Heavy metal contamination of brown seaweed and sediments from the UK

coastline between the Wear river and the Tees river

Lorenzo Giusti*

Department of Environmental Sciences, Faculty of Applied Sciences, University of the West of England, Frenchay Campus, Coldharbour Lane,

Bristol BS16 1QY

Received 1 December 1999; accepted 23 November 2000

Abstract

The concentration of Fe, Mn, Zn, Cu, Pb, Ni, Cr, Cd, and Ag were determined in the brown alga Fucus vesiculosus and intertidal surface

sediments from coastal locations of northeast England. Levels of heavy metals similar to those of polluted areas of the British coastline were

detected. There is evidence of contamination (especially with Zn and Pb) in sediments from sites affected by colliery spoil and from the Wear

estuary. The pelitic fraction ( < 63 mm) is usually more enriched in heavy metals, but it represents a very small percentage of the bulk samples.

The fine-grained sand is a very important repository of contaminants especially where particles of colliery spoil, secondary mineral, and

amorphous phases are present. Aqua regia-extracted Zn, Cu, and Pb in sediments are significantly correlated with those in seaweed. Despite

the closure of all base metal and coal mines, and the cessation of many industrial activities in the region, sediments and brown algae are

contaminated with heavy metals. The control site (Holy Island) and the Tees estuary appear to be the least affected. D 2001 Elsevier Science

Ltd. All rights reserved.

Keywords: Heavy metals; Seaweed; Sediment; Estuarine and coastal pollution

1. Introduction

For many centuries, the economic development of the

northeast of England has been strongly linked to base

metal mining in the Pennines and to coal mining in the

Durham and Northumberland Coalfields. Urbanised indus-

trial centres grew mainly around the estuaries of the Tyne

River, the Wear River, and the Tees River (Fig. 1). The

production of iron and steel, and shipbuilding, were

located on the Tyne and Wear estuaries, whereas the

petrochemical industry developed on the Tees mouth. All

coal mining, heavy metal mining, and shipbuilding activ-

ities have now ceased, and steel production has been

scaled down. As a result, there has been a significant

reduction in industrial discharges into the local estuaries

and coastal waters. Domestic sewage, previously dis-

charged untreated into the rivers, has been largely diverted

to treatment plants located on or near the coast.

With the exception of Holy Island, which consists of

sandstone intruded by a quartz±dolerite dyke, the coastline

sampled in this study is characterised by magnesian lime-

stone cliffs of Permian age overlain by Pleistocene glacial

deposits. The beaches are mostly composed of relatively

coarse material (boulders, cobbles, gravel, pebbles, and

sand). Natural clastic material eroded from the cliffs is mixed

with alluvium carried by the local rivers and drifted south-

ward by tidal currents. At sites such as Horden, Easington,

and Blackhall Rocks, millions of tonnes of coal waste were

dumped along the coast (Norton, 1985). In some cases, the

colliery spoil has been reworked into terraces where weath-

ering processes have produced clay minerals and iron oxide

coatings on sand particles (Humphries, 1996).

Large volumes (presently about 300,000 m3 day ÿ 1) of

minewater are still being pumped into the River Wear and its

tributaries in order to prevent groundwater rebound

(Younger, 1995). This is equivalent to about 15% of the

average Wear River flow. The alluvium of the main river

systems of this region has been contaminated by historic

mining, especially of minerals such as galena (PbS), spha-

lerite (ZnS), cerussite (PbCO3), smithsonite (ZnCO3), pyrite

(FeS2), fluorite (CaF2), and baryte (BaSO4; Dunham, 1934).

0160-4120/01/$ ± see front matter D 2001 Elsevier Science Ltd. All rights reserved.

PII: S0 1 6 0 - 4 1 2 0 ( 0 0 ) 0 0 11 7 - 3

Tel.: +44-117-344-2487; fax: +44-117-344-2904.

E-mail address: lorenzo.giusti@uwe.ac.uk (L. Giusti).

www.elsevier.com/locate/envint

Environment International 26 (2001) 275±286

The aim of this work was to find out whether changes in

economic development and recent cleanup measures have

produced an improvement in environmental conditions in

the marine environment. The main objective was an assess-

ment of the present heavy metal concentration in sediments

and in the brown alga Fucus vesiculosus. Signs of recovery

Fig. 1. Map of the northeast of England and sampling sites.

L. Giusti / Environment International 26 (2001) 275±286276

of macroalgal populations in the Tyne, Wear, and Tees

estuaries have recently been reported (Hardy et al., 1993).

Sediment samples have been traditionally used in sedi-

mentological and geochemical exploration studies, and over

the past few decades they have also been extensively

analysed to assess anthropogenic impacts in the aquatic

environment. Unpolluted marine and freshwater sediments

from many sites around the world generally contain less

than 50 mg kgÿ 1 Zn, up to 20 mg kgÿ 1 Cu, between 2

and 50 mg kgÿ 1 Pb, up to about 100 mg kgÿ 1 Ni, less

than 60 mg kgÿ 1 Cr, and less than 1 mg kgÿ 1 Cd (Moore

and Ramamoorthy, 1984; Bryan and Langston, 1992).

Typical background Ag concentration in surface sediments

is about 0.1 mg kgÿ 1 and in polluted estuaries this metal

normally ranges up to 5 mg kgÿ 1 (Luoma et al., 1995).

Unfortunately, the concentration of trace metals in sedi-

ments does not provide sufficient information on metal

availability to the biota living in it or in the overlying water

column. Nonetheless, trace metals present in the water

column are transferred to the sediments especially by

adsorption onto suspended material and deposited to the

seabed. Estuaries and coastal areas are thus the largest

repositories of contaminants. Detritus-feeding organisms

are directly exposed to sediment-bound metals. Many

workers have assessed environmental conditions and metal

bioavailability by means of biomonitors such as seaweed

and mussels.

Some of the lowest heavy metal concentrations (in mg

kgÿ 1 dry weight) found in F. vesiculosus were reported by

Riget et al. (1997) for the GodthaÊbs Fjord of west Green-

land, with particular reference to Zn (7.2±17.3 mg kgÿ 1),

Pb (0.3±0.4 mg kgÿ 1), and Fe (33±77 mg kgÿ 1). Other

elements reported in their study included Cr (0.6 mg kgÿ 1),

Cu (2.1±5.3 mg kgÿ 1), and Cd (0.5±3.9 mg kgÿ 1). These

values are quite low in comparison to those of F. vesiculosus

from other sites in North America and Europe not signifi-

cantly affected by local sources of metals. For example, up

to 400 mg kgÿ 1 Zn were found in the southern North Sea

(Dutton et al., 1973), and up to 514 mg kgÿ 1 Zn in the

Sannager Fjord of Norway (Pedersen, 1984). Iron is nor-

mally up to about 100±250 mg kgÿ 1 (Lunde, 1970; Preston

et al., 1972; Fuge and James, 1974; Phillips, 1979; SoÈder-

lund et al., 1988), but average Fe values of up to about 600

mg kgÿ 1 can be expected in the North Sea (Struck et al.,

1997); Pb is often more than 10 mg kgÿ 1, but it can be as

low as 0.1±0.2 mg kgÿ 1 in uncontaminated areas with low

Pb background values (Dutton et al., 1973; Stenner and

Nickless, 1975; Phillips, 1979). Cu is rarely found to be

more than about 50 mg kgÿ 1 (e.g. Preston et al., 1972;

Fuge and James, 1974; Forsberg et al., 1988). The few Cr

determinations reported in the literature for uncontaminated

locations are usually less than 1 mg kgÿ 1 (Forsberg et al.,

1988; Riget et al., 1997). Higher Cr levels (about 10 mg

kgÿ 1) were found by Jayasekera and Rossbach (1996) in F.

vesiculosus from the North Sea. British coastal areas in the

North Sea do not normally exceed 1 mg kgÿ 1 Ag, and most

of the reported values are in the range of 0.1±0.7 mg kgÿ 1.

Similar Ag values were given by Preston et al. (1972) for

coastal sites on the Atlantic side of the British Isles. The

latter study also gave a range of about 1±20 mg kgÿ 1 Ni

for selected locations around the British coastline, with a

geometric mean of about 6 mg kgÿ 1.

There is evidence of seasonal variations of trace metal

concentration in macroalgae (Bryan and Hummerstone,

1973; Fuge and James, 1973, 1974; Young, 1975), espe-

cially for Mn, Fe, Zn, Cu, Cd, Co, and Al. The general trend

appears to be an increase in concentration in the winter and

early spring, and minimum concentrations in the summer

and autumn.

Samples of mussels from Tees mouth and Holy Island

have been analysed during a survey of the UK coastline of

the North Sea (Widdows et al., 1995), but there is limited

published information on heavy metals in seaweed from the

stretch of coastline comprised between the Wear River and

the Tees River. Also, the author is not aware of any

published report on combined studies of local biomonitors

and sediments. This paper reports the trace metal concentra-

tions in the seaweed F. vesiculosus and in sediments from

coastal sites of northeast England. The data on seaweed are

also compared with information about the common mussel

Mytilus edulis obtained in a parallel investigation (Giusti et

al., 1999).

2. Materials and methods

2.1. Sampling methods

Seaweed samples were collected during the winter

1997±1998 from the upper to middle tidal area at 17 sites

(Fig. 1): Roker North Pier, Roker estuary, Easington,

Horden, Blackhall Rocks, Middleton, North Gare, five sites

at Bran Sands, and four sites at Holy Island. Holy Island

was chosen as a control location as the main activities on

this island are fishing and tourism, and because it is

situated off the coast of a rural part of Northumberland.

The beaches of Whitburn, Easington, Horden, and Black-

hall Rocks have been heavily impacted by coal waste

dumping until 1993, when mining activities ceased. Bran

Sands was chosen because it is located downstream of a

very industrialised area.

At each site, a composite sample of seaweed was

obtained by combining the most recent 8±10 cm of fronds

removed from 20±30 randomly chosen plants. Metal con-

centrations in F. vesiculosus have been reported to be

normally lower in the growing tips than in older stalky

growth (e.g. Bryan and Hummerstone, 1973; Forsberg et al.,

1988). If typical growth rates of 2±3 cm month ÿ 1 are

assumed (Knight and Parke, 1950), the samples collected in

this study would give an integrated concentration of heavy

metals for a time span of about 3±5 months. The seaweed

was cleaned in the field as much as possible with marine

L. Giusti / Environment International 26 (2001) 275±286 277

water, placed in polyethylene bags containing seawater from

the local environment, and taken to the laboratory after a

few hours.

Intertidal surface (top 5 cm) sediments were collected at

eight of the above sites, namely: Holy Island (Site 1), Roker

estuary, Easington, Horden, Blackhall Rocks, Middleton,

North Gare, and Bran Sands (Site 13). At each site, three

samples were taken within an area of about 10 m2. They

were removed with a polyethylene scoop and immediately

wet-sieved with marine water to separate the pelite ( < 63

mm) and the fine-grained sand (more than 63 mm to less than

180 mm). Large detritus was separated by sieving through 2-

mm sieves. The sediment fractions were transferred to

polyethylene bottles and carried to the laboratory together

with the bags of seaweed. Additional samples were sieved

to determine the sediment grain size distribution.

The pelitic fraction is usually the main scavenger of

heavy metals. However, heavy metals can be present in

more coarse-grained sediment fractions, especially in

regions heavily impacted by human activities. Microscopic

observations of our samples have shown that oxide coatings

and particles of coal and shale are often present in the fine-

grained sand. Also, as indicated in Table 1, fine-grained

sand represents about 35±49% by weight of each sample,

whereas the pelite is in the range of 0±6.5%.

2.2. Analytical methods

2.2.1. Seaweed

On arrival to the laboratory, the seaweed was briefly

washed with deionised water, dried at 105°C for 48 h,

cooled, weighed, and ashed at 475°C in a muffle furnace

for 24 h (Fuge and James, 1973). From each sample, three

5-g aliquots of the ashed material were kept in 50-ml glass

beakers with 20 ml aqua regia (5 ml of 16 M HNO3 and 15

ml of 16 M HCl) for 48 h. They were later refluxed on a hot

plate, and diluted to 50 ml with deionised water.

2.2.2. Sediment

Sediments were dried in the oven at 105°C for 48 h.

Three aliquots of 1 g of each dry sediment fraction were

separated. The sediment aliquots were prepared for diges-

tion by grinding them to a fine powder with an agate mortar

and pestle, and ashed at 475°C in a muffle furnace for 2 h.

This step allowed the determination of the organic content

Table 2

Average recovery of metals in Standard Reference Material NIES No. 9 Sargasso seaweed

Element

NIES 9

(certified value) This study

Recovery

(%) n

Fe 187 � 6 172 � 4 92.0 6

Mn 21.2 � 1.0 20.4 � 0.5 96.2 6

Zn 15.6 � 1.2 13.1 � 0.7 84.0 6

Cr 0.2a 0.27 � 0.06 6

Cu 4.9 � 0.2 4.8 � 0.2 98.0 6

Pb 1.35 � 0.05 1.40 � 0.04 103.7 6

Ni b

Cd 0.15 � 0.02 0.17 � 0.02 113.3 6

Ag 0.31 � 0.02 0.33 � 0.05 106.5 6

Concentrations are quoted as mg/g dry weight.

n = number of replicates.a Reference value (not certified).b No reference or certified value reported.

Table 1

Grain size distribution (in wt.%) of sediment from coastal sites of northeast England

Site

% gravel

( > 2 mm)

% coarse/

medium sand

( < 2 mm, > 180 mm)

% fine sand

( < 180 mm, > 63 mm)

% pelite

( < 63 mm)

Holy Island 1.4 55.0 38.2 5.4

Whitburn 2.0 60.3 34.8 2.9

Roker (North Peer) 5.9 52.0 40.1 2.0

Roker (estuary) 4.6 40.4 48.5 6.5

Easington 23.2 38.2 38.6 0

Horden 15.7 35.0 49.3 0

Blackhall Rocks 5.4 50.0 42.6 2.0

Middleton 1.7 51.8 40.8 5.7

North Gare 2.2 51.9 41.5 4.4

Bran Sands 4.1 55.7 37.2 3.0

L. Giusti / Environment International 26 (2001) 275±286278

as percentage loss on ignition (% LOI). The aqua regia

digestion method was used on 0.500 � 0.002 g of the ashed

aliquots. Aqua regia digestion of sediments extracts only a

fraction of the major elements because silicates are not

completely dissolved with this method. However, most

heavy metals not bound to silicates are efficiently dissolved

(Ure, 1990). The method of standard addition was used to

correct for matrix effects. Salt matrix effects for Ag, Cd, Ni,

Pb, and Cu were overcome by using matrix modifiers.

All digest solutions were analysed, at least in duplicate,

by flame atomic absorption spectrophotometry (Varian

SpectrAA-10Plus) and by graphite furnace atomic absorp-

tion spectrophotometry (Varian SpectrAA-300 with GTA96

graphite tube atomiser). Metals analysed included Fe, Mn,

Zn, Cu, Pb, Ni, Cr, Cd, and Ag.

2.3. Quality control

The precision and recovery of the procedures were

checked using the following certified standard reference

materials: NIES No. 9 Sargasso seaweed, GBW07302

stream sediment, GBW07313 marine sediment, and

SRM2711 Montana soil. Blanks were run with each batch

of samples. All reagents were ultrapure and glassware/

plasticware/filters cleaned according to the method of Laxen

and Harrison (1981). Blank values were negligible in

comparison to the sample concentrations.

A comparison between certified values of Sargasso sea-

weed and those found in this study (Table 2) indicates that Fe,

Mn, Zn, and Cu concentrations in our samples may have been

underestimated by about 8%, 4%, 16%, and 2%, respectively,

whereas Pb, Cd, and Ag may have been overestimated by

about 4%, 13%, and 7%, respectively. No correction was

applied to our data. Replicate analyses gave coefficients of

variation of less than 5% for all elements except Cr, Cd, and

Ag for which variations were up to 11%. The seaweed fronds

from each location were manually mixed, and the resulting

composite sample was separated into three subsamples before

ashing took place. The standard deviations listed in Table 4

refer to these three subsamples. Therefore, the values of

standard deviation are a combination of analytical error and

of the natural variability in metal concentration at a specific

Table 4

Concentration of metals (mg kgÿ 1 dry weight) and percentage ash (at 450°C) of F. vesiculosus

No SITE Fe Mn Zn Cu Pb Ni Cr Cd Ag

%

ash

1 Holy Island 65.0 � 4.1 276.2 � 21.6 14.9 � 1.1 5.7 � 1.2 0.1 0.3 � 0.1 0.8 � 0.1 0.28 � 0.06 1.1 � 0.4 20

2 Holy Island 94.7 � 6.2 479.4 � 32.0 17.7 � 2.4 5.6 � 0.8 0.3 0.4 1.1 � 0.1 0.45 � 0.05 1.0 � 0.1 21

3 Holy Island 273.0 � 12.0 353.9 � 24.3 12.9 � 0.8 4.8 � 2.0 0.6 � 0.1 0.4 1.2 � 0.2 0.33 � 0.12 0.9 � 0.2 22

4 Holy Island 616.1 � 8.6 778.4 � 38.8 16.9 � 2.0 9.4 � 1.3 1.1 � 0.1 0.7 � 0.2 1.8 � 0.3 0.22 � 0.07 1.4 � 0.5 23

5 Whitburn 636.5 � 14.5 490.6 � 22.0 560.2 � 17.4 29.6 � 4.6 3.6 � 0.4 3.0 � 0.4 5.0 � 0.6 2.53 � 0.18 2.6 � 1.3 20

6 Roker 300.3 � 16.6 360.0 � 36.1 511.4 � 25.3 23.3 � 2.2 5.9 � 0.4 20.2 � 1.9 3.0 � 0.4 2.41 � 0.31 1.6 � 0.4 22

7 Roker 490.6 � 41.2 176.0 � 12.6 740.0 � 20.7 30.7 � 1.3 7.8 � 2.5 30.6 � 2.4 3.6 � 1.1 2.02 � 0.81 1.8 � 0.8 22

8 Easington 1208.9 � 98.2 80.6 � 4.2 1015.5 � 54.4 50.6 � 10.6 12.1 � 4.0 36.0 � 5.1 3.8 � 2.3 10.03 � 4.12 4.2 � 0.6 20

9 Horden 920.1 � 51.3 105.4 � 18.6 904.8 � 33.3 35.9 � 6.8 8.4 � 4.1 70.5 � 8.9 3.5 � 2.2 9.18 � 2.06 3.8 � 1.5 20

10 Blackhall Rock 815.1 � 64.6 107.9 � 15.3 140.3 � 16.7 20.2 � 4.8 5.7 � 3.2 32.1 � 3.2 2.6 � 0.4 2.16 � 1.14 3.0 � 1.4 21

11 Middleton 1027.0 � 81.2 83.0 � 9.9 45.4 � 2.2 9.7 � 4.7 0.6 � 0.2 0.4 � 0.1 1.1 � 0.2 0.14 � 0.05 1.8 � 0.3 28

12 North Gare 80.4 � 3.8 31.6 � 3.9 23.6 � 2.6 8.4 � 2.5 4.9 � 0.8 0.7 � 0.1 2.1 � 0.2 0.21 � 0.03 1.2 � 0.4 23

13 Bran Sands 658.8 � 28.9 136.2 � 14.4 62.9 � 3.1 15.8 � 2.4 3.2 � 1.0 2.9 � 0.3 2.4 � 0.2 0.06 � 0.01 1.3 � 0.9 22

14 Bran Sands 123.2 � 16.2 118.1 � 9.1 46.8 � 5.8 12.3 � 1.1 1.1 � 0.5 2.1 � 0.1 1.2 0.04 � 0.01 1.1 � 0.1 28

15 Bran Sands 130.9 � 9.1 93.5 � 6.1 42.1 � 6.8 10.0 � 0.7 2.0 � 0.7 1.6 1.2 � 0.1 0.04 � 0.01 1.3 � 0.2 26

16 Bran Sands 95.6 � 8.1 55.2 � 3.0 36.2 � 2.3 13.9 � 1.2 0.7 � 0.1 1.5 1.0 � 0.1 0.03 1.1 � 0.1 26

17 Bran Sands 67.5 � 6.1 18.8 � 2.2 41.8 � 4.9 10.2 � 0.8 0.5 � 0.1 0.6 � 0.1 0.9 � 0.2 0.02 0.9 � 0.2 29

Table 3

Average recovery of metals in standard reference sediments GBW07302 (stream sediment), GBW07313 (marine sediment), and SRM2711 (Montana soil)

Element

GBW07302

(certified value) This study

Recovery

(%)

GBW07313

(certified value) This study

Recovery

(%)

SRM2711

(certified value) This study

Recovery

(%) n

% Fe a 1.29 � 0.02 a 3.82 � 0.02 2.89 � 0.06 2.94 � 0.16 101.7 8

Mn 240 210 � 0.01 87.5 a 638 � 28 580 � 11 90.9 8

Zn 44 41.3 � 2.6 93.9 160 120 � 13 75.0 350.4 � 4.8 351.0 � 0.2 100.2 8

Cr 12.2 13.7 � 2.1 112.3 58.4 46.2 � 5.3 79.1 a 8

Cu 4.9 5.3 � 0.3 108.2 424 367 � 12 86.6 114 � 2 132 � 3.2 115.8 8

Pb 32 30.9 � 3.1 96.6 29.3 30.9 � 3.2 105.5 1162 � 31 1149 � 15 98.9 8

Ni 5.5 4.3 � 0.3 78.2 150 140 + 2 93.3 20.6 � 1.1 14.7 � 3.3 71.4 8

Cd 0.065 0.021 � 0.011 32.3 a 41.70 � 0.25 45.60 � 2.40 109.4 8

Ag 0.066 0.052 � 0.012 78.8 a 4.63 � 0.39 3.15 � 0.78 68.0 8

Concentrations are quoted as mg kgÿ 1, with the exception of Fe for which a percentage value is given.

n = number of replicates.a No certified value reported.

L. Giusti / Environment International 26 (2001) 275±286 279

geographical location. For the most abundant elements (Fe,

Mn, Zn) the coefficients of variation were up to 18% and

usually less than 10%, whereas larger coefficients (up to 40±

67%) were typical of less abundant trace elements.

The recovery of metals in standard reference sediments by

the aqua regia digestion method was normally in the range of

78±116% of the certified total concentrations (Table 3). The

most notable exception was that of Cd as only 32% was found

for GBW07302. However, the Cd recovery in SRM2711 was

109.4%. This points to some problems in the detection of the

low Cd levels present in the former standard and explains the

poor Cd detection in some of our samples.

3. Results and discussion

3.1. Seaweed

The most abundant elements found in the seaweed

material analysed are Fe, Mn, Zn, and Cu, and the least

Table 5

Concentration of metals (in mg kgÿ 1 dry weight, except for Fe, which is expressed as percent) and % LOI in sediments

No Site and size fraction Fe Mn Zn Cu Pb Ni Cr Cd Ag % LOI

1 Holy Island

< 180 mm 1.04 � 0.13 172 � 30 40.7 � 9.7 34 � 7 10 � 3 15 � 2 18 � 4 nd 13.3 � 1.9 1.06 � 0.19

< 63 mm 1.26 � 0.16 207 � 40 11.3 � 2.0 12 � 3 20 � 2 23 � 3 15 � 2 nd 16.9 � 1.8 0.49 � 0.03

7 Roker

< 180 mm 3.14 � 0.86 1787 � 259 527 � 75 54 � 22 653 � 58 40 � 5 58 � 15 3.1 � 0.6 6.6 � 0.6 0.76 � 0.07

< 63 mm 4.46 � 0.30 2597 � 258 1284 � 272 110 � 30 1137 � 197 75 � 9 87 � 12 5.3 � 0.9 7.5 � 0.9 0.92 � 0.03

8 Easington

< 180 mm 3.36 � 1.79 578 � 203 2230 � 496 230 � 57 643 � 133 61 � 16 13 � 2 11.2 � 2.9 5.6 � 1.3 2.53 � 0.40

9 Horden

< 180 mm 4.47 � 2.02 625 � 192 1962 � 279 172 � 75 880 � 272 77 � 22 16 � 3 6.1 � 3.5 3.8 � 0.7 1.17 � 0.22

10 Blackhall Rock

< 180 mm 4.25 � 0.47 993 � 117 496 � 155 209 � 60 414 � 69 51 � 6 20 � 5 2.2 � 0.82. 4.7 � 1.1 2.38 � 1.11

< 63 mm 3.08 � 0.41 1209 � 256 560 � 111 113 � 27 628 � 79 66 � 10 43 � 9 3 � 0.4 4.2 � 1.4 1.48 � 0.13

11 Middleton

< 180 mm 2.78 � 0.66 879 � 151 327 � 76 25 � 9 226 � 55 60 � 19 35 � 5 2.2 � 0.4 4.8 � 0.9 0.53 � 0.03

< 63 mm 4.30 � 0.74 1271 � 195 301 � 97 161 � 28 286 � 60 105 � 20 52 � 10 2.8 � 0.9 7.5 � 1.6 0.59 � 0.08

12 North Gare

< 180 mm 1.10 � 0.27 317 � 45 52 � 10 9 � 2 25 � 4 12 � 4 10 � 2 nd 4.0 � 1.1 0.43 � 0.02

< 63 mm 1.56 � 0.56 393 � 80 151 � 35 141 � 20 47 � 6 19 � 7 18 � 3 nd 4.9 � 1.8 1.68 � 0.21

13 Bran Sands

< 180 mm 1.77 � 0.21 394 � 44 116 � 49 28 � 9 41 � 4 14 � 3 12 � 2 nd 15.0 � 2.7 0.59 � 0.08

< 63 mm 3.24 � 0.45 1126 � 141 113 � 68 99 � 11 156 � 13 27 � 4 35 � 5 nd 19.3 � 5.7 1.07 � 0.09

Tyne estuarya ( < 100 mm) 2.82 395 421 92 187 34 46 2.17 1.55

Continental crustb 4.32 716 65 25 14.8 56 126 0.01 0.07

Guideline valuesc 150± 410 34± 270 46.7±218 20.9± 51.6 81± 370 1.2± 9.6 1.0±3.7

nd = not detected.a Bryan and Langston, 1992 (HNO3 digestion).b Wedepohl, 1995 (HNO3/H2O2 digestion).c Long et al., 1995.

Fig. 2. Relationship between the concentration of (a) Pb and Cu, and (b) Zn and Cu in F. vesiculosus. For n = 17 at P < .01, the critical r is .606. The error bars

combine analytical error and natural variations of sample concentration at each site.

L. Giusti / Environment International 26 (2001) 275±286280

abundant are usually Cd and Ag (Table 4). However, Cd and

Ag appear quite concentrated in samples from Easington

and Horden (about 9±10 and 4 mg kgÿ 1, respectively), and

Ni (about 20±70 mg kgÿ 1) in samples from Roker and

Blackhall Rocks. The concentration sequence of the most

abundant elements is usually Fe > Mn > Zn > Cu. However,

at Holy Island, Mn > Fe, and at Whitburn, Roker, Easington,

Blackhall Rock, and one site at Bran Sands (No. 17),

Zn > Mn. The highest Mn enrichment in seaweed is at Holy

Island (276±778 mg kgÿ 1), which is also characterised by

the lowest concentrations of Zn (13±18 mg kgÿ 1), Pb

(0.1±1.1 mg kgÿ 1), and Ni (0.3±0.7 mg kgÿ 1). At Bran

Sands, Fe and Mn enrichment in seaweed decreases sig-

nificantly from Sites 13 to 17, going downstream along the

southern part of the Tees estuary. There is also an apparent

parallel decrease in all other trace metals, though this is not

statistically significant.

A significant correlation ( P < .001) exists between Fe

and Ag (r =.826), Zn and Cu (r =.957), Zn and Pb (r =.887),

Zn and Cr (r =.830), Zn and Ag (r =.822), Cu and Pb

(r =.910), Cu and Cr (r =.839), Cu and Ag (r =.881), and Pb

and Cr (r =.780). No element was correlated with Mn or

with ash content. Fig. 2a,b illustrates examples of these

statistical relationships.

The possibility that seaweeds may have been contami-

nated with metals scavenged by iron oxyhydroxides present

in fine sediment particles was considered and tested in two

ways: (1) assuming that all the iron in the seaweed samples

originated from sediment contamination, and (2) comparing

metal/Fe ratios in sediment and seaweed. Potential contam-

ination from sediment particles appears theoretically possi-

ble only for Pb.

3.2. Sediment

Observations of sediment samples with a binocular

microscope revealed that the sediments were largely com-

posed of quartz, carbonates, and feldspars, some coated by

oxides, and mixed with shell debris. Opaque minerals

(mostly pyrite) were present. Coal particles were also

common in all sediments. Very small grains could not be

identified. The fine sand fraction of surface sediments was

available from eight of the sites investigated, whereas the

pelitic fraction was available in sufficient amount only at six

of the sites sampled: At Easington and Horden, only sand

and gravel were present in the sediment (Table 1).

The concentrations (mean � S.D.) of heavy metals in

sediments are given in Table 5. Iron is the most abundant

(about 1±4.5 wt.%) of the metals analysed, and, exception

made for Blackhall Rocks, it is more enriched in the pelitic

fraction. Manganese is always the most abundant of the

trace metals in the pelite, with mean values ranging from

207 mg kgÿ 1 at Holy Island to 2597 mg kgÿ 1 at Roker. In

most cases, the least abundant elements are Ag and Cd.

For comparative purposes, Table 5 lists also the heavy

metal concentrations in sediments of the Tyne estuary (Bryan

and Langston, 1992) and in the continental crust (Wedepohl,

1995). Unfortunately, data sets cannot be readily compared

as different digestion methods were used on different sedi-

ment fractions. More meaningful estimates of sediment

contamination can be made with reference to background

values from the same area investigated. Rowlatt and Lovell

(1994) reported median values of Pb (11 mg kgÿ 1), Zn (15

mg kg ÿ 1), and Cr (18 mg kg ÿ 1) for < 2-mm seabed

sediments analysed in the Joint Monitoring Group Sediment

Baseline study. They studied the shelf region of the North

Atlantic and its marginal areas, including the North Sea. Pb,

Zn, and Cr background values from a sediment core taken 16

km off the Tyne estuary were 12, 38, and 45 mg kgÿ 1,

respectively (Rowlatt and Lovell, 1994). In general, these

authors found that the seabed sediments of Tyneside and

Teesside were above these background values. Even though

a direct comparison with our data cannot be made due to the

different size range of the sediment fraction analysed, these

values can be referred to as baseline concentrations.

The sediment quality guideline values proposed by Long

et al. (1995) are also listed in Table 5, as they can be used to

estimate the probability that adverse effects to the local biota

may occur. These effects are possible within the concentra-

tion range indicated, and frequently observed at higher

concentrations. These values refer to bulk sediments

digested with strong reagents and cannot be compared with

Table 7

Correlation coefficient matrix for heavy metals in aqua regia-digested

sediments ( < 63 mm fraction)

Fe Mn Zn Cu Pb Ni Cr Cd Ag % LOI

Fe .864 .666 .515 .689 .813 .784 .716 ÿ .152 .184

Mn .916 .322 .921 .612 .926 .910 ÿ .228 ÿ .084

Zn .232 .982 .516 .856 .801 ÿ .395 .045

Cu .212 .491 .253 ÿ .110 ÿ .545 .395

Pb .549 .868 .762 ÿ .386 .032

Ni .685 .000 ÿ .400 ÿ .300

Cr .740 ÿ .332 ÿ .173

Cd .460 ÿ .268

Ag ÿ .472

% LOI

Critical r = .468 at P < .05, or r = .590 at P < .01 (n = 18).

Table 6

Correlation coefficient matrix for heavy metals in aqua regia-digested

sediments ( < 180 mm fraction)

Fe Mn Zn Cu Pb Ni Cr Cd Ag % LOI

Fe .538 .649 .761 .833 .871 .247 .358 ÿ .425 .539

Mn .089 .141 .548 .401 .881 ÿ .370 ÿ .329 .055

Zn .793 .826 .761 ÿ .134 .900 ÿ .394 .579

Cu .716 .706 ÿ .205 .651 ÿ .369 .901

Pb .829 .308 .581 ÿ .510 .453

Ni .207 .469 ÿ .567 .468

Cr ÿ .430 ÿ .145 ÿ .228

Cd .134 .000

Ag ÿ .228

% LOI

Critical r = .404 at P < .05, or r = .515 at P < .01 (n = 24).

L. Giusti / Environment International 26 (2001) 275±286 281

our data listed in Table 5. However, it is possible to calculate

minimum bulk metal concentration, taking into account the

percentage of fine-grained sand and pelite, and assuming no

metal contribution from gravel and coarse/medium sand.

This means a dilution effect of about 50±60%. The recal-

culated sediment levels of Zn, Pb, Ni, Cd, and Ag for Roker,

Easington, Horden, Blackhall Rocks, and Middleton are

either within or higher than the guideline values of Long

et al. (1995).

In our study, the surface sediment at control Site 1

(Holy Island) has lower or similar Pb, Zn, and Cr con-

centrations than the background values of Rowatt and

Lovell (1994). Background Cr is exceeded only at Roker

and Middleton. All other sites show Zn and Pb contamina-

tion. Iron is significantly ( P < .01) correlated with many

elements in the fine-grained sand, including Mn, Zn, Cu,

Pb, and Ni, and with Mn, Zn, Pb, Ni, Cr, and Cd in the

pelitic fraction (Tables 6 and 7). Some of the deviations

from a linear trend are due to metal enrichment of sedi-

ments at some of the sites investigated. More specifically,

Pb contamination in the pelitic and sand fractions can be

inferred for Roker, Easington, Horden, and only for the

pelitic fraction at Blackhall Rocks. Both fractions are

enriched in Ag at Holy Island and Bran Sands. Examples

of scatter plots of Fe concentration (expressed as percent)

vs. the concentration of other metals (in mg kgÿ 1) are

shown in Fig. 3. The scatter found for the fine-grained

sand fraction is usually due to high metal values (espe-

cially Zn, Pb, and Cd) at Easington and Horden. Similar

trends were observed when these metals are plotted against

Mn (Fig. 4). Zinc enrichment at Easington and Horden is

also shown by the trends in the Zn vs. Pb and Zn vs. Cr

scatter diagrams (Figs. 5 and 6, respectively). If the

samples from Horden and Easington are excluded from

the correlation calculations, a highly significant ( P < .001)

correlation would be observed between Fe and Zn

(r =.872), Mn and Zn (r =.874), Mn and Pb (r =.968),

and Mn and Cd (r =.714) in the sand fraction. Silver is

negatively correlated to all elements except Cd. This may

be partially due to the similar speciation of these two

metals in aquatic environments.

The organic matter content (as % LOI) in sediments is

generally in the range 0.4±3.6%. The relatively higher

percentage found at Easington, Horden, North Gare, and

Fig. 4. Scatter plot of (a) Mn vs. Pb and (b) Mn vs. Zn concentration in sediment fractions (pelite and fine sand) from the coast of northeast England.

Fig. 3. Scatter plot of (a) Fe vs. Pb and (b) Fe vs. Zn concentration in sediment fractions (pelite and fine sand) from the coast of northeast England.

L. Giusti / Environment International 26 (2001) 275±286282

especially at Blackhall Rocks are partly due to the presence

of small particles of coal, especially in the sand fraction.

Copper shows the highest positive correlation with %

LOI (r =.901, P < .01) in the fine-grained sand (Fig. 7 and

Tables 6 and 7). The strong affinity of Cu for organic

material in sediments is quite well known (e.g. Luoma

and Bryan, 1981; Davies-Colley et al., 1984; Borg and

Jonsson, 1996), although other phases such as Fe±Mn

oxides and hydroxides can also be good Cu scavengers.

Other metals positively correlated with organic matter in the

sand fraction are Fe, Zn (both at P < .01), Pb, and Ni (both at

P < .05).

3.3. Comparison between heavy metal concentrations in

sediments and marine organisms

The aqua regia-extracted Zn, Cu, and Pb in sediments

are positively correlated ( P < .05) with those of F. vesicu-

losus, as shown for example in Fig. 8 for Zn. A sig-

nificant correlation ( P < .05) was also found for Ni

extracted from the sand fraction. These relationships

indicate that some of the metals held in the sediment

may become available to the seaweeds. This may occur,

for example, when Fe and/or Mn are remobilised (together

with the scavenged trace metals) from anoxic sediments

back into the water column. The biodegradation of organic

material will also cause a release of heavy metals to

marine water. Even though Ag is widely distributed in

all sediments, and especially those of Holy Island and

Bran Sands, this metal is more accumulated in F. vesicu-

losus at sites affected by mining activity.

Metal concentrations in surface sediments (Table 5) and

in the soft tissue of the mussel M. edulis (Giusti et al., 1999)

appear to be generally unrelated. It is possible that although

Fe oxides/hydroxides and organic matter can bind high

Fig. 7. Relationship between Cu concentration and organic matter content

(as % LOI) in marine sediments from the northeast coast of England. The

regression line and the correlation factor (r =.901) refer to the sand fraction

(full circles). The empty circles represent the pelitic fraction.

Fig. 8. Relationship between Zn concentrations in F. vesiculosus and Zn in

aqua regia extracts of sediment fractions from the same sites in northeast

England (n = 14, P < .05).

Fig. 6. Plot of Zn vs. Cr concentration in sediments from the coast of

northeast England, showing the Zn enrichment of sand samples from

Easington and Horden.

Fig. 5. Plot of Zn vs. Pb concentration in sediment fractions from the coast

of northeast England. The pelite is represented by empty circles, the fine

sand by full circles. The regression line and the correlation factor (r =.965)

refer to the pelitic fraction only (n = 18). For n = 18, at P < .01, the critical r

is .590.

L. Giusti / Environment International 26 (2001) 275±286 283

concentrations of trace metals, they also cause a reduction in

trace metal bioavailability in the digestive tract of mussels

(Luoma and Bryan, 1978; Langston, 1980). This is more

likely to result in a correlation of heavy metals in mussels

with the ratio metal/Fe in sediment. In our study, we found a

significant positive correlation (at P < .01) between Pb in

mussels and the Pb/Fe ratio in the aqua regia extracts of

surface sediments.

3.4. Metal pollution index (MPI)

The overall metal burden of F. vesiculosus was compared

with the total aqua regia-extracted metal content in sedi-

ments, using the MPI calculated with the formula (Usero et

al., 1996, 1997):

MPI � �M1 �M2 �M3 � . . .�Mn�1=n

where Mn is the concentration of metal n expressed in mg

kgÿ 1 of dry weight.

Lower MPI in algal material is to be expected, as

accumulated heavy metals derive only from dissolved

species present in marine water. Sediments are normally

larger repositories of contaminants. However, the variations

in algal MPI between sites appear to be similar, though of a

different order of magnitude, to the variations of sediment

(fine sand) MPI. Fig. 9 shows that the two sets of MPI are

significantly correlated (r =.959, n = 8). The correlation

between pelite MPI and algal MPI (n = 6) is not significant.

Both monitoring methods (i.e. with sediment and with

algae) have thus proved to be quite effective in highlighting

metal concentration gradients.

3.5. Comparison between heavy metal concentrations in

seaweeds and mussels

Along the coastline studied, the concentration of Cu, Zn,

Pb, Cd, and Ag in seaweed is usually lower than in soft

tissue of mussels (Giusti et al., 1999) from the same sites.

Only at Roker was the Zn accumulated by F. vesiculosus

higher than in M. edulis. Nickel is more abundant in

seaweeds than in mussels from Holy Island, Roker, and

Blackhall Rocks, and Cr levels are higher in seaweeds at

Holy Island and Middleton.

Our seaweed samples showed a more pronounced accu-

mulation of Mn than the mussels from the same sites (Giusti

et al., 1999). This appears to be quite commonly observed

elsewhere. For example, the average North Sea and Baltic

Sea Mn concentration in F. vesiculosus is 356 and 748 mg

kg ÿ 1 dry weight, respectively, which is one order of

magnitude higher than in mussels from the same areas, i.e.

29.7 and 47.2 mg kgÿ 1, respectively (Struck et al., 1997).

High levels of Mn or Zn in water are known to suppress

the accumulation of trace amounts of dissolved Cd, Co, Ni,

Zn, or Mn in seaweed as a result of competition for

available binding sites (Bryan et al., 1985). It is thus

possible that the low Zn, Ni, and Cd values in seaweeds

at Holy Island might be caused by the high accumulation of

Mn. Also, the general lack of a significant correlation

between Mn and any of the other metals analysed in

seaweed may be partially due to the same reason. In our

study, the significant positive correlation between Zn and

Cu in seaweed rules out large competition effects between

these two metals.

4. Conclusions

Given the seasonal and short-term variability of estuar-

ine and coastal environments, large variations in dis-

solved and particulate metal concentrations should be

expected, thus making the interpretation of heavy metal

distribution gradients quite problematic. Nonetheless,

some conclusions can be drawn based on the combina-

tion of information obtained from seaweed, sediment, and

previously published data on heavy metals in mussels

from the same sites.

(i) Seaweeds from Whitburn, Roker, Easington, and

Horden, have a relatively high burden of Zn (511±1016

mg kgÿ 1), Cu (23±51 mg kgÿ 1), Cr (3.0±5.0 mg kgÿ 1),

and, at the latter three sites, of Ni (20±71 mg kgÿ 1) and Pb

(6±12 mg kgÿ 1). Also, Cd (6±10 mg kgÿ 1) and Ag (4 mg

kgÿ 1) are high at Easington and Horden. In general, these

Cd and Ag levels are comparable to those of contaminated

estuarine and coastal sites around the UK. Seaweed at Holy

Island and Bran Sands appears to be the least enriched in

trace metals.

(ii) Concentrations of Pb, Zn, Cu, Cd, and Ag in F.

vesiculosus are usually lower than in M. edulis from the

same area, whereas Mn is normally an order of magnitude

higher in seaweed.

(iii) The fact that aqua regia-extracted Zn, Cu, and Pb in

sediments are positively correlated with the concentrations

of these metals in seaweed, but not to those in mussels,

suggests that metal uptake from ingested sediment is less

important than ingestion of dissolved metal species. This

conclusion can also be inferred on the basis of theFig. 9. Scatterplot of correlation between MPI of fine-grained sand and MPI

of F. vesiculosus.

L. Giusti / Environment International 26 (2001) 275±286284

significant correlation between MPI in sediment and MPI

in algae.

(iv) Sediments from Roker, Easington, Horden, Blackhall

Rocks, and Middleton have concentrations of Zn, Pb, Ni,

Cd, and Ag likely to cause adverse biological effects.

(v) The pelitic fraction is usually more enriched in heavy

metals, but it represents a very small portion of the sediment

samples (0±6.5% by weight). The fine-grained sand is also

a very important repository of contaminants, especially

when mixed with particles of colliery spoil and secondary

mineral and amorphous phases. Therefore, the normalisation

of bulk sediment composition based on the percentage of

pelite is not applicable to sediments of the area studied. This

is likely to be the case at other sites contaminated with waste

from mining activity or where secondary accumulation of

Fe and Mn compounds are common. Coatings of oxides,

hydroxide, or of organic matter can increase significantly

the concentration of heavy metals of particles larger than 63

mm. In this study, a stronger affinity of most metals for Fe

was found in the fine-grained sand fraction and for Mn in

the pelitic fraction. In both fractions, Cr is more strongly

correlated with Mn. The negative correlation between Ag

and Fe and between Ag and Mn reflects the affinity of silver

for organic fractions such as humic acids, and its tendency

to form chlorocomplexes in marine water.

(vi) Despite the closure of all base metal mines and coal

mines in the region studied, sediments are still contaminated

with heavy metals. The heavy metal burden of seaweed (and

mussels) at the sites investigated is similar to those of other

polluted areas of the British coastline. Silver enrichment in

seaweed is more pronounced at sites affected by past mining

activities, whereas the highest Ag concentrations in sedi-

ments were found at Holy Island and Bran Sands. It is

difficult at this stage to point to specific sources of Ag at

these two sites, but sewage is a likely source.

(vii) Our monitoring took place over a short period of

time and although seaweed samples give information relat-

ing to a number of months before sampling, further work is

necessary before firm conclusions can be drawn on the

apparent reduction of anthropogenic impact on the marine

environment at Teesside. As sedimentation rates can vary

considerably over the year, and dredging is routinely carried

out in the Wear and Tees estuaries, more systematic sam-

pling is necessary to confirm our preliminary conclusions.

One of the limitations of environmental impact studies

based on the analysis of tissue of biomonitors is the fact

that a significant proportion of the dissolved metals present

in surface water may be present as nonbioavailable organic

complexes, especially in estuarine areas and near industrial

and sewage outfalls. Iron is the only metal which is known

to become increasingly available to phytoplankton when

chelating agents such as ethylenediaminetetraacetate

(EDTA) are present (Luoma, 1983). If complexation with

strong organic ligands takes place, the metal burden found

in seaweed may not be proportional to the dissolved fraction

of metals in seawater. Other information such as salinity,

pH, concentration of humic and fulvic acids, and concentra-

tion of synthetic chelating agents is required to be able to

interpret more precisely any data of metal uptake from

solution by aquatic organisms.

Acknowledgments

The author is indebted to Arun Mistry and Peta Carter for

their technical support.

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