J Mar. Biol.Ass. u.K. (2000), 80, 587-597Printed in the United Kingdom

The subtidal macrobenthos in the mesohaline part of the

Schelde Estuary (Belgium): influenced by man?

Tom Ysebaert*\ Liesbeth De Neve* and Patriek Meire*~

*Institute of Nature Conservation, Kliniekstraat 25, B-J070 Brussel, Belgium. tE-mail: tom.ysebaert@instnat.be*Present address: University of Antwerp, Department of Biology,Universiteitsplein I, B-26JOWilrijk, Belgium

The macrobenthos of the subtidal, mesohaline zone of the Schelde Estuary (Belgium) was sampled inOctober 1996 and 1997 at 54 and 73 sampling locations respectively. Sediments ranged from silty to verycoarse, with the dominant sediment type being silt (33% of alliocations). Of the 35 macrobenthic speciesobserved, only seven species occurred in more than 20% of the samples. The polychaete Heteromastus

filiformis and Oligochaeta were most common. Multivariate techniques revealed three distinct commu-nities, linked mainly with sedimentological factors: (I) a species-poor (nine species) community with adominance of the amphipod Bathyporeiapilosa, a low mean abundance and biomass (86 ind m -2,0.0189 gash-free dry weight (AFDW) m-2), and a mean median grain size of 215 ::!:I9Jlm (fine sand); (2) aspecies-rich (22) community, with the small polychaete Polydoraligerica as indicator species, a relativelyhigh mean abundance and biomass (2298 ind m - 2, 1.395 g AFDW m - 2, oysters excluded), a meanmedian grain size of 133 ::!:41Jlm, and also the occurrence of sediments with hard substrates being char-acteristic for this community; (3) a community with an intermediate species richness (12), abundance andbiomass (248 ind m - 2, 0.249 g AFDW m - 2), with H filiformis and Oligochaeta as indicator species, and amedian grain size of 76 :!:9 Jlm. In the study area several typical brackish water species were observed(e.g. Polydoraligerica, Corophiumlacustre, Gammarus salinus).

Mean total abundance and biomass were very low, and the benthic commu9-ities appeared to be understress, with a dominance of mainly smaIl, subsurface deposit and surf ace dej:losit feeding opportunisticspecies. This is probably a combined effect of both natural physical and human-induced disturbance.Only sediments with hard substrates (e.g. rocks) seems to favour species richness, providing a shelteragainst physical disturbance.

INTRODUCTION

The inner and upper parts of estuaries are oftenseverely impacted by man. Land reclamation results in ahigh degree of estuarine habitat loss. Drainage of wastewater, dredging for shipping, safety constructions (e.g.dykes, storm surge barriers), fixation ofbanks, etc. changethe chemical and physical proper ties of these estuarinehabitats (Costanza et al., 1993; Gray, 1997).

The Schelde Estuary is one of the larger north-westEuropean estuaries with a complete salinity gradient,including a large freshwater tidal area. Especially thepart between the Dutch - Belgian border and the Rupel isseverely impacted and heavily polluted by domestic,industrial and agricultural waste loads and the concentra-tions of micropollutants are high (Van Eck & De Rooij,1993; Soetaert & Herman, 1995a,b; Zwolsman, 1999).From the 1980s on water quality has started to improveslowly, and th is improvement continues in the 1990s (VanDamme et al., 1995; Van Eck et al., 1998). Near theOutch - Belgian border, the large industrialized area ofAntwerpen Harbour is situated. Being a major sedimen-tation area, this zone is dredged intensively in order tokeep it accessible for navigation (Claessens et al., 1991).Ouring the last decade several harbour infrastructures(e.g. container terminals) have been constructed in thearea, and the shipping channel has been deepened.

Although the intertidal macrobenthic communitiesalong the Schelde Estuary are weIl known (e.g. Ysebaert

}ournal tif the Marine Biological Association tif the United Kingdom (2000)

et al., 1993, 1998), recent data about the spatial distribu-tion of macrobenthos in the mesohaline subtidal part ofthe Zeeschelde were so far almost completely lacking.However, knowledge about the present status of themacrobenthos in this part of the estuary could give anindication of the present ecosystem health, since benthosis recognized as a suitable ecological group for moni-toring and detecting effects of stress and pollution (e.g.Pearson & Rosenberg, 1978; Boesch & Rosenberg, 1981;Warwick & Clark, 1993; Diaz & Rosenberg, 1995; Gastonet al., 1998).

In this study the spatial distribution of macrobenthiccommunities in the mesohaline subtidal part of theZeeschelde is described based on data collected in 1996

and 1997. The results are compared with the speciesdiversity along the complete Schelde salinity gradient andwith data from 1952 (Leloup & Konietzko, 1956). Possibleeffects on benthic communities of dredging operationsand ot her anthropogenic influences, like the occurrenceof hard substrates within the sediment are discussed.

MATERlALS AND METHODS

Study area

The Schelde Estuary, a macrotidal coastal plainestuary, is situated near the border between The Nether-lands and Belgium. It measures 160 km with a surf ace

588 T. Ysebaert et al. Subtidal macrobenthosin the mesohalineScheldeEstuary

Sampling locations

o1996. 19975km

The Ndbcrlands

Vlissingen

Study area

/

11I Dredging sites

. Dumping sites

Figure 1. Geographical view of the Beneden Zeeschelde area with indication of the 54 and 73 sampling locations in 1996 and1997, and with the main dredging and dumping sites in this part of the estuary.

area of approximately 350 km2. The Westerschelde(55 km) represents the downstream Dutch part with thepoly-/mesohaline zone of the estuary; the Zeeschelde(105 km), the Belgian part of the Schelde Estuary, repre-sents the meso-/oligohaline and freshwater tidal zones(Figure I). The mean tidal ran~e is 3.8 m in Vlissingen,5.2 m in Antwerpen and 2.0 minGent.

The study area is situated in the maximum turbidityand mesohaline zone of the Zeeschelde (Baeyens et al.,1998; Fettweis et al., 1998), between the Dutch-Belgianborder and Fort Liefkenshoek (Figure I). In this part ofthe estuary mean tidal range is about 4.94 m.

Sampling and laboratory ana(ysis

Temperature, salinity and oxygen concentrations weremeasured monthly at two buoys in the study area (FigureI). The macrobenthos was sampled in October 1996 andOctober 1997 in 9 and 10 transects respectively (Figure I).In every transect about 6-7 locations were sampled,divided over th ree depth strata «2.95m; 2.95-7.95m;> 7.95 m below mean low low water spring). In total 54and 73 locations were sampled in 1996 and 1997. On eachlocation one Van Veen grab (0.105 m2) was taken, fromwhich one small core (4)2 cm) for sediment analysis wastaken. The benthic samples were sieved through a I mmmesh in the field and preserved in neutralized formaline.Position and water depth of the grab sample were noted.

In the labo ra tory samples were sorted after stainingwith 0.02% rose bengal. All organisms were identified tospecies level, except for the genus Ostrea, the Oligochaetaand one spionid specimen, and counted. The ash-rree dryweight (AFDW) biomass was obtained by drying allspecimens at 105°C [or 12hand ashing them at 550°C.

Journal qf the Marine Biological Association qf the United Kingdom (2000)

1614

~ 12S: 10~ 8:§ 6~ 4

2o

,l~ -.. :-.". ." ~..-I\

Ii '.~

ONDJFMAMJJASONDJFMAMJJASONDJ

1995 1996 1997C 14

E12'"":"10o

g 8~ 6~ 4>.o 2

o .ONDJFMAMJJASONDJFMAMJJASONDJ

1995 1996 1997

Figure 2. Monthly measurements of salinity and oxygenconcentrations at buoy 89 and 92 within the study area (forgeographic positions of the buoys, see Figure I).

Sediment characteristics (median grain size, mudcontent (percentage volume < 63 J1.m)) were determinedby laser diffraction with a Malvern Mastersizer S. Sixsediment types were distinguished, according to Krameret al. (1994). Sediment samples containing hard substrates(e.g. stones) were aH classified as type 7. Maximum ebband flood current velocities were estimated for an averagetide with the hydrodynamical model SCALDIS (van der

1Suhtidal macrohenthosin the mesohalineScheldeEstuary T. Ysebaert et al. 589

Table 1. Sediment types, hased on median grain size, oJ the suhtidal sampling locations in 1996 (N=54) and 1997 (N=73)respectively.

Sediment type Range (Jlm)

Type 1Type 2Type 3Type 4Type 5Type 6Type 7

cIaysiltvery fine sandfinesandmedium sandcoarse sandhard substrate

<22-63

63-125125-250250-500

500-1000

Table 2. Numher oJ ohservations (%), mean density (ind m -2) and mean hiomass (g AFD W m-2) oJ aU macrohenthic speciesohservedin thesuhtidal,mesohalinezoneoJtheZeescheldeEstuaryin 1996(N =54) and 1997(N = 73) respectively.

1996 1997

No. of samples % No. of samples 0/0

0 0.0 0 0.018 33.3 24 32.99 16.7 9 12.3

17 31.5 16 21.93 5.5 7 9.60 0.0 2 2.77 13.0 15 20.5

1996 1997

No. of No. ofobservations Density Biomass observations Density Biomass

(%) (indm-2) (g AFDWm-2) (%) (indm-2) (g AFDWm-2)

AnnelidaEteonelonga(P) 5.5 0.9 0.0004 * * *

Harmothoeimpar (P) 3.6 0.4 0.0004 1.4 0.1 0.0001

Heteromastusfilijormis(DF) 65.5 143.4 0.0575 32.9 74.4 0.0642

Marenzelleriaspp. (P) 1.8 0.4 - 1.4 0.3 *

Nereisdiversicolor(0) * * * 1.4 0.1 0.0001

Nereissuccinea(DF) 25.5 23.0 0.0492 26.0 22.2 0.0403

Oligochaeta (DF) 61.5 58.2 0.0015 50.7 72.3 0.0014

Polydoraligerica(SDF-SF) 34.5 479.6 0.0908 27.4 232.0 0.0501

Polydoraligni (SDF-SF) 23.6 47.0 0.0085 27.4 55.3 0.0077

Pygospioelegans(SDF-SF) 16.4 4.2 0.0002 15.0 6.0 0.0016

Spionidaespp. (SDF-SF) 1.8 0.2 - * * *

MolluscaBarneacandida(SF) 1.8 0.4 0.0040 * * *

Cerastoderma edule (SF) 1.8 0.2 0.0004 * * *

Crassostrea angulata (SF) 5.5 2.4 0.8432 * * *

Hydrobiaulvae(SDF) 3.6 0.4 0.0001 * * *

Macomabalthica(SDF-SF) 16.4 2.9 0.0267 16.4 3.3 0.0206

Mya arenaria(SF) 9.1 2.1 0.0037 4.1 1.2 0.0004

Mytilus edulis (SF) 7.3 1.0 0.0002 2.7 0.4 0.0006

Ostreaspp. (SF)* * * 2.7 0.4 0.1337

Petricolapholadijormis.(SF) * * 0.0004 1.4 0.4

Arthropoda fHathyporeiaelegans(SDF) 7.3 0.9 0.0002 1.4 0.1 0.0000

HathyporeiaPilosa (SDF) 31.0 23.4 0.0023 22.0 5.9 0.0004

Corophiuminsidiosum(SDF) 11.0 8.3 0.0005 13.7 5.7 0.0002

(.'orophiumlacustre (SDF) 14.5 15.2 0.0019 13.7 16.2 0.0016

(,'orophiumvolutator (SDF) 23.6 23.7 0.0049 32.9 38.4 0.0055

Crangoncrangon(P) 14.5 1.4 0.0517 15.1 1.8 0.1755

J';llrydicepulchra (P) 9.1 1.9 0.0015 9.6 1.0 0.0022

(;ammarussalinus (0) 1.8 0.2 0.0003 4.1 1.3 0.0011

.l1elitapalmata (SDF) 1.8 0.2 0.0004 1.4 0.3 0.0006

\JeJopodopsisslabberii (0) 3.6 0.4 0.0001 5.5 0.7 0.0000

\/'omYJisinteger(0) 1.8 0.2 * * *

I'a/aemonlongirostris(P) 3.6 0.5 0.0845 9.6 1.0 0.1241

/'/msymtesglaber (SDF) 12.7 4.8 0.0008 15.1 8.7 0.0011

I<hithropanopeusharrisii (P) 3.6 0.5 0.0186 9.6 1.3 0.0481

/la/anusspp. (SF) Present present

lIot lound; -, not determined.

I' 1/l11IJ!I!! theMarineBiologicalAssociationrif theUnitedKingdom(2000)

590 T. Ysebaert et al. Subtidal macrobenthosin the mesohalineScheldeEstuary

30

25

~ 20>-u~ 15::J

~ 10IJ..

5

o 1.-11..I."I.II.1t.II."I.~I..I. I- I- 1-.a1"1 I D, ,I Io 1 2 3 4 5 6 7 6 9 10 11 12 13 14 15 16 17

Number of species

7. ot '<:h. "'~7. , ~'/h. -'Q7. "b..cq, ~ ""tb ~oo 'tb

Density (ind m-2)

400- 35~ 30g 25~ 20~ 15IJ.. 10

5o

Biomass (9 AFDW m-2)

Figure 3. Species distribution (%), density distribution(%) and biomass distribution (%) ofthe 54 and 73 samplinglocations in 1996 and 1997 respectively.

Meulen & Sileon, 1997), having a spatial resolution oflOOm.

Data ana!Jsis

Macrobenthic species were classified into trophicgroups based on the food source: subsurface deposit-feeders (SSDF), surf ace deposit-feeders (SDF), suspension-feeders (SF), omnivores (0) and predators (P). Spionidspecies and Macoma balthica (Linnaeus) were classified asSDF -SF, as these species may switch between bothfeeding types.

The abundancefbiomass comparison method (ABC)(k-dominance curves for species abundance and biomass(Lambshead et al., 1983)) was used to detect environ-mental stress (Warwiek, 1986; Meire & Dereu, 1990).

To identify groups of similar locations the followinganalyses were performed on the density datasets of 1996,1997 and 1996-1997 together (fourth root transformed):a classification (clustering based on the Bray-Curtissimilarity index and group ave rage sorting (GAS)) (Clif-ford & Stephenson, 1975), an ordination (multi-dimensional sealing (MDS)) (Kruskal & Wish, 1978),

Journalof the Marine Biological Association of the United Kingdom (2000)

_ 1996.. 1997

Mollusca Arthropoda

Mollusca Arthropoda

Figure 4. Mean density (ind m -2) and mean biomass(g AFDWm-2) of Annelida, Mollusca and Arthropoda in1996 and 1997. The biomass of oysters is not included in themean total biomass of the Mollusca.

and a hybrid technique (two-way Indicator SpeciesAnalysis (TWINSPAN)) (Hill, 1979). Cut-levels usedwere 0, 2.0, 2.3, 2.7, 3.5, 4.5. Rare species (single observa-tion), the epibenthic shrimps Cr~ngon crangon (Linnaeus)and Palaemon longirostris (Milne-Edwards), empty samples(three in 1996, five in 1997) and samples with only oneindividual were excluded from the analyses. The relation-ship between the spatial distribution of the locations inthe MDS ordination and the environmental variables was

indicated by a Spearman rank order correlation betweenthe axes from the ordination and the environmental vari-

ables. The clusters, resulting from the multivariateanalyses, were characterized by their typical speciescomposition, diversity (Shannon - Wiener diversity index

H') and environmental variables. Statistical differencesfor biotic and abiotic variables among groups wereanalysed by Kruskal- Wallis test. Mean values are givenwith standard error (SE).

RESULTS

Abiotic characteri;::ation of the sampling locations

Water quality measurements at the two buoys in thestudyarea (Figure I) showed astrong seasonal pattern inwater temperature and smaller seasonal ftuctuations insalinity and oxygen concentrations, which were related tothe river run-off, being higher in winter (Figure 2). Thearea was mesohaline (yeadyaverage 1996: 10.5 psu; 1997:10.1psu) throughout the year (one exception in December1996). Oxygen concentrations were often less than 5 mg021-1, especially in summer.

50

l 40 . 1.19961

(;'30

11I1997

c:20

CTQ)u: 10

0

120011001000900

'" 800E 700"C 600g.?;> 500<ij 400c:<D 300a

200100

0Annelida

0,500,450,40

'" 0,35E

0,303:a 0,25u.oe(E! 0,20f/) 0,15f/)<0

0,10E0ffi 0,05

0,00Annelida

Subtidal macrobenthosin the mesohalineScheldeEstuary T. Ysebaert et al. 591

,................

....

__ abundancebiomass

10

Species rank

Figure 5. Combined k-dominance curves for speciesabundance and biomass (ABC-curve), based on aH samplinglocations (1996and 1997together).

Mean median grain size and mean mud content were141 ::1:19p.m and 38 ::1:4%respectively, both showing a largevariation. In both years the dominant sediment type was silt(Tabie 1); 5.5% in 1996 and 12% in 1997 belonged to thesediment types medium sand (250-500 p.m) and coarsesand (500-1000 p.m), hereafter considered together as thesediment type medium-coarse sand. Thirteen per cent in

1996 and 20.5% in 1997 of the samples were of sedimentswith hard substrates. Mud fraction slightly decreased andmedian grain size slightly increased with depth, but therewas no significant correlation with depth (median grainsize: Spearman r=O.l8; P=0.06 and mud fraction: r=O.l7;P=0.08; N =86).

Based on model ca1culations, mean maximum ebb andflood current velocities were 0.886 ::1:0.06m s-1 and

0.786 ::1:0.020m S-l (N =127) respectively. The modelca1culated current velocities lower then 0.20 m s -I at onlyth ree locations. Highest current velocities observed were1.23 and 1.16m s-1 under ebb and flood conditions respec-tively. No correlation was found between current veloci-ties and depth (N =127; r=O.l3; P=O.l6), nor betweencurrent velocities and median grain size (N =106; r=O.l3;P=0.20) or mud content (N =106; r= -0.12; P=0.22).

General characteristics of the macrobenthic fauna

Of the 35 species observed (28 in 1996; 24 in 1997),31% were annelids, 26% molluscs and 43% arthropods(Tabie 2). Only seven species occurred in more than 20%of the samples. The polychaete Heteromastus filijOrmis(Claparède) (65% of the samples in 1996, 33% in 1997)and Oligochaeta (61.5% in 1996, 50.7% in 1997) were

A MOS 1996-1997stress:0.147

....

x

B

~.

.

.

-

xx x

x

.. 88

x xx

.cluster 18 cluster 2Acluster 3X group4

MOS 1996-1997

stress: 0.147

/:;.

8

8

~ 88

8 8

8/:;.sdt

.vetyftne sand

. ftnesandxmedlum-coarse sand8 hardsubstmtes

Figure 6. Multi-dimensional sealing (MDS) ordination of species density data from 1996 and 1997 together: (A) clusters super-imposed on the ordination; (B) sediment types superimposed on the ordination.

]ournal qJ the Marine Biological Association qJ the United Kingdom (2000)

100

90

80

c: 70'"c:'Ë eo0"0

<ft.!50

. 40-1a;"3 30E .''"(.)

20

10

0

592 T. Ysebaert et al. Subtidal macrobenthosin the mesohalineScheldeEstuary

Table 3. Spearman rank order correlations between environmentalfactors (depth, mud content, median grain size) and the numberof species, biomass, density, and MDS x- and Y- coordinates. The Spearman rand the P-value are given. Significant correlationsatthe level P < 0.05 are in bold.

Depth (N=105)

r P

Number of speciesBiomass

DensityMDS X coordinates

MDS Y coordinates

-0.052-0.108

0.040.150.10

0.600.270.670.120.31

MDS, multi-dimensional sealing.

Mean biomass of cluster 2 with oysters included, without oysters mean biomass amounted to 1.40 :1:0.372 g AFDW m -2.

most common. Six species were observed only once. Thenumber of species per location was low (Figure 3); loca-tions with one or two species were most common (44%).

The mean total density of all locations was681 .xl7l ind m -2, the mean density in 1996 (861 :1:341ind m -2) was noticeably higher than in 1997 (549 .x158ind m-2), although not significantly (Mann-WhitneyU-test: N(1996)=54; N(1997)=73; U=I720; P=0.2227).Densities were dominated by annelids (87% of the totaldensity; 89% in 1996; 84% in 1997) (Tabie 2). Arthro-pods occurred to alesser extent and molluscs occurredonly in very low densities (Figure 4). Most locations had atotal density between 100-1000indm-2 in 1996 (42%)and between 10 and 100 ind m -2 in 1997 (44%) (Figure3). Highest densities observed were 17352 and 9286 indm -2 in 1996 and 1997 respectively.

The mean total biomass of alliocations was 0.94 .x0.35 gAFDW m -2. In 1996 mean biomass (1.26 .x0.75 gAFDW m -2) was higher than in 1997 (0.68 .x0.24 gAFDW m - 2), although not significantly (Mann - WhitneyU-test: N(1996)=54; N(1997)=73; U=19Il.5; P=O.77).The

Journalof the Marine Biological Association of the United Kingdom (2000)

difference in biomass was caused by the high biomass of afew oysters (Crassostreaangulata (Lamarck ) and Ostreaspp.)found at three and two sampling locations in 1996 and 1997respectively, making 67% oftotal biomass in 1996 and only20% of total biomass in 1997. If oysters were removed fromthe dataset, mean biomass ofboth years was more compar-abie (1996: 0.41 .xo.l3 g AFDW m -2, 1997: 0.55 .xO.l6 gAFDW m -2). Contrary to density, biomass was not onlydominated by annelids (1996: 50%; 1997: 30%), but also byarthropods (1996: 42%; 1997: 66%) (Figure 4). The domi-nant annelids were Polydora ligerica (Ferronière) and H.fili-Jormis; the dominant arthropods were CrangoncrangonandPalaemonlongirostris(Tabie 2). It should be emphasized thatthese arthropods were aUepibenthic species, and thereforedo not belong to the sedentary infauna. Most locations(55%) had a total biomass between 0.01 and I g AFDW m-2(Figure 3), with a maximum of 40 g AFDW m - 2 (a locationwith 12oysters) in 1996 and 15g AFDW m -2 in 1997.

The macrobenthic community was numerically domi-nated by SDF -SF species (59%), which were mainly thespionids Polydoraligerica and Polydoraligni (Webster). The

Mud fraction (N=86) Median grain size (N=86)

P r P

0.24 0.03 -0.14 0.20

0.05 0.63 0.001 0.990.30 0.005 -0.20 0.050.57 <0.0001 -0.41 <0.0001

-0.42 <0.0001 0.39 0.0002

Table 4. Biotic and abioticwcharacterization of the th ree clusters (mean .xSE), with indication of the test statistic (H) of theKruskal-Wallis test together with the P-levelfor differences among the th ree clusters.

Cluster 1 Cluster 2 Cluster 3 H P-Ievel

(N=23) (N=35) (N=31)

Total number of species 9 22 12

Mean number of species 2.3 :1:0.25 8.8 :1:0.56 2.9 :1:0.22 71.245 <0.0001

Shannon-Wiener diversity H' 0.53 :1:0.079 1.20 :1:0.097 0.69 :1:0.069 16.037 0.0003

Mean density (ind m-2) 86 :!:l8 2298 :1:613 248 :1:76 40.513 <0.0001

Mean biomass (g AFDW m-2) 0.02 :1:0.004 3.07 :1:1.343 0.25 :1:0.087 44.397 <0.0001

Indicator speciesBathyporeia pilosa 65 :1:13 0.6 :1:0.43 2.7 :1:1.81 68.873 <0.0001

Polydora ligerica 5.2 :1:4.36 1379 :1:571 0 58.779 <0.0001

H eteromastusfiliformis 2.4 :1:0.86 234 :I:143 170 :1:70 20.876 <0.0001

01igochaeta 6.3 :1:4.75 168 :1:56 54 :1:11 22.275 <0.0001

Mud content (%) 7.5 :1:3.38 48 :1:5.9 48 :1:4.1 22.509 <0.0001

Median grain size (*m) 215 :1:19 133 :1:41 76 :1:9 22.776 <0.0001

Depth 6.2 :1:1.1 6.3 :1:0.8 5.1 :1:0.8 0.827 0.661

Subtidal macrobenthosin the mesohalineScheldeEstuary T. Ysebaert et al. 593

A. Bathyporela pi/osa (Ind m")

o

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o

"e f) .~:.:.A . . ollil, : . . .':' .- :...:.\.,'....

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B. PoIydora tlgatica (Ind m")

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D. OlIgochaata (Ind m")

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,

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o (11)0 .~

'Oindm" o1-50lndm" 8S0-S00indm' .SOO-SOOOindm' 8>sooolndm"

Figure 7. Multi-dimensional scaling (MDS) configurationli'om Figure 6 with circles scaled in size to represent individualspecies density of: (A) Bathyporeia pilosa; (B) Polydora ligerica;(G) Heteromastusfiliformis; and (D) Oligochaeta.

other important group were SSDF with 29%, beingrepresented by H. filijörmis and Oligochaeta. Suspension-Iceders (oysters) dominated the biomass (47%), but when(hese few oysters were excluded predators dominated(55%), followed by SDF-SF (spionids) with 20%. Thepredators were mainly the epibenthic shrimps C. crangonand Palaemon longirostris, not being a permanent part ofIhe benthic infauna.

The k-dominance curves for species abundance andbiomass (besides oysters) (ABC-curves) showed a stressedpattern, as indicated by the abundance curve fallingabove the biomass curve (Figure 5). This means that thebenthic community was dominated by one or a few verysmall species and only a few larger species were present.

Community structure and environmental variables

The multivariate analyses did not produce a distinctionbetween the datasets of 1996 and 1997. Therefore the

}ournal rif the Marine Biological Association rif the United Kingdom (200())

H. filiformis3%

P. ligerica6%

Cluster 1Balhyporeiapilosa

Others9%

B. pi/osa75%

Mean density: 86 ind m.2

P.ligni7%

Cluster 2Polydora ligerica

H. filiformis10%

P. ligerica60%

Mean density: 2298 ind m.2

M ba/thic84%

H. filiformis69%

Cluster 3Heleromastus

filiformis

Oligochaeta22%

Others3%

Mean density: 248 ind m.2

Figure 8. Mean species density per cluster based ondensity data 1996 and 1997 together. For full species namessee Table 2.

further analysis and discus sion of community structure isbased on the data of both years together. Both TWIN-SPAN and cluster analyses produced three clusters, whichalso returned in the MDS ordination (Figure 6A). In theGAS-classification the first cluster (cluster I) was sepa-rated at a 15% similarity, the two remaining at a 35%similarity. Sixteen locations mutually showed very littlesimilarity and did not form a cluster. These locationswere considered as group 4 (rest group).

Neither macrobenthos species richness, density,biomass, nor one of the MDS-axes were significantlycorrelated with depth (Tabie 3). On the other hand, mudcontent was significantly correlated with macrobenthosspecies richness and density, being highest for the silt typesediment. Both axes of the MDS ordination were signifi-cantly correlated with mud content and median grainsize, indicating that the distribution of the samples in theMDS ordination was mainly determined by the sedimentparameters. The superimposed sediment types on the

594 T. Ysebaert et al. Subtidal macrobenthosin the mesohalineScheldeEstuary

ordination (Figure 6B) showed a clear tendency ofgrouping. Cluster I mostly occurred on fine sand sediment(70%), cluster 2 on silt (34%) and hard substrate (34%)sediments, and cluster 3 mainly on silt (58%) -very finesand (39%) sediments.

The ABC-curves for each cluster seperately showed asimilar stressed pattern as observed for all sampling loca-tions together (see Figure 5).

The abiotic and biotic characteristics of the three clus-

ters and the statistical difference among the clusters aresummarized in Table 4. Cluster I was characterized by aspecies-poor benthic fauna with a typical dominance ofthe amphipod BathyporeiaPilosa (Lindström) (Figures 7A& 8A). Cluster 2 consisted of locations with a relativelyspecies-rich benthic fauna with a high mean density andbiomass. The small polychaete Polydora ligerica was theindicator species (Figures 7B & 8B). Oysters occurredexclusively in this clustex;, eXplaining the relatively highbiomass. Cluster 3 was'" characterized by intermediatespecies richness, density and biomass. The indicatorspecies of this cluster were Heteromastus filifórmis andOligochaeta (Figures 7C,D & 8C). Macoma balthica, onlypresent in low densities, appeared almost exclusively incluster 3. Sediment characteristics were significantlydifferent among the th ree clusters, depth was not signifi-cantly different.

Of group 4, 37% of the locations were situated in thesilt sediment type, 30% on hard substrates, and theremaining locations in the other sediment types. Gener-ally the samples contained few species in low densities.Characteristically 57% of the locations of group 4 werefound in the depth stratum > 7.5 m, with a mean depth of9.5 :f:1.4m, which was noticeably deeper than the meandepth of the three clusters.

DISCUSSION

Species diversity along the salinity gradient in the Schelde Estuary

The most important variables controlling the occur-rence of benthic organisms on an estuarine scale are sali-nity and sediment characteristics (e.g. Wolff, 1973;Boesch, 1977; Holland et al., 1987; Rakocinski et al.,1997; Ysebaert et al., 1998), which are in turn determinedlargely by hydrodynamic conditions (e.g. Wildish &Kristmanson, 1979; Warwick & Uncles, 1980; Warwickct al., 1991; Hall, 1994). It is assumed that the environ-mental stress, due to salinity and hydrodynamic condi-tions, is greatest in the subtidal part of the middle anduppcr rcgions of estuaries, resulting in a lower diversity ofbcnthic invertcbrates predicted in these areas. The aim ofthis study was to investigate the macrobenthic commu-nit y or the subtidal mesohaline part of the ZeescheldeEst uary.

Scys ct al. (1999) recently investigated the benthosor the Zeeschcldc, but this study concentrated onOligochaeta, and there/ore was based on only onesmal! sediment core per sampling location (diameter3.5 cm). Only a Icw locations were situated within thesubtidal mesohaline part or the Zeeschelde Estuary. Apartfrom two Oligochaeta species found (Heterochaetacostata(Claparède) and 1übificoides heterochaetus (Michaelsen) ),

Journal if the Marine Biological Association if the United Kingdom (2000)

only four macrobenthic species were determined in theselocations: Polydora ligerica, Heteromastus filifórmis, Nereissuccinea (Frey & Leuckart) and Macoma balthica. Thedifferent sampling method and the small amount of loca-tions may explain the large difference in species numberas compared to this study.

The subtidal part of the Westerschelde was recentlystudied as part of a monitoring programme (e.g.Brummelhuis et al., 1997; Craeymeersch, 1999). For thesame period (autumn 1996-1997), 55 macrobenthicspecies were observed. Species diversity decreased fromthe polyhaline zone (40 species, 30 sampling locationseach year), over the poly-/mesohaline transition zone(31 species, idem) to the a-mesohaline zone (27 species,idem). In this study no further decrease in the number ofspecies was observed in the p-mesohaline partofthe estuary.Instead, species diversity slightly increased (35 species).The presence of sediments with hard substrates, oftenhaving a high macrobenthic species richness, mayaccount for this. Also, the sampling effort in this studywas larger as compared to the sampling effort in themonitoring program me of the Westerschelde. Whenconsidering the available data from this study for allsampling years (1990-1997), to increase the samplingeffort, about 100 taxa were found in the subtidal part ofthe Westerschelde. The number of species also decreasedfrom the polyhaline (70 species) towards the mesohalinezone (50 species). Therefore, the observed species diver-sity was also a function of sampling effort. Many specieswere reported to occur irregularly and rather acciden-tally, with in general very few species per sampling loca-tion, and this was also observed in th is study. On theother hand, species diversity 'hot spots' were sometimesobserved. In this study one sampling location represented17 macrobenthic species, half of the total number ofspecies observed.

Species diversity was reported to be much lower in theoligohaline zone of the Zeeschelde, characterized by animpoverished benthic fauna, with a few Oligochaetaspecies and very few macrobenthic species, such asP. ligerica and Corophium volutator (Pallas) (Ysebaert et al.,1993; Seys et al., 1999). In the subtidal freshwater tidal zonethe community was almost completely composed of afew Oligochaeta species (Seys et al., 1999). This very lowspecies diversity was eXplained by the heavy pollution inthe oligohaline and freshwater tidal zones of theZeeschelde.

The subtidal mesohaline part of the Zeeschelde wascharacterized by some typical 'genuine brackish-water'species, species which according to Remane (1969)showed a distribution strictly limited to the mixohalinezones without expansion into the marine or freshwaterregions (Wolff, 1973 ; Michaelis et al., 1992). In our studythe observed 'brackish-water' species are the polychaetePolydora ligerica, the amphipods Gammarus salinus(Spooner), Corophiuminsidiosum (Crawford) and C. lacustre(Vanhöffen), the shrimp Palaemon longirostris and the crabRhitropanopeus harrisii (Gould). The remaining specieswere euryhaline and also occurred in the wholeWesterschelde. The observation of Marenzelleria spp., animmigrant from North American shores (Bastrop et al.,1997; Essink & Schöttler, 1997), and for the first timereported to occur in Europe in 1982 (McLusky et al.,

Subtidal macrobenthosin the mesohalineScheldeEstuary T. Ysebaert et al. 595

1993), is the most southern observation of Marenzelleria todate (Ysebaert et al., 1996; Essink, 1999).

Subtidal vs intertidal macrobenthos

The observed species richness of the subtidal zone ofthe Zeeschelde was higher than that of the intertidalzone, the densities and biomass however were 10wer. In astudy from 1990-1996 on 24 intertidal locations withinthe study area, 24 species were found, five of which(G. volutator, Heteromastus filiformis, Nereis diversicolor(Müller1 Macoma balthica and Oligochaeta) contributed[0 96 % of mean densities and 99.3 % of mean biomass

(personal observations). The same five species were alsofound subtidally, but gene rally at much lower densities.Polydora ligerica, the most abundant species of thesubtidal zone of the Zeeschelde, was not found inter-tidally. Total mean intertidal densities were 7000:I:1060 ind m -2, being dominated by G. volutator (37%)and total intertidal mean biomass was 4.79 :1:0.34 gAFDW m -2, being dominated by N. diversicolor (40%).

Historicalcomparisonwith Leloup & Koniet;dw(1956)

The macrobenthos of the p-mesohaline part of theZeeschelde has been studied in 1952 on 21 subtidal loca-[ions in the same area of the Zee schelde (Leloup &Konietzko, 1956). At that time anthropogenic pressurewas lower but water quality was already bad. Thenumber of species in 1952 (15 species) was lower ascompared to this study (35 species), but sampling effortwas also lower. Eleven of the taxa were found in both

studies. Some recently very abundant species, like P. ligericaand H. filiformis, were totally absent in 1952. The subtidalmacrobenthic community in 1952 resembied cluster I ofthis study, being dominated by Bathyporeia pilosa, andshowing low mean densities (85 :l:24ind m-2). Commu-nities of cluster 2 and 3 were nearly absent. As shown in[his study, the occurrence of the community of cluster I isrelated to the presence of relatively coarse, sandy sedi-ments. In 1952, the sediment was indeed coarser ascompared with this study, as 70% of the sampling loca-[ions contained less than 5% of mud (fraction < 50 J1m,

determined by sieving).

Human impacts

The mesohaline subtidal zone of the Zee schelde is bynature characterized by a high degree of 'unstability',caused by large fluctuations in salinity, high current velo-cities and high turbidity, making an assessment of humanimpacts on the benthic communities difficult. Humanactivities, such as the discharge of waste and dredging ofsludge, are superimposed on these natural processes and,moreover, interfere with them. The combination offavourable hydrodynamic conditions, several finesuspended matter sources (including a large anthropo-genic part), and the flocculation process, leads in salinityzone 2-10 psu to bottom sediments that locally containhigh percentages of fine material (Baeyens et al., 1998).Being a major sedimentary environment, the shippingchannel is extensively dredged. The processes of sedimen-tation and resuspension, at least locally, are probably

Journal rif the Marine Biological Association rif the United Kingdom (2000)-

enhanced by these dredging operations, that increasedfrom 11million m3 dredged and 4 million m3 dumped inthe period 1951-1960 to 20 million m3 dredged and11million m3 dumped in 1981-1990 (j. Claessens,personal commmunication).

The fact that the subtidal zone of the Zeeschelde is a

highly stressed environment was in this study confirmedby the very low density and biomass of the macrobenthos,and the most common occurrence of H. filiformis and tubi-

ficid Oligochaeta, small, subsurface deposit-feeding,opportunistic species. It was also clear from the ABC-curves that the communities considered were under stress.

This provides st rong evidence that the communitiesremain in early succession, and indicates stress or distur-bance (e.g. Warwick, 1986; Gaston et aL, 1998). Theoccurrence of three different macrobenthic communities

in 1996-1997, two of which are typical for muddy sedi-ments (clusters 2 and 3), might be eXplained by a differ-ence in origin and magnitude of disturbance. A lesscommon, typically low-diversity community (cluster I)was found on more sandy sediments, being dominated bythe amphipod Bathyporeiapilosa, a well-adapted inhabitantof unstable, sandy sediments (Khayrallah & Jones, 1980).This community is characteristic for the mesohaline,subtidal part of the Schelde Estuary, at places where bynature tidal current speeds and instability of the (sandy)sediment become the limiting factors (Craeymeersh et al.,1999). It was also the only dominant community in 1952.

The dredging and dumping activities might have directeffects (being washed out, b~ing buried) on the occurrenceof macrobenthos. Seventy per cent of the samples taken at10cations where intensive dredging took place (Figure 1)belonged to cluster 3, dominated by the capitellid H.filiformisand tubificid Oligochaeta, which are known to be verytolerant to both physical and chemical (organic enrichment,anoxia) disturbance factors (Rakocinski et al., 1997; Gastonet al., 1998). Although most of the locations from cluster 2and 3 occurred in silty sediments, species characteristic forcluster 2 (e.g. Polydoraligerica) were almost completely absentat dredging and dumping sites.

In the study area also several 'hard substrates' wereconstructed (e.g. dams, dykes, rubbles) to suppresserosion, to conduct the streamflow and for safety reasons.In many places these constructions subsided, causing theoccurrence of stones and other similar hard substrates inthe river, next to natural1'substrates like peat and shells.Most of the sediments with hard substrates were charac-

terized by a high number of species and a relatively highdensity (cluster 2), although a lot of the samples takenwere incomplete. Hard substrates can form a suitablehabitat for several soft bottom species, as these substratesmight provide shelter and prohibit species being washedout from the sediment. Balanus spp., often found in

.several layers on these hard substrates, might provideshelter for other animais, or create a multitude of habitatsfor other species, even for soft bottom ones, when silt isdeposited in between (Dittmer, 1983). The hard substratesalso allowed the settlement of bivalves, like oysters. Thesesuspension-feeders could be considered an indication ofimproving water quality.

We are grateful for the financial assistance provided by theMinistry of the Flemish Community (AWZ) and for the

596 T. Ysebaert et al. Subtidal macrobenthosin the mesohalineScheldeEstuary

logistical support by Ir. Taverniers, Ir. Wouters and the crews ofthe 'Veereman'. Data on the model calculations for current

velocities were provided by Ir. Harm Verbeek (RWS-RIKZ)and Ir. Claessens provided data on the dredging anddumping activities in the Zeeschelde. We thank Nico DeRegge and Jan Soors for their support in the field and in thelaboratory.

REFERENCES

Baeyens W., Van Eck, B., Lambert, C., Wollast, R. & Goeyens,L., 1998. General description of the Scheldt Estuary.Hydrobiologia, 366, 1-14.

Bastrop, R., Röhner, M., Sturmbauer, C. & Jürss, K., 1997.Where did Marenzelleria spp. (Polychaeta: Spionidae) inEurope come from? Aquatic Ecology, 31, 119-136.

Boesch, D.F., 1977. A new look at the zonation of bent hos alongthe estuarine gradient. In Ecology of marine benthos (ed. B.C.

CoulI), pp. 245-266. ColUlpbia, South Carolina: UniversityofSouth Carolina Press, Columbia, Sou th Carolina. [The BelleW. Baruch Library in Marine Science, no. 6.]

Boesch, D.F. & Rosenberg, R., 1981. Response to stress inmarine benthic communities. In Stress e.fJèctson natural ecosystems

(ed. G.W. Barrett and R. Rosenberg), pp. 179-200. New Vork:John Wiley & Sons.

Brummelhuis, E., Craeymeersch, J, Markusse, R. &Sistermans, W., 1997. Het macrobenthos van de Westerschelde,de Oosterschelde, het Veerse meer en het Grevelingenmeer inhet najaar 1996. Rapport in het kader van het Biologisch MonitoringProgramma, NIOO-GEMO lérseke, 43 pp.

Claessens, J, Van Hoof, J & De Ruig, JH.M., 1991. Interactiemorfologie en baggerwerken. Water, 60, 182-189.

Clifford, H.T. & Stephenson, W., 1975. An introduction to numericalclassification.New Vork: Academic Press.

Costanza, R., Kemp, W.M. & Boynton, W.R., 1993.Predictability, scale, and biodiversity in coastal andestuarine ecosysems: implications for management. Ambio,22, 88-96.

Craeymeersch, JA., 1999. The use of macrobenthiccommunities in theevaluation of environmentalchange.PhD thesis, University of Gent,Belgium.

Diaz, RJ. & Rosenberg, R., 1995. Marine benthic hypoxia: areview of its ecological effects and the behavioural responsesof benthic macrofauna. Oceanographyand Marine Biology. AnnualReview, 33, 245-303.

Dittmer, J-D., 1983. The distribution of subtidal macrobenthosin the estuaries of the rivers Ems and Weser. In Ecology of theWadden Sea, vol. I (ed. W. Wolff), pp. 4{188-4{206.Rotterdam: AA. Balkema.

Essink, K, 1999. Dispersal and development of Marenzelleriaspp. (Polychaeta, Spionidae) in NW Europe and TheNetherlands. HelgoländerMeeresuntersuchungen,52, 367-372.

Essink, K & Schöttler, u., 1997. Studies on Marenzelleria spp.(Polychaeta: Spionidae). Aquatic Ecology,31, 117-258.

fèttweis, M., Sas, M. & Monbaliu, J, 1998. Seasonal, neap-spring and tidal variation of cohesive sediment concentrationin the Scheldt Estuary, Belgium. Estuarine, Goastal and SheifScience, 47,21-36.

Gaston, G.R., Rakocinski, C.F., Brown, S.S. & Cleveland,C. M., 1998. Trophic function in estuaries: response of macro-bcnthos to natural and contaminant gradiems. Marine andFreshwater Research,49, 833 -846.

Gray, ].S., 1997. Marine biodivcrsity: patterns, threats andeonscrvation nccds. Biodiver.rityand Gon.rervation,6, 153-175.

Hall, SJ., 1994. Physical disturbancc and marine benthiccommunities: lifc in unconsolidated sedimcnts. Oceanographyand Marine Biology. Annual Review, 32, 179-239.

Journal rif the Marine Biotogicat Association rif the United Kingdom (2000)

Hili, M.O., 1979. TWINSPAN: a Fortranprogramjór arranging multi-variate data in an ordered two-way table by classification of theindividuals and attributes. New Vork: Section of Ecology andSystematics, Cornell University.

Holland, A.F., Sbaughnessy, AT. & Hiegel, M.H., 1987. Long-term variation in mesohaline Chesapeake Bay macrobenthos:spatial and temporal patterns. Estuaries, 10, 227-245.

Khayrallah, N.H. & Jones, A.M., 1980. The ecology ofBathyporeia pilosa (Amphipoda: Haustoriidae) in the Tayestuary. Il. Factors affecting the microdistribution. Proceedingsof the Royal Society of Edinburgh B,78, 121-130.

Kramer, KJM., Brockmann, U.H. & Warwick, R.M., 1994.Tidal estuaries. Manual of sampling and analYtical procedures.Rotterdam: AA Balkema.

Kruskal, JB. & Wish, M., 1978. Multidimensional scaling. BcverlyHills: Sage Publications.

Lambshead, P.JD., Platt H.M. & Shaw, KM., 1983. The detec-tion of differences among assemblages of marine benthicspecies based on an assessment of dominance and diversity.Journalof Natural History, 17,859-874.

Leloup, E. & Konietzko, B., 1956. Recherches biomogiques surles eaux saumatres dus Bas-Escaut. Verhandelingen van hetKoninklijk Belgisch Instituut voor Natuurwetenschappen, no. 132,100 pp.

McLusky, D.S., Huil, S.C., Elliot, M., 1993. Variations in theintertidal and subtidal macrofauna and sediments along asalinity gradient in the upper Forth Estuary. .NetherlandsJournalof Aquatic Ecology,27, 101-109.

Meire, P.M. & Dereu, ]., 1990. Use of the Abundance{Biomass Comparison method for detecting environmentalstress: some considerations based on intertidal macrozoo-

benthos and bird communities. Journalof Applied Ecology, 27,210-223.

Meulen, A. van der, & Sileon, M., 1997. Overzicht vanmodellen in gebruik bij het RIKZ en het RI ZARijkswaterstaat, Rapport RIK?-97.008, 109 pp.

Michaelis, H., Fock, H., Grotjahn, M. & Post, D., 1992. Thestatus of intertidal zoobenthic brackish-water species in estu-aries of the German Bight. .NetherlandsJournal of Sea Research,20, 201-207.

Pearson, T.H. & Rosenberg, R., 1978. Macrobenthic successionin relation to organic enrichment and pollution of the marineenvironment. Oceanographyand Marine Biology. Annual Review,16,229-311.

Rakocinski, C.F., Brown, S.S., Gaston, G.R., Heard, R.W.,Walker, W.W. & Summers, JK, 1997. Macrobenthicresponses to natural and contaminant-related gradients innorthern Gulf of Mexico estuaries. Ecological Applications, 7,1278-1298.

Remane, A., 1969. Wie erken nt man eme genmneBrackwasserart? Limnologica, 7, 9-21.

Seys, J, Vincx, M. & Meire, P., 1999. Spatial distribution ofOligochaeta in the tidal freshwater and brackish parts of theSchelde Estuary (Belgium). Hydrobiologia,406, 119-132.

Soetaert, K. & Herman, P.M.J, 1995a. Carbon flows in theWesterschelde Estuary (The Netherlands) evaluated by meansofan ecosystem model (MOSES). Hydrobiologia, 311, 247-266.

Soetaert, K. & Herman, P.M.J, 1995b. Estimating estuarineresidence times in the Westerschelde (The Netherlands) usinga box model with fixed dispersion coefficients. Hydrobiologia,311, 215-224.

Van Damme, S., Meire, P., Maeckelberghe, H., Verdievel, M.,Bourgoing, L., Taverniers, E., Ysebaert, T. & WatteI, G., 1995.De waterkwaliteit van de Zeeschelde: evolutie in de voorbijedertig jaar. Water, 85, 244-256.

Van Eck, G.T.M., De Bruijckere, F.L.G., De Meyer, E. &Maeckelberghe, H., 1998. Naar een Schone Schelde. f'Vtzter,102, 293-303.

Subtidal macrobenthosin the mesohalineScheldeEstuary T. Ysebaert et al. 597

Van Eck, G.T.M. & De Rooij, N.M., 1993. Potential chemicaltime bombs in the Schelde Estuary. Land Degradation andRehabilitation, 4, 317-332.

Warwick, R.M., 1986. A new method for detecting pollutioneffects on marine macrobenthic communities. Marine Biology,92, 557-562.

Warwick, R.M. & Clark, K.R., 1993. Comparing the severity ofdisturbance: a meta-analysis of marine macrobenthic commu-nity data. Marine Ecology ProgressSeries, 92, 221-231.

Warwick, R.M., Goss-Custard, j.D., Kirby, R., George, C.L.,Pope, N.D. & Rowden, A.A., 1991. Statie and dynamicenvironmental factors determining the community structureof estuarine macrobenthos in SW Britain: why is the SevernEstuary different? Journalof Applied Ecology,28, 329-345.

Warwick, R.M. & Uncles, R.j., 1980. Distribution of benthicmacrofauna associations in the Bristol Channel in relation to

tidal stress. Marine EcologyProgressSeries, 3, 97-103.Wildish, DJ. & Kristmanson, D.D., 1979. Tidal energy and

sublittoral macrobenthic animals in estuaries. Journal of theFisheriesResearchBoard of Canada, 6, 1197-1206.

" 11111,,10/ the Marine Biological Association I!! the United Kingdom (2000)

Wolff, W.j., 1973. The estuary as a habitat. ZoologischeVerhandelingenLeiden, no. 126, 242 pp.

Ysebaert, T., Meire, P., Coosen, j. & Essink, K., 1998. Zonationof intertidal macrobenthos in the estuaries of Schelde and

Ems. Aquatic Ecology,32, 53-71.Ysebaert, T., Meire, P., De Block, M., De Regge, N. & Soors, j.,

1996. First record of Maren;:,elleria viridis (Verril, 1873)(Polychaeta, Spionidae) in the Schelde Estuary (Belgium).Biologischjaarboek Dodonea, 64, 176-181.

Ysebaert, T., Meire, P., Maes, D. & Buijs, j., 1993. The benthicmacrofauna along the estuarine gradient of the ScheldeEstuary. MtherlandsJournal of Aquatic Ecology, 27, 327-341.

Zwolsman, j.j.G., 1999. Geochemistry of trace metals in theScheldt Estuary. Geologica Ultraiectina, Mededelingen van deFaculteit Aardwetenschappen, Universiteit Utrecht, no. 17l, 183 pp.

Submitted 1 November 1999. Accepted 30 MaTCh 2000.

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