Marine Pollution Bulletin xxx (2008) xxx–xxx

ARTICLE IN PRESS

Contents lists available at ScienceDirect

Marine Pollution Bulletin

journal homepage: www.elsevier .com/ locate /marpolbul

The sandhopper Talitrus saltator (Crustacea: Amphipoda) as a biomonitorof trace metal bioavailabilities in European coastal waters

W. Fialkowski a,*, P. Calosi b, S. Dahlke c, A. Dietrich d, P.G. Moore e, S. Olenin f, L.E. Persson g,B.D. Smith h, M. Špegys f, P.S. Rainbow h

a Jagiellonian University, Institute of Environmental Sciences, Aquatic Biology Group, ul. Gronostajowa 7, 30-387 Krakow, Polandb Marine Biology and Ecology Research Centre, School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, Devon, UKc Ernst-Moritz-Arndt-Universität Greifswald, Institut für Ökologie, Schwedenhagen 6, 18565 Kloster/Hiddensee, Germanyd Department of Hydrobiology and Ichthyopathology, Faculty of Bioresources and Nature Use, Kaliningrad State Technical University, Sovetsky prospekt, 1, 236000 Kaliningrad, Russiae University Marine Biological Station Millport, Isle of Cumbrae, Scotland KA28 0EG, UKf Coastal Research and Planning Institute, Klaipeda University, H. Manto 84, 92294, Klaipeda, Lithuaniag Department of Biology and Environmental Science, University of Kalmar, Barlastgatan 11, SE-391 82 Kalmar, Swedenh Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK

a r t i c l e i n f o

Keywords:TalitrusBiomonitoringMetal bioavailabilityBaltic SeaIrish SeaMediterranean

0025-326X/$ - see front matter � 2008 Elsevier Ltd. Adoi:10.1016/j.marpolbul.2008.09.013

* Corresponding author. Tel.: +48 12 664 5182; faxE-mail addresses: wojciech.fialkowski@uj.edu.pl

@plymouth.ac.uk (P. Calosi), sven.dahlke@uni-greifswmova@mail.ru (A. Dietrich), pmoore@udcf.gla.ac.uk (POlenin), Lars-eric.Persson@hik.se (L.E. Persson), p.raibow).

Please cite this article in press as: FialkowPollut. Bull. (2008), doi:10.1016/j.marpolb

a b s t r a c t

The amphipod crustacean Talitrus saltator is an established, easily accessible, biomonitor of trace metalbioavailabilities in coastal waters. We have carried out a geographically widespread collection of T. sal-tator from European shores, stretching from the north-west Atlantic through the Baltic to the Mediterra-nean. A primary aim of the work was to establish a database of accumulated trace metal concentrations(Cd, Cr, Cu, Fe, Mn and Zn) in this biomonitor. Statistical analysis has shown significant geographical dif-ferences in the bioavailabilities of all the metals, the most distinct being copper, iron and manganese. Ithas proved possible to identify unusually high accumulated concentrations of Cd, Cr, Cu, Fe, Mn and Zn inthis biomonitor, indicative of high metal bioavailability at a particular site. These may serve as referencepoints for future biomonitoring programmes seeking to identify metal contamination in coastal waters.

� 2008 Elsevier Ltd. All rights reserved.

1. Introduction

Toxic metal contamination of coastal waters can be measuredon a relative scale using biomonitors (Phillips and Rainbow,1994; Rainbow, 1995, 2006; Luoma and Rainbow, 2008). Biomon-itors accumulate trace metals in proportion to their ambient bio-availability, and accumulated concentrations are time-integratedmeasures of the exposure of that biomonitor to all bioavailablesources of the trace metal over a previous time period (Phillipsand Rainbow, 1994; Rainbow, 1995, 2006). Thus the accumulatedtrace metal concentration in a biomonitor is a measure of the totalintegrated bioavailability of that trace metal to that organism atthat location over that previous time period. Strictly, a single bio-monitor of trace metal contamination provides information onthe integrated availabilities of metals specifically to that biomoni-tor, although it might be reasonable to extrapolate from that bio-

ll rights reserved.

: +48 12 664 6912.(W. Fialkowski), piero.calosiald.de (S. Dahlke), annanissi-.G. Moore), serg@gmf.ku.lt (S.nbow@nhm.ac.uk (P.S. Rain-

ski, W. et al., The sandhoppeul.2008.09.013

monitor to draw conclusions about local metal bioavailabilities tothe biota in general.

Talitrid amphipod crustaceans typically live in the strandlinesof shores. They take up metals from both solution and food (Weeksand Rainbow, 1991, 1993), which consists of cast-up plant material– usually macrophytic algae. Such algae receive their metals fromsolution, and it is arguable that talitrid crustaceans are biomonitor-ing predominantly the bioavailable metal in the water column(Rainbow, 1995, 2006). In some areas, however, the density of sub-littoral algae is so low, that their remnants washed ashore are tooscarce to constitute the bulk of sandhoppers’ diet. This is the caseat many spots on the southern Baltic shores, and the animals livingthere have to rely for food on other jetsam, containing organic mat-ter of different origin, which may result in locally changed bio-availability of some metals to the sandhoppers (Fialkowski et al.,2000).

Talitrus saltator offers great potential as an easily collected bio-monitor widely distributed in European waters from the southernBaltic through the north-west Atlantic to the Mediterranean. Geo-graphically patchy data are available on accumulated trace metalconcentrations in T. saltator, along the Polish coast of the Baltic(Rainbow et al., 1998; Fialkowski et al., 2000, 2003), in the UK(Moore and Rainbow, 1987; Moore et al., 1991; Rainbow et al.,

r Talitrus saltator (Crustacea: Amphipoda) as a biomonitor ..., Mar.

2 W. Fialkowski et al. / Marine Pollution Bulletin xxx (2008) xxx–xxx

ARTICLE IN PRESS

1989) and in the Mediterranean from Italy and Corsica (Ugoliniet al., 2004, 2005).

We have carried out a geographically widespread, approxi-mately simultaneous collection of T. saltator in European coastalwaters, in order to establish a database of accumulated trace metalconcentrations in this easily accessible biomonitor (Table 1). Wehope to identify typical accumulated concentrations in T. saltator,understanding that even phylogenetically closely related speciescan accumulate appreciably different metal concentrations (Mooreand Rainbow, 1987; Rainbow, 1995, 2006; Ugolini et al., 2005), aswell as higher accumulated concentrations reflecting raised localtrace metal bioavailabilities. Bioaccumulated metal concentrationsoffer cost-effective measures of toxic metal pollution, and their po-tential use in the environmental management of metal contamina-tion is being increasingly appreciated (Luoma and Rainbow, 2008).

We have chosen sites located on the shores of the Irish Sea inthe north, the Mediterranean in the south, and the Baltic Sea,where the distinctly lower salinity (generally less than 15 PSU)influences the bioavailability of dissolved trace metals. Collectionshave therefore been made from UK sites: Millport in the Firth of

Table 1Talitrus saltator: Details of collection sites, numbers (n) of samples (usually individuals butsandhoppers analysed

Collection site Co-ordinates Date

Baltic SeaLithuaniaKlaipeda N 55 40 29 May 2005

E 21 05Kaliningrad (Russia)Kulikovo N 54 56 24 28 May 2005

E 20 19 35Baltijsk N 54 39 27 May 2005

E 19 53Baltijsk-2 N 54 37 27 May 2005

E 19 52PolandJantar N 54 20 41 30 May 2005

E 19 02 40Gorki Wschodnie N 54 22 03 30 May 2005

E 18 47 18Osada Rybacka N 54 33 41 30 May 2005

E 18 33 06Hel N 54 37 03 29 May 2005

E 18 49 38Lake Jamno N 54 09 17 28 May 2005

E 15 22 11Swinoujscie N 53 55 01 27 May 2005

E 14 18 22GermanyHiddensee N 54 35 23 4 June 2005

E 13 05 54SwedenNybrostrand N 55 26 03 10 June 2005

E 13 56 00KattegatSwedenSkälderviken N 56 15 08 7 June 2005

E 12 50 02Mellbystrand N 56 32 05 6 June 2005

E 12 57 02

Irish SeaMillport, Scotland N 55 46 78 31 May 2005

W 04 55.83Dulas Bay, Wales N 53 22 25 14 July 2005

W 04 16 57

Mediterranean SeaGrosseto, ItalyAlbegna N 42 25 09 28 May 2005

E 11 15 16Feniglia N 42 30 35 28 May 2005

E 11 11 29

Please cite this article in press as: Fialkowski, W. et al., The sandhoppePollut. Bull. (2008), doi:10.1016/j.marpolbul.2008.09.013

Clyde, Scotland, and Dulas Bay, a site in Anglesey, Wales, wellknown to have high trace metal availabilities from a history of re-ceipt of metal-rich mine effluent (Foster, 1976; Foster et al., 1978;Boult et al., 1994); from the Baltic shores in Lithuania, the Kalinin-grad region of Russia, Poland (Rainbow et al., 1998; Fialkowskiet al., 2000, 2003), Germany and Sweden, and along the nearbySwedish coast in the Kattegat; and finally from two Italian beachesin Tuscany (Ugolini et al., 2004, 2005) (Table 1).

2. Materials and methods

The talitrid amphipod crustacean T. saltator (Montagu) was col-lected from the strandlines of sandy beaches at 18 sites in Europeancoastal waters, between the 27 May and 10 June 2005 for all but onesite (Dulas Bay 14 July 2005) (Table 1). Approximately 20 amphi-pods were collected from each site by hand, either by digging orfrom beneath cast-up driftwood or other jetsam on the shore.

On the day of collection, individual amphipods were rinsedbriefly in distilled water and frozen, to be later dried at 60 �C in

occasionally up to three pooled amphipods) and ranges of individual dry weight (g) of

Number of individuals Individual dry weight range

20 0.0090–0.0283

20 0.0108–0.0365

20 0.0149–0.0426

18 0.0121–0.0344

14 0.0070–0.0197

18 0.0058–0.0238

19 0.0090–0.0492

32 0.0073–0.0215

19 0.0122–0.0383

16 0.0068–0.0265

18 0.0079–0.0266

15 0.0140–0.0390

16 0.0109–0.0350

18 0.0132–0.0231

17 0.0142–0.0312

15 0.0058–0.0384

19 0.0058–0.0217

14 0.0047–0.0188

r Talitrus saltator (Crustacea: Amphipoda) as a biomonitor ..., Mar.

5g

amph

ipod

s(a

ses

tim

ated

from

best

-fit

doub

le-l

ogre

gres

sion

sof

met

alco

ncen

trat

ion

agai

nst

indi

vidu

aldr

yw

eigh

t)fr

om18

site

sin

oppe

rIr

onM

anga

nes

eZi

nc

once

ntr

atio

nC

LC

once

ntr

atio

nC

LC

once

ntr

atio

nC

LC

once

ntr

atio

nC

L

58.9

54.6

,63.

623

718

0,31

215

.012

.5,1

8.0

147

132,

164

52.2

41.8

,65.

268

.754

.9,8

6.1

18.6

15.4

,22.

512

611

2,14

252

.845

.1,6

1.9

211

97.8

,456

35.4

20.7

,60.

413

610

5,17

636

.731

.3,4

3.1

79.7

55.8

,114

31.9

28.3

,35.

914

113

0,15

255

.842

.3,7

3.6

67.3

41.0

,110

23.8

17.5

,32.

315

611

7,20

668

.062

.3,7

4.2

97.0

66.7

,141

26.4

19.3

,36.

014

313

0,15

861

.454

.9,6

8.7

59.2

44.2

,79.

334

.327

.8,4

2.3

158

141,

178

61.6

58.2

,65.

166

.848

.2,9

2.5

29.5

23.8

,36.

716

815

6,18

155

.046

.0,6

5.7

116

68.6

,197

31.2

22.5

,43.

413

712

2,15

462

.557

.1,6

8.4

99.9

80.8

,124

37.7

30.2

,47.

218

315

9,21

068

.565

.8,7

1.3

214

183,

250

17.5

16.2

,18.

910

910

2,11

657

.645

.0,7

3.7

60.7

33.2

,111

32.1

24.2

,42.

712

696

.2,1

6555

.148

.7,6

2.4

229

132,

399

46.8

35.0

,62.

719

017

3,20

765

.055

.3,7

6.3

533

379,

750

26.1

19.2

,35.

417

315

0,20

140

.233

.3,4

8.6

47.7

23.1

,98.

517

.612

.6,2

4.6

153

129,

182

0316

9,24

411

0380

3,15

1357

.243

.1,7

6.0

235

211,

263

47.1

44.3

,50.

023

018

5,28

776

.466

.3,8

8.2

125

118,

133

49.7

44.7

,55.

328

116

8,47

132

.620

.0,5

3.3

169

148,

192

W. Fialkowski et al. / Marine Pollution Bulletin xxx (2008) xxx–xxx 3

ARTICLE IN PRESS

pre-weighed acid-washed polythene vials. Most amphipods weredried individually, but smaller amphipods were pooled in groupsof two or three. Amphipods to be pooled in any sample were cho-sen to be of similar size, and the mean dry weight of the pooledamphipods was used as the individual dry weight in all subsequentanalyses. Individual and pooled amphipods were subsequentlydried to constant weight, digested in Aristar concentrated nitricacid (B.D.H. Ltd., Poole, UK) at 100 �C, and made up to 5 ml withdouble distilled water for analysis of concentrations of trace metals(Cd, Cr, Cu, Fe, Mn and Zn) on a Vista-Pro CCD simultaneous ICP-OES.

All concentration data are quoted in terms of dry weight(lg g�1). Samples of TORT-2 Lobster Hepatopancreas Certified Ref-erence Material (National Research Council, Canada) and MusselTissue (National Institute of Standards and Technology, USA) wereanalysed simultaneously. Agreement has been considered satisfac-tory, except in the case of copper. Probably as a result of matrix ef-fects and the concentration ranges of Cu and other trace metals inthe digests, measured Cu concentrations of both these certified ref-erence materials were beneath the certified values. All Cu concen-trations in the amphipods have therefore been adjusted by acorrection factor.

Amphipod crustaceans typically show an effect of body size onaccumulated trace metal concentrations. Data were thereforetransformed logarithmically, to improve their fit to normal distri-butions and to transform the power function (y = axb) to a linearrelationship for comparison of best-fit regression lines.

All data sets were examined for size effects on the accumulatedtrace metal concentrations in the talitrids. Correlation analyses ofthe relationship between metal concentration and individual dryweight (logged data) were carried out for the complete amphipoddata set for each metal. Size effects were apparent in at least onedata set for each metal. What is more, occasionally a data set fora particular metal at a particular site showed a significantly differ-ent regression coefficient from the data sets for that metal at othersites. Therefore, we employed the Kruskal–Wallis test as a non-parametric alternative to the analysis of variance (Sokal and Rohlf,1995). All the statistical computations were performed using theSTATISTICA package (StatSoft, 2005).

Tabl

e2

Talit

rus

salt

ator

:tr

ace

met

alco

ncen

trat

ions

(in

lg

g�1

wit

h95

%co

nfide

nce

limit

sCL

)of

0.01

Euro

pean

coas

tal

wat

ers

Site

Cad

miu

mC

hro

miu

mC

Con

cen

trat

ion

CL

Con

cen

trat

ion

CL

C

Kla

iped

a1.

91.

7,2.

1K

uli

kovo

1.0

0.7,

1.4

2.4

1.6,

3.6

Bal

tijs

k1.

31.

0,1.

71.

70.

4,7.

8B

alti

jsk-

20.

80.

1,6.

91.

20.

1,15

.8Ja

nta

r2.

40.

9,6.

0G

orki

Wsc

hod

nie

2.2

1.9,

2.4

Osa

daR

ybac

ka2.

11.

8,2.

3H

el2.

11.

7,2.

6La

keJa

mn

o2.

01.

5,2.

7Sw

inou

jsci

eH

idde

nse

eN

ybro

stra

nd

3.6

2.9,

4.4

Skäl

derv

iken

3.3

2.8,

3.8

Mel

lbys

tran

d3.

32.

6,4.

2M

illp

ort

1.9

1.6,

2.3

Du

las

Bay

3.3

2.3,

4.8

2A

lbeg

na

1.1

0.9,

1.2

1.1

0.8,

1.5

Fen

igli

a1.

31.

1,1.

50.

90.

6,1.

3

3. Results

Because of the presence of size effects on the metalconcentrations accumulated by the amphipods, and because thedifferent collections contained amphipods of slightly differentindividual size ranges (Table 1), it is not valid to quote comparativedata in terms of means. Accumulated metal concentrations (Ta-ble 2) are therefore quoted in terms of the concentration in a stan-dard-sized amphipod as estimated (with 95% confidence limits)from the best-fit double-log regressions of metal concentrationagainst individual dry weight. The standard weight chosen is0.015 g, within the weight range of the collection made at everysite (Table 1).

Table 2 presents these metal concentration data, for every sitefor Cu, Fe, Mn and Zn, but for a restricted number of sites for Cdand Cr. In the latter cases, missing data are explicable from therelationships between the amount of metal present in a digest (afeature of accumulated concentration and the number and size ofamphipod(s) comprising a sample) and the sensitivity of the ICP-OES analysis for that particular metal.

Table 3 presents the results of the Kruskal–Wallis test. For eachmetal, sites are ranked in descending order of the elevations of theregression lines. Sites sharing a common letter for a metal do notdiffer significantly in the accumulated concentration of that metalin the amphipods.

Please cite this article in press as: Fialkowski, W. et al., The sandhopper Talitrus saltator (Crustacea: Amphipoda) as a biomonitor ..., Mar.Pollut. Bull. (2008), doi:10.1016/j.marpolbul.2008.09.013

Table 3Talitrus saltator: Kruskal–Wallis test comparisons of best-fit double-log regressions of metal concentrations against individual dry weight for six trace metals in amphipodscollected from up to 18 European coastal sites. Concentrations of each particular metal sharing a common letter do not differ significantly (p P 0.05)

Cadmium Chromium Copper Iron Manganese Zinc

Nybrostrand a Dulas Bay a Dulas Bay a Dulas Bay a Albegna a Dulas Bay aMellbystrand b Jantar a,b Gorki Wschodnie b Mellbystrand b Dulas Bay a,b Feniglia bSkälderviken b Gorki Wschodnie b,c Hiddensee b,c Klaipeda c Skälderviken b,c Skälderviken b,cFeniglia c Hel b,c Mellbystrand b,c Albegna c Swinoujscie c Swinoujscie b,c,dAlbegna d Osada Rybacka b,c Hel b,c Hiddensee c Osada Rybacka c Mellbystrand b,c,dBaltijsk d Baltijsk b,c Osada Rybacka b,c,d Skälderviken c Nybrostrand c,d Jantar b,c,dKulikovo d Millport b,c Swinoujscie b,c,d Feniglia c Baltijsk-2 c,d Hel b,c,d,eBaltijsk-2 d Kulikovo b,c Nybrostrand b,c,d Lake Jamno c,d Hel c,d,e Osada Rybacka c,d,e,f

Klaipeda b,c Klaipeda b,c,d Gorki Wschodnie d Lake Jamno c,d,e,f Klaipeda d,e,fLake Jamno c,d Jantar b,c,d Swinoujscie d,e Jantar c,d,e,f Gorki Wschodnie e,fAlbegna d Baltijsk c,d Baltijsk d,e,f Gorki Wschodnie c,d,e,f,g Millport e,fFeniglia d Lake Jamno b,c,d Nybrostrand d,e,f Feniglia c,d,e,f,g,h Baltijsk-2 fBaltijsk-2 d Kulikovo c,d,e Jantar d,e,f Mellbystrand d,e,f,g,h Albegna f,g

Skälderviken d,e,f Baltijsk-2 d,e,f Baltijsk e,f,g,h Lake Jamno g,hFeniglia e,f Millport d,e,f Millport f,g,h Kulikovo g,hAlbegna f Hel e,f Hiddensee g,h Nybrostrand g,hBaltijsk-2 g Osada Rybacka f Kulikovo h Baltijsk g,hMillport g Kulikovo f Klaipeda h Hiddensee h

Table 4Talitrus saltator: identification of atypically high accumulated trace metal concentra-tions in sandhoppers, indicative of atypically high metal availabilities, in comparisonwith a more typical range of concentrations (in 0.015 g amphipods as estimated frombest-fit double-log regressions of metal concentration against individual dry weight –lg g�1)

Atypically high bodyconcentration

Typical range of bodyconcentrations

Cadmium 35 1–5Chromium 180 1–5Copper 200 30–75Iron 1110 45–550Manganese 75–110 15–50Zinc 300 100–250

4 W. Fialkowski et al. / Marine Pollution Bulletin xxx (2008) xxx–xxx

ARTICLE IN PRESS

The copper comparative data set is relatively complete withthree sites showing a significantly different concentration-sizeregression coefficient from the others. The accumulated concentra-tion in the Dulas Bay amphipods was huge compared to all others(Table 2). Correspondingly the Dulas Bay amphipods stand signifi-cantly different from all others in Table 3 for Cu. After Dulas Baythere was a sequence of sites with concentrations in 0.015 gamphipods decreasing from Hiddensee to Albegna, with Millportand Baltijsk-2 slightly detached from the others. Indeed amphi-pods at these latter two sites had significantly lower Cu concentra-tions than all other amphipods (Table 3).

Similarly, the data set for iron is relatively complete. The great-est accumulation of Fe by amphipods was recorded at Dulas Bay.The concentration-size regression coefficient, calculated for thoseanimals differed significantly from the others. Of the remainingsites, accumulated Fe concentrations in 0.015 g amphipods werehigh at Mellbystrand and Klaipeda, although the latter is not de-tached from the sequence of concentrations at all other sites (Ta-bles 2 and 3). At the bottom end, amphipods from OsadaRybacka and Kulikovo had low accumulated Fe concentrations,although these were not significantly different from the Fe concen-trations of amphipods at six other sites (Table 3).

In the case of manganese, accumulated concentrations inamphipods at Albegna were the highest and, as a probable result,the concentration-size regression coefficient differs significantlyfrom most of the others (Tables 2 and 3). Following Albegna, T. sal-tator from Dulas Bay also had very high accumulated Mn concen-trations, significantly higher than those in amphipods from allbut one remaining sites (Tables 2 and 3). Thereafter follows a se-quence of accumulated Mn concentrations down to those in thesandhoppers from Klaipeda.

Dulas Bay amphipods also showed the highest accumulatedzinc concentrations, significantly raised above all others (Tables 2and 3). After Dulas Bay there was again a sequence of amphipodaccumulated Zn concentrations with incremental differences fromSkälderviken down to Hiddensee (Tables 2 and 3).

There is no full data set available for cadmium (Table 2). The re-sults of the Kruskal–Wallis test suggest that no site has amphipodswith extremely high Cd concentrations, their values falling fromNybrostrand to Baltijsk-2 (Table 2).

A similar situation seems to exist for chromium (Tables 2 and3). Accumulated concentrations were highest in Dulas Bay amphi-pods, but these are at one end of a sequence down to accumulatedconcentrations at Feniglia (Table 2).

Please cite this article in press as: Fialkowski, W. et al., The sandhoppePollut. Bull. (2008), doi:10.1016/j.marpolbul.2008.09.013

4. Discussion

This study has provided a geographically widespread data set ofaccumulated trace metal concentrations in the sandhopper T. salta-tor in European coastal waters, collected within a narrow temporalwindow. Furthermore it has proved possible in the case of threetrace metals (Cu, Fe and Mn) to use these data to identify atypicallyhigh accumulated concentrations, indicative of atypically high lo-cal toxic metal bioavailability to the amphipods at a particular site.This could explain significantly different concentration-size regres-sion coefficients for some data sets, resulting from a different pat-tern of accumulation of the metal by the amphipods at a given site.This is quite likely to be the case for the Dulas Bay amphipods andiron, and the Albegna amphipods and manganese. After furtherconsideration of literature data (see below), Table 4 summarisesthe accumulated trace metal concentrations in T. saltator identifiedas being atypically high, compared against more typical ranges ofbody concentrations in this amphipod in European coastal waters.

Copper, iron, manganese and zinc were present in high localbioavailabilities to T. saltator at Dulas Bay. The situation there isnot unexpected for this estuary receives input from Afon Goch,an acid mine stream rising on Parys Mountain which was minedfor Cu until the late nineteenth century (Foster et al., 1978). AfonGoch and therefore Dulas Bay have very high levels of Cu, Fe, Mnand Zn (Foster, 1976; Foster et al., 1978; Boult et al., 1994), re-flected in the atypically very high concentrations of Cu and Fe (Ta-ble 2). Also the concentrations of Mn and Zn in the amphipodswere very high (Tables 2 and 4).

r Talitrus saltator (Crustacea: Amphipoda) as a biomonitor ..., Mar.

W. Fialkowski et al. / Marine Pollution Bulletin xxx (2008) xxx–xxx 5

ARTICLE IN PRESS

As far as manganese is concerned, the accumulated concentra-tion at Albegna can also be considered atypically high (Tables 2–4). Ugolini et al. (2004) collected T. saltator from Albegna, but theydid not measure their accumulated Mn concentrations.

The Dulas Bay sandhoppers in this study were actually collectedfrom the inner side of the sandbar delimiting the seaward edge ofthe bay, as opposed to those analysed for Cu and Zn by Rainbowet al. (1989) which were collected in 1984 from the seaward sideof the sandbar adjacent to the outflow of water from the Bay. Nev-ertheless amphipod body concentrations were high in both col-lected samples. As in this study, Cu and Zn concentrations in theDulas Bay amphipods were much above those recorded for T. salta-tor from Millport (Rainbow et al., 1989).

The data compiled here agree well with other trace metal con-centrations of T. saltator reported in the literature. Copper concen-trations in this amphipod from along the Polish coast (Fialkowskiet al., 2000, 2003), Millport, Scotland (Rainbow et al., 1989; Rain-bow and Moore, 1990) and Italy and Corsica (Ugolini et al., 2004,2005) almost all fall within the typical range of Cu concentrationsidentified in Table 4. The population from Calambrone (Livorno,Italy) had a mean Cu concentration of 87.7 lg Cu g�1, suggestingsome local contamination (Ugolini et al., 2004).

Excluding Dulas Bay concentrations (Rainbow et al., 1989),other zinc concentrations of T. saltator in the literature mostlyagree with, but do reach slightly higher values than, those reportedhere (even for Dulas Bay). Thus Fialkowski et al. (2003) reportedzinc concentrations equivalent to 211 lg g�1 in 0.015 g sandhop-pers from Osada Rybacka in the Gulf of Gdansk in 2000, and rela-tively high Zn concentrations have been reported forsandhoppers from Millport (Rainbow et al., 1989; Rainbow andMoore, 1990). Ugolini et al. (2004) reported similarly relativelyhigh mean body concentrations of Zn in sandhoppers at two sitesin the Mediterranean (Piombino, Livorno, Italy, and La Piantarella,Corsica, France). In contrast to the situation at Dulas Bay, there isno evidence for extreme Zn contamination at Osada Rybacka (Fial-kowski et al., 2000, 2003) or Millport (Rainbow et al., 1989). It maywell be that typical Zn concentrations in T. saltator do reach250 lg Zn g�1 without being indicative of strong zinc contamina-tion (Table 4). The higher Zn concentrations reported for the DulasBay sandhoppers collected in 1984 (Rainbow et al., 1989) may bet-ter represent concentrations above the typical range reflectingatypically high Zn bioavailability (Table 4).

Comparative data for iron concentrations in sandhoppers fromthe Baltic coast of Poland (Rainbow et al., 1998; Fialkowski et al.,2000, 2003) and from the Mediterranean (Ugolini et al., 2004) allfall in the typical Fe concentration range identified in Table 4.

Accumulated Mn concentrations in T. saltator collected alongthe Polish coast in 1998 (Fialkowski et al., 2000) and 2000 (Fial-kowski et al., 2003) mostly all fall in the typical range identifiedin Table 4. The highest concentration reported from these collec-tions (Swinoujscie at the mouth of the River Odra in 1998 (Fial-kowski et al. 2000)) may be attributable to a size effect. Theconcentrations of Mn in Swinoujscie sandhoppers measured in2005 were in the typical range (Table 4). A few 2000 Mn concentra-tions (Fialkowski et al., 2003) and nearly all 1996 Mn concentra-tions in the Gulf of Gdansk T. saltator were above the typicalrange in Table 4 and indicated atypically high Mn availability,probably as a result of ambient Mn input from the Vistula River(see Fialkowski et al., 2000). Mn concentrations in the sandhopperscollected in the Gulf of Gdansk in 2005 were much lower (Table 2),indicating lower Mn bioavailability to these amphipods then.

Cadmium concentrations measured in the sandhoppers col-lected in this study in 2005 agree well with those measured insandhoppers collected from Poland in 1998 and 2000 (Fialkowskiet al., 2000, 2003) and in the Mediterranean in 1999 and 2000(Ugolini et al., 2004), and can be considered typical (Table 4). Much

Please cite this article in press as: Fialkowski, W. et al., The sandhoppePollut. Bull. (2008), doi:10.1016/j.marpolbul.2008.09.013

higher Cd concentrations in amphipods collected in the Gulf ofGdansk in 1996 (Rainbow et al., 1998) indicate atypically raised lo-cal Cd bioavailabilities at that time, perhaps again resulting fromthe ambient outflow of the Vistula River.

Comparative data for accumulated chromium concentrations inT. saltator are available from the Mediterranean (Ugolini et al.,2004). Those sandhoppers reached the extraordinary mean accu-mulated Cr concentration of 182 lg Cr g�1 at Cateraggio d’Aleria,Corsica, France, surely indicative of atypically raised Cr bioavail-ability. Such bioavailability, however, is considered to be of naturalorigin in certain localities in Corsica (see Ugolini et al., 2004 andreferences within). Sandhoppers from the remaining Italian siteshad mean Cr concentrations (Ugolini et al., 2004) more similar tothose recorded here.

Table 4 is an attempt to identify accumulated trace metal con-centrations indicative of potentially ecotoxicologically significantambient metal bioavailabilities in a common, widely distributed,easily collected inhabitant of sandy shores, even in the absenceof tides as in the Baltic and Mediterranean Seas. We hope that thisinformation will prove of value in cost-effective management pro-grammes seeking to identify and subsequently control anthropo-genic contamination of coastal waters by toxic metals.

Acknowledgements

The original idea of the project was put forward by the late Pro-fessor Ludwik Zmudzinski, who later took part in the initial stagesof its planning. We sadly miss his friendship, advice and co-operation.

We are grateful to Professor Maciej Wolowicz (University ofGdansk) and Dr. Krzysztof Skora (University of Gdansk Marine Sta-tion Hel) for their assistance during the stay of WF, BDS and PSR inPoland in May 2005. We also appreciate the help of Galina Gilden-berg, MSc and Dr. Oleg Potutko in sampling on the Russian coast.

References

Boult, S., Collins, D.N., White, K.N., Curtis, C.D., 1994. Metal transport in a streampolluted by acid mine drainage – the Afon Goch, Anglesey, UK. EnvironmentalPollution 84, 279–284.

Fialkowski, W., Rainbow, P.S., Fialkowska, E., Smith, B.D., 2000. Biomonitoring oftrace metals along the Baltic coast of Poland using the sandhopper Talitrussaltator (Montagu) (Crustacea: Amphipoda). Ophelia 52, 183–192.

Fialkowski, W., Rainbow, P.S., Smith, B.D., Zmudzinski, L., 2003. Seasonal variationin trace metal concentrations in three talitrid amphipods from the Gulf ofGdansk, Poland. Journal of Experimental Marine Biology and Ecology 288, 81–93.

Foster, P., 1976. Concentrations and concentration factors of heavy metals in brownalgae. Environmental Pollution 10, 45–53.

Foster, P., Hunt, T.E., Morris, A.W., 1978. Metals in acid mine stream and estuary.Science of the Total Environment 9, 75–86.

Luoma, S.N., Rainbow, P.S., 2008. Metal Contamination in Aquatic Environments:Science and Lateral Management. Cambridge University Press, Cambridge.

Moore, P.G., Rainbow, P.S., 1987. Copper and zinc in an ecological series oftalitroidean Amphipoda (Crustacea). Oecologia 73, 120–126.

Moore, P.G., Rainbow, P.S., Hayes, E., 1991. The beach-hopper Orchestia gammarellus(Crustacea: Amphipoda) as a biomonitor for copper and zinc: North Sea trials.Science of the Total Environment 106, 221–238.

Phillips, D.J.H., Rainbow, P.S., 1994. Biomonitoring of Trace Aquatic Contaminants,second ed. Chapman and Hall, London. 371pp.

Rainbow, P.S., 1995. Biomonitoring of heavy metal availability in the marineenvironment. Marine Pollution Bulletin 3, 183–192.

Rainbow, P.S., 2006. Biomonitoring of trace metals in estuarine and marineenvironments. Australasian Journal of Ecotoxicology 12, 107–122.

Rainbow, P.S., Moore, P.G., 1990. Seasonal variation in copper and zincconcentrations in three talitrid amphipods (Crustacea). Hydrobiologia 196,65–72.

Rainbow, P.S., Fialkowski, W., Smith, B.D., 1998. The sandhopper Talitrus saltator as atrace metal biomonitor in the Gulf of Gdansk, Poland. Marine Pollution Bulletin36, 193–200.

Rainbow, P.S., Moore, P.G., Watson, D., 1989. Talitrid amphipods as biomonitors forcopper and zinc. Estuarine, Coastal and Shelf Science 28, 567–582.

Sokal, R.R., Rohlf, F.J., 1995. Biometry, third ed. W.H. Freeman & co., New York.StatSoft, Inc., 2005. STATISTICA (data analysis software system), version 7.1.

<www.statsoft.com>.

r Talitrus saltator (Crustacea: Amphipoda) as a biomonitor ..., Mar.

6 W. Fialkowski et al. / Marine Pollution Bulletin xxx (2008) xxx–xxx

ARTICLE IN PRESS

Ugolini, A., Borghini, F., Calosi, P., Bazzicalupo, M., Chelazzi, G., Focardi, S., 2004.Mediterranean Talitrus saltator (Crustacea, Amphipoda) as a biomonitor ofheavy metals contamination. Marine Pollution Bulletin 48, 526–532.

Ugolini, A., Borghini, F., Focardi, S., Chelazzi, G., 2005. Heavy metals accumulation intwo syntopic sandhopper species: Talitrus saltator (Montagu) and Talorchestiaugolinii Bellan Santini and Ruffo. Marine Pollution Bulletin 50, 1328–1334.

Please cite this article in press as: Fialkowski, W. et al., The sandhoppePollut. Bull. (2008), doi:10.1016/j.marpolbul.2008.09.013

Weeks, J.M., Rainbow, P.S., 1991. The uptake and accumulation of zinc and copperfrom solution by two species of talitrid amphipods (Crustacea). Journal of theMarine Biological Association UK 71, 811–826.

Weeks, J.M., Rainbow, P.S., 1993. The relative importance of food and seawater assources of copper and zinc to talitrid amphipods (Crustacea; Amphipoda;Talitridae). Journal of Applied Ecology 30, 722–735.

r Talitrus saltator (Crustacea: Amphipoda) as a biomonitor ..., Mar.