Vol. 4: 11 - 37, 2011

Journal of Oceanography, Research and Data

Census and analysis of zooplankton metadata of the French coasts since 1955 RAYBAUD V.1,2,*, HEROIN D.3,4, RAUD T.5,6,7, BRYLINSKI J-M.5,6,7, STEMMANN L.1,2, THIBAULT-BOTHA D.8, SAUTOUR B.3,4 1)

UPMC Université Paris 6, UMR 7093, Laboratoire d'Océanographie de Villefranche, Observatoire Océanologique de Villefranche-sur-Mer, F-06230 Villefranche-sur-Mer, France 2) CNRS, UMR 7093, LOV, Laboratoire d'Océanographie de Villefranche, Observatoire Océanologique de Villefranche-sur-Mer, F-06230 Villefranche-sur-Mer, France 3) Université Bordeaux 1, UMR 5805, EPOC, Station Marine d'Arcachon, 2 rue du Professeur Jolyet, F-33120 Arcachon, France 4) CNRS, UMR 5805, EPOC, Station Marine d'Arcachon, 2 rue du Professeur Jolyet, F-33120 Arcachon, France 5) Université Lille Nord de France, F-59000 Lille, France 6) Université du Littoral Côte d’Opale, ULCO, LOG, Laboratoire d’Océanologie et de Géosciences, 32 Avenue Foch, F-62930 Wimereux, France. 7) CNRS UMR 8187, F-62930 Wimereux, France 8) Université de la Méditerranée, UMR 6535, Laboratoire d’Océanographie Physique et Biogéochimique, Centre d’Océanologie de Marseille, Campus de Luminy, Case 901, 13288 Marseille, France *Corresponding author: [email protected] _________________________________________________________________________ ABSTRACT: In the framework of the Marine Strategy Framework Directive (MSFD), and for the first time, a census and analysis of the available metadata on zooplankton along the French coasts have been conducted (for both long-term time series and short-term oceanographic cruises). This study provided a comprehensive examination of zooplankton within the French metropolitan coastal system, i.e., the North Sea, the English Channel, the Atlantic Ocean and the Mediterranean Sea. The investigation revealed a wide disparity in the spatial distribution of studies, highlighting some wellsampled areas as well as other regions quite unexplored. In addition, this approach also exposed the heterogeneity in zooplankton sampling methods and taxonomic determination levels. The wide variety of sampling methods defined the whole zooplankton community, from the smallest fauna (such as crustacean nauplii) to the largest (such as euphausiids) to the most delicate (gelatinous forms). Unfortunately, the possibilities for cross-analysis of 11

Zooplankton meta-data census the different data are limited. This paper presents a preliminary analysis of the data available for meta-analysis (in term of sampling method and taxonomic determination). In order to understand current and future environmental fluctuations (climate change, ocean acidification, anthropogenic pollution and persistent overfishing), it is essential to identify and analyze all the biological data collected in the different French marine areas. This indispensable first step is crucial for defining the environmental status of marine waters. The nexus of our results provides recommendations for a standardization of procedures to be followed in subsequent studies of zooplankton, specifically sampling strategies, sampling methods and taxonomic determinations. KEY WORDS: Marine Strategy Framework Directive, Zooplankton, French coasts, Environmental status, Census, Monitoring. ACONYMS: MSFD: Marine Strategy Framework Directive (in French, DCSMM) DCSMM: Directive-Cadre Stratégie pour le Milieu Marin NCB: North sea, English Channel and west coasts of Brittany BBI: Bay of Biscay and Iberian coasts WMS: Western Mediterranean Sea SOMLIT: Service Observation en Milieu LITtoral ESA: Environmentally Sensitive Area ________________________________________________________________________

Introduction The mandate of the Marine Strategy Framework Directive (MSFD), a European directive, is to establish a framework for community action in the field of marine environmental policy (European Commission, 2008). The main objectives are to define the characteristics of water masses and maintain a Good Environmental Status (GEnS), although the definition and interpretation of GEnS remains a source of debate (Mee et al., 2008; European Commission, 2010). The implementation of the MSFD requires the application of an ecosystem-based approach to the management of human activities. The European Water Framework Directive was established in 2000 (WFD; European Commission, 2000) with a spatial application restricted to the littoral area (i.e., 1 nautical mile from the coastline). The MSFD encompasses the coastal 200 nm area, a region currently implemented in other countries of the European Union (Borga et al., 2010 and 2011) and applied in several disciplines of marine science, i.e., fisheries (Rätz et al., 2010), eutrophication (Ferreira et al., 2011), contaminant monitoring (Zaldivar et al., 2011), benthic organisms studies (Van Hoey et al., 2010) and pelagic zooplankton populations (this study). The initial evaluation of French marine waters is coordinated by IFREMER (Institut Français de Recherche pour l’Exploitation de la MER) under the aegis of the Ministry of Ecology. In order to understand current and future environmental changes (climate change, ocean acidification, anthropogenic pollution and persistent overfishing), it 12

Raybaud et al. (2011) JORD 4: 11 - 37 is essential to assemble all available biological data within the French coastal system, i.e., the North Sea, the English Channel, the Atlantic Ocean and the Mediterranean Sea, and to define common sampling strategies and analysis. This information will be analyzed to determine common parameters that define the environmental status of the marine waters. Zooplankton species are major components of pelagic food webs. They control carbon production through predation on microplankton (phyto- and microzoo-plankton) and export organic matter to depth through sinking of mucus (Robison et al. 2005), carcasses (Turner, 2002), faecal pellets (Fowler and Knauer, 1986) and via diel vertical migrations (Longhurst, 1989; Raybaud et al., 2008). As food for upper trophic levels, mesozooplankton can also affect the growth of commercially exploited fish populations (Beaugrand et al., 2003) as well as the development of gelatinous predators (Richardson et al., 2009). In addition, it has been shown that zooplankton could be used as an indicator of the impact of global change (Beaugrand et al., 2002). This study constructed the first comprehensive metadataset on zooplankton within the French coastal zone. The abundance and specific composition of zooplankton are classically well documented. However, a wide disparity of sampling/counting methods have been used and the temporal/spatial distribution of the studies varies greatly. The present study describes a preliminary analysis of the nature of the data potentially usable to define an initial ecological state. Moreover, only samples collected with plankton nets, bottles and pumps were considered. Datasets based on automatic systems such as the Continuous Plankton Recorder, or acoustic and optical sensors, as well as those collected from submersibles equipped with cameras have been scarcely used in our areas of concern and were not taken into account. The spatio-temporal evolution of the location of the sampling site during the past 60 years is described and environmentally sensitive areas for zooplankton monitoring in each marine sub-region are identified. In the conclusion, we propose standardized sampling strategies and analysis as well as the taxonomic level of the determination for zooplankton taxa.

Material and methods All classical databases on zooplankton are working on the same principle: every author must complete a form for each set of data. This procedure is the principal reason why not a single zooplankton database is really comprehensive. In our study, we selected a different approach. We assemble a list of potential sources of zooplankton datasets and then each person or organization was contacted individually to discuss this new marine environmental policy. We collected metadata on each of the survey that was available. In parallel, we obtained metadata from the literature (publications, PhD theses), especially for studies for which authors could not be contacted. For each zooplankton sample, the metadata provided included: name of the author(s) and its (their) affiliation(s), source of funding, name and location of the sampling site (latitude, longitude), sampling date, objectives of the project, type of cruise (spatial and/or temporal study), depth of collection of the sample, sampling method (bottle, pump or net and mesh-size), available 13

Zooplankton meta-data census environmental parameters, zooplankton variables measured (biomass, biovolume, abundance and/or size-spectrum), level of the taxonomic determination and format of archive if available. The working approach used in the MSFD was to consider the marine sub-regions in each country. The mainland French coasts are therefore divided into four sub-regions: -

“North Sea and English Channel” sub-region “West Coasts of Brittany” sub-region “Bay of Biscay and Iberian coasts” sub-region “Western Mediterranean Sea” sub-region

Due to a low number of datasets, the “West Coasts of Brittany” was combined with the “North Sea and English Channel” to form the sub-region “North Sea, English Channel and west coasts of Brittany”. Each map presented here has been built using ArcGIS. Operational sub-regions used in this paper are: “North sea, English Channel and west coasts of Brittany” : NCB “Bay of Biscay and Iberian coasts”: BBI “Western Mediterranean Sea”: WMS

Results General overview of zooplankton studies collected along the French coasts The census of zooplankton studies performed in the metropolitan French waters since 1955 consists of 319 data sets, involving 60930 samples (Table 1). The listed zooplankton metadata were derived from 147 authors and co-authors (Appendix 1). Table 1: The zooplankton metadata census. NCB = North Sea, English Channel and West coasts of Brittany; BBI = Bay of Biscay and Iberian coasts; WMS = Western Mediterranean Sea. NCB

BBI

WMS

TOTAL

13145

28449

19336

60930

Number of data sets

77

145

97

319

Number of identified authors

54

38

84

176*

Number of samples listed

Number of contacted authors

19

17

30

66

Percentage of returned forms

84%

94%

77%

83%

Percentage of authors not wishing to participate

16%

6%

23%

17%

* The total of “Number of identified authors” differs from the total number of authors (147; see the complete list in Appendix) because some authors are working in several sub-regions.

Figure 1 gives the location of all zooplankton sampling stations.

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Raybaud et al. (2011) JORD 4: 11 - 37

Figure 1: Spatial distribution of all zooplankton samples collected on the metropolitan French coasts since 1955. A high definition figure is presented in supplementary files. (Data sources: CNRS, IFREMER, IRD, Parc naturel marin d’Iroise, Universities: Littoral Côte d’Opale, Lille1, Paris 6, Bordeaux, La Rochelle, Méditerranée, Toulon-Var, Liège, Montpellier).

15

Zooplankton meta-data census In the NCB sub-region, there is a strong heterogeneity in the spatial coverage (Fig. 1), with a great number of stations in the coastal waters from the Bay of Seine to the Belgian border, in the Bay of “Mont Saint Michel”, in the North of Brittany and in the Iroise Sea. Relatively few samples were collected around the Cotentin peninsula. On the western coast of Brittany, the majority of samples were obtained near the coast: the offshore area is quite unexplored. Four permanent long-term monitoring programs have been conducted near nuclear power plants since the 1970s (Gravelines, Penly, Paluel and Flamanville). A fifth program was initiated off Wimereux in 1996 in the framework of the SOMLIT network (Goberville et al, 2010). In the BBI sub-region, the number of samples is very large in coastal waters especially in the south of the Gironde’s plume. Sampling is more dispersed past the continental shelf. There are currently seven permanent long-term monitoring stations; all of them are littoral. The time series in the Gironde estuary is the oldest, beginning in 1978, with the implementation of the Blayais nuclear power plant (David et al, 2005, 2006, 2007). Six of these permanent stations belong to the SOMLIT network. In the WMS sub-region, the spatial distribution of zooplankton samples also shows a large heterogeneity (Fig. 1). Some areas, like the Ligurian Sea and the Gulf of Lion, have been studied intensively, while no sampling has been conducted in central and southern sub-region. The sites that appear to be located "on land" correspond to sampling performed in coastal lagoons. There are now six permanent long-term monitoring stations: five coastal stations and one offshore station (DYFAMED site, in the central part of the Ligurian Sea). The time series at Villefranche-sur-Mer is the oldest, beginning in 1966 (Molinero et al., 2005). The series at Toulon (Great and Little Bay) began in 1995 (Jamet et al., 2005), followed in 2001 by DYFAMED, by Marseille in 2002 (Riandey, 2005) and finally by Calvi in 2003 (Frangoulis et al., 2011). However, two long-term time series at the Bay of Banyuls-sur-Mer and Toulon-Niel sites were discontinued due to lack of human resources.

Zooplankton sampling methods Zooplankton sampling methods have varied (Harris et al., 2000). The choice of the tools and mesh sizes depends on the scientific objectives of the studies. Most samples were collected by nets, pumps and/or bottles. Acoustic and optical devices are used less frequently; these methods are not shown in figures 2 and 3. In the NCB sub-region, more than 60.7% of the samples were collected with plankton nets (15.1% with pumps and 24.2% with bottles). "WP2 type" nets were mostly used (52% of samples; Fig. 2). This type of net with a 200 µm mesh size (40.3%) allows effective mesozooplankton sampling (UNESCO, 1968). Samples collected with mesh size less than 200 µm (80 and 63 µm) were deployed in the Seine estuary (25.9%; Fig. 2 and Fig.3). Nets with mesh size larger than 200 µm targeted large copepods, euphausiids or gelatinous zooplankton in the Celtic Sea region. In the BBI sub-region, the majority of samples were collected with plankton nets (97%; Fig 2) and pumps. 200 µm WP2 net were mainly used (60% of the samples), followed by Hensen and Pairovet nets. Only 19.7% of the sampling was conducted with nets of smaller mesh size (< 200 µm), specifically 12 transects from the bay of Marennes16

Raybaud et al. (2011) JORD 4: 11 - 37 Oléron to the Adour River plume; Gironde; Audierne and Arcachon bays; Fig. 3) (Zarauz et al., 2008). The use of larger mesh-size nets (> 200 µm) was dedicated to samplings performed off the continental shelf to study the larvae and eggs of mackerel, chaetognaths, siphonophores, medusae, salps and doliolids (Arbault & Lacroix, 1977; Beaudouin, 1971)

Figure 2: Ratio of the different tools used to sample zooplankton (A) in the “North Sea, English Channel and West Coasts of Brittany” sub-region (NCB), (B) in the “Bay of Biscay and Iberian coasts” sub-region (BBI), (C) in the “Western Mediterranean Sea” sub-region (WMS).

In the WMS sub-region, the spatial distribution of the sampling methods clearly shows the dominance of the use of plankton nets (99.8% of the samples; Fig. 2 and Fig 3). However, the number of different types of nets deployed is much higher (> 17) than in the other sub-regions. In most cases (52.7%), the nets had a mesh size larger than 200 µm. In the Ligurian Sea and the Gulf of Lion only a few samples (16.5%) were collected with mesh size lower than 200 µm. In comparison with the other sub-regions, a 200 µm WP2 net was only used in 25.1% of the studies (40.7% in NCB and 60% in BBI). It could be explained by e greater number of studies focusing on macrozooplankton in the WMS than in other sub-regions (Braconnot, 1971; Sardou et Andersen, 1993; Labat & Cuzin-Roudy, 17

Zooplankton meta-data census 1996; Sardou et al., 1996; Andersen et al., 1998; Andersen et al., 2001a et 2001b; Raybaud et al., 2009). Nets with mesh size higher than 200 µm were deployed predominantly in the Ligurian Sea and around Corsica. The selection of se larger mesh sizes seems to be spreading within the Gulf of Lion in response to the increasing number of studies that focus on sampling the gelatinous zooplankton.

Figure 3: Spatial distribution of the sampling tools and mesh-sizes used. A high definition figure is presented in supplementary files. (Data sources: CNRS, IFREMER, IRD, Parc naturel marin d’Iroise, Universities: Littoral Côte d’Opale, Lille1, Paris 6, Bordeaux, La Rochelle, Méditerranée, Toulon-Var, Liège, Montpellier).

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Additional environmental data Measurements of temperature and salinity (Fig 4) were conducted at most (>95%) of the study sites. Phytoplankton measurements, often in terms of Chlorophyll a, were made at 60% of the locations. Meteorology, nutrients concentration, and Suspended Matter (SM), data were less frequently obtained. In the Mediterranean Sea, zooplankton data were most often accompanied by meteorological records and nutrients data. Suspended Matter was often measured in NCB and BBI sub-regions but rarely determined in the WMS.

Figure 4: Percentage of samples collected in French sub-regions with meteorological and environmental parameters. Hydro = temperature and salinity, Phyto = phytoplankton, SM = Suspended Matter, NCB = “North Sea, English Channel and West Coasts of Brittany” sub-region, BBI = “Bay of Biscay and Iberian coasts” sub-region, WMS = “Western Mediterranean Sea” sub-region.

Level of zooplankton analysis All studies involving zooplankton are quite heterogeneous. The sampling methods were highly disparate. Furthermore, the method and level of zooplankton analyses differed from one investigation to another (Fig 5). Some studies quantified zooplankton only as dry weight or total biovolume. When taxonomic determinations were made, we distinguish between the studies where the whole community was identified and those where the focus was limited to particular groups, e.g., copepods (Gaudy, 1962), euphausiids (Labat & Cuzin-Roudy, 1996), decapods, mysidacea (David, 2006), polychaetes and echinoderms larvae (Lagadeuc & Brylinski, 1987; Pedrotti & Fenaux, 1992; Ayata et al., 2009), siphonophores (Buecher, 1999), salps (Gorsky et al., 1991) and ichthyoplankton (Grioche, 1998). Taxonomic determination to the species level is a long and tedious process. In the sub-region BBI, whole community determinations were common (Fig 5). In the NCB subregion, taxonomic determination was generally limited to a few groups. In the WMS subregion, the ratio between the two approaches was roughly equivalent. The spatial distribution of the samples with the level of analysis for each of them is shown for each sub-region (supplementary figures 3, 4 and 5). 19

Zooplankton meta-data census

Figure 5: Different levels of zooplankton studies. NCB: “North Sea, English Channel and West Coasts of Brittany” sub-region; BBI: “Bay of Biscay and Iberian coasts” sub-region; WMS: “Western Mediterranean Sea” sub-region. For each subregion, this histogram presents the ratio of studies without any taxonomic determination, the ratio with taxonomic determination limited to a few groups and the ratio of studies with determination of the whole community.

Temporal evolution of the samplings Temporal variation in the number of zooplankton samples collected on a yearly basis, within each sub-region, revealed different patterns (Fig 6). The number of samples collected in the NCB sub-region before 1974 is low (< 200 samples per year), in comparison with the other regions. Between 1974 and 1985, the majority of samples were collected for long-term monitoring in the vicinity of nuclear power plants. In the following decade, the number of oceanographic cruises increased but collapsed again between 1998 and 2001. Since 2002, the number of samples per year was extremely variable (between 23 and 1418 samples per year). The BBI sub-region has been the most studied area for zooplankton. The number of samples collected each year was usually greater than 300 and much more regular than in the NCB sub-region. Apart from a study that was conducted in 1955 (Reyssac, 1971), zooplankton sampling began in 1964. In 1978, a long-term monitoring started in the vicinity of the nuclear power plant “Le Blayais”, with over 150 samples per year (Quintin et al., 2008). Between 1978 and 1996, the number of recorded samples was nearly constant with about 200 samples.y-1 collected in the framework of long-term monitoring and 400 samples.y-1 collected during cruises. Since 1997, the number of samples increased substantially (with a maximum of 1648 samples.y-1 in 2003). The frequency of samples collected per year in the WMS sub-region is intermediate between the NCB and the BBI sub-regions. Two main periods were distinguished, with a number of samples largely above the mean: 1960-1970 and 1982-1995. Long-term monitoring began in 1966, with the implementation of the “Point B” sampling station in the bay of Villefranche-sur-Mer (Molinero et al., 2005; Garcia-Comas et al., 2011). The total number of samples acquired in the framework of long-term time series regularly increased since this year, but never exceeded 200 samples.y-1. Before 1996, the majority of the samplings was done during single cruises. Since 1996, most samples have been collected in the framework of long-term monitoring.

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Raybaud et al. (2011) JORD 4: 11 - 37

Figure 6: Temporal variations of the number of samples collected each year since 1955, (A) in the “North Sea, English Channel and West Coasts of Brittany” sub-region (NCB), (B) in the “Bay of Biscay and Iberian coasts” sub-region (BBI), (C) in the “Western Mediterranean Sea” sub-region (WMS).

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Zooplankton meta-data census

Spatial evolution of the samplings Since 1955, zooplankton sampling coverage in the NCB sub-region appears to be heterogeneous (Fig. 7). Before 1970, samples were essentially collected in the Celtic Sea (Le Fèvre & Grall, 1970). The coverage was extended, between 1970 and 1979, to a larger scale and long-term monitoring began in the vicinity of the nuclear power plants of Gravelines, Penly, Paluel and Flamanville. During the 1980’s, samples were mainly collected in the bay of Seine and in the bay of the Mont St Michel, while in the 1990’s, sampling focused northward between the bay of Seine and the Southern bight of the North Sea.

Figure 7: Spatial distribution of all zooplankton samples collected in the “North sea, English Channel and west coasts of Brittany“(NCB) sub-region per decades. (A) Before 1970 (our census begins in 1955); (B) between 1970 and 1979; (C) between 1980 and 1989; (D) between 1990 and 1999; (E) Since 2000. More detailed figures are presented in supplementary files. (Data sources: CNRS, IFREMER, IRD, Parc naturel marin d’Iroise, Universities: Littoral Côte d’Opale, Lille1, Paris 6, Bordeaux).

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Raybaud et al. (2011) JORD 4: 11 - 37

Figure 8: Spatial distribution of all zooplankton samples collected in the “Bay of Biscay and Iberian coasts” (BBI) sub-region per decades. (A) Before 1970 (our census begins in 1955); (B) between 1970 and 1979; (C) between 1980 and 1989; (D) between 1990 and 1999; (E) Since 2000. A high definition figure is presented in supplementary files. (Data sources: CNRS, IFREMER, Universities: Paris 6, Bordeaux, La Rochelle).

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Zooplankton meta-data census

Figure 9: Spatial distribution of all zooplankton samples collected in the Western Mediterranean Sea (WMS) sub-region per decades. (A) Before 1970 (our census begins in 1955); (B) between 1970 and 1979; (C) between 1980 and 1989; (D) between 1990 and 1999; (E) Since 2000. A high definition figure is presented in supplementary files. (Data sources: CNRS, IFREMER, IRD, Parc naturel marin d’Iroise, Universities: Paris 6, Méditerranée, Toulon-Var, Liège, Montpellier).

In BBI sub-region, the first survey was conducted in 1955 (Reyssac, 1971) but the sampling effort remained limited to the Bay of Biscay until 1970 (Arbault & Lacroix, 1977). During this period, the majority of the samples was collected over the continental 24

Raybaud et al. (2011) JORD 4: 11 - 37 shelf and studies conducted offshore remained scarce. In the following decade, the spatial coverage of zooplankton samples decreased, even over the continental shelf. This trend continued during the next decade (1980-1989), where only the northern part of the subregion and Arcachon Bay were sampled. In the 1990’s, studies moved to the southern part of BBI sub-region. Since 2000, the number of samplings increased but remained located over the continental shelf. The southern part of the sub-region has been the most studied area. Concerning WMS sub-region, the studies performed before 1970 include 13 years of data. During this period, the samples are numerous and their spatial distribution was fairly uniform over the entire sub-region, except for the southern part of the area (below 41°N) which remained unexplored. These samples were mainly collected during cruises with the research vessels Jean-Charcot, Catherine Laurence, President-Theodore-Tissier and Korotneff. During the 1970s, lack of interest in zooplankton is obvious with very few cruises organized. During the 1980s, the sampling effort was high, but mainly limited to the Ligurian Sea (MEGLIG, PROLIG2, TROPHOS2 and FRONTAL programs). In the 1990s, most cruises were conducted in the Gulf of Lion (EUROMARGE, MOOGLI, PANACHE-RHONE, PELAGO-BERRE) and in the Ligurian Sea (BIOMED, VALCAN, DYNAPROC, MIGZOO, DISCO, MEG2). The central and southern parts of the subregion remained neglected and unexplored. Since 2000, spatial samplings focused mainly on the Gulf of Lion (COSTAS and GELAMED programs). The central and southern parts of the WMS sub-region remain unexplored. In the Ligurian Sea, the majority of samples collected since 2000 have been collected with the objective to study the temporal variation of zooplankton at a fixed point, both during the oceanographic cruises (Raybaud et al., 2008) and for long-term monitoring (Molinero et al., 2005; Garcia-Comas et al., 2011).

Discussion Zooplankton along the French coast have been intensively studied, although most studies were often limited in time or focused only on specific taxa. Nevertheless, Environmentally Sensitive Areas (ESA) can be recognized in each sub-region.

“North Sea, English Channel and west coasts of Brittany” sub-region (NCB) In the NCB sub-region, several ESA can be identified in the North Sea and English Channel: the bay of “Mont St Michel”, the "coastal river" and its frontal area and, more generally, the offshore waters in the Channel and the Southern bay of the North Sea. 1- Bay of “Mont St Michel”: This bay (Fig.10-1) is characterized by a shallow depth, a macrotidal regime and complex patterns of currents as well as an intensive shellfish farming program. In this habitat the gastropod Crepidula fornicata controls the primary production and its pelagic larvae are dispersed by the currents for about one month. These larvae compete for trophic resources with the cultivated species (Cugier et al., 2010). The entire “Normano-Breton”

25

Zooplankton meta-data census Gulf has been characterized as a hydrodynamic retention phenomenon (Salomon et al., 1993). Future research should be devoted to its influence on the zooplankton communities.

Figure 10: Location of the Environmentally Sensitive Areas (ESA) in each sub-region. See text for ESA numbers.

2- The Seine estuary: This estuary, like most estuaries, is a highly productive ecosystem (Fig.10-2). High abundances of zooplankton have been observed in this area, making it an ideal nursery for the development of the larval and juvenile stages of crustaceans and fishes (Morin et al., 2010). 3- The frontal zone and the "coastal river" in the Eastern Channel: The phytoplankton production generated offshore of the Somme estuary flows northward and along the coast to the Strait of Dover. Abundance of zooplankton is very 26

Raybaud et al. (2011) JORD 4: 11 - 37 high in this area. A permanent frontal zone separates the drifting coastal waters (Fig.10-3, called the "coastal river", Brylinski et al., 1991) from the offshore waters (Brylinski & Lagadeuc, 1990), and regulates exchanges between the inshore and offshore communities for both plankton (Brylinski & Aelbrecht, 1993) and fish larvae (Grioche et al., 1997). The highly developed hydrodynamic system supports different benthic organisms (Lagadeuc & Brylinski, 1987; Lefebvre, 1999), through the transport of their larvae. 4- Offshore waters: A wider scientific interest in the location of the inflow of Atlantic waters into the North Sea (Salomon & Breton, 1991, Fig.10-4). This habitat would be ideal for observation of the northward extension of temperate species. A long-term station located off Wimereux (station L) serves as a lookout for the arrival of new species. 5- Southern bay of the North Sea: This area (Fig.10-5) presents high zooplankton biomass. Some specific differences with the English Channel can be highlighted. Despite the main northward flowing current preventing the transfer of species from the North Sea into the English Channel, the Atlantic jackknife clam (Ensis directus) has established a large population in the Eastern part of the English Channel from larvae released in the North Sea (Luczak et al., 1993). Therefore, this region is currently considered as a monitoring area in the southward progression of the invasive ctenophore, Mnemiopsis leidyi. Two other frontal zones can also be identified off the West coast of Brittany: the Celtic Sea shelf break and the Ushant tidal thermal front (Le Fèvre et al., 1983). 6- The Celtic Sea shelf break: The most striking features are 2°C cooler waters observed at the Shelf Break and a 100-miles strip located along the continental shelf-break in a North-West to South-East direction (Fig.10-6). High concentrations of phytoplankton and zooplankton are often reported in this area in connection with the upwelling of nutrient-rich deep waters. 7- The Ushant Tidal Thermal Front: This habitat (Fig.10-7) is one of the most studied areas of the Celtic Sea region. The frontal feature occurs in summer separates the thermally stratified open Celtic Seawaters from the tidally mixed coastal waters. Surface waters localized offshore of the frontal area are therefore warmer than the inshore ones.

“Bay of Biscay and Iberian coasts” sub-region (BBI) In the BBI sub-region, the ESA can be regrouped into three regions: coastal and estuarine areas, continental shelf and “Cap-Breton” canyon. 8- Coastal and estuarine areas: The highest biomass and diversity of zooplankton occur in coastal area of the BBI sub-region (Fig.10-8). Productivity is linked to continental inputs and to the intensity of the bentho-pelagic coupling. In Arcachon bay, the zooplankton community follows the classical seasonal pattern in the North Atlantic temperate ocean, with highest production during late spring and summer (meroplankton) linked with the high primary production (Vincent et al., 2002). Large-size zooplankton is mainly observed during late winter and small organisms during the spring production (Ayata, 2010). The long-term time series implemented in the Gironde estuary in 1997 has revealed a high annual variability of 27

Zooplankton meta-data census zooplankton abundance and an increase in the contribution of neritic taxa. River plumes from the Gironde, the Loire and the Adour affect the adjacent coastal zone. 9- Continental shelf and slope: High biomass and diversity are characteristic of these regions (Fig.10-9, Beaudouin, 1975; Sourisseau & Carlotti, 2006; Irigoien et al., 2009). Historical zooplankton data showed a relationship between zooplankton abundance and large-scale climate indices (Beaugrand et al., 2000). Further studies are needed to characterize the general seasonal pattern of zooplankton communities. 10- “Cap-Breton”canyon: The south section of the Bay of Biscay (Fig.10-10) is characterized by the presence of eddies, formed in connection with the “Cap-Breton” canyon, which induces a high planktonic diversity (Irigoien et al., 2009).

“Western Mediterranean Sea” sub-region (WMS) In the WMS sub-region, the ESA can be regrouped into three regions: lagoons and coastal waters, hydrological fronts and offshore convection area. 11- Coastal waters from Marseille to Italy: In coastal waters (Fig.10-11), most zooplankton data come from long-term time series. These data are very useful to establish the dynamics of zooplankton communities in relation to climate changes (Molinero et al., 2005; Garcia-Comas et al., 2011) or human activities (Jamet et al., 2001). 12- The frontal zone associated with the northern current: Hydrology of the Northwestern Mediterranean Sea along the French coasts is characterized by the presence of a westward flowing current, called the Ligurian or northern current. The presence of this current is associated with a highly productive hydrological front (Fig.10-12, Sournia et al 1990; Niewiadomska et al., 2008; Stemmann et al., 2008). Zooplankton and fish larvae are more numerous in this area than in the surrounding waters (Molinero et al., 2008). 13- Offshore area of winter deep convection: The Northwestern Mediterranean Sea is one of the few regions in the world where open-ocean deep convection occurs during winter (Fig.10-13). Two sub-areas are affected by this phenomenon: the south-east section off the Gulf of Lion and the center part of the Ligurian Sea. This process is mainly driven by the combination of strong northerly winds with the local anticlockwise oceanic circulation. In this oligotrophic basin, convection plays a major role in the functioning of pelagic ecosystems: phytoplankton spring blooms intensity is linked to the amount of nutrients transported from the bottom to the surface euphotic zone during winter convection episodes (Jacques et al., 1973, Hermann et al., 2008). In addition, large mammal’s populations are often observed in the North West Mediterranean sea (Bentaleb et al., 2011).and in the central part of the Ligurian Sea where the Pelagos sanctuary for marine mammals has been established. 14- The Gulf of Lion: The continental shelf water of the Gulf of Lion is another coastal ESA (Fig.10-14). The Rhone discharge creates a current flowing westward (due to the Coriolis effect). The input of Rhone leads to colder temperature and lower salinity conditions near the coast as 28

Raybaud et al. (2011) JORD 4: 11 - 37 well as richer food conditions for zooplankton (Gaudy et al., 2003). The enrichment effect of the Rhone also acts as a source of nutrition for fish larvae which make this region an excellent spawning ground for several commercially exploited species (Aldebert et al., 1997). 15- Coastal lagoons: Coastal lagoons (Berre, Thau and Bages, Fig.10-15), which are small marine systems under permanent stress from human activities, should also be carefully monitored for zooplankton and other factors. In these areas, zooplankton communities are strongly impacted by human activities (fishing and tourism), and lately are the sites where large proliferations of gelatinous zooplankton species occur (e.g., the ctenophore Mnemiopsis leydi in the Berre Lagoon).

Conclusion The first-ever comprehensive meta-dataset on zooplankton within the French coastal system has been organized. The results highlighted a wide disparity in the zooplankton studies, both in term of spatial coverage, sampling methods and level of analysis of samples. In addition, ESA could be defined. The next step should be the development of a database on diversity and counts of zooplankton. In sight of these results, we can propose some recommendations to harmonize the sampling strategy, the sampling method and the level of taxonomic analysis for future studies on zooplankton.

29

Zooplankton meta-data census

Acknowledgments This study has been funded by IFREMER, through the French part of the European MSFD project, called, in French, DCSMM (Directive-Cadre Stratégie pour le Milieu Marin). We thank all authors of zooplankton data who helped us in our census of metadata (Appendix 1). We thank John Dolan and Marsh Youngbluth for English corrections and helpful comments on the early version of the manuscript. We also thank Paul Nival, Martine Fioroni, Isabelle Palazzoli, Laure Mousseau, Nicolas Lavesque, Aurélie Chaalali, Jean-David Grattepanche and Dorothée Vincent for their helpful assistance.

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Appendix Table A1: List of all identified authors and co-authors (127) who worked on zooplankton of French metropolitan waters and whose metadata were used in this study. ALBANIA A.

DAGAULT F.

LABAT J-P.

PREJGER F.

ALDEBERT Y.

DALLOT S.

LACROIX-BOUTIN N.

PUSTELNIK G

AMINOT A.

DANIEL J-Y.

LAGADEUC Y.

QUINNIOU F.

ANDERSEN V.

DAUBY P.

LAM-HOAI T.

QUINTIN J-Y.

ANTAJAN E.

DAUVIN J-C.

LAPERNAT P-E.

RAMPAL J.

ARBAULT S.

DAVID V.

LAVAL P.

RAYBAUD V.

ARNAL O.

DE LA BIGNE C.

LEFEBVRE A.

RAYNAL F.

AUDEMARD C.

DEMER D-A.

LEFÈVRE G.

RAZOULS C.

AYATA S-D.

DI MENTO R.

LEFÈVRE J.

REYSSAC J.

BANDEIRA B.

DIAMOND E.

LICANDRO P.

RICHARD S.

BEAUDOUIN J.

DICENTA A

LOIZEAU V.

ROGER C.

BERGERON J-P.

DUPUY C.

MACQUART-MOULIN C.

ROMAGNAN J-B.

BOGE G.

ELBEE (D') J.

MARCANO G.

ROSSI N.

BONNET D.

FENAUX R.

MARINARO J-Y.

ROUGIER C.

BORSANI J-F.

FURNESTIN M-L.

MARTIN J.

RUMEBE M.

BOSC E.

GASPARINI S.

MATSAKIS S.

SABATIER R.

BOUCHER J.

GASSER B.

MATTHIVAT-LALLIER M-H.

SAMAIN J-F.

BOUGIS P.

GAUDY R.

MAYZAUD P.

SARDOU J.

BRACONNOT J-C.

GOFFART A.

MCGEHEE D-E.

SAUTOUR B.

BRETON E.

GORSKY G.

MOAL J.

SENTZ-BRACONNOT E.

BRYLINSKI J-M.

GOY J.

MOLINERO J-C.

SERTORIO Z.

BUECHER E.

GRALL J-R.

MOUNY P.

SOUISSI S.

CABAL J.

GRIOCHE A.

MOUSSEAU L.

SOURISSEAU M.

CAMUS P.

HALGAND D.

NIVAL P.

STEMMANN L.

CARLOTTI F.

HARTMANN H.

NIVAL S.

THIBAULT-BOTHA D.

CARRE C.

HECQ J-H.

NOWACZYK A.

THIEBAUT E.

CASANOVA B.

HERLORY O.

OMNES M-H.

THIRIOT A.

CASANOVA J-P.

HURET M.

PAGANO M.

TOULARASTEL F.

CASTEL J.

IBANEZ F.

PATRITI G.

VALLET C.

CAZAUX C.

ICARDI P.

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VANDROMME P.

CERVETTO G.

IRIGOIEN X.

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JAMET D.

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VU DO Q.

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PICCINETTI C.

WANG Z.

COMTET T.

JEAN N.

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COPPOLA L.

KOUBBI P.

PLOUNEVEZ S.

YOON W-D.

COTONNEC G.

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PRIEUR L.

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