Contaminants in fine sediments and their consequences for biota of the Severn Estuary

Marine Pollution Bulletin 61 (2010) 68–82

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Contaminants in fine sediments and their consequences for biota of the Severn Estuary W.J. Langston a,*, N.D. Pope a, P.J.C. Jonas b, C. Nikitic c, M.D.R. Field d, B. Dowell e, N. Shillabeer e, R.H. Swarbrick e, A.R. Brown e a

Marine Biological Association, Citadel Hill, Plymouth PL1 2PB, United Kingdom Environment Agency, Manley House, Kestrel Way, Exeter, EX2 7LQ, United Kingdom Jacobs Consultancy, Southampton, United Kingdom d Ecospan Environmental Ltd., Unit 3 Embankment Lane, Plymouth, PL4 9LQ, United Kingdom e Brixham Environmental Laboratory, AstraZeneca (UK) Limited, Freshwater Quarry, Brixham, TQ5 8BA, United Kingdom b c

a r t i c l e

i n f o

Keywords: Severn Estuary Metals PAHs PCBs Sediment Bioaccumulation Hediste (=Nereis) diversicolor

a b s t r a c t When the first MPB special issue was published 25 years ago it was suggested that high body burdens of metals and selected organic pollutants in the Severn Estuary were the result of anthropogenic loadings from a variety of sources. The objective of this synopsis is to illustrate recent trends for contaminants (metals, PAHs, PCBs) in sediments and benthic biota and to consider the evidence for improved environmental quality over the last quarter of a century. Contaminants in sediments and sediment-dwelling fauna such as Hediste (=Nereis) diversicolor are, generally, evenly distributed over the estuary – which is the consequence of extensive re-suspension and redistribution of fine sediment by strong tidal currents. Such dispersal tends to mask the influences of individual discharges and physical characteristics are considered to be the major drivers affecting biodiversity in the Severn Estuary, often overshadowing contaminant concerns. Following the closure of major industries and the introduction of stricter pollution control, many inputs have ceased or been reduced and there are indications that environmental concentrations are now lower. Bioaccumulation of most contaminants has declined accordingly (with the possible exception of Cr). Intuitively, better environmental quality should be linked to ecological improvements. However, due to the dynamic nature of the system (and a lack of biological-effects data) it is difficult to establish direct relationships between inputs, body burdens and biological/ecological consequence. Uniquely, the long-term integrated monitoring program of AstraZeneca (Avonmouth) indicates that recovery of faunal diversity and abundance has occurred in mid-sections of the estuary in recent years implying that contaminants have indeed been a forcing feature for Severn biota. In this context, we highlight contaminant issues and biogeochemical changes which may need to be addressed in connection with the development of proposals for tidal energy schemes. Ó 2010 Elsevier Ltd. All rights reserved.

1. Introduction 1.1. Constraints on Severn Estuary biota and the choice of biomonitoring species The Severn Estuary is characterized by strong physical gradients. The UK’s highest tidal range, powerful tidal currents, sediment erosion and re-suspension result in high suspended particulate loads and the ensuing rapid light attenuation within the water column limits primary production. OSPAR’s Quality Status Report on the Celtic Sea (OSPAR, 2000) concluded that the shore and seabed of the estuary are naturally impoverished for * Corresponding author. Tel.: +44 1752 633 232; fax: +44 1752 633 102. E-mail address: [email protected] (W.J. Langston). 0025-326X/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2009.12.014

these reasons. Considerable salinity variation and deoxygenation, particularly in the upper estuary, are also important constraints affecting biological communities (Warwick et al., 1991; Warwick and Somerfield, 2010). The influence of pollutant pressures, manifested as trends in bioaccumulation or subtle deleterious effects, is likely to be difficult to discern against the background of such strong physical gradients. This is in broad agreement with DEFRA’s Integrated Assessment of the State of UK Seas (DEFRA, 2005); nevertheless, toxicity thresholds (ecotoxicological assessment criteria – EAC) and background reference concentrations (BRC) proposed by OSPAR were exceeded for some contaminants (i.e. Pb in sediments; PCBs in shellfish). According to the Joint Nature Conservation Committee’s Marine Nature Conservation Review (Moore et al., 1998), habitats and species or stated ‘interest features’ of most concern from a chemical

W.J. Langston et al. / Marine Pollution Bulletin 61 (2010) 68–82

contamination perspective include: (i) Intertidal mud-flats, sandbanks and saltmarsh which represent deposition zones within the estuary; (ii) Atlantic salt meadows (Puccinellia maritima/Festuca rubra); (iii) Nationally scarce or threatened sedimentary reefbuilding polychaetes Sabellaria alveolata and Sabellaria spinulosa; (iv) Protected species of birds (e.g. Bewick’s swan Cygnus columbianus) and fish (e.g. migratory salmon Salmo salar and eels Anguilla anguilla, Allis shad Alosa alosa and Twaite shad Alosa fallax, sea lamprey Petromyzon marinus and river lamprey Lampetra fluviatalis). However, benthic fauna and demersal fish in general might be considered susceptible because of their potential exposure to sediment-borne contaminants, especially in lower-energy deposition zones, within the intertidal estuary. Infaunal organisms such as the polychaete Hediste (=Nereis) diversicolor, the crustacean Corophium volutator and the molluscs Hydrobia ulvae, Macoma balthica and Scrobicularia plana are important dietary items (and potential sources of contaminants) for large numbers of fish such as flounder, bass and whiting, and for wading birds such as shelduck and curlew (Little and Shaw, 1980). Any impact causing a significant reduction in the diversity and abundance of intertidal organisms, or an increase in bioaccumulation, can therefore have consequences for populations of estuarine fish and wading birds. The National Marine Monitoring Programme appraisal of the quality of UK coastal waters (1993–1995) concluded that the diversity and abundance of sediment-dwelling invertebrate fauna in the Severn Estuary (Site 635) corresponded to median values derived from all UK estuaries. However, the number of benthic species was noted to be low in the Severn, typically around 15–20 species compared to >100 in Belfast Lough, the Tamar Estuary and Southampton Water (MPMMG, 1998). Greatest species diversity and abundance occurs at the sides of the main channel and within the intertidal areas, but highly variable salinities and sediment instability limit overall species diversity (Mettam, 1997; Moore et al., 1998; Warwick and Somerfield, 2010). Very few filter feeders are present due to sediment instability and the associated high particulate load in the water column (Warwick et al., 1991; see also Warwick and Somerfield, 2010). Several species of barnacle exist inter-tidally, including Elminius modestus, Semibalanus balanoides and Balanus improvisus (Boyden et al., 1977), but larger organisms such as the edible cockle (Cerastoderma edule) and the soft-shelled clam Mya arenaria are absent or very rare (Warwick et al., 1991). The ragworm Hediste diversicolor, the catworm Nephtys hombergi, the laver spire shell H. ulvae, the Baltic tellin M. balthica and the peppery furrow-shell S. plana are among the most abundant macrobenthic species, at least in parts of the estuary (Boyden and Little, 1973; Warwick et al., 1991; Warwick and Somerfield, 2010) and are therefore potentially most useful as biomonitors of contaminants (Bryan et al., 1985). No species of macroalgae or microalgae are highlighted as being of major conservation importance in the Severn Estuary, although the assemblages of different algal species on the intertidal flats provide food and shelter for a range of invertebrates and also wildfowl such as wigeon Anas penelope. There is virtually no macroalgal growth below the low water mark in the majority of the estuary, due to high turbidity. Intertidal microalgae, in the form of a diatom film, are probably most important in terms of primary production (Smith and Little, 1980; STPG, 1989; Paterson and Underwood, 1992; Underwood, 2010). However, intertidal rock and sediment provide suitable substrates for a range of macroalgal species, notably at the entrance of the estuary around Lavernock Point and Brean Down, and beneath the Second Severn Crossing, on the English Stones. The lower estuary is dominated by brown algae, whereas the upper estuary is dominated by green algae Enteromorpha spp. due to increased freshwater run-off. Isolated colonies of Fucus vesiculosus and Ascophyllum nodosum can be found as far upstream as Sharpness Point in the upper Estuary (Moore et al., 1998). Because

69

of their widespread distribution and efficiency as accumulators of dissolved metals (concentration factors in the range 103–104 for many elements), macroalgae such as F. vesiculosus and F. serratus have been used to monitor long-term trends in water quality in the Severn Estuary since the 1970s (Bryan et al., 1985; Martin et al., 1997; Brown, 1998).

2. Objectives 2.1. Characterization of sediment contaminant loadings and biological response The main objective of this review is to draw together a range of published and unpublished data concerning contaminants in sediment and biota in the Severn Estuary in order to distil current understanding of the spatial and temporal trends in distributions and impacts, and define key knowledge gaps. Although somewhat disparate, the majority of these data have been generated using standard methods (e.g. NMMP and more recently CSEMP) and many have been quality controlled according to appropriate AQC schemes such as Aquacheck, Quasimeme, NMBAQC and BEQUALM (for details of methods see Supplementary information in Appendix 1). Estimates of the quantities of contaminants entering the Severn Estuary from industrial and sewage discharges, rivers and other sources were first provided a quarter of a century ago by Owens (1984). Significant industrial inputs have included smelters (now closed), incinerators, fertilizer and numerous other chemical plants in the Avonmouth area; coal and steel industries (now much reduced production), paper mills, chemical and pharmaceutical manufacturers in south Wales; nuclear power plants at Hinkley, Berkeley (being decommissioned) and Oldbury (scheduled for decommissioning). Sewage from the urban centres of Bristol, Gloucester, Newport and Cardiff add directly to the pollutant load, as do domestic and agricultural sources in the large number of tributaries entering the tideway (notably the Avon, Usk and Parrett). The list of potential chemical pressures is substantial and includes metals, hydrocarbons, nutrients, solvents, mineral acids, biocides, fungicides, flame retardants, PCBs, pesticides and radionuclides. However, the decline in heavy industry and introduction of pollution control in the later part of the 20th century has seen a general reduction in inputs (with the exception of nitrates and, to a lesser extent, Cr) – a trend which will presumably continue (see Jonas and Millward, 2010). An EA overview of pollution management at the Avonmouth complex provides examples of some of the improvements implemented and recorded by industry under discharge consents and self-monitoring arrangements (Environment Agency, 2002). Historical contaminant information for the Severn Estuary (up to 2002) has been assessed as part of the review of consents process (Langston et al., 2003). Data used in the current synopsis is derived from a variety of sources but principally the Environment Agency (EA) and the Marine Biological Association (MBA) using established methodology (see Supplementary information in Appendix 1; also Jonas and Millward, 2010). Axial surveys of metals, PAHs and PCBs in sediments and H. diversicolor, initiated by the EA in 2004 and 2005, have added to this evidence-base – enabling chemical and biological trends to be put in a more contemporary perspective (for locations of principal EA, MBA sediment sampling sites see Appendix 2 in Supplementary material). Despite inevitable constraints in the available information, it has been possible to distill a broad appraisal for major contaminant groupings in the following sections, and to establish some useful baselines for assessing progress towards targets set, for example, under the water framework and habitats directives. This includes compari-

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sons with guideline values for contaminants in sediments and an evaluation of spatial and temporal bioaccumulation patterns in biota. In addition, an appraisal of the ecological and chemical dataset at Avonmouth (and other sites in this section of the estuary), collected by AstraZeneca’s Brixham Environmental Laboratory (BEL), provides some unique insights into the long-term effects of chemical and pharmaceutical industry discharges on biodiversity in the vicinity of a major outfall, set in the context of estuary-wide changes recorded at ‘baseline sites’. A number of the environmental quality issues (and knowledge gaps) identified in the sections below will need to be addressed in the forthcoming debate over proposed tidal power options. The fate and impact of particulate contaminants are especially important in the Severn, given that the hydrodynamic regime may change considerably within the estuary.

3. Metals Metals have been a major concern in the Severn, because of smelting and other metal-based industries. Metal concentrations in sediments have become enriched throughout most of the estuary, and enhanced bioaccumulation has been described in invertebrates, macroalgae and, occasionally, higher organisms. Loadings data, summarised by Owens (1984) are now more than 25 years old, though many of the conclusions drawn still usefully indicate likely sources. Rivers were estimated to contribute the greatest proportions of Cu, Fe, Mn and Ni together with substantial inputs of Hg, Cd, Pb and Zn. Domestic sewage was deemed an important source of Cd and Cr, whilst industrial discharges provided major loadings of Hg, Cr, and significant proportions of Cd, Cu, Fe, Pb, Mn and Zn. Atmospheric deposition contributed approximately half of the Pb and Zn input to the estuary, together with substantial proportions of Cd, Cu, and Ni. These inputs may still influence axial distributions in the water column; however, since the appraisal of late 1970s water quality data by Owens (1984), inputs (from consented discharges and freshwater) are estimated to have declined for a number of metals including Hg (89%), Cd (53%), Cu (71%), Pb (83%) and Zn (79%) (Jonas and Millward, 2010). This reduction is reflected in improved estuarine water quality, consistently so for Cd and Pb (twofold reduction over the last 25 years). Most metals are now compliant with environmental quality standards (EQSs), based on annual averages, although sporadic high values for Cu, Zn, Cr and, occasionally, other metals can still occur in the mid-estuary, the cause of which remains to be resolved. It is possible that these ‘anomalies’ are the result of recent discharges, though more likely they are a function of bed-sediment remobilization and re-release of previously sorbed contamination: these events appear to coincide with spring tides when tidal re-suspension of fine fractions is at its highest (Langston and Millward, 2008). There is, therefore, still some uncertainty about the overall distributional patterns of a number of metals in estuarine water, and the scale of any improvements in recent years, because of such events (whose origins and variability require further characterization). Particulates often form an important part of the pollutant loading discharged to estuaries. Scavenging of dissolved metals also occurs (to varying degrees) so that sediment metal concentrations tend to provide a more stable, integrated picture of contamination history, particularly if normalized to grain size or some other geochemical feature. Because of the larger surface area and greater density of organic and oxyhydroxide binding sites, contamination loadings – particularly non-residual forms – are highest in fine sediment fractions (primarily located between Avonmouth and Severn Beach; New Passage to Oldbury; Caldicot Flats; River Parrett and outer Bridgwater Bay; and between the mouths of the Usk and

Taff) and lowest on coarser sands (e.g. Middle to Welsh Grounds, Culver Sands). The bulk sediment metal content is therefore, generally, a function of the proportion of fine sediment, although precise relationships between grain size and metal content can vary depending on metal, location and season (Duquesne et al., 2006). The hydrodynamic energy in the Severn Estuary ensures considerable mixing and redistribution of fine sediments (Manning et al., 2010) and their associated contaminant burden – resulting in homogenous, axial distributions of metals in muds and silts (material which is easily resuspended), rather than the linear gradients seen in ‘typical’ estuaries. It is only downstream of the more turbid sections, outside the mouth of the estuary, where there is a marked decrease in sediment metals. Within the estuary, concentrations of metals in suspended particulates do not differ significantly from those in benthic surface sediment, consistent with a single population of re-suspendable fine particulates. As a result, metal contamination in fines tends to be chronic and evenly dispersed over a large area, including sub-estuaries. This is typified by Cd distributions shown in Figs. 1 and 2. Intensive spatial sampling of sediment on a local scale may, occasionally, pick up a signal from point sources even within this dynamic, fine sediment regime. Such localized enrichment can be seen in Fig. 3 for Cu and Pb at Holesmouth, and for Cd at Kingsweston and Stup Pill (EA survey of <63 lm sediments from the Avonmouth area, 1995). Sediments close to industrial discharges at Avonmouth have also been shown by BEL to be enriched in Cd, Hg, Cu and Zn, compared with regional baselines, though this differential may now be receding. EA sediment surveys in 2004/ 2005 highlight transient ‘hotspots’ at other sites (Fig. 2): of particular note were the exceptional concentrations of Cu (up to 723 mg kg1), together with high values for Cr and Ni, in the sediments at Berrow Flats and Sand Bay in 2004. Another cluster of elevated Cu values was observed upstream (Purton and Lydney Harbour – Fig. 2). Similarly, at Cardiff, high concentrations of Cr were detected in 2004 and 2005, while in 2005 elevated concentrations of As, Cd, Hg, Pb (Fig. 2) and Zn were also found here. ‘Anomalous’ sites of sediment contamination have been described elsewhere in the literature, although it is uncertain whether this reflects sediment transport patterns, rather than the influence of local discharges (Langston et al., 2007a,b; Langston and Millward 2008). A better understanding of such ‘anomalies’ is required to reduce uncertainty over the distribution and impact of sedimentbound metals. For much of the Severn Estuary it is not possible to reconstruct accurately the long-term history of contamination from core profiles due to the mobile nature of the surface deposits, although where consolidated sediment cores have been analysed (e.g. in Swansea Bay, Frampton and Pill House) these reveal the history of increasing metal (Fe, Pb, Zn, Cu) deposition since the middle of the 19th century, indicative of industrialization (Clifton and Hamilton, 1979; Allen, 1987). Estimates by French (1993), based on comparisons between contemporary mudflat samples and preindustrial salt marsh sediments, indicate that the industrial era may have been responsible for a two-to-fourfold enrichment of Cu, Zn and Pb. Some of the core data provide tentative evidence of declines in inputs to surface layers post-industrialization, though more convincing affirmation comes from surface sediment time-series which consistently indicate downward trends in metal loadings. In their comparisons of early data sets, Little and Smith (1994), for example, suggested that Pb, Cu, Cr, Ni and Zn concentrations in fine sediments decreased by 25–50% between the 1970s and 1990s, perhaps due to the contraction or closure of metalbased industries. Inevitably, there is some uncertainty over the extent to which sampling (n.b. grain size) and analytical techniques influences the comparison of disparate sediment data sets; however, scrutiny

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Hediste diversicolor 1978

Hediste diversicolor 2004

Hediste diversicolor 2005

A

B

B

Cd mg/kg

Cd mg/kg

Cd mg/kg

10

10

10

8

8

8

6

6

6

4

4

4

2

2

2

0

0

100 km.

0

100 km.

100 km.

Sediments 1978

Sediments 2004

Sediments 2005

A

B

C

Cd mg/kg

Cd mg/kg 2.5

2.5

2

2

2

1.5

1.5

1.5

1

1

1

0.5

0.5

0.5

0 100 km.

Cd mg/kg

2.5

0 100 km.

0 100 km.

Fig. 1. Cadmium (mg kg1 dw) in Hediste (=Nereis) diversicolor (top) and sediments (bottom): years sharing the same letters share homogenous groupings, otherwise significantly different (P < 0.05 Tukeys HSD test). (1978; HNO3 digest of <100 lm sediment fraction. 2004, 2005; HNO3 digest of <63 lm sediment fraction).

of fine surface sediment data sets generated by MBA and EA (and BEL) demonstrate remarkably consistent composition in the Severn, dominated by silt–clay. Thus, although MBA and EA data are based on different mesh size (100 and 63 lm, respectively) this is unlikely to be a major source of discrepancy since the composition of sediments is dominated by fractions <63 lm (85 ± 2% – median grain size 6.5 ± 0.1 lm – in 2005, for example). Provided that some form of sieving is employed to minimise the influence of grain size, the precise mesh size may not be critical when comparing broad contaminant trends. Comparable organic content (4.24 ± 1.17% and 4.39 ± 0.23%, respectively), whether sieved at <100 lm (1978) or at <63 lm (2005), supports this contention. Observed decreases in sediment metals are therefore consistent with declines in inputs. Estuary-wide reductions of 40–50% for Hg and Cd (Fig. 1), and 18% for Pb, are indicated over the 25 year period up to 2005 (from MBA/EA surveys), with biggest changes occurring prior to 1995. Results of Duquesne et al. (2006) for sites on the English shore (between Redwick and Brean) also suggest Pb and Zn in bulk (unsieved) sediments have decreased by two to sixfold, and Cd by as much as tenfold, over three decades since the early 1970s, due to declining aqueous and atmospheric discharges. Improvement is further indicated by observations at Severnside,

upstream of some of the major historical metal discharges (from smelters at Avonmouth), where reductions in bulk sediment1 Cd, Cu, Hg and Zn, monitored by BEL, were 85%, 33%, 33% and 34%, respectively, between 1975 and 20052 (Swarbrick and Brown, 2007). At ‘reference sites’ in this part of the estuary (Severn Beach, New Passage, Littleton Warth, Shepperdine, Goldcliff, Redwick, Blackrock and Oldbury) reductions were lower at 74%, 8%, 18%, 2%. The ‘weight of evidence’ therefore supports significant reductions of Cd, Cu, Hg and Zn. Few other metals exhibit consistent changes in sediment, with the exception of Cr which appears to have increased in the fine fraction by a factor of two between 1978 and 2005; methodological differences are a possible contributory factor, although Cr concentrations in Hediste show a similar rising trend (see below) and consented discharges of Cr to the estuary have also increased by 16% over this period (Jonas and Millward, 2010), implying the possibility of a real supplement. Enrichment of metals in Severn Estuary fine sediments, relative to UK ‘baselines’, has been described in previous reviews (Bryan 1 Whole sediment samples with a mean silt and clay (<63 lm) content typically in the range 93 ± 2%–98 ± 2%, microwave-assisted digestion in aqua regia; 2 Comparisons for Hg are between 1990 and 2005.

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Fig. 2. Metals in Severn Estuary sediments 2004/2005 (mg kg1 dw), plotted as a function of distance from the tidal limit at Maisemore, in relation to PELs (probable effects levels) and TELs (threshold effects levels) derived from CCME (1999). (HNO3 digest of <63 lm fraction).

Fig. 3. Metals in sediments (mg kg1 dw, <63 lm fraction, HNO3 digest) showing ‘hotspots’ in the Severnside region.

and Langston 1992; Little and Smith, 1994; Langston et al., 2003). Even some of the sandier sediments from deeper waters have exhibited contaminant concentrations in excess of that predicted from their sedimentological characteristics such as Al or organic

content (Little and Smith, 1994). With the advent of recent water quality improvements, excesses above background are in decline, though data from 2004/2005 still indicate consistent, low-level enrichment over much of the Severn which, for most metals, is just

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above the ‘threshold effects level’ – TEL (ecotoxicological guidelines defined by CCME, 1999), with occasional ‘hotspots’, discussed above, which exceed ‘probable effects levels’ – PEL (Fig. 2). On this basis, acute effects are likely only at a small number of contaminated sites, though chronic effects cannot be excluded across much of the estuary. Interestingly, concentrations of Cd (one of the more important metals from a bioaccumulation aspect) now fall consistently below the TEL (Fig. 2), suggesting that direct toxicological impacts of sediment-bound Cd are unlikely. The bioavailability of sediment-bound contaminants in the Severn Estuary can be gauged using relevant, practical biomonitors such as H. diversicolor, and deposit-feeding clams M. balthica and S. plana. In contrast, the seaweed F. vesiculosus is favoured for assessing the bioavailability of dissolved contaminants (Bryan et al., 1985; Bryan and Langston 1992; Langston et al., 2007b). It is important to note that the relative accumulation of metals by different organisms in the Severn may differ markedly, depending on their physiology, feeding strategy, and the physicochemical behaviour of the metal itself. For example Ag, a highly particle reactive metal (Shafer et al., 1998), is accumulated preferentially in deposit-feeding clams, whereas the more soluble metal Cd is accumulated to highest levels in macroalgae Fucus spp. (Bryan et al., 1980). Despite differences in comparative bioaccumulation rates, most biomonitors display common trends in the Severn, and whilst no single species is ideal, H. diversicolor probably best serves to illustrate spatial and temporal trends because of its widespread distribution. This polychaete worm is also an important prey item for birds, fish and other predators: it therefore plays a significant role in the transfer of sediment-bound contaminants along food chains. The dynamic nature of the Severn, and the dispersed nature of fine sediments with their associated contaminant load, might be expected to result in bioaccumulation spread over a large area. Based on MBA (1978) and EA (2004/2005) data sets for H. diversicolor, this broadly appears to be the case – as indicated in the example for Cd in Fig. 1: similar homogeneity within the estuary occurs for a range of metals including Ag, Cr, Cu, Hg, Ni, Pb, Zn (see means ± SE for H. diversicolor, Table 1). Body burdens in biota from the major sub-estuaries are also comparable to those within the Severn itself, consistent with the concept of extensive mixing. Thus, within the Severn Estuary, the homogenous trends in metal burdens in H. diversicolor do not appear to be strongly affected by any individual outfall but, rather, reflect the combined loading. Slight gradients in bioaccumulation, decreasing downstream, are becoming less marked, as contamination levels wane: axial trends were significant for Ag, Cd and Hg in H. diversicolor in 1978 (P < 0.05) and in 2004 (Cd only), but none were evident in 2005. Metal concentrations in tissues of H. diversicolor and other biomonitors only decline, substantially, beyond the mouth of the estuary, in the Bristol Channel (Fig. 1, 1978 data).

Because of the narrow range of contaminant concentrations in the Severn, there are few significant correlations between sediments and body burdens in H. diversicolor, the best being for Hg, and, to a lesser extent Cd and Cr. Concentrations of Cd, Cu and Hg in H. diversicolor exceed levels in sediment, though for Cd the degree of magnification is declining: the relative ratio (bioaccumulation factor – BAFsed) is currently near unity, compared with an average value of 3.5 in 1978. Other metals examined do not appear to be bioaccumulated significantly in relation to sediment loadings. The decrease in Cd in Severn Estuary biota over the last 25 years is most notable and is consistent with trends in tidal waters and benthic sediments over the same period – though, as implied from BAFsed, above, and illustrated in Fig. 1 and Table 1, Cd concentrations in H. diversicolor have declined proportionately more (>80% as an estuary-wide average) than those of sediments (50%). It may be that the steeper reduction in bioaccumulated Cd reflects the preferential decrease of labile (bioavailable) fractions from sediments which, though biologically dominant, may represent only a small proportion of the total sediment Cd load. The decrease in Cd body burdens is partly an indication of the success of pollution control measures in reducing inputs, and partly the result of industrial decline. Recent closure of the smelter at Avonmouth may result in further Cd reductions in the future. Body burdens of Ag, Ni, Pb and Hg in Severn H. diversicolor have also declined during the last two–three decades, by 73%, 58%, 39% and 60%, respectively (Table 1). There were few changes in body burdens between 2004 and 2005, relative to the larger reductions seen in earlier years, and conditions for a number of metals may now be approaching steady state. 30 years ago, the degree of metal enrichment in Severn H. diversicolor (compared to background values in UK estuaries) decreased in the order Cd > Ag > Hg >> Pb > Cr > Ni > Cu > Sn > As > Mn > Zn and Fe (Table 2), with anthropogenic (pollutant) metals displaying most enhancement. The most recent data (2005) indicate that these enrichment factors have decreased, with the exception of Cr: the relative ranking of enrichment is now Cr > Ag > Hg > Cd > Pb > Cu > Ni > Zn (Table 2). The atypical increases for Cr in H. diversicolor coincide with increases in sediment concentrations and Cr discharge consents, as discussed above. Biomonitoring is best approached using a combination of several species, which encompass different exposure routes and compensate for variations in metal metabolism. Body burdens of Zn in H. diversicolor, for example, may underestimate environmental contamination, since, as an important essential element in the ragworm, it may be controlled by a degree of internal regulation (perhaps contributing to the low ranking of Zn in the above sequences). The use of Fucus spp. has proved a useful supplement for depicting trends in bioavailability of such metals. Thus, time-series data (1975–2005) for F. vesiculosus from Severnside and other stations around the estuary, gathered by BEL, highlight substantial and con-

Table 1 Hediste diversicolor. Comparisons of mean (±SE) concentrations (mg kg1 dw) in Severn Estuary samples collected in 1978 (MBA), 2004 and 2005 (EA).

1978 2004 2005

Ag

Cd

Cr

Cu

Hg

Ni

Pb

Zn

7.86 ± 1.18 4.54 ± 0.42 2.14 ± 0.33

3.47 ± 0.39 0.59 ± 0.07 0.43 ± 0.05

0.19 ± 0.02 2.11 ± 0.30 1.80 ± 0.25

46.9 ± 5.3 76.5 ± 7.59 59.7 ± 9.18

1.53 ± 0.21 0.62 ± 0.06 0.61 ± 0.09

5.22 ± 0.26 2.64 ± 0.20 2.19 ± 0.19

2.87 ± 0.18 1.92 ± 0.18 1.75 ± 0.17

250 ± 9.98 205 ± 11.3 192 ± 15.5

Table 2 Hediste diversicolor. Metals enrichment in Severn Estuary worms, relative to UK baselines, in 1978 (MBA data) and 2005 (EA data).

1978 2005

Ag

Cd

Cr

Cu

Fe

Mn

Ni

Pb

Zn

Hg

As

Sn

133 35

189 21

17 60

7 7

1.8 na

3.5 na

7.8 3.4

22 10.9

3 2.1

71 31

4 na

6.2 na

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areas where they are found (Bryan et al., 1985). Alternative monitoring organisms which might be considered relevant for future investigations in the Severn Estuary, because of their distribution, abundance, importance in the food chain, and sediment-dwelling habitat, are the bivalves M. balthica and S. plana and crustaceans C. volutator. 4. PAHs

Fig. 4. Fucus vesiculosus: trends in Cd, Cu, Zn (mg kg1 dw) at Severnside and background beaches between 1985 and 2005.

sistent reductions in Zn (Cd and Cu), particularly in earlier years (Fig. 4). The scale of Cd reductions in F. vesiculosus at Severnside, Avonmouth (almost tenfold) reflects proximity to major sources in this part of the estuary. Similar surveys with other species, including the shore crab Carcinus maenas, provide further evidence of the success and extent of Cd remediation. However, C. maenas regulates Cu (because it is an essential component of the blood pigment, haemocyanin); its value as an indicator of Cu (and Zn which is also partially regulated), is therefore limited. The mobility of shore crabs further reduces their value as sentinel organisms. Other species used as biomonitors of metal contamination in the region have included Mytilus edulis, monitored as part of the National Marine Monitoring Programme (MPMMG, 1998): tissue residues in Severn mussels were classified as moderately contaminated with Cd (up to 10 mg kg1 dry weight) and Hg (0.6 mg kg1 dry weight). Unfortunately, mussels are absent throughout much of the estuary (most likely due to limiting substrates, salinity and high turbidity) and are also partial regulators of Cu and Zn, potentially underestimating contamination in the

In comparison with other industrialized estuaries (e.g. River Tees), PAH concentrations measured in waters of the Severn appear to be unexceptional (Law et al., 1997; DEFRA, 2005) and in recent EA surveys, the majority of values were below limits of detection (DL). Assuming a nominal value of ½DL in these samples, P the ‘median’ total ( PAH) concentration of nine PAHs in 2005 was estimated at 55 ng l1 – below OSPARCOM guideline ecotoxicological assessment criteria for pyrene, fluoranthene and benzo(a)pyrene (OSPAR, 2000) and substantially below the threshold of P 1 lg l1 for PAH proposed by Cole et al. (1999) to be environmentally important. The higher molecular weight homologues (including benzo(a)pyrene, fluoranthene, pyrene and chrysene) are readily adsorbed onto particulates. Their principal fate in typical accreting estuaries is sediment burial due to their high particulate affinity and microbial refractivity, and in macro-tidal estuaries PAH distributions in the water column are often correlated with suspended solids. As with metals, identification of specific PAH sources in Severn Estuary sediments is therefore hindered not only by the complexity and diversity of inputs, but also by the considerable re-suspension and redistribution of particulates. Previously, sources of PAHs in the Severn have been suggested to include drainage from the South Wales coalfield (including coal dust), oil bearing shales in Bridgwater Bay, (John et al., 1979; Cooke et al., 1979) and combustion of fossil fuels (sourced via land run-off and the precipitation of airborne particulates). Sediment loadings determined in the past have included PAHs which may be expected to harm the estuarine environment such as B(a)P (470 lg kg1), phenanthrene (1100 lg kg1) and methylphenanthrene (550 lg kg1) (Thompson and Eglinton, 1978). As a result of this legacy, PAH contamination in Severn Estuary sediments has been considered as being moderately high – principally reflecting anthropogenic origins. Concentrations of PAHs in Severn sediments, however, were not as high as those recorded from industrialized estuaries of north-east England. Results of UK coastal surveys published by Woodhead et al. (1999) indiP cated that the 15 PAHs in sediments from Severn Beach (adjacent to the M4 road bridge) was 5425 lg kg1 (dry weight), and a similar concentration, 5472 lg kg1, was measured in sediments from the English Grounds in mid-estuary (between Cardiff and P Weston Super-Mare). Further west at Port Talbot, PAH concen1 trations in sediments were higher (7124 lg kg ) but values decreased to below threshold effects levels outside the Bristol Channel (464–1014 lg kg1, Celtic Deep). To put these data in perspective, the highest UK value was >100,000 lg kg1 at an oil-impacted site in Milford Haven (Woodhead et al., 1999). P Summary statistics for 10 PAHs in more recent Severn sediment samples suggest lower values to those reported in the previous decade by Woodhead et al. (1999). The median values of 2628 and 3076 lg kg1 in 2004, 2005, respectively, were above the TEL P of 1684 lg kg1 (dry weight), but well below the PEL for PAHs 1 of 16,770 lg kg (dw). Concentrations of the ten individual PAHs co-varied significantly (P < 0.01), and, like metals, were homogeneously spread throughout the estuary, as typified by anthracene in Fig. 5. Elevated values near Cardiff were a consistent feature, P however. PAHs were related to sediment organic carbon content (r = 0.53, P < 0.001 in 2004) though this relationship was weakened by the anomalous PAH enrichment at several Cardiff sites.

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These plots highlight the apparent ‘hotspot’ in the vicinity of Cardiff and its potential ecotoxicological relevance. Here, concentrations of anthracene, naphthalene, phenanthrene, and in one sample fluoranthene, were above the PEL in 2005. For the majority of samples, PAH sediment concentrations were just above the lower threshold (TEL). On this basis, deleterious effects are only likely at a small number of sites, though chronic effects cannot be excluded across much of the estuary. Inter-annual variation (2004– 2005) was small but significant (P < 0.001) for most PAHs, with higher mean values observed in 2005 – probably due to the inclusion of additional contaminated sites in the latter survey. For naphthalene, the difference in mean concentrations between years was not significant (P > 0.05). The general trend in PAH bioaccumulation in biota of the Bristol Channel/outer Severn Estuary was demonstrated in a 1996 study of benzo(a)pyrene residues in mussels sampled along the Welsh coast (CEFAS, 2000). A steep increase in bioaccumulation from west Wales towards Cardiff Flats was tentatively related to the trend in urban development along the coastline (increasing eastwards) and to the delivery, from upstream, of PAHs derived from other parts of the Severn catchment. Recent data on PAHs in H. diversicolor collected in 2004/2005 suggest a more complex picture within the Severn Estuary itself and also indicate greater spatial variability in concentrations compared with the more homogenous distributions in sediments (Fig. 7 illustrates H. diversicolor data for 2005). H. diversicolor from Caldicot had higher body burdens for a number of PAHs than other sites; however, it should be noted that there were no H. diversicolor samples taken at Cardiff, where sediment PAHs were highest. This may partly explain why there were no

Sediments 2005 Anthracene

µg/kg 1000

800

600

400

200

0 100 km. Fig. 5. Concentrations of anthracene (lg kg1 dw) in Severn Estuary sediments, 2005. The distribution shown is similar for all PAHs measured.

Fig. 6 depicts concentration trends as a function of distance along the estuary for several individual PAHs, in relation to sediment quality guidelines – PELs and TELs (Macdonald et al., 1996).

Naphthalene

Anthracene 500

Naphthalene (µg kg-1dw)

2004

450

Anthracene (µg kg-1dw)

800

2005

400

TEL

350

PEL

300 250 200 150 100

2004

700

2005

600

TEL

500

PEL

400 300 200 100

50

0

0 10

30

50

70

10

90

30

Phenanthrene

2005

1000

TEL

Fluoranthene (µg kg-1dw)

Phenanthrene (µg kg-1dw)

2004

1200

PEL

800

70

90

Fluoranthene

2500

1600 1400

50

km downstream from Maisemore

km downstream from Maisemore

600 400 200

0

2004 2005 TEL PEL

2000

1500

1000

500

0 10

30

50

70

km downstream from Maisemore

90

10

30

50

70

90

km downstream from Maisemore

Fig. 6. PAHs in Severn Estuary sediments, 2004, 2005 (lg kg1 dw), plotted as a function of distance from the tidal limit at Maisemore, in relation to PELs = probable effect levels and TELs = threshold effect levels.

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Anthracene

Benz[a]anthracene

Benzo[ghi]perylene

µg/kg 100

80

µg/kg

µg/kg

100

25

60 80

20 40

15

60 40

10 20

20

5 0

0

100 km.

0

100 km.

Pyrene

100 km.

Chrysene

Fluoranthene

µg/kg

µg/kg

100

100 µg/kg

80

80

100

60

80

60

60

40

40

40 20

20

20

0

0

100 km.

0

100 km.

Ideno(1,2,3CD)pyrene

100 km.

Naphthalene

Phenanthrene

µg/kg 100

80

µg/kg

µg/kg

500

250

400

200

300

150

200

100

100

50

60

40

20

0 100 km.

0 100 km.

Fig. 7. Hediste (=Nereis) diversicolor. PAH concentrations in 2005 (lg kg1 dw).

0 100 km.

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clear relationships between body burdens and sediment concentrations. Most individual PAHs were significantly correlated in H. diversicolor (35 out of a total of 45 possible combinations), reflecting similar patterns of bioavailability for many of the homologues, although PAH bioaccumulation factors (BAFsed) in H. diversicolor were variable and were highest for naphthalene. In 2005, the mean naphthalene BAFsed was 0.4, compared with 2 the previous year. This implies that the majority of PAHs are unlikely to be concentrated significantly (in polychaetes at least) in relation to sediment loadings. 5. PCBs and other synthetic organics PCBs are amongst the most persistent contaminants, implicated in a range of ecotoxicological effects (reproductive, immunological) and are of concern in the Severn because of their historical manufacture at Newport. In a study of PCB contamination of sediments from the inner Severn, conducted 25 years ago, Cooke et al. (1979) reported high levels of PCBs adsorbed, preferentially, to coal dust. The highest PCB concentrations (1120 lg kg1 dw) were found where sediments contained a high proportion of coal (Arlingham); at Aust and Sharpness, mean concentrations of total

A

PCB were 791 and 589 lg kg1 dw, respectively – above the current sediment quality guideline (TEL) value for total PCBs of 21.5 lg kg1 dw, and also above the probable effect level (PEL) of 189 lg kg1 dw (CCME 1999). These levels are also significantly higher than the OSPAR provisional ecotoxicological assessment criP ICES 7 congeners). teria (EAC), set at 1–10 lg kg1 (for the NMMP surveys of sediments in the early 1990s highlighted that PCB concentrations in the Severn Estuary were amongst the uppermost in the UK. The highest reported levels (e.g. up to 25 lg kg1 of the individual congener, PCB 153) were those close to where PCBs were previously manufactured (MPMMG, 1998). The more recent surveys in 2004/2005, which included analysis P of the ICES 7 congeners (PCB 28, 52, 101, 118, 138, 153 and 180), indicate a homogenous distribution in fine sediments throughout most of the Severn Estuary, similar to metals and PAHs. The distribution of congener 153, shown in Fig. 8A, is typical of this pattern (all PCB congeners co-varied significantly). Concentrations of the P ICES 7 congeners ranged from 11–41 lg kg1 in 2004/2005, with a mean value of 26 ± 4.8 lg kg1. All values therefore exceeded the P precautionary OSPAR provisional EAC (for the ICES 7 congeners), placing them in a ‘high’ category (OSPAR, 2000), but were mostly at, or just above, the TEL, and well below PEL (Fig. 8C). Compared with earlier published values, PCB concentrations appear to have

B

Sediments 2004 PCB153

Hediste diversicolor 2004 PCB153

µg/kg 100 µg/kg

80

10 60

8 6

40

4 20

2 0

100 km.

C

200

PCBs in sediment (ICES 7)

2004 2005 TEL PEL

150

µg kg-1 dw

0

100 km.

100

50

0

0

20

40

60

80

100

Km downstream Maisemore Fig. 8. PCB (congener 153) concentrations (lg kg1 dw) in sediment (A) and Hediste (=Nereis) diversicolor (B) and PCBs ( from the tidal limit at Maisemore, in relation to PELs = probable effect levels and TELs = threshold effect levels (C).

P ICES 7) in sediment plotted as a function of distance

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decreased. The concentration range for congener 153 in 2004/2005 was 1.99–7.32 lg kg1 compared with an upper value of 25 lg kg1 reported for the same congener near Newport during the previous decade (MPMMG, 1998). Bioaccumulation of PCBs varies between congeners and is the net product of uptake and excretion/degradation. In H. diversicolor sampled in 2004/2005, readily-metabolised, lower chlorinated congeners (28, 52 and 101) were generally below detection. The spatial distributions of more highly chlorinated PCBs in the Severn Estuary was typified by concentrations of congener 153 (2,4,520 ,40 ,50 hexachlorobiphenyl), shown in Fig. 8B. It is difficult to discern any distinct trend in bioaccumulation from these data and there was no significant correlation with PCB concentration in sediment for any of the congeners because of the homogeneous distributions. Nevertheless, the vulnerability of infaunal species to the accumulation of lipophilic compounds is illustrated by bioaccumulation factors (BAFsed) in H. diversicolor, which were highest for the hexachlorobiphenyl 153 (sixfold relative to sediment). The hexachlobiphenyl 138 and heptachlorobiphenyl 180 displayed BAFs of 4. The predominance of these persistent forms suggests origins in the more highly chlorinated mixtures such as Arochlors 1254 and 1260, though these have not been manufactured in the area for a number of years. Persistent PCB congeners can thus be transferred from sediment and accumulated in the tissues of invertebrates like H. diversicolor, and may subsequently be magnified along the food chain, potentially resulting in high concentrations in upper trophic levels (fish, birds and marine mammals). There are no recent studies on biomagnification of residues in higher estuarine fauna, though PCB burdens in the muscle of eels A. anguilla which use the estuary for migration were determined in earlier specimens caught in Welsh rivers (Weatherley et al. 1997). Concentrations of PCB exceeded 1000 lg kg1 (ww) in eels from river stretches in industrialized areas draining into the Severn Estuary such as the Taff, the Afon Llwyd (which joins the Usk above Newport), and the Sirhowy (Weatherley et al. 1997). In contrast, the concentrations of PCB congeners in freshwater eels from Stourport-on-Severn, upstream, were much lower and ranged between 1.8 and 30 lg kg1 ww, with BAFsed ranging from 4–6 (Harrad and Smith, 1997). It may be prudent to update the assessment of distributions and risks from PCBs to wildlife in the estuary, particularly in the context of future remobilization of sediment. A number of other synthetic organic compounds have been detected, occasionally, in elevated concentrations in Severn Estuary samples (e.g. DDT, dieldrin and endrin in sediments; DDT, lindane and dieldrin in eels; dieldrin, triazines and endosulphan in water). This is despite long-existing bans or restrictions on many of these substances. Rivers draining catchment areas with intensive agriculture probably introduce the largest pesticide and herbicide loadings; however, high concentrations can sometimes occur in point discharges. Water quality monitoring of rivers entering the Severn Estuary has indicated several EQS excedences for pesticides and herbicides in the past (Langston et al., 2003), though currently, these occur rarely, if at all. The majority of organochlorine pesticides analysed in H. diversicolor in the 2004/2005 survey (drins, P DDT, HCHs, HCB(D)) were below detection limits making accurate assessment of bioaccumulation trends impossible. Nevertheless, despite the paucity of data with which to characterize, fully, the distributions and threats to biota, it seems unlikely that these compounds, individually, pose widespread risk across the Severn Estuary. Data on organotins in the Severn are also scarce, particularly for biota. Whilst available evidence indicates relatively low levels in estuarine waters, there are indications of sporadic inputs from a number of discharges and catchments throughout the region (Langston et al., 2003, 2007b). Analyses of dredge spoils in and

around the SAC suggest there may be localized reservoirs of TBT near major ports and conurbations, such as Newport and Cardiff. Given the well-documented effects of triorganotin compounds and their ready sequestration and accumulation in estuarine sediments, the sources, sinks and impacts of TBT around the Severn Estuary may merit further investigation. The same is true of the wider effects of endocrine disruption (ED). In the review of ED information in UK SACs by Allen et al. (2000), the absence of data for the Severn seems remarkable, for such a major estuary. Recently, elevated levels of ovotestis – an intersex condition in which oocytes are found in the testis of males, and analogous to (xeno)oestrogen-related effects in freshwater fish – have been observed in clams S. plana from sites in the lower Severn and South Wales (Langston et al., 2007a). Better understanding of the severity, extent and causes of this condition may help to address the ED information gap and assist in screening for effects throughout the area. 6. Nutrients Nutrient Impacts from point sources are probably localized, because of rapid dilution – even those which are components of large-volume discharges. For, example, ICI identified ammonia as their most significant discharge component to the Severn Estuary at Severnside (now ceased), with a typical effluent concentration of 240 mg l1 (compared to a consent allowing discharge at 1500 mg l1). The safe environmental concentration in estuary (receiving) water was assumed to be 1 mg l1 of total ammonia, of which the more toxic un-ionized ammonia was estimated to comprise 2% (20 lg l1) – comparable to the proposed EQS of 21 lg l1 (Brown, 1998). Therefore, the minimum dilution required to meet this standard was determined to be 240 under normal discharge conditions, and was considered likely to be achieved within a short distance of the outfall (Riddle, 1995). Nutrient levels and loadings in the Severn Estuary are significant in UK terms (Langston et al., 2003; Underwood, 2010) and there are indications that, in contrast to most ‘toxic’ contaminants, nitrate inputs to the estuary have been increasing in recent years (Jonas and Millward, 2010). However, with the exception of unionized ammonia, nutrients per se are not directly toxic: the main concern is indirect toxicity, through the promotion of undesirable algal blooms and associated effects of enhanced primary productivity (reviewed in further detail by Underwood, 2010). High turbidity in the Severn Estuary means that light penetration and resultant algal productivity is generally low, except in localized areas. Eutrophication is therefore not currently a major issue within the SAC (but could become so if nutrient concentrations continue to rise and if turbidity is reduced as a result of modifications associated with tidal power development). Intermittent oxygen sags occur in low salinity regions of the Severn and in some of the principal rivers feeding the Estuary. These probably originate from the high densities of suspendable solids and associated particulate organic matter, perhaps enhanced by discharge outfalls: this too could become a more significant issue if the pattern of tidal incursion and flushing characteristics change markedly. 7. Radionuclides Transuranic radionuclide contamination in the Severn Estuary, from local nuclear power operations, is low, and exposure risks to humans from all sources are considered minimal, based on results from routine monitoring (RIFE, 2007). Widespread occurrence of tritium (3H) has been described in waters of the Severn Estuary, with elevated levels at Hinkley and Cardiff, though 3H concentra-

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Table 3 Long-term changes in intertidal benthic fauna abundance and diversity at Severnside and the wider Severn Estuary (‘background’) 1980–2005. For lists of sites and species see Appendices in ‘Supplementary material’. Year

1980 1985 1990 1995 2000 2005

Mean No. of individuals per 0.1 m2

Mean No. of taxa per 0.1 m2

Total No. of taxa

Severnside pipeline

Background

Severnside pipeline

Background

Severnside pipeline

Background

All stations

222 294 912 381 567 1092

211 87 207 162 286 657

5 4.5 5.8 7.8 4.3 11.1

3.3 3.3 3.3 7 5.3 7.3

13 16 19 19 17 23

17 10 15 19 12 17

17 16 19 22 17 25

tions generally decrease seaward and at the mouth of the Bristol Channel are below the detection limit of 2 Bq kg1 (CEFAS, 2007). Anomalously high concentrations of organically bound tritium in sediments and benthic biota in the Cardiff area have been attributed primarily to a local industrial discharge and remedial action has been initiated in recent years which has been effective in reducing sediment loadings and body burdens in benthic organisms (RIFE, 2007). Somewhat surprisingly, much of the tritium in biota near Hinkley also appears to be in organic form, suggesting similar origins to the Cardiff anomaly, although bioaccumulation pathways, sources and effects appear to warrant additional research.

8. Ecological effects Contaminant concentrations now comply with environmental quality standards and sediment quality guidelines over much of the Severn. Extrapolating from these generic ecotoxicological thresholds (EQSs, PELs, TELs), biological-effects on marine life due to contaminants would be anticipated to be chronic, rather than acute, across much of the Severn Estuary, if they occur at all. However, direct evidence to support this contention, by, for example, application of sub-lethal biological-effects tools, is lacking. Data on impacts at higher levels of biological organisation (population, community) are equally sparse and often anecdotal, retrospective or correlative. For example, concentrations of most contaminants have declined during the last quarter of a century, coinciding with increases in a number of fish populations in the estuary (Potter et al., 2001), and it may be speculated that such ecological improvements are one of the beneficial effects of better water quality (Duquesne et al., 2006). However, further mechanistic evidence of cause and effect linkage between contaminants and biota, and in particular the benefits of remediation, would be useful, as there are few studies which address this important issue. One exception is the long-term benthic monitoring of industrial discharges at Severnside by the AstraZeneca (AZ) Brixham Environmental Laboratory (BEL). This 40 year programme, first established by ICI in 1965 and subsequently sponsored by AZ and Terra Nitrogen UK, is one of the longest and most consistent data sets of its kind. Throughout this period, intertidal surveys have been conducted annually, by hovercraft – from Avonmouth to Oldbury and from Goldcliff to Blackrock, along the English and Welsh shorelines, respectively, an intertidal area of approximately 10 km2. This encompasses sites close to the Severnside discharges as well as ‘background’ sites in the area (Appendix 3). These extensive foreshore mud-flats, which support nationally and internationally important bird populations (Avon Bird Report, 2005; BRERC, 2005) and fish (Langston et al., 2003), have gradually increased in benthic macro-invertebrate fauna diversity and abundance (Table 3; Fig. 9). The levels of heavy metals in representative biomonitors, and in the sediments to which they

Fig. 9. Changes in intertidal benthic macro-invertebrate fauna diversity at longterm Brixham Environmental Laboratory monitoring stations in the Severn Estuary 1980–2005; means and 95% confidence intervals shown. See Appendices in Supplementary information for sites and species.

are exposed have decreased, correspondingly; however, so too have populations of predating waterfowl. Following standardisation of BEL survey methods prior to 1980, changes in the diversity and abundance of benthic macro-invertebrate infaunal taxa (>0.5 mm) at long-term survey stations have been monitored annually (Appendix 3, 4, Supplementary material). The changes summarised in Fig. 9 and Appendix 4 span the same intervals as chemical monitoring which illustrates the decline in metal concentrations in sediments and estuarine fauna and flora, discussed in Section 3, above (including bladder wrack F. vesiculosus (Fig. 4) and the shore crab C. maenas). Benthic invertebrate faunal diversity on the Severnside foreshore, including Chittening Warth adjacent to AstraZeneca’s and Terra Nitrogen’s Severnside effluent pipeline, and Severn Beach, has almost doubled from 13 taxa in 1980 to 23 taxa in 2005, whilst mean faunal abundance – though varying considerably – has shown a similar upward trend, peaking at over 1000 individuals per 0.1 m2 (Table 3). Comparable trends have been discernable for background stations beyond the potential sphere of influence3 of the pipeline discharge. Superimposed on the overall pattern of ecological improvement, both sets of data emphasise a dip in benthic macro-invertebrate fauna communities in the wider estuary in 2000, before recovery is resumed (Table 3). This is illustrated in a multi-dimensional scaling (MDS) plot of annual average community data, but is most evident for the MDS plot of background stations, in which the chronological sequence of change in faunal communities, from left to right, is clearly interrupted in 2000 (Fig. 10). Several factors

3 The sphere of influence of the AZ/Terra Nitrogen UK discharge has been defined by the hydrodynamic dispersion model BELPLUME (Riddle, 1995).

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SEVERNSIDE FORESHORE 2D Stress: 0 Transform: Square root Resemblance: Bray Curtis similarity

%Similarity

1990

40 60

2000 1995 1985

2005 1980

BACKGROUND BEACHES 2D Stress: 0 Transform: Square root Resemblance: Bray Curtis similarity

including Sphaeroma sp., Hyale sp., Hyale prevostii and the brown shrimp C. crangon. These are not noted as warm-water species. Therefore their appearance or increase in abundance is further evidence supporting the links between improvements in chemical and ecological quality (as opposed to climate-driven change), especially given that crustaceans are generally considered to be more sensitive than other invertebrate phyla to chemical contaminants (Dallinger and Rainbow, 1993; OECD, 1998; Larsson et al., 2000). Both the Severnside pipeline and background stations currently support seven crustacean taxa, with three being common to both: the isopods Cyathura carinata and Sphaeroma sp. and the widespread amphipod C. volutator. Considering that the reproductive biology of these crustaceans involves parental brooding rather than broadcasting via a planktonic larval phase (as is the case for members of other phyla such as molluscs and annelid worms), looking ahead, their distribution may become more localised as a result of reduced dispersion following the construction of a barrage in the estuary. This could act as a physical barrier possibly preventing the dispersal of holo-benthic species and limiting future changes in the benthic communities of the estuary.

%Similarity

40 60

1985

9.1. Marine water quality issues and tidal power development

2000

2005 1980

9. Conclusions and recommendations

1990 1995

Fig. 10. Multi-dimensional scaling plots of annual average benthic macro-invertebrate fauna abundance data for Severnside Foreshore and background beaches.

which have previously been shown to affect the population dynamics of brown shrimp Crangon crangon in the Bristol Channel, such as river in-flow, salinity variation and the annual mean abundance of predating fish (Henderson et al., 2006; Henderson and Bird, 2010) do not correlate with the long-term community changes at Severnside and surrounding background sites in the lower Severn Estuary. At first glance the underlying reasons for these variations appear to be linked to other climatic factors, including gradually increasing water temperatures (Joyce, 2006) coupled with repeated high storm surges in 2000 (POL, 2008) and presumably increased tidal scouring. It is conceivable that the pipeline itself may provide some physical shelter from such events for nearby faunal communities. Another factor potentially influencing benthic faunal abundance, besides declining contaminant concentrations and climatic factors, is reduced predation by waterfowl. However, the comparatively higher densities of waders including black-tailed godwit Limosa limosa, curlew Numenius arquata and turnstone Arenaria interpres at Severnside and Severn Beach – constituting more than 10% of their total populations in this small area of the Severn Estuary (BRERC, 2005; WeBS 1999– 2000; Avon Bird Report 2005; Burton et al., 2010) – would tend to suggest that predation is of lesser importance compared to chemical and physical pressures on benthic macro-invertebrate communities. Examining the combined list of 46 infaunal (sediment-dwelling) taxa recorded from all survey stations during the standardised BEL monitoring programme (Appendix 4) reveals that recent ‘‘improvements” have been due in part to an influx of crustaceans

Some of the main principles governing contaminant distributions in the Severn Estuary, resultant consequences for biota, and changes that have taken place in recent years have been assembled from available evidence. Though somewhat disparate, the information has at least provided an opportunity to consider the status of contaminants in the Severn in a broad context and to identify some of the knowledge gaps most pertinent to sustainable energy planning. The energetic hydrodynamic regime within the Severn Estuary dominates sediment distribution and composition, which are, in turn, primary components governing the distribution of both contaminants and organisms. This co-variance makes the identification of cause and effect difficult: because physical conditions tend to dominate the majority of biological communities, there is little unequivocal evidence of impact due to contaminants. Judging from recent recovery scenarios described above, detrimental effects due to pollution have probably occurred but, as with the distribution of contaminants in sediments, may have been obscured by dispersal. However, elevated levels of metals and PAHs are occasionally observed in a small number of sediment (and water) samples. Further investigation is needed to establish whether these transient ‘hotspots’ are indicative of discharges, or are related to tidally induced remobilization and deposition events, and to confirm their toxicological significance. Tidal power schemes under consideration are likely to impact upon the geomorphology of the system and its sediment dynamics, therefore changes in contaminant distributions and behaviour, including bioavailability, would seem inevitable. The fate of nutrients and changes to the eutrophication status of the Severn Estuary will be a major concern if turbidity is reduced, as discussed elsewhere in this issue (see Underwood). Predicting the nature, magnitude, and direction of change for other classes of contaminants is hindered by limitations in understanding their behaviour in response to altered hydrodynamics. The need to consider generic modifications which may arise as the sediment, salinity and tidal regimes change is therefore a fundamental requirement to progress the debate. There are other contaminant issues about which we are poorly informed. Trends in bioavailability have been described here for H. diversicolor, mainly, but it would be a sensible precautionary

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measure to screen bioaccumulation in other key organisms, notably in molluscs such as M. balthica and S. plana and the crustacean C. volutator. On a more specific theme, the unexpected anomaly of organic tritium in sediments and benthic organisms from the Cardiff area has been effectively managed but highlights the fact that the bioavailability, assimilation pathways and effects of radionuclides on marine life require detailed consideration, particularly if there is the possibility of nuclear power development around the estuary, alongside tidal barrage construction. The consequences of thermal pollution should be included in these deliberations and the threat of endocrine disruption evaluated further, as part of the risk assessment process. Pollution control and industrial decline has resulted in significant reductions in metals, PAHs and PCBs over the last 25 years and it is reasonable to assume that, individually, most contaminants are now below acute toxicity thresholds. However, pollutants may act in combination through subtle, sub-lethal effects and it is this aspect of the knowledge-base for the Severn Estuary which is particularly lacking. Generation of robust baseline information on the current ‘health’ of the system, including the use of relevant biomarkers and other sub-lethal indicators alongside statutory Water Framework Directive tools – as part of an integrated programme for assessing future changes in the biology and chemistry of the SAC – should be a priority. Monitoring the extent to which benthic communities are influenced by physical and chemical change should continue as an integral part of this scheme, building on established long-term surveys, such as those of BEL. The types of modifications to communities seen in the Severn Estuary as a result of anthropogenic pressures may have significant implications for the wider estuarine food web and key feedback processes including top-down and bottom-up predator–prey relationships. Invertebrates (i.e. H. diversicolor, oligochaetes, molluscs and crustacea) are important prey items whose consumption, along with incidental ingestion of sediment, are the most likely route of contaminant exposure for estuarine fish, sea birds and waders feeding on mud-flats of the Severn. The consequences of the altered geomorphology and tidal regime which might arise from large-scale tidal power proposals therefore encompass a number of plausible, if unquantified, risks – in terms of changing contaminant distributions, bioavailability and biological impact. These processes should be understood more comprehensively, even if tidal energy projects were not to reach fruition. The ecological and strategic importance of the Severn Estuary merits a better evaluation of its present condition, irrespective of major modifications, particularly in view of concerns regarding recent declines in numbers of SPA-qualifying birds using the estuary. Acknowledgements Thanks are due to Rachel Hudson for help with Environment Agency data. Thanks are also due to ICI and Terra Nitrogen UK for providing access to their environmental monitoring data for this publication. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.marpolbul.2009.12.014. References Allen, J.R.L., 1987. Microscopic coal-burning residues in the Severn Estuary, southwestern UK. Marine Pollution Bulletin 18, 13–18. Allen, Y.T., Hurrell, V., Reed, J., Matthiessen, P., 2000. Endocrine Disruptors and European Marine Sites in England. Centre for Environment Fisheries and Aquaculture Science (CEFAS). Contract C01042 for English Nature, p. 159.

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