History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description

SEARES-01319; No of Pages 14 Journal of Sea Research xxx (2014) xxx–xxx

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History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description Jean-Claude Dauvin ⁎ Normandie Université, France Université de Caen Basse Normandie, Laboratoire Morphodynamique Continentale et Côtière, UMR M2C, 24 rue des Tilleuls, F-14000 Caen, France CNRS UMR CNRS 6143M2C, 24 rue des Tilleuls, 14000 Caen, France

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Article history: Received 3 February 2014 Received in revised form 12 November 2014 Accepted 13 November 2014 Available online xxxx Keywords: Benthic Communities General Distribution Habitat Approach Multidisciplinary Approach

a b s t r a c t Benthic studies in the English Channel (EC), a shallow megatidal and epicontinental sea, began in the 1960s and 1970s with the work of teams led by Norman Holme (UK) and Louis Cabioch (F). During this period, benthic sampling was mainly qualitative, i.e. using a device such as the ‘Rallier du Baty’ dredge in the case of the French team and a modified anchor dredge in the case of the British team. Studies were focused on acquiring knowledge of the main distributions of benthic communities and species. Surveys on the scale of the whole EC led to the recognition of general features and two main patterns were identified: 1) the role of hydrodynamics on the spatial distribution of sediment, benthic species and communities; 2) the presence of a west–east climatic gradient of faunal impoverishment. Benthic studies in the 1980s–1990s were focused on the beginning of the implementation of long-term survey at a limited number of sites to identify seasonal and multi-annual changes. In the first decade of the 2000s, the implementation of the European Water Framework Directive and the Marine Strategy Framework Directive to define the Ecological Quality Status of marine environments increased the need to acquire better information of the structure and functioning of benthic communities, since benthic species and habitats were recognised as good indicators of human pressure on marine ecosystems. Faced with the increase of human maritime activities, the appearance of invasive species and the need to preserve sensitive marine habitats, benthic studies have been focused on developing a ‘toolkit’ to help in the decision-making and planning for both sound governance and sustainable management of marine resources and human activities in the English Channel. Multidisciplinary approaches were used to differentiate habitats in a more precise detail. Both indirect (side-scan sonar, ROV) and direct (grab sampling with benthos identification and grain-size analyses) approaches were used and combined to allow the description of benthic habitats using numerous descriptors. These approaches were mainly applied on a local scale, leading to the identification of habitat mosaics mainly in coarse sands, gravels and pebbly areas which cover 80% of the EC seabed. They also allowed the enrichment of the EUNIS habitat classification for infralittoral and circalittoral zones taking into account the scale of observations of benthic habitats. Moreover, several recommendations for future benthic studies are proposed within a HABITAT approach. © 2014 Elsevier B.V. All rights reserved.

1. Introduction The English Channel (EC), called ‘La Manche’ in French, is a sea area shared between the United Kingdom to the north and France to the south. After a long historical process, the marine parts of each of these two bordering countries are now clearly delimited, especially for the Normano-Breton Gulf where the territories of the Channel Islands are not included in the European Union. At the end of the 19th century, there was an increase in marine biology research mainly focused on the description of marine biodiversity and ⁎ Université de Caen Basse Normandie, Laboratoire Morphodynamique Continentale et Côtière, UMR M2C, 24 rue des Tilleuls, F-14000 Caen, France. E-mail address: [email protected].

developmental biology to investigate the evolutionary mechanisms and phylogeny of marine organisms. During this period, marine biological laboratories (Marine Stations) were established to conduct this type of research. Four main marine stations were created along the EC coast: in 1872 at Roscoff in North Brittany (Paris University), in 1874 at Wimereux in the Dover Strait (Lille University), in 1888 at Plymouth in the United Kingdom (Marine Biological Association) and in 1891 at Tatihou on the North Cotentin coast (National Museum of Natural History, Paris). Since 1935, this latter station has been located at Dinard in the Normano-Breton Gulf. Eighty years later, research on benthic communities at the scale of the EC was initiated at Plymouth under the authority of Norman Holme and at Roscoff under the authority of Louis Cabioch, following their regional observations (Cabioch, 1961; Holme, 1961). These two authors were the pioneers of benthic research

http://dx.doi.org/10.1016/j.seares.2014.11.005 1385-1101/© 2014 Elsevier B.V. All rights reserved.

Please cite this article as: Dauvin, J.-C., History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description, J. Sea Res. (2014), http://dx.doi.org/10.1016/j.seares.2014.11.005

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in the entire EC, which probably represents one of the most intensively studied seas on the scale of the north-eastern Atlantic continental shelf, along with the North Sea and the Baltic. More recently, with the intensification of human activities, there has been a dramatic increase of benthic studies in the EC, aimed at identifying the contribution of anthropogenic factors to climatic change and assessing benthic quality status under the European Directives. This paper presents a history of benthic habitat mapping in the English Channel over the last five decades (1960–2012) as a compilation of published and unpublished works and result. An overview of the researches performed on benthic communities and benthic habitat mapping is presented to show 1) the evolution of the research objectives; 2) the development of sampling and surveying methods to map benthic habitats, 3) the increase of studies dedicated to assessing the impact of various human activities on benthic communities, since the benthos is a good indicator of the ecological quality status of the marine environment and 4) the new challenges on benthic patterns occurring in the Channel. The overview takes into account the whole of the EC during the first two decades (1960–1970), but mainly concerns the eastern basin of the English Channel (EBEC) for three more recent decades (1980–2012). The choice to focus this paper on the eastern area is justified for several reasons: 1) the existence of a general map of benthic communities based on the EUNIS classification (Cabioch et al., 1978); 2) human pressures on benthic habitats are significant, especially in relation to aggregate extraction; and 3) the benthic research of the European INTERREG CHARM project was mainly concentrated on this eastern basin.

2. The EC context The EC is a shallow epicontinental sea (maximum depth of 174 m in the central trench) extending over an area of about 77,000 km2 and comprising two main basins (Cabioch, 1968): the western basin of the English Channel (WBEC) and the eastern basin of the English Channel (EBEC) (Fig. 1). The WBEC is deeper than the EBEC (Paphitis et al., 2010) and shows distinct characteristics in terms of oceanographic and human pressures (Dauvin, 2012). In the WBEC, hydrologic and oceanographic characteristics are influenced by the Atlantic water and the presence of a summer thermocline offshore Plymouth in the northwest, while the characteristics of the EBEC are mainly affected by the Seine Estuary. The most important forcing for the benthic habitats in the EC is the presence of very strong currents due to the tidal flow propagating from west to east. Nevertheless, due to the Coriolis force, the current velocities are higher along the French coast than the English coast. The strongest currents recorded during spring tide are N3 knots in north Brittany, off the Cotentin Peninsula and in the Dover Strait, rising to N 8 knots off the Cap de La Hague (Salomon and Breton, 1991,

1993). Significant gyres are present around the Channel Islands and to the east of the headlands of Frehel, Barfleur, Antifer and Gris Nez (Salomon and Breton, 1991, 1993). Hence, the distribution of superficial sediments is the result of tidal circulation, with the development of an offshore–inshore hydrodynamic regime leading to a sedimentary gradient: extensive pebbly sediments dominate in areas of strong tidal currents located offshore and to the east of the headlands, whereas fine sands and muddy fine sands appear in areas of weak tidal currents in bays and estuaries (Larsonneur et al., 1982; Vaslet et al., 1979). As a result of hydrodynamic forces, areas of fine-grained sediment are more extensive on the English side than on the French side; the coarse-grained surface sediments are dominated by coarse sands and pebbles, which cover N 80% of the EC seabed area (Larsonneur et al., 1982). Another particular feature of EC sediments is their high content in biogenic calcareous material, ranging up to 70% in the bioclastic sediments which dominate the central part of the WBEC; the proportion of terrigenous material is higher in the EBEC than in the WBEC (Larsonneur et al., 1982). The Channel is a biogeographical transition zone since it is situated between the Lusitanian province to the south and the Boreal province to the north (Forbes, 1858); in this way, the EC is affected by a balance between the recovery of warm temperate species during warming periods and the recovery of boreal species during cooling periods (Southward et al., 2004). Finally, the EC is strongly impacted by human activities (Dauvin, 2008, 2012). Halpern et al. (2008) pointed out that the North Sea, the EC and Japanese waters represent coastal marine zones where cumulative human impacts have the greatest influence on the worldwide Ocean. Moreover, Dauvin and Lozachmeur (2006) and Dauvin (2012) have stressed that the EBEC is more impacted by human activities than the WBEC, due to the accumulation of traditional activities (fisheries, navigation, sediment deposition, etc.) and the emergence of new activities (aggregate extraction, offshore wind farm installations, etc.).

3. Mapping studies in the English Channel during the early 1960s and 1970s The main objective of the studies carried out by Holme and Cabioch was to describe the species and distribution of macrobenthic communities at the scale of the EC (see also Coggan and Diesing, 2011 for a review). They mainly used the Decca navigational positioning system, as well as anchor-type or Rallier du Baty dredges, to collect qualitative or semi-quantitative data, respectively, by sieving a constant volume of 30 L in the case of the French team. They also utilised automatic sub-marine photography to obtain supplementary information on the nature of the sediment and the composition of the epifauna, mainly made up of sessile species on hard substrates (Cabioch, 1967; Holme

Fig. 1. Map of the English Channel. WBEC: Western Basin of the English Channel. EBEC: Eastern Basin of the English Channel, with indication of the cited locations.

Please cite this article as: Dauvin, J.-C., History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description, J. Sea Res. (2014), http://dx.doi.org/10.1016/j.seares.2014.11.005

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and Barrett, 1977). At the end of the 1950s, English and French teams began to explore the areas in the WBEC, by sampling 167 stations off the Plymouth Marine Laboratory (Holme, 1961) and by collecting ca. 800 dredges offshore from Roscoff (Cabioch, 1961). In 1960–1962, Holme (1966) sampled the benthic habitats on 144 stations covering the entire EC, using mainly north–south transects from the western approaches of the EC to the Dover Strait. Based on 311 stations, Holme's team determined five boreal offshore benthic associations with different sediment types: i) a gravel association, covering the widest area; ii) a muddy-gravel association; iii) a sand association; iv) a mud association, observed at only three stations on the English side of the Dover Strait, and v) a muddy-sand association, observed in bays on the English side of the EC and on two stations from the eastern part of the Baie de Seine. Holme focused his 1966 paper on the distribution patterns of the macrobenthic species and identified seven categories of species distribution: 1) species occurring throughout the EC; 2) western species limited along the coast of western England and having a southward distribution around Guernsey; 3) western Channel species present in the WBEC; 4) Cornubian species, corresponding to warm species with limited penetration into the EC from the west; 5) Sarnian species, mainly present in the Normano-Breton Gulf; 6) eastern species, also called northern species; and 7) miscellaneous species. In the first species group, Holme distinguished three sub-patterns: 1) species generally distributed throughout the EC; 2) species present along the English coast, but rare or absent along the French coast; and 3) species mainly present along the French coast of the EC. In his thesis, Cabioch (1968) described the distribution of the benthic species and communities in terms of population, biocoenosis and facies (‘peuplement’, ‘biocoenose’ and ‘faciès’ in French) for offshore Northern Brittany. In these first maps of the benthic communities of the EC, Cabioch distinguished two main domains: the ‘frontolittoral’ domain, located mainly in the shallow sub-tidal zone (‘étage infralittoral’ in French) showing a mosaic of habitats, and the more homogenous offshore domain (‘prélittoral’ in French) corresponding to the circalittoral zone. In the ‘frontolittoral’ domain, Cabioch described three main groups composed of six communities: 1) three groups of communities in the infralittoral zone, including the Abra alba–Corbula gibba fine sand community, the maerl community and the hard bottom community; 2) the Axinella dissimilis hard bottom community of the circalittoral zone and 3) communities developed independently of the different zones (‘étages’ in French), including the Venus fasciata coarse sand community and the Musculus discors hard bottom community. In the ‘prélittoral’ domain, Cabioch identified three main communities: 1) the A. dissimilis hard bottom community; 2) the gravel and pebble communities, developed in both nearshore and offshore circalittoral zones and, 3) the V. fasciata coarse sand community. These distributions

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are consistent with the observations of the North-Eastern Atlantic continental shelf communities (see Glémarec, 1973, 1994). During the explorative phase of studies on the benthic communities of the EC, Cabioch and Gentil (1975), Cabioch and Glaçon (1975, 1977), Gentil (1976) and Gentil and Cabioch (1997) used a sediment Rallier du Baty dredge for sampling. After completing his PhD thesis work and producing a map of the benthic communities off northern Brittany (Figs. 2, 1), L. Cabioch formed a team during the early 1970s bringing together researchers from Caen University (C. Larsonneur) to study the characteristics of the surface sediments, in association with Dinard (C. Retière) and Wimereux (R. Glaçon) to study the distribution of macrozoobenthic communities and species. During the same period, Gentil (1976) began his PhD thesis on the mapping of benthic communities in the Baie de Seine. This was also the period when the French government decided to develop nuclear power plants along the coast. For this development, it was necessary to establish reference points prior to the industrial production of electricity, since these activities would entail the pumping and release of large volumes of water leading to warming of the sea; consequently, the number of sampling sites was higher in the expected area of construction of nuclear power plants, i.e. the sites of Baie des Veys, Palluel and Penly along the Upper Normandy coast and Gravelines in the southern part of the North Sea (the Baie des Veys project was later abandoned). As well as the sampling stations near the nuclear power plants, the number of stations was higher near the coast than offshore and along the English side of the EC. In this way, a total of 1495 benthic stations were sampled during the period from 1971 to 1976 at the scale of the EBEC (San Vicente-Añorve, 1995). From these data, several maps of benthic communities were drawn up (Fig. 2): for the Baie de Seine and the central part of the EC offshore from the Baie de Seine (Gentil and Cabioch, 1997) as well as for the eastern part of the EBEC along the French coast (Cabioch and Glaçon, 1975, 1977). Considering all the available data on macrobenthic communities in the EBEC, Cabioch et al. (1978) published the first map of this area taking into account both physical and biological characteristics, in a way that was similar to the modern EUNIS habitat classification scheme. As a result, seven main macrobenthic communities were identified corresponding to the EUNIS habitats (Cabioch et al., 1978; Dauvin, 1997): – Coarse gravels and pebbles community (A4-13_FR01: sessile fauna on circalittoral coarse gravels and pebbles), with the type facies (i.e. gravel and pebble community), a facies with just pebbles and a facies with an impoverished community on gravelly pebbles. – Sandy gravels and gravels community (A4-13_FR02: sandy gravel habitats).

Fig. 2. Regional map showing benthic communities of the English Channel. 1. Cabioch, 1968; 2: Retière, 1979; 3; Cabioch and Gentil, 1975; 4: Cabioch and Glaçon, 1975; 5: Cabioch and Glaçon, 1975; 6: Gentil and Cabioch, 1997; 7: Davoult et al., 1978; 8: Cabioch et al., 1978.

Please cite this article as: Dauvin, J.-C., History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description, J. Sea Res. (2014), http://dx.doi.org/10.1016/j.seares.2014.11.005

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– Amphioxus lanceloatus coarse sand community (A5-135 Branchiostoma lanceolatum on circalittoral coarse sand with shell gravel). – Ophelia borealis–Nephtys cirrosa fine and medium clean sands community (A5-251 Echinocyamus pusillus, Ophelia borealis and Abra prismatica on circalittoral fine sand). – A. alba muddy fine sand community (A5-244 Spisula subtruncata and Nephtys hombergii on shallow muddy sand). – Heterogeneous muddy mixed community, considered by Dewarumez et al. (1992) as an ecotone between the pebbles community and the A. alba community (A5.43_FR03 Pista cristata on shallow sub-tidal mixed sediment). – Macoma balthica community in estuarine muddy fine sand and mud (A5.222. N. cirrosa and M. balthica on shallow sub-tidal mobile sand under variable salinity conditions). Due to a climate effect related to a higher amplitude of seatemperature variation between winter and summer in the EBEC, the biodiversity of benthic invertebrates is impoverished (Cabioch et al., 1977). Cabioch and his co-workers concluded that species distribution reflects their tolerance to the environmental conditions (Cabioch et al., 1977). Three main types of distribution were identified. The first type is determined by ‘climate’, primarily the temperature and salinity gradients, and leads to the progressive disappearance of stenotherm species from the WBEC, due to their drifting towards the EBEC. A second type of distribution, known as edaphic, is controlled by the occurrence of areas of rocky or stony seabed with strong currents. Finally, edapho-climate distributions correspond to a blend of the previous distributions, and are shown by taxa influenced by both seabed and climate conditions. This latter type of distribution is absent from the areas of the WBEC furthest from the European mainland, but is associated with the pebbly and gravelly bottoms distributed widely throughout the Channel, from the Brittany coast to the central and EBEC (Coggan and Diesing, 2011). Working on the EBEC database (including 1477 stations × 630 identified taxa, mainly at the species level), L. San Vicente-Añorve (San Vicente-Añorve, 1995; San Vicente-Añorve et al., 1996, 2002) described several habitat typologies and derived some information about the biodiversity of the area and the species distribution of dominant species. This author used multivariate analyses with different statistical distances (Hellinger, Euclidian, Chi2), and different selections of species in relation to their occurrence and abundance (presence/ absence; abundance; occurrence N 5 and 10 stations) on raw and transformed data, and selection of the number of stations. She pointed out the very high consequence of statistical analysis and selection of species and stations on the mapping of benthic communities. Some of San Vicente-Añorve's maps are comparable to the sediment map of Larsonneur et al. (1982) or the benthic community map of Cabioch et al. (1978), which were drawn by hand based on the expertise of researchers concerning the sediment types and the dominant or characteristic benthic species. Other maps show strong discrepancies with the Larsonneur and Cabioch maps being influenced to a greater or lesser extent by the presence of surficial pebble and gravel communities within the wider EBEC. Moreover, San Vicente-Añorve discussed the important role of rare species in the statistical analyses; similar effects of statistical methods and selection of species were pointed out in the PhD of Carpentier studying a sub-set of stations from the eastern part of the EC (Carpentier, 1999). The research team of the Marine Station of Wimereux teams have published several local maps of the benthic communities for the Dover Strait (Bourgain et al., 1985; Clabaut and Davoult, 1989; Davoult, 1988; Davoult and Clabaut, 1988; Davoult and Richard, 1988; Prygiel, 1987; Prygiel et al., 1988; Souplet and Dewarumez, 1980; Souplet et al., 1980). However, a synthesis of all available data has been published in the map of benthic communities for the French part of the North Sea (Davoult et al., 1988) (Fig. 2).

Retière (1975, 1979) produced the first integrated map of the distribution of macrobenthic communities in the Normano-Breton Gulf (Fig. 2, 2) which was revisited three decades later per Trigui (2009). So, as a result of this very intensive exploration of the EC, general maps had been drawn up for the EBEC, but only regional maps were available along the French side of the WBEC. The other available historical data (1960–1980) should be analysed to obtain similar benthic communities maps for the WBEC comparable with those existing for the EBEC. After the explorative phase at the scale of the EC, benthic research during the 1980s and 1990s entered into a phase of long-term observations on some local communities, such as the muddy fine sand A. abra communities in the Bay of Morlaix after the Amoco Cadiz oil spill or concerning the Gravelines area in the framework of the monitoring of the nuclear power plant (Ghertsos et al., 2000; Dauvin, 2010). Other studies were focused on the seasonal changes and functioning of the Ophiothrix fragilis community in the Dover Strait (Davoult, 1988; Migné and Davoult, 1995, 1997). These quantitative studies used several types of grabs, sampling by divers, in situ chambers placed on the sea bed, and precise systems of ship positioning. At the same time, the research on aggregates and their extraction gave rise to renewed interest in benthic studies integrating the need for knowledge of aggregate resources and the impact of extraction on benthic habitats (Arnal et al., 1985; Dauvin, 1997). This provided the opportunity to develop new techniques for benthic observations (Birchenough et al., 2010; Boyd et al., 2003; Brown et al., 2002, 2004a,b, 2011; Cooper, 2012, 2013; Eastwood et al., 2007; Foster-Smith et al., 2004; Le Bot et al., 2010). 4. Aggregate extraction Aggregate extraction is a recent challenge for marine economic activity management in the eastern English Channel (Dauvin and Lozachmeur, 2006). This shallow sea has an extensive network of paleo-valleys, which are partly filled with coarse sediment up to several metres thick in some areas (Dingwall, 1975; Gupta et al., 2007). This kind of sediment represents a major source of aggregates for industry. The impact of aggregate extraction on benthic habitats in the EBEC and the North Sea has been addressed through numerous scientific publications (Boyd and Rees, 2003; Boyd et al., 2003; Cooper et al., 2007; Desprez, 2000; Desprez et al., 2010; Foden et al., 2009, 2010; James et al., 2007, 2010; Newell et al., 1999, 1998). Marine resources represent only 1% of the national aggregate production in France (Sutton et al., 2008), but the granting of three exploration licences to aggregate companies for three sites (initially called Charlemagne, Saint Nicolas and Côte d'Albâtre) in the eastern EC foreshadow a change in the French extraction industry in the next few years (Dauvin and Lozachmeur, 2006). As an example of the French procedure, the company owning the Charlemagne exploration licence site carried out benthic monitoring in 2007 to compile a reference state based on a biannual sampling survey (pre- and post-recruitment). The site was renamed ‘PER Manche Orientale’ because its status was changed to Permis Exclusif de Recherche by a ministerial order of 26 January 2006; the extraction of aggregates (2 million m3 per year) began at the end of 2012 for a duration of 30 years. In collaboration with research laboratories, the pre-extraction period (2007–2010) provided a good opportunity to obtain a better baseline, as recommended by certain authors (Lozach, 2011; Lozach and Dauvin, 2012). In fact, there are few quantitative studies on the natural spatial and temporal variability of coarse sediment communities in the eastern English Channel because this type of sediment has been difficult to sample before widespread adoption of the use of the Hamon grab, as this type of sediment is hard and the organisms are highly dispersed (Dauvin and Ruellet, 2008). In their review, Brown et al. (2011) summarised the different strategies and methods to produce benthic maps using acoustic remote

Please cite this article as: Dauvin, J.-C., History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description, J. Sea Res. (2014), http://dx.doi.org/10.1016/j.seares.2014.11.005

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sensing techniques coupled with in situ sampling. These authors highlight the rapid increase and evolution in the level of sophistication in the ability to acquire high-resolution images and map seafloor habitats. They also defined three main strategies for the production for benthic habitat maps: 1) abiotic surrogates only (unsupervised), using only environmental (physical) data layers; 2) assemble first, predict later, using ‘Top Down’ (unsupervised) approach, taking into account both in situ biological/geological data and environmental (physical) data layers and 3) predict first assemble later, using ‘Bottom Up’ (supervised) approach, with the same biological, geological and physical layers. Mainly for the areas of aggregate extraction in the EC, the CEFAS team developed an integrated approach (Brown et al., 2002, 2004a,b) using both sidescan sonar and grab sampling to map a variety of benthic biotopes as well as their distribution, i.e. seabed habitats and their associated biological communities. As an example, these authors investigated a study area (28 km × 12 km) to the east of the Isle of Wight in a zone of homogeneous substrate, using a sidescan sonar on board a vessel equipped with a Differential Global Positioning System (DGPS), an underwater video camera dropped to the seabed and sampling 43 stations with a 0.1 m2 Hamon grab. A total of 223 taxa were identified, corresponding to seven assemblages grouped together in five distinct biotopes: A, E. pusillus — Maldanidae and B, E. pusillus–Spisula sp. on gravelly sand; C, A. prismatica–Glycera sp. on clean mobile sand; D, Lumbrineris gracilis — Maldanidae on heterogeneous sediment; E, Ampelisca sp.–Amphipholis squamata on heterogeneous mixed sediment; F, O. borealis–Bathyporeia sp. on sand and gravelly sand, and G, Crepidula fornicata–Scalibregma inflatum on cobbles with algae. The CEFAS team concluded that the combination of techniques was useful for mapping sea-bed biotopes, and this approach appeared to have many advantages over more traditional methods for identifying a mosaic of biotopes. 5. The Baie de Seine The Baie de Seine is the largest bay of the English Channel (~5000 km2). After an exploratory phase for studying the benthic communities of the Baie de Seine (Cabioch and Gentil, 1975; Gentil, 1976; Gentil and Cabioch, 1997), quantitative data was initially collected only at local scales, i.e. to the east and at the mouth of the Seine estuary (Cabioch, 1986; Elkaim et al., 1982; Ghertsos et al., 2001; Irlinger, 1985; Proniewski and Elkaim, 1980; Thiébaut, 1994; Thiébaut et al., 1997). Subsequently, quantitative data was collected in the western part of the bay in the Baie des Veys (Dauvin et al., 2004) and finally at the scale of the whole Baie de Seine (Ghertsos, 2002). The broad-scale distribution of benthic communities has been shown to be dependent on sediment texture, giving rise to a bio-sedimentary classification, varying from gravels and pebbles in the north-western part of the Baie de Seine, in areas with strong hydrodynamics, to fine sand and muddy fine sands in the inner part of the Bay opposite the Seine mouth and the Baie des Veys in areas with weaker hydrodynamics. Since 1986, the macrofaunal distribution in the eastern Baie de Seine has been regularly studied during winter benthic surveys, especially in the context of the PECTOW (Pectinaria/Owenia) campaigns, organised before the recruitment period of the dominant species, which took place in 1986, 1987, 1988, 1991, 1996, 2001, 2006, and 2011 (Thiébaut et al., 1997; Barnay, 2003; Dauvin et al., 2007; unpublished data). At present, data are available from a total of eight campaigns, with a grid of 40 to 77 stations according to the year. These winter samples were collected using a Hamon grab (0.25 m2, about 15 cm depth, 2 mm sieve mesh) with two benthic macrofauna replicates at each station. Two supplementary campaigns were organised in September 2008 and 2009 (five replicate samples using a 0.1 m2 Van Veen grab, 1 mm mesh sieve) to determine the effect of recruitment on the distribution of benthic assemblages (Alizier, 2011). In spite of human and natural impacts such as dredging and sediment deposition, changes in the freshwater inflow of the Seine in relation to the

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hydrological regime (low discharge during the last decade) and increase of fine particles in the eastern part of the Baie de Seine, there are persistent patches of high diversity and abundance in this area, with high abundances opposite the mouth of the Seine, along the coasts of the ‘Pays de Caux’ and the ‘Pays d'Auge’. In parallel with the silting up of the area, some species such as the polychaete Melinna palmata or the decapod Asthenognathus atlanticus have recently colonised the muddy fine and mixed sediments of the eastern part of the Baie de Seine (Dauvin et al., 2007; Jourde et al., 2012). Sedimentary organic matter content also plays an important role in controlling the structure of benthic populations and assemblages, mainly opposite the mouth of the Seine estuary (Thiébaut et al., 1997). During the PNEC (Programme National d'Environnement Côtier) project, two quantitative campaigns were organised at the scale of the Baie de Seine. A total of 44 and 46 sites were sampled in September 1998 and May 1999, respectively, although only 35 sites were common to both sampling campaigns. Four replicates from each site where obtained using the 0.25 m2 Hamon grab. Sediment was sieved with a 2 mm mesh. An additional grab sample was taken at each of the sites for the analysis of environmental parameters. Based on a successful application of the Souissi et al. (2001) method for mapping marine communities, the unpublished Fig. 3 shows an assemblage map derived from the 1998 and 1999 datasets (Ghertsos, 2002). The macrobenthic sampling stations can be characterised by four main assemblages (Fig. 3). Correspondences with the Cabioch et al. (1978) map using the EUNIS classification are given bellow. Assemblage A corresponds to the A. alba-P. koreni community on fine and muddy sand. It is situated at the south-western and south-eastern extremities of the Baie de Seine, as well as in a small patch farther south which developed in 1998 along the Calvados coast. Two subgroups can be distinguished (A1 and A2) which are located only in the eastern part of the Bay near the mouth of the Seine estuary. A1 is characterised by Ensis arcuatus, N. cirrosa and Echinocardium cordatum (A5. 251. E. pusillus, Ophelia borealis and A. prismatica in sub-littoral fine sand), while A2 is characterized by A. alba, Owenia fusiformis and P. koreni (A5.244. S. subtruncata and N. hombergii in shallow muddy sand). Assemblage B corresponds to an intermediate zone situated along the southern coast of the Bay, as well as at the centre and in the northeastern corner. This assemblage is defined by the presence of epifaunal species such as Pomatoceros triqueter, Pista cristata and Psammechinus miliaris and Branchiostoma lanceolatus. This latter species is an indicator of coarse sandy sediments, associated with a heterogeneous mixture of sediments including coarse gravels, coarse sands and the presence of muds (corresponding to a mixture between A5.135 B. lanceolatum in sub-littoral coarse sand with shell gravel and A5.43_FR3 P. cristata in infralittoral mixed sediments). Assemblage C corresponds to the patchy O. fragilis sites on gravel substrates, particularly in the northern part of the Bay. (A4.13_FR02 sandy gravel habitats). Assemblage D includes all the ‘residual’ sites on gravels, many in the north-western part of the bay. The characteristic species of this assemblage are represented by the bivalves Tellina crassa, Moerella donacina, Glycymeris glycymeris and the polychaete Aonides oxycephala. (A4.13_FR02 sandy gravel habitats). Therefore, quantitative Hamon grab sampling on a limited number of stations has revealed a bio-sedimentary gradient from the offshore part of the bay, characterized by high hydrodynamic forces and so low content of fine particles, to the shallow coastal zone, characterised by muddy sandy and weak tidal currents. Moreover, patches of O. fragilis can be clearly identified. These patches of O. fragilis play an important role in the functioning of the benthic ecosystem of the Baie de Seine because they represent zones of high benthic biomass (Ruellet and Dauvin, 2008). O fragilis is the most important contributor to total biomass at the scale of the Baie de Seine. Although the populations of O. fragilis show high densities (sometimes N 20 g AFDW m−2), that it

Please cite this article as: Dauvin, J.-C., History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description, J. Sea Res. (2014), http://dx.doi.org/10.1016/j.seares.2014.11.005

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Fig. 3. Map of macrobenthic assemblages in the Baie de Seine obtained by Ghertsos (2002) from the 1998 and 1999 PNEC quantitative samples.

is difficult to sample them repeatedly because they tend to move about over time (i.e. the O. fragilis aggregations have a degree of mobility and are not sessile) so their location (on any given day) cannot be predicted (Dauvin et al., 2013; Lozach et al., 2011). Research has indicated that their distribution cannot be explained by the recorded environmental parameters, i.e. granulometry, organic matter and pigment content in the sediment (Dauvin and Ruellet, 2008).

6. The CHARM project From 2003 to 2012, during the three phases of the CHARM (Channel Habitat Atlas for Marine Resource Management) European project, studies were undertaken on the role of the macrobenthos as a fundamental prey resource for demersal fish (Carpentier et al., 2005, 2009). The main objectives of the CHARM INTERREG project were to develop an atlas as a ‘toolkit’ to help in decision-making and planning for both sound governance and sustainable management of the English Channel's marine resources and human activities (Carpentier et al., 2005, 2009; Martin et al., 2009, 2010). In addition, research on benthic communities included sensitive habitats, and a knowledge of their distribution and functioning remained an important challenge for marine protected areas (MPA) (Delavenne, 2012; Delavenne et al., 2012). Delavenne et al. (2012) had compared two software packages, respectively Marxan and Zonation taking into account biological and socio-economic data to identify the best arrangement of protected sites to create an MPA network at the scale of the eastern basin of the English Channel. MPA appeared to be a possible tool in the context of the ecosystem-basedmanagement. The authors showed that the choice of cost metric was more important to a conservation-planning analysis than the choice of the software and that the existence of real-world data such as those that existed for the Channel gave far greater confidence when identifying areas selected by both the Marxan and Zonation software. In the same vein, Metcalfe et al. (2013) used a large macrobenthic data set containing 1314 sampling stations to test the impact of data quality on the setting of conservation objectives using the species– area relationship applied to the presence/absence data for species. The SAR approach to setting habitat targets provided an objective method for converting judgements of minimum species representation into a quantitative conservation target and provided an approach for distinguishing between different habitat types, thereby tailoring such targets to account for differences in patterns of species richness and turnover. Metcalfe et al. (2013) showed that habitat targets based on the SAR had been mainly affected by sample size, choice of richness estimator, the amount and quality of biological survey data employed, and the level of habitat classification, i.e. the EUNIS classification levels 3 and 4 (see Coggan and Diesing, 2011, for the first map of EUNIS levels 3 and 4 at the scale of the whole English Channel).

Both studies (Delavenne et al., 2012 and Metcalfe et al., 2013) underlined the need to have a large database of good quality data for such exercises of MPA planning. Similar remarks were expressed by Robinson et al. (2011) in the case of the HABMAP model used to predict the distribution of seabed biotopes in the southern Irish Sea: “the accuracy of predicted habitat maps is dependent on both quality and quantity of the input data”. During the first phase of the CHARM project (2003–2005), which focused on the Dover Strait as a connection between the North Sea and the EC, the benthic sampling consisted of a network of 46 stations sampled in April–March 2004 (Carpentier et al., 2005; Foveau et al., 2008). The ‘Rallier du Baty’ dredge was used following the same strategy adopted by Cabioch's team in the 1970s, i.e.: sieving of 30 L of sediment on a 2 mm mesh size. The aim was to compare the distribution of benthic species and communities in this area between 1972–1976 and 2004 (Carpentier et al., 2005). Temporal changes were assessed by comparing the 10 most abundant taxa and sub-tidal benthic communities between 1972–1976 and 1998–2007. Although close similarities are observed between these periods, especially regarding the species richness and average number of species per station, the diversity hotspot found off the Cap Blanc Nez in the 1970s was nevertheless located farther to the east in 2004. The observed increase in the total abundance was mostly the result of a significant increase in the abundance of the echinoderm species Ophiothrix fragilis, a species characteristic of gravel and pebble bottoms. A comparison of biosedimentary characteristics highlights the appearance of sand on the seabed, and consequently the replacement of sessile communities associated with a pebble bottom by gravelly and sandy communities (Carpentier et al., 2005). The second phase (2006–2008) of the CHARM project concerned the EBEC (Carpentier et al., 2009). New benthic data were obtained mainly during the MAcroBEnthos de Manche Orientale et du sud de la mer du Nord (MABEMONO) campaigns (2006–2007: 315 stations located east of the Greenwich meridian) (Foveau, 2009; Foveau et al., 2013; Garcia, 2010). Due to the long time required to sort and identify the macrobenthos (including epifauna and endofauna), a sub-set of 195 stations were selected including 135 stations sampled with an 0.25 m2 Hamon grab, 16 stations with a 0.1 m2 Van Veen grab, and 44 stations on hard sediment bottom using a Rallier du Baty dredge; the sieve mesh size was 2 mm (Foveau, 2009; Garcia, 2010). Other data collected in the Baie de Seine (Ghertsos, 2002; Lozach, 2011) and along the Côte d'Opale (Desroy et al., 2003) were also aggregated to compare the recent overview of benthos with the historic data from Cabioch's team (Carpentier et al., 2009). Temporal changes in the 23 most abundant taxa were analysed between the periods 1972–1976 and 1998–2007. Comparison between the historic and modern distribution of surface sediments showed that approximately half of the surveyed area underwent no change in sediment type, in particular in the pebbly

Please cite this article as: Dauvin, J.-C., History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description, J. Sea Res. (2014), http://dx.doi.org/10.1016/j.seares.2014.11.005

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zones (Foveau, 2009). More than one third of the surveyed area showed a fining of sediment grain size, being located mainly on either side of the Dover Strait in the more or less sub-tidal sand banks with medium grain sized sediment oriented parallel to the coast. The remaining surface corresponded to an increase in grain size which is mainly found in three areas: off the Baie de Veys, in bays on the English side of the EC with sandy–muddy sediments and in the North Sea near the Belgian border. Results obtained on the macrobenthic fauna (during the last period of sampling (2004–2007; 318 sampling stations — 875 species) could be compared with the data obtained by L. Cabioch and co-workers for the period 1971 – 1976; 1477 sampling stations — 630 species). In the present approach, the macrobenthic communities were studied separately for each period and then compared. It appeared at this large spatial scale of observation that the distribution of benthic communities is mainly governed by the sedimentary cover (N 55% of the stations remained in the same type of sediment over time). This was principally due to the hydrodynamic regime which had not changed significantly over the last three decades and which was the dominant factor controlling the structure and functioning of the benthic habitats in the EBEC. Foveau (2009) conducted a multivariate analysis and hierarchical classification taking account of several faunal categories, namely: vagile (motile) endofauna, sessile epifauna and total number of macrobenthic species (i.e. species richness). She used an optimal objective clustering method to identify assemblages (Ratkowsky, 1984), and she obtained respectively 17 assemblages for the first period of sampling (1971– 1976) and 64 other assemblages for the second period (2004–2007). This higher number of assemblages was mainly due to the sessile epifauna. Among the 64 assemblages only seven are sufficiently common at the local scale (i.e. over few km) to enable them to be represented as polygons on a habitat map. The other 57 groups were much more dispersed in their occurrence (with a maximum of only eight stations) so they can only be represented as point locations (rather than polygons) on a habitat map. This underlined the difficulties to identify and cartography macrobenthic habitats in the case of a large dataset within available statistical analyses which were sensitive to species with low occurrence and spatial location of stations. In her database, 32% of the species recorded were only observed at single stations, and 10% were only observed at two stations; so well over a third of the 875 species recorded were only present at one or two stations. A total of 25% of all species recorded were epifauna, and these were collected mainly at stations with gravel or pebble substrates. However, due to differences in the methodologies applied for each period (types of sampling gear, dredge and grabs, sorting of animals, expertise of researchers…), it was impossible to carry out a true comparison in the strict sense of the word. The results of benthic habitat mapping showed that four entities or communities were recurrent over time depending on the sediment type associations: 1) pebble and gravel community with sessile epifauna and O. fragilis; 2) coarse sand community with B. lanceolatum; 3) fine-to-medium clean sand community with O. borealis; and 4) muddy fine sand community with A. alba, which appeared to be permanent and showed little change over the three decades (Foveau, 2009). Nevertheless, the species richness shows a significant increase in the western area sampled in 1998–2007 (Foveau et al., 2013). The abundance levels are particularly high during both periods in the pebble community, with a very marked hot spot observed in the Dover Strait area (Carpentier et al., 2009; Foveau, 2009). Enhanced diversity is encountered in the EBEC (875 taxa), with high-diversity areas indicated by recent data mainly corresponding to gravelly and pebbly habitats (Foveau et al., 2013). This observation is consistent with previous analyses carried out on the 1972–1976 database (San Vicente-Añorve et al., 1996, 2002). The available quantitative data allows us to evaluate the functioning of the benthic systems (Garcia, 2010; Garcia et al., 2011). Thus, a steadystate trophic model can be used to assess the functioning of the three

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main benthic communities (i.e. gravel and pebbles, coarse sand and fine sand communities) in three sub-zones: the southern part of the North Sea, the Dover Strait and the Baie de Seine. This method leads to an estimation of the matter and energy fluxes within and between the units of the benthic system and allows an assessment of the amount of trophic energy stored in these units (available mostly to fish). The results show that, whatever the geographic area, the trophic structure is strongly linked to the sedimentary conditions. The third and last phase (2009–2012) of the CHARM project concerned the entire EC. As regards the benthic compartments, one of the actions involved the classification of marine habitats. This action aimed to produce a typology of the main habitats in the EC according to EUNIS classification, while taking into account oceanographic, sedimentary, macrobenthic and ichthyological patterns. Two main targets were defined in this action: 1) to pool together all the available quantitative sampling stations into a common British and French macrobenthic database (Fig. 4). All French sampling sites were sampled by 0.25 m2 Hamon or 0.1 m2 Van Veen grabs, while the British sampling was carried out either by 0.25 m2 Hamon grab, by 0.1 m2 Hamon grab or by 0.1 m2 Day grab (a few stations) (see Metcalfe et al., 2013), and 2) to improve our knowledge of poorly characterized benthic sampling areas in the middle part of the EC. Following a general trend in the study of benthic habitats and especially their mapping, the benthic sampling strategy has changed dramatically over the last decades. There has been a shift from the approaches used by Cabioch and Holme, which were based on dredge and grab sampling of sediments according to a more or less standardised distribution of stations in transects or forming a grid network (5′ latitude 5′ longitude for the French team), towards the use of acoustic remote sensing techniques, television and video observation systems, which allow the coverage of large areas. Before, Holme and Wilson (1985) used sonar and television to determine the benthic assemblages of the central EC to the south of the Isle of Wight. Subsequently, the CEFAS promoted this type of integrated approach on the English side of the Channel especially to study the pattern of mixed soft-hard bottoms (see Brown et al., 2002, 2004a,b, 2011). The ‘REseau BENthique’ (REBENT programme has also studied benthic habitats using several techniques around the Brittany coast, including sidescan sonar and grab sampling. Such approaches to assess the respective roles of physical and biological components have been commonly employed in most of the continental shelf of the World Ocean (see review of Brown et al., 2011). Following the generalisation of such complementary approaches for the observation and sampling of benthic habitats, and to address the second objective of the CHARM III phase, two VIDEOCHARM 2010 and 2011 surveys (2 × 10 days at sea) were carried out to acquire a better characterisation of habitats in the middle part of the EC. The study area corresponds to a transect across the EC (Fig. 4), and was designed in continuity with the CHARM II sampling grid with the aim of supplementing existing databases and complementing surveys on the English side of eastern EC (see Coggan and Diesing, 2011, 2012; Coggan et al., 2012; Diesing et al., 2009). During the surveys, benthic habitats were studied using acoustic remote sensing techniques, coupled with in situ sampling and small remotely operated vehicles (ROV). In fact, seven descriptors were defined: 1) side scan sonar with the interpretation of different acoustic responses to identify acoustic facies, 2) Hamon grab snapshot of collected sediment of all replicates; 3) endofauna identified and counted after sieving the sediment on a 2 mm mesh; 4) endofauna identified and counted after sieving the sediment on a 1 mm mesh; 5) epifauna identified but not counted; 6) sediment grain-size distribution and 7) video footage obtained with a small ROV (SeaBotix LBV 200 L). The preliminary available results show a progressive change in the residual tidal current velocities and the habitat structure from the western approaches towards the east. The diversity not only varies at the scale of a local study area depending on the sediment type and the presence

Please cite this article as: Dauvin, J.-C., History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description, J. Sea Res. (2014), http://dx.doi.org/10.1016/j.seares.2014.11.005

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Fig. 4. Location of quantitative benthic samples recorded or sampled during the INTERREG CHARM programme.

of pebbles or hard substrates, but also over the entire English Channel. The substrates and sediment characteristics are highly variable, showing a topographical heterogeneity, and this applies on diverse scales. It has been suggested that EUNIS habitat typology is updated to enable it to take account of such variation in bedforms, rather than relying on a single descriptor based purely on grain size distribution. First of all, a coding was developed for side-scan sonar images to incorporate seabed morphology descriptors (Table 1). For this purpose, different types of seabed morphology are distinguished in the observed acoustic images, in the observed acoustic images and classified according to the bedform typology published by Ashley (1990). So, it is suggested to add at the level 2 of the EUNIS classification, for the A4 (circalittoral rocks and

other substrata) A5 (sub-littoral sediment) additional information on the forms of the rocks and the presence of ribbon and dune bedforms (including dune wavelength), and to note evidence of anthropogenic activity (Table 1). It is worth noting that, unlike EUNIS, the seabed habitat classification used in North America, known as CMECS (Coastal and Marine Ecological Classification Standard) already takes into account such seabed morphology in a term it calls ‘Geoform’ (see Schumchenia and King, 2010). Therefore, since views of the benthic habitats were obtained at different scales according to the sampling gear used (ROV or grab), the biological data are processed with the different available descriptors to improve the coding of EUNIS habitats. The final step will be to cross-

Table 1 Suggestion to integrate the geomorphology to the EUNIS hierarchy at the level 2 of the EUNIS classification. Level 2 — EUNIS 1st code

2d code

3d code

A5 (sub-littoral sediments)

Hz (homogeneous zones) Rb (ribbons) Sd (small and medium dunes) Ld (large and very large dunes) Tr (table rocks) Mr (massive rocks)

– Wavelength (λ) of dunes in metres (λ) F (furrows) –

A4 (Circalittoral rocks and other hard substrata)

4th code Anthropogenic evidence Nt (Net or trawls marks) Wk (Wreck)

Please cite this article as: Dauvin, J.-C., History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description, J. Sea Res. (2014), http://dx.doi.org/10.1016/j.seares.2014.11.005

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check the EUNIS interpretations against the coding of seabed signatures and integrate these descriptions into benthic habitat typology. 7. Recent benthic studies on the English side Other research studies on the English side of the EC have been conducted over the two last decades (Rees et al., 1999). A survey of benthic communities in a heavily fished scallop ground was undertaken by Kaiser et al. (1998). Two main faunal assemblages associated with either gravelly sand sediments or sandy sediment were identified from samples obtained with fine-meshed scallop dredges. A third assemblage occurs in either sandy or gravelly muddy sand sediments. The highest abundance of scallops in both small and large size-classes is associated with the assemblage containing the highest species diversity as well as the highest abundances. This assemblage accounts for the highest concentrations of biomass, being composed of emergent fauna such as hydroids and the soft-coral Alcyonium digitatum. Several taxa (echinoderms, polychaetes, bivalves and crustaceans) decline immediately after trawling and are shown to have recovered six months later. Bolam et al. (2008) have described the spatial distribution of assemblages along the whole English side of the EC from grounds off Plymouth to the Dover Strait using a 0.1 m2 Hamon grab on 31 stations using the CEFAS vessel fitted with a dynamic global positioning system. In addition to grab samples, multibeam acoustic data have been obtained for each station. A total of 693 taxa (546 non-colonial and 147 colonial) was sampled, leading to the identification of seven assemblages: A) Echinocyamus/Nemertea; B) Verruca/Sabelleria spinulosa; C) Balanus/Spiophanes; D) Echinocyamus/Polycirus; E) Distomus/Balanus; F) Abra/Scalibregma and G) Nephtys–Bathyporeia. Bolam et al. (2008) stressed that the biological communities do not exhibit any E–W differentiation, even though their study includes a relatively low number of stations. Coggan et al (2012) reported that the distribution of sediment type and benthic communities was polarised around a distinctive local hydrodynamic feature in the centre of their sampling transect from 3° W to 3°E using a large dataset of samples in the vicinity of the Isle of Wight and the Cotentin Peninsula. They state clearly that ‘Sediments and communities at the eastern and western ends of the transect were more similar to each other than to those in the middle’. These authors identified four main biotopes (assemblages) along the transect: 1) a circalittoral Pomatoceros triqueter assemblage with barnacles and bryozoan crusts; 2) a circalittoral mixed sediment assemblage; 3) a circalittoral assemblage containing Flustra foliacea and Hydrallmania falcata and 4) O. fragilis and Ophiocomira nigra brittle-star beds on sub-littoral mixed sediment. Bolam et al. (2010) also estimated macrofauna production based on the benthic macrofauna on the English side of the EC. Similar to the CHARM approach, which is based on a comparison of benthic communities separated by several decades (Foveau, 2009), Capasso et al. (2010) utilised a historic benthic dataset and resurveyed an area west of Eddystone reef to the south of Plymouth to describe the current benthic community structure and investigate potential differences between 1895 and 2007. A total of 41 stations from six benthic grounds were re-surveyed in 2007 (36 original sites plus 5 added stations) with the same type of Naturalist's dredge as used by Allen in 1895 (sieving of 5 L of sediment on 5 and 1 mm mesh sizes). Echinoderm diversity shows a clear reduction between 1895 and 2007. Polychaetes, molluscs and crustaceans show a shift from large species to small species. Due to differences between the two surveys, and because a detailed description of the methodology for sorting the fauna was not available for the historic survey, Capasso et al. (2010) argued that some of the discrepancies highlighted in their study could stem from the possible application of different methodologies. In general, when species are small and inconspicuous, we can only draw tentative conclusions about increases in their abundance. This is because the greater precision in the sorting of dredged samples in 2007 might have led to a greater possibility of finding cryptic organisms. In the same vein Hinz et al.

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(2011) revisited 50 Holme’s stations located along the England coast and sampled in 1958-1959 then in 2006 and showed any clear broadscale distribution changes in benthic communities between these two periods. At a larger scale than the Eddystone reef, Foveau (2009) pointed out that the same situation applied to the two surveys from the EBEC. Therefore, such long-term temporal changes can only be analysed on large-sized taxa that have been collected and identified with the same accuracy during successive surveys. Such changes have also been revealed by modelling of the impact of biogeographical variations in the distribution of the benthic species in relation to climatic change (see Rombouts et al., 2012). R. Coggan and co-workers from the CEFAS have been very active in the field of habitat mapping using complementary methods to describe marine habitats in the framework of the EUNIS classification on the English side of the EC, especially in the middle part of the EBEC (Coggan and Diesing, 2011, 2012; Coggan et al., 2007; Coggan et al., 2011, 2012). For example, Coggan and Diesing (2011, 2012) and Diesing et al. (2009) identified a complex acoustic facies and three different geomorphological features in the central EC, i.e. flat smooth seabed, bedrock ridges and paleo-valley. These authors also observed sediment patches on the bedrock ridges corresponding to mixed gravel and rock habitats similar to those observed during the VIDEOCHARM campaigns. The EUNIS classification of marine habitats (EEA, 2006) was established as a result of the marine classification of habitats for Britain and Ireland (Connor et al., 2004), and was promoted in the MESH (2008) European INTERREG project, now continued in the MESHATLANTIC project as an extension for the southern European countries. During the MESHATLANTIC project, a synthesis was discussed concerning the possibility of using the EUNIS habitat classification for benthic mapping in European seas (Galparsoro et al., 2012). Some perspectives for the future development of the EUNIS classification were proposed in five points: 1) structure and hierarchy; 2) biology; 3) terminology, 4) mapping and 5) need to include new habitat classes in the present classification. Dauvin et al. (1994, 2008a,b) discussed the need for a clear and comparable terminology in benthic ecology, to facilitate application of the European Directives while bearing in mind the ecological concepts and the differences between French and English terminology. In addition, Coggan and Diesing (2011) also carried out a habitat mapping survey on an extensive area of the central EC using acoustic, photographic and traditional grab sampling techniques to produce full-coverage modelled maps for classifying biotopes according to the EUNIS habitat classification system. The previous interpretations of Holme and Cabioch for the central English Channel are entirely consistent with these new interpretations. Moreover, Coggan and Diesing (2011) have published the first modelled EUNIS map for the EC corresponding to EUNIS level 3 for rock habitats and EUNIS level 4 for soft bottom habitats, which is used by Metcalfe et al. (2013) to determine the benthic habitats for their conservation planning targets.

8. Conclusions and final recommendations The development of benthic mapping has taken place in the context of marine management and conservation faced with the intensification of human activities concerning a large part of the continental shelves of the North Atlantic (for example, see Schumchenia and King, 2010 for the Narragansett Bay in North America and Robinson et al., 2011 for the southern Irish Sea; see also http://seachmesh.net/). Modelling methods have also been enhanced to map the distribution of seabed biotopes in zones where survey data may be absent, such as in the case of the HABMAP project using a multi-parameter predictive tool to improve maps of the Irish Sea. Mapping habitats shows that, in many cases, the sea bed is characterized by a wide range of physical conditions (from hard to soft-bottom) and biological communities (Robinson et al., 2011). Moreover, when using predictive modelling, the distribution of seabed biotopes needs to be validated by experts because, in some

Please cite this article as: Dauvin, J.-C., History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description, J. Sea Res. (2014), http://dx.doi.org/10.1016/j.seares.2014.11.005

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Fig. 5. Map of cumulative human impact in the eastern part of the English Channel. From Comité Régional des Pêches de Basse Normandie, Daniel Lefèvre, personal communication.

cases such as the southern Irish Sea, the modelling process tends to overestimate the areal extent of biotope distributions. For the English Channel, the recent renewal of benthic mapping research has been spurred on by the increase of aggregate extraction zones, which require accurate descriptions of benthic habitats at small scales of observation (1–10 km2). The development of benthic mapping has also been favoured by the progress of European INTERREG programmes such as MESH (http://www.searchmesh.net/) and CHARM (http://www.charm-project.org/fr/), and also the implementation of Marine Protected Areas including, for example, the mapping of the French Natura 2000 sites (http://cartographie.aires-marines.fr/? q=node/43). While the EC is one of the seas in the world which is the most severely impacted by human activities (Fig. 5) (Halpern et al., 2008), it also represents a coastal marine zone covered by benthic data acquired over five decades at multiple spatio-temporal scales of observation. In particular due to the accumulation of data during the last two decades (1990–2010), we are now entering a new era of benthic research. Historically, the CEFAS and French collaborative teams (Roscoff, Dinard, Caen and Wimereux in association with the IFREMER) have played an important role in the development of benthic research, which has progressed from the mapping of benthic communities by dredge sampling with approximate vessel positioning in the 1960s to complementary geophysical and ecological methods to produce benthic maps using acoustic remote sensing techniques coupled with in situ sampling with precise DGPS, which have been used to describe a mosaic of benthic habitats. Moreover, the implementation of the Marine Strategy Framework Directive (MSFD-2008/56/EC) has stimulated the search for more effective indicators to assess the quality of European water bodies, and thus provides an opportunity to review the existing literature on the spatial distribution of benthic communities (see Rolet and Desroy, 2012). Furthermore, it is recommended that the future of seabed habitat mapping will benefit from a common approach, not only for the English Channel but also for other shallow seas on the continental shelves around the world. To support this, I propose the following outline that I call the ‘HABITAT’ approach. H, first step: Have a scientific objective to prospect and map the benthic sea bed. As a result of the development of new approaches of

observation of the sea bed, i.e. multi-beam, side-scan, ROV, video and GPS, and the need to evaluate the impact of human activities in coastal zones, there has been an increase in the number of surveys and descriptions of the marine environment. At the scale of the English Channel (EC), only some parts of the sea bed have been surveyed, mainly in shallow waters on the French side (Brittany coast, Normandy–Brittany Gulf, Cherbourg harbour, Bay of Seine and Opal coast), along the English side (Isle of Wight, eastern basin of the EC, see Brown et al., 2002, 2004a, b) and in the Central part of the EC (Coggan and Diesing, 2011, 2012; James et al., 2007, 2010, 2011). Moreover, it appears necessary to adapt the sampling and observation protocol to the objectives of the studies. For example, it is unnecessary to have precise morphological data to identify the general distribution of a species at the scale of the whole English Channel; on the contrary, this technique is indispensable before the emplacement of piles for wind farms. As is often the case in research, difficulties arise in adapting a suitable scale of observation to the spatial patterns when classifying benthic habitats. Therefore, describing the benthic habitat at levels 3 or 4 of the EUNIS classification demands less sampling effort than obtaining descriptions at levels 5 or 6, which require expertise in faunal taxonomy. Table 2 sets out technical recommendations according to the scale of observations in accordance with the EUNIS level of habitat classification. A, second step: Adapt the sampling protocol and observations to the scientific objective. The sampling process corresponds to the collection of discrete observations, which must be compatible with the time available for sorting and identifying the recorded species (number of replicates) and is not based on the monitoring of benthic environment maps representing the best estimate of habitat distribution at a given moment, by making the best use of the knowledge available at that time (http://www.seachmesh.net/). A top-down approach, as used in the case of the VIDEOCHARM campaigns (e.g. acoustic surveys followed by bottom sampling, as in Narragansett Bay; Schumchenia and King, 2010), allow us to characterize acoustic facies. This leads to the definition of a limited number of sampling stations in each backscatter zone, which then enables the identification of biotic assemblages. The bottom-up approach is to establish a priori relationships between abiotic and biotic variables, and then use these to describe and delineate the habitat map units. Assemblages are examined based on biological similarity. This approach is typically more resource-intensive and less rapid than the top-down method.

Please cite this article as: Dauvin, J.-C., History of benthic research in the English Channel: From general patterns of communities to habitat mosaic description, J. Sea Res. (2014), http://dx.doi.org/10.1016/j.seares.2014.11.005

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Table 2 Scale of observation and recommendation for habitat resolution following the EUNIS classification for the English Channel benthic studies. EUNIS classification

Scale of observation

Technical recommendations

Level 1 — marine habitats Level 2 — substratum, depth and light Level 3 — exposure, sediment characteristics Level 4 — biology for hard substratum Depth for sub-littoral sediment Level 5 — biology Level 6 — biology

– Large Large Medium

– Side-scan sonar and dredges Side-scan sonar, dredges, shipek grab for sediment sampling Grabs and dredges, video for hard bottom, identification of epifauna and megafauna Grabs, video, trawl for megafauna, identification of taxa Grabs, video and photography, identification of species

Medium to small Small

B, third step: Build a data set including abiotic and biotic data. For biotic data, this approach requires the identification of macroflora and macrofauna, which is often a long and fastidious task demanding robust expertise, thus incurring costs to establish long lists of identified species. To reduce the time-cost, the use of taxonomy sufficiency can be appropriate to reduce the errors of identification, without losing significant information useful for identification of assemblages by statistical analysis (Dauvin, 2005). The approach consists of establishing a stations × species matrix which can be later analysed by statistical methods. I, fourth step: Interpret the assemblages. As noted by numerous authors (see Carpentier, 1999; Foveau, 2009; San Vicente-Añorve, 1995), the available multivariate statistical analysis techniques for identifying benthic assemblages are currently sensitive to the number of available sampling stations and the number of rare species, which tend to be very abundant in benthic collections. Such analyses on a large dataset generate numerous clusters that are difficult to interpret, requiring professional expertise to validate the most effective assemblage clusters to be used for identifying benthic communities (Foveau, 2009). In the future, appropriate statistical methods will be used to analyse all the available quantitative data on benthic samples at the scale of the entire EC recorded during the INTERREG CHARM project. These methods should be developed during a Franco-British collaborative project over the next few years to improve the classification of marine habitats at EUNIS levels 4 and 5. T, fifth step: Trace the limits of the habitats. This phase requires integrating the results of assemblage clustering and the mapping of available abiotic environmental variables, i.e. acoustic facies and sediment analyses to define the limits of the benthic habitats. There is always some subjectivity involved in the interpretation by the expert of the limit between two benthic habitats (more or less abrupt limits between two benthic communities or continuum between two separate entities). A, sixth step: Adopt a Marine Habitat classification (see Harris, 2012 for a review of the existing marine habitat classifications). For European coastal seas, there is an consensus of the European scientific community to use and extend the EUNIS classification of marine habitats which also justifies further collaboration at the scale of the North-eastern European seas (see Galparsoro et al., 2012). The EUNIS classification follows the biotope classification proposed in the 1990s in the framework to the BIOMARE project. During the same period, a typology called ZNIEFF (‘Zones Naturelles d'Intérêt Ecologiques Floristiques et Faunistiques’) was proposed on the French side (Dauvin et al., 1994, 2008a, b). Nevertheless, the benthic habitats of the Natura 2000 sites follow the Habitats Directive, which is poorly adapted for marine habitats (Dauvin et al., 2008a, b). As suggested by Galparsoro et al. (2012), there are the need to enrich the EUNIS habitat classification especially for levels 5 and 6. The mosaic of habitats observed in the central part of the EC corresponds to the high variability of abiotic conditions, and the existence of a mixed soft-bottom (gravelly and coarse sand) in hard bottom zones (Coggan and Diesing, 2011, 2012, and observed during the VIDEOCHARM campaigns: unpublished data) suggests that this specific habitat should be added to the classification. We also suggest integrating the geomorphology into the hierarchy at Level 2 of the EUNIS classification (Table 1).

T, seventh and last step: Trace and produce a map of benthic habitats. This is the last and final result of the HABITAT approach representing the different benthic habitat surfaces. The map of benthic habitats will serve later as a tool for the users and managers to develop activities such as aggregate extraction, implementation of Renewable Marine Energies (wind farms and tidal turbines) and protect marine areas (Delavenne, 2012; Delavenne et al., 2012). The generalisation and application of Geographic Information Systems allow us to draw up maps of benthic communities from a marine area using different scales of representation, from some km2 up to the whole English Channel, as proposed by Coggan and Diesing (2011), for the EUNIS classification levels 3 and 4, which is now a benchmark for this area.

Acknowledgements This study was carried out under the INTERREG IV A France (Channel)–England cross-border European cooperation programme, co-financed by the European Regional Development Fund as part of the CHannel integrated Approach for marine Resource Management (CHARM) Phase 3 project. It was presented as an invited oral communication during the MeshAtlantic Conference ‘Mapping Atlantic Seabed Habitats Area for a Better Marine Management’ at the University of Aveiro (Portugal) on 15–17 September 2013. I thank Jacques Populus, IFREMER, who provided financial support for participation at the conference, and the team of Victor Quintino of the Aveiro University for the meeting organisation. I also thank the crews of RV Côtes de la Manche, as well as all the scientists and students who helped during the cruises and CHARM benthic studies. I wish to thank M.S.N. Carpenter for correcting the English grammar, syntax and style, as well as Alexandrine Baffreau and Jean-Philippe Pezy for drafting the figures and Daniel Lefèvre for the map of cumulative human impact in the Eastern part of the English Channel. Finally; I thank the three reviewers for their very useful remarks and suggestions which greatly improved the first and second versions of this paper. References Alizier, S., 2011. Echelles spatio-temporelles d'observation des relations macrobenthos/ sédiments: organisation et changements à long-terme (1988–2009) des communautés benthiques subtidales de la partie orientale de la baie de Seine. Université de Lille 1, France (PhD Thesis). Arnal, O., Augris, C., Delpech, J.P., 1985. Recherche de sites pour l'extraction de granulats marins dans le Nord-Pas-de-Calais. Rapport IFREMER, Région Nord-Pas-de-Calais (104 pp.). Ashley, G.M., 1990. Classification of large-scale subaqueous bedforms: a new look at an old problem. J. Sediment. Petrol. 60, 160–172. Barnay, A.S., 2003. Structure des peuplements de sables fins plus ou moins envasés en Manche: échelles spatiales et biodiversité. (PhD Thesis), Université Pierre & Marie Curie (Paris VI) (250 pp.). Birchenough, S.N.R., Boyd, S.I.E., Vanstaen, K., Coggan, R.A., David, S., Limpenny, D.S., 2010. Mapping an aggregate extraction site off the Eastern English Channel: a methodology in support of monitoring and management. Estuar. Coast. Shelf Sci. 87, 420–430. Bolam, S.G., Eggleton, J., Smith, R., Mason, C., Vanstaen, K., Rees, H.L., 2008. Spatial distribution of macrobenthic assemblages along the English Channel. J. Mar. Biol. Assoc. U. K. 88, 675–687. Bolam, S.G., Barrio-Frojan, C.R.S., Eggleton, J.D., 2010. Macrofauna production along the UK continental shelf. J. Sea Res. 64, 166–179. Bourgain, J.L., Dewez, S., Beck, C., Richard, A., 1985. Effets des rejets de vases portuaires sur les sédiments et les peuplements benthiques au large de Boulogne. Actes du

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