Soft bottom macrobenthic communities of North Biscay revisited: Long-term evolution under fisheries-climate forcing

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Estuarine, Coastal and Shelf Science 78 (2008) 413e425 www.elsevier.com/locate/ecss

Soft bottom macrobenthic communities of North Biscay revisited: Long-term evolution under fisheries-climate forcing C. Hily a,*, F. Le Loc’h a,b, J. Grall a, M. Gle´marec a a

LEMAR UMR 6539 CNRS, Institut Universitaire Europe´en de la mer, Universite´ de Bretagne Occidentale, Place Copernic, 29 280 Plouzane´, France b UR 070 RAP, IRD, Centre de Recherche Halieutique Me´diterrane´enne et Tropicale, Avenue Jean Monnet, B.P. 171, 34203 Se`te Cedex, France Received 10 July 2007; accepted 7 January 2008 Available online 17 January 2008

Abstract Thirty-five years after the first description of the benthic community and sediments of the North Bay of Biscay continental shelf (80e200 m depth in the ‘‘Grande Vasie`re’’ region) by Gle´marec (personal communication), the sampling stations were revisited to provide a new reference on the status of the macrozoobenthic communities to help our understanding and management of fisheries that are highly developed in this area. Results showed that large modifications occurred in the communities and sediments of the central part of the ‘‘Grande Vasie`re’’, while these modifications remained moderate in the surroundings on the outer continental shelf. Revisited, macrobenthic communities differed greatly from those recorded in the 1960s, and were less numerous and more homogeneous. The dominant species which characterized the communities and sub-communities had also changed. The main factor that can explain these differences is the granulometry of the sediments which has shown large changes: a strong decrease in the mud fraction and increase in the fine sand fraction. These sedimentary changes should be linked with human activities: increase in bottom trawling effort that induces the resuspension of fine mud particles and the homogenization of sediments over large areas, and decrease in terrigenous particulate fluxes due to anthropic activities on the shoreline and in coastal waters. Effects of global climatic change on the observed evolution remain low, even if some species common in the south of the Bay of Biscay in the 1960s but rare or absent in the north, had increased in density and spread to the north. Trawling activities are probably the main force driving benthic community evolution in the North Bay of Biscay both through direct action on the fauna (inhibition and facilitation processes) and indirect action by modifying sediment characteristics. Ó 2008 Elsevier Ltd. All rights reserved. Keywords: habitat; biodiversity; climate; marine sediments; community structure; bottom trawling; long term

1. Introduction Increasing anthropic pressure on natural ecosystems and particularly on benthic communities has incited many studies on the changes brought about by the human activities. To understand the processes involved and to identify the relative role of the natural and anthropic factors, two types of approach have been developed. Firstly the initiation of long-term surveys with the acquisition of high and medium frequency data series (Buchanan and Moore, 1986; Pearson et al., 1986; Frid et al., 1996). This type of monitoring focuses on few stations because of the high sampling effort required. The advantage is to give * Corresponding author. E-mail address: [email protected] (C. Hily). 0272-7714/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2008.01.004

an accurate description of dynamics over time, that facilitates understanding of the processes, but the disadvantage is that this limits the extrapolation of results spatially. The second approach compares the situation at a few (often two) points in time, but on a large spatial scale (many stations), separated by long periods (Pearson et al., 1985; Reise and Schubert, 1987). In this case the comparison of two situations (t0, tx) gives a good spatial description over large areas, but the community dynamics that led to the final (tx) situation remain unexplored. In such a situation, though the main objective is to obtain a clear view of overall change at a large spatial scale, it is often difficult to explain the causes of this change. The descriptor used must be robust, stable and also shows clear responses to the abiotic and biotic pressure factors. In marine environments, macrozoobenthic invertebrate populations have such characteristics

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and the evolution of their community structures is a pertinent indicator of overall ecosystem evolution. Mean individual lifespan varies from 1 to 10 years making the macrofauna useful for long-term monitoring and also for comparing spatial situations separated by a long time period. These two approaches were used experimentally for some years and are complementary (Reise, 1982). However, the second approach can only be realized when the original data of the first point in time are available and can be totally reanalysed using up-to-date mathematical methods. Moreover, the sampling protocols need to be similar despite the technical changes that could have taken place. These constraints have limited the number of long-term comparative marine studies but those made have shown very interesting results because of their large spatial scale, e.g. in the North Sea (Kro¨ncke, 1992; Kro¨ncke et al., 1998). The present work takes this type of approach for the study of the northern area of the Bay of Biscay continental shelf. The invertebrate benthic fauna of the Bay of Biscay was firstly sampled with a beam trawl (Le Danois, 1948), consequently the species described were mostly the epibenthic and few infauna. In the early 1960s, Gle´marec studied the entire macrofauna using a dredge (Rallier du Bathy dredge) (Gle´marec, personal communication). Gle´marec’s original data, collected in the field in autumn 1966 (Gle´marec, PhD thesis, unpublished data) described the communities and assemblages of macrobenthic fauna and the associated sediments. After this study, no macrobenthic study was done in this large area until our study in 2001. The objectives of this paper were to compare the spatial patterns of benthic communities 40 years after, to know if their biodiversity and structure had changed. We reanalyzed data set from autumn 1966 sampling using recent multifactorial methods and in 2001e2002 we collected new samples at the same localization that in 1966, using the original protocol. To explain the results, the changes of sediment characteristics were analyzed because the nature of sediments is largely recognized as the main factor structuring soft bottom macrobenthic communities (Gray, 1981). Other factors also considered included both natural (hydroclimatic) and anthropogenic factors, particularly trawling activities. 2. Material and methods

The whole study area, including the Grande Vasie`re area and the external zone (80e200 m depth) lies from Penmarc’h point (47 48 N) to the north and the Rochebonne rocky plateau to the south (46 10 N). 2.2. Sampling Fifty-four stations of the Gle´marec 1960s data set were resampled in 2001e2002 using a protocol as similar as possible to the original. The sampling was performed during the same season as Gle´marec’s (early autumn), one dredge per station. The same type of dredge was used (i.e. a Rallier du Baty dredge), equipped with a 30e40 l bag which retains the sediment without washing. Sediment samples for granulometric analysis (100e200 g wet weight sediment) were collected from the center of the dredged bag to insure that the finest muddy part of the sediment was preserved. The samples were then sieved on board on 1.5 mm mesh and formalin fixed. At the laboratory, fauna were sorted from the mineral fraction. After identification of all individuals to the species level (except sipunculids and hydrozoa), the taxonomic groups which had not been considered by Gle´marec, personal communication (shrimps, mysids and fishes) were removed from the species list (consisting of endo- and epi-invertebrates) to avoid a methodological error. The Gle´marec study produced a map of the different communities (i.e. biosedimentary units) of this area. To avoid any problem arising from the relative imprecision of geographical localizations of the original sampling stations due to the technical limits of the positioning system used at that time (DECCA system) only the stations positioned far from borders between two different communities were considered. To minimize the spatial variability within each faunal assemblage and/or community, several stations were selected from each biosedimentary unit on the 1969 map. Finally, the stations sampled were as distant as possible from each other (a few nautical miles). The result of this selection was a data set of 54 stations (Fig. 1) for which the entire original faunal list was available. Using this strategy and because of the low small scale heterogeneity of bottom features shown in the 1966 community analysis, any bias in the comparison of the 1966 and 2001 data sets due to imprecision of localization in the 1960s’ cruises can be considered negligible and was not considered to contribute to changes observed in the communities.

2.1. Study area 2.3. Data analysis The North Bay of Biscay continental shelf is structured into three zones lying parallel to the shoreline: (1) close to the coastal area, the internal zone, 0e80 m depth is named the ‘‘pre-littoral zone’’ its bottom is composed of pre-littoral troughs more or less filled with soft sediments, and rocky outcrops which are the basis of the Armorican islands; (2) the median zone, offshore, is a large uniform plain of muddy sediments known as the ‘‘Grande Vasie`re’’ (i.e. ‘‘great mud bank’’); (3) the external zone 120e200 m depth extends to the end of the outer shelf. Here, the bottom is made up of an alternation of sandy sediments and rocky smooth plateaus with few paleo-channels (Lesueur and Klingebiel, 1976).

2.3.1. Fauna Species lists of the two data sets were harmonized according to the taxonomical reference ‘‘Species Directory of the Marine Fauna and Fauna of the British Isles and the Surrounding Seas’’ (Howson and Picton, 1997). Because the Rallier du Baty dredge is a qualitative sampler, the abundances of species in a sample cannot be related to a surface area. However, after a data transformation, semi-quantitative methods can be used for statistical analyses. Data transformation was achieved by calculating the Dominance  Presence coefficient. This coefficient had been previously used for this type of data analysis

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415

Fig. 1. Map showing the locations of common sampling stations in 1966 and 2001.

(Gle´marec, personal communication). It is a valuable coefficient for identifying species assemblages and species which are frequently present together and abundant in a group of samples.
Pij ¼ 100  fij = fi1 þ / þ fij þ / þ fik ð1Þ with fij ¼ 100  nsij =Nsj

ð2Þ

where f is the frequency of a species i in an assemblage j, nsj is the number of samples in which the species i is present and Nsj is the total number of samples in the assemblage j. An assemblage j is the group of samples identified by statistical analysis (here the hierarchical ascendant classification method, Lebart et al., 1982). This P coefficient minimizes the component of heterogeneity due to differences in the number of samples between different assemblages. The Dominance Dij ¼ 100  neij =Neij

ð3Þ

where ne is the total abundance of the species i, and Ne is the total abundance of all the species in the assemblage j. Hierarchical ascendant classification (HAC) (Lebart et al., 1982) was used with euclidian distance as the dissimilarity index and Ward’s inertia increase as aggregation criterion (Legendre and Legendre, 1984). The results of this analysis were represented graphically as dendrograms on which stations were grouped (i.e. clustered) according to their similarity/dissimilarity values. The clusters were hierarchically

structured into sub-clusters at lower dissimilarity values. As the clusters grouped different stations with close species composition, they are considered to group together stations with the same assemblage/community of species. In the same manner, a sub-cluster can be identified as a sub-community: a group of stations in which the structure of the species assemblage showed differences from the other stations of the community (frequently one or more species are dominant that are different from the leader species of the community). 2.3.2. Sediment analysis Sediment granulometry was characterized using a series of 14 AFNOR sieves from 63 mm to 10 000 mm. The respective amounts of sediment in each sieve were grouped into four types for further analysis: pelitic fraction (<63 mm), fine sands (63e 250 mm), coarse sands (250e500 mm) and gravels (>500 mm). Classification into these types was previously used by Chasse´ and Gle´marec (1976) for mapping the sedimentary units of the Bay of Biscay which defined various types: MFS: muddy fine sands; MMS: muddy medium sands, SM: sandy muds; HMS: heterogeneous muddy sands; MG: muddy gravels; G: gravels, SMS: slightly muddy medium sands; SM: medium sands. 3. Results 3.1. Taxonomical analysis at the scale of the whole area The total cumulated number of species over the two sampling periods was 223. Only 82 species occurred in both

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Table 1 Species richness (S ¼ number of species) and abundances (A) in the two data sets (1966 and 2001) 1966

2001

ST (total no. sp.) s (mean no. sp./sample)

146 11.1

163 19.8

S S S S

33; 65; 18; 18;

29; 76; 37; 14;

Mollusks (no.; %) Polychaetes Crustaceans Echinodermata

A (mean abundance/sample)

23 45 12 12

35.4

Total no. of species found in the two series Number of species occurring in the two series Number of species occurring only in 1966 Number of species occurring only in 2001 Main species missing in 2001 Main species new in 2001

18 47 23 9

48.8 223 82 64 77 Chaetopterus sarsi Nephthys caeca

sampling periods representing 38% of the cumulated number of species. Out of the species found in 1966, 64 were missing in 2001e2002, 17% of these species were abundant (i.e. >5 ind. among all the stations.), 34% were at low densities (i.e. 2e4 ind.) and 49% were rare (i.e. 1 individual identified). Conversely, 77 species found in 2001 were not present in the 1966 collections (18% abundant, 35% low density, 47% rare). The epibenthic tubicolous polychaete Chaetopterus sarsi, that had high abundances and high occurrence in 1966, was totally absent in 2001. The carnivorous mobile polychaete Nephthys caeca, however, missing in 1966, was present and often abundant at 25 sampling stations in 2001. The total number of species sampled and the mean number of species per sample increased between 1966 and 2001 (Table 1). The highest variations were due to crustaceans where the number of species doubled (18 in 1966 vs 37 in 2001), while the dominance of echinodermata decreased about 50% (18% in 1966 and 9% in 2001).

3.1.1. Changes in occurrence All species were ranked according to the number of samples in which they occurred in the two data sets (Fig. 2). Rare species represented about 40% of the total number of species for both periods. In 2001 the number of species with a high occurrence was greater. In 1966 no species occurred in more than 50% of the sampling stations, while in 2001 four species did: Glycera rouxi, Terebellides stroemi, Lumbrineris impatiens and Nothria britannica. Fig. 3 presents a comparison of occurrence patterns of the most abundant species (decrease, stability or increase in occurrence). Nephthys caeca, not observed at all in 1966, occurred in 50% of the samples in 2001. Lumbrineris impatiens, present at low density in five samples in 1966 (5 ind. sample1), occurs in 2001 in 29 samples. 3.1.2. Changes in abundances In this study, the total abundance per sample remained very low (<200 ind. sample1). The list ranking the species in order of decreasing abundance (Table 2) shows that large shifts occurred between 1966 and 2001. Ditrupa arietina left this list, while three mobile carnivorous polychaetes e Glycera rouxi, Nephthys caeca and Lumbrineris impatiens e attained third, fourth and fifth position, respectively. 3.2. Identification of communities and sub-communities A hierarchical cluster analysis was performed on each standardized data set separately using Ward’s minimum-variance method. For 1966, clusters of stations are organized according their species composition at two levels of dissimilarities (Fig. 4A): firstly one cluster group stations situated in the Grande Vasie`re and is broken down at a second level into six sub-clusters (numbered 6e11); and a second cluster group stations (1) in the coastal zone (sub-clusters 2, 4, 5), (2) on the margin of the continental shelf (sub-cluster 3) and (3) in a

Fig. 2. Distribution of the species occurrence (number of stations where a species is present) in the two periods (white: 1966, black: 2001). For example, in 1966, only one species (Glycera rouxi) was present in 41 stations (occurrence ¼ 41) while 68 species were present in only one station (occurrence ¼ 1, i.e. rare species). Leader species are named.

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Fig. 3. Occurrence of the most abundant species between the two periods.

transitional zone between the Grande Vasie`re and the outer margin (sub-cluster 1). The same type of analysis was applied to the 2001 data set (Fig. 4B). Apart from a few stations, the two main clusters identified in 1966 are also found in 2001. However, the pattern of differences in species composition has changed and causes a different clustering (eight sub-clusters) at the second level of similarity: two grouping the coastal stations and external margin stations (sub-clusters 7 and 8) and five in the Grande Vasie`re cluster (sub-clusters 1 and 3e6). One station from the shelf margin is isolated from these clusters (station 919, sub-cluster 2). It should be noted that the station 918 situated in the vicinity of the station 919, had not been included in the 2001 analysis because it did not satisfy

cluster analysis requirements (i.e. more than five taxa, according to Lebart et al., 1982; Legendre and Legendre, 1984). By comparing the localization of each station in the clusters of the two periods, the evolution of the assemblages can be described. The stations represented in six communities on a coastal-offshore gradient. (1) A Chamelea striatulaeLumbrineris gracilis assemblage was localized on the external margin of the continental shelf (group 2, 1966). In 2001, it became either an Aponuphis bilineataeArcopella balaustina assemblage or a Astropecten irregulariseMolgula sp. assemblage (groups 7 and

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Table 2 Prominent species and feeding behavior ranked by decreasing abundance in 1966 and 2001

1 2 3 4 5 6

1966

2001

Chaetopterus sarsi e tubicolous suspensit feeding polychaete Nothria britannica e tubicolous surface deposit feeding polychaete Ditrupa arietina e tubicolous suspensit feeding polychaete Terebellides stroemi e tubicolous surface deposit feeding polychaete Aponuphis bilineata e tubicolous surface deposit feeding polychaete Dasybranchus gajolae e subsurface deposit feeding polychaete

Aponuphis bilineata e tubicolous surface deposit feeding polychaete Glycera rouxi e mobile subsurface carnivorous polychaete Nephthys caeca e mobile subsurface carnivorous polychaete Lumbrineris impatiens e mobile carnivorous surface polychaete Terebellides stroemi e tubicolous surface deposit feeding polychaete Nothria britannica e tubicolous surface deposit feeding polychaete

(2)

(3)

(4)

(5)

4) (C. striatula had become a rare species by 2001). Drastic changes had taken place in the whole species composition. The assemblage Ditrupa arietinaeNothria britannica (i.e. group 9 of the 1966 data set), which defines a transitional zone between the coastal margin and the Grande Vasie`re, was greatly modified: the original leader species D. arietina was missing in 2001 and the population of the second species N. britannica had decreased drastically. In 2001 the fauna of these stations belonged to three assemblages Astropecten irregulariseMolgula sp. (group 4), Terebellides stroemieNephthys caeca (group 6) and Ampelisca spinipeseMelinna palmata (group 5). The Nothria britannicaeTerebellides stroemi community of Grande Vasie`re (sub-cluster 11, 1966), characterized 11 stations in 1966, that by 2001 contained four different assemblages: Aponuphis bilineata and Antalis entalis (sub-cluster 8) of the coastal margin, or one of the three assemblages in which T. stroemi has high densities and high occurrence (Aponuphis fauvelieT. stroemi (sub-cluster 1), T. stroemieNephthys caeca (sub-cluster 6), Ampelisca spinipeseMelinna palmata (sub-cluster 5). In a differing manner, the 1966 mud assemblages (Ninoe armoricanaeTerebellides stroemi assemblage and Dasybranchus gajolaeeT. stroemi assemblage (sub-clusters 6 and 7)) were missing in 2001 and had been replaced by the T. stroemieNephthys caeca (sub-cluster 6) and Aponuphis fauvelieT. stroemi (sub-cluster 1) assemblages. Likewise, the Turritella communiseAmphicteis gunneri assemblage (sub-cluster 10, 1966) was missing in 2001 and the corresponding stations aggregated into the T. stroemi community (sub-clusters 1 and 5). Finally the stations which had formed the D. gajolaeeUpogebia deltaura assemblage (sub-cluster 8, 1966) were found in the Astropecten irregulariseMolgula sp. (sub-cluster 4), or in the T. stroemi community (sub-clusters 1, 5 and 6). The tubicolous crustacea U. deltaura had been replaced by its sister species Callianassa subterranea. The Chaetopterus sarsi assemblage (group 1, 1966) situated in the transition zone between the Grande Vasie`re communities and the external continental shelf margin had totally disappeared in 2001 and was replaced by the

Aponuphis fauvelieTerebellides stroemi assemblage (subcluster 1, 2001). (6) The benthic communities of the external margin (groups 5 and 4) remained more stable than the others between 1966 and 2001. The main changes which occurred in the Ditrupa arietinaeAponuphis bilineata assemblage resulted from the severe density decrease of D. arietina and the increase of Antalis entale (sub-clusters 7 and 8). (7) Finally the Grypheus vitreusePhaxas pellucidus (group 3) localized in the outermost area of the continental shelf was replaced by the Astarte sulcataeSthenelais minor assemblage (group 2). However, the number of stations studied is too small (n ¼ 2) to draw a firm conclusion. In the second stage of analysis, for 1966 and 2001, data of the stations grouped in each of the sub-clusters were considered together (i.e. as replicates of one set) allowing richness parameters (mean number of species, diversity, etc.) of the faunal assemblages of each sub-community to be calculated (Tables 3 and 4 for 1966 and 2001, respectively). D  P coefficient also was calculated for each species of each sub-cluster (i.e. for each species of each cluster, we calculated the mean of the D  P values of this species in this cluster). These data were put in a matrix and a hierarchical cluster analysis realized (Fig. 5). Three main groups of clusters were identified: (1) the communities of the northern area in 2001, (2) the Aponuphis bilineata community in 2001 and in 1966, (3) a large group with (a) the communities of the Grande Vasie`re in 1966 associated with the 2001 Aponuphis fauveli community (Southern Grande Vasie`re) (sub-cluster 1), and (b) the 1966 coastal sands community. These results confirm that the external margins (A. bilineata community) were little modified between 1966 and 2001 while the communities of the Grande Vasie`re changed greatly, mostly in the northern area. In terms of community structure, the 2001 A. fauveli community (grouping the southern stations of the Grande Vasie`re) remained close to the 1966 A. bilineata community.

3.3. Synthesis of the community changes Multifactorial analysis of Gle´marec’s 1966 data confirmed the community description given by this author. By comparing the localization of the corresponding sampling stations, the changes occurred in these communities can be summarized: e The ‘‘Ninoe/Sternaspis, Scalibregma, Nephrops, Goneplax, Terebellides muds’’ described by Gle´marec had become Ampelisca spinipes and Aponuphis fauveli muddy sands in 2001. e The stations grouped in 1966 as ‘‘Nucula sulcata, Brissopsis lyrifera sandy muds’’ were redistributed in 2001 between Nephthys caecaeTerebellides stroemi, Ampelisca spinipese Melinna palmata muddy sands, Callianassa subterranea muds, or a CallianassaeBrissopsis sub-community. e The 1966 ‘‘Terebellides stroemi and A. crinata muds’’ were distributed between the three sub-communities of

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Fig. 4. Dendrogram resulting from ascendant classification analysis of the matrix species dominance/site for (A) 1966 and (B) 2001.

the T. stroemi, Aponuphis fauveli, Ampelisca spinipes community in 2001. e The 1966 ‘‘Astarte and Arcopella balaustina coarse muddy sands’’ were not found in 2001. There were no sediments at the locations of the corresponding stations but hard substrata. High sediment displacement can therefore be presumed to have occurred at the western border of the Grande Vasie`re between the two dates studied. e The ‘‘Astropecten fine sands’’ of 1966 remained in 2001, although some stations showed an assemblage of species dominated by Aponuphis bilineata and Arcopella balaustina. e The polychaete Chaetopterus sarsi dominated the transition areas between the Grande Vasie`re and the external continental platform in 1966 (areas named by Gle´marec as ‘‘the Chaetopterus pass’’). In 2001 no individuals of this species were found by any of the sampling cruises,

and the corresponding stations there had Terebellides stroemi or Astropecten muddy sand communities. e Finally, when the ‘‘Ditrupa arietina sands’’ of 1966 were revisited in 2001, the abundances of D. arietina had drastically decreased and this species had lost the leader position in the communities leading the corresponding stations to be distributed either in the AstropecteneMolgula sp. assemblages, or in the Ampelisca spinipeseTerebellides stroemi muddy sands.

3.4. Sedimentary change The granulometry data from 40 stations were available for both periods, while for 13 stations the sedimentary unit (i.e. sandy mud, coarse sand.) was only available for the first period. Comparison of these data revealed large changes

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Table 3 Overall characteristics of species assemblages defined by the clusters in Fig. 4B (1966 data): no. of the clusters in Fig. 4B, dominating and associated species, sediment type, number of stations in the cluster, total and mean species richness, mean abundance by sample, ShannoneWeaver index and equitability. Standard deviations are given in brackets. MFS: muddy fine sands; MMS: muddy medium sands, SM: sandy muds; HMS: heterogeneous muddy sands; MG: muddy gravels; G: gravels, SMS: slightly muddy medium sands; SM: medium sands; nb: number of individuals Total species richness

Mean species richness

Mean abundance (nb ind. dredge1)

Shannon diversity index

Equitability

2

36

22.5

241.0

e

e

MFS

3

32

14.3 (4.2)

20.0 (4.6)

3.52 (0.61)

0.92 (0.09)

SM

2

7

4.0

5.5

e

e

SMS G

3 7

24 50

10.0 (1.7) 11.4 (6.6)

54.0 (41.5) 26.4 (27.5)

1.94 (0.54) 2.78 (0.74)

0.59 (0.15) 0.84 (0.14)

SM

3

14

7.0 (1.7)

28.0 (9.5)

1.98 (0.29)

0.71 (0.02)

MG

4

22

8.8 (3.0)

22.8 (10.2)

2.89 (0.42)

0.89 (0.04)

HMS

7

30

6.7 (1.9)

14.4 (5.8)

2.25 (0.44)

0.83 (0.11)

MMS

4

51

19.8 (6.8)

65.2 (39.0)

3.53 (0.43)

0.84 (0.08)

MFS

2

12

8.5

17.0

e

e

MFS

11

71

15.5 (6.2)

37.6 (18.7)

3.18 (0.67)

0.82 (0.07)

Cluster

Dominating species

Associated species

Sediment type

1

Chaetopterus sarsi

SMV

2

Chamelea striatula Lumbrineris gracilis Apporhais pespelicani Amphictene auricoma

3

Grypheus vitreus Phaxas pellucidus

4 5

Ditrupa arietina Aponuphis bilineata

6 7

Ninoe armoricana Terebellides stroemi Dasybranchus gajolae

8

Dasybranchus gajolae

9

Ditrupa arietina

10

Turritella communis

11

Terebellides stroemi Nothria britannica

Hydroides norvegica Scalpellum scalpellum Ditrupa arietina Sthenelais limicola Dosinia lupinus Acteon tornatilis Anapagurus laevis Aonides oxycephala Aphrodita aculeata Circomphalus casina Aglaophamus rubella Echinocyamus pusillus Nephthys bilobata Ditrupa arietina Aponuphis bilineata Notomastus latericeus Marphysa belli Lumbrineris impatiens Dasybranchus gajolae Terebellides stroemi Glycera rouxi Upogebia deltaura Goniada norvegica Tellina donacina Terebellides stroemi Nothria britannica Glycera rouxi Nothria britannica Phoronis sp. Corbula gibba Nephthys hystricis Phoronis sp. Auchenoplax crinita

Number of station

between the two samplings: more than half of the stations showed a decrease in the pelitic fraction, while only two had an increased pelitic fraction. The mean pelitic fraction (n ¼ 40) decreased from 19.8% to 9.1%. The sand fraction increased greatly at 27 stations, was stable in eight stations and decreased in five stations; the mean increased from 50.5% to 68.3%. Mean coarse sand and gravels fractions decreased from 34.9% to 24.8%. When 1966 stations in one hand, and 2002 station in an other hand, were grouped according to the faunal analyses (Table 5), the mean pelitic fractions decreased in all groups, varying from 2.1% to 17.3%. Some groups (6, 7, 10, 11) showed a decrease >50% with mean pelitic fraction around 11e12%. 4. Discussion Comparison of macrofauna in the North Bay of Biscay between 1966 and 2001 showed that deep modifications had taken place. These changes occurred at all levels of the community structure, in terms of species and abundances. Only

38% of the species occurred in both periods, between which their relative dominance changed. This revealed profound restructuration of the communities, with new leader and dominant species. However, it should be underlined that almost 50% of species in the two data sets are rare, meaning that a stronger sampling effort should lead to the inclusion of the missing species. Taking this consideration in account though, there remains 17% of the species missing in 2001 that were abundant in 1966. 4.1. Role of sedimentary changes in the modifications observed in community structures Sediment characteristics have long been recognized as a determining factor directly controlling the presence and abundances of the soft bottom fauna (Gray, 1981). Each species tolerates a specific sediment particle size range. The central part of this gradient corresponds to the optimal conditions for the species in terms of abundances, individual mean weight and biomass (Hily, 1987). The amplitude of the

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421

Table 4 Overall characteristics of species assemblages defined by the clusters in Fig. 4B (2001 data): no. of the clusters in Fig. 4B, dominating and associated species, sediment type, number of stations in the cluster, total and mean species richness, mean abundance by sample, ShannoneWeaver index, equitability. Standard deviations are given in brackets. MFS: muddy fine sands; MMS: muddy medium sands, SM: sandy muds; HMS: heterogeneous muddy sands; MG: muddy gravels; G: gravels, SMS: slightly muddy medium sands; SM: medium sands; nb: number of individuals Cluster

Dominating species

Associated species

Sediment type

Number of station

Total species richness

Mean species richness

Mean abundance (nb ind. dredge1)

Shannon diversity index

Equitability

1

Aponuphis fauveli

SFBeFV

11

30

10.9 (2.2)

40.6 (36.3)

3.06 (0.34)

0.89 (0.05)

2

Astarte sulcata

SFB

1

17

17.0

29

e

e

3

Callianassa subterranea

VS

4

36

12.5 (4.5)

22 (9.5)

3.22 (0.63)

0.91 (0.05)

4

Astropecten sp.

SFS

4

63

25.0 (11.7)

98.5 (69.3)

3.93 (0.44)

0.88 (0.05)

5

Ampelisca spinipes

FV

6

54

20.8 (4.6)

58.8 (22.3)

3.87 (0.38)

0.89 (0.05)

6

FV

8

59

18.0 (5.3)

39.6 (15.7)

3.66 (0.40)

0.90 (0.05)

7

Nephthys caeca Terebellides stroemi Aponuphis bilineata

SHVeSG

6

65

16.3 (6.1)

51.0 (28.1)

3.29 (0.72)

0.83 (0.11)

8

Aponuphis bilineata

Terebellides stroemi Nothria britannica Glycera rouxi Lumbrineris impatiens Sthenelais minor Scololepis cantabra Hinia reticulata Similipecten similis Striarca lactea lactea Syllis cornuta Brissopsis lyrifera Nucula sulcata Dasybranchus gajolae Alpheus glaber Ascidiacea Lumbrineris impatiens Nephthys caeca Urothoe marina Iphinoe serrata Glycera rouxi Ditrupa arietina Melinna palmata Terebellides stroemi Nephthys caeca Amphicteis gunneri Glycera rouxi Dasybranchus gajolae Arcopella balaustina Nephthys caeca Caryophyllum smithi Lumbrineris impatiens Leptometra celtica Antalis entalis

SFBeSG

9

69

14.9 (4.9)

78.9 (67.5)

2.71 (1.00)

0.70 (0.23)

gradient tolerated varies considerably from one species to another. Consequently each modification of sediment characteristics is followed by a modification of the species composition by complex inhibition/facilitation processes. The composition of sites after a long time interval reveals major changes in the structure of benthic communities (Reise and Schubert, 1987; Rosenberg et al., 1987; Gre´mare et al., 1998) but the dynamics of these communities remain unknown and explanations of these changes remain often as hypotheses because of the lack of environmental parameters. Among the causes invoked to interpret the faunal changes the impact of sediment characteristics is of main importance. Pe´re`s and Picard (1957) already invoked the shift of sediment characteristics to explain the Ditrupa arietina populations variability and more recently Gre´mare et al. (1998) explained the large extension of this suspension feeder polychaete by a decrease of the fine particles at the soft bottom interface possibly due to changes in the terrigenous particle inputs and resuspension process linked with modification of wind conditions. In this study, the comparison of the sediments between the two periods revealed that at most

of the sampling stations very large changes occurred in the relative levels of the main grain size fractions. At the scale of the whole area, these modifications show a coherent pattern: (1) an overall decrease in the mud and coarse fractions and an increase in the fine sands in the sediments; (2) variation is higher in the shallower stations close to the coast. In many stations the comparison of 1966 and 2001 granulometric curves frequently showed a homogenization of the sediment (greater uniformity of particle size, less complexity). At a large spatial scale this resulted in a decrease in the number of stations with heterogeneous sediments (i.e. less sandy gravels, sandy muds and muddy coarse sands), while the number of stations with fine muddy sands increased. The homogenization of the sediment on a large scale induced a homogenization of species composition, i.e. a decrease in the b biodiversity. This was observed in the results as a decrease in the number of assemblages between the two periods at an equivalent level of discrimination in dendrograms, and an expansion of the Terebellides stroemi community to a large part of the studied area. Furthermore, the increasing dominance of a ‘‘median’’

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422

Fig. 5. Dendrogram resulting from ascendant classification analysis of the matrix species dominance/assemblage for 1966 and 2001.

type of sediment (the muddy sands: not too coarse, not too muddy) is a facilitation process for species which are not greatly specialized in terms of sediment, i.e. those species which have a large amplitude of granulometric gradient. It can be concluded that the modifications observed in the fauna are consistent with those observed in the sediments’ characteristics, and that these changes in sediment explain most of the changes in communities. In the context of new type designation for benthic communities in Europe (EUNIS classification) these changes can be considered as a shift from the Circalittoral fine muds (4-A5.35) and Circalittoral sandy muds (45.36) to the Circalittoral muddy sands (4-A5.26) and Deep Circalittoral sands (4-A5.27). Table 5 Mean variation of the mud fraction in percentage (<63 mm) of the sediments in groups of stations identified by faunal data clustering (Fig. 4). Mean mud fraction in 1966: 19.8% (n ¼ 40); mean mud fraction in 2001: 9.08 (n ¼ 40) Group no.

% Mud 1966

% Mud 2001

Diff. 1966e2001

1 2 3 4 5 6 7 8 9 10 11

10.00 14.33 6.5 8.5 5.8 25.00 22.00 15.4 12.33 27.00 14.71

3.20 4.86 1.95 6.35 6.00 11.09 13.36 8.48 8.45 9.6 11.81

()6.8 ()9.47 ()4.55 ()2.14 ()0.2 ()13.91 ()8.64 ()6.92 ()3.88 ()17.4 ()2.90

4.2. The role of hydroclimatic factors (temperature and hydrodynamism) on the community changes This question implies that one or several factors concerning the water mass, changed between the two periods. Available data are not localized to the scale of the sampling stations. As for temperature and hydrodynamism, the North Atlantic Oscillation (NAO) index was in a negative phase in the 1960s (i.e. weak west winds and cold winters) but has been positive since the early 1990s (strong west winds and mild winters) (Hurrell, 1995). This index supports the hypothesis of a stronger effect of spring floods on deeper sediments, with an increased resuspension of the fine fraction. This suspended mud fraction can be carried out to the bathyal zone by bottom currents and leads to a decrease of the pelitic fraction of the sediment. Another factor to consider was if a temperature change of the water mass could explain the macrofauna changes. An increase of 0.8  C in mean surface water temperature has been recorded in the Bay of Biscay since the 1950s (Koutsikopoulos et al., 1998; Planque et al., 2003), but because the depth is superior to 100 m, the bottom water mass did not change to this extent. The Grande Vasie`re is characterized by permanent stratification and the existence of a bottom water layer with a stable temperature of 11  C (Vincent and Kurc, 1969). There are no direct temperature measurements available to support the hypothesis that the 0.8  C increase of the surface layer induced a temperature increase in the bottom layer. However, some elements can be used as indirect indices of a temperature increase on the bottom layer. Poulard and Blanchard

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(2005) described an evolution in the demersal fish communities compatible with the effect of warming. About invertebrates, temperature increase could have affected the distribution of a few species such as the polychaete Aponuphis fauveli that spread northwards in the Bay of Biscay, a pattern compatible with water mass warming. Aponuphis fauveli was not sampled by Gle´marec in 1966 in North Biscay, but was abundant in South Biscay during the same period (Monbet, personal communication, 1972; Cornet et al., 1983). By 2001, this species had become a leader species of one assemblage and was present in samples from 11 stations. It can therefore be supposed that temperature as well as sediment evolution participated in the northward spreading of its distribution. However, on these bottoms, even if accurate data are lacking, most of the benthic macro-invertebrate species have a much larger latitudinal distribution than the area studied and are not a priori highly sensitive to slight temperature increases. It can be concluded that temperature cannot explain the large changes shown in the benthic macrofauna in this study. 4.3. Role of anthropic factors in community changes 4.3.1. Eutrophication The widespread raise in nutrients, measured in most coastal waters of the world as a consequence of human activities favors the increase of primary production and eutrophication (Grall and Chauvaud, 2002). An increase in growth in phytoplankton biomass and production has been observed in many coastal areas of European waters, as described in German Bight by Hickel et al. (1993). The increased sedimentation of organic particles as a consequence of this phytoplanktonic production augments the input of matter and energy to the benthic trophic system and should induce a raise of biomass and production in this system favoring small opportunistic species (Hily, 1991). Because biomass was not measured in 1966, this hypothesis cannot be explored. However, the analysis of the 1966 and 2001 taxa lists did not show either an increase in the number of small opportunist species or in their relative abundances, which supports the assumption that there had not been strong carbon increase in the benthic Biscay system between the two periods. 4.3.2. Bottom trawling Fishing potentially causes much disturbance to benthic communities. There is no doubt that the fishing effort by bottom trawling increased between 1966 and 2001. The ICES reports published over this period showed that the increase of the fishing effort was not uniformly distributed in the whole of the area, but was stronger in the coastal area and the north-eastern part of the Grande Vasie`re. Trawling reduces the abundance of some species, either by direct mortality or indirect relationships, while it favors other species by reducing predation or competition (spatial and/or trophic) or increasing their trophic resources (e.g. scavengers) (Jennings and Kaiser, 1998; Kaiser and de Groot, 2000). In the Bay of Biscay, the ophiura Amphiura filiformis which lives in the top 5 cm of the sediment showed a very strong decrease in presence and abundance

423

over the whole area. By its behavior, it is a species particularly vulnerable to effects of dredges and trawls. In the North Sea, the occurrence of Amphiura sp. decreased from 62.5% in 1962 to 7.5% in 1986 in the heavily trawled sea bottoms (Lindeboom and de Groot, 1998). Fishing effort has increased significantly since the Second World War and the two periods analysed here represent two observation points of a longterm trend. It can thus be noted that the epibenthic pennatulid Pennatula phosphorea, that lives fixed in the sediment, used by Le Danois in 1948 as one of the flag species characteristic and representative of the Grande Vasie`re, was only found in two stations by Gle´marec in 1966 (total abundance ¼ 3) and in one station (total abundance ¼ 1) in 2001. Brissopsis lyrifera, a fragile sand urchin that lives deep enough in the sediment to escape trawling impact, remained stable in terms of occurrence between 1966 and 2001. The polychaete suspension feeder Ditrupa arietina which lives on the sediment surface in a small free calcareous tube, showed a severe decline. While it was present in four of the 1966 assemblages and was leader species in two others, in 2001 it was only present in one assemblage and in a nondominant position. A likely hypothesis is that the direct physical impacts of chain trawls largely explain the decrease of D. arietina. Inversely, several species showed a strong increase in their occurrence and abundances in 2001 compared with 1966. Among those, five free-living polychaetes (Leanira yhleni, Sthenelais limicola, Nephthys caeca, Lumbrineris impatiens, Glycera rouxi) that inhabit the sediment surface or in the uppermost sediment layer, are highly tolerant of a large gradient of fine sediments and were consequently facilitated by the homogenization and surface spreading of muddy sands in the whole area. Moreover, these species are carnivores and are therefore favored by trawling induced mortality which increases the available food (Jennings and Kaiser, 1998; Kaiser and de Groot, 2000). These processes can also facilitate populations of tubicolous species. At the bottom of their tube in the sediment these species can escape trawling effects, and they can exploit the organic particles either sedimented on the sediment surface (Terebellides stroemi, Melinna palmata, Pista cristata) or in the bottom water layer (Owenia fusiformis). As remarked by Kro¨ncke (1992), it is obvious that eutrophication and fisheries cause rather similar augmenting effects on abundance and biomass, whereas species number drops under fisheries impact due to the damage to the long-lived species. The changes in species abundances support the hypothesis that increasing organic particle flux supplies more trophic resources for the benthos. Associated with this process, the reduction in abundances of large species, that are highly sensitive and vulnerable to trawling impact, suggests that the trawling impact acted via these two synergic effects. However, some changes shown by our results cannot be explained accurately by these two processes. This is the case for the substitution of two Nephtyidae, Nephthys hombergii and Nephthys bilobata by another, Nephthys caeca, which was totally absent in 1966. This substitution does not necessarily imply functional differences for the food web. Mis-identification of the

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species cannot be hypothesized to explain the shift in the Nephthys species because the high level expertise of the authors and the relative easiness of the taxonomical identification of the species in this genus. This last species spread across six of the eight assemblages in 2001. There was a similar shift between Lumbrineris gracilis and Lumbrineris impatiens, two species that can be distinguished quite easily from one another. It can be concluded that bottom trawling undoubtedly played a role in these great macrofaunal community changes through direct impact. However, we have shown that modifications in sediment granulometry (particularly the large decrease of the fine fraction) also contributed considerably to these changes and need to be explained. How and why did the sediment characteristics change? Two types of hypotheses can be suggested: those which invoke the export of the fine fraction out of the system and those which consider a decrease in the import of the fine fraction into the system. These two processes are not incompatible and can even act synergistically. Several studies have demonstrated the export of sediments to the west (which induces a further final sedimentation in the bathyal zone) by the bottom currents, and that this process was facilitated by the strong swell episodes (Delanoe¨ and Pinot, 1980; Pinot, 1974; Castaing et al., 1999). However, there is no information available to demonstrate that this phenomenon increased either in frequency or in intensity since the 1960s. However, the amount of fine particles suspended in the bottom waters could have increased (and increased final export out of the system) under anthropic pressure. Fishing effort and the trawl effectiveness have increased, leading to much greater sediment resuspension into the water column and a bottom water layer heavily loaded with suspended matter (Churchill, 1989; Dayton et al., 1995; Ramsay et al., 1998). The rapid re-sedimentation of sands due to gravity should have induced a covering of the non re-suspended coarser fraction with fine sands, while the turbid water would be progressively carried beyond the continental platform by the bottom currents. This process could explain both the decrease in the mud and coarse fractions of the sediment surface and the increase in the sand fraction. Conversely, other particle fluxes arriving on the continental platform may have reduced between the two sampling periods. The recent silting up of the soft bottom areas along the coasts of South Brittany (Gle´marec et al., 1986; Afli and Gle´marec, 2000) is acknowledged and reinforces the probability of the decrease of the fluxes of fine particles to the Grande Vasie`re. Three processes may have acted together: (1) recent modifying work on the main rivers, particularly the large dam built (Arzal dam) on the Vilaine river, on the coast directly opposite to the center of the studied area, stopped the offshore evacuation of terrigenous effluents by swelling episodes. The estuary and the Vilaine Bay have shown high silting up since this dam was built (Le Bris, unpublished data). (2) A new regulation stopped bottom trawling in the coastal waters within 12 nautical miles offshore. Resuspension of sedimented mud consequently decreased reducing the flux to the offshore mud banks.

5. Conclusion In all, this work has shown that a great change has taken place in the North Bay of Biscay communities since the 1960s, particularly in the Grande Vasie`re area. There is little evidence that global warming has played much of a role in benthic community structure changes. Sedimentary modifications, due to several processes including the resuspension of the fine mud particles by bottom trawling, are undoubtedly the main factor explaining the modifications observed in the macrobenthic fauna. The direct effects of the trawling activities, facilitating some species (particularly small mobile deposit feeders and carnivores) but destroying some others (particularly epibenthic non-mobile fauna) also played a role in macrobenthic community changes. At a regional scale these processes have led to the dominance of a few species that are tolerant to the physical constraints of trawling, modifications of the suspended matter levels in the bottom waters, and the changes in the granulometry of the sediments. The consequences are a homogenization and standardization of the sediments and associated communities, accompanied by a decrease of the b diversity (i.e. less number of assemblages of species at the regional scale in 2001). Because there are just two sampling series 35 years apart, it is not possible to discuss about the temporal scale of the changes. However, the large changes in the sediment characteristics argue that these processes acted over a large spatiotemporal scale and that they are probably still active, as fishing effort in the early years of the XXI century remained equivalent (or superior) to the level of the end of the 1990s. Acknowledgments This study was funded by the CNRS and University of Brest. The authors are grateful to the crews of the RV ‘Coˆtes de la Manche’ and Robert Marc for drawing the map. References Afli, A., Gle´marec, M., 2000. Fluctuations a` long terme des peuplements macrobenthiques dans le Golfe du Morbihan (Bretagne, France). Cahiers de Biologie marine 41, 67e89. Buchanan, J.B., Moore, J.J., 1986. A broad review of variability and persistence in the Northumberland benthic fauna e 1971e85. Journal of the Marine Biological Association UK 66, 641e657. Castaing, P., Froidefond, J.M., Lazure, P., Weber, O., Prud’homme, R., Jouanneau, J.-M., 1999. Relationship between hydrology and seasonal distribution of suspended sediments on the continental shelf of the Bay of Biscay. Deep-Sea Research II 46, 1979e2001. Chasse´, C., Gle´marec, M., 1976. Principes ge´ne´raux de la classification des fonds pour la cartographie se´dimentaire. Journal de la Recherche Oce´anographique 1, 1e11. Churchill, J.H., 1989. The effect of commercial trawling on sediment shelf resuspension and transport over the middle Atlantic Bight continental shelf. Continental Shelf Research 9, 841e864. Cornet, M., Lissalde, J.P., Bouchet, J.-M., Sorbe, J.-C., Amoureux, L., 1983. Donne´es qualitatives sur le benthos et le suprabenthos d’un transect du plateau continental Sud-Gascogne. Cahiers de Biologie Marine 24, 69e84.

C. Hily et al. / Estuarine, Coastal and Shelf Science 78 (2008) 413e425 Dayton, P.K., Thrush, S.F., Agardy, M.T., Hofman, R.J., 1995. Environmental effects of marine fishing. Aquatic Conservation: Marine and Freshwater Ecosystems 5, 205e232. Delanoe¨, Y., Pinot, J.-P., 1980. Aperc¸us sur la dynamique se´dimentaire du pre´continent atlantique breton: 2. La mobilite´ des sables, son influence sur la morphologie actuelle et les structures se´dimentaires. Annales de l’Institut Oceanographique 56, 61e72. Frid, C.L.J., Buchanan, J.B., Garwood, P.R., 1996. Short communication: variability and stability: twenty-two years of monitoring of Northumberland. ICES Journal of Marine Science 53, 978e980. Gle´marec, M., Le Bris, H., Le Guellec, C., 1986. Modifications des e´cosyste`mes des vasie`res coˆtie`res du sud-Bretagne. Hydrobiologia 142, 159e170. Grall, J., Chauvaud, L., 2002. Marine eutrophication and benthos: the need for new approaches and concepts. Global Change Biology 8, 813e830. Gray, J.S., 1981. The Ecology of Marine Sediments: an Introduction to the Structure and Function of Benthic Communities. Cambridge University Press, Cambridge, 185 pp. Gre´mare, A., Amouroux, J.M., Ve´tion, G., 1998. Long-term comparison of macrobenthos within the soft bottoms of the Bay of Banyuls-surmer (Nothwestern Mediterranean Sea). Journal of Sea Research 40, 281e302. Hickel, W., Mangelsdorf, P., Berg, J., 1993. The human impact in the German Bight: eutrophication during three decades (1962e1991). Helgolaender Meeresuntersuchungen 47, 243e263. Hily, C., 1987. Spatio-temporal variability of Chaetozone setosa (Malmgren) population on an organic gradient in the Bay of Brest (France). Journal of Experimental Marine Biology and Ecology 112 (3), 201e216. Hily, C., 1991. Is the activity of the benthic suspension feeders a factor controlling water quality in the Bay of Brest? Marine Ecology Progress Series 69, 179e188. Howson, C.M., Picton, B.E., 1997. The Species Directory of the Marine Fauna and Flora of the British Isles and Surrounding Seas. Ulster Museum & The Marine Conservation Society, Belfast, 508 pp. Hurrell, J.W., 1995. Decadal trends in the North Atlantic Oscillation: regional temperatures and precipitations. Science 7, 676e679. Jennings, S., Kaiser, M.J., 1998. The effects of fishing on marine ecosystem. Advances in Marine Biology 34, 201e352. Kaiser, M.J., de Groot, S.J., 2000. Effects of Fishing on Non-Target Species and Habitats. Blackwell Science, 399 pp. Koutsikopoulos, C., Beillois, P., Leroy, C., Taillefer, F., 1998. Temporal trends and spatial structures of the sea surface temperature in the Bay of Biscay. Oceanologica Acta 21, 335e344. Kro¨ncke, I., 1992. Macrofauna standing stock of the Dogger Bank. A comparison: III 1950e54 versus 1985e87. A final summary. Helgolaender Meeresuntersuchungen 46, 137e169. Kro¨ncke, I., Dippner, J.W., Heyen, H., Zeiss, B., 1998. Long term changes in macrofaunal communities off Nordeney (East Frisia, Germany) in relation to climate variability. Marine Ecology Progress Series 167, 25e36.

425

Le Danois, E., 1948. Les profondeurs de la mer. Payot, Paris, 303 pp. Lebart, L., Morineau, A., Fe´nelon, J.P., 1982. Traitement des donne´es statistiques. Me´thodes et programmes. Dunod, Paris, 510 pp. Legendre, L., Legendre, P., 1984. Ecologie nume´rique. Tome I: Le traitement multiple des donne´es e´cologiques. Masson, Paris, 260 pp. Lesueur, P., Klingebiel, A., 1976. Carte des se´diments superficiels du plateau continental du Golfe de Gascogne e Partie septentrionale (e´chelle 1/500 000). BRGM, IFREMER. Lindeboom, H.J., de Groot, S.J., 1998. The Effects of Different Types of Fisheries on the North Sea and Irish Sea Benthic Ecosystems. Netherlands Institute of Sea Research, Texel, 404 pp. Pearson, T.H., Duncan, G., Nuttall, J., 1986. Long term changes in the benthic communities of Loch Linnhe and Loch Eil (Scotland). Hydrobiologia 142, 121e127. Pearson, T.H., Josefson, A.B., Rosenberg, R., 1985. Petersen’s benthic stations revisited, I. Is the Kattegatt becoming eutrophic? Journal of Experimental Marine Biology and Ecology 92, 157e206. Pe´re`s, J.M., Picard, J., 1957. Note pre´liminaire sur une communaute´ benthique re´cemment mise en e´vidence: la bioce´nose a` Dentalium rubescens Desh. et Lucina (Miltha) borealis Lin. Recueil des Travaux de la Station Marine d’Endoume 21, 45e47. Pinot, J.-P., 1974. Le pre´continent breton entre Penmarc’h, Belle-Ile et l’escarpement continental, e´tude ge´omorphologique. Impram, Lannion, 256 pp. Planque, B., Beillois, P., Je´gou, A.-M., Lazure, P., Petitgas, P., Puillat, I., 2003. Large-scale hydroclimatic variability in the Bay of Biscay: the 1990s in the context of the interdecadal changes. ICES Marine Science Symposia 219, 61e70. Poulard, J.-C., Blanchard, F., 2005. The impact of climate change on the fish community structure of the eastern continental shelf of the Bay of Biscay. ICES Journal of Marine Science 62, 1436e1443. Ramsay, K., Kaiser, M.J., Hughes, R.N., 1998. Responses of benthic scavengers to fishing disturbance by towed gears in different habitats. Journal of Experimental Marine Biology and Ecology 224, 73e89. Reise, K., 1982. Long-term changes in the macrobenthic invertebrate fauna of the Wadden Sea: are polychaetes about to take over? Netherlands Journal of Sea Research 16, 29e36. Reise, K., Schubert, A., 1987. Macrobenthic turnover in the subtidal Wadden Sea: the Norderaue revisited after 60 years. Helgolander Marine Research 41, 69e82. Rosenberg, R., Gray, J.S., Josephson, A.B., Pearson, T., 1987. Petersen’s benthic stations revisited. II. Is the Oslofjord and the eastern Skaggerak enriched? Journal of Experimental Marine Biology and Ecology 105, 219e251. Vincent, A., Kurc, G., 1969. Hydrologie, variations saisonnie`res de la situation thermique du Golfe de Gascogne en 1967. Revue des Travaux de I’Institut des Peˆches Maritimes 33, 79e96.