Vol. 124: 247-258.1995 1 MARINE ECOLOGY PROGRESS SERIES Mar Ecol Prog Ser l Published August 10 Specific phytoplankton signatures and their relationship to hydrographic co:nditionsin the coastal northwestern Mediterranean Sea Jose Bustillos-Guzman, Herve Claustre, Jean-Claude Marty Observatoire Oceanologique d e Villefranche, CNRS-INSU, Laboratoire d e Physique e t Chimie Marines, B.P. 08. F-06230Villefranche-sur-mer, France ABSTRACT: Between March 1992 and April 1993, a n intensive sampllng p r q g a m was carried out at a coastal station in the Northwestern Mediterranean Sea to study the relations9:p between phytoplankton distributions, as evaluated by taxonomic pigments, and the hydrographx structures of the water column. The study period covered the range of hydrographlc conditions whlct prevail in the Mediterranean Sea. The 0 to 75 m integrated chlorophyll a concent]-ation averaged 23 3 m g m 2 ,with the highest values (above 45 mg m-') restricted to semi-mixed penods. The major ph floplankton signature and water column structure r e l a t ~ o n s h ~ p s were: (1) phytoplankton~cprokaryotes (ryanobacteria and prochlorophytes] appear sensitive to water column mixing with prochlorophylc~ being the most sensitive group a s strong stratification is associated with the highest biomass found mainly in deeper waters; (2) prymnesiophytes and chrysophytes (19'-BF and 19'-HF) appear the most a b u n d a n t under a variety of conditions and therefore seem able to adapt to various water column structures; (3) diatoms bloom in semi-mixed conditions, but while these conditions a r e necessary, they a r e not sufficient for bloom formation; and ( 4 ) green chlorophyll b-containing flagellates appear to requlre sI.jsng mixing. During the stratification period, 2 noticeable wlnd-induced mixing events occurred, arc while the first d ~ d not have any marked influence on the phytoplankton community, the second was i-~llowed a subsurface by development of green flagellates and diatoms. This second wind-mixlng e v e 3 #alsoaltered the vertlcal prokaryote distribution, but 1 wk after this perturbation vert~calsegregatitm of prochlorophytes and cyanobacteria was reestablished. The results suggest that, while different ~ h ~ r ~ l p l a n ktaxa are genton erally adapted to speciflc water column structures, this is not always the case l r p e c ~ a l l y small scales at where specific lighthutrient requirements may have to be met. KEY WORDS: Cyanobacteria . Chemotaxonomy Hydrography trophic sea Pigments . Phytoplankton - Prochlorophytes HPLC kTer iterranean Sea - Oligo- INTRODUCTION For most of the world's oceans, it is recognized that phytoplankton signatures may characterize specific hydrographic conditions. For example, large species (mostly diatoms) dominate in upwelling environments while minute picophytoplankton are a common feature of the oligotrophic stratified open ocean (e.g. Chisholm 1992). Nevertheless, superimposed on a phytoplankton signature at the macroscale (regional as well as seasonal), a particular phytoplankton dynamic exists at the mesoscale (Harris 1984) which generally corresponds to changes in hydrodynamic conditions, a result, for example, of transition between different O Inter-Research 1995 Resale of full article not permitted oceanic provinces a* atmospheric forcing events. These structures i a v ~ x high carbon fixation rates by particular phytoplankton species, often diatoms, so that, although limited in time and space, these transitional structures a r e of considerable importance for fisheries and carbonbldgets at higher scales (Claustre 1994, Townsend et d 1994). Therefore, research has increasingly been 1 w ~ s e on phytoplankton dynamics d and associated bioge &chemicalproperties at the mesoscale. For spatial s t u d e s , this may concern the phytoplankton signature associated with the transition between the coastal m d the open ocean zone (Welschmeyer, 1994) as well .c$ with the effect of cross-frontal secondary circulalioa on phytoplankton community welldefined hydrographic conditions and determine if particular taxa could be associated with transitional periods between stratified and mixed conditions. N~trate samples were analyzed using a EV2 Alliance Instrument according to Treguer & Le Corre (1975). but major difficullies remain for temporal studies. These changes in the hydrological regime are hi. or by intensive sampling where a location is occupied for a sufficient time to be sure that seasonal forcing will be integrated (Harrison et al.iterranean Sea is oligotrophic (Minas & Bonin 1988). (10 min. Such constraints can be overcome for spatial studies (as soon as structures have been located from synoptic observation. Extraction was carried out under dim light conditions. 1991). 1993. resolution of chlorophyll a (chl a ) and divinyl-chlorophyll a (DV-chla) to achieve quantification. Solvent B): (0 mini 100.). Solvent A ( M e 0 H : l N aq. 1993). Gieskes & Kraay 1983. see Etienne et al. loo). moreo over. (15 min. especially those dedicated to the open oligotrophic ocean where temporal variability is the most difficult to assess. O). The present study investigated phytoplankton dynamics. ivell mixed in winter. Procedures for pigment identification and quantification have been described elsewhere (Claustre et al.Mar E d Prog Ser 124: 247-258. and a Milton Roy SM spectromonitor set up at 440 nm]. limiting their use for providing a fine temporal and spatial description of phytoplankton community d. because it is dzfficult to predict.ghly related to phyloplankton community dynamics (e. MATERIALS AND METHODS Hydrographic observations as well as pigments and nitrate measurements were conducted between March 1992 and April 1993 at a fixed coastal station of the Northwestern Mediterranean Sea (Stn B: 43" 41' 10" N and 7" 19' 00" E. 50. An aliquot (500 p1) of the clarified extract was mixed with 250 p1 of 1 M ammonium acetate solution and used to fill a 200 p1 loop of the HPLC system [CM 4000 Milton Roy Constametric Pump. Filters were ground and sonicated in 2 m1 of high performance liquid chromatograph (HPLC) grade methanol and then clarified by filtration (25 mm GF/C Whatman glass fiber filters). 10 X 0. mainly results from difficulties in conducting studies with high resolution.g.g. as evaluated by pigment biomarkers. and transition periods of stratification occur during spring (March-April) and late fall-early winter (November-December). and its hydrological regime has been extensively studied (e. 10. Water samples for nitrate and pigment analysis were collected using a Van Dorn bottle system at 0. For pigment determinations. Temporal variability can be solely assessed by opportunity (DiTullio & Laws 1991). especially at small and mesoscales.ynamics. amonium acetate. ship or satellite). Everitt et al. 1990). Bethoux & Prieur i983j. microscopy) fails to resolve the smallest organisms (e. 40. appears to be a good alternative. 1994). these methods are time-consuming. Most of the Med. 30. The RP 18 HPLC system used here provides a sufficient. although not baseline. 1993. e. Claustre & Marty 1995).g. . The pigment chemotaxonomic approach. 2 1 of seawater were filtered onto 25 mm GF/F Whatman glass fiber filters which were immediately stored at -20°C. 1988.g North Atlant~cbloom experiment. Rassoulzadegan 1979. and hydrodynamics with a high temporal (weekly or biweekly) and spatial (9 depths in a 0 to 75 m layer) resolution during a 14 mo period at a coastal station of the Ligurian Sea (Northwestern Mediterranean Sea). Lowest detection limits of DV-chl a ranged between 5 and 10 ng 1-l. 80:20) and Solvent B (MeOH:acetone. (18 mini 100. Coastal areas of the Northcvestern Mediterranean Sea are also charactenzcd by the presence of this well-defined hydrographic cycle (e. cover the whole size range of phytoplankton and can be applied Ior a large sample set (e. 1994. The water column is well stratified in summer.g. The precise aim was to identify what phytoplankton signatures could be associated with specific. Vertical profiles of temperature and density were obtained weekly or biweekly using a Seabird conductivity. 60. 5. classical phytoplankton evaluation (e. Prochlorococcus spp. and 75 m depth.g. 0. Gieskes et al. able to overcome most of these methodological constraints: carotenoids are quantitative. When dedicated to p h ~ o p l a n k t o n dynamics. as such. 20. temperature and density profiler (CTD) system. The prevailing uncertainty about the relationship between phytoplankton dynamics and hydrcdynamism at small and mesoscales.g. for site background. 1991) and. High sampling frequencies also imply. 60:40) were programmed at 1 m1 min-' on the following gradient (Solvent A. M'eeks et al. 1995 structure and primary production (Claustre et al. Nival & Corre 1976. Chlorophylls and carotenoids were detected by their absorbance at 440 nm. Harrison et al. Etienne et al. 0).46 cm 3 pm ODS Hypersil column (Societe Franqaise de Chromato colonne). Verity et al. More1 & Andre 1991). Numerous temporal studies have focused on the relationship between seasonal forcing and phyloplankton blooms (e. 1993. specifically carotenoids (Liaaen-Jensen 1979.high frequency of analysis.g. 0. 1993. loo). Verity et al. are pertinent case studies where high sampling frequencies can be developed to examine the relationship between phytoplankton dynamics and hydrological forcing. 1993) as well as on the effect of atmospheric perturbation on resulting biogeochemical properties (DiTullio & Laws 1991). 19@. Weeks et al. 1990). Table l . . . 3: Hooks et al. Gieskes et al. 1976.o 0.The estimated lutein (product of the ratio by chlorophyll b concentration) was subsequently subtracted from the zeaxanthinlutein stock to obtain the zeaxanthin strictly associated with cyanobacteria. v E g 20 30 40 (PM) $ so 60 70 0. (2) In the presence of prochlorophytes. zeaxanthin was simply estimated by subtracting prochlorophyte zeaxanthin from the whole zeaxanthin signal. mostly prymnesiophytes and chrysophytes Fig. . 1988.This procedure was facilitated by the fact that. Variations in hydrographic and nitrate (NO3) conditions at Stn B. . DV-chla: divinyl chlorophyll a. 13: Goericke & Repeta 1992 Pigment signature Fucoxanthin Peridinin 19'-BF+19'-HF ChlorophylI b Alloxanthin Zeaxanthin DV-chl a. for cyanobacteria. 4: Liaaen-Jensen 1985.1 L . 11. (2) lutein (green flagellates) and zeaxanthin coelute. 4 . . To characterize the degree of water column stability. 5: Jeffrey 1974. DV-chl b Phytoplankton group Diatoms Dinoflagellates Nanoflagellatesd Green flagellates Cryptophytes Cyanobacteria Prochlorophytes Sources 1. . . 6. Partensky et al.5 0. depending on the absence or presence of prochlorophytes. Northwestern Mediterranean Sea. spring conditions: SM2: semi-mixed period.Bustillos-Guzman et al. Then. 6). 1993). 1988.2 0. 2 . 4 5 1. M: mixed period. 1988. . 13 RESULTS Hydrographic conditions Water temperature was homogeneous with depth (13°C) at the beginning (March 1992) a n d at the e n d (December 1992 to March 1993) of the study (Fig. . 1 upper panel).0 "Chlorophyll c-containing nanoflagellates. 2 wind-driven events (data not shown. 9 June a n d 3 September) induced a mixing of the top 4 0 m layer.:Taxon-specific pigment var~ation and hydrographic structure The chemotaxonomic significance of diagnostic pigments is given in Table 1. 1993). 2. 3. see Fig. 1. 2.ll 12. 8: Jeffrey 1976. In the study area. T h s ratio was determined for each hydrographic condition (see 'Results: Hydrographic conditions'). Taxonomic pigment significance. This was achieved using the following procedure. a during the presence of prochlorophytes (DV-chl ) . The value of 0 10 . 9: Gieskes & Kraay 1983. . units m"). l : Wright & Jeffrey 1987. . ST: summer stratified period. 3. 19'-BF+ 19'-HF: 19'butanoyloxyfucoxanthm+ 19'-hexanoyloxyfucoxanthm. During stratification. . and (3) both prochlorophytes and cyanobacteria contribute to zeaxanthin.' (0 to 75 m) calculated from each 5 m data. DV-chlb: divinyl chlorophyll b. . . However.Kana & Glibert 1987. waters were stratified and surface temperature reached 26°C in July-August. Stratification index in the lower panel calculated as the average density difference m-' of the 0 to 75 m layer (o. . the slope of the regression between the chl band zeaxanthin-lutein was assumed to represent the chl b lutein-' ratio in green flagellates. Barlow et al. . SM1 and SM3: semi-mixed period. the estimation of the contribution of green flagellates using chlorophyll b (chl b) and of cyanobacteria via zeaxanthin required some deconvolution because: (1) chl b and DV-chl b coelute. (1) In the absence of prochlorophytes (no DV-chl a ) . fall-winter conditions. . 7 8 9 10. Between both periods. between March 1992 and Apnl 1993. 7: Gieskes & Kraay 1986. E l and E2: atmosphere events associated with wind forcing during the ST penod . 2: Bjornland et al. This was confirmed by the purity of zeaxanthin and DV-chl b peaks using photodlode array detection. . 1985.These ratios were determined at each sampling depth in order to take into consideration the light dependency of such criteria in prochlorophytes (Goericke & Repeta 1993. . .6 1 . 6: Arpin et al. a multiple regression analysis of the concentrations of DV-chl a vs [zeaxanthin + lutein] and [DV-chlb + chl b] was performed a n d the resulting constants were assumed to represent DV-Chl a zeaxanthin-' and DV-chl a DV-chl b-' ratios in prochlorophytes (e. 10: Guillard et al. . density is n~ostly temperature-driven so that isopycnal contours (data not shown) match temperature.green flagellates (chl b) were absent (except in 1 case. . 1992.g. 12: Chisholm et al. a stratification index was computed (Peterson & Bellantoni 1987) as the difference of density m . alloxanthin ?* Y. . * . . .. . Chlb .. .2 mg m-2.. In contrast. On average... 2 mg m-'. while the lowafter ST).*?.** -. Uppermost part of figure refers to tions but associated with the E2 event (from stratification conditions as defined in Fig. L.tions with divinyl chlorophyll a reaching valbutanoyloxyfucoxanthin. SM3 El E2 - - - - (Fig. . for the mixed winter conditions. In the top 2 to 10 mg m . ... . DV-Chla: divinyl chlorophyll a ues up to 6 mg m . h J m ... The integrated chlorophyll a concentration varies between 13 a n d 48 mg m-2. .250 Mar Ecol Prog Ser 124: 247-2518.. . 2. * *r . f':. . * .. . . chlorophyll a increase was mainly d u e to a diatom bloom with a particularly high value of fucoxanthin (18 mg m-*). > - - : . . nitrate levels higher than 0. Integrated pigments variation fucoxanthin peridinin 1 . 19'-HF+19'-BF: 19'-hexanoyloxyfucoxanthin+19'. - . . * .1 pM were always recorded. nitrate concentrations were constant with depth and above (1 PM) while for semi-mixed conditions nitrate concentrations were still homogeneous but always below 0. .*\ .Prochlorophytes were exclupanel the dashed line (March to April 1992) represents the chlorophyll a sively with such stratified variation as measured by spectrophotometry (Charra R. ..-.. \ . 1995 ---. -. Superimposed on these recorded during SM1 and the lowest during ST Alloxconditions. # .2 (average value of 1 . a mixed period (hereafter M) and 3 semiest cyanobacteria values are associated with mixed mixed periods (SM1 and SM3 for spring conditions and conditions. this pigment was below the detection limit for other periods (Fig. Variations in 0 to 75 m integrated pigment concentration at Stn B were also recorded during stratified condibetween March 1992 and April 1993. I The temporal variations of the 0 to 75 m integrated concentrations of taxonomic pigments are shown in Fig. unpubl.5 yM. respectively) than m-' for SM1 mixed conditions (34 and 32 m g for stratified (20 m g m-2) or mived (22 mg m-2) conditions (Table 2). *? & .... L .2 ) .on 25 November. -.. 1 middle panel).. nitrates were always centration was always below 1.. .*. data) to ffl unsampled period.. . 1 (stratiflcation index). 10. namely centration was recorded for the SM3 (up to 3 mg m-2) (Fig.. 2 and this index permits definition of specific periods associTable 2).. (.e. Below the 14°C isotherm.. .. i.. SMl ST SM2 M W .. - 3. higher chlorophyll a levels (t-test.. Table 2). recorded for SM1 and SM2 conditions. . .. the . :\:*~:: *t - 19'-HFt19'-BF _ X.. p < 0. f - m 'E 4 :I 1 1 0 M zeaxanthin ?W . a. S ..1 PM in the upper 50 m . Highest values in chlorophyll b were SM2 for fall-winter conditions). 8 DV-Chla :*v . with the erosion of the thermocline. - Chla " E € m 205 . . . C. The highest cyanobacteria zeaxanthin conated with defined hydrological characteristics. For the 2 semi-mixed conditions.: . * € 15 m10 E 5 0 201 0 25 5.\. . high pigment concentrations levels were not associated with the same phytoplankton populations. except during the 2 The relative contribution of the different groups to incursions associated with the E l a n d E2 mixing events the total chlorophyll a (chlorophyll a + divinyl chloro. . . Rapid change in fucoxanthin concentrations Fig..while for SM2. -\ . 2. $- f E 30 .. -r l A M J A O . . Peridinin conUnder stratified conditions. below 0. --#W . .. a n d Table 2 summarizes the average values for the previously defined periods. 4-d&&k.f ~ B < . 1 bottom panel): a summer stratified period (hereand at the end of SMl/beginning of ST.\ . . \\ \ . When stratification began (SM1 and SM3) increases of chlorophyll a were associated with increases in phytoplankton containing 19'-BF and 19'-HF. .~*-I . ..01) were recorded for semia n d SM3. the atmospheric events associated with anthin integrated concentrations were very low wind forcing during the ST period a r e referred to a s E l throughout but the highest average values were and E2. . 6 0. according to Barlow et al.4 10.5 0.0) phyll a) was evaluated using a multiple correlation analysis. the constant values. Comparison between temporal variation of measured (continuous line) and reconstructed (dashed line.6) (0. but their contribution during the ST period was also highly variable and represented up to 40% of the chlorophyll a in some cases.9) (0.0 (5.5) (1. Standard deviation in parentheses. 1988). the agreement between measured and reconstructed chlorophyll a + &vinyl chlorophyll a is good (Fig.8 1.8) (0.7 (8. where highest integrated concentration were recorded 148 mg m-2.0 3. I ] Mixed SM l SM2 n=lO n 6 n =6 Stratified n = 38 20.0) (1.0) 34.0-22 0 0.5 0. since they did not contribute significantly to the autotrophic biomass) allowed us to refine the general trends described above (Fig.0 1.1) (0.0 4. Nano-sized flagellates (green flagellates.0 (7.4) (0.3) (0.5-9.2-2. 3. 1990).0 6.4) 13.05 119'-BF+ 19'-HF] + 1. . which allows a more accurate estimate of the contribution of various taxa to total chlorophyll a (Fig.0 0.0) 0. the maxima (800 ng l-l) was deeper (40 m ) .0 3. 3).0 (0. pryrnnesiophytes.0 0.0-1.7) (1. which represent the ratio of diagnostic pigment to chlorophyll a.0 0.0 0. These ratios are in the range given by Barlow et al. Lowest chlorophyll a concentrations (below 200 ng I-') were recorded below 60 m all year around and during the M period over the whole water column.0 (4.1) (3.0) 15.0 0.3 6. 1 in 'Results .1) (2.2 0. Diatoms represented o n average more than 40% of the total chlorophyll a (and up to 70%) in the semi-mixed conditions (SM2).0 7.2) (0.0 3.5) (0.6 0. (1993). 4 and Table 3).0) (1.0 3.5 Hydrographic conditions (defined in Fig. 1994) and cyanobacteria (Kana et al.0) (0.01). Nanoflagellates which contain 19'-BF and 19'-HF were the dominant contributor in this nano-size fraction.4 (0. Using such a procedure.2) (3. and their contribution as high as 20 % of the overall chlorophyll a.0) (2. 5).0) (1. chrysophytes and cryptophytes) were ubiquitous throughout the study and contributed between 46 and 80 '30 of the total chlorophyll a.0 1.1) (0.0) 3.6) (0.7 0.0 2.Hydrographic conditions') total autotrophlc biomass (chlorophyll a + divinyl chlorophyll a ) at Stn B between March 1992 and April 1993 Vertical distribution data for chlorophyll a and other taxonomic pigments (except alloxanthin and peridinin.0 (4.0 (1.83 [zeaxanthin] + [divinyl chlorophyll a 1.3 3.84 [fucoxanthin] + 3.82. p <0.4 14. cryptophytes (Claustre et al. (1990) using an iterative procedure for the western equatorial Pacific.5 0.8) 4.0 0.4 10.0-48.5) 2.7) (0.0 4.0) 32.0-5.0 0.0 0.4) (0.0-10.24 [chlorophyll b] + 1.8 0. In this equation.0 (0.0 0.5) (0.Bustillos-Guzman et al.measured A I Vertical distribution Fig.6) 1. between the diagnostic integrated pigment concentration and chlorophyll a (the divinyl chlorophyll a was only added to the final equation): [Chlorophyll a + divinyl chlorophyll a] = 2.7 (0. (1993) for a similar analysis in the north Atlantic Ocean and by Everitt et al.34 [alloxanthin] + 2. (r2= 0.0 0. A I .6) 22.since in a preliminary similar analysis (results not shown) the constant values were unrealistic. Prochlorophytes were the third most important group when stratification was maximal.2) (0. The other peak chlorophyll a concentration (up to 600 ng 1-' at 10 m) was associated with the second E2 mixing event.86 + 1.0) 28.0 (0.2 - SM3 n-6 Chlorophyll a Fucoxanthin Peridinin 19'-BF+19'-HF Chlorophyll b Alloxanthin Zeaxanthin DV-Chl a (5. the chlorophyll maxima were generally associated with the top 20 m while for SM2 conditions.3 8.0 1.6) (5.2) (0.8) (3.4) (3 5) (2 8) (0. Mean integrated pigment concentration (mg m-2) for the whole period studied and for each hydrographic condition.2) (0.25 [peridinin] + 0.8 0.0-10.0 (11.9) (2.1) (6.0 0. Fig. For SM1 and SM3 conditions.0 3.0 0. 3).3) 0. E q . have been constrained for dinoflagellates (Everitt et al. Taxon-specific pigment var~ation and hydrographlc structure Table 2. n: sample number. DV-Chla: divinyl chlorophyll a Plgments Whole period n = 66 Mean Range 23.9) (0. 19'-BF+19'-HF: 19'-butanoyloxyfucoxanthin+l9'-hexanoyloxyfucoxanthln.1) (0. 5 that mixed conditions were not associated with the development of these dinoflagellates prokaryotic phytoplankton. 1995 Table 3 Phytoplanktonic group 'ontribution ("A) to total autotrophic biomass (chlorophyll a + divinyl chlorophyll a ) as determined by the taxonomic p ~ g m e n lconcentration and Eq ( l ) 'Results .0-21. 1) Mixed SMl SM2 n = l0 n=6 n=6 SM3 n=6 Diatoms Dinoflagellates Nanoflagellates Green flagellates Cryptophytes Cyanobacteria Prochlorophytes Fucoxanthin maximum abundance was recorded between 20 and 50 m depth.Mar Ecol Prog Ser 124: 247-258. Nevertheless.0 0.0-8.0-18. The deep winter mixing brings up new nutrients into the upper layers. 6) clearly shows that they have complementary distributions in the water column: cyanobacteria are restricted to the upper layers (generally above 40 m) with maximal values in SM2 M % the top 10 m." c 5 0 Fig.2) (5.0 15. which modifies phytoplankton community dynamics and presumably has implications for the food chain structure. and particularly during summer stratification.0 2.3) (2.0 3. Fig. 4.6) (12.-----at depth with the highest d~vinyl chlorophyll a concentration below 30 m.0-75.0 4. We were able to follow and to associate phytoplankton dynamics to overall seasonal changes in environmental conditions.0 Stratified n = 38 Hydrographic conditions (defined in Fig.0-8. Moreover. for such oligotrophic conditions. This surface layer becomes stabilized during spring and summer and is characterized by a well-established pycnocline which constitutes a strong barrier to nutrient replenishment of surface layers.3) (4. while prochlorophytes dominate --. Green flagellates were more abundant (up to 230 ng 1-') during the S M 1 and M periods and also during the wind-driven perturbations (Fig. Contribution (as X ) of the d~fferentphytoplankton groups to the total autotrophic biomass (chlorophyll a + divinyl chlorophyll a ) at Stn B between March 1992 and April 1993.Hydrographic cond~tions' Standard devidtion in parenthesis n: sample number Group Whole period n = 66 Mean Range 26. DISCUSSION P m c 0 o A 60 40 nanoflagellates S v. although coastal.0 14 0 9. it is clear from Fig. is a good model of the succession of hydrological conditions that may prevail in the Northwestern part of the Mediterranean Sea (Gostan 1967).0 (11. Maximum values of 19'-BF and 19'-HF were observed in the top 40 to 50 m layer ( u p to 400-500 ng I-') durlng SM1 and S M 2 and below 40 m during ST (up to 200 ng I-') and follow- --- SMl ST El 1 E2 I lng E2. 6 ) .0 0. . 1 (stratification Index) The study site. Uppermost part of figure refers to stratification condit~onsas defined In Fig.0) (1.0 45. Depth distribution of the prokaryote pigment zeaxanthin (cyanobacteria) and divinyl chlorophyll a (prochlorophytes.0-70.5) 12.0-33.0 3. except for mixed conditions and for the bloom during SM2 where diatoms occupied the whole water column. The sampling strategy we used.1) (9.0 0. 20 0 25 20 15 10 cyanobacteria 0 .0 0. wind-driven events may disrupt this stabilization and allow injection of significant new nutrients in the surface layers. Claustre et al. These conditions offer the best compromise between light and nutrient availability because the associated . Li et al. 5 Vert~cal distribution of chlorophyll a (Chl a ) . Therefore. variation coefficient = 34 %). 1992). Ondrusek et al. Claustre 1994). in deep mixed layers. The recorded average chl a + DV-Chla (24 mg m-2) is well within the range of those zones considered as oligotrophic (e. shows that the system displays a wide range of trophic conditions which are principally linked to hydrodynamics. Uppermost part of figure refers to stratification conditions as defined in Fig. diatoms do not dominate. 6. 1991. 1 (stratification index) Fig. Uppermost part of figure refers to stratification conditions as defined in Fig. Packard & Dortch 1975. the variability of this autotrophic biomass concentration (range = 13 to 48 mg chl a + DV-chl a m-'. Vertical distribution of chlorophyll b (Chl b ) . 1994). evidence also suggests that. are a likely contributor to new production in the open ocean (Goldman 1993. fucoxanthin and 19'-hexanoyloxyfucoxanthn t 19'-butanoyloxyfucoxanthin (19'-HF+19'-BF) concentration at Stn B between March 1992 and April 1993. 1 (stratification index) which is a pnori impossible to set up for open ocean waters. allowed us to investigate in detail the close linkage between hydrodynamic and phytoplankton dynamics and. probably as a consequence of limited photoadaptational ability. as well as the change in phytoplankton community structure. allowed us to evaluate the time necessary for the system to become stable again.zeaxanthin and divinyl chlorophyll a (DV-Chl a ) concentration at Stn B between March 1992 and April 1993. However.Nevertheless.: Taxon-specific pigment variation and hydrographic structure 253 1:: (ng I-') 1 !! J A S O N D 1992 Fig. most of the diatom bloom records are generally restricted to the spatio-temporal transition between mixed and stratified conditions (Kiorboe 1993. Diatoms are recognized as the most opportunistic species as far as taking advantage of nutrient availability is concerned (Fogg 1991) and as such.Bustillos-Guzman et al. Let us examine in detail the phytoplankton signature of typical hydrological situations. in particular.g. Dortch & Packard 1989. Barlow et al. One of the surpnses of this investigation was the lack of the classical spring diatom bloom generally associated with the beginning of water stabilization in the Fig. (1989) Mediterranean Sea (Claustre et al. the phytoplankton biomass which is characterized by 19'-BF and 19'-HF shows the lowest quantitative variation. 2 & 4).'). and (3) their ability to 'bloom' in specific conditions. 1991) and the 1992 spnng where no dlatom bloom occurred. when light (and stabilization) became optimal for diatom development. Temporally. 1993) which contain 19'-BF as their main marker suggest that nano. such events correspond to the large phytoplankton new production scheme of Goldman (1993). Therefore. 1990.254 Mar Ecol Prog Ser 1 turbulence appears to be a prerequisite for nutrient uptake and floatability in such generally large cells (review in Fogg 1991. 2 ) . nutrients were at this time depleted or at low levels. 1994). but the recent description of new classes like pelagophytes (Andersen et al. Figs.1 pM nitrate level reached 30 m) and the water was stable enough (Fig. and. and phytoplankton was dominated by nano-sized taxa with the highest contribution recorded in this study (85% on 9 June. More1 & Andre 1991). The pigments 19'-HF and 19'-BF have been reported for most oceanic conditions (Gieskes & Kraay 1986.and certainly pico-eukaryotic fractions are not very well known. However. other diatom increases in this study were observed during the stratified period and were restricted to a limlted band in the water column. 1993). The relative ubiquity and stability of this group. 1) for diatoms to use such a nutrient pulse. This difference seems to be important for the bloom-forming species. 1988. 1992.No remarkable chlorophyll a increase was recorded at this time (Flg. unlts m-'). 5). Comparison between environmental conditions for the 1986 spring diatom bloom (data from Etienne et al. most of the new production may be due to temporally and spatially (vertical) limited diatom blooms. the surface waters were replenished with nutrients (the 0. 7. Nanoflagellates containing 19'-BF and 19'-HF are the largest contributor to chlorophyll a (all period mean = 45 %) in this study. 1 fucoxanthin bloom was associated with such a temporal transition between stratified and mixed conditions (SM2. Superimposed on this ubiquity. 1991). Fig. Everitt et al. Gieskes et al. Light penetration may be critical in spring bloom formation (Townsend et al. (2) the relative stability of thelr pigment concentration over large scales. Williams & Claustre 1991. 4). The general distribution of this group is remarkable with respect to 3 main aspects: (1) their ubiquity. the highest fucoxanthin concentrations of this study (up to 800 ng 1-') were recorded between 5 and 10 m (Fig. the low Light regime may have prevailed for a longer time (by mixing). during this transition period. When 1992 hydrographic conditions are compared to that of a typical diatom bloom year (1986) at the same location (Etienne et al. therefore. Such conditions can be better exploited by nano-sized flagellates (see below). whatever the water masses are. Particularly during the second wind-driven event (E2.the diatom bloom occurred just before the water column abruptly stabilized and coincided with an increase of irradiance (Fig. but in this study.This stability has also been described spatially. irradiance increase may have occurred when the water column was not stable enough. and it was matched by a shift of phosphate uptake dominance from the 1 to 5 mm to the > l 0 pm fraction in a separate study (Dolan et al. ( B ) Strat~ficationindex (a. Following the wind event. Fig. chrysophytes and prymnesiophytes are the most wellknown phytoplankton classes with 19'-BF and 19'-HF. 1995). Kiarboe 1993). who suggested that. Further work is required on taxonomy and physiology . 7). in stratified oligotrophic ocean. The horizontal line in (B) shows bloom period according to Claustre et al. In fact. Density conditions in 1992 were slightly stronger and irradiance increased earlier (March-April). may result either from a large adaptability of this phytoplankton group or from a large diversity of species. ( A ) Irradiance (Eln m-' d. 5 ) . Table 3). Chisholm 1992. since 19'-HF and 19'-BF have been reported to be the most stable taxonomic markers over a large range of trophlc conditions in the Atlantic (Claustre 1994)and over a cross frontal section (Claustre et al. 1989. confirming the advantage of diatoms under these conditions. It has also been suggested that periodic diatom development occurs during the stratification in the Spanish Mediterranean coastal waters (Latasa et al. During the period studied. 1994). 1992). this clearly appears in the present data where the flagellate markers present the lowest variability over an 1 yr study (variation coefficient = 38%. Campbell & Vaulot 1993). In contrast. the differences 80 80 between cyanobacteria and prochlorophyte disBEFORE E2 DURING E2 AFTER E2 tribution are evident at 2 levels: (1) ~ r o c h l o r o Fig. bloom situation (Barlow e t al. In this study. High biomasses of flageltions in the open ocean (Chisholm et al. Claustre & Marty 1995) carried out by grazers (more likely from the microbial may be d u e to their ability to b e photosynthetically loop) with growth rates that respond over the same competent in high light intensities (Kana & Glibert time scale as the autotrophic groups themselves (e. Nevertheless. during (B and fied waters while c ~ a n o b a c t e r i a maximum E) and after (C and F) the hydrographic perturbation E2 (see Fig.and nano-phytoplankton standing 10 18 26 10 18 26 10 18 26 stocks. This has been particularly demonstrated domain (phycobilins. 1990. Ong et al. Figs. generally recorded for diatom blooms. on a smaller scale. some depth. 8. 1994).. 1987) or to their ability to absorb photons in the green Banse 1992).and nano-sized plankton domain is probably 1986. This observation is in agreement with now nutional periods between mixed a n d stratified conditions merous records of prochlorophytes for stratified condi(SM1 and SM3. these 'elevated' biomasses never reached those Welschrneyer 1993). 1993).g. Vaulot et al. increased cyanobacteria conincreasing evidence that the biomass control in the centrations in surface layers (Campbell & Carpenter pico. Gieskes & Kraay 1986. the presence (at and below the nitracline) in the stratified tropical of prochlorophytes (at low abundance) has also been reoligotrophic ocean (Claustre & Marty 1995). a transitional situlike winter mixed conditions in the Mediterranean Sea or ation (Claustre et al. Chlorophyll b is the main auxiliary photosynthetic pigment of this group 0 50 100 0 50 100 0 50 100 and it could be responsible for the predomi0 nance of green flagellates at low light levels because its absorption characteristics permit the absorption in the blue-violet spectrum (Glover in et al. for typical for the area studied (Bernard 1991) and it is likely that grazers control the increase of Temperature ("C) the pico. Chlorophyll b-containing flagellates repreE sented the third most important group that conO T tributes to total chlorophyll a and were associ40 ated with mixed conditions. 1990.g. copepods) and diatoms. Kilarboe 1993). allow diatoms to bloom (e. and they considered it as 'typical' of such transition conditions. this stateria accumulated in surface layers. Chl a ) and cyanobacteria zeaxanthin before (A and D). Goericke & less. 1986). Taxon-specific pigment variation and hydrographic structure 255 of this group in order to better understand their SM3 or at the beginning of stratification. 1988. But. Typ~cal depth profiles of temperature. (1994) showed that a high blomass of flagellates (green and chloro5 40 DV-Chla phyll c-containing) was present in the transient situations of the Almerian-Oran front (Mediterranean Sea) associated with nutrient enrichment.6). or even at specific depths semi-mixed conditions in the Sargasso Sea.) growth (Andre 1990). prochlorophytes at bility of flagellate biomass is not always the rule. (2) Cyanobacdynamics. 4 & 5 ) . During this last period 1 I the populations could be continuously mixed far 80 80 80 from the euphotic zone so light could limit their Pigment concentration (ng I .Claustre et al. . This group also g responded to mixing events as evidenced by increases in chlorophyll b concentrations during I the mixed period (Fig. But in special cases. the time lag between the development of micro-sized cell grazers (i. Neveux et lates have also been described for a n end diatom al. 1) of September 1992 at Stn B abundances were recorded during SM1 and A g 4:r 4:7 I j ' L g \ 2 1 . 1986). Nevertheported (Olson et al. the stability of the water column physical features are associated with higher 19'-BF seemed to be a prerequisite for prochlorophyte develand 19'-HF concentrations: this is the case for transiopment. Fogg 1991.e. divinyl chlorophyll a (Dvphytes were exclusively associated with strati. There is As already reported.Bustillos-Guzman et al. 80 Within the prokaryotic group. 1989. 1979. Chang and J . The event induced a mixing of the water column and phytoplankton. Prymnesiophytes and chrysophytes appear to be the most abundant and seem able to adapt to. and particularly prochlorophytes were the most sensitive since the highest divinyl chlorophyll a concentrations. Glover et al.256 Mar Ecol Prog Ser 124: 247-258. Paskind GW. Gough MA. In: Falkowski PG. are able to quickly respond to atmospheric events that enhance homogenization and replenish surface layers with nutrients. Prieur L (1983) Hydrologie et circulation e n Mediterranee Nord-occidentale. 1995 oligotrophic conditions. and B. Woodhead AD (eds) Primary productivity and biochem~calcycles in the sea. Diatoms accumulate mainly in semi-mixed conditions. Dolan for improvements In the English of the manuscript. In the stratified oligotrophic open ocean. 1988). Contribution to MAST-MTP Geodyme subproject (MAS 2 CT 9300611. Charra and D Betti for field assistance. Dolan. suggesting adaptability of the cyanobacteria (e. Claustre & Marty 1995).g. Deep Sea Res 40:459-477 Bernard C (1991) Comportement trophique des principaux cilies pelagiques marins en Mer Ligure: phagotrophie. while different phytoplankton taxa are generally adapted to specific water column conditions. were associated with a strong stratification. Gulllard RRL. Biochem Syst Ecol 16: 445-452 Campbell L.a wide range of water column hydrographic structures. Fileman TW (1993) Pigment signatures of the phytoplankton composition in the northeastern Atlantlc during the 1990 spring bloom. this is not always the case. prochlorophytes were virtually absent from the surface layer. R.This observation is supported by the dynamics of prokaryotes associated with the E2 event (Fig 8).grant to J. This property may explains why this group appears to be . when the water column was stratified. resulting in a homogeneous distribution of prochlorophytes. mainly in deep layers. Sauders G G . Goericke and the anonymous reviewers for comments. a typical profile of zeaxanthin and divinyl-chlorophyll a suggested that cyanobacteria grew at the surface and prochlorophytes at depth. R. Williams. Plenum Press. Prochlorophytes did not appear to increase in concentration under such conditions. and the microbial loop in the open sea. M . Mantoura RF. 1993. D Pizay for nitrate analysis. France Bethoux JP. temporal changes of phytoplankton concentrations. PhD thesis. and the description of a new algal class. nov. Liaaen-Jensen S (1976) New-fucoxanthinrelated carotenoids from Coccolithus huxleyi. et sp. Paris V1 Arpin N. P. Sexton JP (1993) Ultrastructure and 1 8 s rRNA gene sequence for Pelagomonas cabeolata gen.-G. suggesting that the population recorded here may more likely be adapted to low light/high nutrient conditions (cf. the Pelagophyceae classis nov. Petrole Techniques 299: 25-34 Bjornland T. they are not sufficient. In stratified ol~gotrophic oceans cyanobacteria grow in layers where nitrate concentrations are very low. Thanks to: J. Campbell & Vaulot 1993). New York. p 409-440 Barlow RG. (Cyanobacteria): the use of CONCLUDING REMARKS The present study allowed us to link the hydrographic structures (from complete mixing to strong stratification) to the development. the biomasses of prochlorophytes and cyanobacteria are nearly the same (Letelier et al. in this study the highest cyanobacteria abundances were observed in semi-mixed conditions where nitrates were relatively abundant. especially at small scales where specific lighthutrient requirements are important. and as soon as stratification was re-established. Acknowledgements. ubiquitous in most of the world's oceans. but while these conditions are necessary. they showed a distribution typical of low light/high nutrient species. In this study. Liaaen-Jensen S (1988) Phaeocyshs sp. 1990. This work was supported by the DYFAMED program (JGOFS-France) and was partially funded by the Consejo Nacional de Ciencia y Tecnologla (Mexico). mutotrophie et autotrophie. Gentili for some figures. Un~versiteBlaisePascal Clermont-Ferrand 11. However. similar to diatoms.which was not the case here during stratified conditions. Our results suggest therefore that. Picoplanktonic prokaryotes (cyanobacteria and prochlorophytes) were unable to prosper in mixed water conditions. Finally. Carpenter EJ (1986) Die1 patterns of cell division in marine Synechococcus spp. B. Waterbury et al. J Phycol 29 701-715 Andre J M (1990) Teledetection spatiale d e la couleur d e la mer: algorithmique d'inversion des mesures du coastal zone color scanner Application a I'etude d e la Mediterranee Occidentale. 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