7/29/2019 114130

1/9

Estuarine, Coastal and Shelf Science(1998) 47, 143151Article No. ec980350

Seasonal Patterns in the Fish and CrustaceanCommunity of a Turbid Temperate Estuary

(Zeeschelde Estuary, Belgium)J. Maes, A. Taillieu, P. A. Van Damme, K. Cottenie and F. Ollevier

K atholieke Universiteit L euven, Zoological I nsti tute, L aboratory of Ecology and A quaculture, N aamsestraat 59,

B- 3000 L euven, Belgium

Received 4 M arch 1997 and accepted in revised form 17 February 1998

Fish and crustaceans were sampled for 1 year in theupper reaches of a temperateestuary characterized by high turbidityand a tidal range of up to 5 m. Samples were taken in the cooling-water circuit of the Doel Nuclear Power station(Zeeschelde, Belgium). Between July 1994 and June1995, 55 fish species, two shrimp species and four crab species wererecorded. T he fish community was composed of 36 marine species, 16 freshwater species and three diadromous species.Shrimps, Gobiidae and Clupeidaedominated thesamplesboth in numbers and biomass. An exceptionally clear seasonalsuccession was observed in the species composition. It is argued that young fish and crustaceans use the highly turbidZeeschelde Estuary as a refuge from predators. 1998 Academic Press

Keywords: estuaries; species composition; temporal variation; fish catches; Crustacea; cooling water; power plants;Belgium

Introduction

Communities of fish and crustaceans inhabitingestuaries represent a combination of freshwater and

marine species both living at the edge of their distri-bution, estuarine resident and migrating species pass-ing the estuary on their way to the spawning grounds(Claridge et al., 1986; Wheeler, 1988; Day et al.,1989; Potter et al., 1990; Potter et al., 1997). Thespatial organization of estuarine species communitiesis highly correlated with salinity and substratum type(Henderson, 1989; Hamerlynck et al., 1993). Thetemporal structure is often the result of seasonalmigrations of young fish and crustaceans movingbetween coast and adjacent estuaries (M cLusky,1989; Robertson & Duke, 1990b). M ost speciesspawn in deeper offshorewaters which may befavour-able for egg survival and dispersion (Blaber, 1997).After hatching, larvae are drifted to the coastal andestuarine nurseries where they become mobile andthen migrate to shallow and turbid areas using thetides as a means of transport (M cLusky, 1989; Daanet al., 1990). For temperate estuaries, this pattern ofmovements results in consecutive migration waves ofjuveniles of marine fish, crabs and shrimps (Wharfeet al., 1984; Claridgeet al., 1986; Pomfret et al., 1991;Potter et al., 1997). In tropical estuaries, seasonality inspecies communities is less apparent (Day et al., 1989;

L arocheet al., 1997) and sometimes masked by largevariances in catch data (Robertson & Duke, 1990a).It has, however, been widely recognized that bothtemperate and tropical estuaries and inshore areas act

as nurseries as they provide almost unlimited foodresources (Day et al., 1989) and offer shelter frompredators (Cyrus & Blaber, 1992; Ruiz et al., 1993).

Seasonal changes in the structure of the fish andcrustacean communities in a highly turbid temperateestuary [Zeeschelde Estuary, Belgium (Figure 1)] arethe focus of this study. T herefore, sampling wasconducted for 1 year in a power station cooling-waterinlet providing a wealth of regular data. T his alterna-tive fishing technique was most convenient in an areawhere trawling and netting are difficult because ofextreme tides, heavy shipping and harbour activities,and unexpected weather conditions. T he nature of

these migrations is further discussed by questioningwhether or not the upper reaches of the Zeescheldeare a nursery area offering enhanced protection.

Material and methods

Sampling site and sampling regime

T helower ScheldeEstuary(Westerschelde) is situatedbetween the BelgianDutch border and the North Sea(Figure 1) and has a complex morphology of gullies,

02727714/98/020143+09 $30.00/0 1998 Academic Press

7/29/2019 114130

2/9

sandflats and channels (Claessens, 1988). T he upperestuary (Zeeschelde) (Figure 1) consists of freshwaterbetween Gent and Antwerp and brackish water be-tween Antwerp and theD utchBelgianborder (Figure1). T he mean freshwater discharge is 105 m3 s1

(Heip, 1988). M ean tidal range at Doel is 485 m(Claessens, 1988).

Samples of fish, shrimps and crabs were collectedsemi-weekly from the cooling-water intake screens ofthe Nuclear Power Plant Doel, located in the brackishpart of the Zeeschelde (Figure 1). Samplingstarted inJuly 1994 and finished in June 1995. T he cooling-water intake is situated 2 m above the bottom andwithdraws251 m3 s1 water correspondingto 035%of thelocal Zeescheldeflow. Sincethemesh sizeof theintake screens is 4 mm, neither larvae nor smallercrustaceans such as M ysidacae could be sampled.Approximately 8106 m3 cooling water was moni-tored in 135 samples.

Fish and crustaceans were separated from debris,identified to species level, counted, measured andpreserved in 7% formaldehyde. T he genus Pomato-schistus was identified according to Hamerlynck(1990). Subsamples were taken for large catches offish or crustaceans by dividing the total catch in equalparts. For each species, biomass (ashfree dry weight)was calculated using length-biomass regressions(H ostens & Hamerlynck, unpubl.; M aes, unpubl.).

During sampling the following environmental vari-ables were measured using a water quality multiprobelogger (H ydrolab, Datasonde 3): temperature, C;

salinity; dissolved oxygen concentration, mgl1; andturbidity, NT U.

Data analysis

Abundancedata (numbers103 m3 cooling-watersampled) and biomass data (g AD W103 m3

cooling-water sampled) were rootroot transformedprior to statistical analysis (Field et al., 1982). T o studythetemporal community structure, correlation biplots,based on principal component analysis (PCA), wereused to project n-dimensional data in two-dimensions(T er Braak, 1994). Variables (species) are representedas species vectors; samples as points. T he species vec-tors are pointing towards samples when reaching theirmaximum abundanceor biomass. Eigenvaluesindicatethe amount of variability expressed by each principalcomponent.

Results

Environmental data

M inimum and maximum temperatures recorded inthe Zeeschelde ranged from 49 C in February to248 C in August. M ean salinity and oxygen con-centrations were 799 and 459 mg l1, respectively.M aximum salinities were measured in summer andminimum salinities in winter. T he oxygen concen-tration showed an opposite pattern with maxima inwinter and minima in summer when the oxygenconcentration dropped just below 2 mg l1. Secchi

5120'

5100'N

5110'

420'E400'340'

Westerschelde

NScheldeEs tua r y

TheNetherlands

Belgium

France

Germany

Gent

DoelAntwerp

Zeeschelde

Belgian-DutchBorder

0 5 20 km

North Sea

F 1. A map showing the Zeeschelde Estuary (Belgium) and the location at which fish and crustaceans were sampled(N uclear Power Plant Doel).

144 J. Maes et al .

7/29/2019 114130

3/9

disc depths were on average 196 cm and neverexceeded 48 cm. M ean turbidity was 165 NT U.

Species number and composition

In total, 55 fish species and six crustacean specieswere caught. Of the fish species, 36 were marinemigrants and 16 species typically occur in fresh water(T able 1). Both groups included species that spendpart of the life in estuaries as well as species occasion-ally entering estuaries. None of the species werestrictly estuarine dependent i.e. they can spawn andmature in either fully marineor in freshwater environ-ments. A nguilla anguilla was the only catadromousspecies while L ampetra fluv iatili s and Alosa fallax areanadromous (T able 1). Crustaceans caught at Doelincluded two shrimp species and four crab species(T able 2). It was noted that except for Carcinusmaenasall crab species wereexotics. A livingspecimenof thebluecrab Callinectessapiduswasrecorded for thefirst time in Belgium.

A bundance and biomass data

In terms of numbers, eight species made up >95% ofthetotal catches. T hemost abundant species were theshrimps Palaemonetes var ians (374%) and Crangoncrangon (298%). T he most numerous fish specieswere gobies [Pomatoschistus microps (126%), P.minutus (78%) and P. lozanoi (10%)], Clupeidae

[Clupea harengus(64%) and Sprattus sprattus(17%)]and the pipefish Syngnathus rostellatus (25%). Interms of biomass the same species, with addition ofDicentrarchus labrax and Pleuronectes flesus, dominatedthe community; C. harengus, 292%; P. varians,180%; P. minutus, 177%; C. crangon, 106%; S.sprattus, 75%; and P. microps, 50%); D. labrax, 45%;P. flesus, 19%; and S. rostellatus, 10%.

Seasonal community structure

T he seasonal changes in the community of fish and

crustaceans were analysed using correlations biplotsbased on PC A. Principal component analysis withabundancedata yielded thesame information as PC Abased on biomass data. T hereforeonly thecorrelationbiplot with biomass data is shown in Figure 2. T hetotal amount of variability explained by the first twoeigenvalues corresponding to the first two principalcomponents was 455%. Only species representing>01% of the total catches were included in theanalysis. Including morespecies onlyaffected thetotalvariability expressed by the eigenvalues but did notchange community structure.

T he analysis placed all samples on a circle [Figure2(a)]. Samples taken in the same month were closelylocated to each other in the biplot and arranged in aclear seasonal succession [Figure2(b)]. Fivegroups ofspecies were more or less separated by the analysis:

Group A [Rhithropanopeus harrisii] comprised onlyone species, an exotic crab species which has recentlysettled in the Zeeschelde.

Group B [C. maenas, S. rostellat us, C. crangon]occurring mainly in late summer and early fall(August, September) when temperature and salinitywere both high.

Group C [P. minutus, P. lozanoi, P. microps] scoringhighest biomass in fall (October, November).

Group D [D . labrax, C. harengus, S. sprattus] ofwhich most individuals were caught in December.High numbers of larvae of both Clupeidae reachedthe Zeeschelde starting from M ay but were notquantified.

Group E [Liza ramada, L . fluv iati li s, Gasterosteusaculeatus, Pleur onectes flesus] with species mainly sam-pled in winter and early spring (January, February,M arch, April) when high oxygen concentrations wererecorded. In this period, numbers of freshwaterspecies caught at D oel were relatively high. Not onlyG. aculeatus, but also Rhoedeus seri ceus, Gymnocephaluscernuus and Abramis brama took advantage of de-creased salinities during winter and early spring.

T heperiod between M arch and Junewas character-ized by low abundance and biomass. T hree species

namely A. anguilla, Sti zostedion lucioperca and P.varians were poorly represented by the analysis andcould therefore not be placed in a species set. T heproper reconstruction ofP. varianswas obstructed bytwo abundance maxima (April and August). Anguillaanguilla and S. lucioperca are present throughout theyear with no marked abundance maximum.

T he dominant species reached maximum abun-dance in the following chronological order startingfrom July: (1) Young of C. maenas; (2) Young ofP. v arians; (3) S. rostellatus; (4) Y oung ofC. crangon;(5) Young of P. microps; (6) Young of P. lozanoi;

(7) Young of P. minutus; (8) Juvenile C. harengus;(9) Juvenile S. sprattus; (10) Recently metamorphosedL . fluviati li s; (11) P. flesus; (12) Spring stock ofP. v arians.

Discussion

Sampling method

Sampling in power station cooling-water inlets hasbeen successfully used to study fish and crustaceanfaunas of temperate estuaries and coasts (Van den

Structure of an estuarine fish and crustacean community 145

7/29/2019 114130

4/9

T 1. Species list, mean abundance (numbers103 m3 cooling-water sampled) andstandard deviation (SD) of fish sampled in thecooling-water of the Nuclear Power Plant Doel overthe period July 1994June 1995

Scientific name Common name M ean SD

Anadromous speciesL ampetra fluv iati li s(L .) River lamprey 006 014A losa fallax (L acepede, 1803) T waite shad

7/29/2019 114130

5/9

Broek, 1979; Hadderingh et al ., 1983; Wharfeet al., 1984; Claridge et al., 1986; T urnpenny, 1988;Henderson, 1989). T his method offers a useful meansto obtain regular, quantitative samples, irrespectiveofweather conditions. T he inlet is a fixed point in thewater column accelerating fish that are near or almostupon the intake into the openings. Unlike beamtrawling, power stations sample pelagic, demersal andbenthic species as they are a pitfall for organismswalking over the substrate and a suction trap forswimmers (Henderson et al., 1992). Since larger fishprobably escape from the apertures, the methodis designed for smaller fish species and juveniles.Although specimens >50 cm of S. lucioperca andA. anguilla have been captured at Doel, the quanti-tative estimate of their abundance as well as of the

abundance of larger Salmonidae and C lupeidae suchas the anadromous A. fallax may be biased. It ishowever unlikely that thecommunity structure wouldhave been affected by the presumed absence of largeindividuals in this data since juveniles form a greaterpart of estuarine fish communities (D ay et al., 1989).

Species number

Henderson (1989) observed a linear relationship be-tween species number and latitude based on cooling-water intake data of seven English coastal power

plants. In addition, the species number generallydeclined in estuaries with declining salinities. Withrespect to latitude and mean salinity of the presentsampling area the maximum expected number of fishspecies is close to 60. Sampling at Doel yielded 55species indicating that almost all species occurringin the Zeeschelde are caught. T he capture of L .fluviat i lis, Osmerus eperlanus and A. fallax is note-worthy, sincethey are indicatorsof good water quality(Hamerlynck et al., 1993). D uring the late 1980s, theZeeschelde Estuary was heavily affected by domesticand industrial wastewater (Van Eck et al., 1991), but

water quality is gradually improving (Van Dammeet al., 1995). T he authors thus expect increasingnumbers of these species for the near future.

Seasonal structure of the fish and crustacean community

Principal component analysis on the sampling datashowed an exceptionally clear annual pattern resultingin well-defined temporal changes in the species com-position. Y oung of Decapoda and pipefish arrive insummer, followed byjuvenile Gobiidae in latefall andO-group Clupeidae in early winter. T here has beenextensive literature published on temporal fish distri-bution of northern temperateestuaries(Iglesias, 1981;Evans & T almark, 1984; Claridge et al., 1986; Costa,1988; Dayet al., 1989; Henderson, 1989; Elliott et al.,

1990; Potter et al., 1997). T he observed changes intemporal fish distribution are likely to be caused byseasonal migrations of marine fish into the brackish-water area and have been related to reproductioncycle, to variations in temperature and salinity, tofood availability and to reduced predation pressure(M cLusky, 1989; Blaber, 1997).

M any fish species complete their life cycle in tropi-cal and subtropical estuaries (Blaber et al., 1989;Robertson & Duke, 1990a), but there is less evidencethey do so in temporal regions (Claridge et al., 1986;Potter et al., 1990). Although Elliott and Dewailly

(1995) listed 27 species out of 186 occurring in 16European estuaries as estuarine dependent, almostall species can mature and spawn at sea. EvidentlyEuropean temperate estuaries are not critical to thesurvival of their visitors, except for diadromousspecies such as A. anguilla and Salmonidae andanadromous Clupeidae.

Abiotic water conditions (salinity and temperature)are often evoked as controls for seasonal patterns ofspeciesoccurrence(T hiel et al., 1995). Although a fewenvironmental variables were measured during thisstudy, correlationswith seasonal fish distribution were

T 2. Species list, mean abundance (numbers103 m3 cooling-water sampled) andstandard deviation (SD ) of crustaceans sampled in the cooling-water of the Nuclear Power PlantDoel over the period July 1994June 1995

Scientific name Common name M ean SD

Crangon crangon (L inneaus, 1758) C ommon shrimp 17532 38373Palaemonetes varians(Leach, 1814) Palaemonid shrimp 21988 33305Eriocheir sinensis(H. M ilne Edwards, 1854) Chinese mitten crab

7/29/2019 114130

6/9

not made because they are trivial. Euryhalinity is aprecondition for estuarine visitors and inhabitants(Blaber, 1997) while temperature is probably relevantwhen it reaches extreme values.

Increased estuarine productivity and food resourcesare linked with immigration of marine juveniles andtherole of estuariesas nursery areas is documented ingreat detail (Haedrich, 1983; Boddeke et al., 1986;

Elliott et al., 1990; Blaber et al., 1995). However,mechanisms to find these nursery areas are poorlyunderstood (Day et al., 1989). Indeed, juveniles ofmany species are probably not attracted to estuarinenursery as such but to shallow and turbid areas ingeneral (Blaber & Blaber, 1980). M obile fish andcrustaceans appear to use these waters as a refugefrom marine predators. It is experimentally proven

3

2.5

2.5

2

Principal component I

PrincipalcomponentII

1.5

0.5

0.5

1.5

1 0 1 2

(b)

3.5

2.5

1.5

0.5

0.5

1.5

(a )

L. ramada

L. f luv ia t i l i s

G. aculeatus

P. flesus

Group E

Gr oup D

S. sprattu s

C. harengus

D. labrax

P. varian sP. mi crops

P. lozan oi

P. min utus

Group C

C. cra ngon

S. rostell atus

C. maenas

Gr oup B

R. harr is i i

Gr oup A

A. angui l l a

S. luci operca

2.5

+

++

++

+

+

+

++++

+

+

++

+

+

++

++++++

+

++

++

+++

++++++

+

++

+

+

+

+

+

+ +++

++

+ +++

+++

+++

++

+

+ ++++++

+++

+++

++

++

+

++

++

++

++

+ +++

++

+

+

+

+

++

+++

+

+

+

+

+

+ +

+

+

December

J uly

March

February

AprilNovember

Ma y

J anua ry

September

October

August

J une

F 2. Correlation biplot based on principal component analysis. Position of thesamplescores (a) and thespecies vectors(b) with respect to first two principal components. For a better interpretation of thebiplot thesample scores are grouped bymonth and the species scores are multiplied by three.R. harrisii, Rhit hropanopeus harri sii; C. maenas, Carcinus maenas; S. rostellant us, Syngnathus rostellatu s; C. crangon, Crangoncrangon; P. minutus, Pomatoschistus minutus; P. lozanoi, Pomatoschistus lozanoi; P. microps, Pomatoschistus microps; D. labrax,

Dicentrarchuslabrax;

C. harengus,

Clupea harengus;

S. sprattus;

Sprattussprattus;

L. ramada,

L iza ramada;

L . fluv iat i li s,

L ampetrafluviat i lis; G. aculeatus, Gasterosteus aculeatus; P. flesus, Pleur onectes flesus; P. varians, Palaemonetes vari ans; A. anguilla, Anguillaanguilla; S. lucioperca, Sti zostedion lucioperca.

148 J. Maes et al .

7/29/2019 114130

7/9

that animals reduce or eliminate their anti-predatorbehaviour under turbid conditions (Abrahams &K attenfeld, 1997). Since this behaviour is costly, as itpreventsfish from matingand foraging, a reduction inanti-predator behaviour should have a compensatory

increase in feeding rates (Abrahams & K attenfeld,1997). It has thus been postulated that turbiditygradients existing between the sea and the adjacentestuaries, act as one of the orientation cues forjuveniles migrating into estuaries (Blaber, 1997).

T he number of studies on the effects of turbidity onbrackish water and marine species is rather limited.T he most detailed studies to date on estuarine fishdistribution and turbidity have been conducted inSouth African and Australian estuaries (Blaber &Blaber, 1980; Cyrus & Blaber, 1992; Blaber, 1997).Evidence was presented that juveniles occurring inestuaries occupy different turbidity ranges from thoseof adults and it was concluded that the influence ofhigh turbidity on fish may be linked to reducedpredation pressure. Visual predatorswere found to bemoreaffected by turbid water than weremacrobenthicspecies (Hecht & van der L ingen, 1992).

T he observed migration sequence of juvenile crus-taceansand fish in these data, match moreor less withchanges in the diet of Gadidae, their major predatorsin theadjoining coastal area (Hamerlynck & H ostens,1993). After feeding on copepods in M ay and June,the fraction of gobies and shrimps in the diet of mostGadidae increases (H amerlynck & Hostens, 1993;

Salvanes & Jarle, 1993). With increasing length of theGadidae, the fraction of gobies in the diet decreasedand the fraction of larger fish including C lupeidaeand juvenile Gadidae increased (Hyslop et al., 1991;Henderson et a l ., 1992). In the highly turbidZeeschelde estuary, numbers of M erlangius merlangus,Gadus morhua and T ri sopterus luscus are unusuallysmall relative to their prey, both in cooling-watersamples and in additional fyke catches (M aes et al.,1997). T his suggeststhat theZeeschelde is avoided bylargenumbers of piscivores and may act as a refugeforprey species.

In the absence of submerged aquatic vegetation orturbid estuarine areas P. minutus, C. crangon andyoung Pleur onectes pl atessa search for shelter in theshallow littoral zone during their juvenile phase(Evans, 1983). T hese areas are avoided by largepredators probably because of their decreased forag-ing ability and their increased physiological stress(Ruiz et al., 1993).

Seasonal changes in tropical species communitiesare often very complex and determined by their dif-ferent breeding patterns (Davis, 1988). T hecomplex-ity of fish movements in the subtropics and tropics

may be enhanced by an increased spatial habitatheterogeneity relative to temperate regions (Blaber &M ilton, 1990, Robertson & Duke, 1990b). Besidesturbid areas and shallows, mangroves, coral reefs andseagrass beds contribute to the protection of young

fish and crustaceans from their predators (Bell et al.,1984; Wright, 1986).

T hough temperate zones differ from tropicalregions in habitat diversity, their species apparentlyexhibit similar patterns of behaviour. Unless they arestarved, juveniles and adults of small species evidentlyavoid larger predators whenever possible and prefer anutritively-poor habitat without predatorsover afood-rich habitat in the presence of predators (Werneret al., 1983; M anhagen, 1988; Schlosser, 1988;Abrahams & K attenfeld, 1997.

T he authors thus hypothesise that the observedseasonal structurein thesedatais likely to betheresultof behavioural responses to changed predation risk.T his behaviour is possibly size-related. Once the preyreaches a vulnerable size relative to the predator, anincreased number of attacks upon the prey might bethe stimulus to start migration towards protectedareas. Consequently emigration to deeper and lessturbid waters, when joining the adult stock, shouldstart with larger, more mature animals. T he chanceto detect and escape from a predator is size-related(T aylor, 1984), resulting in a prolonged stay ofyounger individuals in the protected habitats.

Acknowledgements

T he authors are grateful to Els T hoelen and FonsWillemsen at Doel Power Station, to Gaston Janssensfor technical support and to all students who assistedwith fieldwork. T he authors thank Peter Smith, FilipVolkaert and Gonda Geets for their critical com-ments. T his study was financed by the Nuclear PowerStation Doel.

References

Abrahams, M . & K attenfeld, M . 1997 T he role of turbidity as aconstraint on predator-preyinteractions in aquatic environments.Behaviour Ecology and Sociobiology 40, 169174.

Bell, J. D., Pollard, D. A., Burchmore, J. J., Pease, B. C. &M iddleton, M . J. 1984 Structure of a fish community in atemperatetidal mangrovecreek in Botany bay, New SouthWales.Australian Journal of M arine and Freshwater Research 35, 3346.

Blaber, S. J. M . 1997 Fish and Fisheries of Tropical Estuaries.Chapman & Hall, L ondon. 367 pp.

Blaber, S. J. M . & Blaber, T . G. 1980 Factors affecting thedistribution of juvenile estuarine and inshorefish. Journal of FishBiology 17, 143162.

Blaber, S. J. M . & M ilton, D. A. 1990 Species composition,community structureand zoogeography of fishes of mangroves inthe Solomon Islands. M ari ne Bi ology105, 259268.

Structure of an estuarine fish and crustacean community 149

7/29/2019 114130

8/9

Blaber, S. J. M ., Brewer, D. T . & Salini, J. P. 1989 Speciescomposition and biomasses of fishes in different habitats of anorthern Australian estuary: their occurrencein theadjoiningseaand estuarine dependence. Estuarine, Coastal and Shelf Science29,247255.

Blaber, S. J. M ., Brewer, D . T . & Salini, J. P. 1995 Fish com-munities and the nursery role of the shallow inshore waters of a

tropical bay in the Gulf of Carpentaria, Australia. Estuarine,Coastal and Shelf Science40, 177193.

Boddeke, R., Driessen, G., Doesburg, W. & Ramaekers, G. 1986Food availability and predator presence in a coastal nurseryarea of the brown shrimp (Crangon crangon). Ophelia 26,7790.

Claessens, J. 1988 Het hydraulisch regime van de Schelde. Water43, 163169.

Claridge, P. N., Potter, I. C. & Hardisty, M . W. 1986 Seasonalchanges in movements, abundance, size composition and diver-sity of the fish fauna of the Severn estuary. Journal of the M arineBi ological A ssociati on of t he U.K . 66, 229258.

Costa, M . J. 1988 T he T agus and M ira estuaries (Portugal) andtheir role as spawning and nursery areas. Journal of Fish Biology,33 (suppl. a), 249250.

Cyrus, D. P. & Blaber, S. J. M . 1992 T urbidity and salinity in a

tropical northern Australian estuary and their influence on fishdistribution. Estuarine, Coastal and Shelf Science35, 454563.Daan, N., Bromley, P. J., Hislop, J. R. G. & Nielsen, N. A. 1990

Ecology of North Sea fish. N etherlands Journal of Sea R esearch26,343386.

Davis, T . L . O. 1988 T emporal changes in the fish fauna entering atidal swamp systemin tropical Australia. Env ironmental Bi ology ofFishes21, 161172.

Day, J. W., H all, C. A. S., K emp, W. M . & Yanez-Arancibia, A.1989 Estuarine Ecology. John Wiley & Sons, Inc., (eds). NewY ork, C hichester, Brisbane, T oronto, Singapore, 558 pp.

Elliott, M . & Dewailly, F . 1995 T he structure and components ofEuropean estuarine fish communities. N etherlands Journal of A quatic Ecology 29, 397417.

Elliott, M ., OReilly, M . G. & T aylor, C . J. L . 1990 T he Forthestuary: a nursery and overwintering area for North Sea fishes.

H ydrobiologia 195, 89103.Evans, S. & T almark, B. 1984 Seasonal dynamics of small vagile

predators on a marine shallow soft bottom. H olartic Ecology 9,138148.

Evans, S. 1983 Production, predation, and food niche segregationin a marine shallow soft bottom community. M arine EcologyProgress Series10, 147157.

Field, J . G., Clarke, K . R. & Warwick, R. M . 1982 A practicalstrategy for analysing multispecies distribution patterns. M arineEcology Progress Seri es8, 3752.

Hadderingh, R. H ., V an Aerssen, G . H. F. M ., G roeneveld, L .,Jenner, H . A . & Van Der Stoep, J. W. 1983 Fish impingement atpower stations situated along the rivers Rhine and M euse in theNetherlands. H ydrobiological B ulletin 17, 129141.

Haedrich, R. L . 1983Estuarine fishes. In Ecosystems of the W orld: 26Estuari es an d Enclosed Seas (K etchum, B. H ., ed.). Elsevier,

Amsterdam, pp. 183207.Hamerlynck, O. & H ostens, F. 1993 Growth, feeding, production,

and consumption in O-group bib and whitingin a shallow coastalarea of the south-west Netherlands. ICES Journal of M arineScience50, 8191.

Hamerlynck, O. 1990 T he identification of Pomatoschistus minutusand Pomatoschistus lozanoi (Pisces, G obiidae). Journal of FishBiology 37, 723728.

Hamerlynck, O., H ostens, K ., Arellano, R. V., M ees, J. & VanDamme, P. A. 1993 T hemobile epibenthic faunaof soft bottomsin the Dutch D elta (south-west N etherlands); spatial structure.N etherlands Journal of A quatic Ecology 27, 343358.

Hecht, T . & van der L ingen, C. D. 1992 T urbidity-inducedchanges in feeding strategies of fish in estuaries. South AfricanJournal of Zoology 27, 95107.

H eip, C. 1988 Biotaand abiotic environment in the Westerscheldeestuary. H ydrobiological B ulletin 22, 3134.

H enderson, P. A. 1989 On the structure of the inshore fishcommunity of England and Wales. Journal of the M arine Bi ologicalA ssociati on of the U.K . 69, 145163.

H enderson, P. A., James, D. & H olmes, R. H . A. 1992 T rophicstructure within Bristol Channel: seasonality and stability in

Bridgewater Bay. Journal of the M arine Bi ological A ssociati on of theU . K . 72, 675690.

Hyslop, J. R. G., Robb, A. P., Bell, M . A. & Armstrong, D. W.1991 T he diet and food consumption of whiting (M erlangiusmerlangus) in the North Sea. ICES Journal of M arine Science48,139156.

Iglesias, J . 1981 Spatial and temporal changes in the demersal fishcommunity of the Rio de Arosa (NW Spain). M ari ne Bi ology65,199208.

L aroche, J., Baran, E. & Rasoanandrasana, N. B. 1997 T emporalpatterns in a fish assemblage of a semiarid mangrove zone inM adagascar. Journal of Fish Biology 51, 320.

M aes, J., T aillieu, A ., Van Damme, P. A. & Ollevier, F. 1997T he composition of the fish and crustacean community of theZeeschelde estuary (Belgium). Belgian Journal of Z oology 127,4755.

M anhagen, C. 1988 Changes in foraging as a response to predationrisk in two gobiid fish species, Pomatoschistus minutusand Gobiusni ger. M ar ine Ecology Progress Seri es49, 2136.

M cLusky, D. S. 1989 T he E stuar in e E cosystem. Chapman & Hall,Glasgow, 215pp.

Pomfret, J. R., Elliott, M ., OReilly, M . G. & P hillips, S. 1991Spatial and temporal patterns in fish communities in two U KNorth Sea estuaries. I n Estuari es and C oasts: Spatial and T emporalI ntercompari sons (Elliott, M . & Ducrotoy, J. P., eds). Olson &Olson, F redensborg, Denmark, pp. 277284.

Potter, I . C ., Beckley, L . E., Whitfield, A. K . & L enanton, R. C. J .1990 C omparisons between the roles played by estuaries in thelife cycles of fishes in temperate Western Australia and SouthernAfrica. Environmental Biology of Fishes28, 143178.

Potter, I . C ., C laridge, P. N ., H yndes, G . A. & C larke, K . R. 1997Seasonal, annual and regional variations in ichthyofaunal compo-

sition in the inner Severn Estuary and inner Bristol Channel.Journal of the M arine Bi ological association of the U .K . 77, 507525.

Robertson, A. I. & Duke, N. C. 1990a Recruitment, growth andresidencetimeof fishes in a tropical Australian mangrovesystem.Estuarine, Coastal and Shelf Science31, 723743.

Robertson, A. I. & Duke, N. C. 1990bM angrovefish communitiesin tropical Queensland, Australia: spatial and temporal patternsin densities, biomass and community structure. M arine Biology104, 369379.

Ruiz, G. M ., H ines, A . H . & P osey, M . H . 1993 Shallow water asa refuge habitat for fish and crustaceans in non-vegetated estuar-ies: an example from Chesapeake Bay. M ari ne Ecology ProgressSeries99, 116.

Salvanes, A. G. V. & Jarle, T . N. 1993 Dominating sublittoral fishspecies in a west N orwegian fjord and their trophic links to cod

(Gadus morhua L.). Sarsia 78, 221234.Schlosser, I. J. 1988 Predation risk and habitat selection by two sizeclasses of a stream cyprinid: experimental test of a hypothesis.Oikos52, 3640.

T aylor, R. J. 1984 Predation. I n Population and Community Biology(Usher, M . B. & Rosenzweig, M . L ., eds). Chapman & Hall,L ondon, 166 pp.

T er Braak, C . J. F. 1994 Canonical community ordination. Part I:Basic theory and linear methods. Ecoscience1, 127140.

T hiel, R., Sepulveda, A., K afemann, R. & Nellen, W. 1995Environmental factors as forces structuringthe fish community ofthe Elbe Estuary. Journal of Fish Biology 46, 4769.

T urnpenny, A. H . W. 1988 F ish impingement at estuarine powerstationsand its significance to commercial fishing. Journal of FishBiology 33 (suppl. a), 103110.

150 J. Maes et al .

7/29/2019 114130

9/9

Van D amme, S., M eire, P., M aeckelberghe, H., Verdievel, M .,Bougoing, L ., T averniers, E., Y sebaert, T . & Wattel, G. 1995Dewaterkwaliteit van de Zeeschelde: evolutie in de voorbije dertigjaar. Water 85, 244256.

Van den Broek, W. F. L . 1979 A seasonal survey of fish populationsin the L ower M edway Estuary, K ent, based on power stationtrash screens. I nternati onal Journal of Envi ronmental St udies 15,

203216.Van Eck, G. T . M ., De Pauw, N., Van Langenbergh, M . & Verreet,

G. 1991 Emissies, gehalten, gedrag en effecten van (micro)veron-treinigingen in het stroomgebied van de Schelde en Schelde-estuarium. Water 60, 164181.

Werner, A. K ., Gilliam, J . F ., H all, D . J . & M ittelbach, G . G . 1983An experimental test of theeffectsof predation riskon habitat usein fish. Ecology 64, 15401548.

Wharfe, J. R., Wilson, S. R. & D ines, R . A . 1984 Observations onthe fish population of an east coast estuary. M arine PollutionBulletin15, 133136.

Wheeler, A. 1988 F ish in estuaries: a summing up. Journal of Fish

Biology 33 (suppl. A), 251254.Wright, J . M . 1986 T he ecology of fish occurring in shallow water

creeks of a Nigerian mangrove swamp. Journal of Fish Biology 29,431441.

Structure of an estuarine fish and crustacean community 151