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Sediment-related distribution patterns of nematodes and macrofauna: Two sidesof the benthic coin?

Jan Vanaverbeke a,*, Bea Merckx a, Steven Degraer b, Magda Vincx a

aGhent University, Biology Department, Marine Biology Section, Krijgslaan 281/S8, B-9000 Gent, BelgiumbRBINS-MUMM, Marine Ecosystem Management Section, Gulledelle 100, 1200 Brussel, Belgium

a r t i c l e i n f o

Article history:Received 26 May 2010Received in revised form29 September 2010Accepted 30 September 2010

Keywords:NematodesMacrobenthosBiogeochemistrySpatial distribution

a b s t r a c t

We investigated the sediment-related distribution of both nematodes and macrofauna on the Belgianpart of the North Sea (Southern Bight of the North Sea) in order to evaluate whether both faunal groupsreflect similar patterns in community composition and diversity. Fine-grained sediments (median grainsize <200 mm) were inhabited by nematode communities characterised by a low diversity and domi-nated by non-selective deposit-feeding nematodes. Nematode communities from coarser sedimentswere significantly different in terms of community composition and diversity. Moreover, all nematodefeeding types were present in coarser sediments. These differences were explained by the contrastingbiogeochemical processes prevailing in both sediment types, rather than granulometry and food avail-ability per se. Macrofaunal distribution patterns were different from those of the nematode communitiesand seem to be related to water column processes (SPM loading, food availability, hydrodynamic stress)that promote the establishment of diverse communities in the coarser sediments but not in the finestsediments. This suggests that data on nematodes and macrofauna reveal different, complementaryaspects of the factors structuring the benthic ecosystem that can be of importance in assessing theecological status of the seafloor.

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1. Introduction

As a consequence of the ever growing anthropogenic impact onthe marine ecosystem, there is increasing demand for scientificdata underpinning a sustainable management of the marine envi-ronment. The European Marine Strategy Framework Directive(2008/56/EC) creates a framework withinwhich European memberstates should take the necessary measures to achieve or maintaina good environmental status in themarine environment by the year2020. Seafloor integrity (i.e. the combination of spatial connect-edness and having natural ecosystem processes functioning incharacteristic ways, Rice et al., 2010) should be at a level thatensures the structure and functions of the ecosystem to be safe-guarded and benthic ecosystems should not be adversely affected.One of the qualitative descriptors of good environmental status isa description of the biological communities associated with thepredominant seabed habitats. So far, ecological status (e.g. in theframework of the implementation of the European Water Frame-work Directive) was based on a large variety of biotic indices based

on data on macrofauna (Gremare et al., 2009) which is justified bythe fact that macrofauna is ecologically important and obviouslypresent, resulting in a wide availability of data on the spatialdistribution of the macrofauna (e.g. Arvanitidis et al., 2009). For thesame reasons, it is realistic to assume that biological indicators forthe description of seafloor integrity will be based on data onmacrofauna as well. Although the smaller sized nematodes areknown to be good indicators of the health of the benthic environ-ment also (Heip et al., 1985; Kennedy and Jacoby,1999), they are notconsidered when assessing the ecological status of the benthicenvironment, probably since extensive datasets covering the needsfor the Water and Marine Strategy Framework Directive purposesare lacking. However, it is to be expected that the communitycharacteristics of both size groups reflect different aspects of thebenthic environment as the small size of the nematodes induces aninterstitial life style opposite to the burrowing of surface dwellingbehaviour of the larger macrofauna (Schwinghamer, 1981). Thedistribution of macrofauna was linked to the combination ofa variety of environmental variables such as grain size, organic andmicrobial content, food supply, trophic interactions (Snelgrove andButman, 1994) and interactions between the organisms and thesediment (Gray, 1974). On the other hand, information on thefactors influencing the spatial distribution of nematodes is still

* Corresponding author. Tel: þ32 9 264 85 30; fax: þ32 9 264 85 98.E-mail address: jan.vanaverbeke@ugent.be (J. Vanaverbeke).

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limited and based on a relatively low number of papers reportingon results gathered from sampling a narrow range of sedimenttypes or a limited amount of stations. Nematode distribution hasbeen mainly linked to granulometric variables (Vanreusel, 1990;Vincx et al., 1990; Vanaverbeke et al., 2002) in combination withtrace metals (Schratzberger et al., 2006). However, detailedresearch on the vertical distribution of nematodes highlighted theimportance of sediment biogeochemistry, food availability andsediment oxygenation (Steyaert et al., 1999; Vanaverbeke et al.,2004a,b; Franco et al., 2008a) but these findings were nevercoupled with the spatial distribution of nematode communities. Inthis paper, we analyse two datasets on the nematode communitiesand macrofauna of the Belgian Part of the North Sea (SouthernBight of the North Sea), covering a wide variety of sediment types.We aim to understand the factors governing the spatial distributionof nematodes by integrating the spatial patterns with the recentlydeveloped ideas on the influence of biogeochemical processes onnematode communities. Characterisation (Van Hoey et al., 2004)and mapping (Degraer et al., 2008) of macrobenthic communitiesat the BPNS was done before and will not be repeated here. Weused the data from Degraer et al. (2008) to compare patterns incommunity composition and diversity of nematodes with similarpatterns in the macrofauna from the same area. This integratedanalysis of different benthic groups with differing life historystrategies and abilities to cope with local environmental stress willresult in a more holistic view of the benthic ecosystem needed forthe implementation of ecosystem-based approaches to marinemanagement.

2. Material and methods

Analysis of similarities in spatial distribution and diversity ofdifferent size groups within the benthos is ideally performed usingdata on both macrofauna and meiofauna that are simultaneouslycollected at identical stations. To our knowledge, these kind of

analyses were only performed twice, based on data collected ina relatively small number of stations (Schratzberger et al., 2006: 19stations along the UK coast in the southwestern North Sea;Schratzberger et al., 2008b: 18 stations in the Celtic Deep and NWIrish Sea) covering a narrow range of sediment types. In order toincrease the knowledge on similarities in distribution of differentlysized benthic groups in a wider ecological setting, we used inde-pendently collected databases representing a wide variety ofsediment types within a rather limited area (3600 km2). All datawere collected by a single research team using the same techniquesat all sampling stations and moments, excluding possible meth-odological bias in the data.

2.1. Study site

The Belgian Part of the North Sea (BPNS) is located in theSouthern Bight of the North Sea (Fig. 1) and has a surface of3600 km2. Despite being small, the BPNS is characterised bya highly variable and complex topography due to the presence offour series of sandbanks (Maes et al., 2005) and by highly variablesediments (Verfaillie et al., 2006). Both meiofauna and macrofaunawere sampled extensively at the BPNS (Fig. 1), resulting in a goodrepresentation of all habitats among the available data.

2.2. Nematode data

Nematode data were obtained from the MANUELA database,which contains 83 component datasets on meiobenthos fromalmost 1300 stations, representing about 140 000 distributionrecords (Vandepitte et al., 2009). This database was queried fordatasets containing both nematode species information and dataon median grain size gathered on the BPNS. All data were collectedand treated in the same way. Sediment sampling was done usingreplicate drops of a Reineck boxcorer, which was subsampled with10 cm2 perspex cores. Macrobenthos was removed by sieving the

Fig. 1. Sampling locations on the Belgian Part of the North Sea. Left panel: nematode sampling locations; right panel macrofauna sampling locations.

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samples over a 1-mm sieve; organisms retained on a 38 mm sievewere included in the analysis. Meiobenthos was extracted from thesediment using the ludox-flotation method (Heip et al., 1985),counted and nematodes were mounted in slides for identification.We only included nematodes identified to species level in theanalysis. Documented (e.g. unpublished drawings in Vincx (1986)and unpublished personal drawings of Jan Vanaverbeke) putativespecies were included in the analysis as well. Nematodes wereallocated to feeding types according to Wieser (1953). This classi-fication is based on the morphology of the buccal cavity and 4feeding tubes are discerned: 1A nematodes (selective deposit-feeding nematodes, with a small toothless buccal cavity); 1Bnematodes (non-selective deposit-feeding nematodes, with largetoothless buccal cavity), 2A nematodes (epistrate feeders, withsmall teeth in the buccal cavity) and 2B nematodes (predators/omnivores, buccal cavity equippedwith large teeth andmandibles).When stations were repeatedly sampled in the same year, we onlyincorporated data obtained in summer/fall in order to exclude theless diverse winter months (Vanaverbeke et al., 2004b). The finaldataset consisted of data on 443 nematode species encountered on74 sampling occasions.

2.3. Macrofauna data

The dataset used for analyses of macrofaunal distributionpatternwas described in Degraer et al. (2008). This dataset containsdata on themacrofauna from the BPNS, collected between 1994 and2004. All samples were collected with a Van Veen grab (samplingsurface: 0.1 m2) and sieved over a 1-mm sieve. The dataset wasquality controlled and rare species were excluded (Degraer et al.,2008). This final dataset initially consisted of 123 species encoun-tered in 773 samples. However, as this dataset contained samplescollected in much coarser sediments than the nematode samples,we excluded macrofaunal samples collected in sediments witha median grain size >500 mm, in order to compare nematode andmacrofaunal distribution patterns over a similar granulometricrange. This resulted in a final dataset consisting of 743 samples and119 species.

2.4. Analysis of community structure

In a first step, we investigated whether nematode communitiessampled from comparable sediments (using median grain size asa proxy for granulometry) harboured nematode communities thatwere more similar than communities collected in differing sedi-ments. Stations were allocated to sediment classes (e.g. class ‘0’:median grain size between 0 and 100mm; class ‘1’: median grainsize between 101 and 200 mm.). In total 5 sediment classes weredistinguished. Analysis of similarities (ANOSIM)was used to test fordifferences in nematode communities from different sedimentclasses, using log(xþ 1) transformed nematode mean abundances(average of 2 or 3 replicates). The log(xþ 1) transformation wasused to minimize possible differences in nematode densities asa consequence of interannual or seasonal variation while main-taining dominance patterns in the data. Results were visualisedusing non-metric Multidimensional Scaling (MDS). The SIMPERroutine was used to identify the nematode species having impor-tant contributions to within group (i.e. within the same sedimentclass) similarity. A cut-off of 50% was used.

In a second step, we investigated whether sediment-relatedcommunity patterns in nematodes, total macrofauna, and importantmacrofaunal taxa (bivalves, gastropods, crustacea and polychaetes)were similar innature. Therefore, sampling stationswere allocated tosediment classes following Arvanitidis et al. (2009) who allocatedstations to geographical provinces andSchratzberger et al., 2006who

allocated stations to geographical rectangles. The new datasets werepresence/absence transformed and similarity matrices were con-structed based on the Jackard coefficient (Legendre and Legendre,1998) and analysed by MDS. Weighted Spearman’s rank correla-tions between these similarity matrices were calculated and used asinput for a second stage MDS. This allows for a comparison of thesediment-related distribution patterns exhibited by the differentfaunal groups. All analyses were performed using Primer 6 (Clarkeand Gorley, 2001). Diversity was investigated by calculating theShannoneWiener diversity index (H0 ¼ �S(pi*loge pi); pi¼ relativeabundance of each species in a sample) . Differences in H0 betweensedimentclasseswere investigatedusing1-wayAnalysisofVariances(ANOVA) after checking for assumptions. When the assumptionswere not met, the non-parametric KruskaleWallis analysis by rankswas applied. When significant differences were observed in theANOVA approach, Tukey’s HSD for unequal N was used to test forpairwise differences between sediment classes. H0 was calculatedusing Primer 6; all ANOVA and KruskaleWallis analyses were per-formed using the Statistica 6 software package.

3. Results

3.1. Sedimentological environment

Median grain size in the nematode database ranged between 88and 494 mm. The majority of the samples (84%) were allocated tosediment class 2 and 3 (i.e. median grain size between 201 and400 mm) (Table 1). Median grain size values in the macrofaunaldatabase ranged between 16 and 490 mm. Again, most sampleswere collected in sediments allocated to sediment class 2 (38%) and3 (31%). However, samples in size class 1 (15%) and size class 4 (12%)were well sampled as well.

3.2. Nematode community structure

Differences in median grain size are reflected in nematodecommunities (ANOSIM: R¼ 0.4, p¼ 0.001; Fig. 2). Pairwisecomparisons between median grain size classes revealed thatnematode communities were increasingly dissimilar withincreasing difference between median grain size classes. Relativelylow differences (pairwise R between 0.11 and 0.24) were observedbetween nematode communities from coarser sediments (sedi-ment classes representing median grain sizes >200 mm) whencompared to differences in nematode communities from the finersediments (pairwise R¼ 0.48 for pairwise comparison of sedimentclasses 0 and 1) (Table 2). This is reflected in the SIMPER analysis(Table 3): Onyx perfectus, Neochromadora munita, Theristus maiorandMicrolaimus marinus are listed among the important nematodespecies in the three size classes with a median grain size >200 mm,while several other species (e.g. Xyala striata, Enoploides spiculo-hamatus, Tubolaimoides aff. tenuicaudatus, Desmodora schulzi) are

Table 1Distribution of samples over the sediment classes for all investigated groups(Sediment class 0: median grain size between 0 and 100 mm. Sediment class 1:median grain size between 101 and 200 mm. Sediment class 2: median grain sizebetween 201 and 300 mm. Sediment class 3: median grain size between 301 and400 mm. Sediment class 4: median grain size between 401 and 500 mm).

Sediment class 0 1 2 3 4 Total

Nematoda 3 4 16 46 5 74Total macrofauna 32 109 283 228 91 743Bivalvia 23 104 183 100 53 463Gastropoda 1 15 57 7 10 90Polychaeta 28 108 280 226 91 733Crustacea 28 86 260 176 74 624

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listed in two neighbouring sediment classes. The abundant speciesof finer grain sediments (<200 mm) are different to those of coarsersediments. Sabatieria punctata contributed strongly to the simi-larity of the nematode communities of both sediment classes 0 and1, but no other species were abundant in both sediment classes.Similarity within sediment classes 0 and 1 was mainly due to thepresence of 1B nematodes. This is certainly not the case in coarsersediments, where all feeding types were represented in eachsediment class and where the contribution of nematodes withteeth (2Aþ 2B nematodes) exceeds the contribution of deposit-feeding (1Aþ 1B) nematodes.

3.3. Sediment-related patterns in distribution and diversity ofmacrofauna and nematodes

The multivariate pattern described above was found whenanalysing presence/absence of nematode species within sedimentmedian grain size classes as well: nematode communities inhab-iting sediments with a median grain size >200 mm are differentfrom nematode communities inhabiting finer grained sediments(Fig. 3A). Grain size classes were plotted more close to each otherwhen representing coarser sediments compared to lower mediangrain size classes, pointing at a higher similarity of communitiesfrom coarser sediments. Similar analyses for the entiremacrofaunalcommunities and macrofauna taxa separately yielded differentoutcomes (Fig. 3BeF): crustaceans and the total macrofaunacommunities inhabiting sediments from median grain size class0 strongly differed from coarser sediments. This large differencewas less obvious when inspecting the MDS plots for polychaetesand gastropods, while bivalve communities seemed to be spreadmost evenly over the MDS plot. Further analysis (2nd stage MDS,Fig. 4 and weighted Spearman’s rank correlations, Table 4)confirmed that the multivariate sediment-related distributionpatterns of nematode communities and polychaetes were moresimilar than the patterns of nematode communities and all mac-rofauna and any other macrofaunal taxon. Largest differences wereobserved between distribution patterns revealed by nematodecommunities and bivalves.

A comparison of sediment-related diversity, expressed as H0 fornematode communities, macrofauna and macrofaunal taxarevealed significant differences for most taxa (Fig. 5). Diversitywas significantly different for nematode communities (1-wayANOVA: F4,69¼ 22.14; p< 0.001) and Tukey HSD for unequal Nshowed that H0 values for median grain size classes 0 and 1 were

significantly different (p< 0.05) from values calculated for mediangrain size class 3e5. Significant differences in H0 values betweenmedian grain size classes were observed for bivalves (Krus-kaleWallis analysis by ranks: H¼ 57.69; p< 0.001), crustaceans(KruskaleWallis analysis by ranks: H¼ 41.69; p< 0.001), poly-chaetes (KruskaleWallis analysis by ranks: H¼ 10.61, p< 0.05)and total macrofauna (1 way ANOVA: F4,738¼ 11.85, p< 0.001).Tukey HSD for unequal N revealed significant differences(p< 0.05) in diversity between median grain size class 0 and allother classes, and between median grain size class 3 and 4. Onlygastropod diversity was not significantly affected by differences inmedian grain size (KruskaleWallis analysis by ranks: H¼ 5.11;p> 0.05).

4. Discussion

4.1. Nematode community patterns

Our results confirm the earlier findings from large-scale studies(Heip et al., 1990; Vincx et al., 1990) showing that nematodecommunity composition and diversity are different in differentsediment types. This is not surprising, as the database used for thepresent paper includes most of the data from the mentionedpapers. Furthermore, similar findings were reported in analyses ofnematode communities from other locations in the North Sea,although based on less stations and more narrow sediment ranges(Schratzberger et al., 2006, 2008a). These differences have beenexplained by a variety of (combinations) of environmental variablessuch as median grain size, clay/silt fractions, food availability,eutrophication and presence of heavy metals (Vincx et al., 1990;Schratzberger et al., 2006, 2008a,b). Therefore, we expected thatchanges in nematode community composition and diversity wouldappear gradually along a gradient in sediment composition(Vanaverbeke et al., 2002). However, our analyses do not revealgradual changes as both nematode community composition anddiversity shift strongly between communities inhabiting sedimentswith a median grain size <200 mm and those living in coarser(median grain size >200 mm) sediments. Indeed, when plotting H0

as a function of median grain size (Fig. 6) it becomes clear that thereis no gradual increase in nematode diversity when median grainsize increases from 100 and 200 mm to coarser median grain sizes.Low H0 values encountered in sediments with a median grain size>200 mmwere always sampled in FebruaryeMarch when diversityis significantly lower in comparison with later months(Vanaverbeke et al., 2004a). Neglecting these winter diversityvalues reveals a graph with low values (<1.5) of H0 in most finesediments, and consistently higher values (H0 ¼ 2e4) in sedimentswith a median grain size >200 mm. We therefore suggest thatsediment granulomety is only indirectly shaping nematodecommunities and we hypothesise that the biogeochemical envi-ronment, resulting from the interplay between hydrodynamicfeatures and granulometry is a key factor structuring nematodecommunities. The biogeochemical characteristics of marine sedi-ments are greatly influenced by the permeability (the capacity ofthe sediment to transport fluids) of the sediment. The influence of

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Fig. 2. Result of MDS analysis on log(xþ 1) transformed nematode densities of allsampling stations on the Belgian Part of the North Sea.

Table 2R-statistics for pairwise ANOSIM, testing for differences in nematode communitycomposition between different median grain size classes.

Class 0 Class 1 Class 2 Class 3

Class 1 0.48Class 2 0.67 0.50Class 3 0.95 0.88 0.24Class 4 1 0.9 0.11 0.17

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the water flow on the biogeochemical processes becomes impor-tant when permeability exceeds 2.5*10�12 m2 (Forster et al., 2003;Wilson et al., 2008). These pore water flows can reach the upper30 cm of sediment (Wilson et al., 2008), providing this part of thesediment with oxygen. This largely increases the sediment volumethat efficiently participates in organic matter decomposition, andresults in sediments of a non-accumulating and organic poorcharacter (Huettel and Rusch, 2000) caused by the fast minerali-sation of organic matter deposited on the sea floor (Rusch et al.,2006). Inclusion of clay and silt, even in small percentages canreduce permeability by orders of magnitude (Wilson et al., 2008)and molecular diffusion and the activities of benthic fauna are thenthe main transport mechanisms for solutes in fine-grained sedi-ments (Aller,1988). The arrival of organicmatter in these sedimentsis often associated with oxygen stress (Graf, 1992), accumulation oforganic matter and retarded mineralisation (Boon and Duineveld,1998). Sediment permeability was never directly measured insediments at the BPNS and data needed for the calculation ofpermeability are not available for most of the stations. We useda dataset from the BPNS (Van Hoey et al., 2009) containing thenecessary data to calculate sediment permeability according to

Hazen (kH¼ 1.1019*103 m�2 s*d210*n; with kH¼ permeability;d210¼ first decile of the grain size distribution and n¼ kinematicviscosity, (Rusch et al., 2001)). Obtained values were correctedaccording to Rusch et al. (2001). About 75% of the sediments witha median grain size <200 mm had a permeability <2.5*10�12 m2

whereas permeability in all coarser sediments exceeded 10�10 m2

(Supplementary material, Fig. 1). Oxygen penetration depth in thesediment (deduced from oxygen profiles or visual inspection of theredox potential discontinuity layer) in the fine-grained sedimentswas much lower compared to the coarser sediments throughoutmost of the year (Supplementary material, Fig. 2), confirming thepresence of biogeochemically different sediments at the BPNS.

Our results indicate that sediments with an increased perme-ability (median grain size >200 mm) were inhabited by nematodecommunities characterised by a high diversity and an importantcontribution of 2A and 2B nematodes to within-class similarity.This suggests a presence of wide range of food items sustaining thevariety of feeding habits present in the community. Detailedinvestigations carried out in the permeable sediments of St. 330(Vanaverbeke et al., 2004a,b; Franco et al., 2007, 2008a) indeedshowed low concentrations of chl a (a proxy for labile organic

Table 3Results of the SIMPER analysis for the nematode communities on the Belgian Part of the North Sea., listing the main characterising species and feeding types per median grainsize class.

Sediment class 0 (median grain size:0e100 mm)

Sediment class 1 (median grain size:101e200 mm)

Sediment class 2 (median grain size: 201e300 mm)

Average similarity: 58.82 Average similarity: 41.41 Average similarity: 26.03

Species FT Contrib% Species FT Contrib% Species FT Contrib%

Sabatieria punctata 1B 41.39 Sabatieria punctata 1B 31.03 Onyx perfectus 2B 7.40Ascolaimus sp. 1 1B 22.16 Ascolaimus elongatus 1B 18.65 Viscosia franzii 2B 7.17

Daptonema tenuispiculum 1B 15.79 Xyala striata 1B 6.64Neochromadora munita 2A 6.05Enoploides spiculohamatus 2B 6.04Theristus maior 1B 4.78Tubolaimoides aff. tenuicaudatus 1A 3.53Bathylaimus capacosus 1B 3.28Microlaimus marinus 2A 2.94Calomicrolaimus monstrosus 2A 2.90

Feeding type contribution (%) Feeding type contribution (%) Feeding type contribution (%)

1A 0 1A 0 1A 3.531B 63.56 1B 65.46 1B 14.72A 0 2A 0 2A 11.892B 0 2B 0 2B 20.61

Sediment class 3 (median grain size: 301e400 mm) Sediment class 4 (median grain size: 401e500 mm)

Average similarity: 29.06 Average similarity: 29.64

Species FT Contrib% Species FT Contrib%

Onyx perfectus 2B 6.4 Neochromadora munita 2A 9.6Chromaspirina pellita 2B 4.81 Microlaimus marinus 2A 6.62Xyala striata 1B 4.76 Ixonoma sordidum 2A 6.44Neochromadora munita 2A 4.11 Onyx perfectus 2B 5.47Enoploides spiculohamatus 2B 4.09 Desmodora schulzi 2A 5.12Microlaimus marinus 2A 3.58 Rhynchonema lyngei 1B 4.62Desmodora schulzi 2A 3.47 Theristus bastiani 1B 4.02Chromaspirina parapontica 2B 2.94 Theristus maior 1B 3.31Tubolaimoides aff. tenuicaudatus 1A 2.94 Paracyatholaimus pentodon 2A 3.23Dichromadora cucullata 2A 2.80 Prochromadorella ditlevensi 2A 3.19Chromadorita n.sp. 2 MV 2A 2.21Theristus maior 1B 2.16Ixonema sordidum 2A 2.13Calomicrolaimus honestus 2A 2.01Sabatieria celtica 1B 1.86

Feeding type contribution (%) Feeding type contribution (%)

1A 2.94 1A 01B 8.78 1B 11.952A 20.33 2A 34.22B 13.43 2B 5.47

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matter (Boon and Duineveld, 1996)), fully oxygenated sedimentsand the presence of bacteria in high densities (comparable to fine-grained sediments). Although chl a values were very low, subsur-face peaks were often detected (Vanaverbeke et al., 2004b; Francoet al., 2008a) suggesting deep penetration of phytodetritus byadvective currents through the sediment (Ehrenhauss and Huettel,2004). This, together with the presence of relatively high numbers

of bacteria (Franco et al., 2007) constitutes the expected food itemsof 1A, 1B and 2A nematodes while these nematodes itself (togetherwith other biota) act as food for the predatory 2B nematodes.

Similarity of nematode communities inhabiting sediments witha median grain size <200 mm was mainly due to a limited numberof non-selective deposit feeders (1B). In other fine-grained sedi-ments (median grain size <200 mm) outside the BPNS, deposit-feeding nematodes are abundant as well, however 2A nematodesare often dominant (Schratzberger et al., 2008a). This supports ourhypothesis that nematode communities are not solely structuredby granulometric characteristics. Sediments investigated bySchratzberger et al. (2008a) are located in more offshore, deeperareas where input of organic matter is much lower compared to ourcoastal stations. Franco et al. (2008a) mention maximum monthlychl a concentrations of >400 mgm�2 at a fine-grained station at13 m depth at the BCS, whereas Schratzberger et al. (2008a) reportmaximum monthly values of only 72 mgm�2 at 55 m water depthoff the coast of the UK, reflecting the difference in surface primaryproduction between both areas (Franco et al., 2008a; Schratzbergeret al., 2008a). Although Schratzberger et al. (2008a) do not mentiondata on vertical profiles and oxygen conditions, it is doubtful that

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Fig. 3. Result of MDS analyses on presence/absence data for different macrofaunal taxa and nematodes. Stations were allocated to median grain size classes.

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Fig. 4. 2nd stage MDS based on the Spearman’s rank correlations between similaritymatrices of original MDS analyses (see Fig. 3). Each symbol represents the spatialpattern of a taxon/group at the Belgian Part of the North Sea.

Table 4Weighted Spearman’s rank correlation coefficients between the similarity matricesof nematodes and macrofaunal taxa.

All macrofauna Bivalvia Gastropoda Crustacea Polychaeta

Nematoda 0.74 0.12 0.78 0.58 0.89

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conditions in the sediments at greater depths are as harsh as at theshallower BPNS where fine sediments are characterised by sharpvertical profiles of chl a concentrations (Franco et al., 2008a;Steyaert et al., 1999), anoxia at relatively shallow sediment depths(Braeckman et al., 2010) and accumulation of ammonia in deepersediment layers (Steyaert et al., 1999). Prey nematodes for preda-tory nematodes are available and it is difficult to believe that thefood sources (bacteria, phytodetritus) exploited by other nematodefeeding types at coarser sediments, and fine-grained sediments atgreater depths are absent at the shallow fine-grained sediments ofthe BPNS. Therefore the absence or low densities of epistratefeeding and predatory nematodes cannot be attributed to a lack offood particles and we suggest that the oxygen stressed environ-ment hampers the development of nematode communities that

include high densities of epistrate and predatory nematodes. This issupported by the observation that 2A nematodes (Chromadora/Ptycholaimellus) migrate away from anoxic spots in the sediment(Franco et al., 2008b) or experience high mortality in experimentalanoxic/suboxic set ups (Steyaert et al., 2007). Deposit-feedingnematodes are not limited to fine-grained sediments (Table 3),however different species contribute importantly to within sizeclass similarity in fine and coarse sediments, suggesting thatdeposit-feeding itself is not an adaptation to surviving oxygenstress. Soetaert et al. (2002) suggested that certain body sizedimensions can be seen as adaptations to live in oxygen stressedenvironments while the opportunistic feeding behaviour of Saba-tieria species (Franco et al., 2008a) explains the high densities ofmembers of this genus in reduced sediments. However, more

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Fig. 5. Mean (�SE) of ShannoneWiener diversity for nematode communities and macrofaunal taxa per median grain size class.

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research is needed to further clarify the mechanisms behindnematode survival in shallow anoxic environments.

4.2. Sediment-related distribution patterns of nematodes andmacrofauna

Our data suggest that the distribution of macrofauna andnematodes is not as similar as previously accepted based on morelimited datasets (Schratzberger et al., 2006). The decreased diver-sity in both sediment classes 0 and 1 was not found for the totalmacrofauna and themacrofaunal taxa. This suggests that the anoxicconditions, expecting to reduce nematode diversity (cr. above) arenot strongly influencing the larger organisms. The lowmacrofaunaldiversity in the finest sediments (class 0) can possibly be related tothe fact that these sediments are located in areas with an increasedamount of suspended particular matter (SPM) (Fettweis et al.,2007) where for many taxa morphological/physiological adapta-tions are required to maintain feeding effective rates and/orprevent clogging of the filter apparatus (Riisgard et al., 2002; Barilléet al., 2006; Dubois et al., 2009). In sediment class 1, wherenematode diversity is still low as a consequence of the biogeo-chemical environment, high diversity of total macrofauna andwithin macrofaunal taxa is observed. The amount of SPM in thewater column is not as high as in the previously mentioned areas(Fettweis et al., 2007). Furthermore, macrobenthic species are largeenough to modify the anoxic sediments to create a habitat whereoptimal circumstances are reached. Indeed, bioturbation and bio-irrigation provide the oxygen stressed sediments locally withoxygen (Braeckman et al., 2010, and references therein) enablingthe macrofaunal species to benefit from the high supply of freshorganic matter (Van Oevelen et al., 2009) without experiencing thenegative effect of a reduced environment, resulting in amacrofaunacommunity characterised by a high diversity.

Another difference in nematode and macrofaunal diversity is tobe found in sediments with a median grain size exceeding 300 mm.Here, nematode diversity remains high, which is not the case fortotal macrofauna and most of the macrofaunal taxa. Van Hoey et al.(2004) also described this decrease in macrofaunal diversity withincreasing grain size and showed that variability at the speciesrichness and species assemblage level decreased as well. Sincea fully oxygenated environment is not required by the macrofauna,the availability of oxygen does not have the same impact as onnematode species. In contrast, the relatively high hydrodynamic

stress (responsible for the coarse grain size and hence the perme-ability and subsequent oxygenation) may prevent the establish-ment of many sessile polychaetes (Van Hoey et al., 2004) and thesettlement of macrobenthic larvae (Pawlik and Butman, 1993;Jonsson et al., 2004). This, in combination with the relatively lowfood availability can explain the observed low diversity anddecreased variability.

The sediment-related distribution patterns of the polychaetesshowed the best resemblance with the nematode distributionpattern. For both taxa, the difference in community compositionbetween fine (median grain size <200 mm) and coarser sedimentswas obvious, but for both taxa a relatively large difference betweensediment class 0 and 1 was observed as well. It is not clear whetherthese patterns in polychaete communities can be linked to sedi-ment biogeochemistry as well. Some polychaetes, present in rela-tively fine sediments (e.g. Lanice conchilega, Owenia fusiformis)create tubes that can be oxygenated by bioirrigation (Braeckmanet al., 2010) enabling species with this behaviour to survive inanoxic sediments where the SPM load does not lead to decreasedfeeding rates (e.g. in sediment class 1).When SPM loading increases(i.e. in areas with the finest sediments) these species do not survivewhile in coarser sediments they are replaced by burrowing/diggingpolychaetes that are otherwise negatively impacted by the pre-vailing oxygen stress.

Although our results indicate that multivariate patterns ofnematode communities and total macrofauna communities revealdifferent aspects of the marine benthic ecosystem, direct implica-tions for the assessment of the health of marine sediments remainunclear. The implementation of the Water Framework Directiveresulted in the development of a wide range of indices based onmacrofaunal communities. Although there is a considerable diver-sity in these indices, they are mainly based on the same paradigm(Gremare et al., 2009): disturbances generate secondary succes-sions during which tolerant species are initially dominant and areprogressively replaced by sensitive species (i.e. the Pear-soneRoseberg model (Pearson and Rosenberg, 1978)). Literature onnematode-based indices is scarce, but promising (Moreno et al., inpress). Nematode initial recovery from disturbance has been notedto be faster than macrofaunal recovery, but full recovery trajecto-ries of nematodes cannot be uncoupled frommacrofaunal activities(Van Colen et al., 2009). As such, nematode communities mightshow a faster response to disturbances affecting the ecologicalstatus of the seafloor. However, integrated research during whichboth macrofaunal and nematode-based indices are calculated iscompletely lacking so far. This kind of studies cannot be based onmeta-analyses of historical datasets and should result from inte-grated sampling campaigns covering a wide range of sediments.

5. Conclusions

Our results strongly suggest that the distribution of nematodecommunities and local nematode diversity is related to sedimentbiogeochemistry. Anoxic conditions, developing in fine-grainedsediment reduce the survival chances of many nematode speciesresulting in communities dominated by deposit-feeding nema-todes and characterised by a low diversity. In sediments with anincreased permeability where nematodes do not have to cope withoxygen stress, highly diverse nematode communities developwhere all feeding types coexist. This strong difference is notobserved in the macrofauna communities or macrofaunal taxa,where community composition and diversity seem to be structuredby water column processes (SPM loading, food availability, hydro-dynamic stress) rather than biogeochemical features of the sedi-ment. All this suggests that data on macrofauna and nematodesreveal different aspects of the benthic ecosystem and future

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Fig. 6. Nematode ShannoneWiener diversity versus median grain size. Open symbolsrepresent winter samples.

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integrated research will result in a better understanding of thefactors influencing the ecological status of the seafloor.

Acknowledgements

We thank all data providers for submitting their data to thedatabases with nematode or macrofaunal data, and FlandersMarine Institute (VLIZ) for hosting a workshop where the initialanalyses for this paper were performed. This paper contributes tothe WestBanks project (www.vliz.be/projects/westbanks), which issupported by the Belgian Science Policy (BELSPO, contract numberno. SD/BN/01B) and to the UGent GOA BBSea project (GOA01600705).

Appendix. Supplementary material

Supplementary material associated with this article can befound in the online version, at doi:10.1016/j.marenvres.2010.09.006.

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