6.19 8.32 7.71 0.15
18.3 17.3 30.7 36.2 32.4 33.4 28.4 20.1 23.5 15.8 28.5 21.6 13.3 0.02
4.68 6.44 6.58 13.30 8.11 6.80 8.15 6.79 5.29 1.26 1.47 1.24 0.87 0.4
0.29 0.33 0.34 0.17 0.19 0.07 0.08 0.21 0.21 0.13 0.11 0.10 nd 0.46
a
nd: no data.
TABLE 5 Concentrations of cadmium (mg kgÿ1 dry weight) in mussels in the Firth of Forth. Year 1981 1982 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998
Tynemouth
1.67 1.89 0.93 1.46 1.37 1.16 1.29 0.95 1.78 1.01 0.80
Leith 11.1 16.5 31.2 29 15.9 9.23 6.74 3.55 2.11 1.91 1.22 1.67 1.57 1.56 1.64 0.86
and seaweed in Fig. 4. The mercury concentrations in both mussels and seaweed have declined, but not nearly to the same extent as the levels of the element discharged. Fig. 5 compares temporal trends in chromium concentrations of biota with the discharge of chromium to the Forth. Concentrations of chromium in the seaweed have decreased more rapidly in response to the changes in the discharge, compared to those in the mussels. It may be noted that contamination of the biota of the Forth Estuary was already established when routine monitoring began. Davies (1987) described the Forth Estuary as one of the most contaminated sea areas around Scotland, on the basis of the relatively high concentrations of lead, cadmium, mercury, copper and zinc in mussels. Contaminants which remain in solution are ¯ushed out of the Estuary over a relatively short timescale, so 1217
Volume 40/Number 12/December 2000
Fig. 4 Temporal trends in mercury in biota and in mercury discharged to the Forth.
Fig. 5 Temporal trends in chromium in biota and in chromium discharged to the Forth Estuary.
there is a rapid response to reductions in the level of inputs. By contrast, particle-reactive contaminants are retained within the sediments over relatively long timescales (years) and the sediments will take longer to recover as discharges are reduced. The Forth is a turbid estuary, and particle-reactive metals are removed from solution eectively with the result that dissolved metal concentrations in the estuary are relatively low, but the concentrations of contaminants in the sediments are relatively high (Balls et al., 1997a). This is particularly well illustrated by the partitioning of mercury in the Forth Estuary. Elliot and Griths, 1986 estimated that 97% of the mercury discharged was retained within the sediments. The concentration of dissolved mercury in the water column remained well below the EQS of 300 ng lÿ1 (dissolved, annual average) at 7 3 ng lÿ1 in 1982 and rapidly decreased to become undetectable (i.e. less than 3 ng lÿ1 ) in response to the decrease in the discharge. 1218
Annual monitoring of mercury in the sediments downstream of the major discharge of this element has shown a high degree of variability in the data. Variability due to sediment structure has been largely removed by analysis of the < 63 lm fraction and normalizing to 1% carbon. Fig. 6 shows the normalized data, which indicate an initial decrease in the mercury content of the sediments, followed by an increase between 1983 and 1991 and no clear change since then. This illustrates the slow response of the sediments to reductions in the discharge of the element. The sediments migrate up and down the estuary in response to ¯uctuations in river ¯ows and tidal range. The annual ¯ux of mercury out of the estuary on particulate matter has been estimated to be in the region of 4 kg dayÿ1 (Davies et al., 1986). This is greater than the discharge of mercury from industry has been since 1985. Between 1982 and 1998 the estimated export of mercury exceeded the input from industry by a total of 16813 kg.
Marine Pollution Bulletin
Fig. 6 Temporal trends in mercury concentrations in the sediments of the Forth Estuary.
However, the concentration in the sediments has not evidently decreased during this period, which suggests that the rate of ¯ux of mercury out of the estuary may have decreased in response to the reduction in input. The mussels give an indication of the bioavailable mercury, and it is encouraging that their concentrations of mercury have decreased relatively quickly in response to reductions in the discharge of the element. The partitioning of chromium in the Forth Estuary has not been as well studied as that of mercury. This is partly due to the greater background concentration of chromium in the sediments, and to the technical diculties of analysis. Annual monitoring of the sediments of the Forth is based on a partial digestion technique, which quanti®es the fraction extracted with concentrated nitric acid. Quanti®cation of the total concentration of chromium present requires a total digestion procedure, to extract chromium present in the clay mineral lattice. Neither technique quanti®es bioavailable chromium. The concentration of dissolved chromium in the Forth Estuary is low (< 1 lg lÿ1 ) which suggests chromium is particle-reactive and is largely removed from solution into the sediments. The sediments of the Forth are enriched with chromium (Balls et al., 1997b), and annual monitoring appears to indicate that the concentration of this element in the sediments is increasing (Fig. 7) which is in direct contrast to the measured reduction in discharges. The concentrations of chromium in Forth Estuary mussels and seaweed are enhanced relative to the `national background' concentrations proposed by ADRIS (1995) of 2 and 1 mg kgÿ1 dry weight, respectively. Chromium concentrations in both mussels and seaweed have decreased over time in the estuary, although the inter-annual variability in mussels was greater than in seaweed. It is concluded that reductions in point source discharges of metals in the Forth catchment have led to rapid reductions in the concentrations of metals in the dissolved phase. However, in a turbid estuary such as the Forth, particle-reactive metals are largely retained within the sediments. Contaminants retained in the sediments are eectively trapped within the estuary (at least for some time) and are available to ®lter-feeding deposit and
Fig. 7 Temporal trends in chromium concentrations in the sediments of the Forth Estuary.
feeding organisms. Biomonitors integrate both the eects of reductions in inputs of metals and their partitioning between sediments and waters, and also provide an indication of the levels of bioavailable metal. Both mussels and seaweed should be included in the monitoring programme, as these constitute eective biomonitors for a range of determinants and respond dierently to metals in the dissolved and particulate phases. The author would like to thank colleagues in SEPA East who have contributed to the production of this paper. In particular I wish to thank Jennifer Fozzard and Una Thom for their analytical work; Tom Leatherland and Anton Edwards for helpful comments; and sta in the General Chemistry section for the discharge information. ADRIS (1995) ADRIS Estuary Classi®cation Scheme. Association of Directors and River Inspectors in Scotland Marine and Estuary Sub-group, Perth, Scotland. Balls, P. W., Owens, R. E. and Muller, F. L. L. (1997a) Dissolved trace metals in the Clyde, Forth and Tay estuaries ± a synopsis and comparison with other UK estuaries. Coastal Zone Topics 3, 46±56. Balls, P. W., Hull, S., Miller, B. S., Pirie, J. M. and Proctor, W. (1997b) Trace metals in Scottish estuarine and coastal sediments. Marine Pollution Bulletin 34, 42±50. Barnet, B. E. and Ashcroft, C. R. (1985) Heavy metals in Fucus vesiculosus in the Humber Estuary. Environmental Pollution (Series B) 9, 193±213. Bryan, G. W. and Hummerstone, L. G. (1973) Brown Seaweed as an indicator of heavy metals in estuaries in South-West England. Journal of the Marine Biological Association of the United Kingdom 53, 705±720. Davies, I. M. (1987) Trace metals and organohalogen compounds in the Forth, Scotland. In Proceedings of the Royal Society of Edinburgh 93B, 315±326. Davies, I. M., Griths, A. H., Leatherland, T. M. and Metcalfe, A. P. (1986) Particulate mercury ¯uxes in the Forth Estuary, Scotland. Rapports et Proces-Verbaux des Reunions du Conseil International pour l'Exploration de la Mer 186, 301±305. Elliot, M. and Griths, A. H. (1986) Mercury contamination in components of an estuarine ecosystem. Water Science and Technology 18, 161±170. Gardner, M. J., Dobson, J. E., Griths, A. H., Jessep, M. A. and Ravenscroft, J. E. (1997) An overview of the UK National marine analytical quality control (NMAQC) scheme and its links with QUASIMEME. Marine Pollution Bulletin 35, 125±132. Leatherland, T. M. (1987) The estuary and Firth of Forth, Scotland: uses and aims. Proceedings of the Royal Society of Edinburgh 93B, 285±297. Luoma, S. N., Bryan, G. W. and Langston, W. J. (1982) Scavenging of heavy metals from particulates by brown seaweed. Marine Pollution Bulletin 13, 394±396.
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Volume 40/Number 12/December 2000 O'Connor, T. P. (1998) Mussel watch results from 1986 to 1996. Marine Pollution Bulletin 37 14±19. OSPAR (1997) JAMP guidelines for monitoring contaminants in biota. Oslo and Paris Commissions Joint Assessment and Monitoring Programme 9 June, 1997. Pedersen, B., Co®no, W. and Davies, I. (1997) The 1993±1995 QUASIMEME laboratory performance study: trace metals in sediment and biota. Marine Pollution Bulletin 35, 42±51. 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±317.
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Phillips, D. J. H. (1980) Quantitative Aquatic Biological Indicators ± Their Use to Monitor Trace Metal and Organochlorine Pollution. Applied Science Publishers, Barking. Phillips, D. J. H. (1995) The chemistries and environmental fates of trace metals and organochlorines in aquatic ecosystems. Marine Pollution Bulletin 31, 193±200. Rainbow, P. S. (1995) Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin 31, 183±192. Rainbow, P. S. and Phillips, D. J. H. (1993) Cosmopolitan biomonitors of trace metals. Marine Pollution Bulletin 26, 593±601.