gomez 2003 villefranche

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INTRODUCTION The Mediterranean Sea is an oligotrophic semi-enclosed basin with an eastward decrease in productivity (Sournia, 1973). However, the concentrations of nitrate and phos- phate are increasing (Béthoux et al., 1998a) and the cultural eutrophication due to the rising demographic impact is becoming an important ecological issue for the Mediterranean coastal zones (UNESCO, 1988; Turley, 1999), along with the effects of the climatic change on the Mediterranean ecosystem (Francour et al., 1994; Bianchi and Morri, 2000). The trophic character of Villefranche Bay varies from oligotrophic [based on chlorophyll or primary production values (Bustillos-Guzmán et al., 1995; Lacroix and Nival, 1998)] to mesotrophic [based on the nitrogen dynamics and plankton composition (Selmer et al., 1993)]. The food web is predominantly based on the microbial loop (Rassoulzadegan and Sheldon, 1986; Dolan et al., 1995; Thingstad et al., 1998). The waters are dominated by pico- and nanoplankton, mainly consisting of cyanobacteria (Synechococcus sp.), nanoflagellates (responsible for the major part of the primary production) and heterotrophic bacteria (Lins da Silva, 1991; Zweifel et al., 1993; Jacquet et al., 1998). Even during the spring and autumn maxima, the abundance of microphytoplankton is low (Hagström et al., 1988; Lins da Silva, 1991; Ferrier-Pagès and Rassoulzadegan, 1994) in comparison to the Gulf of Lions ( Jacques, 1969) and to the Gulf of Marseille (Travers, 1971) where river input and wind forcing are more important. The studied area is influenced by the Ligurian current Journal of Plankton Research 25(4), © Oxford University Press; all rights reserved Annual microplankton cycles in Villefranche Bay, Ligurian Sea, NW Mediterranean FERNANDO GÓMEZ * AND GABRIEL GORSKY 1 DEPARTMENT OF AQUATIC BIOSCIENCES, THE UNIVERSITY OF TOKYO, -- YAYOI, BUNKYO, TOKYO -, JAPAN AND 1 CNRS/UPMC, LABORATOIRE DOCÉANOGRAPHIE DE VILLEFRANCHE/MER, UMR , OBSERVATOIRE OCÉANOLOGIQUE, BP , VILLEFRANCHE-SUR-MER CEDEX, FRANCE *CORRESPONDING AUTHOR: fernando.gomez@fitoplancton.com Abundance and composition of microplankton were studied over a period of 2 years at two depths in Villefranche Bay (Ligurian Sea, NW Mediterranean Sea). Diatoms dominated the microplankton in late spring and autumn, whereas dinoflagellates composed the major part of the microplankton in summer. The silicoflagellate Dictyocha fibula and the diatom Thalassionema frauenfeldii dominated in winter. Ciliates showed low variability throughout the year with the lowest abundance in February and an increase which coincided with the diatom maxima during autumn in both years. In 1998, the spring bloom (in May) was mainly composed of dinoflagellates near the surface and of diatoms in deeper layers. Subsurface diatom maxima were observed in August–September and November. In 1999, diatoms peaked in May both at the surface and at the depth of 50 m. They showed a strong maximum in October. Dinoflagellates and tintinnids showed maxima in early November. Compari- sons with previous studies reveal that (i) changes in species composition have not been significant, (ii) the silicoflagellate’s abundance is lower during the present study, (iii) the sequential spring bloom is composed of a pico-nanoplankton bloom in March and microphytoplankton in May, whereas in other western Mediterranean areas the spring microphytoplankton bloom is reported in February and March, (iv) high water transport through the Corsica channel coinciding with low or negative winter values of North Atlantic Oscillation (NAO) index are associated with the anomalous strong develop- ment of the spring diatom blooms in the Bay of Villefranche, whereas the usual trend is the lack of or weak development of the spring diatom bloom. This feature may determine the nature and the fate of primary production and the interannual variability in the relative importance of the microbial food web versus the microbial loop. JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES

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Page 1: Gomez 2003 Villefranche

I N T RO D U C T I O N

The Mediterranean Sea is an oligotrophic semi-enclosedbasin with an eastward decrease in productivity (Sournia,1973). However, the concentrations of nitrate and phos-phate are increasing (Béthoux et al., 1998a) and thecultural eutrophication due to the rising demographicimpact is becoming an important ecological issue for theMediterranean coastal zones (UNESCO, 1988; Turley,1999), along with the effects of the climatic change on theMediterranean ecosystem (Francour et al., 1994; Bianchiand Morri, 2000).

The trophic character of Villefranche Bay varies fromoligotrophic [based on chlorophyll or primary productionvalues (Bustillos-Guzmán et al., 1995; Lacroix and Nival,1998)] to mesotrophic [based on the nitrogen dynamics

and plankton composition (Selmer et al., 1993)]. The foodweb is predominantly based on the microbial loop(Rassoulzadegan and Sheldon, 1986; Dolan et al., 1995;Thingstad et al., 1998). The waters are dominated by pico-and nanoplankton, mainly consisting of cyanobacteria(Synechococcus sp.), nanoflagellates (responsible for themajor part of the primary production) and heterotrophicbacteria (Lins da Silva, 1991; Zweifel et al., 1993; Jacquetet al., 1998). Even during the spring and autumn maxima,the abundance of microphytoplankton is low (Hagströmet al., 1988; Lins da Silva, 1991; Ferrier-Pagès andRassoulzadegan, 1994) in comparison to the Gulf ofLions ( Jacques, 1969) and to the Gulf of Marseille(Travers, 1971) where river input and wind forcing aremore important.

The studied area is influenced by the Ligurian current

Journal of Plankton Research 25(4), © Oxford University Press; all rights reserved

Annual microplankton cycles inVillefranche Bay, Ligurian Sea,NW MediterraneanFERNANDO GÓMEZ* AND GABRIEL GORSKY1

DEPARTMENT OF AQUATIC BIOSCIENCES, THE UNIVERSITY OF TOKYO, -- YAYOI, BUNKYO, TOKYO -, JAPAN AND1CNRS/UPMC, LABORATOIRE D’OCÉANOGRAPHIE DE VILLEFRANCHE/MER, UMR , OBSERVATOIRE OCÉANOLOGIQUE, BP , VILLEFRANCHE-SUR-MER CEDEX, FRANCE

*CORRESPONDING AUTHOR: [email protected]

Abundance and composition of microplankton were studied over a period of 2 years at two depths

in Villefranche Bay (Ligurian Sea, NW Mediterranean Sea). Diatoms dominated the microplankton

in late spring and autumn, whereas dinoflagellates composed the major part of the microplankton in

summer. The silicoflagellate Dictyocha fibula and the diatom Thalassionema frauenfeldii dominated

in winter. Ciliates showed low variability throughout the year with the lowest abundance in February

and an increase which coincided with the diatom maxima during autumn in both years. In 1998,

the spring bloom (in May) was mainly composed of dinoflagellates near the surface and of diatoms

in deeper layers. Subsurface diatom maxima were observed in August–September and November. In

1999, diatoms peaked in May both at the surface and at the depth of 50 m. They showed a strong

maximum in October. Dinoflagellates and tintinnids showed maxima in early November. Compari-

sons with previous studies reveal that (i) changes in species composition have not been significant,

(ii) the silicoflagellate’s abundance is lower during the present study, (iii) the sequential spring bloom

is composed of a pico-nanoplankton bloom in March and microphytoplankton in May, whereas in

other western Mediterranean areas the spring microphytoplankton bloom is reported in February and

March, (iv) high water transport through the Corsica channel coinciding with low or negative winter

values of North Atlantic Oscillation (NAO) index are associated with the anomalous strong develop-

ment of the spring diatom blooms in the Bay of Villefranche, whereas the usual trend is the lack of

or weak development of the spring diatom bloom. This feature may determine the nature and the fate

of primary production and the interannual variability in the relative importance of the microbial food

web versus the microbial loop.

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[or Northern current; sensu (Millot 1999)], characterizedby a low chlorophyll concentration (Goffart et al., 1995).This current is part of a basin-wide cyclonic circulationinvolving Modified Atlantic Water at the surface and theLevantine Intermediate Water at depth (Béthouxet al., 1988; Millot, 1999). It is formed from the mergingof two independent currents flowing northwards on bothsides of Corsica Island, the Western Corsica Current(WCC) and the Eastern Corsica Current (ECC orTyrrhenian Current).

In Villefranche Bay, the wind stress can modify thecirculation pattern (Nival and Corre, 1976). During calmperiods, the surface current circulates from the south(open sea) towards the north of the Bay and subsurfacecurrents tend to circulate southwards near the bottom.During the events of eastward wind, surface waters circu-late towards the open sea and subsurface waters areupwelled, allowing deeper waters to ascend the slope.Deeper waters reach the surface when the strong eastwardwind regime is persistent (Nival et al., 1975).

As oligotrophic areas are very sensitive to environ-mental variations, their monitoring is essential for theevaluation of the long-term changes in the communitystructure. The Bay of Villefranche, regularly sampledsince 1957 (Etienne et al., 1991), is especially interestingdue to the high number of studies performed in this areawhich facilitates comparison.

The present work focuses on (i) the comparison ofcomposition, seasonal cycle and dynamics of micro-plankton succession in 1998 and 1999 with previousstudies, and (ii) the evaluation of the relationship between

hydrographic conditions and the causes of the inter-annual variability.

M E T H O D

Study site and sampling

The Bay of Villefranche is located in the northern part ofthe Ligurian Sea (NW Mediterranean Sea, Figure 1).Sampling was performed at a permanent coastal stationcalled Point B. The station is located at the entrance ofthe Bay of Villefranche (43°41�10�N, 7°19�00�E, watercolumn depth ~80 m) which is open towards the sea andis not protected much from the wind (Nival and Corre,1976).

Conductivity–Temperature–Depth (CTD) and watersampling were performed weekly between 10 and 11 a.m.Water column profiles of temperature and salinity wererecorded with a Seabird SBE25 CTD. A stratificationindex calculated as the average density difference m–1 ofthe 0–80 m depth layer (�t units m–1) was used to char-acterize the degree of water column stability.

Phytoplankton analysis was carried out weekly duringlate spring and autumn when changes were moreapparent, and fortnightly in winter and summer. Samplesfor microplankton analysis were collected using Niskinbottles at the surface (1 m) and at 50 m depth and fixedwith acid Lugol’s solution. In the laboratory, 100 mlsubsamples were allowed to settle (48 h) in compositechambers. The entire chamber bottom was alwaysexamined using the Utermöhl technique. Organisms that

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Mediterranean Sea

Fig. 1. The NW Mediterranean Sea with an inset showing the Bay of Villefranche-sur-Mer and the sampling station Point B (43°41�10�N,7°19�00�E).

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could not be identified to the species level were assignedonly to genera, for example diatoms as Navicula or dino-flagellates as Gymnodinium, Gyrodinium or Amphidinium andsuprageneric groups such as naked ciliates. Dominanceand diversity indices were computed using taxa identifiedat species level only.

Although the counting error of the abundance estima-tions was generally lower than 20% (Lund et al., 1958), itincreased in the cases of low microplankton concentra-tions. Colonies (usually diatoms) were considered as oneunit for abundance estimations and small cells mainlybelonging to the flagellate group were not considered. Itshould be noted that these small cells deteriorate in fixedsamples and that their abundance may be underestimatedby the methodology used (Hewes et al., 1984). This canalso affect the non-loricated ciliate’s quantification(Stoecker et al., 1994).

Data analysis

The phytoplankton species diversity was estimatedaccording to Shannon’s formula (H� = –Σpi log2 pi, wherep = n1/N, n1 = number of individuals of one species andN the total number of individuals) (Margalef, 1967).Microphytoplankton species dominance was calculatedaccording to the formula � = 100 (n1 + n2)/N, where � isthe dominance index equal to the percentage of the totalstanding stock contributed by the two most importantspecies (n1 + n2) and N the total cell concentration(Hulburt, 1963).

For the statistical analyses, the data for microplanktonabundance were converted to log10(x + 1) and the wholedataset was reduced to 27 (surface) and 23 (50 m depth)microphytoplankton taxa by merging poorly representedspecies or congeneric species, which are supposed to havesimilar ecophysiological characteristics. The inclusion ofsupraspecific and heterogeneous taxa has probablyresulted in overestimated similarity values. A hierarchicalflexible cluster analysis with b = –0.3 on a Euclideanmatrix of distance (Legendre and Legendre, 1998) wasused in order to define groups of co-occurrentmicroplankton species. The statistical programPASSTEC developed at the Observatoire Océanologiqueof Villefranche was used for calculations (Ibañez andEtienne, 1998).

RESULTS

Hydrographic conditions

The average water column temperature from January toApril 1998 was 14.13°C (minimum 13.47°C) during 1998,whereas in 1999 for the corresponding period the average

temperature was 13.37°C (minimum 12.84°C). In latesummer 1999, temperature values in the surface layer wereexceptionally high (24ºC isotherm reached 27 m depth).In summer 1998, temperatures were lower and the 24ºCisotherm extended to 18 m only (Figure 2). According toRomano et al., temperatures in 1999 were the highest inthe NW Mediterranean since 1995 (Romano et al., 2000).The stratification of the water column started earlier in1998 than in 1999 (Figure 2), probably due to the lowerwinter temperatures in 1999. Mixing events, induced bywind during the stratification period, resulted in lowervalues of the stratification index.

Seasonal cycles of the main microplanktongroups

Total microplankton abundance and the main groupsconsidered (dinoflagellates, diatoms, ciliates; non-loricated ciliates and tintinnids; and silicoflagellates) at thesurface and 50 m depth are shown in Figure 3. Theaverage microphytoplankton abundance during theperiod studied was ~1 ind ml–1. In both years, the micro-phytoplankton abundance remained low from Decemberto March with a rapid increase in May, in late summer(August–September) and in October and November,when diatoms were the taxa responsible for abundancefluctuations. In 1998 the spring maximum was notobserved at the surface as usual, but only at 50 m depth.Dinoflagellates were concentrated mostly in the surfacelayer. The highest abundance was recorded in May 1998(up to 4 ind ml–1). It coincided with the deep (50 m)diatom peak. The comparison of the observed abundancebetween the surface and 50 m depth showed that dino-flagellates are mainly surface-dwelling organisms.However, the decrease in the surface abundance valueswas followed by an increase in the abundance at 50 mdepth (November–December, 1998; Figure 3). Generally,this group displayed low abundance during winter.

The annual cycle of silicoflagellates fluctuated inverselywhen compared with the annual cycle of the bulk micro-plankton, with maximal surface values in winter. Fromspring to autumn they were detected only under the ther-mocline (50 m depth). In winter 1999 their abundancewas higher than in 1998, coinciding with lower tempera-tures observed during this year.

The abundance of naked ciliates ranged between 0.2and 1 ind ml–1 throughout the year. The lowest valueswere observed in winter, especially in February. Thesurface abundance of ciliates increased during the springand during autumnal diatom maxima (more pronouncedin 1999). The distribution of tintinnids showed large fluc-tuations with some of the maxima occurring shortly aftera diatom peak (August 1998, 50 m depth; January 1999,1 m). In autumn 1999, an increase in the diatoms 50 m

F. GÓMEZ AND G. GORSKY ANNUAL MICROPLANKTON CYCLES IN NW MEDITERRANEAN SEA

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deep (early September) was followed 2 weeks later by anincreased abundance of tintinnids at the same depth.

Composition, dominance, diversity andsuccession

More than one 150 taxa (Table I), mainly composed of 25genera of dinoflagellates (80 species) and of 37 diatomgenera (65 species), were identified. The dominantbloom-forming diatoms are Dactyliosolen fragilissimus,

Leptocylindrus danicus, L. minimus, Guinardia striata andPseudo-nitzschia spp. Regarding species number, the genusChaetoceros, with nine species, is the most important,followed by Leptocylindrus (four species) and Guinardia (threespecies) (Table I). Within the dinoflagellates, the Ceratium

group with 18 species is the most important, followed bythe genus Protoperidinium (nine species), Dinophysis (sevenspecies) and Prorocentrum (six species) (Table I). In add-ition to these taxonomic groups, the silicoflagellate

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Fig. 2. Seasonal variations of the temperature and density at the mouth of the Villefranche Bay (NW Mediterranean Sea) from January 1998 toJanuary 2000. The stratification index was calculated as the average density difference m–1 of the 0–80 m depth layer each 5 m (�t units m–1). Notethe different scale of each group.

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Dictyocha fibula was the most abundant. For ciliates, wewere not able to make precise taxonomic identifications,although the observed species consisted mostly of Halteria

sp., Laboea sp., Lohmanniella sp. and Strombidium-like cells(Rassoulzadegan, 1977; Rassoulzadegan and Sheldon,1986).

The dominant phytoplankton species and dominanceindex for both years are summarized in Figure 4. Inwinter 1998, the dominant species were Thalassionema

frauenfeldii (which dominated until July at 50 m depth) andD. fibula. Both species generated the highest degree ofdominance ( January at 50 m depth). Towards thesummer, these species were progressively replaced in thesurface layer by an assemblage composed of dinoflagel-lates. In May 1998, this assemblage was composed of

F. GÓMEZ AND G. GORSKY ANNUAL MICROPLANKTON CYCLES IN NW MEDITERRANEAN SEA

Table I: Taxonomic composition of

microplankton in the Villefranche Bay

Dinoflagellates Diatoms

Amphidinium spp. Amphora spp.

Amphisolenia bidentata Schröder Asterionellopsis glacialis (Cast) Round

Asterodinium libanum Abboud-Abi Saab Asteromphalus sp.

Ceratium arietinum Cleve Asteromphalus flabellatus (Bréb) Grev

Ceratium candelabrum (Ehr) Stein Bacteriastrum delicatulum Cleve

Ceratium carriense Gourret Bacteriastrum elegans Pav

Ceratium contortum (Gourret) Cleve Bacteriastrum hyalinum Lauder

Ceratium declinatum (Karsten) Jörg Bleakeleya notata (Grun) Round

Ceratium extensum (Gourret) Cleve Cerataulina pelagica (Cleve) Hendey

Ceratium furca (Ehr) Clap et Lach Chaetoceros affinis Lauder

Ceratium fusus (Ehr) Dujardin C. compressus Lauder

Ceratium hexacanthum Gourret C. curvisetus Cleve

Ceratium horridum (Cleve) Gran C. dadayi Pavillard

C. horridum var.buceros (Zach) Sournia C. danicus Cleve

Ceratium limulus Gourret C. decipiens Cleve

Ceratium longirostrum Gourret C. densus Cleve

Ceratium macroceros (Ehr) Vanh C. didymus Ehr

Ceratium massiliense (Gourret) Karsten C. lorenzianus Grun

Ceratium pentagonum Gourret C. messanensis Castracane

Ceratium pulchellum Schröder C. peruvianus Brightwell

Ceratium setaceum Jörg C. rostratus Lauder

Ceratium symmetricum Pavillard C. tortissimus Gran

Ceratium teres Kofoid Coscinodiscus spp.

Ceratium tripos (Müller) Nitzsch Cylindrotheca closterium (Ehr) Reim and Lew

Ceratocorys armata (Schütt) Kof Dactyliosolen fragilissimus (Bergon) Hasle

Ceratocorys gourretii Paulsen Detonula pumila (Castracane) Gran

Ceratocorys horrida Stein Diploneis spp.

Cladopyxis brachiolata Stein Ditylum brightwellii (West) Grun

Cochlodinium spp. Grammatophora spp.

Corythodinium constrictum (Stein) Taylor Guinardia delicatula (Cleve) Hasle

Corythodinium elegans (Pav) Taylor Guinardia flaccida (Cast) Per

Corythodinium frenguellii (Rampi) Balech Guinardia striata (Stolt) Hasle

C. tessellatum (Stein) Loeb and Loeb III Hemiaulus hauckii Grun

Dinophysis acuminata Clap and Lach Hemiaulus sinensis Grev

Dinophysis caudata Saville-Kent Hemidiscus cuneiformis Wallich

Dinophysis cf. punctata Jörg Leptocylindrus danicus Cleve

Dinophysis sacculus Stein L. mediterraneus (Per) Hasle

Dinophysis schroederi Pav Leptocylindrus minimus Gran

Dinophysis tripos Gourret Licmophora spp.

Dinophysis spp. Melosira sp.

Erythropsidinium sp. Navicula spp.

Gonyaulax spp. Nitzschia longissima (Brév ex Kutz) Ralfs in Prich

Gonyaulax verior Sournia Odontella mobiliensis (Bailey) Grun

Gymnodinium spp. Paralia sulcata (Ehr) Cleve

Gyrodinium spp. Pleurosigma spp.

Heterodinium sp. Proboscia alata (Brightwell) Sundström

Histioneis spp. Pseudo-nitzschia delicatissima ‘complex’

Micracanthodinium sp. Pseudo-nitzschia sp. ‘Nitzschia seriata complex‘

Ornithocercus heteroporus Kofoid Pseudosolenia calcar-avis (Schultze) Sundström

Ornithocercus magnificus Stein Rhabdonema adriaticum Kütz

Oxytoxum longiceps Schiller Rhizosolenia bergonii Per

Oxytoxum milneri Murray and Whitting Rhizosolenia hebetata Bailey f. hebetata

Oxytoxum scolopax Stein Rhizosolenia hebetata f. semispina (Hensen) Gran

Phalacroma doryphorum Stein Rhizosolenia imbricata Brightwell

P. rotundatum (Clap and Lach) Kof and Mich Rhizosolenia styliformis Brightwell

Podolampas elegans Schütt Skeletonema costatum (Grev) Cleve

Podolampas palmipes Stein Striatella unipunctata (Lyngbye) Agardh

Table I: Continued

Dinoflagellates Diatoms

Podolampas spinifera Okamura Synedra spp.

Pronoctiluca spinifera (Lohm) Schiller Thalassionema frauenfeldii (Grun) Hallegraeff

Prorocentrum balticum (Lohm) Loeb III Thalassionema nitzschioides Grun ex

Mereschkowsky

Prorocentrum compressum (Bailey) Abé Thalassiosira spp.

Prorocentrum dentatum Stein Thalassiothrix longissima Cl and Grun

Prorocentrum micans Ehr

Prorocentrum rotundatum Schiller

Prorocentrum triestinum Schiller Ciliates

Protoperidinium claudicans (Paulsen) Balech Ascamphelliella sp.

P. crassipes (Kof) Balech Amphorides quadrilineata Clap and Lach

P. depressum (Bailey) Balech Climacocylis sp.

P. diabolus (Cleve) Balech Codonella spp.

P. divergens (Ehr) Balech Codonellopsis spp.

P. minusculum Pav (=Minuscula bipes Lebour) Dadayiella ganymenes Entz

P. oceanicum (vanHöffen) Balech Dictyocysta elegans Jörg

P. pellucidum (Schütt) Balech Dictyocysta spp.

P. steinii (Jörg) Balech Eutintinnus fraknoii Daday

Protoperidinium spp. Eutintinnus lusus-undae Entz

Pseliodinium vaubanii Sournia Epiplocylis spp.

Pyrocystis elegans Pav Favella sp.

Pyrocystis fusiformis Wyville-Thomp. Mesodinium rubrum Lohman

Pyrocystis lunula Schütt Rhabdonella spiralis Fol

Pyrocystis obtusa Pav Salpingella acuminata Jörg

Pyrocystis robusta Kofoid Salpingella decurtata Jörg

Scaphodinium mirabile Margalef Salpingella spp.

Scrippsiella cf. trochoidea (Stein) Balech Steenstrupiella steenstrupii Clap and Lach

ex Loeb III Stenosemella nivalis (Meun) Kof and Campb

Stenosemella ventricosa (Clap and Lach) Jörg

Tintinniosis campanula (Ehr) Dad

Other phytoplankton groups Tintinniosis radix (Imhof) Brandt

Dictyocha fibula Ehr Tintinniosis spp.

Dictyocha speculum Ehr Tintinnus inquilinus (Muller) Schrank

Halosphaera viridis Schmitz Undella claparedei Entz

Phaeocystis sp. Undella marsupialis (Brandt) Kof and Campb

Pterosperma sp. Xystonella treforti Daday

Rhizosomonas setigera (Pav) Patterson et al. Xystonellopsis cymatica Brandt

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Ceratium furca (2.4 ind ml–1) and Prorocentrum micans,followed by P. balticum, Ceratium fusus and also other typicalred tide species (Dinophysis sacculus/acuminata, Dinophysis

caudata, Mesodinium rubrum and Gonyaulax sp.). Two weeksafter this Ceratium furca/Prorocentrum micans maximum, thediversity index reached its highest value (3.7 bits ind–1) forthis year in an assemblage dominated by Gyrodinium andGonyaulax. In late spring the assemblage of Ceratium andProrocentrum was progressively replaced by smalldinoflagellates belonging to the genera Gymnodinium andGyrodinium. In early autumn the water column was dom-inated by Chaetoceros spp. Towards the winter, D. fibula andT. frauenfeldii dominated again.

In winter 1999, D. fibula was the dominant species untilApril, followed by Gymnodinium sp. and by tychoplanktonicdiatom species such as Navicula sp. and Pleurosigma sp. Inearly May, Proboscia alata and Dactyliosolen fragilissimus

bloomed at the surface. In summer C. furca and P. micans

dominated. At the end of August an assemblagecomposed of D. fragilissimus, Leptocylindrus danicus andL. minimus dominated at both depths. In September,Guinardia striata, Chaetoceros spp. and Bacteriastrum delicatulum

were the dominant species. Finally in November 1999(after the autumnal maximum), the abundance of tintin-nids (mainly Amphorides quadrilineata and Salpingella spp.)became high. They were associated with the highest valueof microphytoplankton diversity index (4.26 bits ind–1).

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Gonyaulax / Gyr.Gyrod. / GonyaulaxGymnod. / Gyrod.Gymno. / P. micansGymno. / S. trochoideaGymno. / P. micansGymno. / B. elegans

Gym. / T. frauenf.

Ch.peruvian./Gym.Ch. peruv. / T. frauenf.D. fibula / T. frauenf.Gymno./ T. frauenf.

D. fibula / Gymn.

D. fibula / Gymnodinium

D.fib./ Pleurosigma

D. fibula / Gymnodinium

P. alata / D. fragilissimusC. furca / P. micansChaetoceros sp/ Gyr.P. micans / C. furcaP. micans / C. furcaGyr. / L. danicusGym. / Gyr.C. furca / D. rotundatumL. minimus / D. fragilis.Chaetoceros sp/ G. striataT. frauenf. / Chaetoceros sp

T. frauenfeldii / D. fibulaT. frauen./ C. furcaT. frauenfeldii / P. seriataT. frauenf./ P. seriata

J

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T. frauenfeldii / D. fibula

T. frauenf/ D. brightwelli

T. frauenf/ D. fibula

D. fibula / T. frauenfeldii

D. fibula / T. frauenfeldiiD. fibula / T. frauen.T. frauen./ Cyl. closteriumT. frauenfeldii / Gymnod.T. frauenfeldii / Gymnod.T. frauenfeldii / Gymnod.D. fragil./P. seriataD. fragil./Chaeto. spGym./ T. frauenf.Gym./ T. frauenf.

Gym./ Cyl. closterium

Ch.peruvian./Gym.D. fibula/T. frauenfeld.D. fibula/T. frauen.

T. frauenf./ D. fibula

D. fibula / Navicula

D. fibula/T. frauenfeldii

D. fibula / C. tripos

D. fibula/Gymnodinium

T. frauenfeld/ D. fragilis.T. frauenf./Gyrod.L. danicus / D. fragilisimusL. danicus / T. frauenfeldiiL. minimus/Ch.curvisetusP. seriata/ BacteriastrumP. seriata/ Ch. affinisL. danicus / D. fragil.G. striata/BacteriastrumP. seriata/ L. danicus

T. frauenfeldii / D. fibulaT. frauenfeldii / D. fibula

T. frauenf./ D. fibula

0 20 40 60 80 100 %

0 20 40 60 80 100 %

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Ch. peruvian./ Gymno.

50 m depthSurface

1998

1999

80 %

Fig. 3. Abundance (ind ml–1) of total microplankton, diatoms, dinoflagellates, silicoflagellates, non-loricated ciliates and tintinnids at the surfaceand 50 m depth during 1998 and 1999 in the Bay of Villefranche.

Fig. 4. Dominance (%) index and dominant species at the surface(1 m) and 50 m depth in 1998 and 1999 in the Bay of Villefranche.

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In surface waters, spring and autumnal peaks coincidedwith the increase of the diversity index values (cf. May1998). At 50 m depth, the abundance maxima generallyoccurred following an increase of the diversity index(Figure 5).

Several groups of species can be separated in thedendrogram (Figure 6). At the surface one group iscomposed mainly of dinoflagellates. This group alsoincludes diatoms such as Hemiaulus hauckii and Bacteriastrum

elegans. Another group is composed from the mostfrequent species of bloom-forming diatoms. Two groupsappear to be clearly separated. One composed of Ceratium

furca and Prorocentrum micans is present all the year but onlywith episodic maxima from spring to autumn. Thesecond, composed of T. frauenfeldii and D. fibula, is inverselyrelated to the rest of the groups, showing the higherabundance in winter. At 50 m depth, the results aresimilar but the separation between dinoflagellates anddiatoms is less clear. Ceratium furca and P. micans appear tobe grouped with the rest of the dinoflagellates, whereasT. frauenfeldii and D. fibula are again clearly separated fromthe rest of the groups.

D I S C U S S I O N

Microphytoplankton distribution

During winter, D. fibula and non-colonial individuals ofT. frauenfeldii dominated the phytoplankton community.They are frequent components of the Mediterranean

deep flora (Kimor et al., 1987). Nival (Nival, 1965)observed a seasonal pattern of D. fibula in the Bay ofVillefranche with the highest abundance in winter. Thistendency is usual in many Mediterranean areas with ahigh development of silicoflagellates in winter, whenthey form an important fraction of the phytoplanktonpopulation (Tolomio et al., 1999). During the rest of theyear the silicoflagellates are only observed in subsurfacewaters (Travers and Travers, 1968). Our results showthat silicoflagellates reach their highest abundance whenthe winter temperature is low, as it was in 1999. In the Bayof Villefranche, Nival (Nival, 1965) reported a maximumof 5.5 silicoflagellate cells ml–1 and Rassoulzadegan(Rassoulzadegan, 1979) 1.8 cells ml–1. More recently, Linsda Silva (Lins da Silva, 1991) reported a maximum valueof 0.4 cell ml–1 in March. This abundance is similar to themaximum value observed (also in March) during thisstudy (0.45 cell ml–1). This long-term decrease insilicoflagellate abundance could be related to the progres-sive increase of water temperature in the Ligurian Seasince 1960 (Astraldi et al., 1995) and to the decrease of thewind force (Fromentin and Ibañez, 1994). At the perma-nent station Point B, Bougis and collaborators reportedtemperatures lower than 12ºC in February–March duringthe 1960s (Bougis et al., 1968). However, during this studythe temperatures were always higher than 12.8ºC.

Among the diatoms, T. frauenfeldii has been cited as themost frequent winter species in Monaco (Pavillard, 1913,1937), Banyuls (Dangeard, 1932) and in otherMediterranean areas (Friligos and Gotsis-Skretas, 1987).

F. GÓMEZ AND G. GORSKY ANNUAL MICROPLANKTON CYCLES IN NW MEDITERRANEAN SEA

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Fig. 5. Diversity (bits ind–1) and abundance of total microplankton in the Bay of Villefranche at the surface and 50 m depth in 1998 and 1999.

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Thalassionema frauenfeldii is a perennial species developingsuccessfully in winter when other diatoms are absent(Travers, 1971). The presence of quasi-perennial speciesdecreases the specific diversity index in the surface watersbetween January and March of 1998 (Figure 5).

During spring, diatom blooms were associated with atemporal transition between mixed and stratifiedconditions generated by the increase in temperature(usually in May). In summer, following the diatom peak,dinoflagellates became the dominant component of themicrophytoplankton community (Figure 4). In the NWMediterranean, according to the review by Velásquez andCruzado (Velásquez and Cruzado, 1995), diatoms anddinoflagellate species represented, respectively, 51% and36% of the total phytoplankton species. In Villefranche,our data showed that diatoms and dinoflagellate speciesrepresented, respectively, 43% and 52% of the totalspecific composition of microphytoplankton. For examplein 1973, diatoms represented 8%, while dinoflagellatescomposed 28% of the average phytoplankton biovolume(Rassoulzadegan, 1979). In the Gulf of Genova,Bernhard and Rampi (Bernhard and Rampi, 1967)reported 31% of diatoms and 48% of dinoflagellates. The

relative abundance of dinoflagellates in the NW Mediter-ranean microphytoplankton community augments fromwest eastwards.

The composition and abundance of dinoflagellates inthis study did not show significant differences fromprevious observations in the area. The most frequentspecies are Prorocentrum micans, Ceratium furca and Ceratium

fusus (Halim, 1960; Rassoulzadegan, 1979). This assem-blage is also typical in other Mediterranean areas (Reve-lante and Gilmartin, 1976). In the surface waters of theBay of Villefranche, C. fusus and P. micans were associatedwith diatom maxima and also with periods of dinoflagel-late dominance. As a consequence, the position of bothspecies in the dendrogram does not appear associatedwith the diatom or the dinoflagellate group (Figure 6).According to Halim (Halim, 1960), the dinoflagellatesreach their maximal values in summer (up to 4 ind ml–1)with peaks in May and June–July. The usual presence ofcongeneric assemblages of Ceratium (C. furca, C. fusus andC. pentagonum), Prorocentrum (P. micans, P. balticum, P. triestinum

and P. rotundatum) and Gonyaulax spp., organisms withapparently the same nutritional requirements, reveals thatthe interspecific competence is not clear. Even genera

JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒

Fig. 6. Dendrogram of the Euclidean distance between the abundant species at the surface (1 m) and 50 m depth.

1

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such as Ceratium or Prorocentrum, considered as autotrophicbecause of the presence of photosynthetic pigment(Lessard and Swift, 1986), have often shown aphagotrophic behaviour (Kimor, 1981; Stoecker et al.,1997). Dominant species in the Bay of Villefranche suchas C. fusus and C. furca are heterotrophic (Mikaelyan andZavyalova, 1999; Smalley et al., 1999). Given that theysucceed peaks of phototrophs, they may feed on theorganic matter pool.

Dinoflagellates are typically surface-dwelling organ-isms; however, the subsurface maximum observed afterthe decrease in the surface abundance could be related tothe motility of this group. Vertical migration may allowthe uptake of new nutrients in deeper waters during theperiod of surface nutrient depletion (Eppley et al., 1968;Blasco, 1978).

During the summer and after the C. furca/P. micans

peak, small dinoflagellates of the genera Gyrodinium andGymnodinium became dominant. Ibañez and Rassoul-zadegan (Ibañez and Rassoulzadegan, 1977) reportedthat Gymnodinium reaches its maximum abundancetowards mid-June. The dominance of these species innutrient-impoverished environments could be related totheir trophic versatility. Many species of Gyrodinium andGymnodinium present an unclear trophic behaviour(Novarino et al., 1997). During summer in the Bay ofVillefranche, despite the presence of some dinoflagellatespecies capable of forming red tides, this phenomenonwas not detected. It is probable that the poor nutritionalconditions prevailing in the Bay with low nitrate concen-tration (<0.3 µM; Ferrier-Pagès and Rassoulzadegan,1994) and the advection of water masses prevent thedevelopment of red tides. The abundance of dinoflagel-lates did not reach the values normally reported in redtide events ( Jacques and Sournia, 1978–79). However,episodes of massive algae proliferation, such as Chattonella,have been reported in the Bay of Villefranche duringsummer (Trégouboff, 1961).

During the stratified period in Villefranche Bay,the Ceratium–Prorocentrum assemblages developed first,followed by the Gyrodinium–Gymnodinium group. Only a fewspecies of diatoms such as Hemiaulus hauckii andPseudosolenia calcar-avis are associated with a completestratification of the water column (Margalef, 1967). Thepresence of genera such as Ornithocercus or Pyrocystis

revealed the complete development of this stage until anew environmental fluctuation (usually wind) interruptedthe succession. The presence of these large diatom anddinoflagellate species can be explained by the presence ofsymbiotic cyanobacteria (Taylor, 1982; Kimor et al.,1992).

During summer stratified conditions, strong windevents were associated with diatom (fucoxanthin) maxima

(Bustillos-Guzmán et al., 1995) and with episodic develop-ment of Dactyliosolen, Leptocylindrus and Rhizosolenia species(i.e. August 1999; Figure 2). Phytoplankton may respondto environmental changes by rapid population increasesin the superficial layer. Bustillos-Guzmán et al. (Bustillos-Guzmán et al., 1995) reported diatom maxima associatedwith wind events in August 1992. This environmentalforcing can inject nutrients into the nutrient-limitedsurface layer and generate high biomass. Experimentalstudies showed that primary production in the Bay waslimited by phosphorus in summer (Thingstad et al., 1998)and in early autumn (Berland et al., 1973; Zweifel et al.,1993). However, late summer events could overlap withthe autumnal bloom (such as in 1998).

Microzooplankton distribution

The specific seasonal distribution of naked ciliates is notdetailed in this study. Their population dynamics may bemore related to the prey (bacteria or detritus) distributionthan to the changes in the physical and nutritionalconditions.

The average abundance of naked ciliates in this studywas ~1 ind ml–1, in the range of the abundance reportedin previous studies (Rassoulzadegan and Gostan, 1976;Rassoulzadegan, 1977).

There is no clear relationship between the tintinnidabundance and the seasonal cycle (Vaqué et al., 1997),chlorophyll concentrations (Dolan et al., 1999) or watercolumn stability (Cariou et al., 1999). We reported tintin-nid maxima in December–January and November(Figure 3) after the breakdown of the thermocline(Figure 2).

Temperature-dependent distribution of differenttintinnid species has been reported in Villefranche (Posta,1963) and in other areas (Koray and Özel, 1983;Abboud-Abi Saab, 1989).

Size and abundance of available prey may also influ-ence the abundance and community structure of tintin-nids. In this study, large tintinnids such as Amphorides

quadrilineata (0.16 cell ml–1) and Salpingella sp. succeededthe microplankton maxima (after the autumnal bloom of1999). This tendency is related to the nutritional inter-dependence with several groups of phytoplankton (Kimorand Golandsky-Baras, 1981) and to the availability oflarge sized prey (Bernard and Rassoulzadegan, 1990,1993).

An increase in large ciliate (>50 µm) populations ingest-ing microplankton cells (Smetacek, 1981) is observedfollowing the nanoplankton maxima in Villefranche (Linsda Silva, 1991), peaking in May and November (Bernardand Rassoulzadegan, 1994).

The isolated peaks in the abundance of tintinnids andthe sudden appearance of predetermined species can be

F. GÓMEZ AND G. GORSKY ANNUAL MICROPLANKTON CYCLES IN NW MEDITERRANEAN SEA

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explained by the seasonal recruitment from cysts as aconsequence of a particular environmental condition(Paranjape, 1987; Kamiyama and Tsujino, 1996).

Seasonal cycles of phytoplankton

The seasonal pattern of phytoplankton in temperatecoastal areas usually shows two annual peaks, in latewinter and autumn in open coastal ecosystems, and inspring and late summer in enclosed coastal ecosystems(Cebrián and Valiela, 1999).

When compared with other Mediterranean coastalareas (Table II), it seems that the bimodal annual cycle isnot the usual trend in the Ligurian Sea and Gulf of Lions(Table III). In the coastal Gulf of Lions (Banyuls),unimodal cycles were reported with a marked maximumin January, whereas in the Gulf of Genova the maximumwas reported in September–October. In the Gulf ofLions, the phytoplankton abundance can be related to thestrong winter northerly winds that generate intensemixing processes associated with high primary production(MEDOC Group, 1970; Lefevre et al., 1997). NearBanyuls, chlorophyll peaks reached 3 µg l–1 ( Jacques,1970) and 6 µg l–1 (Ibarra, 1981). In the Gulf of Marseille,the phytoplankton is seasonally influenced by the Rhôneriver outflow plume (Leveau et al., 1990; Soto et al., 1993).Eastward, these phenomena can be less relevant and thetrophic character is gradually more oligotrophic. InVillefranche Bay, the average chlorophyll a concentration

is 0.32 µg l–1 (ranging between 0.17 and 0.64 µg l–1) andis considered within the range of oligotrophic values(Bustillos-Guzmán et al., 1995). Villefranche Bay canrepresent an intermediate position between the adjacentzones (Gulf of Lions–Gulf of Genova). The higherbiomass usually observed in autumn suggests that theseasonal cycle in Villefranche displays a transition frombimodal to unimodal annual cycles with the maximumaround October–November. At the beginning of the lastcentury, Pavillard reported the lack of the spring diatombloom in some years during his study near Monaco,whereas the autumnal maxima were more prominent.This feature surprised him after his studies on the usualspring bloom in the Gulf of Lions (Pavillard, 1937).

In Table IV, we have compiled studies on seasonalcycles performed in the Bay of Villefranche. The phyto-plankton biomass has been evaluated using different esti-mators such as chlorophyll, fluorescence, particles (usinga Coulter particle counter) and the abundance of severaltaxonomic groups.

Generally the spring bloom of phytoplankton inVillefranche develops in two phases. In March–April, afirst maximum is composed of pico-nanoplanktonicautotrophs followed by a second maximum in Maycomposed of microphytoplankton. In some cases the peakof large diatoms was not observed. Bustillos-Guzmán etal. compared the hydrographic conditions between atypical diatom bloom year [1986, in (Claustre et al., 1989)]

JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒

Table II: Some examples of phytoplankton peak periods in coastal areas of the Mediterranean Sea

Location Months of peaks Year Reference

Venice Lagoon Mar, Aug 1988–89 Tolomio et al., 1999

Saronicos Bay Mar, Oct 1967 Ignatiades, 1969

Saronicos Bay Apr, Oct 1975–1976 Ignatiades, 1984

Saronicos Bay Apr, Oct 1984–85 Siokou-Frangou, 1996

Israel coast Mar, Aug, Sep, Oct 1983 Azov, 1986

Lebanon coast Mar, Oct 1973–75 Lakkis and Novel-Lakkis, 1981

Gulf of Naples Mar, May, Oct 1955 De Angelis, 1956

Gulf of Naples May, Oct 1984–1988 Zingone et al., 1995

Castellón Coast Feb 1956–57 Herrera and Margalef, 1957

Castellón Coast Feb, Nov 1957, 1961 San Feliu and Muñoz, 1975

Castellón Coast Mar 1962 San Feliu and Muñoz, 1975

Castellón Coast Feb, Dec 1970 San Feliu and Muñoz, 1975

Catalonian Coast Mar, Nov 1966 Margalef and Castellví, 1967

Catalonian Coast Mar, Nov 1965–66 Margalef and Ballester, 1967

Catalonian Coast Mar, Oct 1978–79 Estrada,1980

Catalonian Coast Feb, Aug 1992 Mura et al., 1996

Catalonian Coast Jan, Aug 1993 Mura et al., 1996

The biomass descriptors are the chlorophyll a concentration or the phytoplankton abundance.

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and a non-typical diatom bloom year [1992, in (Bustillos-Guzmán et al., 1995)]. Air temperatures were colder in1986 than in 1992 (Fromentin and Ibañez, 1994). Bustil-los-Guzmán et al. reported that the diatom bloom in 1986occurred when the water column began to stabilize whilein 1992 this occurred prior to stabilization [late April, in(Claustre et al., 1988]. In March–April 1992 theirradiance increased when the water column was notstabilized. The authors concluded that the conditions of1992 favoured the development of nanoflagellates versusdiatoms. When the light and stabilization became optimalfor diatoms, the nutrients had already been depleted bynanoflagellates. In an oligotrophic environment thisphenomenon may generate a significant interannual vari-ability. In more eutrophic areas, nutrient concentrationscould support a regular spring diatom bloom despite thenanoflagellate population growth.

Interannual variability of micro-phytoplankton: comparison with previousstudies

The Mediterranean climate is under the continental influ-ence of Europe and Asia. The Sahara Desert and theAtlantic Ocean favour thermal anomalies and changes ofcirculation patterns (Maheras et al., 1999). The Mediter-ranean Sea is very sensitive to variations in heat or thewater budget (Béthoux et al., 1999). Changes in theeastern and western basin are frequently out of phase asa consequence of different processes that affect theclimate of the two basins (Reddaway and Bigg, 1996).

In southern Europe and the Mediterranean Sea,positive values of the North Atlantic Oscillation (NAO)are related to dry winter conditions, whereas negativeNAO years are associated with wet winters (Hurrell,1995). In the Ligurian Sea, precipitation is associated withthe increase of wind stress (Andersen and Prieur, 2000)and with a rapid increase of nutrients in the surfacewaters (Martin et al., 1989).

The variable intensity of the Corsica channel transportis correlated with the winter NAO index. Higher trans-ports are associated with negative NAO and less water istransported in the Corsica channel during positive NAOyears (Vignudelli et al., 1999). According to Astraldi et al.the long-term survey of the Corsica channel circulationprovides the first evidence of the NAO influence on theinterannual variability of the physical and biologicalprocesses in the Western Mediterranean (Astraldi et al.,1999). The Corsica channel transport that feeds theLigurian current (Northern current) presents a strongseasonality. The prominent interannual variability of theLigurian current (Le Floch, 1963; Béthoux et al., 1982;Astraldi and Gasparini, 1992; Sammari et al., 1995) mayinfluence the nature of the spring phytoplankton bloomintensity on the northern coast of the Ligurian Sea. Yearswith high transports (and low or negative winter NAOindices) are associated with a remarkable development ofthe spring diatom bloom. When the intensity of the circu-lation is lower (positive NAO index) the level of the springbloom is low (Table V). During productive years thespring bloom develops earlier (late March) than during

F. GÓMEZ AND G. GORSKY ANNUAL MICROPLANKTON CYCLES IN NW MEDITERRANEAN SEA

Table III: Phytoplankton peak periods in coastal areas of the French–Italian coast of the NW

Mediterranean Seaa

Location Months of peaks Biomass estimator Year Reference

Gulf of Lions Jan, Mar, Sep, Oct Nanoplankton volume 1937 Bernard, 1938

Gulf of Lions Feb/Sep, Oct Chlorophyll 1965–68 Jacques, 1970

Gulf of Lions Jan Chlorophyll 1973 Neveux et al., 1975

Gulf of Lions Jan Chlorophyll 1977 Ibarra, 1981

Gulf of Marseille Mar, May/Sep, Nov Phytoplankton – Travers, 1962, 1973

Monaco coast Oct–Nov Phytoplankton 1910 Pavillard, 1937

Monaco coast Nov Phytoplankton 1913 Pavillard, 1937

Monaco coast Feb, Aug, Oct Nanoplankton volume 1937 Bernard, 1938

Monaco coast Feb, Oct Chlorophyll 1965 Kane, 1967

Monaco coast May, Oct Phytoplankton 1965 Kane, 1967

Gulf of Genova Jun, Sep, Dec Microphytoplankton 1959 Bernhard and Rampi, 1967

Gulf of Genova Jun, Aug, Dec Microphytoplankton 1962 Bernhard and Rampi, 1967

Gulf of Genova Sep Microphytoplankton 1965 Bernhard et al., 1969

Gulf of Genova Oct Organic matter 1980–81 Fabiano et al., 1984

aVillefranche Bay is not included.

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the periods of lower production (May). In the EnglishChannel, Irigoien et al. reported that the proportion ofdiatoms during the phytoplankton spring bloom wassignificantly correlated with the NAO index, whereas thetotal phytoplankton carbon and the timing of the springbloom were not correlated (Irigoien et al., 2000).

During the period 1985–1987 in the Corsica channel,transport was estimated to be the highest in the last 15years, up to 2.0 Sverdrup (Astraldi et al., 1995; Vignudelliet al., 2000). During this period the winter air tempera-tures were the lowest since 1957 (Fromentin and Ibañez,1994; Santoreli et al., 1995). During the 1980s, the highestlevels of precipitation on the Mediterranean basin wererecorded between 1985 and 1987 (Boukthir and Barnier,2000). For example, in Sardinia the precipitation levelrecorded in 1985 was the highest since 1964 (Delitalaet al., 2000).

According to the model of Lacroix and Nival, based onmeteorological data from 1985, the beginning of thestratification and the development of the spring diatombloom took place at the end of March near the coast ofNice (Lacroix and Nival, 1998). Claustre et al. and Lins daSilva reported the development of an extraordinarydiatom bloom in the Bay of Villefranche in 1986(Claustre et al., 1988/1989; Lins da Silva, 1991). From astudy between 1987 and 1989, Fernex et al. pointed out

high phytoplankton abundance in late March 1987,followed by high copepod concentration, whereas during1988 and 1989 this latter sequence did not occur (Fernexet al., 1996). In the Gulf of Genova an exceptionalincrease in the zooplankton abundance was also reportedin 1987 (Licandro and Ibañez, 2000).

After the 1985–1987 period, winter transport in theCorsica channel decreased (higher values of the NAOindex) and the intensity of the spring bloom declined.

The analysis of the long-term temperature and salinityvariations in the western Mediterranean shows anincreasing trend in the deep water temperature (Béthouxet al., 1990; Francour et al., 1994; Roether et al., 1996;Krahmann and Schott, 1998). Thermal anomalies, as inlate summer of 1999 (Figure 2), are associated withunprecedented events of mass mortality of sessile inverte-brates in the western Mediterranean Sea (Perez et al.,2000; Romano et al., 2000). From the analysis of sapro-pels, the increase in the freshwater input appears to becorrelated with the increase in the abundance of diatomsin the Mediterranean Sea (Kemp et al., 1999). Thedecrease in precipitation due to the NAO (Hurrell, 1995)and the damming of rivers (Milliman, 1997) could beassociated with the progressive decrease in diatom abun-dance in the Mediterranean Sea, and conversely theincrease in nanoflagellates and dinoflagellates over

JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒

Table IV: Interannual variability of biomass peaks (using different estimators) in the Bay of Villefranche

Biomass peaks Biomass descriptor Period Reference

Apr, Aug Cyanobacteria 1986 Lins da Silva, 1991

Apr, Nov Picoflagellates 1986 Lins da Silva, 1991

May–Jun Nanoflagellates 1986 Lins da Silva, 1991

May, Aug, Sep Microphytoplankton 1986 Lins da Silva, 1991

Mar Microphytoplankton 1987 Fernex et al., 1996

Apr/Mar Cyanobacteria 1988/1989 Bernard and Rassoulzadegan, 1994

Mar, Aug Nanoplankton 1989 Bernard and Rassoulzadegan, 1994

Mar, Sep Cyanobacteria 1990 Ferrier-Pagès and Rassoulzadegan, 1994

Feb, Mar, Apr, Jun Nanophytoplankton 1990 Ferrier-Pagès and Rassoulzadegan, 1994

May Microphytoplankton 1990 Ferrier-Pagès and Rassoulzadegan, 1994

May Microphytoplankton Nov’90–Jun’91 Selmer et al., 1993

Apr, Aug, Oct Chlorophyll 1992 Bustillos-Guzmán et al., 1995

Mar, Apr, May Fluorescence Feb–Jun, 1995 Therond, 1995 (unpublished data)

May (and Mar) Particles (3–10 µm) Feb–Jun, 1995 Therond, 1995 (unpublished data)

Mar, May Fluorescence/chlorophyll Oct’95–May’96 Senior, 1996 (unpublished data)

May Particles (3–10 µm) Oct’95–May’96 Senior, 1996 (unpublished data)

Mar, May Fluorescence Jan–Jun, 1999 Mandleberg, 1999 (unpublished data)

May Particles (2–15 µm) Jan–Jun, 1999 Mandleberg, 1999 (unpublished data)

May, Aug, Nov Microphytoplankton 1998 This study

May, Sep, Nov Microphytoplankton 1999 This study

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diatoms or silicoflagellates. There is a progressive increasein nitrate and phosphate concentrations in the Mediter-ranean basin, whereas the silicate concentrations appearto be stationary (Béthoux et al., 1998a). This could haveconsequences on the decrease of the relative importanceof diatoms (Turley, 1999). The modification of the N:Siand Si:P molar ratios could induce a shift from the diatomcommunities to flagellate-dominated communities, whichdo not need silicate in their cell structures (Officer andRyther, 1980, Escaravage et al., 1996). This shift mayinfluence the community structure, favouring filterfeeding zooplankton (Fernex et al., 1996; Gorsky andFenaux, 1998; Gorsky et al., 1999) over selective feederssuch as copepods (Berggreen et al., 1988). Thus, the conse-quence of anthropogenic and climatic changes such asthe greenhouse effect and the decrease in the freshwaterinput (Rohling and Bryden, 1992; Béthoux and Gentili,1996; Béthoux et al., 1998b; Boukthir and Barnier, 2000)may contribute to a progressive change in the structure ofthe pelagic food web in the Mediterranean Sea.

AC K N OW L E D G E M E N T S

We thank S. Dallot for providing CTD data from theSOMLIT program, I. Palazzoli for technical assistanceand the skippers D. Betti and J.-Y. Carval for collectingthe samples at Point B. F.G. wishes to thank B. Gasser,P. Licandro, J. C. Molinero, M. Picheral and S. Souissi for

help during his stay at Villefranche. We thank P. Nival forhelpful comments and suggestions on the manuscript. Weacknowledge the support from the EuropeanCommission’s Marine Science and TechnologyProgramme (MAST III-EURAPP) under contractMAS3-CT98-0161. This work was undertaken in theframework of the French PNEC ART 4 program. F.G.acknowledges financial support by the Spanish Ministryof Science and Technology and by the EuropeanCommission (IBC2-CT-2001-80002).

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F. GÓMEZ AND G. GORSKY ANNUAL MICROPLANKTON CYCLES IN NW MEDITERRANEAN SEA

Table V: Spring phytoplankton bloom intensity (evaluated as high or low) Villefranche Bay compared

with the winter transport (Sverdrups = 1 � 106 m3 s–1) in the Corsica Channel reported by Astraldi

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1962 – –2.38 High Nival, 1965

1963 – –3.60 High Nival, 1965

1985 2.0 –0.63 High Lacroix and Nival, 1998

1986 1.6 0.50 High Claustre et al., 1988; Lins da Silva, 1991

1987 1.3 –0.75 High Fernex et al., 1996

1988 0.9 0.72 Low Fernex et al., 1996

1989 – 5.08 Low Fernex et al., 1996

1990 – 3.96 Low Ferrier-Pagès and Rassoulzadegan, 1994

1991 0.6 1.03 Low Selmer et al., 1993

1992 0.4 3.28 Low Bustillos-Guzmán et al., 1995

1993 0.2 2.67 – –

1994 0.8 3.03 – –

1998 1.0 0.72 Low This study

1999 – 1.70 Low This study

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Received on May 15, 2000; accepted on August 1, 2002

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