.

Journal of Marine Systems 17 1998 159177

Nitrogen uptake regime and phytoplankton community structure
in the Atlantic and Indian sectors of the Southern Ocean
M. Semeneh
a
, F. Dehairs
a
, M. Elskens
a
, M.E.M. Baumann
b
, E.E. Kopczynska
c
,
C. Lancelot
d
, L. Goeyens
a,)
a
( ) ( ) Analytische Chemie ANCH , Vrije Uniersiteit Brussel VUB , Pleinlaan 2, B-1050 Brussels, Belgium
b
( ) Alfred Wegener Institut fur Polar-und Meeresforschung AWI , Postfach 120161, D-27515 Bremerhaen, Germany
c
Department of Antarctic Biology, Polish Academy of Sciences, Ustrzycka 10, 02141 Warsaw, Poland
d
( ) ( ) Groupe de Microbiologie des Milieux Aquatiques GMMA , Uniersite Libre de Bruxelles ULB , Campus de la Plaine, CP 221,
Bouleard du Triomphe, 1050 Brussels, Belgium
Received 15 December 1995; accepted 15 October 1996
Abstract
Phytoplankton nitrogen uptake is studied in relation to the biomass and structure of phytoplankton community in the
Atlantic and Indian sectors of the Southern Ocean. Two scenarios of seasonal evolution of uptake regime and phytoplankton
community structure are described. The first scenario includes the Marginal Ice Zone areas of the Weddell Sea and adjacent
areas where a predominantly nitrate based, diatom dominated assemblage, thriving in a stable water column at the beginning
of the season was transformed into a mainly ammonium based, flagellate dominated assemblage, towards the end of the
season. The change in phytoplankton community structure was caused by selective grazing by large grazers and reduced
stability of the water column and the shift in uptake regime was due to increased ammonium availability and changes in
.
community structure. In the second scenario, in the Coastal and Continental Shelf Zone CCSZ and Open Oceanic Zone
.
OOZ of the Indian sector, a shift in uptake regime occurred without a big change in phytoplankton community structure.
These areas were sampled late in the growth season and were characterized by prolonged water column stability, less grazing
pressure on large diatoms and high ammonium availability. Diatoms dominated the assemblage and about 80% phytoplank-
ton biomass was on the )10 mm size fraction. Unlike the first scenario, diatoms were largely based on ammonium. Thus,
in areas of persistent water column stability and less selective grazing pressure, a shift in uptake regime can occur without
change in community structure. The dominance of diatoms under regenerated production provides a physiological evidence
for the excess net removal of silicate over nitrate occurring in certain provinces of the Southern Ocean.
Resume
Lassimilation dazote dans les secteurs Atlantique et Indien de lOcean Austral est etudiee en fonction de la biomasse et
de la structure de la communaute phytoplanctonique. Deux scenarios decrivant levolution saisonniere du regime dassimila- `
tion et les changements de structure dans la communaute du phytoplancton sont presentes. Au debut de la saison, dans la
zone marginale des glaces de la mer de Weddell, les nitrates representent la principale source dazote avec un assemblage
)
Corresponding author. Tel.: q32-2-629-3264; Fax: q32-2-629-3274; E-mail: Leo.Goeyens@ihe.be
0924-7963r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved.
. PII: S0924- 7963 98 00036- 0
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 160
phytoplanctonique domine par les diatomees. Vers la fin de la saison, le taux dabsorption de lammonium est preponderant
et lassemblage du phytoplancton est domine par des flagelles. Les changements de structure dans la communaute du
phytoplancton sont attribues a un broutage selectif et a une reduction de la stabilite de la colonne deau, tandis que la ` `
transition du regime dassimilation est imputee a un accroissement de la disponibilite en ammonium et a levolution de la ` `
communaute du phytoplancton. Pour la zone cotiere et du plateau continental, ainsi que locean ouvert dans le secteur `
Indien, une transition du regime dassimilation est observee sans changements importants dans lassemblage du phytoplanc-
ton. Ces zones, qui ont ete echantillonnees a la fin de la saison de croissance, sont caracterisees par une grande stabilite de la `
colonne deau, une pression de broutage faible sur les larges diatomees et une haute disponibilite en ammonium. Les
diatomees dominent avec environ 80% de la biomasse du phytoplancton )10 mm. Au contraire du scenario decrit pour la
mer de Weddell, lammonium represente la principale source dazote pour les diatomees. En consequence, dans les zones ou `
la stabilite de la colonne deau persiste, et ou la pression de broutage est moindre, une transition du regime dassimilation `
peut survenir sans etre associee necessairement a un changement de structure dans la communaute phytoplanctonique. `
Dautre part, la predominance de diatomees sous un regime de production de type regenere est un argument en faveur
dobservations anterieures montrant que certaines provinces de lOcean Austral sont caracterisees par des depletions en
silicate excedant celles des nitrates. q1998 Elsevier Science B.V. All rights reserved.
Keywords: Nitrogen uptake; Phytoplankton community structure; Southern Ocean; Seasonal variability
1. Introduction
Considering its nutrient potential for primary pro-
duction, the Southern Ocean falls within the High
.
Nutrient Low Chlorophyll HNLC trophic category
showing a very low capacity to utilise the available
.
nutrient Dugdale and Wilkerson, 1991 . Phytoplank-
ton biomass and primary productivity are, however,
controlled by several bottom-up and top-down fac-
tors whose relative importance can change in time
and space. Despite functional oligotrophy, large spa-
tial and seasonal variability in production and nutri-
ent regime occur in the Southern Ocean pelagic
.
ecosystem El-Sayed, 1988 . This has led to the view
that several functional units constitute the Southern
Ocean pelagic ecosystem each with different mecha-
nisms of control on phytoplankton and nutrient dy-
.
namics Treguer and Jacques, 1992 . For example,
high biomass and enhanced primary productivity oc-
.
cur in the Marginal Ice Zone MIZ , Coastal and
.
Continental Shelf Zone CCSZ and Polar Front
.
Zone PFZ whereas low biomass and productivity
prevail in the Permanently Open Oceanic Zone
.
POOZ El-Sayed et al., 1983; Smith and Nelson,
1985; El-Sayed, 1988; Smith and Nelson, 1990;
Jacques and Panouse, 1991; Smetacek et al., 1992;
Treguer and Jacques, 1992; Kang and Fryxell, 1993;
Jacques and Fukuchi, 1994; Kopczynska et al., 1995;
.
Fiala et al., 1998 .
One of the widely used methods for assessing the

production regime of a pelagic ecosystem new vs.

.
regenerated production is the f-ratio which is sim-
ply the fraction of total primary production which
results from the assimilation of newly available ni-
.
trogen, mainly nitrate Eppley and Peterson, 1979 .
When averaged over an appropriate time scale it can
be equated to export production. Field nitrogen up-
take studies involve the measurement of uptake rates:
absolute and specific uptake rates. Since these uptake
parameters are community responses, they are af-
fected by the biomass and structure of the au-
totrophic community. Most uptake studies in the
Southern Ocean often relied on bulk parameters such
.
as particulate nitrogen PON and chlorophyll Chl
.
a concentrations, disregarding the above aspects

Glibert et al., 1982; Ronner et al., 1983; Smith and

Nelson, 1990; Goeyens et al., 1991a; Kristiansen et
.
al., 1992 . Simultaneous studies on nitrogen uptake
and phytoplankton community analysis are scarce
and, hence, it is difficult to make generalisations.
In low latitude oceans, where nitrogen limits pri-
mary productivity, diatoms dominate the phytoplank-
ton assemblage when ambient nitrate concentration

is high. In these ecosystems new production nitrate

.
based production is usually associated with domi-
nance of diatoms andror dinoflagellates. In the
Southern Ocean diatoms represent the most impor-
tant phytoplankton group and their silica deposit on
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 161
the ocean floor bears a direct evidence for their

significant contribution in export production Treguer

.
et al., 1995 . Their relative importance exhibits large
spatial and temporal variability. In this ecosystem
nitrate concentrations hardly reach limiting levels

with strong preference for ammonium Glibert et al.,

1982; Ronner et al., 1983; Probyn and Painting,
1985; Smith and Nelson, 1990; Owens et al., 1991;
.
Goeyens et al., 1991a, 1995 . In some parts of the
Southern Ocean the net removal of silicate during
the growth season exceeds that of nitrate and this
uncoupling of Si and N cycles in surface waters is

due to the rapid cycling of N as ammonium Treguer

.
and Jacques, 1992; Goeyens et al., 1998 .
Depending on the underlying biological and
physico-chemical factors governing the growth and
maintenance of phytoplankton in the euphotic zone,

a shift in nitrogen uptake regime i.e., from new to

.
regenerated production can proceed with or without
big change in community structure. For example, in
the ScotiaWeddell Confluence marginal ice zone
.
MIZ a shift in uptake regime from a predominantly
new production to regenerated production was ac-
companied by a change in phytoplankton assemblage
from a rich, diatom dominated, microplankton as-
semblage to a cryptophyte dominated nanoplankton

assemblage Goeyens et al., 1991a,b; Jacques and

.
Panouse, 1991 . Whereas the change in community
structure is caused by selective grazing by large
grazers such as krill and reduced water column
stability, the shift in uptake regime is driven by
enhanced ammonium availability and by the change
in community structure itself. In other hydrographic

zones such as in the CCSZ of Prydz Bay Kopc-

.
zynska et al., 1995 and in the Southern part of the
.
Weddell Sea Nothig et al., 1991 blooms of di-
atoms, which usually appear early in the season,
were observed late in the growth season. These areas
are characterized by stable water column and en-

hanced heterotrophic activity hence high ammonium

.
availability . In these areas, unlike the MIZ, diatoms
were dominant under predominance of regenerated
.
production Semeneh, 1992 .
Here we discuss the biomass and structure of the
phytoplankton community and uptake regime from
several expeditions in the Atlantic and Indian sectors
of the Southern Ocean. For the first time we docu-
ment the nitrogen nutrition of phytoplankton in a
shallow and highly productive coastal and continen-
tal shelf zone of the Prydz Bay area. Our main
objectives are to show that a shift from new to
regenerated production can proceed with or without
a shift in phytoplankton community structure. In
particular, we describe the dominance of diatoms in
a system where regenerated production is predomi-
nant.
2. Materials and methods
2.1. Sampling
Samples were collected during five cruises in the
Atlantic and Indian sectors of the Southern Ocean
.
Fig. 1 . Table 1 shows the regions and sampling
periods of all cruises. The sampling periods and sites
cover different functional zones and different stages

of the growth season. The ANTARKTIS IXr2 ANT

. .
IXr2 and ANTARKTIS Xr7 ANT Xr7 cruises
in the Weddell Sea were done on the same transect
except differences in sampling period and direction

of cruise track. Moreover, the Larsen Shelf the

.
south-western part of the Weddell Sea was investi-
gated during the ANT Xr7 cruise. For each cruise
physico-chemical parameters such as temperature,
salinity, nitrate, ammonium, phosphate and silicate
as well as biological parameters such as Chl a, PON
.
and particulate organic carbon POC concentrations
were measured according to the standard protocols
and the details are in their respective cruise reports

Goeyens et al., 1991c; Van Bennekom and Veth,

.
1991; Fiala, 1994 . B. Tilbrook and S. Wright pro-
vided us the physico-chemical data for the Marine
.
Science Voyage 6 cruise MSV 6 .
2.2. Phytoplankton counting
Samples for phytoplankton count were taken from
.
the surface layer upper 20 m and fixed with a

hexamine buffered formalin solution final concen-

.
tration ;0.4% . A subsample of either 10 or 50 ml
was settled for 24 h and counted under inverted
microscope according to the Utermohl method
.
Utermohl, 1958 . Cell volume was calculated using
cell dimensions and appropriate cell geometry. Cell
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 162
. Fig. 1. Map showing the locations of the study areas in the Seasonal Ice Zone, SIZ indicated by the solid line , of the Southern Ocean.
. . 1sEPOS LEG 2 cruise ScotiaWeddell Confluence zone ; 2 and 3sANTARKTIS IXr2 and Xr7 cruises Weddell Sea ; 4sMarine
. . . Science Voyage 6 cruise Prydz Bay ; 5sANTARES 2 cruise 628E meridian transect . The Polar Front PF is indicated by dashed line.
. Adapted from Treguer and Van Bennekom 1991 .
.
carbon C, pg was estimated from cell volume V,
3
.
mm using the conversion factor of Eppley et al.
. .
1970 : logCs0.76= logV y0.352 for diatoms
.
and logCs0.94= logV y0.6 for non-diatoms. No
attempt was made to distinguish between autotrophic
and heterotrophic dinoflagellate species except few
known heterotrophic species. With this method only
cells )2 mm were counted. It is worth mentioning
that this method can overestimate cell carbon due to
errors associated with determining cell volumes.
Nevertheless, it provides an invaluable information
on the composition and structure of the phytoplank-
ton community. Data on phytoplankton biomass dur-
ing the EPOS LEG 2 were kindly provided by S.
Becquevort.
2.3. Nitrogen uptake rates
Uptake rates of nitrate and ammonium by phyto-
.
plankton in the surface layer 020 m were mea-
sured using the
15
N tracer technique. Surface water
sample in 2.7 l sized polycarbonate bottle was en-
15 15

15
.
riched either with NO or NH 99% N and
3 4
incubated for 24 h under natural light in a Plexiglas
on-deck incubator in which surface sea water tem-
perature was maintained by a continuous flow of

surface sea water. Addition of labelled nitrogen i.e.,

15 15
.
NO or NH increased the ambient concentra-
3 4
tion by about 10%. At the end of the incubation
period the water sample was filtered on a precom-
.
busted 4508C Whatman GFrF glass-fibre filter,
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 163
Table 1
Locations of the study areas and their sampling periods in the Atlantic and Indian sectors of the Southern Ocean
Sector Cruise Region Position Sampling period Research vessel
Atlantic EPOS LEG 2 ScotiaWeddell Confluence 57861850 S 20.11.8807.01.89 Polarstern
. NorthSouth transect 47498W
. ANTARKTIS IXr2 ANT IXr2 Weddell Sea 6382671805 S 14.11.9030.12.90 Polarstern
. WestEast transect 128153837 W
. ANTARKTIS Xr7 ANT Xr7 Weddell Sea 6383271812 S 03.12.9222.01.93 Polarstern
. EastWest transect 0882461811 W
. . Indian Marine Science Voyage 6 MSV Prydz Bay Grid 6583769837 S 03.01.9120.03.91 Aurora Australis
6784978811 E
ANTARES 2 Indian Sector 4983566841 S 26.01.9423.03.94 Marion Dufresne
. NorthSouth transect 628E
dried and sealed in a petri-dish for later
15
N analysis.
In order to measure the
15
N abundance in particulate
material all PON has to be converted to N gas. A
2
discharge tube containing a subsample of particulate
material together with CuO rods and CaO bricks was

y5
.
subjected to a high vacuum pressure -10 mbar
with occasional heating to remove atmospheric and
adsorbed gases. Then the samples were combusted at
7508C for 8 h.
15
N abundance was measured by
emission spectrometry.
Uptake rates of nitrate and ammonium were cal-
.
culated according to Dugdale and Wilkerson 1986 .
The ammonium uptake rates are not corrected for
isotope dilution. For each nutrient two uptake param-
eters were calculated: absolute and specific uptake

y1
.
rates. Absolute uptake rates r , nM day repre-
N
sent the amount of nitrogen taken up during the

incubation period whereas specific uptake rates n ,

N
y1
. .
h represent the normalised by PON uptake rates
or the turnover rates of cell nitrogen. f-ratio was
.
calculated according to Eppley and Peterson 1979 .

f-ratio)0.5 indicates predominance of new nitrate

.
based production. Other nitrogen sources such as
urea, nitrite and amino acids were not considered.
2.4. Statistical analysis
Multivariate techniques such as principal compo-
.
nent analysis PCA were used to identify stations
with similar physico-chemical and biological charac-
teristics. Only stations in the seasonally ice covered
. .
zone SIZ were considered Fig. 1 . The parameters
include: temperature, salinity, nitrate, ammonium

availability i.e., the percentage of ammonium in the

.
total dissolved inorganic nitrogen, DIN , phosphate,
silicate, Chl a and POC concentrations. Prior to the
analysis, all parameters were standardised to over-
come differences in measurement units. Then PCA
was applied using a CANOCOe 3.10 statistical
.
package Ter Braak, 1990 .
3. Results
3.1. Physico-chemical characteristics
3.1.1. Weddell Sea
Table 2 shows the summaries of the physico-
chemical and biological characteristics of the surface
water during different cruises. During ANT IXr2
.
cruise 1990 near freezing surface temperature ;
. .
y1.738C , high salinity ;34.36 , high nutrient
.
concentration NO s29.4 mM and low phyto-
3

y1
.
plankton biomass Chl as0.1 mg l indicated a
near winter water situation. Most parameters showed
very small variability indicating a high degree of
spatial homogeneity.
Due to large spatial variability in most parameters
during the ANT Xr7 cruise, principal component
analysis was used to identify stations with similar
physico-chemical and biological characteristics.
Three clusters of stations representing three different
stages were identified: Central Weddell Sea, Eastern
.
Weddell Sea and Larsen Shelf Table 2 . Separate
PCA analysis on species biomass data gave similar
.
groups of stations data not shown . The first group
.
Central Weddell Sea consisted of stations in the
(
)
M
.
S
e
m
e
n
e
h
e
t
a
l
.
r
J
o
u
r
n
a
l
o
f
M
a
r
i
n
e
S
y
s
t
e
m
s
1
7
1
9
9
8
1
5
9

1
7
7
1
6
4
Table 2
. Summaries mean and standard deviation of the physico-chemical and biological characteristics of the surface water at various regions in the seasonally ice covered zone
. n Temperature Salinity NO PO Si OH NH Av. POC Chl a
3 4 4 4
y1 y1
. . . . . . . . 8C mM mM mM % mg C l mg l
. Weddell Sea ANT IXr2 9 y1.73"0.12 34.36"0.03 29.4"1.1 2.0"0.1 72.4"7.3 0.5"0.3 36.8"17.8 0.1"0.1
. Central Weddell Sea ANT Xr7 16 y1.26"0.42 33.95"0.22 27.6"1.4 1.9"0.1 71.7"2.6 1.0"0.6 117.6"68.9 0.4"0.5
. Eastern Weddell Sea ANT Xr7 4 y1.36"0.44 34.23"0.02 24.5"3.2 1.7"0.2 58.3"1 0.8"0.3 350"148.5 3.7"1.5
. Larsen Shelf ANT Xr7 5 y0.67"0.61 33.75"0.16 15.9"3.6 1.1"0.2 60.6"13 0.8"0.7 474"105.2 3.8"0.8
ScotiaWeddell, SWC A 8 y1.41"0.27 33.84"0.27 27.9"2.9 1.7"0.2 72.5"6.0 0.7"0.5 121"68.5 1.2"0.8
ScotiaWeddell, SWC B 6 y0.29"0.68 33.59"0.17 22.3"3.4 1.4"0.3 62.5"10.2 4.7"2.4 157.4"53 1.0"0.8
. Prydz Bay, CCSZ MSV 6 4 y0.15"0.47 33.49"0.51 12.9"4.5 0.9"0.3 31.7"11.6 0.9"0.5 412"182 ND
. Prydz Bay, OOZ MSV 6 5 0.98"1.12 33.81"0.09 26.8"0.9 1.8"0.1 42.2"7.4 1.0"0.8 84.3"30.6 ND
ANTARES 2, OOZ 4 0.40"0.54 33.92"0.13 28.0"0.4 1.8"0 42.6"6.7 1.5"0.2 62.4"26 0.2"0.1
NDsno data.
nsNumber of stations.
NH Av.sammonium availability
4
. SWCsScotiaWeddell Confluence zone SWC Asearly season and SWC Bslate season .
CCSZsCoastal and continental shelf zone.
OOZsOpen oceanic zone.
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 165
central Weddell Sea with physico-chemical charac-
teristics very similar to ANT IXr2 but with slightly
.
lower nitrate concentrations ;27.6 mM and

slightly higher phytoplankton biomass Chl as0.4

y1
.
mg l . This group and the ANT IXr2 stations
indicate the early stage of the growth season. The
.
second group of stations Eastern Weddell Sea were
located in the extreme eastern part of the transect
.
Table 2; Fig. 1 . These are shallow stations charac-
.
terized by low surface temperature ;y1.368C ,
.
high salinity ;34.23 and moderate levels of
.
nutrients NO s24.5 mM; Fig. 2 . Phytoplankton
3
bloom was apparent with surface Chl a concentra-
tions in some stations reaching up to 6 mg l
y1
. A
.
very sharp and shallow pycnocline 1030 m indi-
cated a stable water column. Despite shallow pycno-

y1
.
cline, high Chl a concentrations )1 mg l ex-
tended down to 75 to 100 m depth. The third group
includes the Larsen Shelf, a short transect on the
.
western side of the Weddell Sea Table 2 . Like the
Eastern Weddell Sea, the Larsen Shelf transect cov-
ers relatively shallow waters showing pronounced
ice melting and maintaining a shallow upper mixed
.
layer 2050 m; Fig. 2 . High nutrient depletion
.
e.g., surface NO concentrations as low as 12 mM ,
3

y1
.
phytoplankton bloom Chl as3.8 mg l and sub-
.
surface ammonium maximum 5075 m character-
.
ize this area Table 2 . Fig. 2 depicts the vertical
profiles of temperature, nitrate, ammonium and Chl
a concentrations in the Eastern Weddell Sea and the
Larsen Shelf. The most remarkable difference is in
terms of ammonium availability. Despite similar val-
.
ues in the surface layer Table 1 , ammonium avail-
ability in the upper mixed layer was significantly
higher in the Larsen Shelf. Very high subsurface
ammonium concentrations can only develop in case
there has been high phytoplankton biomass and ex-
tensive heterotrophic activity. By and large, the
growth season was more advanced in the Larsen
Shelf than in the Eastern Weddell Sea.
. . .
y1
. Fig. 2. Vertical profiles of temperature 8C , nitrate mM , ammonium mM and chlorophyll a concentrations mg l at Station 11 70849
. . . . S, 8824 W in the Eastern Weddell Sea ( and at Station 76 698S, 57889 W in the Larsen Shelf I during the ANTARKTIS Xr7
cruise.
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 166
( )
3.1.2. ScotiaWeddell Confluence SWC
.
Sampling during the EPOS LEG 2 cruise 1989
was done in the ScotiaWeddell Confluence area,
.
located north of the Weddell Sea proper Fig. 1 .
Two major groups were identified in the marginal
.
ice zone of this area Table 2 . The early stage of the
MIZ, SWC A, was characterized by low surface
.
temperature ;y1.418C , more saline surface water
.
;33.83 , high nitrate and silicate concentrations
. .
NO s27.9 mM; Si OH s72.5 mM , low ammo-
3 4
.
nium availability ;0.7% and high phytoplankton

y1
.
biomass Chl a ;1.2 mg l ; Table 2 . On the

contrary, relatively high surface temperature ;

. .
y0.228C , less saline surface water ;33.53 ,

decreased nitrate and silicate concentrations NO s

3
. .
22.3 mM; Si OH s62.5 mM , high ammonium
4
.
availability ;4.7% and relatively low phytoplank-

y1
.
ton biomass Chl as1.0 mg l in SWC B indi-
cate a more advanced stage of the MIZ.
3.1.3. Prydz Bay
Surface water circulation in the Prydz Bay area

as observed during Marine Science Voyage 6, Table

.
1 and Fig. 1 is characterized by a cyclonic gyre and
by a continuous supply of fresh melt water from two
ice shelves: the Amery Ice Shelf in the south and
West Ice Shelf on the south-eastern part of the Bay
.
Jacques and Fukuchi, 1994 . The Antarctic diver-
.
gence AD in this area is located around 668S which
coincides with the shelf break. PCA analysis of the
physico-chemical data separated stations in the

Coastal and Continental Shelf Zone CCSZ, south of

.
AD or shelf break from the Open Oceanic Zone
.
OOZ .
At the moment of sampling the CCSZ was free of
ice and the water column was very stable. Severe

depletion of nutrients e.g., the lowest NO and

3
.
Si OH concentrations were 2.8 and 11.0 mM, re-
4
.
spectively and huge build up of ammonium 23
. . . . . Fig. 3. Profiles of temperature 8C , salinity , nitrate mM and ammonium concentrations mM at Station 38 658S, 758E in the Open
. . . Ocean Zone OOZ, I and at Station 29 698S, 74830 E in the Coastal and Continental Shelf Zone CCSZ, ( of the Prydz Bay
area during the Marine Science Voyage 6 cruise.
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 167
.
mM at the subsurface layer suggest extended high
.
productivity during the growth season Fig. 3 . Al-
though Chl a values are not available, POC and
.
phytoplankton carbon biomass PPC data indicate
.
dense phytoplankton bloom Tables 2 and 3 .
The OOZ, which was far from ice shelves for a
continuous fresh water supply, was subjected to

strong wind stress and hence deep mixed layer Fig.

.
3; Semeneh, 1992 . Nitrate and silicate concentra-

tions were relatively high NO s26.8 mM and

3
. .
Si OH s42.2 mM; Table 2 . The vertical profiles
4
of temperature, salinity, nitrate and ammonium in
two typical stations representing the CCSZ and OOZ
parts of the Prydz Bay are shown in Fig. 3.
3.1.4. Meridian transect along 628E

During ANTARES 2, JanuaryMarch 1994,

.
Table 1 and Fig. 1 , the area was free of ice hence
.
OOZ . Nutrient concentrations were high e.g., NO
3
. .
s28.0 mM and Si OH s42.6 mM; Table 2 . The
4
Antarctic divergence was located between 64 and
658S. South of the divergence surface temperature
.
was low 08C and the vertical profile in the upper
200 m was rather uniform. Between the divergence

and the northern limit of the ice cover i. e. between

.
648 and 588S surface water temperature increased
.
slightly ;0.51.58C and the vertical profile was
characterized by a pronounced subsurface minimum
.
E. Charriaud, personal communication . A very
sharp vertical temperature gradient in this area indi-
cated stable water column conditions. Despite this
stable water column, the area was very oligotrophic

y1
.
Chl as0.2 mg l ; Table 2; Fiala et al., 1998 .
3.2. Biomass, species composition and size structure
of phytoplankton community
Table 3 shows the summaries of phytoplankton

2
carbon biomass of all cruises. A slope of 0.20 r s
.
0.71, p-0.05 was obtained when phytoplankton
.
carbon PPC of all cruises was plotted against par-
.
ticulate organic carbon POC , indicating that phyto-
plankton represented about 20% of POC. However,

when phytoplankton biomass was very low e.g.,

. .
ANT IXr2 , PPC was not related to POC p)0.05 .
3.2.1. Weddell Sea
.
Early in the growth season ANT IXr2 flagel-
.
lates non-Phaeocystis sp dominated the phyto-
.
plankton assemblage Table 3 . The autotrophic
community structure was characterized by greater
importance of small cells. About 66% of the total
biomass was represented by the -20 mm size frac-
tion, although the -10 mm fraction in Table 3
contributed only 40.6%.

During ANT Xr7 the Central Weddell Sea ex-

.
cept few stations was relatively poor in phytoplank-
ton biomass and flagellates dominated the assem-
.
blage Table 3 . The community structure was domi-
.
nated by the -10 mm fraction ;61% . On the
other hand, in the Eastern Weddell Sea and the
Larsen Shelf, where dense phytoplankton blooms
were observed, diatoms were dominant with a rela-
.
tive contribution of 46% 1867% and 40% 16
.
56% , respectively. Moreover, a greater proportion
of the total biomass was on the )10 mm fraction:
.
4474% means59% in the Eastern Weddell Sea
.
and 3087% means54% in the Larsen Shelf.
Phaeocystis sp. was a very important component of
these blooms with a mean relative contribution of
25%. Thus, the apparently high relative abundance
of the -10 mm size fraction in bloom stations of
the Weddell Sea was entirely due to Phaeocystis sp.
.
Table 3 .
In terms of species composition, the Central Wed-
dell Sea was characterized by abundance of small
diatoms and autotrophic flagellates. Cryptophytes and
other unidentified flagellates formed the bulk of the
biomass. Phaeocystis sp. contributed only 7.4%.
Pennate diatoms contributed about 18% to the total
biomass. These include small pennates such as
Nitzschia cylindrus, chain forming species of the

group Pseudonitschia Nitzschia prolongatoides and

.
Nitzschia lineola , and Tropidoneis sp. Centric di-
atoms of the genus Coscinodiscus, Thalassiosira,
Corethron, Asteromphalus and Actinocyclus were
also important. On average, centric diatoms repre-
sented about 13% of the total biomass.
The phytoplankton assemblages in the Eastern
Weddell Sea and the Larsen Shelf were characterized
by high abundances of diatoms and Phaeocystis sp.
Unlike the Central Weddell Sea, Phaeocystis sp. in
these areas was very important with an average
contribution of 26.5% in the Eastern Weddell Sea
and 23% in the Larsen Shelf. Differences in diatom
species composition were observed between the
Eastern Weddell Sea and Larsen Shelf. In the East-
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 168
T
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( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 169
ern Weddell Sea centric diatoms such as Thalas-
siosira sp., Coscinodiscus sp. and Corethron crio-
philum were very important. The genus Thalas-
siosira alone represented about 14% of the total
biomass. On the contrary, in the Larsen Shelf pen-
nate diatoms were dominant with a relative contribu-
tion of 32%. The main pennate diatoms in the Larsen
Shelf include species such as N. cylindrus, Thalas-
siothrix sp., Fragilariopsis sp. and chain forming
Pseudonitzschia species such as N. prolongatoides
and N. lineola. Centric diatoms contributed only 9%,
compared to the 21% relative contribution in the
Eastern Weddell Sea.
3.2.2. ScotiaWeddell Confluence
.
The two MIZ groups i.e., SWC A and SWC B ,
despite similar biomass, showed differences in
.
species composition Table 3 . Diatoms dominated
the assemblage during the early stage of the MIZ
.
SWC A . However, late in the growth season SWC
. .
B flagellates non-Phaeocystis dominated over di-
atoms. In some stations bloom of cryptophytes were
observed late in the growth season. A greater propor-
tion of the total biomass during early season was due
to the )20 mm size fraction but as the season
progressed the dominance shifted to the -20 mm
size fraction. This seasonal shift in community struc-
ture was caused by deepening of the mixed layer and

selective grazing of diatoms by krill Jacques and

.
Panouse, 1991 .
3.2.3. Prydz Bay
This area was characterized by a stable water
column as well as by a rich and diverse phytoplank-
.
ton assemblage Table 3 . Both POC and PPC data

indicate dense phytoplankton bloom Tables 2 and 3;

.
Kopczynska et al., 1995 . Like the Eastern Weddell
Sea and the Larsen Shelf, the CCSZ is a relatively
shallow area with depth ranging from a few hundred
.
meters to the shelf break ;1000 m . However, we
observed important differences in species composi-
tion between the CCSZ and the bloom stations of the
.
Weddell Sea Eastern Weddell Sea and Larsen Shelf .
While the bloom in the Eastern Weddell Sea and the
Larsen Shelf was due to diatoms and Phaeocystis
sp., the bloom in the CCSZ was entirely due to
.
diatoms; about 83.6% 67.799.7% of the total
phytoplankton biomass was due to diatoms. The
phytoplankton community in the CCSZ was domi-

nated by the )10 mm size fraction 67.784.3%,

.
means78.3% . Pennate diatoms were particularly
very abundant, representing 70% of the diatom
biomass and 58% of the total phytoplankton biomass.
In particular, N. curta was the most dominant pen-
nate species which, on average, contributed 28.2%.
At one station this species virtually formed a
monospecific bloom. This species together with N.
antarctica and N. subcurata contributed over 45%
to the total biomass. Centric diatoms, compared to
the pennate species, were less dominant with a mean
relative contribution of 24.4%. Important centric
species include: C. criophilum, Rhizosolenia hebe-
tata, Thalassiosira sp., Dactyliosolen sp. and Bid-
dulphia sp. The relative contribution of Phaeocystis
.
sp. in the CCSZ was very small 5.4% compared to
a mean contribution of about 25% in the Eastern
Weddell Sea and the Larsen Shelf.
As in the CCSZ, the assemblage in the OOZ was

also dominated by diatoms 62.699.2%, means

.
85.6% and the )10 mm size fraction 71.598.8%,
.
means87.8%; Table 3 . Unlike the CCSZ, the dom-
inant diatoms were centric species with a mean
relative contribution of 55%. These include Thalas-
siosira, R. hebetata, C. criophilum and Chaetoceros
dichaeta. Pennate diatoms such as N. curta, N.
lecontei and Fragilariopsis sp. were also important.
Dinoflagellates such as Prorocentrum sp. were very
abundant in some stations. Therefore, in Prydz Bay
the phytoplankton assemblage was dominated by
diatoms, mainly by pennate species in the CCSZ and
by centric species in the OOZ.
3.2.4. Meridian transect along 628E
During ANTARES 2, although the water column
was stable, phytoplankton biomass was very low

y1
.
Chl as0.2 mg l ; Table 2; Fiala et al., 1998 .
.
Diatoms dominated the assemblage Table 3 and
.
much of the phytoplankton biomass ;72% was on
the )10 mm size fraction. As in the OOZ of Prydz
Bay, the dominant diatoms were centric species
which represented about 31% of the PPC. The main
species include C. criophilum, Proboscia sp., Rhi-
zosolenia sp and Cha. dichaeta. Among pennate

diatoms, species of the genus Nitzschia N. kergue-

.
lensis and N. cylindrus , Thalassiothrix T. antarc-
.
tica , Tropidoneis sp. and Pseudonitzscha sp. were
very important. Cryptophytes were very abundant
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 170
Table 4
Specific and absolute nitrogen uptake rates and f-ratios in the surface waters of the Southern Ocean
y3 y1 y1
. . n Specific uptake rate =10 h Absolute uptake rate nM day f-ratio
n n n r r r
NO NH N NO NH N
3 4 3 4
. Weddell Sea ANT IXr2 9 3.5"2.6 1.3"0.5 4.8"2.8 22.8"16.9 9.1"5.6 31.9"19.3 0.69"0.1
. Central Weddell Sea ANT Xr7 14 3.3"3.5 1.3"0.6 4.6"3.3 109.0"131.5 40.3"29.4 149.3"132.5 0.62"0.2
. Eastern Weddell Sea ANT Xr7 5 8.7"4.5 0.9"0.3 9.6"4.5 919.6"757.8 84.7"39.0 1004.3"784.8 0.89"0.1
. Larsen Shelf ANT Xr7 4 5.8"3.8 0.9"0.4 6.7"3.5 678.4"286.1 119.6"67.2 798.0"222.4 0.83"0.1
. ScotiaWeddell, SWC A EPOS 8 5.4"2.1 2.6"1.6 8.0"3.4 194.3"155.1 78.4"34.4 272.7"180.7 0.66"0.1
. ScotiaWeddell, SWC B EPOS 6 2.7"3.0 2.0"0.7 4.7"3.3 122.8"127.8 98.8"42.9 221.7"151.2 0.44"0.2
. Prydz Bay, CCSZ MSV 6 4 0.5"0.4 0.7"0.3 1.2"0.7 61.4"37.1 85.8"47.7 147.2"71.9 0.42"0.1
. Prydz Bay, OOZ MSV 6 5 1.0"0.9 0.4"0.2 1.3"1.0 27.6"20.5 11.3"7.1 38.9"24.7 0.68"0.1
ANTARES 2, OOZ 4 1.0"0.6 1.9"0.6 3.0"1.2 22.9"14.8 39.2"16.2 62.0"31.1 0.34"0.1
. nsNumber of samples stations .
n sn qn .
N NO NH
3 4
r sr qr .
N NO NH
3 4
n
NO
3
f-ratios .
n
N
.
14% . Silicoflagellates contributed about 8%.
Phaeocystis sp. biomass was very low.
3.3. Nitrogen uptake regime
The results of the nitrogen uptake rates are sum-
marised in Table 4. Specific nitrate uptake rates
.
n of all five cruises in the SIZ ranged from
NO
3
0.0002 to 0.06 h
y1
and specific ammonium uptake
.
y1
rate n from 0.0002 to 0.006 h . A wide range
NH
4
of variations in n compared to n indicates
NO NH
3 4
greater spatial and temporal variability in nitrate
uptake rate than ammonium.
3.3.1. Weddell Sea
High specific nitrate uptake rates in this region

were associated with bloom conditions i.e., Eastern

.
Weddell Sea and Larsen Shelf; Table 4 . Ammonium
uptake rates, on the other hand, were rather similar

both during bloom and non-bloom conditions Table

. .
4 . Absolute nitrate uptake rates r for bloom
NO
3
stations were one order of magnitude higher than for
non-bloom stations. High r can be due to either
N
high n , high biomass or both. Fast dividing cells
N
exhibit high n . Very high n in the Eastern
NO NO
3 3
Weddell Sea, compared to the Larsen Shelf, indi-
cates more active phytoplankton.
.
Early in the season ANT IXr2 both diatoms
.
and flagellates depended on nitrate Table 4 . f-ratios
were )0.5, indicating the predominance of new
production. Although flagellates dominated the as-
.
semblage Table 3 , r was equally related to
NO
3

2
.
both diatoms slopes0.0048 and r s0.70 and

2
.
flagellates slopes0.0047 and r s0.76 . Among
diatoms the biomass of pennate species correlated

2
.
strongly with nitrate uptake rate r s0.76 . During
ANT Xr7, as a whole, only diatom biomass showed

strong correlation with nitrate uptake rate Figs. 4

.
and 5 . Despite large variability in biomass and

species composition during ANT Xr7 Tables 2 and

.
3 , the production regime was rather similar with

y1
. Fig. 4. Relationship between diatom biomass mg C l and

y1
. specific nitrate uptake rate n , h during spring time in the
NO
3
. Weddell Sea ANTARKTIS Xr7 cruise .
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 171

y1
. Fig. 5. Relationship between diatom biomass mg C l and

y1
. absolute nitrate uptake rate r , mM day during spring time
NO
3
. in the Weddell Sea ANTARKTIS Xr7 cruise .

overwhelming importance of new production Table

.
4 .
3.3.2. ScotiaWeddell Confluence
The uptake regime in this area varied depending
on dominance of diatoms or flagellates. At the begin-
ning of the season a diatom dominated assemblage
thriving in stabilised surface water was characterized
by high specific nitrate uptake rates and predomi-
.
nance of new production SWC A; Tables 3 and 4 .
.
With the progress of the season SWC B , the phyto-
plankton composition shifted to dominance by flagel-
.
lates mainly cryptophytes . This was accompanied
.
by an increase in ammonium availability Table 1 , a

y1
. Fig. 6. f-ratio vs. total diatom biomass mg C l in Prydz Bay
. area during summer ( s OOZ and I sCCSZ .

y1
. Fig. 7. f-ratio vs. pennate diatom biomass mg C l in the Prydz
Bay area.
decrease in nitrate uptake rate and preponderance of
.
regenerated production Table 4 .
3.3.3. Prydz Bay
In the CCSZ phytoplankton biomass was still very

high but growth rate was low, i.e., low n Tables 3

N
.
and 4 . High biomass under low growth rate imply
little or no loss rate. Stable water column, high
.
subsurface ammonium concentrations Fig. 3 and
.
dominance of diatoms, mainly by pennates Table 3 ,
were the salient features of this area. Specific nitrate

y1
.
uptake rates were very low n s0.0005 h , an
NO
3
order of magnitude less than the bloom stations in
.
the Weddell Sea Table 4 . The production regime
was characterized by predominance of regenerated

y1
. Fig. 8. Relationship between centric diatom biomass mg C l
and f-ratio in the Prydz Bay area.
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 172

y1
. Fig. 9. Specific ammonium uptake rate n , h vs. pennate
NH
4

y1
. diatom biomass mg C l in Prydz Bay area.
.
production f-ratio-0.5, Table 4 . In the OOZ,
.
however, diatoms mainly centric species were dom-
inant and the community was largely based on new
.
production f-ratio)0.5 . In Prydz Bay, as a whole,
f-ratio correlated negatively with diatom biomass
.
Fig. 6 . However, pennate and centric diatoms
showed different relationships with the f-ratio.
Whereas the biomass of pennate diatoms correlated
negatively with f-ratio, the opposite was true for
.
centric diatoms Figs. 7 and 8 . Moreover, the
biomass of pennate diatoms was positively correlated
.
to specific ammonium uptake rate Fig. 9 .
3.3.4. Meridian transect along 628E
During ANTARES 2, the OOZ was characterized
by a stable water column, a diatom dominated as-
semblage and predominance of regenerated produc-
.
tion Tables 3 and 4 . Unlike in the CCSZ, phyto-

y1
. Fig. 10. Relationship between total diatom biomass mg C l

y1
. and specific nitrate uptake rate n , h during the ANTARES
NO
3
2 cruise in summer period.

y1
. Fig. 11. f-ratio vs. total diatom biomass mg C l during the
ANTARES 2 cruise.
.
plankton biomass was very low Table 3 . As in the
CCSZ, diatom biomass correlated negatively with
.
n and f-ratio Figs. 10 and 11 .
NO
3
4. Discussion
Two lines of seasonal evolution are apparent from
the physico-chemical characteristics of the environ-
ment as well as from the relationship between nitro-
gen uptake regime and phytoplankton biomass, com-
position and structure. In the first scenario, repre-
sented by the MIZ areas of the Weddell Sea and
ScotiaWeddell Confluence, a shift in uptake regime
.
new to regenerated production during the growth
season was accompanied by a change in phytoplank-

ton community structure i.e., from a diatom domi-

nated microplankton assemblage to a flagellate dom-
.
inated nanoplankton assemblage . In the second sce-
nario, represented by the CCSZ and OOZ of Prydz
Bay and the OOZ of ANTARES 2, a shift in the
uptake regime occurred without change in commu-
nity structure. In discussing the seasonal evolution,
the factors that control the growth and maintenance
of phytoplankton biomass, community structure and
uptake regime are considered.
The first scenario is typical for the MIZ areas of
the Weddell Sea and ScotiaWeddell Confluence.
High ice cover, high nutrient levels, low ammonium
availability characterized the early stage of MIZ
.
ANT IXr2 and Central Weddell Sea, Table 2 .
.
Autotrophic flagellates non-Phaeocystis dominated
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 173
.
the phytoplankton assemblage Table 3 . Much of
the phytoplankton biomass was on the -10 mm size
.
fraction Table 3 . Despite low phytoplankton
biomass, relatively high n indicated an active
NO
3
.
phytoplankton community Table 4 . During winter
and early spring phytoplankton biomass is kept low

by sub-optimum growth conditions mainly due to

.
low light availability and temperature and predomi-
.
nance of heterotrophic activity Garrison et al., 1993 .
During this period ammonium concentrations were
low, nitrate was the main nitrogen source and the
community was largely based on new production
.
Table 4 .

As the season progressed e.g., SWC A, Eastern

.
Weddell Sea and Larsen Shelf a rise in temperature
caused ice melting which created a shallow upper
mixed layer, 1050 m. The shallow mixed layer
optimises growth conditions and reduces loss rate,

leading to phytoplankton bloom Chl a)1.5 mg

y1
. .
l ; Table 1 . Sakshaug and Holm-Hansen 1984
stressed the importance of water column stability and
suggested a maximum depth of 50 m of pycnocline
for a bloom to develop. With the stabilisation of the
surface water diatoms dominated the assemblage due
to their fast division rate under optimum light condi-
tion. This is corroborated by the fact that both n
NO
3
and r during bloom periods were strongly related
NO
3
.
to diatom biomass Figs. 4 and 5 . Other dominant
species include Phaeocystis sp. whose relative con-
tribution increased from about 7% early in the sea-
.
son Central Weddell Sea to about 25% with the

progress of the season Eastern Weddell Sea and

.
Larsen Shelf . Coincidence of diatom bloom with
Phaeocystis sp. during this period implies a similar
strategy to increase biomass and reduce loss rate.
During its life cycle Phaeocystis sp. changes from a
solitary form to a colonial form and back to a
solitary form when the colony disintegrates. Colony
formation by Phaeocystis sp. is analogous to chain
formation by bloom forming diatoms; a morphologi-
cal strategy that may reduce grazing pressure by
microheterotrophs.
In predominantly light-controlled systems, such as
the Southern Ocean, physical stabilisation of the
euphotic zone may lead to an increase in new pro-
.
duction Riegman et al., 1993 . Indeed, during stable
conditions, nitrate was the predominant source of
nitrogen both during the pre-bloom and bloom peri-
.
ods Table 4 . For example, in the Eastern Weddell
Sea it supplied about 90% of the phytoplanktons
nitrogen requirement. In the Larsen Shelf the bloom
taking up nitrate with an average n of 0.006 h
y1
NO
3
reduced the ambient nitrate concentration from win-

ter concentrations of about 30 to 12 mM or less Fig.

.
2 . This extended bloom was accompanied by en-
hanced heterotrophic activity as attested by the sub-
.
surface ammonium build up Fig. 2 . Although n
NO
3

in the Larsen Shelf was reduced compared to the

.
Eastern Weddell Sea , the phytoplankton did not
.
switch to ammonium f-ratios0.83 .
.
Late in the growth season e.g., SWC B the MIZ
is characterized by deeper mixed layer, high ammo-
.
nium availability ;4.7% , dominance of flagellates
and predominance of regenerated production, f-ratio
.
s0.44 Tables 24 . Due to decreased stability of
the water column and selective grazing of diatoms
by krill, the community structure shifted to domi-
nance of the smaller size fraction, mainly crypto-

phytes Table 3; Jacques and Panouse, 1991; Bec-

.
quevort et al., 1992; Schloss and Estrada, 1994 .
This combined bottom-up and top-down control
mechanisms selectively reduced the biomass of the
active and important component of the bloomthe
diatoms. In areas of high krill concentration and deep
vertical mixing flagellates dominate over diatoms
.
Kopczynska, 1992 . High krill abundance is the
main feature of the north-western Weddell Sea and

ScotiaWeddell Confluence area Priddle et al.,

.
1988 . In the MIZ of the ScotiaWeddell Conflu-
ence area, grazing by krill not only structured the
community but also enhanced the ammonium avail-
ability primarily through its direct excretion and
secondarily by producing substrate for remineraliza-
.
tion El-Sayed, 1988; Goeyens et al., 1991b . Under
this condition small cells which tend to satisfy their
nitrogen requirement by assimilating ammonium

dominate the assemblage Probyn and Painting, 1985;

.
Koike et al., 1986; Owens et al., 1991 .
.
Total specific uptake rate n reflects the growth
N

rate of phytoplankton Dugdale and Wilkerson,

.
1991 . Much of the variability in total specific up-
.
take rate was mainly due to nitrate uptake Table 4 .
.
Goeyens et al. 1995 showed that n during the
NO
3
growth season exhibits an increase at the beginning
and decreases towards the end of the season. Our
nitrate uptake rates also reflect this general trend. As
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 174
can be seen in Table 4, uptake rates were low at the

beginning of the season ANT IXr2 and Central

.
Weddell Sea , increased as the season progressed
.
SWC A , reached its maximum Eastern Weddell
. .
Sea , decreased slightly Larsen Shelf and became
.
very low at the end of the season SWC B . This
trend in specific nitrate uptake rate was mirror-
.
imaged by the f-ratio Table 4 . Thus, in the MIZ, a
diatom-dominated, predominantly nitrate-based, mi-
croplankton assemblage thriving in a stable water at
the beginning of the season was transformed into a
flagellate dominated, ammonium-based, nanoplank-
ton assemblage towards the end of the season.
In the second scenario, applying to the CCSZ and
OOZ of Prydz Bay and the OOZ of the ANTARES 2
cruise, only a shift in uptake regime was observed.
The main features of these areas include stable water
column, high phytoplankton biomass, dominance of
diatoms, greater importance of the larger size frac-
.
tion, low n , high ammonium availability CCSZ
NO
3

and predominance of regenerated production Tables

.
24 . A bloom can develop only when the rate of
biomass increase exceeds the loss rate, i.e., grazing
.
rate and sedimentation rate Sakshaug et al., 1991 .
Once the bloom has developed it can be sustained
for a longer period under low growth rate if the loss
rate is small. This appears to be the case in the
CCSZ of the Prydz Bay. Stable water column due to
continuous freshwater supply from the ice shelves,
high biomass, low n and high ammonium avail-
NO
3
ability indicate prolonged phytoplankton bloom. High
ammonium availability can develop without the con-
tribution of migratory herbivores such as krill through
prolonged heterotrophic activity by the micro-
heterotrophs. This is corroborated by high hetero-
trophic activity of dinoflagellates, ciliates and

nanoflagellates in this area Archer et al., 1995;

.
Kopczynska et al., 1995 . Microheterotrophs can
consume as much as 48% of the daily production
.
Becquevort et al., 1992 and this results in high
ammonium availability. These heterotrophs preferen-
.
tially graze on small cells -20 mm and their
grazing pressure increases with the progress of the
.
season Archer et al., 1995; Froneman et al., 1995 .
This keep the biomass of small cells low thereby
reducing their competition for ammonium with the
large cells.
The dominance of diatoms late in the growth
season implies little or no selective grazing pressure
by meso- and macroheterotrophs and persistence of
stable water column. This also suggests that diatoms
were dominant throughout the season. In a similar

environment, the Ross Sea ice edge, diatoms mainly

.
pennate diatoms dominated the assemblage from the

beginning to the end of the season El-Sayed et al.,

1983; Smith and Nelson, 1985; Nelson and Smith,
. .
1986 . Although El-Sayed et al. 1983 reported high
abundance of Phaeocystis sp. in the Ross Sea, we
have no evidence to suggest that this species was
abundant at the beginning of the season.
Despite bloom conditions in the CCSZ, phyto-
plankton production was largely based on ammo-
.
nium Tables 1 and 4; Semeneh, 1992 . In particular,
large diatoms, which often are considered to live
mainly on nitrate and export organic material to the
deep sea, were predominantly based on ammonium
.
or regenerated production Fig. 6 . On the contrary,
in MIZ a mixed diatom-Phaeocystis sp. bloom was

based on nitrate, new production Tables 3 and 4;

.
Figs. 4 and 5 . In Prydz Bay, despite preponderance
of regenerated production, pennate and centric di-
atoms exhibited differences in nitrogen nutrition.
Centric diatoms were more abundant in the OOZ and
.
were mainly based on nitrate Tables 2 and 4 . Their
.
biomass correlated positively with f-ratio Fig. 8 .
On the other hand, pennate diatoms tended to be
abundant in shallow areas with high ammonium
.
availability e.g., in the CCSZ and Larsen Shelf and
.
showed negative correlation with f-ratio Fig. 7 . In
these areas pennate diatoms constituted a major frac-
tion of the total biomass. Moreover, these diatoms

often dominate ice assemblages Garrison and Buck,

.
1985 . Elevated ammonium concentrations can occur
.
in the ice 1.52.4 mM; Fritsen et al., 1994 . When

encountered with high ammonium concentrations as

.
in the CCSZ , these diatoms can increase their up-
.
take capacity Smith and Nelson, 1990; Fig. 9 . This
enables them to change their nitrogen source depend-
ing on the availability of ammonium. Thus, pennate
diatoms are opportunistic species with a flexible
physiology that enables them to live successfully
both in the ice and water column. Such flexible
nitrogen nutrition is particularly important in systems
such as the Southern Ocean where nitrate utilisation

can be limited by iron availability Martin et al.,

.
1990 . Greater dependence on ammonium offers
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 175
more advantage for slowly dividing large diatom
.
cells in the CCSZ low n ; Table 4 . This is
NO
3
because large cells have high iron requirement and,
in particular, this requirement is higher when they

assimilate nitrate Raven, 1988; Doucette and Harri-

.
son, 1991 . The shift in nitrogen nutrition from
nitrate to ammonium reduces the overall community
demand for iron, thus, enables part of the community
to subsist on nitrate. Although the relative contribu-
.
tion of nitrate in the CCSZ was low f-ratios0.42 ,
its absolute uptake rate was high due high phyto-
plankton biomass. This explains the observed very

low ambient nitrate concentrations in the CCSZ Ta-

.
ble 2 . In the MIZ, however, large diatoms which
formed the bulk of the bloom were selectively re-
moved from the euphotic zone through grazing and
water column destabilization and the remaining com-
munity had low biomass, mainly composed of
nanoplanktonic flagellates, was sustained by ammo-
nium.
The community structure, unlike in the MIZ, did
not change during the season. The )10 mm size
fraction in Prydz Bay represented 28.9 to 98.8%
.
means80.6% of total phytoplankton biomass. The
)10 mm size fraction was dominant concurrent
with the predominance of regenerated production
.
Tables 3 and 4 . The situation in the CCSZ is the
extension of the first stages of the MIZ in the
Weddell Sea and adjacent areas. Therefore, under
persistent physical stability and absence of selective
grazing pressure, a diatom dominated microplankton
assemblage persisted to late season and shifted its
.
uptake regime from nitrate to ammonium in re-
sponse to increased ammonium availability. The
dominance of diatoms under regenerated production
provides a further physiological evidence for the
excess net removal of silicate over nitrate occurring

in certain provinces of the Southern Ocean Treguer

.
and Jacques, 1992; Goeyens et al., 1998 .
From the export production point of view, export
can occur in both systems. The first system proceeds
with abundance of diatoms which are either grazed
or directly exported to deep water due to destabiliza-
tion of the water column. The proportion of organic
material channelled through a higher trophic level or
directly exported to bottom water and sediments
depends on the degree of grazing pressure, degree of
destabilization and rate of remineralization. More-
over, it also depends on the time at which grazing
starts as well as the time at which stable water
column lasts. Early termination of phytoplankton
bloom by heavy grazing pressure or water column
destabilization will lead to small absolute export
production.
Traditionally, nitrate uptake represents new pro-
.
duction hence export production and is mediated
by a diatom dominated microplankton assemblage
.
Eppley and Peterson, 1979 . In the CCSZ, although
diatoms were dominant, the assemblage was pre-
dominantly based on ammonium or regenerated pro-
duction. The predominance of regenerated produc-
tion in the CCSZ, according to Eppley and Peterson
.
1979 , would suggest little export production but the
dominance of large diatom cells implies export pro-
duction. This contradiction underlines the importance
of phytoplankton community analysis in interpreta-
tion of field nitrogen uptake results. The significance
the CCSZ for export production can be resolved by
using other measures of export production such as
sediment trap or accumulation of barite at
.
mesopelagic layer Dehairs et al., 1992 .
Acknowledgements
We are grateful to the captains and crew members
of the R.V. Polarstern, Marion Dufresne and Au-
rora Australis. We thank M. Leermakers for her
assistance. This is AWI publication 1458.
References
Archer, S., Leakey, R., Sleigh, M., Burkill, P., Appleby, C., 1995.
Microbial dynamics in sea ice at a coastal Antarctic site:
taxonomy, biomass and production. In: International sympo-
sium on Carbon Fluxes and Dynamic Processes in the South-
ern Ocean: Present and Past, Institut Universitaire Europen de
la Mer, Brest, France, p. 80.
Becquevort, S., Mathot, S., Lancelot, C., 1992. Interaction of the
microbial community of the marginal ice zone of the north-
western Weddell Sea through size distribution analysis. Polar
Biol. 12, 211218.
Dehairs, F., Baeyens, W., Goeyens, L., 1992. Accumulation of
suspended barite at mesopelagic depth and export production
in the Southern Ocean. Science 258, 13321335.
Doucette, G.J., Harrison, P.J., 1991. Aspects of iron and nitrogen
nutrition in the red tide dinoflagellate Gymnodinium san-
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 176
guineum: I. Effects of iron depletion and nitrogen source on
biochemical composition. Mar. Biol. 110, 165173.
Dugdale, R.C., Wilkerson, F.P., 1986. The use of
15
N to measure
nitrogen uptake in eutrophic oceans: experimental considera-
tions. Limnol. Oceanogr. 31, 673689.
Dugdale, R.C., Wilkerson, F.P., 1991. Low specific nitrate uptake
rate: a common feature of high-nutrient, low-chlorophyll ma-
rine ecosystems. Limnol. Oceanogr. 36, 16781688.
El-Sayed, S., 1988. Seasonal and interannual variabilities in
Antarctic phytoplankton with reference to krill distribution. In:
. Sarhage D. Ed. , Antarctic Ocean and Resources Variability.
Springer, Berlin, pp. 101119.
El-Sayed, S., Biggs, D.C., Holm-Hansen, O., 1983. Phytoplankton
standing crop, primary productivity, and near-surface nitroge-
nous nutrient fields in the Ross Sea, Antarctica. Deep-Sea Res.
. 30 8 , 871886.
Eppley, R.W., Peterson, B.J., 1979. Particulate organic matter flux
and plankton new production in the deep ocean. Nature 282,
677680.
Eppley, R.W., Reid, F.M.H., Strickland, J.D.H., 1970. The ecol-
ogy of the plankton of La Jolla, California, in the period April
. through September 1967. In: Strickland, J.D.H. Ed. , Esti-
mates of Phytoplankton Crop Size, Growth Rate and Primary
Production Part III, Vol. 17. Bull. Scripps. Inst. Oceanogr., pp.
3342.
Fiala, M., 1994. Les rapports des campagnes a la mer: ANTARES `
2rMD 78. Institut Francais pour la Rechereche et la Tech-
nologie Polaires, No. 95-01, Brest, France, pp. 1178.
Fiala, M., Semeneh, M., Oriol, L., 1998. Biomass, size fraction-
ated phytoplankton and species composition in the Indian
sector of the Southern Ocean during austral summer. J. Mar.
Syst. 17, 179194.
Fritsen, C.H., Lytle, V.I., Ackley, S.F., Sullivan, C.W., 1994.
Autumn bloom of Antarctic pack-ice algae. Science 266,
782784.
Froneman, P.W., Perissinotto, R., McQuaid, C.D., 1995. Micro-
zooplankton grazing and community structure in the Southern
Ocean: seasonal variations and implications for carbon cy-
cling. In: International symposium on Carbon Fluxes and
Dynamic Processes in the Southern Ocean: Present and Past.
Institut Universitaire Europen de la Mer, Brest, France, p. 56.
Garrison, D.L., Buck, K.R., 1985. Sea-ice algal communities in
the Weddell Sea: species composition in the ice and plankton
. assemblages. In: Gray. J.S., Chritiansen. M.E., Eds. , Marine
Biology of Polar Regions and Effects of Stress on Marine
Organisms. Wiley, pp. 103122.
Garrison, D.L., Buck, K.R., Gowing, M.M., 1993. Winter plank-
ton assemblage in the ice edge zone of the Weddell and Scotia
Seas: composition, biomass and spatial distributions. Deep-Sea
. Res. 40 2 , 311338.
Glibert, P.M., Biggs, D.C., McCarthy, J.J., 1982. Utilisation of
ammonium and nitrate during austral summer in the Scotia
Sea. Deep-Sea Res. 29, 837850.
Goeyens, L., Farbach, E., Behmann, T., Hinrichsen, H., Krest, J.,
Ross, A., Wisotski, A., 1991c. Summer Weddell Gyre study.
Data Report No. 1. Alfred Wegener Institute for Polar Re-
search, Bremerhaven, Germany.
Goeyens, L., Srresen, F., Treguer, P., Morvan, J., Panouse, M.,
Dehairs, F., 1991a. 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, 719.
Goeyens, L., Treguer, P., Lancelot, C., Mathot, S., Becquevort, S.,
Morvan, J., Dehairs, F., Baeyens, W., 1991b. Ammonium
regeneration in the ScotiaWeddell Confluence area during
spring 1988. Mar. Ecol. Prog. Ser. 78, 241252.
Goeyens, L., Treguer, P., Baumann, M.E.M., Baeyens, W., De-
hairs, F., 1995. The leading role of ammonium in the nitrogen
uptake regime of Southern Ocean marginal ice zones. J. Mar.
Syst. 6, 345361.
Goeyens, L., Semeneh, M., Elskens, M., Shopova, D., Baumann,
M.E.M., Dehairs, F., 1998. Phytoplankton nutrient utilisation
and nutrient signature in the Southern Ocean. J. Mar. Syst. 17,
143157.
Jacques, G., Panouse, M., 1991. Biomass and composition of size
fractionated phytoplankton in the WeddellScotia Confluence
area. Polar Biol. 11, 315328.
Jacques, G., Fukuchi, M., 1994. Phytoplankton in the Indian
. Antarctic Ocean. In: S.E. El-Sayed Ed. Southern Ocean
Ecology: the BIOMASS perspective. Cambridge Univ. Press,
pp. 6378.
Kang, S.H., Fryxell, G.A., 1993. Phytoplankton in the Weddell
Sea, Antarctica: composition, abundance and distribution in
water-column assemblage of the marginal ice-edge zone dur-
ing austral autumn. Mar. Biol. 116, 335348.
Koike, I., Holm-Hansen, O., Biggs, C., 1986. Inorganic nitrogen
metabolism by Antarctic phytoplankton with special reference
to ammonium recycling. Mar. Ecol. Prog. Ser. 30, 105116.
Kopczynska, E.E., 1992. Dominance of microflagellates over
diatoms in the Antarctic areas of deep vertical mixing and krill
concentrations. J. Plankton Res. 14, 10311054.
Kopczynska, E.E., Goeyens, L., Semeneh, M., Dehairs, F., 1995.
Phytoplankton composition and cell carbon distribution in
Prydz Bay, Antarctica: relation to organic particulate matter
13
. and its d C values. J. Plankton Res. 17 4 , 685707.
Kristiansen, S., Syvertsen, E., Farbrot, T., 1992. Nitrogen uptake
in the Weddell Sea during late winter and spring. Polar Biol.
12, 245251.
Martin, J.H., Fitzwater, S.E., Gordon, R.M., 1990. Iron deficiency
limits phytoplankton growth in Antarctic waters. Global Bio-
geochem. Cycles 4, 512.
Nelson, D.M., Smith, W.O. Jr., 1986. Phytoplankton bloom dy-
namics in the western Ross Sea ice edge: II. Mesoscale
. cycling of nitrogen and silicon. Deep-Sea Res. 33 10 , 1389
1412.
Nothig, E.M., von Bodungen, B., Sui, Q., 1991. Phyto- and
protozooplankton biomass during austral summer in surface
waters of the Weddell Sea and vicinity. Polar Biol. 11, 293
304.
Owens, N.J.P., Priddle, J., Whitehouse, M.J., 1991. Variations in
phytoplanktonic nitrogen assimilation around South Georgia
. and in the Bransfiend Strait Southern Ocean . Mar. Chem. 35,
287304.
Priddle, J., Croxall, J.P., Everson, I., Heywood, R.B., Murphy,
( ) M. Semeneh et al.rJournal of Marine Systems 17 1998 159177 177
E.J., Prince, P.A., Sear, C.B., 1988. Large scale fluctuations in
distribution and abundance of krilla discussion of possible
. causes. In: Sarhage, D. Ed. , Antarctic Ocean and Resources
Variability. Springer, Berlin, pp. 118.
Probyn, T.A., Painting, S.J., 1985. Nitrogen uptake by size-frac-
tionated phytoplankton in Antarctic surface waters. Limnol.
Oceanogr. 30, 12371332.
Raven, J., 1988. The iron and molybdenum use efficiencies of
plant growth with different energy, carbon and nitrogen
sources. New Phytol. 109, 279287.
Riegman, R., Kuipers, B.R., Noordeloos, A.A.M., Witte, H.J.,
1993. Size-differential control of phytoplankton and the struc-
. ture of plankton communities. Neth. J. Sea Res. 31 3 ,
255265.
Ronner, U., Srrenson, F., Holm-Hansen, O., 1983. Nitrogen
assimilation by phytoplankton in the Scotia Sea. Polar Biol. 2,
137147.
Sakshaug, E., Holm-Hansen, O., 1984. Factors governing pelagic
. production. In: Holm-Hansen, O., Bolis, L., Gilles, R. Eds. ,
Marine Phytoplankton and Productivity, Lecture Notes on
Coastal and Estuarine Studies, Vol. 8. Springer, Heidelberg,
pp. 118.
Sakshaug, E., Slagstad, D., Holm-Hansen, O., 1991. Factors con-
trolling the development of phytoplankton blooms in the
Antarctic Oceana mathematical model. Mar. Chem. 35,
259271.
Schloss, I., Estrada, M., 1994. Phytoplankton composition in the
WeddellScotia Confluence area during austral spring in rela-
tion to hydrography. Polar Biol. 14, 7790.
Semeneh, M., 1992. Variation in new and regenerated production
in the Southern Ocean. MSc Thesis, Vrije Univ. Brussel,
Brussels, 63 pp.
Smetacek, V., Scharek, R., Gordon, L.I., Eicken, H., Fahrbach, E.,
Rohardt, G., Moores, S., 1992. Early spring phytoplankton
blooms in ice platelet layers of the southern Weddell Sea,
. Antarctica. Deep-Sea Res. 39 2 , 153168.
Smith, W.O. Jr., Nelson, D.M., 1985. Phytoplankton bloom pro-
duced by a receding ice edge in the Ross Sea: spatial coher-
ence with the density field. Science 227, 163166.
Smith, W.O. Jr., Nelson, D.M., 1990. Phytoplankton growth and
new production in the Weddell Sea marginal ice zone in the
. austral spring and autumn. Limnol. Oceanogr. 35 4 , 809821.
Ter Braak, C.J.F., 1990. Update notes: CANOCO version 3.10.
Agricultural Mathematics Group, Wageningen, The Nether-
lands.
Treguer, P., Van Bennekom, A.J., 1991. The annual production of
biogenic silica in the Antarctic Ocean. Mar. Chem. 35, 477
487.
Treguer, P., Jacques, G., 1992. Dynamics of nutrients and phyto-
plankton and fluxes of carbon, nitrogen and silicon in the
Antarctic Ocean. Polar Biol. 12, 149162.
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, 375379.
Utermohl, H., 1958. Zur Vervollkommnung der quatitativen Phy-
toplankton-Methodik. Mitt. Int. Verein. Theor. Angew. Lim-
nol. 9, 138.
Van Bennekom, A.J., Veth, C., 1991. EPOS LEG 2 Data Report:
Hydrography, Part 1, 2nd edn. NIOZ, Texel, The Netherlands.