CSIRO PUBLISHING

www.publish.csiro.au/journals/mfr Marine and Freshwater Research, 2005, 56, 69–83

Plankton succession and assemblage structure in two neighbouringlittoral ecosystems in the north-west Mediterranean Sea

J.-L. JametA,C, N. JeanB, G. BogéA, S. RichardA and D. JametA

AUniversité du Sud Toulon-Var, Equipe de Biologie des Milieux Aquatiques, Laboratoire PROTEE,E. A. 3819. B. P. 20132. F-83957 La Garde cedex, France.

BInstitut National des Sciences et Techniques de la Mer, CNAM/INTECHMER Laboratoire d’Etudeset de Recherches Marines, E. A. 3202 B. P. 324. F-50103 Cherbourg cedex, France.

CCorresponding author. Email: jamet@univ-tln.fr

Abstract. We studied seasonal variations in bacterial abundance and succession in phyto- and zooplankton assem-blages (particularly small taxa) in two neighbouring shallow bays (near Toulon, Mediterranean Sea, France): LittleBay (polluted, eutrophic), and Niel Bay (less polluted, oligotrophic). In Little Bay, bacteria developed in northernspring and phytoplankton (Dinophyceae >20 µm) in late northern winter–early spring. Zooplankton levels peakedat the end of northern spring and in autumn; this community was dominated by Oithona nana. In Niel Bay, bacteriallevels peaked during northern spring and autumn. Phytoplankton (Dinophyceae, Bacillariophyceae) abundance waslow and only peaked in June. Zooplankton levels peaked in northern mid-summer. Little Bay was influenced moreby the land and by human activities than by the sea. Seasonal factors (e.g. water temperature) and sudden influences(e.g. rain and, indirectly, Mistral wind) may have modified the succession of the plankton communities in thisbay. Successions did not follow Margalef’s model and the classical scheme for zooplankton. Conversely, Niel Bayfunctioning and plankton assemblages were most influenced by the physical environment of the sea than by theland or by human activities. Successions were closely related to the classical scheme of the Mediterranean Sea.

Extra keywords: bacteria, ecology, marine ecosystem, phytoplankton, pollution, zooplankton.

Introduction

Ecological and economic interest in coastal marine ecosys-tems has increased over recent decades. As most peoplein the world live within 100 km of a bay or an estuary,these systems are probably severely modified by anthro-pogenic disturbances and inputs. Estuaries and bays aresituated between terrestrial and pelagic environments andconstitute ecotones that may be strongly affected by humanactivities, directly or indirectly, with consequences for thefunctioning of ecosystems (see Cummins et al. 2004). Suchactivities can modify the dynamic, structure and evolution ofmarine populations and/or communities, particularly plank-tonic ones, thriving in coastal systems. Such modificationsmay also mask the underlying seasonal patterns in organismabundance, biomass and diversity (Calbet et al. 2001).

NearToulon (north-west Mediterranean Sea, France), thereare several neighbouring bays that are differently affectedby anthropogenic perturbations and pollution. Zooplanktoncommunities operate differently in these proximate sub-systems that are subject to identical climatic conditions. LittleBay is characterised by a high level of pollutants and byeutrophication. Conversely, Niel Bay, located several kilo-metres east of Little Bay, is less polluted and can legitimately

be considered to be a natural site (Jamet et al. 2001; Richardand Jamet 2001; Jean et al. 2003).

The aim of this work was to study the seasonal varia-tions of bacterial abundance and succession in phyto- andzooplankton assemblages in Little Bay and Niel Bay duringa one-year period; we also measured abiotic parameters.We determined patterns of abundance and distribution ofassemblages of organisms using methods recommended byUnderwood (1996). We also tested whether the phytoplank-ton communities followed Margalef’s model (Margalef 1958,1968). According to this model, phytoplankton successionoccurs each year and represents an annual repetition ifthe environment is not heavily stressed. The phytoplanktoncommunities in the Mediterranean Sea (and other marine sys-tems) are characterised by three annual succession stagesthat drive the pioneer winter populations to a final stateby increasing the maturity of the system. Margalef’s modeldiffers from the traditional succession model proposed by theAmerican school (Cowles 1911), which ends with a climaxstage. In addition, because data on the structure of commu-nities of small zooplankton are scarce (Calbet et al. 2001;Jamet et al. 2001), we used a net with 90-µm mesh for col-lection. Our study should provide some new information

© CSIRO 2005 10.1071/MF04102 1323-1650/05/010069

70 Marine and Freshwater Research J.-L. Jamet et al.

about small copepod taxa in littoral ecosystems of theMediterranean Sea.

Materials and methods

Study sites

Little Bay is located on the north-west Mediterranean coast of France(central point: 43◦5′N 6◦0′E) (Fig. 1) and harbours a major commercialand military port.This bay is highly affected by anthropogenic inputs andis greatly affected by raw sewage from theToulon area (c. 350 000 inhab-itants), as well as maritime (French Navy and commercial) traffic. Thehydrodynamic characteristics of Little Bay were presented in Richardand Jamet (2001) (i.e. surface: 11 km2; volume: 1 × 108 ML; residencetime of seawater: c. 30–60 days). Urban runoff enters Little Bay by tworivers (Las and Eygoutier Rivers) and is particularly abundant duringrainfalls. This pollution includes suspended solids (organic compounds,hydrocarbons and heavy metals) assessed to 1800 tonnes year−1. Con-sequently, lead, mercury, zinc, copper and cadmium may reach highconcentrations in Little Bay as recorded by the ‘Réseau Nationald’Observation, RNO’ of IFREMER (1993) for the ‘mussel watch’ pro-gramme (i.e. 18.7 Pb, 1.2 Hg, 330 Zn, 19.1 Cu and 2.5 Cd mg kg−1

dry weight of mussels). High concentrations of polychlorinatedbiphenyls (PCBs) have also been recorded in mussels. Little Bay is par-ticularly affected by tributyl tin (TBT) used in the anti-fouling paints andits concentration in seawater varied between 50 and 60 ng L−1 and mayreach 237 ng L−1 (IFREMER 1993). Conversely, outside of Little Bay,TBT concentrations were much lower and ranged from 0.6 to 2.6 ng L−1

(IFREMER 1993). Sediments in Little Bay release pollutants in thewater column, leading to a deterioration of water quality. These sedi-ments are highly contaminated by hydrocarbons (300 to 1200 mg kg−1)and PCBs (31 to 228 ng g−1) (IFREMER 1993). In addition, sedi-ments contain high concentrations of heavy metals such as zinc (93to 264 µg g−1), lead (46 to 149 µg g−1) and copper (23 to 117 µg g−1)(IFREMER 1993). Previous studies (Jamet et al. 2001; Richard andJamet 2001) showed the eutrophic character of Little Bay, in contrastwith all surrounding bays (particularly Niel Bay). For example, in 1997,P-PO3−

4 and P-PT reached 1.8 and 5.7 µm respectively and N-NO−3

reached 0.05 µm. Little Bay also contains high levels of chlorophyll a(>3.0 µg L−1) (Jamet et al. 2001), showing the eutrophic character ofthis bay according to patterns in Jacques and Tréguer (1986) and toPsyllidou-Giouranovits et al. (1997). Toxic phytoplankton species suchas Alexandrium minutum and Dinophysis spp. occur in Little Bay; Posi-donia oceanica is absent (IFREMER 1993; Belin et al. 1995). Little Bayis also characterised by a high abundance of zooplankton, low zooplank-ton diversity and a single dominant species (Cyclopoida : Oithona nana)(Richard and Jamet 2001). According to IFREMER (1993), there is nosignificant risk of eutrophication and phytoplankton blooms outside of

Mediterranean Sea

LARGE BAY

Niel Bay

S2

S1

FRANCETOULON

Little Bay

0 5 Km

Grande Passe

6º00�E

43º04�N

Fig. 1. Map of the Toulon area showing the two sampling stations (S1and S2) in Little Bay and Niel Bay respectively.

Little Bay. The sampling station in this bay was named station 1 (S1,depth 10 m).

The oligotrophic (IFREMER 1993; Jamet et al. 2001) Niel Bay(10 km east of Little Bay) is located just 3 km north of PorquerollesIsland (official French Conservation Area). The hydrodynamic of thisbay is influenced by the east–west Liguro–Provençal stream, whichallows exchanges between pelagic and coastal ecosystems all year. Thisbay is very less affected by human activity (including anthropogenicinputs and pollution) than Little Bay. There is limited tourist and fishingactivity and there are large Posidonia spp. meadows. Niel Bay has lowlevels of chlorophyll a (<0.2 µg L−1) (Jamet et al. 2001) and is charac-terised by low zooplankton abundance, low dominance index and highzooplankton diversity. In addition, O. nana is rare in this bay (Jametet al. 2001). The sampling station in this bay was named station 2 (S2,depth 5 m).

Field sampling

As tides are very moderate and no significant vertical migration of plank-ton have been recorded in shallow water in Little Bay and Niel Bay(N. Jean, personal communication), and as there is relatively uniformdistribution of plankton in the bays (Jamet and Ferec-Corbel 1996; Jametet al. 2001), samples were taken at one representative station for eachbay. Samples were collected at the same time every day from September1999 to September 2000. Samples were always collected between 0800and 1100 hours. Water samples were collected at 2-m depth using a10-L Niskin (General Oceanic Inc., Miami, FL) sampling bottle forchlorophyll a, nutrients, bacteria and phytoplankton analysis.

Abiotic parameters

Daily precipitation values (mm day−1) for the whole year were obtainedfrom Météo-France (the national French weather service). At each site,temperature (± 0.1◦C) and salinity (± 0.1) of the water were measuredwith an electronic multi-parametric sensor (WTW, Wilheim, Germany)at 2-m depth. We analysed chlorophyll a (chl a ± 0.1 µg L−1) with vis-ible spectrophotometry (acetone extract; Uvikon Kontron InstrumentsLtd, Milton Keynes, UK), orthophosphate (P-PO3−

4 ± 0.1 nm) using thecolourimetric method (ammonium molybdate) and nitrate concentra-tions (N-NO−

3 ± 0.1 µm) using a Technicon II (Diamond Diagnostics,Holliston, MA) autoanalyser (cadmium reduction).

Bacteria counts and biomass

Samples were preserved in a 25% glutaraldehyde solution in high-density polyethylene bottles. Bacteria were counted by epifluorescencemicroscopy as described by Porter and Feig (1980). A seawater volumenecessary to yield 25–100 cells per field was filtered through a blackpolycarbonate isopore Nuclepore (Whatman plc, Brentford, UK) filter(mesh size 0.2 µm, 25-mm diameter). After filtration, the membranewas covered with 1 mL of DAPI (4′,6-diamidino-2-phenylindole) solu-tion (50 µg mL−1; Fluka–Aldrich–Sigma, Fallavier, France) and left tostain in the dark. After 5 to 10 min, the filter was observed in a darkroom under an epifluorescence microscope (×1000; Nikon, Champigny,France) using immersion oil. The bacteria in at least 30 fields werecounted, with at least 30 cells per field for each sample. Bacterial abun-dance is expressed as the number of bacterial cells per litre of seawater.The data were converted into biomass by applying a conversion factorof 20 fg C cell−1.

Phytoplankton counts and biomass

Only large phytoplankton cells were considered in this study (>5 µm).Samples of phytoplankton were preserved in an alkaline Lugol solu-tion (Fluka–Aldrich–Sigma). Phytoplankton were identified to specieslevel if possible and cells were counted under an inverted microscope(×400) according to Utermöhl (1958) and Lund’s ‘cell technique’(Lundet al. 1958). Phytoplankton were counted in at least 40 fields, with atleast 400 cells over all fields. At least 100 cells of the most abundant

Plankton assemblages in NW Mediterranean Sea Marine and Freshwater Research 71

species were counted. Counts were then extrapolated to provide con-centrations per litre (cells L−1). To calculate the biomass for eachspecies, we used the specific relationship between cell volume andcarbon content (Strathmann 1967) for phytoplankton. As Bacillario-phyceae possess larger vacuoles with less carbon per unit volume thanother taxonomic groups, and because the relationship between organiccarbon and cell volume depends on the species composition of thecommunity, we used different equations for each taxon: for Bacil-lariophyceae: log10 C = −0.314 + 0.712 log10 V and for Dinophyceae:log10 C = −0.460 + 0.866 log10 V, where carbon units are 10−12 g cell−1

(pg cell−1) and volume (V) units are µm3 (10−18 m3).

Zooplankton counts

A net (0.5-m mouth diameter, 2.5-m long, 90-µm mesh) equipped witha flowmeter was swept vertically (Little Bay) and obliquely (Niel Bay)through the water column. For each sample, ten consecutive sweeps weremade at the same site and pooled to collect a large number of animalsrepresentative of the assemblage.

Samples were preserved in seawater-buffered 5% formaldehyde withCaCO3. The total sample volume was adjusted to 250 mL and aliquotsfor counts were taken using a Hensen pipette. At least 250 organismswere counted per sub-sample. All organisms were identified to specieslevel, if possible. In addition, Copepoda were separated into naupliiand copepodite stages. When the abundance of species was low, and/orwhen there was doubt about a species identification that could leadingto possible errors (i.e. Acartiidae and Oncaeidae), we used the nexthigher taxonomic level to ensure that the results were not skewed whencomparing the two bays.

Biodiversity analysis

The use of a single numerical index to describe the structure and evo-lution of a community oversimplifies its real diversity. Thus, we usedthree complementary indices to define the complexity of the phyto- andzooplankton assemblages.

(1) The Shannon–Wiener Index (H′) (Shannon and Weaver 1949):

H′ = −S∑

i=1

f i × log2 fi,

where fi is the frequency of species i.

(2) The evenness (R) of the distribution of individuals between thetaxonomic groups:

R = H′/H′ maximum <=> R = H′/log2 S,

where S is the specific richness of the community.

(3) Rank–frequency diagrams (RFDs) were constructed to describe allphyto- and zooplankton samples (Frontier 1976). Rank–frequency dia-grams give a more detailed global representation than a single numericvalue.The species were ranked by decreasing abundance along the x-axisand by relative frequency along the y-axis.To improve the discriminationof the RFD, both axes were represented on a log10 scale. For phytoplank-ton, RFDs show the ecological gradient that links the pioneer communityto the final equilibrium state. The stages were empirically definedaccording to the trend of the RFD curves. In borderline cases, the curvewas analysed mathematically by use of the Curve Expert 1.3 software(Microsoft Corporation, Redmond, WA), using a second-order polyno-mial model. Rank–frequency diagrams were interpreted as describedby Frontier (1976). In stage 1 (beginning of the succession), the curve isconcave at the top left, indicating that a small number of species dom-inate. The curve then inflects and the right part becomes convex. Theabundance of rare species decreases quickly; diversity is low. As succes-sion proceeds, the convex part of the curve moves further to the right.

The common species become more numerous and regularly distributed.Diversity increases.The abundance of rare species continues to decrease.In stage 2 (maturity of the community), the curve becomes entirely con-vex. Diversity is maximal. In stage 3 (end of the succession), the trendline becomes relatively straight owing to the increased abundance of themore abundant species. The left part of the curve may be bent. Diversityis lower than during stage 2. The community becomes older.

Results

Abiotic parameters

The subsurface water temperature varied from 11.0◦C(February) to 25.1◦C (August) in Little Bay (meanvalue = 17.4◦C) and from 11.6◦C (February) to 23.6◦C(August) in Niel Bay (mean value = 17.3◦C) (Fig. 2). Salin-ity (mean values = 36.7 in Little Bay and 37.2 in Niel Bay)was low until January 2000 and high between Februaryand September 2000 in both bays (Fig. 2). Salinity wasparticularly low in October in Little Bay (29.0) owing toheavy rainfalls. Although the difference was not signif-icant, the annual mean orthophosphate and nitrate con-centrations appeared to be slightly higher in Little Bay(P-PO3−

4 = 133 nm and N-NO−3 = 9.0 µm) than in Niel Bay

(97 nm and 5.5 µm respectively) (Fig. 2). In Little Bay, theP-PO3−

4 concentration peaked in May, coincident with thedecline of the phytoplankton community. In this ecosys-tem, P-PO3−

4 and N-NO−3 concentrations were relatively

high in October, just after the period of heavy rainfall. InNiel Bay, relatively high concentrations of nutrients wereobserved at the end of autumn and at the beginning ofwinter (November to January). The chlorophyll a concen-tration was always significantly (P = 0.001, Wilcoxon test)higher in Little Bay than in Niel Bay. It ranged from 0.8 to9.0 µg L−1 (mean chl a concentration = 2.4 µg L−1) in LittleBay and from 0.1 to 1.0 µg L−1 in Niel Bay (mean chl aconcentration = 0.4 µg L−1) (Fig. 2).

Bacteria

With the exception of November, bacteria were always signifi-cantly less abundant in Niel Bay than in Little Bay (P = 0.002,Wilcoxon test).

In Little Bay, the bacterial abundance varied from1.24 × 108 cells L−1 (2.48 µg C L−1) in November to7.88 × 108 cells L−1 (15.76 µg C L−1) in April, with anannual average of 3.37 × 108 cells L−1 (2.17 × 108 s.d.) and6.74 µg C L−1 (4.33 s.d.) (Fig. 3). The succession of bacteriashowed a bimodal trend, with low levels in autumn and win-ter and high levels in spring and early summer. In the secondhalf of summer, bacterial abundance was low.

In Niel Bay, the bacterial abundance varied from9.16 × 107 cells L−1 (1.83 µg C L−1) in February to2.92 × 108 cells L−1 (5.84 µg C L−1) in April, with anannual average of 1.63 × 108 cells L−1 (0.64 × 108 s.d.) and3.26 µg C L−1 (1.27 s.d.) (Fig. 3). The seasonal variationsshowed two development periods (October and April).

72 Marine and Freshwater Research J.-L. Jamet et al.

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phyll a in Little Bay (A) and Niel Bay (B) at 2-m depth.

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Fig. 3. Seasonal variations in the abundance (Ab) and biomass (Bio) ofbacteria and of phytoplankton community and changes in zooplanktonabundance in relation with water temperature (2-m depth) in Little Bay(A) and Niel Bay (B).

Phytoplankton assemblage

In Little Bay, the development of the phytoplankton com-munity followed an unambiguous unimodal curve. Thealgal abundance and biomass clearly peaked in late winter–early spring (Fig. 3). Algal abundance peaked at 7839cells L−1 in April and biomass peaked at 2.47 µg C L−1

in March. Abundance and biomass were minimal at theend of summer (September 1999 and August 2000, 233cells L−1, 0.20 µg C L−1 and 119 cells L−1, 0.12 µg C L−1

respectively).Phytoplankton abundance and biomass were significantly

lower in Niel Bay than in Little Bay (P = 0.001, Wilcoxontest). They peaked at the end of spring (914 cells L−1 and

Plankton assemblages in NW Mediterranean Sea Marine and Freshwater Research 73

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Cylindrotheca closterium B (�20 �m)

Navicula sp.B (�20 �m)

Coscinodiscus sp.B (�20 �m)

Alexandriumminutum

D (�20 �m)

Prorocentrumarcuatum

D (�20 �m)

Ceratium furcaD (�20 �m)

Dinophysisacuminata

D (�20 �m)

Fig. 4. Seasonal variations in the abundance and biomass of the main phytoplankton species inLittle Bay (B = Bacillariophyceae, D = Dinophyceae).

0.43 µg C L−1, in June and May respectively), two monthslater than in Little Bay.

In Little Bay, Bacillariophyceae were less abundant thanDinophyceae (Fig. 4). The most common Bacillariophyceaewere the small Cyclotella spp. (<20 µm) and the largeCylindrotheca closterium, Navicula spp. and Coscinodis-cus spp. (>20 µm). Dinophyceae were dominant both interms of abundance and in biomass. The main Dinophyceaewere, in decreasing order of importance, Alexandrium spp.,

Prorocentrum arcuatum, Ceratium furca and Dinophysisacuminata (>20 µm).

In Niel Bay (Fig. 5), the dominant Bacillariophyceaespecies were Cyclotella spp., Navicula spp., Licmophora gra-cilis and Coscinodiscus spp. Dinophyceae were the dominantphytoplankton group and peaked in late spring–early summer.Nevertheless, Dinophyceae were less abundant than in LittleBay. Prorocentrum compressum and Gymnodinium spp. werethe most abundant Dinophyceae.

74 Marine and Freshwater Research J.-L. Jamet et al.

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Prorocentrum micansD (�20 �m)

ProtoperidiniumpellucidumD (�20 �m)

Fig. 5. Seasonal variations in the abundance and biomass of the main phytoplankton species in NielBay (B = Bacillariophyceae, D = Dinophyceae).

In Little Bay, the Shannon–Wiener values were high inautumn (maximum H′ = 3.18 bits cell−1 in December) andwinter (Fig. 6). The lowest diversity was recorded at thebeginning of spring (April, H′ = 1.81 bits cell−1). Diversitywas generally higher in Niel Bay than in Little Bay, exceptin November (H′ = 2.38 bits cell−1), April (H′ = 0.55 bitscell−1), June (H′ = 1.49 bits cell−1) and September 2000(H′ = 2.54 bits cell−1) (Fig. 6). Diversity then increased(excepted in July), peaking in August (H′ = 3.40 bits cell−1).In both bays, the trend of the regularity curve (R) followedthat of the diversity (H) curve (Fig. 6).

In Little Bay, the RFDs for autumn and winter wereconvex, indicating that the community was in stage 2 ofsuccession (Fig. 7). During autumn and winter, the phyto-plankton community was highly diverse, but did not reachthe mature stage 3. Several species developed during stage 2(e.g. Gymnodinium spp., Navicula spp., Coscinodiscus spp.,Chaetoceros spp., Cylindrotheca closterium, Prorocentrummicans, Ceratium furca, Cyclotella spp. and Scrippsiellatrochoidea). Stage 3 was first reached at the end of win-ter (March). At the beginning of spring (April), the curveswere concave (stage 1), showing a new succession. The latter

Plankton assemblages in NW Mediterranean Sea Marine and Freshwater Research 75

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(bits

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Phytoplanktondiversity

Zooplanktondiversity

Fig. 6. Seasonal variations in the Shannon–Wiener Index (H′) and theevenness (R) of phyto- and zooplankton assemblages in Little Bay (A)and Niel Bay (B).

reached stage 3 at the end of the summer (August). No stage 1was seen between the end of summer and the beginning ofthe autumn.

In Niel Bay (Fig. 7), stage 3 was first recorded in autumn(October). Like in Little Bay, the phytoplankton commu-nity was highly diverse (stage 2) between November andJanuary. We did not detect stage 1 beforehand. During thisperiod, several species were observed (e.g. Gymnodiniumspp., Navicula spp., Navicula delicatula, Coscinodiscus spp.,Cylindrotheca closterium and Cyclotella spp.). The concavediagrams obtained in February showed the beginning of a newstage 1 community. This period continued until May. In sum-mer, the structure of the phytoplankton community quicklychanged from a stage 1 to a final stage 3 (July). The end ofsummer and the beginning of autumn were characterised bya diverse stage 2.

Zooplankton assemblage

In Little Bay (Fig. 3), total zooplankton abundance was highlyvariable, ranging from 3675 individuals m−3 in December to129 676 individuals m−3 in June, with an average of 44 009individuals m−3 (29 904 s.d.). Copepoda (copepodites andadults) dominated the zooplankton assemblages throughout

the year and their abundance varied from 3209 individ-uals m−3 in December to 123 176 individuals m−3 in June.The cyclopoid Oithona nana was very abundant during theentire study period and was often the dominant Copepoda(and zooplankton) (except in November with 12%). Thisspecies (all stages) peaked in June (106 276 individuals m−3,82% of total zooplankton), but did not exhibit obvious season-ality. However, the seasonal variations of O. nana followedthe same basic trend as the bacteria curve (Fig. 8). Acartiidaespecies occurred all year with an average of 2285 individ-uals m−3 (2578 s.d.; maximum in May = 8161 individualsm−3). We recorded a high abundance of Euterpina acu-tifrons in September 1999 (11 005 individuals m−3). Oithonaplumifera (females) peaked in November (10 153 individualsm−3). Evadne spp. showed clear seasonality, developing atthe end of winter and beginning of spring with a peak inMarch (511 individuals m−3). Podon spp. were not clearlyseasonal and their abundance peaked in September 1999 (937individuals m−3). Mollusca larvae (Gastropoda larvae 5599individuals m−3 in April; Bivalvia larvae 3669 individualsm−3 in October) peaked in the spring and autumn. Appen-dicularia were also abundant all year round in Little Bay, witha maximum of 4375 individuals m−3 in January. Cirripedialarvae peaked in summer (400 individuals m−3 in August).The annual succession of the main taxonomic groups in LittleBay is summarised in Table 1.

In Little Bay, the development of zooplankton dependedon the water temperature (r = 0.518, P = 0.073, Spearmantest) (Fig. 3). We detected significant correlations betweenwater temperature and harpacticoids (r = 0.757, Spearmantest) and particularly with E. acutifrons (r = 0.837, P < 0.1,Spearman test). Cirripedia abundance was also correlatedwith water temperature (r = 0.716, P < 0.1, Spearman test).

In Niel Bay, total zooplankton abundance was significantlylower (Fig. 3) than in Little Bay (P = 0.001, Wilcoxon test),varying from 165 individuals m−3 (June) to 44 473 individ-uals m−3 (August) (average 6144 individuals m−3; 12 246s.d.). Zooplankton abundance was generally below 1720 indi-viduals m−3 in Niel Bay, although two other peaks wererecorded (October 11 482 individuals m−3; February 10 399individuals m−3). In October, copepod nauplii constitutedthe bulk of the zooplankton (5542 individuals m−3), togetherwith calanoid copepodites (1962 individuals m−3) and gas-tropod and polychaete larvae. In February, copepod naupliiwere dominant (36% of total abundance) followed by Oncaeaspp. (24%) and O. similis (15%). In August, two taxonomicgroups were dominant: copepod nauplii (32%) and Acarti-idae copepodites (32%). Bivalve larvae were also abundant(1011 individuals m−3). Cladocera were not very abundant.

As in Little Bay, Copepoda (copepodites and adults) dom-inated the zooplankton assemblage (between 76% in Juneand 97% in February). Copepoda were mainly representedby cyclopoids (23 to 87%). However, a higher proportion ofharpacticoids and calanoids were recorded in Niel Bay than

76 Marine and Freshwater Research J.-L. Jamet et al.

September 1999

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August 2000

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Fig. 7. Rank–frequency diagrams of the phytoplankton assemblage in Little Bay and Niel Bay. Both axes are on a logarithmic scale.

Plankton assemblages in NW Mediterranean Sea Marine and Freshwater Research 77

in Little Bay. Copepoda nauplii accounted for up to 71%of the total zooplankton community. Acartiidae copepoditesshowed an extreme peak in August (14 403 individuals m−3)and a second smaller peak in autumn. Oncaea spp. were abun-dant and exhibited clear seasonality, with peaks in autumn(October 610 individuals m−3) and winter (2540 individualsm−3). Euterpina acutrifrons occurred all year, particularly inlater summer–early autumn. Microsetella norvegica was anaccompanying species and peaked in October (689 individ-uals m−3). Unlike in Little Bay, O. nana was not dominantin Niel Bay; it was an accompanying species and developedat the end of summer and in autumn (maximum in October,503 individuals m−3 all stages considered). Oithona similiswas more abundant than O. nana and showed marked season-ality with strong development in autumn and winter (peakin February with 1888 individuals m−3). Paracalanus spp.developed essentially in autumn. The annual succession ofthe main taxonomic groups of zooplankton in Niel Bay issummarised in Table 1.

In Little Bay, diversity (H′ = 2.88 bits individuals−1,Fig. 6) was high in September 1999 (slightly curvedRFD, Fig. 9) but not in September 2000 (H′ = 1.70bits individuals−1). Diversity was maximal in Decem-ber when zooplankton were least abundant (H′ = 2.94 bitsindividuals−1). This peak in diversity was confirmed by the

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Bacteria

Fig. 8. Seasonal variations in the abundance of Oithona nana andbacteria in Little Bay.

Table 1. Succession of the main zooplankton taxonomic groups (in order of importance) in Little Bay and Niel Bay

Season Little Bay Niel Bay

Autumn Oithona nana, Euterpina acutifrons, Bivalvia larvae, Podon spp., Copepoda nauplii, Oithona spp., Oncaea spp.,Paracalanus spp., Temora stylifera Gastropoda larvae, M. norvegica

Winter Oithona nana, Copepoda nauplii, Acartiidae copepodites, Appendicularia, Copepoda nauplii, Oncaea spp., Oithona spp.Mollusca, Oithona similis, Oncaea spp., Echinodermata larvae

Spring Oithona nana, Acartiidae copepodites, Gastropoda larvae, Copepoda nauplii, Euterpina acutifrons, Mollusca,Copepoda nauplii, Evadne spp., Podon spp. Ostracoda

Summer Oithona nana, Acartiidae copepodites, Copepoda nauplii, Copepoda nauplii, Acartiidae copepodites, Mollusca,Euterpina acutifrons Euterpina acutifrons

convex curve of RFD. Diversity was lowest at the end ofspring (H′ = 1.56 bits individuals−1), as confirmed by themost concave RFD curve. At this period, the zooplanktonassemblage was dominated by copepodites of O. nana, whichrepresented 76% of the total zooplankton abundance. Insummer, diversity increased again.

Zooplankton diversity (Shannon–Wiener Index) was sig-nificantly higher in Niel Bay than in Little Bay (P = 0.022)(Fig. 6). H′ varied between 1.30 bits individuals−1 in Augustand 3.48 bits individuals−1 in September 1999. This lowestvalue was a result of the high abundance and dominance ofBivalvia. The RFD curve in August was highly concave, withan abrupt decrease before rank 0.4 (Fig. 9). The RFD curvewas convex in September 1999 when diversity was maximal,and frequencies decreased by only 1.1 ranks. In winter, zoo-plankton diversity was high, as confirmed by convex RFDcurves. In spring (April–June), the diversity of the zooplank-ton assemblage was generally low (generally concave RFDcurves).

In both bays, the trend of the curve of regularity R followedthat of diversity H′, varying between 0.42 (June) and 0.77(December) in Little Bay and between 0.41 (August) and0.82 (July) in Niel Bay (Fig. 6). The regularity was slightlyhigher in Niel Bay (annual average = 0.63, 0.12 s.d.) than inLittle Bay (annual average = 0.61, 0.10 s.d.).

Schematic representation of the evolutionof plankton assemblages

We attempted to generalise the structure and the evolution ofthe plankton assemblages in the two bays (Fig. 10a,b).

In Little Bay, bacteria developed essentially in the spring,following an increase in seawater temperature. Phytoplank-ton development was maximal in late winter–early spring,with the lowest abundance in summer; no significant develop-ment occurred in autumn.The phytoplankton assemblage wasessentially composed of large Dinophyceae (>20 µm); smallDinophyceae (<20 µm) predominated in winter. Bacillario-phyceae were rare all year round. Zooplankton developmentfollowed that of bacteria and phytoplankton. The second zoo-plankton peak in August–September was associated withbacterial development.

78 Marine and Freshwater Research J.-L. Jamet et al.

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Little BayNiel Bay

October 1999

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2

Ranks (log10)Fr

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g 10)

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November 1999

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Fig. 9. Rank–frequency diagrams of the zooplankton assemblage in Little Bay and Niel Bay. Both axes are on a logarithmic scale.

Plankton assemblages in NW Mediterranean Sea Marine and Freshwater Research 79

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(a)

(b)

Bacteria (� 10)

Fig. 10. Schema of the ecological succession of bacteria (cells mL−1 × 10), phytoplankton (cells L−1) and zooplankton (individuals m−3)assemblages in the polluted and eutrophic ecosystem Little Bay of Toulon (A) and in the less polluted and oligotrophic ecosystem Niel Bay (B).

In Niel Bay, bacterial abundance peaked in spring andautumn. Phytoplankton abundance was much lower than inLittle Bay. The development of algae was maximal in latewinter and in spring, with a second peak in autumn (Bacillar-iophyceae). Large Dinophyceae were dominant from Januaryto June; small Dinophyceae were extremely rare all year.Bacillariophyceae occurred all year round; small Bacillar-iophyceae developed in late summer–early autumn and inwinter and large Bacillariophyceae developed essentially inautumn. Zooplankton development did not follow phyto-plankton development, but seemed to be partly dependenton that of bacteria.

Discussion

This study showed that the seasonal variations of bacteriaand the successions of phyto- and zooplankton assemblagesin Little Bay and Niel Bay during a one-year period are

differently affected by anthropogenic inputs. The presentstudy also provides new data on the structure of small zoo-plankton communities. Although these communities in thetwo bays studied are geographically close, our results showthat they operate differently. The data interpretation wasseparated into four distinct catagories: abiotic parameters,bacteria, phyto- and zooplankton.

Abiotic parameters

Two rainy periods occurred during this study: the first in theautumn, with over 105 mm of rain on 19 October (12% of thetotal annual rainfall); and the second in spring, with 24 mmof rain on 16 April. Little Bay was more sensitive than NielBay to meteorological conditions, probably owing to the con-fined character of the system. In addition, trends observedwith water temperatures may vary strongly as a result of thecold north-west Mistral wind, which may blow up to more100 km h−1 during several consecutive days. Consequently,

80 Marine and Freshwater Research J.-L. Jamet et al.

water temperature and salinity were more variable in LittleBay than in Niel Bay.

The concentrations of nutrients and chlorophyll a showedLittle Bay to have a eutrophic character and Niel Bay to havean oligotrophic character. In Little Bay, the supply of nutri-ents, and consequently phytoplankton development, seem tobe partly, but directly, affected by land runoff. In addition,the release of nutrients from sediments in Little Bay alsoincreased their availability in the water column. Relativelyhigh concentrations of nutrients were sometimes observed inNiel Bay, independently of meteorological conditions.

Although Haury et al. (1978) indicated that broad-scalevariables do not always explain the majority of variationin plankton abundance and distribution, our results showedthat abiotic factors may affect the seasonality of plankton.Photoperiod seemed to have the greatest effect on Dino-phyceae growth in the both bays. Water temperature alsodrove zooplankton development in Little Bay, because, unlikeNiel Bay, phytoplankton was not limiting. The temperaturealso affected bacterial development in both sites. Nutrientswere responsible for the development of Bacillariophyceaeand seem to be the limiting factor in the development ofDinophyceae in both bays.

Bacteria

Bacteria were more abundant in Little Bay than Niel Bay,particularly in spring, when orthophosphate concentrationswere high and Dinophyceae abundance decreased.Water tem-perature may play an important role in the development ofbacteria all year round, except in summer when nutrients arelimited. The decrease observed in autumn was concomitantwith the drop in temperature. Inversely, the bacterial develop-ment observed in spring coincided with the warming of thewater. As for phytoplankton, bacteria are important for thedevelopment of zooplankton, particularly that of O. nana.

Water temperature seemed to have a greater effect onbacterial development in Niel Bay than in Little Bay. How-ever, from May to the end of the study, bacterial levels wereindependent of temperature.

Phytoplankton

Phytoplankton development in the pelagic Mediterranean Seapresents a clear succession, with a first peak at the beginningof spring and a second, smaller peak in autumn. A commonfeature of the planktonic dynamics in Mediterranean baysis the recurrence of a phytoplankton bloom in late winter(Scotto di Carlo et al. 1985). Duarte et al. (1999) showedthat this phenomenon is associated with periods of high atmo-spheric pressure and may be triggered by a combination ofdecreasing water-column stability and increasing irradiationas a result of clear skies. In addition, although the processesto explain the spatio-temporal distributions of phytoplanktoncommunities have been the aim of several studies for decades

(i.e. Turpin and Harrison 1979), linkages between eutroph-ication and phytoplankton structure are poorly understoodin coastal ecosystems (Cloern 1996). Nevertheless, accord-ing to Chrétiennot-Dinet (1998), Dinophyceae commonlydevelop in eutrophic areas and the presence of Bacillario-phyceae indicates that the phytoplankton community is in agood state.

Our results show that although the two bays studied aregeographically close, their phytoplankton assemblages oper-ate differently. Phytoplankton levels peaked in late winter–early spring in Little Bay essentially owing to the occurrenceof Dinophyceae, as observed by Pinckney et al. (1998) inthe eutrophic Neuse River Estuary in North Carolina (USA).The community in Little Bay was dominated by large Dino-phyceae all year round, but no autumnal peak was recorded.Bacillariophyceae were rare in this bay, essentially occur-ring in autumn and early winter. In autumn, this taxonomicgroup was principally composed of small cells. In winter,these cells were progressively replaced by large Bacillario-phyceae and by Dinophyceae. In summer, the densities ofBacillariophyceae and Dinophyceae were much lower. InJune, abundance was high, whereas biomass was low, indicat-ing that cells were small. Dinophyceae tended to grow slowly,but their motility and migration allowed for better survivalin stratified waters with oligotrophic upper water columns.In Niel Bay, phytoplankton abundance peaked at the end ofspring and a second peak occurred in autumn. Large Bacillar-iophyceae developed in autumn and the Dinophyceae bloomwas still present later in the year than in Little Bay. Bacil-lariophyceae bloom is predictable in the autumn in Niel Bay.However, the Dinophyceae bloom developed at the end ofwinter (i.e. earlier than predicted by the model) owing to theavailability of nutrients.

Margalef’s theory of ecological succession (1958, 1968)can be partly or totally applied to both marine (Travers 1971;Frontier 1976) and limnetic ecosystems (Amblard 1988).According to this theory, small Bacillariophyceae, whichdevelop quickly, are the first species to develop during thecold period (November to April). Bacillariophyceae tend todivide rapidly, especially in relatively turbulent and nutrient-rich waters. They are then replaced by large Bacillario-phyceae, which are in turn replaced by mobile Dinophyceae,which grow slowly during the warm period (May to October).According to Amblard (1988), the theory of ecological suc-cession formulated by Margalef (1968) and Odum (1969)can be applied to seasonal phytoplankton development onlyin the case of autogenic succession. In Little Bay, the phyto-plankton succession did not follow the classical scheme. Theseasonal periodicity of phytoplankton appears as a possibleautogenic succession (i.e. April to August), which may bebroken by allogenic perturbations that may change the direc-tion of the succession. A similar situation was observed byJacques (1968) in the Banyuls area, where the classical phy-toplankton succession is altered by external factors. In Little

Plankton assemblages in NW Mediterranean Sea Marine and Freshwater Research 81

Bay, there was no real stage 1 and the community tendedto be mature in either stage 2 or 3. The variations in spe-cific diversity were also less marked, ranging from 2 to 3bits cell−1. In this system, which appears to be highly depen-dent on external factors, large Dinophyceae (which have a‘K’ strategy of development) were predominant. Contraryto Little Bay, phytoplankton periodicity in Niel Bay closelyfollows Frontier’s theoretical model (Frontier 1976) and Mar-galef’s model and may be globally considered as an autogenicsuccession. In agreement with this theory, the phytoplanktonsuccession seemed to be more classical in Niel Bay, with amarked stage 1 between February and May. The communitystructure moved from stage 2 in June to final stage 3 at theend of winter (January). During stage 1, Bacillariophyceaewere abundant. They are considered to be a pioneer speciesand developed according to an ‘r’ strategy. During stage 2,large Dinophyceae, which present a K-type developmentalstrategy, were more abundant. A similar scheme was alsorecorded in the Gulf of Marseille (Travers 1971): successionbegins at the end of March (stage 1) with the monospecificdevelopment of the Bacillariophycea Skeletonema costatum.From April (stages 1 and 2), several other species appear(e.g. Nitzschia delicatissima, N. seriata, Lauderia borealis,Rhizosolenia fragilissima and R. imbricata). The real stage 3occurs at the end of summer (August–September), when cli-matic conditions are extreme (absence of rain, high water andair temperatures) and nutrients are limited.

In conclusion, in the confined, polluted and eutrophic Lit-tle Bay, the phytoplankton community was driven essentiallyby meteorological conditions, which control salinity and thenutrient supply. In addition, Little Bay is shallow and con-fined, with intense maritime traffic, which favours the supplyof nutrients from sediment and is more influenced by landthan by sea. Conversely, the oligotrophic and less pollutedNiel Bay was less dependent on meteorological factors and onthe supply of nutrients from sediments. Although nanophyto-plankton were sometimes present, the Little Bay communitywas dominated by large phytoplankton (Dinophyceae) allyear round. In Niel Bay, Dinophyceae were significantly lessabundant than in Little Bay and Bacillariophyceae dominatedthe phytoplankton community in autumn. These ecologicalfeatures corroborate the ‘pristine/natural’ status of Niel Bayand the ‘polluted/disturbed’ status of Little Bay.

Zooplankton

Zooplankton succession in the Mediterranean is charac-terised by a first peak in late winter (or early spring) anda second in autumn (Scotto di Carlo et al. 1985) owing tophytoplankton development. However, numerous studies inMediterranean coastal areas have recorded an increase inzooplankton in spring–summer (see Calbet et al. 2001). InGreek waters, total zooplankton abundance peaks later inthe year, between summer and early autumn (and partially

in spring) (Siokou-Frangou 1996). Conversely, several stud-ies have revealed a lack of seasonality, such as in the Gulfof Saronikos (Christou 1998). In Blanes Bay, the total zoo-plankton abundance is highly variable and lacks any clearseasonal pattern (Calbet et al. 2001). The reason why theannual zooplankton cycle in this bay does not resemble thatof other Mediterranean coastal areas is probably the inher-ent ecological characteristics and variability associated withopen coastal environments.

In this study, zooplankton abundance peaked at the end ofspring and in early autumn in Little Bay and in the middleof summer in Niel Bay. These seasonal patterns in Little Baydiffer from those observed in a previous study (Jamet et al.2001), where zooplankton abundance peaked in late winter–early spring. This non-repetitive seasonality of zooplanktonassemblage in Little Bay suggests that this ecosystem isaffected by external factors such as human activities, asobserved for phytoplankton. In Niel Bay, which is more influ-enced by sea than by land, the seasonality of zooplanktonseems to be more repetitive. In addition, in Niel Bay, contraryto Little Bay, no significant correlation was found betweenwater temperature and zooplankton abundance, suggestingthat intrinsic factors may control the development of the zoo-plankton community or other physical processes perceivedby zooplankton at small scales (Daley and Smith 1993).

Siokou-Frangou (1996) showed that Cladocera and Cope-poda developed in summer and that Copepoda were abundantand dominant in spring. These observations were corrobo-rated by Calbet et al. (2001), who found that calanoids(Clausocalanus spp., Paracalanus spp., Centropages typicus)were most abundant in winter and spring, whereas cyclopoids(Oithona spp.) and Cladocera were most abundant in summerand cyclopoids and Cladocera in autumn.

In this work, the dominant species in Little Bay wasO. nana throughout the year. However, no species was dom-inant in Niel Bay. Previous studies showed that O. nana wasdominant in Little Bay and that its abundance falls drasti-cally just outside of this polluted bay (Jamet et al. 2001;Richard and Jamet 2001). Other studies in the Mediterraneansea showed that O. nana is dominant in polluted areas (Yamazi1964; Gaudy 1971; Patriti 1984; Krsinic 1995). Lampitt andGamble (1982) indicated that this proliferation is a resultof the ability of O. nana to consume a wide range of food-particle sizes and its low metabolic rate, which may enablethis cyclopoid to maintain a high population level through-out the year. Accordingly, we found that this species wastolerant to heavy pollution. We tested several in situ hypothe-ses experimentally in our laboratory. Unpublished data fromthese laboratory experiments (Y. Di Pietri, personal com-munication) show that, in the absence of food, O. nanapopulations decreased drastically within three days and thisspecies was one of the first zooplankton species to disappear.Several other zooplankton groups (i.e. in decreasing order ofresistance: medusa larvae, Cirripedia larvae, harpacticoids,

82 Marine and Freshwater Research J.-L. Jamet et al.

calanoids) were much more resistant to a lack of food. Thissuggests that the dominance of O. nana in Little Bay is morea result of trophic determinisms than to the resistance of thiscyclopoid to pollutants. Thus, the strong development of thissmall, omnivorous species that can consume a wide rangeof food particles may be explained by the high abundanceof small plankton groups in Little Bay (IFREMER 1993),notably bacteria, as shown in this study.

In conclusion, the two bays are affected differently byanthropogenic disturbancies and have different morpholo-gies, which have consequences for hydrography and currents.It was not possible to test the real influence of currents in thisstudy. However, we believe that the trophic status and thedegree of pollution in Little Bay play important roles in thefunctioning of this system and in the succession of the com-munities. Little Bay is more influenced by the land and byhuman activities than by the sea. There is also evidence ofa seasonal pattern related to external factors (e.g. tempera-ture) and sudden influences (e.g. rain and, indirectly, Mistralwind), which modify the succession of the plankton com-munities. In Little Bay, phytoplankton succession does notfollow Margalef’s (1968) model and zooplankton successiondoes not correspond to the classical scheme of MediterraneanSea. Conversely, Niel Bay was more influenced by the phys-ical environment of the sea than by land and anthropogenicinfluences. Successions in Niel Bay were closely related tothe classical scheme of this sea.

Acknowledgments

The authors thank the Institut Universitaire de Technologie ofthe Université du Sud Toulon-Var (Director of the IUT, Prof.B. Rossetto) and the Département de Génie Biologique fortechnical support (Chief of Department, Prof. M. Camail).The authors are also indebt to Dr C. Le Poupon andJ.-M. Ginoux for their scientific advices. They also thankthe two anonymous referees for suggestions that improvedthe manuscript.

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Manuscript received 17 May 2004; revised 16 September 2004; andaccepted 25 November 2004.