Small- to Large-Scale Geographical Patterns Within the Macrobenthic Abra Alba Community

Estuarine, Coastal and Shelf Science 64 (2005) 751e763 www.elsevier.com/locate/ECSS

Small- to large-scale geographical patterns within the macrobenthic Abra alba community

Gert Van Hoey*, Magda Vincx, Steven Degraer

Marine Biology Section, Department of Biology, Ghent University, Krijgslaan 281/S8, B-9000 Gent, Belgium

Received 29 November 2004; accepted 18 March 2005 Available online 27 June 2005

Abstract

The Abra alba community is widely spread in the coastal zone of the English Channel and the Southern Bight of the North Sea. The community is located on shallow, fine muddy sands. Its spatial distribution can be broken up into a number of isolated patches (Atlantic French, British and German coast) and one large continuous distribution area (northern France up to the Netherlands). The aim of this study is to investigate the geographical patterns within the macrobenthic A. alba community at different scales: the community’s full distribution range (i.e. large scale) and a selected area with a continuous distribution of the A. alba community (i.e. small scale) in relation to structuring environmental variables. Therefore, an analysis of newly collected samples along the Belgian coastal zone was combined with available information on the A. alba community throughout its distribution range. Although the community structure shows a high similarity across the full distribution range of the A. alba community, large- as well as small-scale changes in community composition were observed: the Belgian Continental Shelf (BCS) should be considered as a major transition from the rich southern to the relatively poorer northern distribution area of the A. alba community. At a large scale (i.e. full distribution range), the differences in community structure are expected to result from (1) the specific hydrodynamic conditions in the English Channel (Atlantic ocean waters) and the Southern Bight of the North Sea, with a consequent differential connectivity between the different areas and (2) the climatological and related faunal shift from temperate (English Channel) to boreal conditions (German Bight). At a small scale (i.e. within the continuous distribution area), structural and functional community aspects may result from geographic differences in (1) detrital food availability, related to riverine input and pelagic productivity, along and across the coastline and (2) the amount of suspended matter, impoverishing the A. alba community when excessively available. Ó 2005 Elsevier Ltd. All rights reserved.

Keywords: Abra alba community; large-scale; small-scale patterns; diversity; English Channel; Southern Bight of the North Sea

1. Introduction increasing concern amongst managers and policy-makers about the potential effects of biodiversity loss on the Nowadays, human activities are considered to be the ‘functioning’ of ecological systems, in particular the primary cause of changes to marine biological diversity goods and services, which they provide (Daily, 1997). (biodiversity), especially in coastal areas. The present rate There are indications that biodiversity can have significant of habitat degradation in marine ecosystems is alarming effects on ecosystem processes, although these effects (Gray, 1997; Snelgrove et al., 1997), and conservation of tend to be mediated through functional traits, rather biodiversity is of critical importance. There is also an than species richness per se (Raffaelli et al., 2003). The measurement and assessment of biodiversity however depend on spatial scale, and a comparison of only * Corresponding author. a few sites between areas is insufficient (Ellingsen, 2001). E-mail address: [email protected] (G. Van Hoey). A detailed knowledge of community diversity and

0272-7714/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2005.03.022 752 G. Van Hoey et al. / Estuarine, Coastal and Shelf Science 64 (2005) 751e763 differences within a single habitat type is needed to community, related to the changing environment, are differentiate among habitats (Ellingsen, 2001) and to documented (Holtmann et al., 1996; Fromentin et al., investigate its naturalness. 1996, 1997; Desroy et al., 2002; Van Hoey et al., 2004). One of the ecologically most important soft-sediment The Belgian part of this continuous area is very macrobenthic communities along the coastal areas of the suitable for investigating small-scale spatial changes English Channel and Southern Bight of the North Sea is within the Abra alba community characteristics, because the Abra alba community, which is characterized by (1) it is the central part of the continuous distribution a high diversity, abundance and biomass and typically area, (2) the community has an aberrant distribution occurs in muddy fine sandy sediments (Jones, 1950; pattern along the Belgian coast compared to the other Gle´marec, 1973; Cabioch and Glaçon, 1975; Souplet and areas, (3) a large dataset is available, and (4) a lot of Dewarumez, 1980; Kingston and Rachor, 1982; Prygiel environmental factors (hydro-sedimentology, river out- et al., 1988; Duineveld et al., 1991; Dewarumez et al., flows, human pressure) influence the area. 1992; Ku¨nitzer et al., 1992; Fromentin et al., 1996; The aim of this study is to investigate the geographical Holtmann et al., 1996; Olivier et al., 1996; Sanvicente- patterns (structural and functional level) within the Anorve et al., 1996; Fromentin et al., 1997; Thie´baut macrobenthic Abra alba community at different scales: the et al., 1997; Dauvin, 1998; Degraer et al., 1999; Rees community’s distribution range in the English Channel et al., 1999; Dauvin, 2000; Konstantinos et al., 2000, and North Sea (i.e. large scale) and a selected area with 2001; Budd, 2002; Desroy et al., 2002; Sanvicente- a continuous distribution of the A. alba community (i.e. Anorve et al., 2002; Dauvin et al., 2004; Van Hoey small scale) in relation to structuring environmental et al., 2004). This type of habitat typically occurs in low variables. This information will form a baseline for energy zones nearby the coast (Larsonneur et al., 1982). future comparisons and it will be contribute to a well- Several descriptions of the Abra alba community in considered conservation of marine biodiversity in the the European seas were made in the past three quarters coastal areas. of a century. From a limited assemblage of species described by Petersen (1911, 1913, 1918), to different specific traits of the A. alba community at different 2. Materials and methods places have lead to several adopted characterizations of the community: ‘Echinocardium cordatumeVenus gallina 2.1. Study area community (Ford, 1923), ‘boreal offshore muddy sand association’ (Jones, 1950), ‘A. alba community (Stripp, The study area covers the full Belgian Continental 1969), associations ‘P’ and ‘M’ (Eagle, 1973, 1975), etc. Shelf (BCS) (2600 km2) situated in the Southern Bight of The Abra alba community is dominated by species the North Sea. The BCS is characterized by the presence having a pelagic larval phase and shows important of several sandbank systems: (1) Coastal Banks, parallel annual changes in the pattern of recruitment of the to the coastline, (2) Flemish Banks, about 10e30 km dominant species (Dewarumez et al., 1986). Consequent- offshore of the western Belgian coast, (3) Zeeland ly, it is characterized by short lived and fast growing Banks, some 15e30 km offshore of the eastern Belgian species with a strong seasonal reproduction and by coast, and (4) Hinder banks, about 35e60 km offshore a high year-to-year variability (Gray et al., 1980; Arntz (Degraer et al., 1999). Because of the presence of these and Rumohr, 1986; Essink and Beukema, 1986; Beukema sandbank systems a high geomorphologic and sedimen- et al., 1993; Turner et al., 1995). The most important tological diversity is found (Degraer et al., 1999). The species are A. alba, Fabulina fabula, Lanice conchilega, physical, chemical and biological characteristics of the Nephtys hombergii and Pectinaria koreni (Prygiel et al., BCS are responsible for a gradient from turbulent, 1988; Desroy et al., 2002; Van Hoey et al., 2004). nutrient rich inshore-waters to more transparent and The Abra alba community is found in the English less productive offshore-waters. Channel and Southern Bight of the North Sea, mostly in bays, estuaries and in a narrow zone along the coastline 2.2. Data origin (Fromentin et al., 1997; Thie´baut et al., 1997; Rees et al., 1999; Konstantinos et al., 2000; Desroy et al., 2002; Within the framework of several studies a total of Dauvin et al., 2004). However, there is one large 1161 macrobenthos samples were collected at the BCS continuous distribution area of the A. alba community: between 1994 and 2003. After analyzing this dataset the coastal area, from Cap Griz-Nez (France) over with different multivariate methods (Twinspan, ordina- Belgium north to the Dutch coast (Vanosmael et al., tion, Cluster-analysis), as described in Van Hoey et al. 1982; Vermeulen and Govaere, 1983; Prygiel et al., 1988; (2004), 204 samples belonging to the same species Fromentin et al., 1997; Desroy et al., 2002). In this assemblage, catalogued as the Abra albaeMysella continuous area gradual changes of the species compo- bidentata community (further called the A. alba com- sition, abundance and diversity within the A. alba munity), were selected for this study. A species G. Van Hoey et al. / Estuarine, Coastal and Shelf Science 64 (2005) 751e763 753 assemblage was considered to represent a community content (volume percentage !64 mm) were used as because of (1) their extreme position along the habitat granulometric variables. gradient (depth, mud content and median grain size) After exclusion of species that were not sampled and, consequently, (2) the absence of overlap between quantitatively (e.g. hyperbenthic and extremely rare the habitat of each species assemblage, based on the taxa) and lumping taxa, because of inconsistent results of the multivariate analyses (Van Hoey et al., identification throughout the different studies (e.g. genus 2004). This community description is based on two level: Bathyporeia, Ensis, Spio and Harmothoe; family approaches to delineate communities (Morin, 1999): level: Cirratulidae), a set of 104 taxa (further referred to (1) physically, by discrete habitat boundaries, and (2) as species) was used for biological analyses. statistically, by patterns of assemblages among species. The discrimination of communities however is a merely arbitrary abstraction of biological gradients: gradual 2.3. Data analysis transitions between macrobenthic communities exist (Gray, 1981). Even within a single habitat type there 2.3.1. Mapping are small differences (Ellingsen, 2001), as will be The map of the BCS is rotated (angle a, parallel with investigated in this study for the A. alba community. the coastline) to investigate the distribution gradient of The set of 204 samples (120 stations) retained by the Abra alba community on the BCS on all the figures. multivariate analyses were accepted as representative The original calibration (UTM: Easting (m) between for the A. alba community. To avoid outbalancing of 451408 and 520000 and Northing (m) between 5659860 stations that were sampled more than once between and 5728240) of the map was transformed as follows: 1994 and 2003 (i.e. temporal series), these stations were the x-coordinates are recalculated by x#Zx cos aCy sin represented by one randomly selected sample. The final a; the y-coordinates are recalculated by y#Zÿx sin aCy reduced dataset, used for all analyses, thus contains cos a. The recalculated x-coordinates (x#) now show the information of 120 samples from 120 different stations distance along the coastline (0 m, FrencheBelgian border; distributed along the Belgian Coast and sampled over 65000 m, DutcheBelgian border), while the recalculated a 9-year period (Fig. 1). The mid-coastal area and the y-coordinates ( y#) show the distance from the coastline southwestern coastal area were sampled during the full (transformed into nautical miles, 0e38 miles). 9 years, whereas the northeastern coastal area was only recently sampled (2000e2003). The samples were taken with a Van Veen grab (sampling surface area: 0.1 m2) and sieved alive over 2.3.2. Diversity a 1 mm mesh-sized sieve. Water depth at each sampling The different diversity patterns within the Abra alba station was recorded in situ and standardized to the community were investigated by interpreting the mean low water spring level (MLWS) using the M2 k-dominance plots (Patil and Taillie, 1977; Lambshead reduction model (Coastal Waterways Division, Flemish et al., 1983) and species-area plots (Connor and McCoy, Community). The grain size distribution of a sub-sample 1979). was measured with a LS Coulter particle size analyzer: Univariate measures of diversity were species rich- e median grain size of the fraction 2e850 mm and mud ness (S ), the exponential form of the Shannon Wiener index (exp H#) (log base 2) and the reciprocal of Simpson’s index (1/Simpson) (Whittaker, 1972; Magur- ran, 1988). Hill (1973) labeled these diversity measures 60000 N0, N1 and N2, respectively. S is the number of all species regardless of abundance. exp H# is most affected 50000 by species in the middle of the species rank sequence, whereas 1/Simpson is primarily a measure of dominance 40000 NCZ (Whittaker, 1972). 30000

20000 2.3.3. Functional diversity MCZ Functional diversity along the distribution gradients 10000 SCZ was examined by comparing distribution patterns of feeding guilds (obligatory deposit feeders, facultative Distance along the coastline (meters) 0 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 deposit-ﬁlter feeders, obligatory ﬁlter feeders, predators Sampling years and omnivores) and mobility classes (non tube-building Fig. 1. The sampling years in function of the distance along the coast sedentary, tube-building sedentary and mobile species) (meters). of the species (Table 1). 754 G. Van Hoey et al. / Estuarine, Coastal and Shelf Science 64 (2005) 751e763

Table 1 MCZ) contained stations situated in the gully between Feeding-classes and their abbreviations (Holtmann et al., 1996; the Middelkerke bank and Kwintebank, as well as Fauchald and Jumars, 1979; Hartmann-Schro¨der, 1996) and the stations on the southwestern part of the Middelkerke mobility classes and their abbreviations (Hartmann-Schro¨der, 1996; Hayward and Ryland, 1995) bank. More to the northeast (the northeastern coastal zone; hereafter abbreviated as NCZ), the community had Feeding guilds Mobility a more offshore distribution along the gullies of the Abbreviation Description Abbreviation Description ‘Wenduine bank’ and the ‘Akkaert bank’ and at the north D Deposit feeder S Non-tube-building of the ‘Vlakte van de Raan’. The A. alba community sedentary species was not detected beyond the 14-mile zone on the BCS. DF Deposit feederC M Mobile species filter feeder The community was also found at five stations nearby the P Predator T Tube-building coastline at the northeast of Nieuwpoort (around the sedentary species Stroombank and at the border of the gully of Zeebrugge). O Omnivor On the BCS the Abra alba community was character- F Filter feeder ized by an abundance fluctuating between 129 and 26697 ind/m2 (average of 4727 ind/m2) and a species richness 2 3. Results fluctuating between 9 and 52 sp./0.1 m (average of 28 sp./0.1 m2). There were no species spanning the whole 3.1. Distribution of the Abra alba sampling area (Fig. 2b). Only eight species (Spiophanes community at the BCS bombyx, Nephtys hombergii, Phyllodoce mucosa, A. alba, Scoloplos armiger, Mysella bidentata and Fabulina fabula) The Abra alba community was found in muddy, fine were represented in more than 75% of the samples, with sandy sediments with an average median grain size of S. bombyx the most commonly found (91% of the samples). 227 mm(G47 mm (SD)). The sediment composition was Conversely, 66 species, or 54% of the total number of characterized by the dominance of the fine sand fraction species (122), were restricted to less than 10% of the (average 49%, Fig. 2a) combined with a low, though samples, with 18 species restricted to one site. These 18 significant, mud fraction (9% clay and silt) and coarse species were excluded from further analysis, as described sand fraction had much lower contributions (!5%). above. The community could be found at depths between 4 m and 29 m (average depth of 15 m). These sedimentological characteristics and the associated 3.2. Geographical patterns in community Abra alba community could be found in the sandbank structure at the BCS gullies along the whole Belgian coastal zone, with a more offshore distribution towards the northeast (Fig. 3). 3.2.1. Sedimentological characteristics Southwest of Nieuwpoort, the community was found The average median grain size was highest at the close to the coastline, especially in the Westdiep and Potje MCZ (249G38 mm (SD)) compared to the SCZ gullies as well as on two spots in the Smalbank gully (the (219G43 mm) and the NCZ (222G45 mm) (Fig. 4a). In southwestern coastal zone; hereafter abbreviated as the SCZ the median grain size range was situated SCZ). The mid-coastal zone (hereafter abbreviated as between 150 and 350 mm, in the MCZ between 200 and

100 350 median grain size 140 fine sand 300 80 medium 120

sand m)

250 µ 100

60 10% 200 80 25% 60 150 40 50% 40 75% coarse number of species very 100

sediment fraction (%) sand 20 20 silt fine median grain size ( sand 50 0 clay 18 15222936435057647178859299106113120 0 0 number of sites Fig. 2. (a) The sediment fraction (left) and the median grain size (right) of the Abra alba community. Median (symbol)Gpercentiles (25e75%) (Boxes) and non-outlier range (minemax) (Whiskers). (b) Distribution of species range size, which is the number of stations occupied by a species out of a total of 120 sites, with indication of the points representing 10, 25, 50 and 75% of the total stations. G. Van Hoey et al. / Estuarine, Coastal and Shelf Science 64 (2005) 751e763 755

38 > 20 m 36 10 - 20 m 5 - 10 m 34 2 - 5 m 32

18 16

14 MCZ NCZ Kwintebank 12 Middelkerke bank Akkaert bank 10

Distance from the coastline (nautical mile) SCZ 8 Vlakte van de Raan 6 Smalbank 4 Westdiep Wenduine bank 2 Potje

0 Nieuwpoort Zeebrugge Oostende 0 1000020000 30000 40000 50000 60000 Distance along the coastline (meters)

Fig. 3. Northeastern spatial distribution gradient of the Abra alba community on the Belgian Continental Shelf with indication of the diﬀerent zones. Black dots (stations where this community is present), open dots (absence of this community).

350 mm and in the NCZ between 150 and 300 (with one ﬁne sand fraction an opposite trend was found, with exception). a signiﬁcant decrease (Spearman rank, pZ0.000153) The highest average value in the mud content towards the northeast (Fig. 4a), with the lowest average (Fig. 4a) was found in the NCZ (14G10.8%), followed value in the NCZ (42G13.6%), 46G15.3% in the MCZ by 8G4.6% in the SCZ and 5G7% in the MCZ. For the and 54G14.7% in SCZ.

(a) (b) 400 100 30000 100

SCZ MCZ NCZ ) SCZ MCZ NCZ 2

25000 350 80 80 m) µ 20000 300 60 60 15000 250 40 40 10000 % mud and fine sand

Median grain size ( 200 20 20

5000 % Polychaetes / Mollusca Macrobenthic abundance (ind/m 150 0 0 0 0 10000 20000 30000 40000 50000 60000 0 10000 20000 30000 40000 50000 60000 Distance along the coastline (meters) Distance along the coastline (meters)

Fig. 4. (a) Median grain size (black points, black line), mud (open points; dotted trend line) and ﬁne sand (open triangles; interrupted black trend line) fraction within the Abra alba community in relation to the distance along the coastline, with indication of the three zones. (b) Macrobenthic abundance (black points, black line), percentage of Annelida (open triangles; interrupted black trend line) and percentage of Mollusca (open points; dotted trend line) in relation to the distance along the coastline, with indication of the three zones. 756 G. Van Hoey et al. / Estuarine, Coastal and Shelf Science 64 (2005) 751e763

3.2.2. Biological characteristics showed more similarity with MCZ and NCZ differs from the SCZ and MCZ. 3.2.2.1. Multivariate analysis. Multivariate analysis (de- trended correspondence analyses, DCA) clearly visual- 3.2.2.3. Diversity. The species dominance curve identi- izes the differences in community organization along the fied NCZ to be strongly different from the two other gradient, with minor overlap between the areas SCZ, zones (Fig. 6a), indicating a lower diversity and a strong MCZ and NCZ (Fig. 5). dominance of one species, in this case Spiophanes bombyx. The species dominance plots for the two other zones were 3.2.2.2. Abundance, higher taxa, species dominance. The more or less similar, with a similar ranking of species macrobenthic density across the three zones was highest contribution to the abundance. The species area plots in SCZ (average of 5181 ind/m2) and NCZ (5941 (Fig. 6b) of the NCZ and MCZ were similar, whereas ind/m2), with a drop in MCZ (average of 3010 ind/m2) the plot of the SCZ was clearly different, indicating (Fig. 4b). The variation in macrobenthic density is higher species richness for the same sampling area. higher in the SCZ and NCZ, than in the MCZ. The number of species per sample (N0) was highest at 2 In SCZ, molluscs and annelids were equally dominant SCZ (31 spp./0.1 m ), compared to the NCZ and MCZ 2 in the macrobenthos (Fig. 4b). The molluscs, mainly with respectively 24 and 25 spp./0.1 m (Fig. 7a). N1 and bivalves, strongly decline (Spearman rank, pZ0.000006) N2 both follow the same pattern, with a decline in relative abundance towards the northeast, while (Spearman rank: p!0.01 for both) towards the NCZ, annelids (mainly polychaetes) strongly increase (Spear- especially in the most northeastern part of it, caused by man rank, pZ0.01) in dominance. This was also visible strong species dominance in this area (Fig. 7b). N1 was in the list of the ten most abundant species (Table 2), highest in the SCZ (average 11.8) and lowest in the NCZ where bivalves were missing in the NCZ. (average 7.3), with an intermediate value at the MCZ When comparing the lists of the ten most common (average 9.7). N2 was also highest in the SCZ (average species (Table 2), a shift in species composition from 7.5) and lowest in the NCZ (average 4.6), with an southwest to northeast could be observed. There were intermediate value at the MCZ (average 6.3). only four species (Spiophanes bombyx, Nephtys hombergii, Scoloplos armiger and Phyllodoce mucosa) in common in 3.2.2.4. Functional biodiversity. The obligatory deposit the top ten species list of the three areas, which were feeders were the dominating feeding guild in the NCZ present in more than 80% (SCZ and MCZ) or 90% (61%), followed by predators (16%) (Fig. 8a,b). The (NCZ) of the samples within each area. Additionally, the obligatory deposit and filter feeders as well as the SCZ had another four dominant species (Abra alba, facultative deposit-filter feeders were almost equally Cirratulidae spp., Mysella bidentata and Fabulina fabula) dominating in the SCZ and MCZ, with respectively 38% in common with MCZ. These species were also present in and 37% for obligatory deposit feeders, 21% and 26% NCZ but in much lower abundances. MCZ had only one for obligatory filter feeders and 28% and 17% for other species (Actinaria spp.) in common with NCZ. The facultative deposit-filter feeders. tube building polychaete Lanice conchilega was present in In the NCZ there was a strong dominance of tube- almost all samples at SCZ (Table 2). NCZ was also building sedentary polychaetes (61%), such as Spiophanes characterized by five dominant species, which were not bombyx, Owenia fusiformis, Lanice conchilega and common in the other areas (Eteone longa, Pariambus Pectinaria koreni (Fig. 7b). This mobility class was less typicus, Eumida sanguinea, Owenia fusiformis and Pecti- represented in the MCZ (17%), where the mobile species naria koreni). In terms of species composition, SCZ were dominating (46%). In the SCZ the non tube- building sedentary polychaetes formed the dominating group (44%). 200 3.2.2.5. Habitat heterogeneity. Within the habitat of the 160 Abra alba community at the three zones on the BCS there was no correlation between community structure (mac- 120 robenthic species richness and density) and granulometry (sediment median grain size and mud content) (Spearman 80 R: pO0.1) (Fig. 9). 40

0 4. Discussion 0 40 80 120 160 200 240

Fig. 5. DCA ordination plot along the first two axes. The The Abra alba community forms a well-established discrimination of the three zones (triangle, SCZ; open points, MCZ; faunal unity in coastal areas of the North Sea black points, NCZ) is made. (Dewarumez et al., 1986), where it is mostly found in Table 2 Overview of the community parameters (abundance, diversity, species top 10), sedimentology and sampling method of different areas in the English Channel and Southern North Sea, where the Abra alba community occurs. Species in bold occur in the top 10 of the three zones on the BCS. The underlined species are present in both the SCZ and MCZ; the species in brackets are present in both the MCZ and the NCZ. French coast Belgian coast Dutch coast German coast English coast Pierre Noire Rivie` re de Baie de Seine Gravelines SCZ MCZ NCZ English channel Morlaix Sampling method ------Smith-McIntyre grab (0.1 m2)------Van Veen Grab (0.1 m2)------Rallier-du-Baty dredge No of samples 117 77 38 81 61 32 22 194 14 10 Type of area Isolated Isolated Isolated ------One continuous area------Isolated Isolated Median grain size 148e184 77e122 80e120 100e150 219 G 43 249 G 38 222 G 45 196.7 G 54.8 Muddy fine Muddy fine (mm) sand sand Mud content (%) 8 G 65G 414G 11 7.2 G 12 Depth (m) 17 10 10.5 10 11.5 17.7 10.8 12 G 4.5 13-45 !10 Density (ind/m2) 7545 G 1641 3320 G 402 5380 G 848 5080 G 1965 5181 G 4542 3010 G 3909 5941 G 5254 2556 G 3458 3828 6304 Total no of sp. 420 308 130 154 118 89 85 83 79 Diversity (No) 32 31 G 824G 725G 614G 737 Diversity (N1) 3.8 2.9 3.2 2.4 2.4 2.17 1.83 1.84 2.2 2.1 G 0.46 Species top 10 % of total % of total % of total % of total Mean Mean Mean Mean Mean % of total based on abundance abundance abundance abundance abundance abundance abundance abundance abundance abundance Species top 10 Ampelisca Chaetozone Owenia Lanice Abra alba Mysella Spiophanes Spisula Nucula nitidosa Abra alba (ind/m2) armoricana setosa fusiformis conchilega bidentata bombyx subtruncata Ampelisca Melinna Acrocnida Abra alba Spiophanes [Actiniaria sp.] Nephtys Magelona Spiophanes Nucula nitidosa sarsi palmata brachiata bombyx hombergii johnstoni bombyx Polydora Polydora Pectinaria Spiophanes Lanice Phyllodoce Phyllodoce Spiophanes Ophiura albida Melinna pulchra pulchra koreni bombyx conchilega mucosa mucosa bombyx palmata Spio decoratus Nephtys Mysella Fabulina fabula Cirratulidae sp. Nephtys Scoloplos Urothoe Mysella Mysella hombergii bidentata hombergii armiger poseidonis bidentata bidentata Paradoneis Mediomastus Aphelochaeta Eumida Mysella Abra alba Eteone longa Macoma Nephtys Notomastus armata fragilis marioni sanguinea bidentata balthica hombergii latericeus Chaetozone Tharyx Abra alba Phyllodoce Nephtys Fabulina fabula Pariambus Fabulina fabula Phoronis sp. Nephtys setosa marioni mucosa hombergii typicus hombergii Marphysa Euclymene Cultellus Nephtys Scoloplos Scoloplos Eumida Mysella Ophiura Euclymene bellii oerstedii pellucidus hombergii armiger armiger sanguinea bidentata ophiura oerstedii Urothoe Lanice Pholoe minuta Pectinaria Phyllodoce Spiophanes Owenia Scoloplos Scoloplos Magelona alleni pulchella conchilega koreni mucosa bombyx fusiformis armiger armiger Aricidea fragilis Thyasira Magelona Notomastus Fabulina fabula Capitella [Actiniaria sp.] Nepthys Abra alba flexuosa mirabilis latericeus capitata hombergii Nephtys Abra alba Nephtys Macoma Oligochaeta Cirratulidae Pectinaria Nepthys cirrosa Pectinaria hombergii hombergii balthica spp. spp. koreni koreni Literature Fromentin Fromentin Fromentin Fromentin Holtmann Salzwedel et al., Sanvicente- et al., 1997 et al., 1997 et al., 1997 et al., 1997; et al., 1996 1985 Anorve et al., Dewarumez 2002 et al., 1992 758 G. Van Hoey et al. / Estuarine, Coastal and Shelf Science 64 (2005) 751e763

(a) (b) 100

100 80 90 80 60 70 60 40 50 40 30 20 20 Cumulative Dominance % 10

0 Cumulative number of species 0 110100 021 3456 Species rank Area (m2)

Fig. 6. (a) Species dominance plot at the three zones (SCZ, black triangle; MCZ, open circles; NCZ, black points). (b) Species area plot for the three zones (similar symbols as (a)). bays, estuaries and in a narrow zone along the coastline, et al., 1997), some bays (Eagle, 1975; Rees and Walker, mostly between 0 and 10 m depth (Souplet and 1983) and coastal areas near the UK coast (St Andrews Dewarumez, 1980; Konstantinos et al., 2000) and thus and Aberdeenshire, Cumberland coast, South-West strongly influenced by terrestrial organic matter inputs England and some locations in the Irish Sea) (Rees (Sanvicente-Anorve et al., 2002). et al., 1999; Sanvicente-Anorve, 2002) and a small area The largest continuous distribution area of the Abra in the German Bight of the North Sea, seaward of the alba community is situated along the northeastern coast rivers Elbe and Weser (area of 1000 km2)(Stripp, 1969; of France (Gravelines) over Belgium north to the Dutch Kingston and Rachor, 1982; Salzwedel et al., 1985). The coast (Kingston and Rachor, 1982; Vanosmael et al., A. alba community is further present along the Atlantic 1982; Vermeulen and Govaere, 1983; Prygiel et al., 1988; coast of France, Spain and Portugal, and in the Holtmann et al., 1996; Fromentin et al., 1997; Desroy Mediterranean Sea. Yet, the community structure et al., 2002; Van Hoey et al., 2004). Next to this within these areas falls out the scope of this study. continuous distribution area, there are a lot of isolated distribution areas in the English Channel, such as the 4.1. Geographical patterns in community structure Bay of Morlaix with two small (6 and 2 km2) spots, respectively Pierre Noire and Rivie` re de Morlaix, the Although the community’s habitat is characterized Bay of the Seine (Cabioch and Glaçon, 1975; Souplet by fine, muddy sands throughout its distribution and Dewarumez, 1980; Fromentin et al., 1997; Thie´baut range (Table 2), it is clear that minor differences in

(a) (b)

60 100 SCZ MCZ NCZ 24 SCZ MCZ NCZ

50 20 80

40 16 60 30 12 % N1;N2 40 20 species richness 8

20 10 4

0 0 0 0 10000 20000 30000 40000 50000 60000 0 10000 20000 30000 40000 50000 60000 Distance along the coastline (meters) Distance along the coastline (meters)

Fig. 7. (a) The distribution of the diﬀerent diversity indices in relation to the distance along the coastline: Species richness: N0, black circles, solid trend line; exponential form of H#: N1, open circles, dotted trend line; the reciprocal of the Simpson’s index: N2, open triangles, interrupted black trend line. (b) The relative abundance of the diﬀerent mobility classes: sedentary species (S): black points, black trend line; mobile species (M): open triangles, interrupted black trend line; tube-building species (T): open circles, dotted trend line. G. Van Hoey et al. / Estuarine, Coastal and Shelf Science 64 (2005) 751e763 759

(a) (b) 100 60 SCZ MCZ NCZ SCZ MCZ NCZ

50 80

40 60 %

% 30 40 20

20 10

0 0 0 10000 20000 30000 40000 50000 60000 0 10000 20000 30000 40000 50000 60000 Distance along the coastline (meters) Distance along the coastline (meters)

Fig. 8. (a) The distribution of the relative abundance of different feeding guilds: facultative deposit-filter feeders (DF): open triangles, interrupted black trend line; obligatory filter feeders (F): black circles, solid trend line; obligatory deposit feeders (D): open circles, dotted trend line. (b) The distribution of the relative abundance of different feeding guilds: predators (P): black circles, black trend line; and omnivores (O): open circles, dotted trend line. sedimentological characteristics occur (Salzwedel et al., varying community parameter, depending on meteoro- 1985; Holtmann et al., 1995; Fromentin et al., 1997; logical conditions (wind) and currents, which can induce Sanvicente-Anorve et al., 2002). The Abra alba com- unpredictable year-to-year changes in the abundance of munity is mostly found at depths of 0e20 m; the deepest some species. Moreover, new recruits are able to form are found along the German coast (45 m) (Salzwedel patches of high abundances after a disturbance (Desroy et al., 1985), MCZ (18 m) and the Pierre Noire site et al., 2002). High variations in abundance characterize (17 m) (Fromentin et al., 1997). most areas only the Bay of the Seine shows a great temporal The highest mean abundance was found at the Pierre stability in abundances, due to the high larval retention Noire area (7545 ind/m2)(Fromentin et al., 1997) and capacity of the bay (Thie´baut et al., 1992, 1996). the lowest at the Dutch coast (2556 ind/m2)(Holtmann There is a clear pattern in the diversity between the et al., 1996)(Table 2). Abundance, however, is a strongly different sites: total number of species, species richness

40 (a) (b)

15 Mud content (%)

0 150 200 250 300 350 400 150 200 250 300 350 400 Median grain size (µm)

2 Fig. 9. The species richness (N0) and abundance (ind/m ) in relation to the sedimentological characteristics (median grain size (mm) and mud content (%)), with indication of the three zones: SCZ, black triangles; MCZ, open circles; NCZ, black circles. (a) Species richness (species/0.1 m2): 9e23; 23e29; 29e36; 36e53, (b) Abundance (ind/m2); !2000; 2000e5000; 5000e10000; 10000e27000. 760 G. Van Hoey et al. / Estuarine, Coastal and Shelf Science 64 (2005) 751e763

(N0) and Shannon index (N1) decrease towards the building sedentary species dominate the NCZ, while the northeast. The total number of species (420 sp.) and the MCZ shows intermediate values for feeding guilds and Shannon index (3.8) are highest at the Pierre Noire site a dominance of mobile species. (Fromentin et al., 1997) and decrease towards the NCZ 2 (total number of species, 85 sp.; N0, 25 spp./0.1 m ; N1, 4.2. Structuring environmental variables 2 1.8 (this study)) and Dutch coast (N0, 14 spp./0.1 m ; N1, 1.8 (Holtmann et al., 1996)), where they displayed Large-scale spatial patterns in community character- the lowest values. At isolated places along the German istics largely result from differences in hydro-sedimen- and southern English coast, the Shannon index (re- tary processes (natural or anthropogenic) (Creutzberg spectively 2.2 and 2.1) and total number of species et al, 1984; Heip et al., 1992). The Abra alba community (respectively 83 spp. and 79 spp.) are comparable with within its southern distribution areas (Bays of Morlaix those of the SCZ and MCZ. In the study of Rees et al. and Seine) is mainly influenced by flood-dominated (1999), the Abra alba community in inshore muddy fine currents from the Atlantic Ocean, while mainly ebb- sand at some places along the east and west coasts of the dominated currents influence the northern areas UK is characterized by a species richness of 25 spp./ (the continuous distribution area and German Bight) 0.1 m2. (Vlaeminck et al., 1989; Grochowski et al., 1993; The most common species in all areas were Abra alba, Lanckneus et al., 1994; Trentesaux et al., 1994). Since Nephtys hombergii and Spiophanes bombyx. Further- hydrodynamic conditions play an important role in more, the dominant species in each area belong to the exchange of planktonic larvae (Eckman, 1983; polychaetes or bivalves; this is opposite to the Pierre Dewarumez et al., 1993; Luczak et al., 1993), only little Noire area (in the Bay of Morlaix), where amphipods (larval) contact between the isolated southern and UK (Ampelisca sp.) dominate (Fromentin et al., 1997). distribution areas on the one hand and the continuous Numerous species are consistently found in the 10 most and German distribution areas on the other hand might common species of the continuous distribution area be expected. The hydrological isolation might partly from the Gravelines over Belgium north to the Dutch explain the differences in community structure observed coast. Along the southern coast of the UK (in the at a large scale. Moreover, the transition from temperate English Channel) the A. alba community was dominated to boreal conditions in the English Channel might by A. alba, Nucula nitidosa, Pectinaria koreni, Ophiura further strengthen the differences in community struc- albida and Echinocardium cordatum (Rees and Walker, ture, mainly the species composition, between the 1983; Budd, 2002; Sanvicente-Anorve et al., 2002). The southern and northern distribution areas (Sanvicente- dominant species in the A. alba community along the Anorve et al., 2002). Because of (1) the obvious strong east and west coast of the UK were Chamelea gallina, exchange between populations within the A. alba Amphiura filiformis, N. nitidosa, S. bombyx and A. alba community and (2) the similar climatological conditions (Rees et al., 1999). The species composition of the A. alba in its continuous distribution area, the differences in community along the German coast, also referred to as community structure here within cannot solely be the N. nitidosa association (Salzwedel et al., 1985), shows explained by differences in the hydrological or climato- a high similarity with the continuous distribution area of logical conditions; other factors should play a structur- the A. alba community. ing role. Although the community structure shows a high Although a relationship between small-scale habitat similarity across the full distribution range of the Abra heterogeneity and community abundance and diversity alba community, changes in community composition could be expected, no such correlation was found at the were observed: the BCS should be considered as a major BCS: habitat heterogeneitydas given by the sediment transition from the rich southern to the relatively poorer characteristics in this studydwithin each of the three northern distribution area of the A. alba community. In zones was independent from community abundance and this transition zone, the A. alba community on diversity. Thie´baut et al. (1997) also found sediment a structural level was characterized by high variation variables to be a poor predictor for the structure within in abundance, high species richness (31 sp./0.1 m2) and the Abra alba community. Another structuring variable high diversity (N1, 11.8; N2, 7.5) in the SCZ, while the might be food availability: increases in species diversity, MCZ was characterized by low variation in abundance, abundance and biomass can be correlated to an low species richness (24 sp./0.1 m2), and lower diversity increased food supply to the system (Rees et al., 1999). (N1, 9.7; N2, 6.3) and the NCZ by high abundance Being dominated by detritivores, detritus is the major variation, low species richness (25 sp./0.1 m2) and the food resource for the A. alba community. The detrital lowest diversity (N1, 7.3; N2, 4.6). On a functional level, food availability is mainly coupled to the hydrology and there was no strong feeding guild and mobility class largely depends on planktonic primary and secondary dominance in the SCZ; they were all more or less production and/or terrestrial inputs (through riverine equal represented. Obligatory deposit feeders and tube- systems). At the BCS the offshore zone mass is typically G. Van Hoey et al. / Estuarine, Coastal and Shelf Science 64 (2005) 751e763 761 characterized by low productive and more transparent 1997; Ysebaert et al., 2003). An inshoreeoffshore waters, whereas turbid, highly productive waters char- gradient of salinity can significantly affect the distribu- acterize the coastal zone (Lancelot et al., 1986). The high tion of species, which are commonly considered to be turbidity and productivity of the coastal zone mainly stenohaline (Strickle and Diehl, 1987), but the absence result from the strong terrestrial input of suspended of such species was (e.g. Echinoderms) not observed in matter and nutrients from the rivers Westerscheldt and this study. The study of Lacroix et al. (2004) confirms Yzer. The turbidity plume of the Westerscheldt can, that the impact of the Westerscheldt on the salinity in depending on the wind direction, intensity and duration, the Belgian coastal area is minimal. Although pollution reach as far as the Cap Gris Nez (northern France) is known to impact the distribution of some species in (Cabioch and Glaçon, 1975), thus influencing the whole the Westerscheldt (Ysebaert et al., 2003), such effects southern part of the continuous distribution area of the were not yet investigated further offshore. A. alba community. Smaller rivers, such as the Yzer, have lower riverine inputs in the coastal zone, but may be locally significant in structuring the A. alba commu- Acknowledgements nity: higher diversity, abundance and biomass were observed in the vicinity of river outflows (Seine, Somme, The major part of the data was obtained through Authie, Canche) (Desroy et al., 2002). The increased different research projects: (1) ‘Structural and Functional food availability in the coastal zone, due to riverine Biodiversity of North Sea ecosystems’ funded by OSTC inputs of suspended matter and nutrients might thus be (Federal Office for Scientific, Technical and Cultural responsible for the high diversity and abundance of the Affairs, Belgium; project number: MN/DD40), (2) A. alba community in the southern part of its ‘Intensive evaluation of the evolution of a protected continuous distribution area (Graveline north to SCZ) benthic habitat (HABITAT)’ funded by OSTC (project in contrast to the lower diversity and abundance in more number: MN/02/89) and AWK (Coastal Waterways offshore areas (e.g. MCZ). Division; dossier numbers: 99380 and 200.455), (3) Despite the general positive influence of river out- ‘Ecological adjustment of a coastal defense project’ flows on the Abra alba community, a clear decrease in funded by AMINAL (Flemish administration responsi- diversity was observed in the NCZ, offshore of the ble for environment, nature, land and water manage- Westerscheldt estuary. This decrease in diversity co- ment, department Nature; project number: AN/1995/ incides with a functional community shift towards nr3) and AWK (dossier number: 97190) and (4) ‘The a dominance of deposit feeders, an increase in predators spatial-temporal variability and population dynamics of e and the expense of filter feeders. It is hypothesized that the Abra alba Mysella bidentata community on the this decrease in diversity and functional community shift BCS’ funded by IWT (Institute for the Promotion of might be due to the outflow of suspended matter from Innovation by Science and Technology in Flanders, larger rivers being too high to support rich populations project number SB-011400). of filter feeding species, as already demonstrated by The authors want to thank everybody who assisted in Snelgrove and Butman (1994). The excess in suspended analyzing the macrobenthos samples (e.g., Klaas De- matter input from the Westerscheldt might also explain neudt, Mercedes Erdey, Katlijn Taveniers, Johan the (near) absence of the A. alba community in the Coenjaerts, Annick Van Kenhove) and the sedimento- Belgian inshore waters south of the river mouth logical samples (e.g., Danielle Schram, Annick Van (NieuwpoorteZeebrugge; less than four nautical miles Kenhove, Dirk Vangansbeke, Myriam Beghyn). offshore). This area is dominated by the Macoma balthica community (less diverse), where A. alba is also References present, but in much lower abundance (Van Hoey et al., 2004). More offshore the distribution of the A. alba Arntz, W.E., Rumohr, H., 1986. Fluctuations of benthic macrofauna community was limited by the occurrence of coarser during succession and in an established community. Meeresfor- sediments (due to strong offshore currents) in the gullies schungen 31, 97e114. further than ten nautical miles to the southwest and 14 Beukema, J.J., Essink, K., Michaelis, H., Zwarts, L., 1993. Year-to- nautical miles to the northeast of the coastline (Van year variability in the biomass of macrobenthic animals on tidal flats of the Wadden Sea: How predictable is this food source for Hoey et al., 2004). Since the A. alba community along birds? Netherlands Journal of Sea Research 31, 319e330. the Dutch and German coast is also confronted with Budd, G.C., 2002. Abra alba, Nucula nitida and Corbula gibba in large rivers, such as Rhine, Meuse, Elbe and Weser, it cricalittoral muddy sand or slightly mixed sediment. Marine Life might also explain the relatively low diversity and information network: Biology and Sensitivity Key Information abundance in the whole northern part of the continuous Sub-Programme (on-line). Marine Biological Association of the United Kingdom, Plymouth (cited 29/11/02). Available from: distribution area. Yet, also other factors, such as salinity http://www.marlin.ac.uk. and pollution can have an effect on the community Cabioch, L., Glaçon, R., 1975. Distribution des peuplements benthi- structure in the proximity of a river (Thie´baut et al., ques en Manche orientale de la Baie de Somme au Pas-de-Calais. 762 G. Van Hoey et al. / Estuarine, Coastal and Shelf Science 64 (2005) 751e763

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