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Size-fractionated phytoplankton biomass and species composition in the Indian sector of the Southern Ocean during austral summer
Journal of Marine Systems 17 Ž1998. 179–194
Size-fractionated phytoplankton biomass and species composition in the Indian sector of the Southern Ocean during austral summer M. Fiala a
a,)
, M. Semeneh b, L. Oriol
a
Laboratoire Arago, UniÕersite´ Pierre et Marie Curie, UMR CNRS 7621, 66650 Banyuls sur Mer, France b Vrije UniÕersiteit Brussel, Analytische Chemie, Pleinlaan 2, 1050 Brussels, Belgium Received 15 October 1995; accepted 15 October 1996
Abstract During the late austral summer of 1994, Antarctic waters were characterized by low phytoplankton biomass. Along the 628E meridian transect, between 498S and 678S, chlorophyll ŽChl.. a concentration in the upper 150 m was on average 0.2 mg my3. However, in the Seasonal Ice Zone ŽSIZ. chlorophyll a concentrations were higher, with a characteristic deep chlorophyll maximum. The highest value Ž0.6 mg Chl. a my3 . was measured at the Antarctic Divergence, 648S, corresponding to the depth of the temperature minimum Ž; 100 m.. This deep biomass maximum decreased from South to North, disappeared in the Permanently Open Ocean Zone ŽPOOZ. and reappeared with less vigour in the vicinity of the Polar Front Zone ŽPFZ.. In the SIZ, the upper mixed layer was shallow, biomass was higher and the ) 10 mm fraction was predominant. In this zone the ) 10 mm, 2–10 mm and - 2 mm size fractions represented on the average 46%, 25.1% and 28.9% of the total integrated Chl. a stock in the upper 100 m, respectively. The phytoplankton assemblage was diverse, mainly composed of large diatoms and dinoflagellate cells which contributed 42.7% and 33.1% of the autotrophic carbon biomass, respectively. Moving northwards, in parallel with the decrease in biomass, the biomass of autotrophic pico- and nanoflagellates Žmainly Cryptophytes. increased steadily. In the POOZ, the picoplanktonic size fraction contributed 47.4% of the total integrated Chl. a stock. A phytoplankton community structure with low biomass and picoplankton-dominated assemblage in the POOZ contrasted with the relatively rich, diverse and diatom-dominated assemblage in the SIZ. These differences reflect the spatial and temporal variations prevailing in the Southern Ocean pelagic ecosystem. Resume ´ ´ A la fin de l’ete ´ ´ austral 1994, les eaux antarctiques sont caracterisees ´ ´ par une faible biomasse phytoplanctonique. Le long de la radiale 628E, entre 498S et 678S, les concentrations en chlorophylle a sont de l’ordre de 0.2 mg my3 dans la couche 0–100 m. Cependant, au sud, dans la Zone Saisonniere ` des Glaces, les biomasses sont plus elevees ´ ´ avec un maximum chlorophyllien profond marque. ´ La plus forte valeur Ž0.6 mg Chl. a my3 . a ete ´ ´ enregistree ´ au niveau de la divergence antarctique Ž648S. a` une profondeur de 100 m correspondant au minimum thermique. Ce maximum chlorophyllien s’enfonce en profondeur vers le nord en diminuant d’intensite´ et disparaıt libre de glace. Au voisinage du ˆ dans la Zone Oceanique ´ Front Polaire, la biomasse augmente legerement, avec des valeurs homogenes, voisines de 0.3 mg Chl. a my3, dans les 150 ´ ` `
)
Corresponding author. Tel.: q33-4-6888-7304; Fax: q33-4-6888-7395; E-mail: [email protected]
0924-7963r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 4 - 7 9 6 3 Ž 9 8 . 0 0 0 3 7 - 2
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premiers metres. En bordure du Continent Antarctique, dans la Zone Saisonniere est ` ` des Glaces ou` la couche de melange ´ reduite et la biomasse elevee, Dans cette zone, les fractions de ´ ´ ´ la fraction phytoplanctonique ) 10 mm est predominante. ´ taille ) 10 mm, 2–10 mm et - 2 mm representent respectivement 46%, 25.1% et 28.9% de la biomasse totale integree ´ ´ ´ entre 0 et 100 m. Les populations naturelles y sont essentiellement composees ´ de grosses diatomees ´ et de dinoflagelles ´ qui representent respectivement 42.7% et 33.1% de la biomasse carbonee a` la diminution ´ ´ autotrophe. Vers le nord, parallelement ` de la biomasse, l’importance des algues picoplanctoniques et des flagelles ´ nanoplanctoniques autotrophes ŽCryptophycees ´ essentiellement. augmente fortement. Dans la Zone Oceanique, la fraction picoplanctonique represente 47.4% de la biomasse ´ ´ chlorophyllienne totale. Il y a une opposition entre la Zone Oceanique libre de glace caracterisee ´ ´ ´ par une biomasse faible dominee ´ par le picoplancton et la Zone Saisonniere ` des glaces ou` la biomasse relativement plus elevee ´ ´ est dominee ´ par les grosses diatomees. dans l’ensemble de l’ecosysteme ´ Cette dualite´ reflete ` la variabilite´ spatiale et temporelle qui prevaut ´ ´ ` pelagique antarctique. q 1998 Elsevier Science B.V. All rights reserved. ´ Keywords: Phytoplankton; Southern Ocean; Species composition; Austral summer
1. Introduction The size distribution of living particles is one of the main factors determining the food web structure and the global flux of organic matter in the marine environment. The classical view of the Antarctic food web structure was characterized by the predominance of large diatoms which form the basis of the food chain leading to krill ŽHasle, 1969; Guillard and Kilham, 1977.. Recently, Hewes et al. Ž1985. suggested an alternate microbial food web coexisting in parallel with the classical food chain. This carbon pathway taking place at the lower trophic level includes pico- and nano-sized primary and secondary producers ŽLancelot et al., 1991.. The presence of nano- and picoplanktonic microorganisms in the Southern Ocean is now recognized. These include small diatoms, flagellates, cyanobacteria and protozoa ŽGieskes and Elbrachter, 1986; Brandini and ¨ Kutner, 1987; Marchant et al., 1987; Becquevort et al., 1992; Menon et al., 1995.. However, the information available on their abundance, distribution and relative importance is still restricted. The question of the relative importance of the different size fractions within Antarctic water is not yet solved. Some studies report the preponderance of nanophytoplankton Žvon Brockel, 1981; Kosaki et al., 1985; Hosaka and ¨ Nemoto, 1986; Jacques and Panouse, 1991; Fiala and Delille, 1992; Jochem et al., 1995; Xiuren et al., 1996.. However, in others circumstances, picoplankton appears as an important component of the phytoplankton assemblage ŽHewes et al., 1985; Weber and El-Sayed, 1987; Carrada et al., 1994.. These scarce results, scattered in space and time, do not allow the
build up of a general picture for the whole Austral Ocean. Generally, diatoms are one of the dominant groups of the Antarctic phytoplankton community ŽHasle, 1969; Jacques et al., 1979; Kopczynska et al., 1986; El-Sayed and Fryxell, 1993. and are the major exporters of organic matter to deep ocean ŽTreguer et ´ al., 1995.. Their importance in the biomass Žboth in absolute and relative terms., however, shows a large temporal and spatial variability. In areas of greater water column stability and often at the beginning of the growth season, diatom biomass constitutes a major fraction of the phytoplankton biomass ŽJacques and Panouse, 1991; Kopczynska, 1992; Smetacek et al., 1992; Kopczynska et al., 1995. whereas during winter and in areas of intense mixing flagellate and dinoflagellate biomass exceeds that of diatoms ŽKopczynska, 1992; Garrison et al., 1993; Kopczynska et al., 1995.. The objective of the present paper is to gain information on Antarctic food webs by the way of analysis of the spatial variability of phytoplankton biomass, species composition and abundance and distribution of the size fractionated phytoplankton. This study was performed during the austral summer in the Indian sector of Antarctic Ocean between the Seasonal Ice zone and the Polar Front Zone. 2. Materials and methods 2.1. Sampling strategy Samples were collected during the Antares 2 cruise ŽRrV Marion Dufresne, 6 February–9 March 1994.
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Fig. 1. Location of the sampling stations during Antares 2 cruise Ž6 February–9 March 1994. along the 628E meridian transect. The 14 X X stations were spaced 1830 apart between 66840 S and 498S.
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conducted in the Indian sector of the Southern Ocean ŽFiala, 1995.. Fourteen stations, distributed along the 628E meridian transect between 498S and 66840X S, were studied while steaming northwards ŽFig. 1.. Sampling in the upper 250 m was performed using a Seabird CTD-O 2-fluorescence probe equipped with 12 Niskin bottles. 2.2. Size fractionation procedure and pigment analysis Size fractionation was performed at 14 stations between the surface Žor sub-surface. and 100 m. The fractionation was carried out by parallel filtering of subsamples of water Ž500 ml. through Nuclepore polycarbonate membranes of 10 mm and 2 mm pore-size and on a Whatman GFrF glass-fibre filter used as reference for the total chlorophyll ŽChl... Treatment of pigment samples was carried either by manual grinding of the filter in the presence of pure acetone ŽGFrF. or by dipping in 90% acetone ŽNuclepore. followed by an extraction lasting about 12 h at 58C and centrifugation for 7 min at 58C and 4000 rpm. Fluorescence of the acetone extract was successively measured on a Perkin-Elmer MPF 66 spectrofluorometer at six excitation and emission wavelengths ŽNeveux and Panouse, 1987.. Each coupled wavelength corresponded to the fluorescence excitation and emission of each pigment analysed: Chl. a, Chl. b, Chl. c, phaeophytins a, b and c. 2.3. Flow cytometry measurements Cell numbers in the ) 10 mm, 2–10 mm and ) 10 mm size fractions were determined from the different Nuclepore filtrates. Samples were fixed with a glutaraldehyde solution ŽMerck, final concentration ; 1%. and stored in liquid nitrogen as described by Vaulot et al. Ž1989.. A Bruker ACR-1000 flow cytometer was used for the analyses. We measured forward light scatter ŽFLS. as an indicator of size, orange fluorescence from phycoerythrin Ž580 " 40 nm. and red fluorescence from chlorophyll Ž680 " 20 nm. after excitation by the 480 mm light of mercury arc-lamp ŽSteen, 1986.. Instrument calibration was frequently monitored by analysing 0.94 mm and 1.96 mm fluorescent standard beads ŽPolysciences..
2.4. Microscopic cell counting and carbon biomass estimation Water samples for species identification and enumeration were taken over the upper 150 m depth at every station and fixed with hexamine-buffered formalin solution Žfinal concentration ; 0.4%.. Cells in a 50 ml subsample were counted under inverted microscope according the Utermohl method ¨ ŽUtermohl, ¨ 1958.. For each station three depths were counted: surface Ž; 10 m., the depth of the chlorophyll maximum and an intermediate depth. The cell volume of each species was calculated from cell sizes using appropriate cell geometry. Carbon biomass was estimated from cell volume and cell abundance using the conversion factors of Eppley et al. Ž1970.: log C s 0.76Žlog V . y 0.352 for diatoms and log C s 0.94Žlog V . y 0.6 for non-diatoms, where V and C are cell volume Žin mm3 . and cell carbon Žin pg., respectively. Only cells ) 2 mm can be quantified with this method, which thus excludes the biomass of picophytoplankton. 2.5. Statistical analysis An ordination technique was used to identify and arrange stations with similar species composition. As the gradient was very short Žgradient length - 2., we used Principal Component Analysis ŽPCA. which assumes a linear species response to the underlying environmental gradient ŽJongman et al., 1987.. Rare species which were encountered in less than 5% of the stations were excluded from the analysis and the biomass was log transformed to reduce the influence of few dominant species. Then PCA was applied to the depth integrated biomass data Žmg C my2 . using the Canocoe 3.10 version statistical package on a Macintosh computer ŽTer Braak, 1990..
3. Results 3.1. Phytoplankton biomass distribution along the 628E transect The main feature marking the study area was the general oligotrophy in terms of phytoplankton biomass. Chl. a concentrations in the upper 150 m
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Fig. 2. Distribution of Chl. a Žmg my3 . in the upper 250 m along the 628E transect from the Seasonal Ice Zone ŽSIZ. to the Polar Frontal Zone ŽPFZ..
ranged from 0.01 to 0.57 mg my3 ŽFig. 2.. Highest levels of Chl. a were located in the Seasonal Ice Zone ŽSIZ, south of 588S. in the vicinity of the
Antarctic Continent. In the southern area Žsts. A05 and A06., Chl. a showed higher concentrations in the upper 100 m. The maximum value Ž0.57 mg
Fig. 3. Vertical profiles of Chl. a in the - 2 mm, 2–10 mm and ) 10 mm size fractions along the 628E transect.
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my3 . was measured at the Antarctic Divergence Ž648S. at the 100 m depth which coincides with the depth of temperature minimum ŽE. Charriaud, personal communication.. This moderate deep biomass maximum decreased from South to North and disappeared in the Permanently Open Ocean Zone, POOZ Ži.e., north of 588S.. The POOZ is the poorest Antarctic area where Chl. a values ranged between 0.1 and 0.2 mg my3 . Moving northwards, phytoplankton biomass increased slightly with values around 0.3 mg Chl. a my3 in the vicinity of the Polar Frontal Zone ŽPFZ.. The concentration of phaeopigments was low and relatively uniform in the sub-surface water. The degradation ratio wi.e., phaeophytin arŽphaeophytin a q Chl. a.x averaged 0.10 in the upper 100 m, indicating a relative high level of Chl. a, and thus giving evidence of a good physiological condition of cells. Moreover, this ratio increased with depth and was on the average 0.20 at the deep chlorophyll maximum in the SIZ.
3.2. Size-fractionated phytoplankton distribution As with total Chl. a distribution, the different size fractions showed spatial variability. From south to north, the - 10 mm fraction was the major contributor to the total phytoplankton stocks but its relative contribution showed regional variations ŽFig. 3.. Inside this fraction the picoplankton dominated but its importance increased northwards. The ) 10 mm size fraction was more important in the SIZ than in the POOZ. However, its contribution increased in the vicinity of the PFZ Žst. A18.. The vertical distribution of the relative proportion of Chl. a in the different size fractions over the study area varied little ŽFig. 3.. However, in the SIZ, the biomass of the ) 10 mm fraction was highest at the Chl. a maximum layer between 80 m and 100 m depth. Along the transect total phytoplankton cell number as estimated by flow cytometry ranged between 1.6 = 10 3 cells mly1 and 4.2 = 10 3 cells mly1 in the surface water ŽFig. 4.. The picoplanktonic cells were
Fig. 4. Vertical profiles of cell numbers as measured by flow cytometry in the - 2 mm, 2–10 mm and ) 10 mm size fractions along the 628E transect.
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always numerically dominant representing 70% to 90% of the total abundance. Their maximum was observed at the Chl. a maximum depth, especially in the SIZ Žaround 5 = 10 3 cells mly1 .. The abundance of the 2–10 mm size-fraction decreased from the SIZ to the POOZ and increased slightly in the vicinity of PFZ. The ) 10 mm fraction showed a tendency to increase in numbers at the rich stations of the SIZ Žsts. A07 and A08. where it varied between 0.8 = 10 3 cells mly1 and 0.9 = 10 3 cells mly1 at 80 m depth. 3.3. RelatiÕe contribution of size-fractionated phytoplankton to the total Chl. a stock The Chl. a stock, integrated over the upper 100 m, decreased progressively from 31.7 mg my2 in the SIZ to 8 mg my2 in the POOZ and then increased to 25.9 mg my2 at 498S in the vicinity of the PFZ ŽFig. 5.. In the SIZ, the - 10 mm size fraction accounted for 54% of the Chl. a stock. Within this fraction, the picoplankton Ž- 2 mm. and the 2–10 mm fraction contributed about 28.9% and 25.1% of the Chl. a stock, respectively ŽTable 1.. While the contribution of these two size fractions was similar in the SIZ, the - 2 mm fraction dominated in the POOZ and PFZ ŽFig. 5 and Table 1.. The ) 10 mm size fraction accounted on the average for 46% of the Chl. a stock, with a maximum contribution of 64% at st. 11. At the deep Chl. a maximum layer, the ) 10 mm size fraction contributed about 50% of the total phytoplankton biomass. In the SIZ, the Chl. a stock in the ) 10 mm, 2–10 mm and - 2 mm size fractions were on the average 11.8, 6.5 and 7.5 mg my2 , respectively ŽTable 1.. In the POOZ, the - 10 mm size fraction represented 67.6% of the Chl. a stock ŽTable 1 and Fig. 5.. The picoplanktonic fraction was clearly dominant, contributing about 47.4% of the total biomass, corresponding to a mean value of 7.6 mg Chl. a my2 . The 2–10 mm and ) 10 mm fractions represented 20.2% Žmean ; 3.2 mg Chl. a m y2 . and 32.3% Žmean ; 5.2 mg Chl. a my2 . of the total Chl. a stock, respectively. 3.4. Carbon biomass and species composition Along the transect, integrated phytoplankton biomass, determined from microscope cell counts, ranged from 326.8 to 2056.6 mg C my2 . The latitudinal distribution pattern was similar to that of Chl.
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a, with a higher biomass in the SIZ Žmean ; 1332.2 mg C my2 . than in the POOZ Žmean ; 640.3 mg C my2 , Table 1.. Fig. 6 shows the distribution of carbon biomass of the main taxonomic groups. Diatom distribution exhibited large spatial variability; their biomass increased dramatically south of 588S ŽSIZ.. Dinoflagellate biomass decreased sharply between 66840X S and 62830X S and increased gradually in the northern part of the SIZ. On the contrary, the distribution of flagellates was rather uniform with the exception of two stations in the southern part of the transect. In the SIZ, the average composition was as follows: diatoms Ž42.7%., dinoflagellates Ž33.1%. and flagellates Ž24.2%.. In the POOZ, on the other hand, the composition of phytoplankton shifted towards dominance by dinoflagellates Ž41.7%.. Flagellates and diatoms contributed 30.2% and 27.8%, respectively ŽTable 1.. Among diatoms, centric species were the dominant types representing ; 69% of the total diatom biomass. In particular, in the vicinity of the PFZ Žsts. A17 and A18. they accounted for over 90% of the diatom biomass. Size fractionation, using cell equivalent spherical diameter ŽESD., indicated that the phytoplankton community in the SIZ was dominated by a microphytoplankton assemblage, ESD ) 20 mm Ž56.5%; Table 1.. Nanophytoplankton ŽESD - 20 mm. represented about 43.5%, of which 23.8% was due to the 10–20 mm fraction. On the contrary, in the POOZ the nanophytoplankton was dominant, representing about 71.3% of the total biomass. Both in the SIZ and POOZ, the 10–20 mm size fraction accounted for over 50% of the nanoplankton biomass. It should be kept in mind that the microscopic cell counts exclude the biomass of picoplankton ŽESD - 2 mm.. This has two consequences: underestimating total carbon biomass and overestimating the relative contributions of the nano- and microphytoplankton. The carbonrChl. a ratio ranged from 20.7 to 203.9 Žmean ; 95.. Low CrChl. values were observed in the vicinity of PFZ. As the sampling was done late in the growth season, the relatively high CrChl. ratio might suggest a declining community. 3.5. Phytoplankton community analysis Since the species data showed large spatial variability, plots of species and sample Žstations. scores
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Fig. 5. Distribution of integrated Chl. a Župper. and percentage contribution to total integrated Chl. a Žlower. in the - 2 mm, 2–10 mm and ) 10 mm size fractions for the 14 stations located along the 628E transect.
were used to characterize the different zones in terms of species composition. The results of PCA are shown in Fig. 7. The eigenvalues were relatively high Ž l1 s 0.29, l2 s 0.16. and these two axes alone explained about 45% of the species variance. Moreover, the third and fourth eigenvalues were smaller compared to the first two axes which indicates that
there were only two major gradients in the species data. Four clusters of stations are apparent from the plots of sample scores ŽFig. 7.. The first axis separates stations in the SIZ from the POOZ. On the other hand, the second axis separates the two subgroups within each main group. Thus, within the SIZ
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Table 1 Summary of mean integrated phytoplankton biomass Žcarbon and chlorophyll a. in the SIZ and in the POOZ during cruise Antares 2 SIZ
Total C biomass Diatom biomass Dinoflagellate biomass Flagellate biomass C biomass - 10 mm C biomass 10–20 mm C biomass ) 20 mm
POOZ
mg C my2
% of total C
mg C my2
% of total C
1333.2 569.3 441.8 322.1 262.4 317.7 753.0
42.7 33.1 24.2 19.7 23.8 56.5
640.3 177.9 267.0 193.2 221.0 235.6 183.8
27.8 41.7 30.2 34.5 36.8 28.7
SIZ
POOZ y2
mg m Total Chl. a Chl. a - 2 mm Chl. a 2–10 mm Chl. a ) 10 mm
25.8 7.5 6.5 11.8
% total Chl. a
mg my2
% total Chl. a
28.9 25.1 46.0
16.0 7.6 3.2 5.2
47.4 20.2 32.3
stations A05, A06 and A07, located south of the Antarctic divergence, from the first cluster ŽCluster I. whereas sts. A08, A09, A10 and A11, located
between the Antarctic divergence and the outer limit of the SIZ, constitute the second cluster ŽCluster II.. In the POOZ, sts. A12, A13 and A14 constitute
Fig. 6. Integrated phytoplankton biomass distribution along the 628 E meridian transect ŽSquaress diatoms, open triangless flagellates and open circles s dinoflagellates..
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cluster III and the rest Žsts. A15, A16, A17 and A18. forms cluster IV. The latter group includes stations at or in the vicinity of the PFZ. The position of a species in the PCA biplot ŽFig. 7. indicates the direction in which the biomass of
that species increases most and the length of a species head from the centre indicates the rate of change of the biomass of that species in that direction ŽJongman et al., 1987.. Thus, cluster I is characterized by greater biomass of small pennate diatoms
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such as Nitzschia cylindrus ŽGrunow. Hasle and many flagellates such as Pyramimonas spp., small comma-shaped flagellates as well as other small unidentified flagellates ŽEDS - 5 mm.. Silicoflagellates were more abundant in stations south of the Antarctic divergence. In Cluster I they represented about 15% of the total biomass. Their position in the plot is, however, contrary to the expected. Since they were mainly present in the SIZ, the first axis explains only a very low percentage of their variance Ž; 2.5%.. Therefore, their position is not well represented. A relatively rich and diverse phytoplankton assemblage characterizes the second cluster. This can be inferred from the number and length of species axes Žmost of them diatoms. pointing to this cluster. Large pennate and centric diatoms were present in this cluster. These include members of the genera Nitzschia, Pseudonitzschia, Tropidoneis, Thalassiothrix, Thalassiosira and Chaetoceros, which often constitute a large fraction of the total biomass. Stations of Cluster III are located at the outer limit of the SIZ and are characterized by greater abundance of Nitzschia kerguelensis ŽO’Meara. Hasle and NaÕicula spp. At st. A12 N. kerguelensis alone accounted for about 11% of the total biomass. Stations in Cluster IV are located at or in the vicinity of the PFZ and are characterized by greater biomass of large centric diatoms, such as Proboscia spp. and Corethron criophilum Castracane, and flagellates such as Cryptophytes. C. criophilum was present over the whole transect with an average relative contribution of 10.3%. Although the diatom biomass was low in the POOZ, C. criophilum together with N. kerguelensis represented a significant proportion of the total biomass. Moreover, C. criophilum is known to be very abundant when the phytoplankton biomass is low and when the ambient silicate to nitrate ratio is
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high ŽSommer, 1991.. Flagellates such as Cryptophytes were very abundant in most stations. About 16% of the total biomass and 64% of the flagellate biomass were due to Cryptophytes. An unidentified flagellate similar in morphology to Phaeocystis was very abundant in the POOZ and accounted for about 35% of the flagellate biomass. The first axis correlates negatively with the total phytoplankton biomass Ž r 2 s 0.5. and, in particular, with the biomass of the larger size fraction Ži.e., ESD ) 10 mm.. As can be seen from the biplot ŽFig. 7., there are few species with long axes pointing to the stations located close to the ‘origin’ ŽCluster IV., indicating dominance by a few very abundant species. On the other hand, stations at the opposite side of the ‘origin’ ŽCluster II. are characterized by high species diversity Ži.e., many species with relatively short axes pointing to Cluster II stations.. Thus, along the first axis the phytoplankton assemblage changes from a rich and diverse assemblage dominated by large pennate diatoms in the SIZ ŽCluster I and II. to a relatively poor and less diverse assemblage dominated by Cryptophytes and few large centric diatoms in the POOZ ŽCluster III and IV..
4. Discussion Our results show a clear picture of the late summer phytoplankton community structure in different functional zones in the Indian sector of the Southern Ocean. The main striking features of this region are the low phytoplankton biomass and the spatial variability in phytoplankton biomass and community structure. The low phytoplankton biomass observed during this study corroborates the general oligotrophic nature of the Indian sector of the Southern Ocean ŽJacques and Minas, 1981; Jacques and
Fig. 7. Plot of sample Župper. and species scores Žlower. of the first two axes of principal component analysis ŽEigenvalues: l1 s 0.29, l2 s 0.16.. Ampdins Amphidinium spp.; Ast spp.s Asteromphalus spp.; Cent dia s centric diatoms; Chae spp.s Chaetoceros spp.; Chae bal s Chaetoceros bulbosum ŽEhrenberg.; Chae cri s Chaetoceros criophilum Castracane; Chae dic s Chaetoceros dichaeta ŽEhrenberg.; Com spp s comma-shaped flagellates; Cor cri s Corethron criophilum Castracane; Cos spp.s Coscinodicus spp.; Crypt spp.s Cryptophyte spp.; Dact spp.s Dactyliosolen spp.; Dinoflas Dinoflagellate spp.; Gym din s Gymnodinium spp.; Nav spp.s NaÕicula spp., Nit ang s Nitzschia angulata Hasle; Nit cyl s Nitzschia cylindrus ŽGrunow. Hasle; Nit ker s Nitzschia kerguelensis ŽO’Meara. Hasle; Nit spp.s Nitzschia spp.; Oth fla s Other flagellates; Proroc s Prorocentrum spp., Prob spp.s Proboscia spp.; Pseunits Pseudonitzschia spp.; Pyr spp.s Pyramimonas spp.; Rhiz chu s Rhizosolenia chunii Karsten; Rhiz spp.s Rhizosolenia spp.; Sil spp.s Silicoflagellate spp.; Tharix s Thalassiothrix spp; Thasir s Thalassiosira spp; Tropids Tropidoneis spp.; Unid fla s Unidentified flagellates.
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Fukuchi, 1994.. Moreover, the spatial variability observed during this cruise is a microcosm reflection of the heterogeneity of the Southern Ocean pelagic ecosystem in terms of phytoplankton biomass and community structure. Data on the seasonal variation for this part of the Southern Ocean are scarce. Sasaki Ž1984. reported higher phytoplankton biomass in the SIZ during spring Žmean Chl. a s 0.61 mg my3 . than in the summer period Žmean Chl. a s 0.19 mg my3 .. Our study area was investigated recently during early spring ŽAntares 3 cruise, October 1995. and the results show low biomass and dominance by diatoms in the SIZ and by flagellates in the POOZ ŽM. Semeneh et al., in press.. The phytoplankton community analysis confirms the presence of three functional units: SIZ, POOZ and PFZ ŽTreguer and Jacques, 1992.. In the SIZ the ´ phytoplankton community structure is characterized by a relatively rich, diatom dominated microplankton Ž) 20 mm. assemblage. On the contrary, the POOZ is characterized by a low biomass and a phytoplankton community predominantly composed of autotrophic pico- and nanoflagellates. The greater importance of the microphytoplankton with increasing biomass in the SIZ agrees with the observations of Sasaki Ž1984. in this sector of Southern Ocean. The above functional zones occupied parallel belts of latitude and displayed a north–south gradient in biomass, composition and size distribution of the phytoplankton community. Superimposed on this gradient was a positive gradient of nutrient availability ŽGoeyens, 1995.. Areas of greater diatom biomass such as the SIZ were characterized by high silicate and nitrate availability whereas regions of relative low silicate and nitrate concentrations in the North were characterized by poor diatom biomass and greater importance of small size fraction Žmainly picoplankton.. The distribution of phytoplankton biomass and community structure along the transect appears to be the reflection of the prevailing environmental variations, especially that of temperature. The distribution of temperature varied along the transect. Cold and more saline surface water with a rather uniform vertical temperature profile characterized stations south of the divergence ŽCluster I, Fig. 8.. On the other hand, relatively warm and less saline surface water with a pronounced subsurface temperature
minimum was present in the stations located between the divergence and the northern limit of the ice cover ŽCluster II, Fig. 8.. This region is characterized by the predominance of diatoms under greater water column stability, evidenced by shallow and steep vertical temperature gradients. This fact corroborates the conclusion of Kopczynska Ž1992. that diatoms dominate in areas of greater water column stability and low krill concentration. Moreover, the SIZ was characterized by the presence of a deep chlorophyll maximum which appeared to be closely associated with the temperature minimum. A phytoplankton assemblage dominated by large diatoms was located below the euphotic zone Žmean depth ; 70 m. and exhibited low photosynthetic capacity ŽP. Treguer, ´ personal communication.. The depth of the chlorophyll maximum in the SIZ deepened upon moving northwards. Although the deep chlorophyll maximum in oligotrophic low latitude oceans is related to nutrient deficiency ŽGould, 1987., its significance in nutrient rich areas such as the Southern Ocean remains unclear. When Chl. a concentration in the upper 200 m depth was plotted against water temperature, different response curves were observed in the SIZ and POOZ ŽFig. 9.. In the SIZ the ambient temperature was - 28C and the relationship was parabolic Žunimodal. with a maximum around 08C. In contrast, in the POOZ the ambient temperature was ) 18C and the relationship was linear. Different ranges of temperature exposure and different response curves indicate different ecophysiological adaptations in these functional zones. In the SIZ ‘warm’ deep water lies below cold surface winter water and higher biomass mainly due to large diatoms was observed around 08C which suggest optimum temperature as a downward driving factor of the deep chlorophyll maximum. Generally, the growth of polar microalgae appears to be controlled by temperature ŽKirst and Wiencke, 1995.. Moreover, some of the dominant species in the SIZ such as C. criophilum and N. kerguelensis are obligatory psychrophylic and exhibit maximum growth below 58C ŽFiala and Oriol, 1990.. The differences in phytoplankton community structure between the SIZ and POOZ are also reflected by the food web structure. Low phytoplankton biomass in this sector of the Southern Ocean
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Fig. 8. Vertical profile of water temperature, phytoplankton biomass and nitrate concentration in four representative stations: st. A06 ŽCluster I., st. A08 ŽCluster II., st. A13 ŽCluster III., st. A18 ŽCluster IV..
does not attract large grazers such as krill; therefore, microzooplankton such as ciliates are expected to structure the phytoplankton community. Ecosystems
of this type would be largely based on regenerated Žammonium. production. Despite differences in community structure, the community both in the SIZ and
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Fig. 9. Relationship between water temperature and phytoplankton biomass in the upper 200 m depth for stations located in the SIZ Župper. and in stations located in the POOZ Žlower..
POOZ was predominantly based on regenerated production ŽSemeneh et al., unpublished data.. Traditionally new production is associated with a diatom dominated microplankton assemblage and regenerated production with a flagellate dominated nano- or picoplankton assemblage. In the POOZ, the observed
phytoplankton community structure, a nano- and picoplankton dominated assemblage is consistent with the expected production regime Žnew production.. In the SIZ, on the other hand, the observed community structure dominated by a diatom microplankton assemblage was not in agreement with the expected
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production regime Žregenerated production.. This, however, supports the recent hypothesis that under conditions of prolonged water column stability and reduced grazing pressure on microphytoplankton, a shift in nitrogen uptake regime Ži.e., from new to regenerated production. during the growth season can occur without a large change in phytoplankton community structure ŽSemeneh et al., 1998.. Both reduced grazing pressure on large cells and persistent water column stability reduce loss rates, and these conditions enable diatoms to overstay in the late season. Several studies in the Southern Ocean have shown that, despite high nitrate availability, phytoplankton preferentially utilizes ammonium and, unlike low latitude ecosystems, the shift from new to regenerated production occurs before nitrate is exhausted ŽGlibert et al., 1982; Ronner et al., 1983; Goeyens et ¨ al., 1991; Jacques, 1991; Owens et al., 1991; Semeneh et al., 1998.. Heterotrophic activity during the season increases ammonium availability, leading to greater contribution to the total nitrogen requirement of phytoplankton and predominance of regenerated production. During this cruise the phytoplankton community was in a state of decline, evidenced by a high CrChl. ratio and low turnover rates of carbon and nitrogen ŽSemeneh et al., unpublished data.. For such community, greater dependence on ammonium Žregenerated production. is advantageous considering the higher energy and iron requirement of nitrate assimilation Žnew production.. Moreover, as our study area was sampled late in summer and much of the herbivory was by microheterotrophs ŽMenon et al., 1995., large diatoms can escape predation and subsist on ammonium.
Acknowledgements This study was carry out during the Antares 2 cruise sponsored by CNRS ŽJGOFS-France Program. and IFRTP. We thank G. Vetion for assistance with the flow cytometric analysis and Dr C. Lancelot for giving access to laboratory facilities. We are grateful to the captain and crew members of RrV Marion Dufresne for their cooperation. The authors are grateful to two anonymous reviewers for their critical comments.
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References Becquevort, S., Mathot, S., Lancelot, C., 1992. Interactions in the microbial community of the marginal ice zone of the northwestern Weddell Sea through size distribution analysis. Polar Biol. 12, 211–218. Brandini, F.P., Kutner, M.B.B., 1987. Phytoplankton and nutrient distributions off the northern south Shetland Islands Žsummer 1984—BiomassrSibex.. Mer 25, 93–103. von Brockel, K., 1981. The importance of nanoplankton within ¨ the pelagic Antarctic ecosystem. Kiel. Meeresforsch. Sonderh. 5, 61–67. Carrada, G.C., Fabiano, M., Povero, P., Saggiomo, V., 1994. Surface distribution of size-fractionated chlorophyll a and particulate organic matter in the Strait of Magellan. Polar Biol. 14, 447–454. El-Sayed, S.Z., Fryxell, G.A., 1993. Phytoplankton. In: Friedmann, E.I. ŽEd.., Antarctic Microbiology. Wiley-Liss, New York, pp. 65–122. Eppley, R.W., Reid, F.M., Strickland, J.D.H., 1970. The ecology of the phytoplankton off La Jolla, California, in the period April through September 1967. In: Strickland, J.D.H. ŽEd.., Estimates of Phytoplankton Crop Size, Growth Rate and Primary Production, Part III. Bull. Scripps. Inst. Oceanogr. 17, 33–42. Fiala, M., 1995. La campagne Antares 2-MD 78 Ž26 Janvier–23 Mars 1994.: etude des processus controlant les flux de matiere ´ ˆ ` dans la colonne d’eau dans le secteur Indien de l’Ocean ´ Austral. Rap. Camp. Mer, IFRTP 95 Ž1., 1–7. Fiala, M., Delille, D., 1992. Variability and interactions of phytoplankton and bacterioplankton in the Antarctic neritic area. Mar. Ecol. Prog. Ser. 89, 135–146. Fiala, M., Oriol, L., 1990. Light–temperature interactions on the growth of Antarctic diatoms. Polar Biol. 10, 629–636. Garrison, D.L., Buck, K.R., Growing, M.M., 1993. Winter phytoplankton assemblage in the ice edge zone of the Weddell and Scotia Seas: composition, biomass and spatial distribution. Deep Sea Res. 40, 311–338. Gieskes, W.W.C., Elbrachter, M., 1986. Abundance of nanoplank¨ ton-size chlorophyll-containing particles caused by diatom disruption in surface waters of the Southern Ocean ŽAntarctic Peninsula region.. Neth. J. Sea Res. 20, 291–303. Glibert, P.M., Biggs, D.C., MacCarthy, J.J., 1982. Utilisation of ammonium and nitrate during austral summer in the Scotia Sea. Deep-Sea Res. 29, 837–850. Goeyens, L., 1995. Nutrient signature and nitrogen uptake during Antares 2 Cruise. Rap. Camp. Mer, IFRTP 95 Ž1., 89–92. Goeyens, L., Sørresen, F., Treguer, P., Morvan, J., Panouse, M., ´ Dehairs, F., 1991. Spatiotemporal variability of inorganic nitrogenic nitrogen stocks and uptake fluxes in the Scotia–Weddell Confluence area during November and December 1988. Mar. Ecol. Prog. Ser. 77, 7–19. Gould, R.W. Jr., 1987. The deep chlorophyll maximum in the World Ocean: a review. The Biologist 66, 4–13. Guillard, R.L.L., Kilham, P., 1977. The ecology of marine planktonic diatoms. In: Werner, D. ŽEd.., The Biology of Diatoms. Univ. California Press, pp. 372–469.
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Hasle, G.R., 1969. An analysis of the phytoplankton of the Pacific Southern Ocean: abundance, composition, and distribution during the Brategg Expedition 1947–48. Hvalradets Skr. 52, 1–168. Hewes, C.D., Holm-Hansen, O., Sakshaug, E., 1985. Alternate carbon pathways at lower trophic levels in Antarctic food web. In: Siegfried, W.R., Condy, P.R., Laws, R.M. ŽEds.., Antarctic Nutrient Cycles and Food Webs. Springer, Berlin, pp. 277– 283. Hosaka, N., Nemoto, T., 1986. Size structure of phytoplankton carbon and primary production in the Southern Ocean south of Australia during the summer of 1983–84. Mem. Nat. Inst. Polar Res. 40, 15–24. Jacques, G., 1991. Is the concept of new regenerated production valid for the Southern Ocean?. Mar. Chem. 35, 273–286. Jacques, G., Fukuchi, M., 1994. Phytoplankton of the Indian Antarctic Ocean. In: El-Sayed, S.Z. ŽEd.., Southern Ocean Ecology: The Biomass Perspective. Cambridge Univ. Press, pp. 63–78. Jacques, G., Minas, M., 1981. Production primaire dans le secteur indien de l‘Ocean ´ Antarctique en fin d’ete. ´ ´ Oceanol. Acta 4, 33–41. Jacques, G., Panouse, M., 1991. Biomass and composition of size fractionated phytoplankton in the Weddell–Scotia Confluence area. Polar Biol. 11, 315–328. Jacques, G., Descolas-Gros, C., Grall, J.-R., Sournia, A., 1979. Phytoplankton distribution in the Antarctic sector of the Indian Ocean in late summer. Int. Rev. Ges. Hydrobiol. 64, 609–628. Jochem, F.J., Mathot, S., Queguiner, B., 1995. Size-fractionated ´ primary production in the open Southern Ocean in austral spring. Polar Biol. 15, 381–392. Jongman, R.H.D., Ter Braak, C.J.F., Van Tengeren, O.F.R., 1987. Data Analysis in Community and Landscape Ecology. PUDOC, Wageningen, The Netherlands. Kirst, G.O., Wiencke, C., 1995. Ecophysiology of polar algae. J. Phycol. 31, 181–199. Kopczynska, E.E., 1992. Dominance of microflagellates over diatoms in the Antarctic areas of deep vertical mixing and krill concentrations. J. Plankton Res. 14, 1031–1054. Kopczynska, E.E., Weber, L.H., El-Sayed, S.Z., 1986. Phytoplankton species composition and abundance in the Indian Sector of the Antarctic Ocean. Polar Biol. 6, 161–169. Kopczynska, E.E., Goeyens, L., Semeneh, M., Dehairs, F., 1995. Phytoplankton composition and carbon distribution in Prydz Bay, Antarctica: relation to organic particulate matter and its d13 C values. J. Plankton Res. 17, 685–707. Kosaki, S., Takahashi, M., Yamaguchi, Y., Aruga, Y., 1985. Size characteristics of chlorophyll particles in the Southern Ocean. Trans. Tokyo Univ. Fish. 6, 85–97. Lancelot, C., Billen, G., Veth, C., Becquevort, S., Mathot, S., 1991. Modelling carbon cycling through phytoplankton and microbes in the Scotia Weddell Sea during sea ice retreat. In: Treguer, P., Queguiner, B. ŽEds.., Biochemistry and Circula´ ´ tion of Water Masses in the Southern Ocean. Mar. Chem. 35, 305–324. Marchant, H.J., Davidson, A.T., Wright, S.W., 1987. The distribution and abundance of chroococcoid cyanobacteria in the Southern Ocean. Proc. NIPR Symp. Polar Biol. 1, 1–19.
Menon, P., Lancelot, C., Becquevort, S., 1995. Dynamique du nano- et du microzooplancton: abondances, biomasses et activites ´ d’ingestion. Rap. Camp. Mer, IFRTP 95 Ž1., 154–163. Neveux, J., Panouse, M., 1987. Spectrofluorometric determination of chlorophylls and pheophytins. Arch. Hydrobiol. 109, 561– 567. Owens, N.J.P., Priddle, J., Whitehouse, M.J., 1991. Variations in phytoplanktonic nitrogen assimilation around South Georgia and in the Bransfield Strait ŽSouthern Ocean.. Mar. Chem. 35, 287–304. Ronner, U., Sørrenson, F., Holm-Hansen, O., 1983. Nitrogen ¨ assimilation by phytoplankton in the Scotia Sea. Polar Biol. 2, 137–147. Sasaki, H., 1984. Distribution of Nano- and Microplankton in the Indian Sector of the Southern Ocean Žspecial issue.. Mem. Natl. Ins. Polar Res. 32, 38–50. Semeneh, M., Dehairs, F., Baumann, M.E.M., Lancelot, C., Elskens, M., Kopczynska, E.E., Goeyens, L., 1998. Nitrogen uptake regime and phytoplankton community structure in the Atlantic and Indian sectors of the Southern Ocean. J. Mar. Syst. 17, 159–177. Semeneh, M., Dehairs, F., Fiala, M., Elskens, M., Goeyens, L., in press. Seasonal variation of phytoplankton structure and nitrogen uptake regime in the Indian Sector of the Southern Ocean. Polar Biol. Smetacek, V., Scharek, R., Gordon, L.I., Eicken, H., Fahrbach, E., Rohardt, G., Moore, S., 1992. Early spring phytoplankton blooms in ice platelet layers of the southern Weddell Sea, Antarctica. Deep-Sea Res. 39, 153–168. Sommer, U., 1991. Comparative nutrient status and competitive interactions of two Antarctic diatoms Ž Corethron criophilum and Thalassiosira antarctica.. J. Plankton Res. 13, 61–75. Steen, H.B., 1986. Simultaneous separate detection of low angle and large angle light scattering in an arc lamp-based flow cytometer. Cytometry 7, 445–449. Ter Braak, C.J.F., 1990. Update notes: CANOCO version 3.10. Agricultural Mathematics Group, Wageningen, The Netherlands. Treguer, P., Jacques, G., 1992. Dynamics of nutrients and phyto´ plankton and cycles of biogenic elements in the Antarctic Ocean. Polar Biol. 12, 149–162. Treguer, P., Nelson, D.M., Van Bennekom, A.J., DeMaster, D.J., ´ Leynaert, A., Queguiner, B., 1995. The silica balance in the ´ world ocean: a reestimate. Science 268, 375–379. Utermohl, ¨ H., 1958. Zur vervollkommung der quantitativen phytoplankton-methodik. Mitt. Int. Verein. Limnol. 9, 1–38. Vaulot, D., Courties, C., Partensky, F., 1989. A simple method to preserve oceanic phytoplankton for flow cytometric analyses. Cytometry 10, 629–635. Weber, L.H., El-Sayed, S.Z., 1987. Contribution of the net-, nanoand picoplankton standing crop and primary productivity in the Southern Ocean. J. Plankton Res. 9, 973–994. Xiuren, N., Zilin, L., Genhai, Z., Junxian, S., 1996. Sizefractionated biomass and productivity of phytoplankton and particulate organic carbon in the Southern Ocean. Polar Biol. 16, 1–11.
Size-fractionated phytoplankton biomass and species composition in the Indian sector of the Southern Ocean during austral summer M. Fiala a
a,)
, M. Semeneh b, L. Oriol
a
Laboratoire Arago, UniÕersite´ Pierre et Marie Curie, UMR CNRS 7621, 66650 Banyuls sur Mer, France b Vrije UniÕersiteit Brussel, Analytische Chemie, Pleinlaan 2, 1050 Brussels, Belgium Received 15 October 1995; accepted 15 October 1996
Abstract During the late austral summer of 1994, Antarctic waters were characterized by low phytoplankton biomass. Along the 628E meridian transect, between 498S and 678S, chlorophyll ŽChl.. a concentration in the upper 150 m was on average 0.2 mg my3. However, in the Seasonal Ice Zone ŽSIZ. chlorophyll a concentrations were higher, with a characteristic deep chlorophyll maximum. The highest value Ž0.6 mg Chl. a my3 . was measured at the Antarctic Divergence, 648S, corresponding to the depth of the temperature minimum Ž; 100 m.. This deep biomass maximum decreased from South to North, disappeared in the Permanently Open Ocean Zone ŽPOOZ. and reappeared with less vigour in the vicinity of the Polar Front Zone ŽPFZ.. In the SIZ, the upper mixed layer was shallow, biomass was higher and the ) 10 mm fraction was predominant. In this zone the ) 10 mm, 2–10 mm and - 2 mm size fractions represented on the average 46%, 25.1% and 28.9% of the total integrated Chl. a stock in the upper 100 m, respectively. The phytoplankton assemblage was diverse, mainly composed of large diatoms and dinoflagellate cells which contributed 42.7% and 33.1% of the autotrophic carbon biomass, respectively. Moving northwards, in parallel with the decrease in biomass, the biomass of autotrophic pico- and nanoflagellates Žmainly Cryptophytes. increased steadily. In the POOZ, the picoplanktonic size fraction contributed 47.4% of the total integrated Chl. a stock. A phytoplankton community structure with low biomass and picoplankton-dominated assemblage in the POOZ contrasted with the relatively rich, diverse and diatom-dominated assemblage in the SIZ. These differences reflect the spatial and temporal variations prevailing in the Southern Ocean pelagic ecosystem. Resume ´ ´ A la fin de l’ete ´ ´ austral 1994, les eaux antarctiques sont caracterisees ´ ´ par une faible biomasse phytoplanctonique. Le long de la radiale 628E, entre 498S et 678S, les concentrations en chlorophylle a sont de l’ordre de 0.2 mg my3 dans la couche 0–100 m. Cependant, au sud, dans la Zone Saisonniere ` des Glaces, les biomasses sont plus elevees ´ ´ avec un maximum chlorophyllien profond marque. ´ La plus forte valeur Ž0.6 mg Chl. a my3 . a ete ´ ´ enregistree ´ au niveau de la divergence antarctique Ž648S. a` une profondeur de 100 m correspondant au minimum thermique. Ce maximum chlorophyllien s’enfonce en profondeur vers le nord en diminuant d’intensite´ et disparaıt libre de glace. Au voisinage du ˆ dans la Zone Oceanique ´ Front Polaire, la biomasse augmente legerement, avec des valeurs homogenes, voisines de 0.3 mg Chl. a my3, dans les 150 ´ ` `
)
Corresponding author. Tel.: q33-4-6888-7304; Fax: q33-4-6888-7395; E-mail: [email protected]
0924-7963r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 4 - 7 9 6 3 Ž 9 8 . 0 0 0 3 7 - 2
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premiers metres. En bordure du Continent Antarctique, dans la Zone Saisonniere est ` ` des Glaces ou` la couche de melange ´ reduite et la biomasse elevee, Dans cette zone, les fractions de ´ ´ ´ la fraction phytoplanctonique ) 10 mm est predominante. ´ taille ) 10 mm, 2–10 mm et - 2 mm representent respectivement 46%, 25.1% et 28.9% de la biomasse totale integree ´ ´ ´ entre 0 et 100 m. Les populations naturelles y sont essentiellement composees ´ de grosses diatomees ´ et de dinoflagelles ´ qui representent respectivement 42.7% et 33.1% de la biomasse carbonee a` la diminution ´ ´ autotrophe. Vers le nord, parallelement ` de la biomasse, l’importance des algues picoplanctoniques et des flagelles ´ nanoplanctoniques autotrophes ŽCryptophycees ´ essentiellement. augmente fortement. Dans la Zone Oceanique, la fraction picoplanctonique represente 47.4% de la biomasse ´ ´ chlorophyllienne totale. Il y a une opposition entre la Zone Oceanique libre de glace caracterisee ´ ´ ´ par une biomasse faible dominee ´ par le picoplancton et la Zone Saisonniere ` des glaces ou` la biomasse relativement plus elevee ´ ´ est dominee ´ par les grosses diatomees. dans l’ensemble de l’ecosysteme ´ Cette dualite´ reflete ` la variabilite´ spatiale et temporelle qui prevaut ´ ´ ` pelagique antarctique. q 1998 Elsevier Science B.V. All rights reserved. ´ Keywords: Phytoplankton; Southern Ocean; Species composition; Austral summer
1. Introduction The size distribution of living particles is one of the main factors determining the food web structure and the global flux of organic matter in the marine environment. The classical view of the Antarctic food web structure was characterized by the predominance of large diatoms which form the basis of the food chain leading to krill ŽHasle, 1969; Guillard and Kilham, 1977.. Recently, Hewes et al. Ž1985. suggested an alternate microbial food web coexisting in parallel with the classical food chain. This carbon pathway taking place at the lower trophic level includes pico- and nano-sized primary and secondary producers ŽLancelot et al., 1991.. The presence of nano- and picoplanktonic microorganisms in the Southern Ocean is now recognized. These include small diatoms, flagellates, cyanobacteria and protozoa ŽGieskes and Elbrachter, 1986; Brandini and ¨ Kutner, 1987; Marchant et al., 1987; Becquevort et al., 1992; Menon et al., 1995.. However, the information available on their abundance, distribution and relative importance is still restricted. The question of the relative importance of the different size fractions within Antarctic water is not yet solved. Some studies report the preponderance of nanophytoplankton Žvon Brockel, 1981; Kosaki et al., 1985; Hosaka and ¨ Nemoto, 1986; Jacques and Panouse, 1991; Fiala and Delille, 1992; Jochem et al., 1995; Xiuren et al., 1996.. However, in others circumstances, picoplankton appears as an important component of the phytoplankton assemblage ŽHewes et al., 1985; Weber and El-Sayed, 1987; Carrada et al., 1994.. These scarce results, scattered in space and time, do not allow the
build up of a general picture for the whole Austral Ocean. Generally, diatoms are one of the dominant groups of the Antarctic phytoplankton community ŽHasle, 1969; Jacques et al., 1979; Kopczynska et al., 1986; El-Sayed and Fryxell, 1993. and are the major exporters of organic matter to deep ocean ŽTreguer et ´ al., 1995.. Their importance in the biomass Žboth in absolute and relative terms., however, shows a large temporal and spatial variability. In areas of greater water column stability and often at the beginning of the growth season, diatom biomass constitutes a major fraction of the phytoplankton biomass ŽJacques and Panouse, 1991; Kopczynska, 1992; Smetacek et al., 1992; Kopczynska et al., 1995. whereas during winter and in areas of intense mixing flagellate and dinoflagellate biomass exceeds that of diatoms ŽKopczynska, 1992; Garrison et al., 1993; Kopczynska et al., 1995.. The objective of the present paper is to gain information on Antarctic food webs by the way of analysis of the spatial variability of phytoplankton biomass, species composition and abundance and distribution of the size fractionated phytoplankton. This study was performed during the austral summer in the Indian sector of Antarctic Ocean between the Seasonal Ice zone and the Polar Front Zone. 2. Materials and methods 2.1. Sampling strategy Samples were collected during the Antares 2 cruise ŽRrV Marion Dufresne, 6 February–9 March 1994.
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Fig. 1. Location of the sampling stations during Antares 2 cruise Ž6 February–9 March 1994. along the 628E meridian transect. The 14 X X stations were spaced 1830 apart between 66840 S and 498S.
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conducted in the Indian sector of the Southern Ocean ŽFiala, 1995.. Fourteen stations, distributed along the 628E meridian transect between 498S and 66840X S, were studied while steaming northwards ŽFig. 1.. Sampling in the upper 250 m was performed using a Seabird CTD-O 2-fluorescence probe equipped with 12 Niskin bottles. 2.2. Size fractionation procedure and pigment analysis Size fractionation was performed at 14 stations between the surface Žor sub-surface. and 100 m. The fractionation was carried out by parallel filtering of subsamples of water Ž500 ml. through Nuclepore polycarbonate membranes of 10 mm and 2 mm pore-size and on a Whatman GFrF glass-fibre filter used as reference for the total chlorophyll ŽChl... Treatment of pigment samples was carried either by manual grinding of the filter in the presence of pure acetone ŽGFrF. or by dipping in 90% acetone ŽNuclepore. followed by an extraction lasting about 12 h at 58C and centrifugation for 7 min at 58C and 4000 rpm. Fluorescence of the acetone extract was successively measured on a Perkin-Elmer MPF 66 spectrofluorometer at six excitation and emission wavelengths ŽNeveux and Panouse, 1987.. Each coupled wavelength corresponded to the fluorescence excitation and emission of each pigment analysed: Chl. a, Chl. b, Chl. c, phaeophytins a, b and c. 2.3. Flow cytometry measurements Cell numbers in the ) 10 mm, 2–10 mm and ) 10 mm size fractions were determined from the different Nuclepore filtrates. Samples were fixed with a glutaraldehyde solution ŽMerck, final concentration ; 1%. and stored in liquid nitrogen as described by Vaulot et al. Ž1989.. A Bruker ACR-1000 flow cytometer was used for the analyses. We measured forward light scatter ŽFLS. as an indicator of size, orange fluorescence from phycoerythrin Ž580 " 40 nm. and red fluorescence from chlorophyll Ž680 " 20 nm. after excitation by the 480 mm light of mercury arc-lamp ŽSteen, 1986.. Instrument calibration was frequently monitored by analysing 0.94 mm and 1.96 mm fluorescent standard beads ŽPolysciences..
2.4. Microscopic cell counting and carbon biomass estimation Water samples for species identification and enumeration were taken over the upper 150 m depth at every station and fixed with hexamine-buffered formalin solution Žfinal concentration ; 0.4%.. Cells in a 50 ml subsample were counted under inverted microscope according the Utermohl method ¨ ŽUtermohl, ¨ 1958.. For each station three depths were counted: surface Ž; 10 m., the depth of the chlorophyll maximum and an intermediate depth. The cell volume of each species was calculated from cell sizes using appropriate cell geometry. Carbon biomass was estimated from cell volume and cell abundance using the conversion factors of Eppley et al. Ž1970.: log C s 0.76Žlog V . y 0.352 for diatoms and log C s 0.94Žlog V . y 0.6 for non-diatoms, where V and C are cell volume Žin mm3 . and cell carbon Žin pg., respectively. Only cells ) 2 mm can be quantified with this method, which thus excludes the biomass of picophytoplankton. 2.5. Statistical analysis An ordination technique was used to identify and arrange stations with similar species composition. As the gradient was very short Žgradient length - 2., we used Principal Component Analysis ŽPCA. which assumes a linear species response to the underlying environmental gradient ŽJongman et al., 1987.. Rare species which were encountered in less than 5% of the stations were excluded from the analysis and the biomass was log transformed to reduce the influence of few dominant species. Then PCA was applied to the depth integrated biomass data Žmg C my2 . using the Canocoe 3.10 version statistical package on a Macintosh computer ŽTer Braak, 1990..
3. Results 3.1. Phytoplankton biomass distribution along the 628E transect The main feature marking the study area was the general oligotrophy in terms of phytoplankton biomass. Chl. a concentrations in the upper 150 m
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Fig. 2. Distribution of Chl. a Žmg my3 . in the upper 250 m along the 628E transect from the Seasonal Ice Zone ŽSIZ. to the Polar Frontal Zone ŽPFZ..
ranged from 0.01 to 0.57 mg my3 ŽFig. 2.. Highest levels of Chl. a were located in the Seasonal Ice Zone ŽSIZ, south of 588S. in the vicinity of the
Antarctic Continent. In the southern area Žsts. A05 and A06., Chl. a showed higher concentrations in the upper 100 m. The maximum value Ž0.57 mg
Fig. 3. Vertical profiles of Chl. a in the - 2 mm, 2–10 mm and ) 10 mm size fractions along the 628E transect.
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my3 . was measured at the Antarctic Divergence Ž648S. at the 100 m depth which coincides with the depth of temperature minimum ŽE. Charriaud, personal communication.. This moderate deep biomass maximum decreased from South to North and disappeared in the Permanently Open Ocean Zone, POOZ Ži.e., north of 588S.. The POOZ is the poorest Antarctic area where Chl. a values ranged between 0.1 and 0.2 mg my3 . Moving northwards, phytoplankton biomass increased slightly with values around 0.3 mg Chl. a my3 in the vicinity of the Polar Frontal Zone ŽPFZ.. The concentration of phaeopigments was low and relatively uniform in the sub-surface water. The degradation ratio wi.e., phaeophytin arŽphaeophytin a q Chl. a.x averaged 0.10 in the upper 100 m, indicating a relative high level of Chl. a, and thus giving evidence of a good physiological condition of cells. Moreover, this ratio increased with depth and was on the average 0.20 at the deep chlorophyll maximum in the SIZ.
3.2. Size-fractionated phytoplankton distribution As with total Chl. a distribution, the different size fractions showed spatial variability. From south to north, the - 10 mm fraction was the major contributor to the total phytoplankton stocks but its relative contribution showed regional variations ŽFig. 3.. Inside this fraction the picoplankton dominated but its importance increased northwards. The ) 10 mm size fraction was more important in the SIZ than in the POOZ. However, its contribution increased in the vicinity of the PFZ Žst. A18.. The vertical distribution of the relative proportion of Chl. a in the different size fractions over the study area varied little ŽFig. 3.. However, in the SIZ, the biomass of the ) 10 mm fraction was highest at the Chl. a maximum layer between 80 m and 100 m depth. Along the transect total phytoplankton cell number as estimated by flow cytometry ranged between 1.6 = 10 3 cells mly1 and 4.2 = 10 3 cells mly1 in the surface water ŽFig. 4.. The picoplanktonic cells were
Fig. 4. Vertical profiles of cell numbers as measured by flow cytometry in the - 2 mm, 2–10 mm and ) 10 mm size fractions along the 628E transect.
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always numerically dominant representing 70% to 90% of the total abundance. Their maximum was observed at the Chl. a maximum depth, especially in the SIZ Žaround 5 = 10 3 cells mly1 .. The abundance of the 2–10 mm size-fraction decreased from the SIZ to the POOZ and increased slightly in the vicinity of PFZ. The ) 10 mm fraction showed a tendency to increase in numbers at the rich stations of the SIZ Žsts. A07 and A08. where it varied between 0.8 = 10 3 cells mly1 and 0.9 = 10 3 cells mly1 at 80 m depth. 3.3. RelatiÕe contribution of size-fractionated phytoplankton to the total Chl. a stock The Chl. a stock, integrated over the upper 100 m, decreased progressively from 31.7 mg my2 in the SIZ to 8 mg my2 in the POOZ and then increased to 25.9 mg my2 at 498S in the vicinity of the PFZ ŽFig. 5.. In the SIZ, the - 10 mm size fraction accounted for 54% of the Chl. a stock. Within this fraction, the picoplankton Ž- 2 mm. and the 2–10 mm fraction contributed about 28.9% and 25.1% of the Chl. a stock, respectively ŽTable 1.. While the contribution of these two size fractions was similar in the SIZ, the - 2 mm fraction dominated in the POOZ and PFZ ŽFig. 5 and Table 1.. The ) 10 mm size fraction accounted on the average for 46% of the Chl. a stock, with a maximum contribution of 64% at st. 11. At the deep Chl. a maximum layer, the ) 10 mm size fraction contributed about 50% of the total phytoplankton biomass. In the SIZ, the Chl. a stock in the ) 10 mm, 2–10 mm and - 2 mm size fractions were on the average 11.8, 6.5 and 7.5 mg my2 , respectively ŽTable 1.. In the POOZ, the - 10 mm size fraction represented 67.6% of the Chl. a stock ŽTable 1 and Fig. 5.. The picoplanktonic fraction was clearly dominant, contributing about 47.4% of the total biomass, corresponding to a mean value of 7.6 mg Chl. a my2 . The 2–10 mm and ) 10 mm fractions represented 20.2% Žmean ; 3.2 mg Chl. a m y2 . and 32.3% Žmean ; 5.2 mg Chl. a my2 . of the total Chl. a stock, respectively. 3.4. Carbon biomass and species composition Along the transect, integrated phytoplankton biomass, determined from microscope cell counts, ranged from 326.8 to 2056.6 mg C my2 . The latitudinal distribution pattern was similar to that of Chl.
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a, with a higher biomass in the SIZ Žmean ; 1332.2 mg C my2 . than in the POOZ Žmean ; 640.3 mg C my2 , Table 1.. Fig. 6 shows the distribution of carbon biomass of the main taxonomic groups. Diatom distribution exhibited large spatial variability; their biomass increased dramatically south of 588S ŽSIZ.. Dinoflagellate biomass decreased sharply between 66840X S and 62830X S and increased gradually in the northern part of the SIZ. On the contrary, the distribution of flagellates was rather uniform with the exception of two stations in the southern part of the transect. In the SIZ, the average composition was as follows: diatoms Ž42.7%., dinoflagellates Ž33.1%. and flagellates Ž24.2%.. In the POOZ, on the other hand, the composition of phytoplankton shifted towards dominance by dinoflagellates Ž41.7%.. Flagellates and diatoms contributed 30.2% and 27.8%, respectively ŽTable 1.. Among diatoms, centric species were the dominant types representing ; 69% of the total diatom biomass. In particular, in the vicinity of the PFZ Žsts. A17 and A18. they accounted for over 90% of the diatom biomass. Size fractionation, using cell equivalent spherical diameter ŽESD., indicated that the phytoplankton community in the SIZ was dominated by a microphytoplankton assemblage, ESD ) 20 mm Ž56.5%; Table 1.. Nanophytoplankton ŽESD - 20 mm. represented about 43.5%, of which 23.8% was due to the 10–20 mm fraction. On the contrary, in the POOZ the nanophytoplankton was dominant, representing about 71.3% of the total biomass. Both in the SIZ and POOZ, the 10–20 mm size fraction accounted for over 50% of the nanoplankton biomass. It should be kept in mind that the microscopic cell counts exclude the biomass of picoplankton ŽESD - 2 mm.. This has two consequences: underestimating total carbon biomass and overestimating the relative contributions of the nano- and microphytoplankton. The carbonrChl. a ratio ranged from 20.7 to 203.9 Žmean ; 95.. Low CrChl. values were observed in the vicinity of PFZ. As the sampling was done late in the growth season, the relatively high CrChl. ratio might suggest a declining community. 3.5. Phytoplankton community analysis Since the species data showed large spatial variability, plots of species and sample Žstations. scores
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Fig. 5. Distribution of integrated Chl. a Župper. and percentage contribution to total integrated Chl. a Žlower. in the - 2 mm, 2–10 mm and ) 10 mm size fractions for the 14 stations located along the 628E transect.
were used to characterize the different zones in terms of species composition. The results of PCA are shown in Fig. 7. The eigenvalues were relatively high Ž l1 s 0.29, l2 s 0.16. and these two axes alone explained about 45% of the species variance. Moreover, the third and fourth eigenvalues were smaller compared to the first two axes which indicates that
there were only two major gradients in the species data. Four clusters of stations are apparent from the plots of sample scores ŽFig. 7.. The first axis separates stations in the SIZ from the POOZ. On the other hand, the second axis separates the two subgroups within each main group. Thus, within the SIZ
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Table 1 Summary of mean integrated phytoplankton biomass Žcarbon and chlorophyll a. in the SIZ and in the POOZ during cruise Antares 2 SIZ
Total C biomass Diatom biomass Dinoflagellate biomass Flagellate biomass C biomass - 10 mm C biomass 10–20 mm C biomass ) 20 mm
POOZ
mg C my2
% of total C
mg C my2
% of total C
1333.2 569.3 441.8 322.1 262.4 317.7 753.0
42.7 33.1 24.2 19.7 23.8 56.5
640.3 177.9 267.0 193.2 221.0 235.6 183.8
27.8 41.7 30.2 34.5 36.8 28.7
SIZ
POOZ y2
mg m Total Chl. a Chl. a - 2 mm Chl. a 2–10 mm Chl. a ) 10 mm
25.8 7.5 6.5 11.8
% total Chl. a
mg my2
% total Chl. a
28.9 25.1 46.0
16.0 7.6 3.2 5.2
47.4 20.2 32.3
stations A05, A06 and A07, located south of the Antarctic divergence, from the first cluster ŽCluster I. whereas sts. A08, A09, A10 and A11, located
between the Antarctic divergence and the outer limit of the SIZ, constitute the second cluster ŽCluster II.. In the POOZ, sts. A12, A13 and A14 constitute
Fig. 6. Integrated phytoplankton biomass distribution along the 628 E meridian transect ŽSquaress diatoms, open triangless flagellates and open circles s dinoflagellates..
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cluster III and the rest Žsts. A15, A16, A17 and A18. forms cluster IV. The latter group includes stations at or in the vicinity of the PFZ. The position of a species in the PCA biplot ŽFig. 7. indicates the direction in which the biomass of
that species increases most and the length of a species head from the centre indicates the rate of change of the biomass of that species in that direction ŽJongman et al., 1987.. Thus, cluster I is characterized by greater biomass of small pennate diatoms
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such as Nitzschia cylindrus ŽGrunow. Hasle and many flagellates such as Pyramimonas spp., small comma-shaped flagellates as well as other small unidentified flagellates ŽEDS - 5 mm.. Silicoflagellates were more abundant in stations south of the Antarctic divergence. In Cluster I they represented about 15% of the total biomass. Their position in the plot is, however, contrary to the expected. Since they were mainly present in the SIZ, the first axis explains only a very low percentage of their variance Ž; 2.5%.. Therefore, their position is not well represented. A relatively rich and diverse phytoplankton assemblage characterizes the second cluster. This can be inferred from the number and length of species axes Žmost of them diatoms. pointing to this cluster. Large pennate and centric diatoms were present in this cluster. These include members of the genera Nitzschia, Pseudonitzschia, Tropidoneis, Thalassiothrix, Thalassiosira and Chaetoceros, which often constitute a large fraction of the total biomass. Stations of Cluster III are located at the outer limit of the SIZ and are characterized by greater abundance of Nitzschia kerguelensis ŽO’Meara. Hasle and NaÕicula spp. At st. A12 N. kerguelensis alone accounted for about 11% of the total biomass. Stations in Cluster IV are located at or in the vicinity of the PFZ and are characterized by greater biomass of large centric diatoms, such as Proboscia spp. and Corethron criophilum Castracane, and flagellates such as Cryptophytes. C. criophilum was present over the whole transect with an average relative contribution of 10.3%. Although the diatom biomass was low in the POOZ, C. criophilum together with N. kerguelensis represented a significant proportion of the total biomass. Moreover, C. criophilum is known to be very abundant when the phytoplankton biomass is low and when the ambient silicate to nitrate ratio is
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high ŽSommer, 1991.. Flagellates such as Cryptophytes were very abundant in most stations. About 16% of the total biomass and 64% of the flagellate biomass were due to Cryptophytes. An unidentified flagellate similar in morphology to Phaeocystis was very abundant in the POOZ and accounted for about 35% of the flagellate biomass. The first axis correlates negatively with the total phytoplankton biomass Ž r 2 s 0.5. and, in particular, with the biomass of the larger size fraction Ži.e., ESD ) 10 mm.. As can be seen from the biplot ŽFig. 7., there are few species with long axes pointing to the stations located close to the ‘origin’ ŽCluster IV., indicating dominance by a few very abundant species. On the other hand, stations at the opposite side of the ‘origin’ ŽCluster II. are characterized by high species diversity Ži.e., many species with relatively short axes pointing to Cluster II stations.. Thus, along the first axis the phytoplankton assemblage changes from a rich and diverse assemblage dominated by large pennate diatoms in the SIZ ŽCluster I and II. to a relatively poor and less diverse assemblage dominated by Cryptophytes and few large centric diatoms in the POOZ ŽCluster III and IV..
4. Discussion Our results show a clear picture of the late summer phytoplankton community structure in different functional zones in the Indian sector of the Southern Ocean. The main striking features of this region are the low phytoplankton biomass and the spatial variability in phytoplankton biomass and community structure. The low phytoplankton biomass observed during this study corroborates the general oligotrophic nature of the Indian sector of the Southern Ocean ŽJacques and Minas, 1981; Jacques and
Fig. 7. Plot of sample Župper. and species scores Žlower. of the first two axes of principal component analysis ŽEigenvalues: l1 s 0.29, l2 s 0.16.. Ampdins Amphidinium spp.; Ast spp.s Asteromphalus spp.; Cent dia s centric diatoms; Chae spp.s Chaetoceros spp.; Chae bal s Chaetoceros bulbosum ŽEhrenberg.; Chae cri s Chaetoceros criophilum Castracane; Chae dic s Chaetoceros dichaeta ŽEhrenberg.; Com spp s comma-shaped flagellates; Cor cri s Corethron criophilum Castracane; Cos spp.s Coscinodicus spp.; Crypt spp.s Cryptophyte spp.; Dact spp.s Dactyliosolen spp.; Dinoflas Dinoflagellate spp.; Gym din s Gymnodinium spp.; Nav spp.s NaÕicula spp., Nit ang s Nitzschia angulata Hasle; Nit cyl s Nitzschia cylindrus ŽGrunow. Hasle; Nit ker s Nitzschia kerguelensis ŽO’Meara. Hasle; Nit spp.s Nitzschia spp.; Oth fla s Other flagellates; Proroc s Prorocentrum spp., Prob spp.s Proboscia spp.; Pseunits Pseudonitzschia spp.; Pyr spp.s Pyramimonas spp.; Rhiz chu s Rhizosolenia chunii Karsten; Rhiz spp.s Rhizosolenia spp.; Sil spp.s Silicoflagellate spp.; Tharix s Thalassiothrix spp; Thasir s Thalassiosira spp; Tropids Tropidoneis spp.; Unid fla s Unidentified flagellates.
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Fukuchi, 1994.. Moreover, the spatial variability observed during this cruise is a microcosm reflection of the heterogeneity of the Southern Ocean pelagic ecosystem in terms of phytoplankton biomass and community structure. Data on the seasonal variation for this part of the Southern Ocean are scarce. Sasaki Ž1984. reported higher phytoplankton biomass in the SIZ during spring Žmean Chl. a s 0.61 mg my3 . than in the summer period Žmean Chl. a s 0.19 mg my3 .. Our study area was investigated recently during early spring ŽAntares 3 cruise, October 1995. and the results show low biomass and dominance by diatoms in the SIZ and by flagellates in the POOZ ŽM. Semeneh et al., in press.. The phytoplankton community analysis confirms the presence of three functional units: SIZ, POOZ and PFZ ŽTreguer and Jacques, 1992.. In the SIZ the ´ phytoplankton community structure is characterized by a relatively rich, diatom dominated microplankton Ž) 20 mm. assemblage. On the contrary, the POOZ is characterized by a low biomass and a phytoplankton community predominantly composed of autotrophic pico- and nanoflagellates. The greater importance of the microphytoplankton with increasing biomass in the SIZ agrees with the observations of Sasaki Ž1984. in this sector of Southern Ocean. The above functional zones occupied parallel belts of latitude and displayed a north–south gradient in biomass, composition and size distribution of the phytoplankton community. Superimposed on this gradient was a positive gradient of nutrient availability ŽGoeyens, 1995.. Areas of greater diatom biomass such as the SIZ were characterized by high silicate and nitrate availability whereas regions of relative low silicate and nitrate concentrations in the North were characterized by poor diatom biomass and greater importance of small size fraction Žmainly picoplankton.. The distribution of phytoplankton biomass and community structure along the transect appears to be the reflection of the prevailing environmental variations, especially that of temperature. The distribution of temperature varied along the transect. Cold and more saline surface water with a rather uniform vertical temperature profile characterized stations south of the divergence ŽCluster I, Fig. 8.. On the other hand, relatively warm and less saline surface water with a pronounced subsurface temperature
minimum was present in the stations located between the divergence and the northern limit of the ice cover ŽCluster II, Fig. 8.. This region is characterized by the predominance of diatoms under greater water column stability, evidenced by shallow and steep vertical temperature gradients. This fact corroborates the conclusion of Kopczynska Ž1992. that diatoms dominate in areas of greater water column stability and low krill concentration. Moreover, the SIZ was characterized by the presence of a deep chlorophyll maximum which appeared to be closely associated with the temperature minimum. A phytoplankton assemblage dominated by large diatoms was located below the euphotic zone Žmean depth ; 70 m. and exhibited low photosynthetic capacity ŽP. Treguer, ´ personal communication.. The depth of the chlorophyll maximum in the SIZ deepened upon moving northwards. Although the deep chlorophyll maximum in oligotrophic low latitude oceans is related to nutrient deficiency ŽGould, 1987., its significance in nutrient rich areas such as the Southern Ocean remains unclear. When Chl. a concentration in the upper 200 m depth was plotted against water temperature, different response curves were observed in the SIZ and POOZ ŽFig. 9.. In the SIZ the ambient temperature was - 28C and the relationship was parabolic Žunimodal. with a maximum around 08C. In contrast, in the POOZ the ambient temperature was ) 18C and the relationship was linear. Different ranges of temperature exposure and different response curves indicate different ecophysiological adaptations in these functional zones. In the SIZ ‘warm’ deep water lies below cold surface winter water and higher biomass mainly due to large diatoms was observed around 08C which suggest optimum temperature as a downward driving factor of the deep chlorophyll maximum. Generally, the growth of polar microalgae appears to be controlled by temperature ŽKirst and Wiencke, 1995.. Moreover, some of the dominant species in the SIZ such as C. criophilum and N. kerguelensis are obligatory psychrophylic and exhibit maximum growth below 58C ŽFiala and Oriol, 1990.. The differences in phytoplankton community structure between the SIZ and POOZ are also reflected by the food web structure. Low phytoplankton biomass in this sector of the Southern Ocean
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Fig. 8. Vertical profile of water temperature, phytoplankton biomass and nitrate concentration in four representative stations: st. A06 ŽCluster I., st. A08 ŽCluster II., st. A13 ŽCluster III., st. A18 ŽCluster IV..
does not attract large grazers such as krill; therefore, microzooplankton such as ciliates are expected to structure the phytoplankton community. Ecosystems
of this type would be largely based on regenerated Žammonium. production. Despite differences in community structure, the community both in the SIZ and
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Fig. 9. Relationship between water temperature and phytoplankton biomass in the upper 200 m depth for stations located in the SIZ Župper. and in stations located in the POOZ Žlower..
POOZ was predominantly based on regenerated production ŽSemeneh et al., unpublished data.. Traditionally new production is associated with a diatom dominated microplankton assemblage and regenerated production with a flagellate dominated nano- or picoplankton assemblage. In the POOZ, the observed
phytoplankton community structure, a nano- and picoplankton dominated assemblage is consistent with the expected production regime Žnew production.. In the SIZ, on the other hand, the observed community structure dominated by a diatom microplankton assemblage was not in agreement with the expected
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production regime Žregenerated production.. This, however, supports the recent hypothesis that under conditions of prolonged water column stability and reduced grazing pressure on microphytoplankton, a shift in nitrogen uptake regime Ži.e., from new to regenerated production. during the growth season can occur without a large change in phytoplankton community structure ŽSemeneh et al., 1998.. Both reduced grazing pressure on large cells and persistent water column stability reduce loss rates, and these conditions enable diatoms to overstay in the late season. Several studies in the Southern Ocean have shown that, despite high nitrate availability, phytoplankton preferentially utilizes ammonium and, unlike low latitude ecosystems, the shift from new to regenerated production occurs before nitrate is exhausted ŽGlibert et al., 1982; Ronner et al., 1983; Goeyens et ¨ al., 1991; Jacques, 1991; Owens et al., 1991; Semeneh et al., 1998.. Heterotrophic activity during the season increases ammonium availability, leading to greater contribution to the total nitrogen requirement of phytoplankton and predominance of regenerated production. During this cruise the phytoplankton community was in a state of decline, evidenced by a high CrChl. ratio and low turnover rates of carbon and nitrogen ŽSemeneh et al., unpublished data.. For such community, greater dependence on ammonium Žregenerated production. is advantageous considering the higher energy and iron requirement of nitrate assimilation Žnew production.. Moreover, as our study area was sampled late in summer and much of the herbivory was by microheterotrophs ŽMenon et al., 1995., large diatoms can escape predation and subsist on ammonium.
Acknowledgements This study was carry out during the Antares 2 cruise sponsored by CNRS ŽJGOFS-France Program. and IFRTP. We thank G. Vetion for assistance with the flow cytometric analysis and Dr C. Lancelot for giving access to laboratory facilities. We are grateful to the captain and crew members of RrV Marion Dufresne for their cooperation. The authors are grateful to two anonymous reviewers for their critical comments.
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