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Fine scale zooplankton distribution in the Bay of Biscay in spring 2004

AITOR ALBAINA* AND XABIER IRIGOIEN
MARINE RESEARCH DIVISION, AZTI FOUNDATION, HERRERA KAIA PORTUALDE, Z/G

20110,

PASAIA (GIPUZKOA), SPAIN

*CORRESPONDING AUTHOR: aitoralbaina@hotmail.com Received January 29, 2007; accepted in principle July 19, 2007; accepted for publication August 9, 2007; published online August 16, 2007 Communicating editor: K.J. Flynn

A ne scale spatial resolution survey (3 15 nautical miles) was conducted during May 2004 in the Bay of Biscay (43.32 46.128N and 1.29 4.318W), to study the zooplankton community during the onset of spring stratication. Cluster analysis classied the 45 most abundant taxa into seven major groups. In the southern part of the surveyed area, a front separating neritic waters from eddies off the shelf delimited distinct zooplankton communities. On the northern side of the surveyed area, river plumes and the generation of internal waves over the shelf break were the main mesoscale structures determining the composition and abundance of the zooplankton assemblages. Canonical correspondence analysis (CCA) and generalized additive models (GAMs) were used to investigate the relationship between zooplankton species distribution and selected environmental variables (sea surface temperature and salinity along with water column stratication and uorescence pattern). Surface salinity and stratication index were the variables explaining the higher percentage of the deviance. The results of the survey conducted during May 2004 in the Bay of Biscay suggest that a limited number of environmental variables may be sufcient to attempt statistical modeling of zooplankton distribution.

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I N T RO D U C T I O N
Peaks in plankton biomass and species aggregations appear to occur on a continuum of scales; a variety of physical and biological phenomena may interact to spatially aggregate planktonic organisms on scales ranging from micro (centimeters to meters) to meso (kilometers to hundreds of kilometers) depending on the spatial extent of the particular oceanographic structures (Haury et al., 1978; Longhurst, 1981; Owen, 1981). Plankton biomass is generally reported to increase in the vicinity of fronts between distinct mesoscale oceanographic structures (ranging from, approximately, 5 to 50 nautical miles) where shifts in species composition also take place (e.g. Le Fevre, 1986; Nielsen and Munk, 1998; Morgan et al., 2005). Limitations in understanding and predicting plankton distributions in highly dynamic regions arise from a mismatch between the scales at which the biological and physical measurements are routinely made in eld surveys and the scales of the

mesoscale structures that inuence plankton communities and processes (e.g. Kushnir et al., 1997; Moore et al., 2003). Much of the research on temporal and spatial variability in plankton communities have been carried out on a large scale, and there has been a tendency to over-average the data (Cowen et al., 1993), thereby overlooking much of the small-scale variability in plankton distribution (Lee et al., 2005). Although studies on the effect of mesoscale structures on zooplankton have been carried out, these are generally limited to the effect of a single structure (e.g. one eddy, ndez one front) (e.g. Kingsford and Suthers, 1994; Ferna et al., 2004; Genin, 2004). On the other hand, there are studies of the inuence of mesoscale structures on zooplankton biomass distribution using automatic systems (e.g. Davis et al., 2004; Ashjian et al., 2005; Kimmel et al., 2006), but current taxonomic identication limits of these methods constrains our understanding of the observed biomass distributions.

doi:10.1093/plankt/fbm064, available online at www.plankt.oxfordjournals.org # The Author 2007. Published by Oxford University Press. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

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In fact, studies on how different mesoscale structures contribute to shape zooplankton communities over a large area are scarce because of the difculties of ne scale sampling over a large area together with high taxonomic resolution. The economic cost of increasing sampling effort in plankton surveys has contributed to the scarcity of this type of study. However, when sampling icthyoplankton in the context of daily egg production method (DEPM) surveys (Lasker, 1985), zooplankton samples are usually collected with a spatial resolution that resolves the mesoscale. In the Bay of Biscay, a DEPM is currently applied to estimate the anchovy (Engraulis encrasicolus) spawning biomass during its peaking spawning period (BIOMAN campaigns; see for example Motos et al., 1996) collecting zooplankton samples with a spatial resolution of 3 15 nautical miles over a large area (Fig. 1). Several studies have investigated mesoscale features in ndez et al., the Spanish part of the Bay of Biscay (e.g. Ferna lez-Quiro s 1991, 1993; Gil, 1995; Gil et al., 2002; Gonza et al., 2003, 2004). However, for the French part of the Bay, apart from the Landes coastal upwelling and river plumes, the occurrence of mesoscale variability is poorly documented because most published hydrological data

are historical, with sampling that is not synoptic enough to resolve mesoscale features (Puillat et al., 2006). The objective of this study is to exploit the DEPM small-scale resolution to elucidate the effect of mesoscale structures on zooplankton abundance and species composition in a highly dynamic region of the Bay of Biscay.

METHOD
The Bay of Biscay is an open oceanic bay located at 43.5 48.58N and surrounded by the north coast of Spain and the French west coast (Fig. 1). The ecosystem is comprised two shelves with different orientation and width and subjected to distinct current and tidal patterns that form a dynamic region where several mesoscale structures occur in a constrained area (see Koutsikopoulous and Le Cann, 1996; Borja and Collins, 2004; for a review). The Spanish part of the surveyed domain (hereinafter called Cantabrian Sea area) is characterized by an east-west orientated narrow shelf (15 20 nautical miles) and by the absence of important river outows (Prego and Vergara, 1998).

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Fig. 1. Location of the PAIROVET stations (crosses) and (highlighted) the transects which CTD vertical proles for density and FL are shown in Fig. 4. Isobaths of 100, 200, 1000 and 2000 m are shown along with the position of the Cap-Breton canyon, Marennes-Oleron and Arcachon bays and Gironde and Adour river mouths.

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The French part has a north-south shelf orientation, with width increasing northwards from 30 on the Landes Plateau to 80 nautical miles on the Aquitaine Shelf shelves). The conspicuous river outows (Gironde and Adour with, respectively, 900 and 300 m3 s21 mean freshwater outows, Puillat et al., 2004) (Fig. 1) also occur on the French shelf. Zooplankton samples were collected from 2 16 May 2004, as part of the Basque Country survey to estimate the biomass of anchovy (Engraulis encrasicolus) (BIOMAN 2004 campaign), in a grid of 267 stations. Consecutive stations were 3 nautical miles apart located in transects spaced 15 nautical miles apart covering the Bay of Biscay from 43.328N to 46.128N and from 1.298W to 4.318W (Fig. 1). The survey track started in the southwestern edge of the domain and ended in the coastal station of the northernmost transect. Samples were collected using vertical hauls of a 150 mm PAIROVET net tted with a owmeter and lowered to a maximum depth of either 100 or 5 m above the bottom at shallower stations. The PAIROVET net consists of a paired net with a mouth aperture of 0.05 m2 that is a version of the CalVET net (Smith et al., 1985). Net samples were preserved immediately after collection with 4% borax buffered formalin. The qualitative and quantitative analysis of zooplankton was carried out under a stereoscopic microscope and identication was made to species or genus level in the majority of the holoplanktonic groups, and to general categories in meroplanktonic forms (Table I). In each sample, a minimum of 200 individuals (all categories included) were counted. When referring to Calanoides carinatus and Calanus helgolandicus, patterns for copepodites IV VI are described. Copepodites I III could not be distinguished and were grouped under another category (Calanidae copepodites I III) (Table I). Fish eggs abundance was computed by sorting the entire sample. The nets were also tted with a conductivity, temperature and depth data logger (CTD; model RBR XR-420) with a uorescence (FL) sensor (Seapoint Chlorophyll Fluorometer; Seapoint Sensors, Inc.). Water density (expressed as sigma-t) was calculated for each meter of water column and a stratication index (SI) was computed by subtracting surface from bottom values. Surface temperature (ST), surface salinity (SS), SI and FL (expressed as FL units per cubic meter) were selected as representative environmental variables (Table II). Because the cruise does not provide a synoptic view, satellite images were obtained from IFREMER (Institut Franc ais de Recherche pour lExploitation de la MER) (http://www.ifremer.fr/cersat/facilities/browse/del/gascogne/browse.htm) for dates at the beginning (we used 25 April instead of 2 May which was cloud-covered)

Table I: Taxonomic list with mean, maximum and minimum values for abundance (ind. m23) and mean values for contribution (%) to total abundance of each taxa
Taxa Noctiluca scintillans Foraminifera Jellyshes except S. Bitentaculata Solmundella bitentaculata Siphonophora Gastropod veliger Bivalve veliger Tomopteris spp. Polychaeta except Tomopteris Podon spp. Evadne nordmanni Phoronida (Actinotroch larvae) Bryozoa (Cyphonautes larvae) Ostracoda Calanoides carinatus IV VI Calanoides carinatus female Calanoides carinatus male Calanoides carinatus V Calanoides carinatus IV Calanus helgolandicus IV VI Calanus helgolandicus female Calanus helgolandicus male Calanus helgolandicus V Calanus helgolandicus IV Calanidae copepodites I III Calanidae copepodites III Calanidae copepodites II Calanidae copepodites I Mesocalanus tenuicornis Neocalanus robustior Eucalanus spp. Rhincalanus spp. Calocalanus spp. Ischnocalanus spp. P-Calanus (Parac./ Claus./Pseud./Cteno. copepod) Paracalanus parvus Clausocalanus spp. Pseudocalanus elongatus Code Mean Maximun Minimun Mean (ind. m23) (ind. m23) (ind. m23) (%) 31 173.00 846.40 553.60 142.20 625.81 777.57 2262.02 69.53 486.74 324.63 1133.80 42.58 764.88 26.16 73.17 20.91 25.52 41.81 31.36 459.55 111.20 37.94 312.49 276.49 339.69 243.28 103.83 121.13 263.38 12.57 176.49 37.36 158.72 55.19 3059.52 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 38.29

4191.38 212.41 JELLY 60.56 SOLMU SIPHO GAVEL BIVEL POLYC PODON EVNOR 13.87 110.89 38.76 61.11 2.58 24.40 38.64 83.84 0.37 11.75 1.08 6.69 0.88 0.38 3.39 2.03 76.74 6.77 2.26 33.20 34.51 CI-III 52.35 24.21 15.67 12.47 MESTE 19.56 0.20 10.43 0.47 14.40 1.73 458.62

0.95 0.38 1.86 0.61 0.66 0.07 0.40 0.73 1.92 0.00 0.07 0.03 0.20 0.03 0.01 0.10 0.06 1.87 0.13 0.05 0.85 0.83 1.14 0.53 0.36 0.25 0.58 0.01 0.26 0.01 0.42 0.02 7.25

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CCARI

CHELG

EUCAL CALOC P-CAL

PARAC CLAUS PSEUD

44.01 33.54 50.98

425.14 139.56 903.95

0.00 0.00 0.00

0.76 0.88 0.50

Continued

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Table I: Continued
Taxa Ctenocalanus vanus Stephos spp. Temora longicornis Temora stylifera Centropages spp. Candacia spp. Euchirella spp. Metridia spp. Pleuromamma spp. Euchaeta spp. Pseudophaenna typica Scolecithricella spp. Aetidius spp. Heterorhabdus papilliger Diaxis spp. Anomalocera patersoni Acartia clausi Oithona similis Oithona nana Oithona plumifera Cyclopina litoralis Corycaeus spp. Oncaea spp. Euterpina acutifrons Microsetella spp. Halithalestris croni Clytemnestra spp. Aegisthus spp. Copepoda nauplius Cirripedia Amphipoda Isopoda Decapod larvae Euphausiacea Mysidacea Cumacea Sagitta spp. Echinodermata larvae Fritillaria spp. Oikopleura spp. Appendicularia spp. Doliolum spp. Tornaria larvae Cephalochordata (Branchiostoma lanceolatum) Anchovy (Engraulis encrasicolus) eggs Sardine (Sardina pilchardus) eggs Other sh eggs Copepoda total Zooplankton total Code CTENO TEMLO CENTR CANDA ME-PL EUCHA Mean Maximun Minimun Mean (ind. m23) (ind. m23) (ind. m23) (%) 17.32 0.40 375.86 0.13 70.71 7.26 0.04 9.60 3.01 0.23 0.06 0.45 0.32 2.40 0.17 136.47 1068.43 209.89 76.17 0.05 83.66 1872.98 48.72 27.32 0.09 1.44 0.34 406.66 58.73 2.13 0.86 9.88 14.61 0.98 0.06 7.83 15.19 395.23 90.45 32.42 0.77 0.23 6.61 103.50 22.49 3504.23 24.21 517.49 65.63 10.66 151.34 48.10 11.84 16.07 24.91 11.87 92.55 24.72 1347.79 4831.07 3289.14 739.17 14.51 672.73 14 257.92 973.88 130.75 12.77 42.67 55.60 3059.52 1876.12 56.52 51.55 379.40 121.64 38.97 15.94 112.19 206.20 7210.17 2642.32 559.57 15.61 15.26 93.90 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 190.35 0.00 0.00 0.00 0.00 15.34 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.46 0.01 5.06 0.00 1.16 0.21 0.00 0.28 0.10 0.01 0.00 0.02 0.01 0.03 0.00 2.37 18.72 2.45 2.07 0.00 1.15 26.34 0.50 0.65 0.00 0.03 0.00 5.61 0.71 0.03 0.02 0.12 0.38 0.02 0.00 0.13 0.30 7.76 0.89 0.62 0.02 0.01 0.14

Table II: Mean values and range of variation for environmental variables used in statistical analysis
ST Mean Standard deviation Maximun Minimun 13.46 0.60 15.40 12.59 SS 34.41 0.98 35.96 29.80 SI 0.86 0.77 4.63 0.00 FL 1.59 0.89 5.02 0.30

ST (8C), SS, SI (kg m23) and FL (relative units m23) calculated from net associated CTD data logger vertical proles (n 241).

ACCLA OITSI OITNA OITPL CORYC ONCAE EUTER MICRO

COPNA CIRRI

DECAP EUPHA

SAGIT ECHIN FRITI OIKOP APPEN

CEPHA

ANCHO

1.01

19.12

0.00

SARDI OTFIS

2.91 0.98 5189.92 6273.74

51.55

0.00

and end of the survey (16 May) to complement the CTD in situ data. The parameters considered from satellite images were ST, Chlorophyll a (Chl a) and inorganic suspended particulate matter (SPM) including coccoliths (see Gohin et al., 2005 for details). Simpsons diversity index (Simpson, 1949) was calculated only for the copepod community because of the higher homogeneity in the taxonomic classication. Multivariate analyses of the sampled stations and the relevant zooplankton taxa were carried out using the squared Euclidean Wards method cluster (Ward, 1963; Pielou, 1984) applied to log10 transformed abundance values using only those taxa that contributed more than 0.1% of the zooplankton community abundance. Canonical correspondence analysis (CCA) and generalized additive models (GAMs) were used to investigate the relationship between zooplankton taxa abundances and selected environmental variables (ST, SS, SI and FL; Table II). Zooplankton taxa abundances were log10 (x 1) transformed before analysis. The CCA test was performed using version 4.5 of CANOCO (ter Braak and Smilauer, 2002); all canonical axes were used to evaluate the signicant variables under analysis by Monte Carlo test (999 permutations). GAMs (Hastie and Tibshirani, 1990) were implemented using the mgcv package (version 1.3-17; http://cran.r-project.org/doc/ packages/mgcv.pdf ) of R (Wood, 2001). The percentage of explained deviance along with generalized crossvalidation (GCV) smoothness estimation was computed for selected variables (each independently or combined) when modeling the zooplankton spatial distributions.

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16.26 0.00 23 454.09 895.03 24 166.70 1033.83

81.17 100.00

R E S U LT S
Environmental variables
The area was sampled during the onset of stratication as inferred from low surface mean temperature (13.468C, Table II) and from satellite images for ST at the beginning and at the end of the survey (Fig. 2a and d).

Column CODE shows the codes used in species cluster where only taxa that conform more than 0.1% of the zooplankton community abundance are taken into account. The protozoans Noctiluca scintillans and Foraminifera were not considered for computing zooplankton total abundance and statistical analysis (see text for further explanation).

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Fig. 2. Temperature (8C; NOAA 17 satellite), Chlorophyll a (Chl a) (mg m23; SeaWiFS satellite) and inorganic SPM coccolith (ln g m23; SeaWiFS satellite) satellite images for 25 April 2004 (signaled respectively a, b and c) and 16 May 2004 (d, e and f ); all scales superimposed. Black areas represent clouds presence; a black line signals the sampled domain.

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As a result, the northern, and chronologically last sampled, transects had the highest temperatures (Fig. 3a). The SI also showed the warming of Biscay waters during the survey (Fig. 3c). Highest temperatures were located in the mouth of Gironde estuary. The Adour and Gironde river plumes (see Fig. 1 for location) had low SS (Fig. 3b) and high salinity occurred in the more oceanic part of the sampled grid. The dominating stratication force in spring was the spreading of river plume waters over the shelf (Fig. 3b and c). Although stratication was weak, the neritic to ocean decreasing stratication pattern was also noted in density vertical proles (Fig. 4a, c and e), where plume waters showed a 20 30 m depth penetration and a mid-shelf extension. The oscillations of pycnoclines with declining amplitude from the shelf break clearly signaled the generation of internal waves over the slope

(Fig. 4c and e). An upwelling of cold water off Landes coast was detected through satellite imagery (Fig. 2d). Maximum FL was related to river plume waters and to the shelf break; minimum FL corresponded to the neritic zone in the south of the survey area and to the 100 200 m depth shelf waters in northernmost transects (Fig. 3d). The vertical distribution of FL showed a distinct pattern for the two peaking areas, revealing a surface maximum and a pycnocline maximum for, respectively, the river plume and shelf break areas (Fig. 4d and f ). In the Cantabrian Sea, a front separated neritic low FL waters from high FL oceanic waters (Fig. 4b). At the beginning of the cruise, satellite imagery showed the above-described bimodal pattern for surface Chl a and revealed an oceanic bloom of phytoplankton coinciding with eddy formation from the shelf break (Fig. 2b and c). By the end of the cruise,

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Fig. 3. Spatial distributions of environmental variables computed from CTD data: (a) ST (8C), (b) SS, (c) SI (kg m23) and (d) FL (relative units m23); all scales superimposed. Isobaths of 100, 200, 1000 and 2000 m are shown.

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Fig. 4. Vertical (0 100 m depth; left axis) proles of density (sigma-t; upper graphs) and FL (relative units; bottom graphs) for transects signaled in Fig. 1 with axes 3.98W (graphs a and b), 44.128N (graphs c and d) and 45.378N (graphs e and f ). Scales are superimposed and bottom prole and sampled depths are shown within the graph; distance to the coast in nautical miles (bottom axis). Sigma-t (kg m23) is the density anomaly of a water sample when the total pressure on it has been reduced to atmospheric pressure (i.e. zero water pressure), but the temperature and salinity are in situ values.

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satellite images indicated phytoplankton maxima at the mouth of the Gironde and at the shelf break (Fig. 2e and f ).

Zooplankton community
From the taxa identied (Table I), although abundant, the protozoans Noctiluca scintillans and foraminifera were not considered in this study because of size-related inadequate sampling. Copepods comprised 81.2% of the total zooplankton abundance. The dominant groups (60.1% of community abundance; Table I) were copepods Oncaea spp., Oithona similis, P-Calanus (involving the copepodite stages of genus Paracalanus, Clausocalanus, Pseudocalanus and Ctenocalanus) and the appendicularian Fritillaria spp. Figure 5 shows the SS and ST weighted mean abundance values for the identied taxa. The distribution of zooplankton abundance was characterized by a pattern with maximum abundance values related to shallower stations to minimum ones in mid-shelf depths and an increase in northern shelf break locations (Fig. 6a). The spatial pattern for copepods differed from that for total zooplankton by showing low total copepod abundance values associated with neritic locations of the Cantabrian Sea (Fig. 6b). Day/night sampling, which would have resolved diel vertical migration, did not affect the abundances measured (data not shown). Simpsons diversity index (S) values for the copepod community are presented in Fig. 6c; while highest diversity values corresponded to the shelf break and Cap-Breton canyon stations, the stations located in shelf waters between both river plumes had the lowest diversity. Four distinctive groups of stations, namely ST-1, ST-2, ST-3 and ST-4, were identied as function of the zooplankton composition with the Wards method cluster analysis (Fig. 7a); groups ST-1 and ST-2 were further divided into two subgroups: ST-1A and ST-1B, and ST-2A and ST-2B, respectively. Looking at the spatial distribution of the stations comprised in each cluster, a clear spatial pattern arose with almost no overlapping of the stations grouped (Fig. 7b). ST-1 cluster involved stations that covered the Cantabrian Sea along with waters in the Cap-Breton canyonAdour river plume zone with subgroups ST-1A and ST-1B occupying, respectively, neritic and more oceanic waters. ST-2 cluster comprised the stations over the French part of the sampled domain characterized with depths greater than 100 m; whereas ST-2A stations followed ST-2B ones in the depth gradient in the Aquitaine Shelf, there was no such gradient on the Landes Plateau. ST-3 and ST-4 groups comprised the inner-shelf community in

French sampled area; ST-4 stations coincided with the Gironde river plume waters and were surrounded to the north and to the south by stations in cluster ST-3 located at the mouth of both Marennes-Oleron and Arcachon Bays. The zooplankton taxa dendrogram identied four large assemblages (TX-A, TX-B, TX-C and TX-D) further subdivided into seven clusters (Fig. 8). TX-A1 cluster comprised taxa with neritic preference over the entire grid but with low abundances in the Gironde plume waters such as Acartia clausi, Podon spp., Oikopleura spp. and Sardina pilchardus eggs (Fig. 9a). TX-A2 showed the same pattern but was restricted to the French part of the domain and was characterized by meroplankton taxa such as Bivalve veliger, Echinodermata larvae and Polychaeta larvae (Fig. 9b). TX-B clusters grouped taxa reaching the highest abundances, comprising 77% of total zooplankton abundance, and with maximum values in neritic waters but being also relatively abundant in the Gironde plume waters. TX-B1 taxa grouped Oncaea spp., Temora longicornis and Engraulis encrasicolus eggs among others, with maximum values associated with the Landes cold water upwelling and hardly present in the Cantabrian Sea waters (Fig. 9c); TX-B2 cluster comprised Oithona similis, P-Calanus category and Copepoda nauplius following a bimodal distribution pattern with high abundances also in shelf break waters (Fig. 9d). TX-C cluster was characterized by the appendicularian Fritillaria spp. and the cladoceran Evadne nordmanni and displayed maximum abundance values in the Cantabrian Sea neritic waters and a minor secondary peak in northern shelf break locations (Fig. 9e). TX-D clusters included taxa restricted to waters deeper than 100 m. Species with maximum abundance at the shelf break, such as Mesocalanus tenuicornis, Calocalanus spp. and Oithona plumifera, formed TX-D1 cluster (Fig. 9f ); TX-D2 put together taxa with maximum abundances in outer-shelf waters such as the copepods Calanus helgolandicus (developmental stages IV VI) and Eucalanus spp. (Fig. 9g). The species environment correlation for the CCA rst axis was 0.84 and the cumulative explained variance for the species environmental relationship was 74.4%; when adding the second axis this improved to 89.3% (Fig. 10). All environmental variables included in the analysis were signicant (P 0.001; 999 Monte Carlo permutations). Zooplankton taxa were grouped by the CCA as in Fig. 8 species Wards cluster analysis (Fig. 10; see legend for further explanation and symbol correspondence). TX-A1, TX-A2 and TX-B1 taxa occurred in the right part of the biplot with lowest SS and highest ST, SI and FL values. TX-C, TX-D1 and TX-D2 occupied the opposite location showing positive

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Fig. 5. SS (left axis) and ST (8C; bottom axis) weighted mean values for identied taxas abundance distribution; only those taxa that conform more than 0.1% of the zooplankton community abundance are shown (except for CI-III, P-CAL, COPNA, APPEN and OTFIS; codes in Table I).

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Fig. 6. Spatial distributions of (a) total zooplankton abundance (ind. m23), (b) total copepods abundance (ind. m23) and (c) Simpsons diversity index (S) values for the copepod community (no units). Higher values for S mean lower diversity; value 1 denotes no diversity (S S(n/N)2; n, number of individuals of one species and N, total number of individuals summing all species). Isobaths of 100, 200, 1000 and 2000 m are shown.

correlation with SS and negative one with ST, SI and FL. TX-B2 taxa were located in the origin of the axes. Table III shows GAMs analysis results for species Wards clusters (Fig. 8; TX clusters) when computing only one environmental variable each time. These revealed that SS and SI were the variables explaining the higher percentage of the deviance. The resulting curves when tting GAMs to all of the TX clusters abundance distributions using selected variables are shown in Fig. 11. The seven clusters differed in their response to selected variables: a sharp decline with SS over 33 and a sharp increase with SI for values within 0 and 2 distinguished TX-A and TX-B taxa from TX-C and TX-D. TX-A taxa were separated from TX-B ones by the steepness of the slope of the relationships with SS and SI, being steeper in both cases for TX-B taxa. TX-C taxa deviated from TX-D ones by their marked negative relationship with FL. Within the TX-A group, the signicant relationship with SI distinguished TX-A2 from TX-A1 taxa. In the

TX-B group, the secondary peak of abundance for TX-B2 species in shelf break habitats was denoted by the bimodal curve for SS separating them from more coastal-river plume restricted TX-B1 group of species. The differentiation between TX-D1 and TX-D2 species was more subtle and determined by the steeper response to SS (in the range . 33) and SI (in the range 0 2) in the TX-D1 cluster species when comparing with the TX-D2 cluster. GAMs allow obtained distributions (TX cluster abundance distributions) to be tted to multiple predictors; Table IV shows the results for applying GAMs of increased complexity to zooplankton data, ranging from two to four predictors (ST, SS, SI and FL), and taking into account or not interactions between them (see legend for further explanation). The model explaining the highest percentage of deviance was (ST, SS, SI) with a mean value for all clusters of 74.4%. Although TX-B1 and TX-B2 reached the maximum percents of explained deviance with, respectively, 86.4 and 83.9,

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Fig. 7. (a) Stations cluster. Squared Euclidean Wards method cluster applied to log10 (zooplankton species abundance 1) transformed data using only taxa that conform more than 0.1% of the zooplankton community abundance (267 cases; 45 taxa), (b) Spatial distribution of different stations cluster subgroups (symbols correspondence superimposed); 100, 200, 1000 and 2000 m isobaths are shown.

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Fig. 8. Species cluster (species code in Table I). Squared Euclidean Wards method cluster applied to log10 (zooplankton species abundance 1) transformed data using only taxa that conform more than 0.1% of the zooplankton community abundance.

TX-A2 achieved the minimum value for this model with 46.9%.

DISCUSSION
Our results show that when sampled with suitable spatial and taxonomic resolution, environmental variables can be used to characterize specic ranges of zooplankton abundance and species composition even in highly dynamic ecosystems such as that studied here. Although DEPM surveys only provide a snapshot of the zooplankton community on the sampled dates, the relatively lack of synopticity related to 2 weeks long survey was not enough to avoid relating zooplankton communities to mesoscale structures. In this sense, zooplankton communities of the Cantabrian Sea (clusters ST-1A and ST-1B; Fig. 7) were governed by eddies located over the shelf break [slope water oceanic eddies (SWODDIES) as described in Pingree and Le Cann (Pingree and Le Cann, 1992); Fig. 2b and e] forming a frontal system between low FL neritic waters and oceanic ones (Fig. 4b); higher levels of Chl a in Bay of Biscay SWODDIES with respect to surrounding waters along with the presence of distinct zooplankton assemblages inside and outside the SWODDY have been previously guez et al., 2003; Ferna ndez et al., 2004; described (Rodr Isla et al., 2004). In the French part of the domain, however, zooplankton communities (clusters ST-2A, ST-2B, ST-3 and ST-4; Fig. 7) were determined by the presence of river plumes and internal wave generation over the slope. These mesoscale structures produce

(Fig. 4d and f ) a FL peak in the river plume surface waters related to the continuous input of nutrients due to continental drainage (Bergeron and Herbland, 2001), low FL mid-shelf stations and a secondary peak over the shelf break promoted by deep waters nutrients injection via internal waves mixing (Pingree and Mardell, 1981; Holligan et al., 1985). Contrary to Cantabrian Sea waters subjected to SWODDY inuence, the zooplankton total abundance spatial distribution in French waters (Fig. 6a) matched well with the above-described pattern for FL. The observed correspondence between mesoscale structures and zooplankton communities is quantitatively reinforced with the strong species environment correlation for the CCA (cumulative explained variance for the species environmental relationship: 89.3%; Fig. 10) and the high percentage of deviance explained by GAM analysis (Table IV). Although statistical models do not provide the underlying mechanisms for the observed relationships, the species groups obtained and their relations to environmental variables (Figs 10 and 11) can be used to infer potential causes. In this sense, the TX-A1 cluster comprising a neritic community with lowest abundances in the Gironde river plume locations (Fig. 9a) might be explained by the presence of species with resting eggs in their development cycle that need sea oor resuspension to hatch (e.g. Podon spp. and Acartia clausi) thus requiring shallow habitats (e.g. Marcus, 1990; Hairston, 1996); but, these species, might be also unable to prosper in the turbid plume waters with a high content of inorganic particles (Froidefond et al., 1998), as shown for Acartia bilosa

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Fig. 9. Spatial distribution of different species cluster subgroups (ind. m23; scales superimposed): (a) Cluster TX-A1, (b) Cluster TX-A2, (c) Cluster TX-B1, (d) Cluster TX-B2, (e) Cluster TX-C, (f ) Cluster TX-D1 and (g) Cluster TX-D2. Code names are as in Fig. 8; 100, 200, 1000 and 2000 m isobaths are shown.

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Fig. 10. CCA biplot for zooplankton taxa abundance and environmental variables. Only zooplankton taxa conforming more than 0.1% relative abundance of the zooplankton community abundance were used (species code as in Table I). Species symbols correspond to Fig. 8 clusters: Cluster TX-A1 (black triangles), Cluster TX-A2 (white triangles), Cluster TX-B1 (black circles), Cluster TX-B2 (white circles), Cluster TX-C (crosses), Cluster TX-D1 (black squares) and Cluster TX-D2 (white squares). CCA identies environmental variables that explain directions of variance in the species data along one or more axes; in this case, only the rst two axes are shown. CCA included four environmental variables: ST , SS, SI and FL. None of the data were weighted. Cumulative explained variance of species environment relation: 89.3% (axes 1 and 2). The length of the environmental arrows and their orientation on the biplot indicate the relative importance of the variable to each axis; the variables with the longest arrows are most highly correlated with the axes. Environmental arrows represent a gradient; the mean value lies at the origin and the arrow points in the direction of increase.

inside the estuary (Irigoien and Castel, 1995). On the other hand, the decreasing pattern of TX-A2 cluster species abundance from both Marennes-Oleron and Arcachon bays locations (Fig. 9b) matches with the tidal ats and the presence of important shellsh farms in both bays (mainly oyster; OSPAR Commission, 2000) as the cluster is composed of meroplanktonic forms with bivalve larvae representing 33% of the total abundance. Meroplankton has been previously cited as representing

an important part of the zooplankton community in these semi-enclosed ecosystems and surrounding areas e and Castel, 1991; (Castel and Courties, 1982; dElbe Sautour and Castel, 1993). The abundance gap between both meroplankton spreading sites corresponding to Gironde river plume waters has also been associated with high SPM values for a lter feeding community to develop (Heip and Herman, 1995). TX-B1 cluster includes typical Bay of Biscay neritic

Table III: Results of GAM analysis for Ward clusters subgroups (Fig. 8; n 241) using each selected environmental variable independently; percentage of explained deviance along with generalized cross validation (GCV; in brackets) smoothness estimation were computed
TX-A1 ST SS SI FL 7.59 (0.24) 13.2 (0.22) 0.925 (0.25) 7.01 (0.24) TX-A2 18 36.4 30.5 6.69 (0.23) (0.18) (0.20) (0.27) TX-B1 16.5 68.7 55.6 24.1 (0.18) (0.07) (0.10) (0.17) TX-B2 21.7 54.1 38.2 17 (0.08) (0.05) (0.07) (0.09) TX-C 13.6 32.5 45 20.9 (0.90) (0.73) (0.59) (0.83) TX-D1 7.44 (0.36) 41 (0.23) 23.7 (0.30) 2.51 (0.37) TX-D2 14.3 (0.20) 20.1 (0.19) 5.24 (0.22) 0.376 (0.23)

The lowest GCV score for a cluster represents the best tting. ST (8C), SS, SI (kg m23) and FL (relative units m23).

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Fig. 11. Partial nonlinear terms ( y-axis) of different species cluster subgroups abundance distributions (codes in left extreme as in Fig. 8; Squared Euclidean Wards method cluster) estimated by means of GAMs using each selected environmental variables independently (variables values in x-axis): ST , SS, SI and FL. The appropriate smoothness for each applicable model term was selected using generalized cross validation (GCV). The solid line in each plot is the estimate of the smooth function, whereas the dashed lines represent the 95% condence limits. Smooth functions are not signicant when the condence region for the smoothing include zero throughout the range of the predictor. Tick marks on x-axis show the locations of the observations on each variable.

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Table IV: GAMs for each Ward clusters subgroups (Fig. 8; n 241); two types of models combining variables were tested: with or without interaction among variables, respectively case (var.1, var.2, var.3. . .) and (var.1) (var.2) (var.3) . . . (see Wood, 2004 for further explanation)
TX-A1 ST,SS ST,SI ST,FL SS,SI SS,FL SI,FL ST SS ST SI ST FL SS SI SS FL SI FL ST,SS,SI ST,SS,FL ST,SI,FL SS,SI,FL ST SS SI ST SS FL ST SI FL SS SI FL ST,SS,SI,FL ST SS SI FL 39.9 (0.18) 20.3 (0.23) 24.7 (0.22) 45.1 (0.16) 41.8 (0.18) 30.7 (0.20) 23 (0.20) 10.8 (0.23) 12.7 (0.23) 44.1 (0.16) 21.2 (0.21) 8.39 (0.24) 81.4 (0.10) 54.1 (0.16) 43.9 (0.19) 64.1 (0.13) 54.6 (0.14) 32.4 (0.19) 17.5 (0.23) 50.9 (0.15) NA 61 (0.12) TX-A2 42.4 (0.18) 33.2 (0.20) 27.8 (0.22) 42.4 (0.18) 40.6 (0.18) 37.6 (0.19) 39.4 (0.18) 32.8 (0.20) 21.3 (0.23) 36.6 (0.18) 39.6 (0.18) 33.6 (0.20) 46.9 (0.17) 42 (0.17) 37.1 (0.19) 42.8 (0.17) 39.3 (0.18) 41.2 (0.18) 35.6 (0.20) 39.8 (0.18) NA 39.7 (0.18) TX-B1 79.3 65.3 43.6 72.3 72.2 66.8 71.7 63.6 35.6 71 71.2 60.6 86.4 82.8 74.4 78.6 75.5 74.2 68.2 74.2 NA 78.5 (0.05) (0.08) (0.14) (0.07) (0.07) (0.08) (0.07) (0.08) (0.15) (0.07) (0.07) (0.09) (0.05) (0.05) (0.07) (0.06) (0.06) (0.06) (0.08) (0.06) (0.06) TX-B2 63.9 50 42.2 57.8 57.5 50.3 59.3 44.9 33.6 55.2 57.4 44.5 83.9 64.9 57.4 67.8 60.8 62.3 50 58.4 NA 63.1 (0.05) (0.06) (0.07) (0.05) (0.05) (0.06) (0.05) (0.06) (0.07) (0.05) (0.05) (0.06) (0.03) (0.05) (0.06) (0.05) (0.05) (0.05) (0.06) (0.05) (0.04) TX-C 52.8 (0.56) 56 (0.52) 37.4 (0.71) 50.5 (0.58) 42.7 (0.66) 53.7 (0.55) 39.7 (0.67) 52.4 (0.53) 32.2 (0.73) 49.4 (0.58) 38.6 (0.69) 51.4 (0.54) 77.7 (0.42) 62.7 (0.53) 65.4 (0.49) 66.8 (0.53) 57.9 (0.50) 46.5 (0.62) 57.9 (0.49) 54.4 (0.52) NA 63.6 (0.45) TX-D1 55.7 31.7 11.9 52.1 53.5 34.4 42.2 24 8.71 46.5 42.6 23.7 74.7 63.2 56.8 72.9 51.7 43.4 24.1 48.4 NA 52.7 (0.20) (0.29) (0.35) (0.21) (0.21) (0.29) (0.23) (0.30) (0.36) (0.22) (0.23) (0.30) (0.16) (0.21) (0.27) (0.17) (0.21) (0.23) (0.30) (0.21) (0.20) TX-D2 37.5 30 20 35 26.8 28 27.5 14.6 15.2 21.2 22.8 8.15 69.9 74 41.4 65.6 33.1 29.9 16.6 24.6 NA 35.5 (0.17) (0.19) (0.21) (0.18) (0.19) (0.20) (0.18) (0.21) (0.20) (0.19) (0.19) (0.22) (0.13) (0.13) (0.19) (0.15) (0.17) (0.18) (0.20) (0.18) (0.17)

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Percentage of explained deviance along with generalized cross validation (GCV; in brackets) smoothness estimation were computed; the lowest GCV score for a cluster represents the best tting when comparing models with distinct variables included. ST (8C), SS, SI (kg m23), FL (relative units m23). The model using all variables with interaction was impossible to compute due to insufcient number of cases (NA, not available).

taxa (Albaina and Irigoien, 2004) comprising 46% of total zooplankton abundance with maximum abundances related to the Landes coast upwelling location (Fig. 9c); spring summer upwelling in the Landes coast gou and Lazure, is a regularly observed structure (e.g. Je 1995; Borja et al., 1996, Froidefond et al., 1996), and the peak abundances could be related to increased primary production due to the injection of nutrients. The observed decrease in abundance in Gironde river plume in clusters TX-A1, TX-A2 and TX-B1 could be a response to extremely high Gironde river outows washing away river plume zooplankton as suggested by Albaina and Irigoien (Albaina and Irigoien, 2004) for a 5-year study of a transect in front of the Gironde Estuary; in this sense, the 34 015 m3 s21 accumulated ow value, for the 15 preceding days to the sampling in 2004 was the highest among the ones reached in the above cited work. The huge contribution of Oncaea spp. to cluster TX-B1 and to the entire zooplankton community (respectively, 65% and 26% of measured abundance) determined the minimum copepod diversity values associated with the Landes Coast locations (Fig. 6c); the highest values were related to Cap-Breton canyon and shelf break locations. Maximum diversity for copepods in the Cap-Breton e, 2001) canyon area has already been observed (dElbe and is due to the transport of oceanic species to coastal

stations where both populations merge. On the other hand, a depth-related increase in diversity from coastal to shelf break locations is a common pattern in copepod communities (see Mauchline, 1998 for a review). TX-B2 cluster taxa were located in the origin of the axes of the CCA showing high tolerance to the range of values of selected environmental variables and explaining their bimodal distribution pattern with prominent abundances in almost all the sampled grid stations (Fig. 9d). However, it has to be taken into account that this plasticity of the taxa in the TX-B2 cluster is explained by two different reasons. On one hand, P-Calanus and Copepoda nauplius are taxonomical categories involving different species, and therefore there is no real plasticity but difculties in separating the early stages of the species. On the other hand, Oithona similis, the principal taxa in TX-B2 cluster (55%) and dominating Bay of Biscay spring community abundance (Albaina and Irigoien, 2004), shows real capability to adapt to different environments as shown by its widespread distribution (Gallienne and Robins, 2001; Nielsen et al., 2002; Castellani et al., 2005). In the Cantabrian Sea, total copepod peak abundances (Fig. 6b) matched with the locations of SWODDIES and can be related to the associated FL pattern or to mechanical transport from adjacent locations or a combination of both (as suggested in

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ndez et al., 2004); however, highest zooplankton Ferna abundances in the neritic domain (Fig. 6a) were related to high abundances of the TX-C cluster species (Fig. 9e). The appendicularian Fritillaria spp. (mainly F. pellucida) comprised 72% of the cluster abundance; the association of F. pellucida with low FL values can be due to the fact that non-phytoplanktonic material seems to be an important part of the diet of F. pellucida in the pez-Urrutia et al., 2003). The Cantabrian Sea (Lo present studys abundances for Fritillaria spp. (maximum of 7210 ind. m23; Table I), a species typical of the Bay of Biscay cold waters at the onset of the spring stratica n, 1992), agree with measured tion (Acun a and Anado temperatures that are among the lowest recorded in n May for the Bay of Biscay (e.g. Motos et al., 1996; Lav et al., 1998; Albaina and Irigoien, 2004). The shelf break associated maximum abundances for TX-D1 cluster species (Fig. 9f ) are explained by their wellknown preference for deep habitats comprising the Bay of Biscay oceanic community (e.g. Beaudouin, 1975; Albaina and Irigoien, 2004). However, TX-D2 cluster taxa (Fig. 9 g) inhabiting the mid-shelf habitat characterized by low zooplankton total abundances (Fig. 6a) and low FL values (Fig. 3d) deserves further discussion; this ecosystem has been recently identied as a stable hydrological structure (Planque et al., 2006) and presents a gap in zooplankton abundance between the innershelf and shelf break systems (Albaina and Irigoien, 2004). Calanus helgolandicus development stages IV VI (CHELG code; Table I) represented 55% of TX-D2 cluster abundances. Calanus spp. reproductive success has been related to depth to avoid the seaoor burial of eggs previous to hatching (Uye, 2000; Irigoien and Harris, 2003); beside this, retention by dominating currents, predation avoidance and a potential off-shelf overwintering source population could contribute to explain the distributions observed and should be taken into account when explaining the recurrent (Beaudouin, 1975; Albaina and Irigoien, 2004) mid-outer shelf habitat for C. helgolandicus in the Bay of Biscay. More studies are needed concerning C. helgolandicus population dynamics in order to elucidate the factors governing the distribution observed. In this sense, although C. helgolandicus is known to overwinter in oceanic deep waters in the nearby Celtic Sea (Williams and Conway, 1988), whether there is overwintering in Bay of Biscay waters remains unclear (Bonnet et al., 2005; Ceballos lvarez-Marque s, 2006). and A Observed and quantied relationships between zooplankton groups and environmental variables can be used for more appropriate sampling design in future surveys and for the development of Bay of Biscay zooplankton distribution models when implementing

integrated ecosystem models. Although in French waters of the Bay of Biscay, most of ecological works have been limited to the study of Gironde river plume waters (e.g. Herbland et al., 1998; Bergeron and Herbland, 2001; Labry et al., 2001; Labry et al., 2002), the present study shows the inuence of different mesoscale structures within the bay forcing zooplankton composition and distribution. In the Bay of Biscay, mesoscale structures are recurrent and spatially predictable, as demonstrated by the modeling of the spreading process of French river plumes over the Bay of Biscay shelf (Lazure and gou, 1998; Puillat et al., 2004) and of the slope internal Je waves and their oceanographic effects (Gerkema et al., 2004; Pichon and Correard, 2006), along with the satellite monitoring of the eddies (Gohin et al., 2005). Our results indicate that this progress in operational physical oceanography can be translated into detailed biological information through statistical modeling, if the biological sampling is carried out with sufcient spatial and taxonomic resolution.

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CONCLUSIONS
Cluster analysis classied zooplankton taxa into seven major groups showing contrasting distributional patterns: although zooplankton communities of the Cantabrian Sea were governed by eddies located over the shelf break, in the French part of the domain, zooplankton communities were determined by the presence of river plumes and internal wave generation over the slope. Correspondence between mesoscale structures and zooplankton communities was supported by both the strong species environment correlation for the CCA, and the high percentage of deviance explained by GAM analysis. SS and SI were the variables explaining the higher percentage of the deviance. Environmental variables can be used to characterize specic ranges of zooplankton abundance and species composition even in highly dynamic ecosystems if the biological sampling is carried out with sufcient spatial and taxonomic resolution.

AC K N OW L E D G E M E N T S
We are grateful to the crew of the R. V . Vizconde de Eza and the on board scientists and analysts for their support during sampling and for counting sh eggs. Thanks are due to R. P . Harris for comments. Satellite images acquired and processed by the CERSAT (Centre ERS dArchivage et de TraitementFrench ERS Processing and Archiving Facility), part of

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IFREMER (French Research Institute for Exploitation of the Sea). Gironde river daily ow was obtained from the harbor authority of Bordeaux.

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FUNDING
Doctoral fellowship of the Education, Universities and Research Department of the Basque Country Government to A.A.; Spanish Ministry of Research (Ramon y Cajal grant) to X.I.; Projects EIPZI (Spanish Ministry of Research) and IMPRESS (Basque Country Government).

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