at SciVerse ScienceDirect

Estuarine, Coastal and Shelf Science 110 (2012) 176e189

Contents lists available

Estuarine, Coastal and Shelf Science

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

Alterations in macroinvertebrate spatial patterns in coastal lagoons: Óbidos(NW coast of Portugal) 1984 versus 2002

Ana Maria Rodrigues a,*, Victor Quintino a, Fábio Pereira a,b, Rosa Freitas a

aDepartamento de Biologia & CESAM, Universidade de Aveiro, Campus Universitário de Santiago, 3810-193 Aveiro, Portugalb Instituto Nacional de Recursos Biológicos (INRB)/IPIMAR, Avenida 5 de Outubro s/n, Olhão 8700-305, Portugal

a r t i c l e i n f o

Article history:Received 15 March 2012Accepted 19 May 2012Available online 26 May 2012

Keywords:sedimentsbenthic macrofaunaspatial patterns alterationsdredging

* Corresponding author.E-mail address: anarod@ua.pt (A.M. Rodrigues).

0272-7714/$ e see front matter � 2012 Elsevier Ltd.doi:10.1016/j.ecss.2012.05.024

a b s t r a c t

The macroinvertebrate spatial distribution patterns in the Lagoon of Óbidos were studied in 1984 andrevisited in 2002. The overall surficial sediments and benthic community patterns show consistentsimilarities in the two sampling periods, but also important differences. The lagoon is relatively shallow,with about 1/3 of the area covered with extensive intertidal sand banks. These are interrupted bya navigation channel bordering the northern margin (1984) and, following dredging operations, a newnavigation channel was opened along the southern margin (2002). The sediments in the navigationchannels were coarser and with less percentage of fines in 2002 than in 1984.

Arthropods dominated the species richness and abundance in 1984, but were much less important in2002, when the community was dominated by molluscs and annelids, both in species numbers as well asin abundance. In 1984, the structure of the macrofauna communities closely followed a general modelproposed for Atlantic and Mediterranean lagoons, with the marine, the transition and the lagooncommunities occupying very well defined areas. This gradient was in accordance with an increase in thefines and organic matter content directed inwards allowing for the coexistence of several characteristiclagoon species with others characteristic of organic enriched sediments. In 2002 this spatial pattern isstill recognized but the marine and the transition communities are spatially mixed, occupying both theentrance region and the navigation channels, whereas the characteristic lagoon community identified in1984 was only recognized in a group of sites located along the southern margin in 2002. Several speciesshow very important changes in their distribution extent in the lagoon system. These changes essentiallyshow a generalized inward expansion of the distribution range of the marine species, in agreement witha larger influence of marine conditions toward the inner areas of the lagoon. This study shows howsensitive lagoon systems can be to the regime of water exchange rate with the ocean being possible toinduce more or less marine conditions to the system as a response to the flow and exchange rate of waterthrough the communication inlet following dredging interventions.

� 2012 Elsevier Ltd. All rights reserved.

1. Introduction

Coastal lagoons are productive transitional ecosystems that, likeestuaries, are submitted to multiple pressures associated mainlywith waste disposal, natural resources exploitation and recrea-tional activities (McLusky and Elliott, 2004). However, lagoons areephemeral habitats whose conservation and management requireshuman intervention. Dredging of the communication channel withthe ocean and of inner channels, to improve the water exchangeand the general circulation inside the system, are amongst themostcommon.

All rights reserved.

The impact of dredging and disposal of dredged material is anenvironmental concern all over the world (Van Dolah et al., 1984;Wilber et al., 2007). Benthic macrofauna is often used as an impactindicator of such disturbance (Roberts et al., 1998) because it isdirectly affected by the removal and disposal of the sediment,integrates the changes in environmental conditions, plays anessential role in the food web and some species are commerciallyexploitable resources (Gray, 1974; Pearson and Rosenberg, 1978;McLusky and Elliott, 2004). The assessment of biological effects onthe areas of bottom sediment removal (Poiner and Kennedy, 1984;Kenny and Rees, 1994, 1996; Rodrigues and Quintino, 2001;Robinson et al., 2005; Szymelfenig et al., 2006) and deposition(Harvey et al., 1998; Smith and Rule, 2001; Van de Wal et al., 2011)is commonly undertaken. The magnitude of the impacts on thebenthic macrofauna depend upon a variety of factors (eg, sediment

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189 177

characteristics, depth, hydrological regime, contamination, volumeand area to be dredged, dredging equipment, period of timerequired) and can range from short to long term (McCauley et al.,1977; Diaz, 1994; Newell et al., 1998; Smith and Rule, 2001; Cruz-Mota and Collins, 2004; Fredette and French, 2004; Ponti et al.,2009; Van de Wal et al., 2011). Sometimes, the re-colonizationprocess may lead to a faunal assemblage not similar to thatwhich existed before the dredging (Kaplan et al., 1975; Kenny andRees, 1994, 1996; Desprez, 2000; Boyd and Rees, 2003;Szymelfenig et al., 2006). The most obvious biological impactregards the physical removal of the benthic communities and thusa reduction in the number of species and abundance. However,changes in the sediment characteristics (e.g. grain-size; organiccontent), sediment re-suspension and associated alteration innutrients, organic matter and pollutants which can contribute toeutrophication and toxicity, or increase in water circulation andoxygenation may also induce alterations on the structure andfunction of benthic communities (Newell et al., 1998, 2004;Rodrigues and Quintino, 2001; McLusky and Elliott, 2004; Blanchetet al., 2005).

The Lagoon of Óbidos, located on the north-western coast ofPortugal is connected to the sea by a narrow inlet which undergoesmigration on monthly time scales and closes frequently. Topromote tidal flushing and to avoid mouth closure, dredgingactivities are implemented as needed. In 1999, 2001 and 2003, thelagoon northern channel was dredged and in 1995, both northernand southern channels were intervened (Oliveira et al., 2006).Following the 1993/1994 winter, a guiding wall was built near thenorthern margin in 1999 because dredging was unable to stopchannel migration endangering of the northern margin. Dredgingrepositioned and deepened the main channel and increased tidalprisms and reduced flood dominance (Oliveira et al., 2006).

9°14'W 9°13'W

39°23'N

39°24'N

39°25'N

39°26'N

Atlantic Ocean

Bom Suc

esso

Lag

Poça das Ferrarias

1 m

2 m

3 m

4 m

1 m

Fig. 1. Lagoon of Óbidos: Study area showing t

The first studies concerning the general ecology of the lagoon ofÓbidos were conducted in 1984 and included the characterizationof the benthic macrofauna and its relationship with the sedimentcharacteristics (Quintino et al., 1986, 1989). Following engineeringworks in 1999 and the repeated dredging activities thereafter,namely the set up of a navigation channel along the southernmargin, monitoring studies were undertaken (Carvalho et al.,2005), restricted to a limited number of sites (24). In the presentstudy a higher sampling effort (107 sites) allowed a better spatialcoverage of the lagoon bottom. The aims of this study are (1) todescribe the main subtidal benthic communities and sedimenttypes occurring in the lagoon, updating the former existing data;(2) to assess the changes in the sediments and the macro-zoobenthic communities from the 1984 study by Quintino et al.(1989), and consequently (3) to test the macrozoobenthos asa tool to detect environmental alterations at the level of the system.

2. Methods

2.1. Study area

The Lagoon of Óbidos, north-west coast of Portugal, has an areaof approximately 7 km2 (Fig. 1). Tidal amplitude ranges from 2 to4 m at the coastal zone and 1e2 m inside the lagoon (Oliveira et al.,2006). Freshwater inputs are negligible, mainly in Spring/Summer,and enter the lagoon through the Barrosa and Bom Sucesso arms.Studies on the lagoon general ecology were conducted in 1984 andincluded the characterization of the benthic macrofauna and itsrelationship with the sediment characteristics (Rodrigues andDauvin, 1985; Rodrigues and Quintino, 1985; Quintino et al., 1986,1989). The benthic communities showed a very distinct pattern:a marine community was located at the entrance over clean coarse

9°12'W 9°11'W

1Km0

Spai

n

Atla

ntic

Oce

an

Po

rtu

ga

l

Barrosa

oon of Óbidos: 2002

Arnóia river

Cal river

Real river

he location of the sampling sites in 2002.

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189178

unstable sand, an inner lagoon community on muddy sedimentsoccupied 85% of the lagoon area and a transition communitybetween the two, was located mainly in the northern navigationchannel (the only existing at that time), on coarse clean and siltymedium sand (Quintino et al., 1989). The study developed later byCarvalho et al. (2005) also detected three different communities,corresponding to the inner and the central parts of the lagoon andalso to the entrance inlet, including the navigation channel thathowever showed diminished species richness when compared tothat described earlier.

In 1984 along the southern margin and inwards of the centralintertidal sandbank, a well-established Zostera marina habitatexisted and high numbers of Corophium insidiosum tubes coveredthe leaves. In 2002 no signs of Z. marina were found.

2.2. Sampling and laboratory procedures

In 1984, sediment samples were collected during March in 48subtidal sites using a small scale model (surface: 0.07 m2) ofa “Ralier du Baty” dredge, commonly used in descriptive benthiccommunity studies in the Atlantic and the British Channel(Cabioch, 1968). In 2002, samples were obtained in July in 107subtidal sites (Fig. 1), using a PONAR grab (0.05 m2), two replicatesper site, one for macrofauna, species richness and abundance

< 5

5 - 25

25 - 50

> 50

Fines (%)

Gravel

Coarse sand

Medium sand

Fine sand

Mud

Very fine sand

Sediment Types(P50)

4

3

21

Atlant

ic

Oce

an

4

3

21

Bom

Suc

esso

B

4891

Fig. 2. Spatial pattern of the sediment fines content and of the sedi

determinations, and the other for sediment grain size, organicmatter content, redox potential and temperature measurements.In both periods, the lagoon mean water depth was about 1 m withmaximum depth of 5 m, in the Bom Sucesso arm (Fig. 1).

Grain size analysis was performed by wet and dry sievingaccording to Quintino et al. (1989). In the gravel class, the biogenicfraction, mostly mollusc shells, was sorted and weighed separately.Sand and gravel content were sieved and weighed at 4 intervals.Organic matter determinations were performed by loss on ignitionat 450 �C (Kristensen and Andersen, 1987). Redox potential andtemperatureweremeasured, on board, at�4 cm from the sedimentsurface with specific probes (Pearson and Stanley, 1979).

The sediment samples for the study of macrofaunawerewashedover a 1.0 mmmesh screen and the remaining material was fixed in4% buffered formalin, stained with Rose Bengal. In the laboratory,the samples were washed, the invertebrates sorted, preserved in70% ethanol and identified to species level whenever possible. Foreach site, a species list and the respective abundance wasdetermined.

2.3. Data analysis

The sediment was classified according to fines (<63 mm), sand(63 mme2 mm) and gravel (>2 mm) content and the median value:

arrosa

2002

ment types based in the median values (P50) in 1984 and 2002.

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189 179

muds - fines content above 50%; coarse sand -median between 500and 1000 mm; medium sand - median between 250 and 500 mm(Rodrigues et al., 2006).

Macrofauna affinity groups were obtained through classificationand ordination analysis of the species abundance data matrix. Theaffinity groups were characterized using environmental and bio-logical descriptors. Data from the two sampling periods werecombined in a single data matrix, to the genus level in order todecrease the effect of species identification differences from bothperiods. This combined data matrix was log (x þ 1) transformedand inter-site similarities were obtained with the BrayeCurtiscoefficient. The similarity matrix was submitted to classificationanalysis using un-weighted arithmetic average clustering (UPGMA)(Legendre and Legendre, 1998) and ordination by principal coor-dinates analyses (PCO) (Clarke and Warwick, 2001), using thesoftware PRIMER v6.0 (Clarke and Gorley, 2006).

3. Results

3.1. Sediments

Fig. 2 shows the distribution of fines content and the surficialsediment types in 1984 and 2002. In both periods, muds occupiedalmost all the lagoon bottom inwards of the intertidal sand banks andcoarse and median sand predominate in the entrance and along thenavigation channels. In 1984 the sediment along the northern navi-gation channel was medium sand and some sites presented more

Table 1Summary of benthic macrofauna characterisitcs in 1984 and 2002 sampling periods.

Sampling periods

Nr. of sitesTotal taxa abundanceRange of total taxa abundance per sampleTotal taxa richnessRange of total taxa richness per sampleDominant taxa (abundance)Abundance of dominant taxa (% total)Dominant taxa (richness)Number of dominant taxa (% total)Number of species sampled once (% total)Abundance of species sampled once (% total)Species present in 50% of the sites (% total)Abundance of species present in 50% of the sites (% total)Species present in 50% of the sites

Species with more than 1000 ind (% total)Abundance of species with more than 1000 ind (% total)Species with more than 1000 specimens

than 5% fines. In 2002 all the sites in that area presented sedimentswith less than 5% fines and some were coarse sand. The navigationchannel along the southern margin, inexistent in 1984 and con-structed by dredging the medium sand intertidal bank, presentedcoarse sand. The influence of the water circulation through thischannel is noticed in the sediments located along the margin inwardof the sand bank, with the substitution of 1984 mud sites by 2002medium and very fine sand with variable fines content (Fig. 2).

Besides these changes and the increased fines content ina particular site near themouth of the lagoon in 2002 (near thewallbuilt in 1999), the sediment spatial pattern was similar in bothperiods in the inner areas, including the central body of the lagoonand the Barrosa and Bom Sucesso arms. Because the percentage ofgravel in the sediments was very low and almost the same in bothsampling periods, the proportion of sand was complementary tothat of fines and so the northern navigation channel sedimentsshowed higher sand content in 2002, when compared to 1984.

In 1984 the organic matter content was not analyzed but duringa temporal survey in 1985 (unpub. data) 10e11% organic mattercontent was registered for sediments in the central lagoon body andthe inner lagoonarms. In2002, thisdescriptorwasbelow1%of the totalsediment, in the entrance and the northern and southern navigationchannels. It increased toward the inner areas and was generally above10% in the BomSucesso and the Barrosa arms. The redox potential onlymeasured in 2002, decreased with the increase of fines content andwas negative in some sites bordering the inner part of the centralintertidal bank and in the inner lagoon arms.

1984 2002

48 10849528 5239713e13004 1e3774116 2194e52 1e45Arthropods Molluscs28984 (58.5) 19881 (37.9)Annelids Annelids40 (30.0) 72 (32.9)20 (17.0) 76 (35.0)31 (0.06) 100 (0.19)12 (10.3) 5 (4.2)38195 (79.0) 31040 (59.0)Hydrobia ulvae Hydrobia ulvaeCerastoderma edule Cerastoderma eduleTubificoides benedii Tubificoides benediiCorophium insidiosum Corophium acherusicumMalacoceros fuliginosus Heteromastus filiformisCapitella capitataLoripes lacteusAbra ovataLekanesphaera hookeriCyathura carinataPhoronis psammophilaChironomids13 (11.2) 10 (4.6)41990 (84.8) 39683 (75.7)Capitella capitata Capitella capitataHeretomastus filiformis Heretomastus filiformisTubificoides benedii Tubificoides benediiCerastoderma edule Cerastoderma eduleHydrobia ulvae Hydrobia ulvaeMicrodeutopus gryllotalpa Microdeutopus gryllotalpaMelita palmata Melita palmataPhoronis psammophila Phoronis psammophilaCorophium insidiosum Corophium acherusicumEricthonius difformis Gammarus insensibilisAbra albaAbra ovataChironomids

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189180

3.2. Macrofauna

3.2.1. Species richness and abundanceThe use of different sampling devices and different number of

sampling sites in 1984 and 2002 did not permit a rigorouscomparison of the species richness and abundance between thetwo periods but allowed to appreciate the alterations in dominanceand in the species distributional patterns. Annelids, molluscs andarthropods dominated in both periods and more than 50% of thespecies found in 1984 were also present in 2002. Some differenceswere noticed between the two sampling periods (Table 1).Arthropods diminished their relative abundance, from over 58% in1984 (Table 1) to about 25% in 2002. The number of speciessampled in more than 50% of the sites and those with more than1000 individuals, were both lower in 2002 (Table 1), whereas thespecies sampled in a single site were more numerous in 2002. Onesuch rare species, not sampled in 1984, was Diopatra marocensis, atthe time only known from the Moroccan coast (Paxton et al., 1995).

Species richness in 1984 showed a distinctive pattern: the lowervalues were found close to the entrance and in both lagoon armsand the higher values were found along the main navigationchannel (Fig. 3). In 2002 the pattern was more confused: the lowervalues were found in sites at the entrance of the lagoon and in theBarrosa arm, but also scattered along the northern navigation

Atlanti

c

Ocean 1211

346 5

7 14

1

17

23

4

13938

37

1211

346 5

14

1 42

17

20

23

33

40 41

45

4

13938

37

Fig. 3. Spatial pattern of the number of species

channel; the higher values were scattered at the lagoon entranceand in the inner areas of the navigation channels (Fig. 3); the BomSucesso arm showed much higher species richness values in 2002than in 1984. For abundance (Fig. 3), the main differences betweenthe two periods were noticed at the entrance (higher values in2002), the northern navigation channel (lower values in 2002) andin both lagoon arms (higher abundance in 2002). For the overallpattern, in 1984 the benthic community was more abundant inareas located inwards of the species richness peak, whereas in 2002a comparable pattern could not be established.

3.2.2. Multivariate analysisFig. 4 shows the spatial distribution of the affinity groups

emphasized by the classification and ordination analyses of thespecies abundance data in 1984 and in 2002. In 1984, the spatialpattern of benthic communities included a marine communitylocated at the entrance, a lagoon community located inwards of theintertidal sand banks and a transition assemblage in between,located along the northern navigation channel. In 2002 this generalstructure was not as simple and seven main groups (A to G) wereemphasized. Their biological and environmental characteristics,including themost abundant species, are presented in Table 2 (1984groups characteristics were published in Quintino et al., 1989).Group A comprised sites located in the entrance and the navigation

98

7652

9998

97

94

91

89

8886

8180

79 78 777573

7271

7069

68

666561 60 59 58

57

5554

52

51

49

46

454443

42

3433

32 31

3029

28

2625

24

23

2221

191716

151413

10

101

36

3

63

41

8

7652

9998

95

9493

92

9089

88

8483

8281

78 7776

7271

70

67

656461

57

5453

51

50

47

46

454443

4240

3129

27

25

24

23

2120

1916

151413

1110

101

100

36

3

41

and abundance per site in 1984 and 2002.

Atlantic

Oce

an

Barrosa

A

BC

DE

FG

51

Atlant

ic

Oce

an

4

3

21

Fig. 4. Benthic communities identified in 1984 (Quintino et al., 1989) and main affinity groups emphasized with the 2002 data.

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189 181

channels and was characterized by clean coarse sand, low organicmatter and low species richness and abundance (Fig. 4; Table 2).Group B sites were scattered along the southern navigation channeland bordering the central intertidal bank, with sandy mud andorganically enriched sediments. Group C comprehended siteslocated in the same area as group A but also included more shel-tered sites (Fig. 4; Table 2). The sediments in group C showed higher

Table 2Characterization of the macrofauna affinity groups identified in 2002 in the lagoon of Ób

2002 Affinity groups

A B C D

Number of sites 17 5 21 23Gravel content (mean; %) 3.32 5.30 5.10 0.Sand content (mean; %) 96.45 36.59 67.47 12Fines content (mean; %) 0.23 58.11 27.43 81Biogenic fraction

(shell debris; mean; %)1.51 3.01 3.39 1.

Organic matter (mean; %) 0.38 5.41 3.33 7.Redox potential

(mean; mV)323.12 11.6 166.06 41

Temperature (mean; �C) 15.47 17.2 20.26 16Abundance

(mean ind/0.05m2)93.8 153.2 460.7 56

Abundance (total) 1595 766 9674 12Species richness

(mean sp./0.05 m2)7.9 9 30 22

Species richness (total) 47 30 166 10Number of

exclusive species4 0 62 19

Most abundantexclusive species

Pontocratesaltamarinus

e Barnea candida Si

Scoloplos armiger AMost abundant

species (not exclusive)Lekanesphaera levii Rissoa sp. Capitella sp. H

Tellina tenuis Abra alba Ph

Spisula subtruncata Notomastus latericeus CoNephtys cirrosa Pomatoceros lamarckii AbSpisula elliptica Mediomastus fragilis EuSpisula solida Venerupis pullastra GOphelia neglecta Caprella acanthifera Ip

Amphipholis squamata Po

fines and organic matter content and lower redox potential thanthose in group A. The abundance, the species richness and thenumber of exclusive species were also higher in group C (Table 2).The highest mean species richness per unit sampling area waslocated in group C.

Groups A and C from the 2002 analysis occupied the entranceand the navigation channels and corresponded to the 1984 marine

idos. See Fig. 4 for their spatial distribution.

E F G

13 23 3005 0.03 0.13 0.82 30.49 24.27 1.27.17 69.48 75.60 98.7308 1.98 9.26 0.08

38 7.2 8.21 11.29.92 72.83 10.44 �148.67

.83 21.26 17.72 21.54.3 179.8 834.7 1296.7

978 2337 19199 3890.1 14.1 23.5 5

2 37 84 103 9 1

gambra tentaculata Alkmariaromijni

Erichtonius difformis Lekanesphaera sp.

mpharetidae n. det.eteromastus filiformis Streblospio

shrubsoliiCorophium acherusicum Hydrobia ulvae

oronopsis sp. Nereisdiversicolor

Gammarus insensibilis

rbula gibba Tubificoides benediira ovata Microdeutopus gryllotalpaclymene palermitana Melita palmataalatowenia oculata Corophium insidiosumhinoe cf serrata Tubificidae n. det.lycirrus sp. Malacoceros fuliginosa

Idotea chelipes

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189182

and transition communities, but presented a more confused spatialpattern. This correspondence is shown in the ordination diagram inFig. 5 combining the data obtained in 1984 and 2002. Axis 1opposed the sites from the marine and the lagoon communities(1984), with the transition assemblage sites located closer to theorigin of the graph, at an intermediate position. Group A and GroupC from the 2002 analysis were represented together with, respec-tively, the marine and the transition assemblages from 1984. Thisclose distribution can also be appreciated in the detailed ordinationdiagram, showing the positioning in axes 1e2 of the groupcentroids.

Group D comprehended the central part of the lagoon and thedeeper zones of the lagoon arm Bom Sucesso (Fig. 4) and showedsediments with high fines and organic matter content. Group E islocated inwards of group D, in direction of the lagoon arm Barrosa(Fig. 4), and seems to be an impoverishment of group D (Table 2).Group F comprised sites located along the margins, on sedimentswith less fines content than those of groups D and E but with thehighest biogenic fraction content (Table 2). The highest meanspecies abundance per unit sampling area was located in group F,mainly due to high numbers of amphipods. The sites near thesouthern margin from 1984 samples have some similar character-istics to group F but were not individualized by the multivariateanalysis. Finally, group G comprised only 3 sites, all located in theinnermost areas of the Barrosa arm. The sediments presentednegative redox potential values, with almost 99% of fines and the

Fig. 5. Ordination analysis (PCO) of the combined 1984 and 2002 macrofauna dataset. T

highest organic matter content. This group corresponds to animpoverished part of the lagoon community. The samplingprogram in 1984 did not cover this area.

The relationship between the lagoon community identified in1984 and the three main affinity groups which represent the samearea of the lagoon in 2002 (groups D, E and F), is shown in theordination diagram of Fig. 5.When compared to the positions of thesites corresponding to the marine and the transition communities,stronger dissimilarities were shown by the lagoon community inboth periods: groups D and E, which comprised most of the lagooncommunity in 2002, do not have a corresponding group in 1984.Such correspondence is stronger with group F, which comprisedmost of the sites located along the margins in 2002 (cf. Figs. 4 and5). The mean BrayeCurtis dissimilarity between the 1984 lagoongroup and group Fwas lower (66.35%) than between groups F and D(72.94%) or between groups F and E (75.5%). The mean BrayeCurtisdissimilarity between the 1984 lagoon community and group D(75.64%) or group E (74.65%) was also high while the meandissimilarity between groups D and E was lower (66.12%). Therelationship between the 3 affinity groups that represented in 2002the area where in 1984 was identified the lagoon community canalso be appreciated in the detailed ordination representing thegroup centroids. In this ordination diagram, axis 2 separated the1984 lagoon community and the 2002 group F (positive pole), fromthe 2002 groups D and E (negative pole). The reason behind theindividualization of 2002 groups D and E from what the lagoon

he small diagram is based on the group centroids identified in the main ordination.

Fig. 6. Spatial distribution patterns of the polychaetes N. cirrosa and M. fragilis and of the bivalves S. solida and V. senegalensis, in 1984 and 2002.

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189 183

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189184

community was in 1984 is better understood by analyzing thespatial distribution of a number of key species in the lagoonenvironment.

3.2.3. Species spatial distribution patternsSeveral species have shown marked changes in their spatial

distributional range inside the lagoon, allowing to better under-stand the differences in the joint ordination of the two data periods.

Figs. 6e10 show the alterations of the spatial distributionpatterns of some of the most characteristic species. Nepthys cirrosaand Spisula solida, in 1984 located mainly in the lagoon entrance(marine community), extended their distribution along the navi-gation channels in 2002. Venerupis senegalensis andMediomastus cf.fragilis (Fig. 6) which in 1984 occupied mainly the entrance and thenavigation channel, extended their distribution further inwards in2002 (Fig. 6). A similar trend was shown by the spatial distributionof the bivalves Spisula subtruncata, Abra alba and Scrobicularia plana

Fig. 7. Spatial distribution patterns of the bivalves S. su

(Fig. 7). The bivalves Parvicardium exiguum and Abra ovata, theisopod Cyathura carinata and the polychaete Nereis diversicolor,found in 1984 along the navigation channel and the central part ofthe lagoon community (Fig. 8), in 2002 were absent from thenavigation channels and were distributed almost exclusivelyinwards of the intertidal sand banks, including the inner arms ofBom Sucesso and Barrosa arms (Fig. 8). The bivalves Venerupisdecussata and Loripes lacteus were present in 1984 around theintertidal bank (Fig. 9). In 2002 these species were sampled only in,respectively, three and two scattered sites in the lagoon. Moreover,the polychaete Scoloplos armiger in 1984 was distributed mainly inthe entrance and bordering the sand bank (Fig. 9) and in 2002 wasonly found in two of these sites.

The affinity group F identified in 2002 in the inner margins ofthe lagoon (cf. Figs. 4 and 5) was shown to be the most similar tothe lagoon community identified in 1984. Fig. 10 shows the distri-bution of some amphipod species which were present in the

btruncata, A. alba and S. plana, in 1984 and 2002.

Fig. 8. Spatial distribution patterns of the bivalves P.exiguum and A. ovata, of the isopod C. carinata and of the polychaete N. diversicolor, in 1984 and 2002.

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189 185

lagoon community in 1984 and that were mainly found along themargins in the 2002 samples: Ericthonius difformis, Melita palmata,Microdeutopus gryllotalpa and Corophium insidiosum. From 1984 to2002 these species extended their distribution toward the innerpart of the lagoon, including the arms Bom Sucesso and Barrosa. In1984 C. insidiosum (Fig. 10) was found in the entire lagoon, mainlyinwards of the main sand bank. This species was then very abun-dant and constructed tubes on the fronds of Zostera marina, and

was thus more abundant along the southern margin where most ofthe Zostera beds were installed. In 2002 the species was almostconfined to the lagoon arms and Poça das Ferrarias. The samehappened with E. difformis (Fig. 10) and other species (not repre-sented), namely the isopod Idotea chelipes present in 1984 mainlyin the lagoon community and in 2002 confined to Poça das Ferrariasand Bom Sucesso. Chironomid larvae, very abundant in 1984 in theentire lagoon, mainly along the northern margin, were found only

Fig. 9. Spatial distribution patterns of the bivalves V. decussata and L. lacteus (abundance classes on the left) and of the polychaete S. armiger (abundance classes on the right), in1984.

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189186

in 15 sites in 2002 with a total of 86 individuals. Finally, Hydrobiaulvae, a ubiquitous species in 1984, maintained this distributionpattern and increased its abundance in 2002.

4. Discussion

This study was based on the comparative analysis of sedimentand benthic macrofauna samples obtained in the Lagoon of Óbidosin 1984 and in 2002. Between the two sampling periods, dredgingactivities repositioned and deepened the main channel andincreased the tidal prism inside the lagoon (Oliveira et al., 2006).This was noticed in the channel sediments in 2002 which werecoarser and with lower fines content than in 1984. Also, the newnavigation channel dredged along themedium sand intertidal bankpresented areas of coarse sand. The influence of this new naviga-tion channel was noticed in the sediments from the southernmargin that changed from mud (1984) to medium and very finesand (2002). However the grain-size and organic content of thesediments in the rest of the lagoonwas very similar in both periods.

Concerning the macrofauna, more than 50% of the species werecommon to the two sampling periods and the species Hydrobiaulvae, Tubificoides benedii and Cerastodema edule were present inmore than 50% of the sites in both periods. Besides these species,Corophium insidiosum, Lekanesphaera hookeri, Cyathura carinata,Chironomids, Abra ovata, Loripes lacteus, Phoronis psammophila,Malacoceros fuliginosus and Capitella capitata were also abundantand frequent in 1984, and Corophium acherusicum and Hetero-mastus filiformis in 2002. All these species are characteristic oftransition systems and commonly associated with organic enrichedareas (e.g. Pearson and Rosenberg, 1978; Quintino et al., 1987; Borjaet al., 2000; Hiscock et al., 2004; Munari et al., 2005; Rodrigueset al., 2006, 2011).

The macrofauna in both sampling periods was dominated byannelids, molluscs and arthropods. In 1984 the arthropods weredominant in terms of total abundance and the annelids in terms ofspecies richness. In 2002 the abundance of arthropods decreased;the species richness was higher in relation to 1984 but the annelidspresented higher species richness and the molluscs higher abun-dance of individuals. A marked decrease in the Zostera marina bedswas noticed from 1984 to 2002 which could induce changes in theassociated fauna. Zostera meadows are refuge for several speciesand retain sediments and organic matter (Boström and Bonsdorff,1997; Hiscock et al., 2004). In 1984 several arthropod specieswere associated with the Zostera beds and decreased their abun-dance in 2002, appearing only in more sheltered sites. This is the

case of Corophium insidiosum one of the most widespreadamphipod in Mediterranean and Atlantic lagoons (Quintino et al.,1987; Prato and Biandolino, 2006) and is found normally in shel-tered sites with certain turbidity and located near the sea becauseof the salinity. It builds tubes with mucus and detritus and isa detritus and suspension feeder (Dahl, 1973; Prato and Biandolino,2006). In 1984 C. insidiosum was one of the most abundant andfrequent species and covered the leaves of Z. marinawith tubes. Thedisappearance of Z. marina should be one of the reasons for themuch lower abundance of the species in 2002, and its restricteddistribution to the more protected areas of the Bom Sucesso armand Poça das Ferrarias. The opening of a navigation channel alongthe southern margins, inexistent in 1984, that promoted anincrease of the hydrodynamism and seawater input to the innerparts of the lagoon (Oliveira et al., 2006) could also account for thechanges in the abundance, frequency and distribution pattern of C.insidiosum and of other macrofauna species. The most abundantamphipod in 2002 was Corophium acherusicum, considered a eur-ihaline species (Bellan-Santini et al., 1982). This species was notfound in the lagoon in 1984. The reduction of Chironomid larvae in2002 could also be due to similar reasons. These organisms aredetritus feeders and prefer stagnant water and silty and organicallyenriched sediments (Arias and Drake, 1994; Hiscock et al., 2004).

An interesting species in the 2002 collection is the polychaeteDiopatra marocensis, firstly described for the south MoroccanAtlantic coast (Paxton et al., 1995) and today also reported along thePortuguese coast (Rodrigues et al., 2009) and in northern Spain(Arias et al., 2010). The individuals collected in Óbidos in 2002constitute the first register of the species outside its type locality(Rodrigues et al., 2009).

In 1984, the structure and spatial distribution of the macrofaunacommunities closely followed the general model proposed forAtlantic and Mediterranean lagoons (Guelorget and Perthuisot,1984; Perthuisot and Guelorget, 1987; Quintino and Rodrigues,1989) with the marine, the transition (named ecotone in Quintinoand Rodrigues, 1989) and the estuarine communities occupyingvery distinct areas that succeeded inwards from the entrancefollowing a gradient of decreasing hydrodynamic energy level orflushing time. This gradient was in accordance with an increase inthe sediment fines and organic matter content toward the inner orless flushed areas, allowing for the coexistence of several charac-teristic lagoon specieswith other characteristics of organic enrichedsediments. In 2002 this spatial pattern was still recognized but themarine and the transition communities were spatially mixed upoccupying both the entrance region and the navigation channels

Fig. 10. Spatial distribution patterns of the amphipods E. difformis, M. palmata, M. gryllotalpa and C. insidiosum, in 1984 and 2002.

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189 187

whereas the lagoon community from 1984 was in 2002 mainlyrecognized in a group of sites located along the margins. In thepresent study, the alteration in the spatial distribution patterns ofmacrofauna species from 1984 to 2002 helps to understand theseresults. In general, the species expanded their distributions inwards;species characteristic of the entrance in 1984 were also sampled in

the navigation channels in 2002 (Nepthys cirrosa, Spisula solida),others that in 1984 were distributed in the entrance and navigationchannels were found in 2002 also inwards of the sand banks (Ven-erupis pullastra, Spisula subtruncata, Abra alba,Mediomastus fragilis)while others were not sampled in the northern navigation channelbut only inwards of the sand banks (Scrobicularia plana,

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189188

Parvicardium exiguum, Abra ovata, Cyathura carinata, Nereis diversi-color and Ericthonius difformis). Some species were sampled in 2002in very few sites and showed very low abundance (Venerupisdecussata, Loripes lacteus and Scoloplos armiger). Some of thesechanges together with those noticed in the sediments could be theresult of the various managing interventions in the lagoon between1984 and 2002. Dredging of existing channels and opening of newones facilitates tidal propagation, increasing tidal amplitudes in thewhole system and thus the input of seawater to inner areas of thelagoon (Oliveira et al., 2006). Similar changes in the spatial distri-bution of species of the marine and “ecotone” communities wereobserved in the northern channel of the Sado estuary (Portugal)followingmaintenance dredging of a navigation channel (Rodriguesand Quintino, 2001). Blanchet et al. (2005) also found communitychanges in the entrance and the northernmain channel in Arcachonbay in their 2002 study relating themwith dredging that permittedstronger hydrodynamics and a marine influence in those areas.

Although dredging improves the water circulation with minorphysical changes in most of the ecosystem area, as is the case of theLagoon of Óbidos and Arcachon bay (Blanchet et al., 2005), it mayinduce important changes in the macroinvertebrate populations,namely their distributional range. In our study more than 50% ofthe species found in 1984 were also present in 2002, suggesting theresilience of the benthic macrofauna of the lagoon of Óbidos inrecovering from disturbance as is the case of other ecosystems thatrecover within months, rather than years, even submitted to highand frequently perturbations (Van der Veer et al., 1985; Fredete andFrench, 2004). However, clear alterations have been noticed, evenin those lagoon areas that did not shown notorious changes insediment grain-size and organic matter. This indicates the power ofbenthic macro-invertebrates as indicators of even slight environ-mental changes.

Lagoon systems have long been exploited for their naturalresources, and such is the case in the lagoon of Óbidos where theexploitation of bivalves, namely Cerastodema edule, Spisula solida,Venerupis senegalensis and Venerupis decussata have been impor-tant at different time periods. About 70 fishermen undertake theiractivities in the lagoon all year round (Carvalho et al., 2005). Duringour surveys we noticed that they concentrated mainly along thenorthern navigation channel in 1984 and in 2002 they moved tothe end of the navigation channels and to a narrow area inwardsthe intertidal bank reflecting the changes in the distribution andabundance of the bivalve species.

Flushing the sediment through increased water circulation andopening up of navigation channels or pushing inwards coarsersediments from the entrance area, may be a benefit to the circu-lation and oxygenation of the lagoon but may affect benthic mac-rofauna populations, namely the bivalves, inducing changes in theecosystem uses.

Adequatemonitoring programmes should be implemented afterthese engineering interventions; sampling collection in only a fewsites can reveal insufficient to detect alterations in the spatialdistribution pattern of the species, rendering the monitoringstudies less costly but eventually expensive in terms of lack ofbiological significance. Lagoons highly depend from the oceanwater exchange and naturally may loose the communication withthe ocean, restored through human intervention. Without suchintervention, lagoon systems can eventually silt up and disappearin the long term as usually the freshwater inflow is not sufficientlystrong to keep the lagoon entrance continuously open. This studyshows how sensitive lagoon systems are to the regime of commu-nication with the ocean allowing a larger distribution of marinespecies inside the lagoon when the water exchange with the oceanis enhanced. In this sense, coastal lagoons are ephemeral ecosys-tems that strongly depend on human interventions.

References

Arias, A., Anadón, N., Paxton, H., 2010. New records of Diopatra marocensis (Anne-lida: Onuphidae) from northern Spain. Zootaxa 2691, 67e68.

Arias, A.M., Drake, P., 1994. Structure and production of the benthic macro-invertebrate community in a shallow lagoon in the Bay of Cádiz. Marine EcologyProgress Series 115, 151e167.

Bellan-Santini, D., Karaman, G., Krapp-Schickel, G., Ledoyer, M., Meyers, A.A.,Ruffo, S., Schiecke, U., 1982. The Amphipoda of the Mediterranean. Mém. Inst.Oceanogr. Mónaco 13 (xiiþ), 1e364.

Blanchet, H., de Montaudouin, X., Chardy, P., Bachelet, G., 2005. Structuringfactors and recent changes in subtidal macrozoobenthic communities ofa coastal lagoon, Arcachon Bay (France). Estuarine Coastal and Shelf Science64, 561e576.

Borja, Á., Franco, J., Perez, V., 2000. A marine biotic index to establish the ecologicalquality of soft-bottom benthos within European estuarine and coastal envi-ronments. Marine Pollution Bulletin 40, 1100e1114.

Boström, C., Bonsdorff, E., 1997. Community structure and spatial variation ofbenthic invertebrates associated with Zostera marina (L.) beds in the northernBaltic Sea. Journal of Sea Research 37, 153e166.

Boyd, S.E., Rees, H.L., 2003. An examination of the spatial scale of impact on themarine benthos arising from marine aggregate extraction in the central EnglishChannel. Estuarine Coastal and Shelf Science 57, 1e16.

Cabioch, L., 1968. Contribuition à la connaissance des peuplements benthiques de laManche Occidentale. Cahiers de Biologie Marine tome IX (Cah. 5 (suppl.)),493e720.

Carvalho, S., Moura, A., Gaspar, M.B., Pereira, P., Cancela da Fonseca, L.,Falcão, M., Drago, T., Leitão, F., Regala, J., 2005. Spatial and inter-annualvariability of the macrobenthic communities within a coastal lagoon(Óbidos lagoon) and its relationship with environmental parameters. ActaOecologica 27 (3), 143e159.

Clarke, K.R., Gorley, R.N., 2006. Primer v6: User Manual/Tutorial. PRIMER-E, Ply-mouth, p. 190.

Clarke, K.R., Warwick, R.M., 2001. Change in Marine Communities: An Approach toStatistical Analysis and Interpretation, second ed. PRIMER-E, Plymouth.

Cruz-Mota, J.J., Collins, J., 2004. Impacts of dredged material disposal on a tropicalsoft-bottom benthic assemblage. Marine Pollution Bulletin 48, 270e280.

Dahl, E., 1973. Ecological range of Baltic and North Sea species. Oikos 15, 85e90.Desprez, M., 2000. Physical and biological impact of marine aggregate extraction

along the French coast of the Eastern English Channel: short and long-termpost-dredging restoration. ICES Journal of Marine Science 57, 1428e1438.

Diaz, R.J., 1994. Response of tidal freshwater macrobenthos to sediment distur-bance. Hidrobiologia 278, 201e212.

Fredette, T.J., French, G.T., 2004. Understanding the physical and environmentalconsequences of dredged material disposal: history in New England andcurrent perspectives. Marine Pollution Bulletin 49, 93e102.

Gray, J.S., 1974. Animal-sediment relationships. Oceanography and Marine Biology:An Annual Review 32, 179e239.

Guelorget, O., Perthuisot, J.P., 1984. Indicateurs biologiques et diagnose écologiquedans le domaine paralique. Ecological Bulletin 15, 67e76.

Harvey, M., Gauthier, D., Munro, J., 1998. Temporal changes in the composition andabundance of the macro-benthic invertebrate communities at dredged materialdisposal sites in the Anse à Beaufils, Baie des Chaleurs, Eastern Canada. MarinePollution Bulletin 36, 41e55.

Hiscock, K., Langmead, O., Warwick, R., 2004. Identification of Seabed IndicatorSpecies from Time-series and Other Studies to Support Implementation of theEU Habitats and Water Framework Directives. Report to the Joint NatureConservation Committee and the Environment Agency from the Marine Bio-logical Association. Marine Biological Association, Plymouth, JNCC ContractF90-01-705, p. 109.

Kaplan, E.H., Welker, J.R., Kraus, M.G., McCourt, S., 1975. Some factors affecting thecolonization of a dredged channel. Marine Biology 32, 193e204.

Kenny, A.J., Rees, H.L., 1994. The effects of marine gravel extraction on the macro-benthos: early post-dredging recolonization. Marine Pollution Bulletin 28,442e447.

Kenny, A.J., Rees, H.L., 1996. The effects of marine gravel extraction on the macro-benthos: results 2 years post-dredging. Marine Pollution Bulletin 32 (8/9),615e622.

Kristensen, E., Anderson, F.Ø, 1987. Determination of organic carbon in marinesediments: a comparison of two CHN-analyser methods. Journal of Experi-mental Marine Biology and Ecology 109, 15e23.

Legendre, P., Legendre, L., 1998. Numerical Ecology, second ed. Elsevier Science B.V,Amsterdam, p. 853.

McCauley, J.E., Parr, R.A., Hancock, D.R., 1977. Benthic infauna and maintenancedredging: a case study. Water Research 11, 233e242.

McLusky, D., Elliott, M., 2004. The Estuarine Ecosystem: Ecology, Threats andManagement, third ed. Oxford University press, p. 214.

Munari, C., Rossi, R., Mistri, M., 2005. Temporal trends in macrobenthos communitystructure and redundancy in a shallow coastal lagoon (Valli di Comacchio,Northern Adriatic Sea). Hydrobiologia 550, 95e104.

Newell, R.C., Seiderer, L.J., Hitchcock, D.R., 1998. The impact of dredging works incoastal waters: a review of the sensitivity to disturbance and subsequentrecovery of biological resources on the sea bed. Oceanography and MarineBiology: An Annual Review 36, 127e178.

A.M. Rodrigues et al. / Estuarine, Coastal and Shelf Science 110 (2012) 176e189 189

Newell, R.C., Seiderer, L.J., Simpson, N.M., Robinson, J.E., 2004. Impacts of marineaggregate dredging on benthic macrofauna off the South Coast of the UnitedKingdom. Journal of Coastal Research 20, 115e125.

Oliveira, A., Fortunato, A.B., Rego, J.R.L., 2006. Effect of morphological changes onthe hydrodynamics and flushing properties of the Óbidos lagoon (Portugal).Continental Shelf Research 26, 917e942.

Paxton, H., Fadlaoui, S., Lechapt, J.P., 1995. Diopatra marocensis, a new broodingspecies of Onuphidae (Annelida: Polychaeta). Journal of Marine BiologicalAssociation of the United Kingdom 75, 949e955.

Pearson, T.H., Rosenberg, R., 1978. Macrobenthic succession in relation to organicenrichment and pollution of the marine environment. Oceanography andMarine Biology: Annual Review 16, 229e311.

Pearson, T.H., Stanley, S.O., 1979. Comparative measurement of the redox potentialof marine sediments as a rapid means of assessing the effect of organicpollution. Marine Biology 53, 371e379.

Perthuisot, J.-P., Guelorget, O., 1987. Les milieux paraliques: diversité et unité.Ecological Bulletin 18, 159e167.

Poiner, I.R., Kennedy, R., 1984. Complex patterns of change in the macrobenthos ofa large sandbank following dredging. Marine Biology 78, 335e352.

Ponti, M., Pasteris, A., Guerra, R., Abbiati, M., 2009. Impacts of maintenance channeldredging in a northern Adriatic coastal lagoon. II: effects on macrobenthicassemblages in channels and ponds. Estuarine Coastal and Shelf Science 85,143e150.

Prato, E., Biandolino, F., 2006. Life history of the amphipod Corophium insidiosum(Crustacea: Amphipoda) from Mar Piccolo (Ionian sea, Italy). Scientia Marina 70(3), 355e362.

Quintino, V., Rodrigues, A.M., Gentil, F., Peneda, M.C., 1987. Macrozoobenthiccommunity structure in the lagoon of Albufeira western coast of Portugal.Journal of Experimental Marine Biology and Ecology 106, 229e241.

Quintino, V., Rodrigues, A.M., Gentil, F., 1989. Assessment of macrozoobenthiccommunities in the lagoon of Obidos western coast of Portugal. Scientia Marina53, 645e654.

Quintino, V., Rodrigues, A.M., 1989. Environment gradients and distribution ofmacrozoobenthos in three Portuguese coastal systems: Óbidos, Albufeira andAlvor. In: Ryland, J.S., Tyler, P.A. (Eds.), Reproduction, Genetics and Distri-butions of Marine Organisms. Olsen & Olsen, Fredensborg, Denmark,pp. 441e450.

Quintino, V., Rodrigues, A.M., Gentil, F., 1986. Etude faunistique et coenotique desMolusques (Bivalves et Gastéropodes) des lagunes d’Obidos et d’Albufeira(Portugal). Haliotis 15, 83e90.

Roberts, R.D., Gregory, M.R.R., Foster, B.A., 1998. Developing an efficient macrofaunamonitoring index from an impact study e A dredge spoil example. MarinePollution Bulletin 36, 231e235.

Robinson, J.E., Newell, R.C., Seiderer, L.J., Simpson, N.M., 2005. Impacts of aggregatedredging on sediment composition and associated benthic fauna at an offshoredredge site in the southern North Sea. Marine Environmental Research 60,51e68.

Rodrigues, A.M., Quintino, V., 2001. Estuarine sediment assessment prior todredging: integration of benthic and ecotoxicological studies. Journal of CoastalResearch Special Issue 34, 306e317.

Rodrigues, A.M., Dauvin, J.-C., 1985. Crustacés Amphipodes des sediments meublessubtidaux des lagunes d’Albufeira et Obidos (Portugal). Péracarides (Amphi-podes, Cumacés et Mysidacés) de la zone cotière de la lagune d’Obidos. CiênciaBiológica. Ecological Systems 5, 251e267.

Rodrigues, A.M., Meireles, S., Pereira, T., Quintino, V., 2006. Spatial patterns ofbenthic macroinvertebrates in intertidal areas of a Southern European estuary:The Tagus, Portugal. Hydrobiologia 555 (1), 99e113.

Rodrigues, A.M., Pires, A., Mendo, S., Quintino, V., 2009. Diopatra neapolitana DelleChiaje, 1841 and D. marocensis Paxton, Fadlaoui and Lechapt, 1995 from thePortuguese coast: morphological and genetic comparison. Estuarine Coastaland Shelf Science 85, 609e917.

Rodrigues, A.M., Quintino, V., 1985. Estudo granulométrico e cartografia dos sed-imentos superficiais da Lagoa de Óbidos (Portugal). Communication of theService Geology Portugal 71 (2), 231e242.

Rodrigues, A.M., Quintino, V., Sampaio, L., Freitas, R., Neves, R., 2011. Benthicbiodiversity patterns in Ria de Aveiro, Western Portugal: environmental/bio-logical relationships. Estuarine Coastal and Shelf Science 95, 338e348.

Smith, S.D.A., Rule, M.J., 2001. The effects of dredge-Spoil dumping on a shallowwater soft-sediment community in the Solitary Islands Marine Park, NSW,Australia. Marine Pollution Bulletin 42, 1040e1048.

Szymelfenig, M., Kotwicki, L., Graca, B., 2006. Benthic re-colonization in post-dredging pits in the Puck Bay (Southern Baltic Sea). Estuarine Coastal andShelf Science 68, 489e498.

Van der Veer, H.W., Bergman, M.J.N., Beukema, J.-J., 1985. Dredging activities in theDutch Wadden Sea: effects on macrobenthic fauna. Netherlands Journal of SeaResearch 19, 183e190.

Van der Wall, D., Forster, R.M., Rossi, F., Hummel, H., Ysebaert, T., Roose, F.,Herman, P.M.J., 2011. Ecological evaluation of an experimental beneficial usescheme for dredged sediment disposal in shallow tidal waters. Marine PollutionBulletin 62, 99e108.

Van Dolah, R.F., Calder, D.R., Knott, D.M., 1984. Effects of dredging and open-waterdisposal on benthic macroinvertebrates in a South Carolina estuary. Estuaries 7,28e37.

Wilber, D.H., Clarke, D.G., Rees, S.I., 2007. Responses of benthic macroinvertebratesto thin-layer disposal of dredged material in Mississippi Sound, USA. MarinePollution Bulletin 54, 42e52.