Notes
MCMAHON, J. W., AND F. H. RIGLER. 1962. Mechanisms regulating the feeding rate of Daphnia magna Straus. Can. J.
Zool. 41: 321-332.
1965. Some factors influencing the feeding behavior
of-Daphnia magna Straus. Can. J. Zool. 43: 603-611.
MILLIKEN, G. A., AND D. E. JOHNSON. 1992. Analysis of messy
data. Chapman and Hall.
MUNRO Fox, H., AND Y. MITCHELL.
19 5 3. Relation of the rate
of antenna1 movement in Daphnia to the number of eggs
carried in the brood pouch. J. Exp. Biol. 30: 238-242.
OBRESHKOVE, V., AND A. ABRAMOWITZ.
1932. Temperature
characteristics for the oxygen consumption of a cladoceran.
J. Cell. Comp. Physiol. 2: 133-139.
ORCUTT, J. D., AND K. G. PORTER. 1983. Diel vertical migration by zooplankton: Constant and fluctuating temperature effects on life history parameters of Daphnia. Limnol.
Oceanogr. 28: 720-730.
PORTER,K.
G.,J. GERFUTSEN, AND J.D. ORCUTT. 1982. The
effect of food concentration on swimming patterns, feeding
behavior, ingestion, assimilation, and respiration by Daphnia. Limnol. Oceanogr. 27: 935-949.
Limnol.
Oceanogr., 41(8), 1996, 1821-1828
0 1996, by the American
Society of Limnology
and Oceanography,
1821
C. W., AND W. G. SPRULES. 1991. Predatorinduced behavioral
defenses and its ecological consequences for two Calanoid copepods. Oecologia 68: 276-286.
SCHMIDT-NIELSEN,
K. 198 3. Animal physiology: Adaptation
and environment, 3rd ed. Cambridge.
STERNS, S. C. 197 5. Light responses of Daphnia pulex. Limnol.
Oceanogr. 20: 564-570.
TESSIER, A. J., AND C. E. GOULDEN.
1982. Estimating food
limitation
in cladoceran populations. Limnol. Oceanogr.
27: 707-7 17.
VAN DUREN, L. A., AND J. J. VIDELER.
1995. Swimming behavior of developmental
stages of the Calanoid copepod
Temora longicornis at different food concentrations. Mar.
Ecol. Prog. Ser. 126: 153-l 6 1.
ZARET, R. E., AND W. C. KERFOOT.
1980. The shape and
swimming
technique of Bosmina longirostris. Limnol.
Oceanogr. 25: 126-l 33.
RAMCHARAN,
Submitted: 9 June 1995
Accepted: 23 April 1996
Amended: 21 August 1996
Inc.
Standing stock and dynamics of picophytoplankton in the
Thau Lagoon (northwest Mediterranean coast)
Abstract-Eucaryotic
picophytoplankton
(PEUC), picocyanobacteria, and larger phytoplanktonic
cells from the
Thau Lagoon (northwest Mediterranean coast) were numbered by flow cytometry from November 199 1 to February
1994. PEUC cells dominated the phytoplanktonic
assemblage and exhibited seasonal dynamics. Monthly mean
abundances of larger phytoplanktonic
cell and PEUC were
significantly correlated with temperature and solar irradiance values, with the highest correlations having been obtained for PEUC abundances. The mean abundance of total
picophytoplankton
(3.5 x lo4 cells ml-l) was among the
highest recorded in marine waters. The dominance of picophytoplankton
over larger phytoplanktonic
cells (average abundance, 5 x 1O3cells ml- ‘) in the nutrient-rich waters of the lagoon was related to grazing from large-scale
shellfish breeding (oyster’s biomass z 35,000 t), which seems
to act preferentially on the largest cells. Several hypotheses,
including the potential selective effect of copper, were proposed to explain the dominance of the PEUC form (average
abundance, 3.4 x lo4 cells ml-l).
During the past 10 yr, numerous studies have shown
that autotrophic picoplankton (0.2-2 pm) are one of the
most abundant phytoplankton
components in marine
ecosystems. Picoplanktonic cells, however are considered
dominant only under oligotrophic conditions (Chisholm
1992; Riegman et al. 1993).
Procaryotes and eucaryotes have been found to compose picoplankton
communities (We&e 1993). In off-
shore oceanic waters, procaryotic algae (cyanobacteria,
prochlorophytes)
have been generally found to outnumber eucaryotic picoplankters. To our knowledge, a significant contribution of eucaryotic cells to the picoplanktonic community has been reported only in the west coast
upwelling region of South Island, New Zealand (Hall and
Vincent 1990), and at times in estuarine areas (e.g. Iriarte
and Purdie 1994).
In a previous study conducted in Thau Lagoon, we
discovered a new eucaryotic picoplankter, Ostreococcus
tauri (Chretiennot-Dinet
et al. 1995). Preliminary data
obtained from flow cytometric analysis of Thau waters
indicate that 0. tauri cells are very abundant and may
represent the main component of the phytoplankton community in the lagoon.
In the present study, based on a 2-yr sampling program,
we report on eucaryotic picophytoplankton
vs. picocyanobacteria and larger phytoplanktonic
cell dynamics and
mean abundances in the Thau Lagoon with special attention to the potential effect of filter feeders, which are
bred on a large scale in this marine lagoon.
Thau Lagoon is on the French Mediterranean
coast
(43”20’-43”28’N,
3”32’-3’42’E).
Large-scale mollusc
farming (oyster production is w 20,000 t yr- I) takes place
in this 7%km2 body of water. Five sampling stations were
selected to represent different zones of the marine lagoon,
and one marine station was located 3.5 km south of Sete
channel (Fig. 1). Four stations were sampled approxi-
1822
Notes
Mediterranean
0 MJIRS
shellfish breeding zone
seawater exchange zone
*
I
0
I
l
sampling station
5km
Fig. 1. Map showing locations of sampling stations in the Thau Lagoon (ZAS, ZBS, TBS,
ROQS, PSM) and in the Mediterranean Sea (MERS).
mately biweekly between 5 November 1991 and 22 February 1994 at about 1000 hours local time. Sampling at
PSM started on 13 February 1992, and at MERS on 12
January 1993. Sampling for Chl a and production measurements at approximately monthly intervals began on
12 January 1993. Samples were collected in sterile vials
50 cm under the water’s surface. They were refrigerated
and transferred to the laboratory in < 1 h.
Two of the five stations (TBS and ZBS, which are located outside and inside shellfish breeding areas, respectively; Fig. 1) were also occasionally sampled daily for
5-d sequences (15-19 July 1991, 14-18 October 1991,
20-22 and 24 January 1992, 6-10 April 1992) to obtain
field data on the potential effect of filter feeders on phytoplanktonic group abundances.
Samples were fixed (formaldehyde, 0.5% final concn)
and stored (liquid nitrogen) as previously
described
(Troussellier et al. 1995). Subsamples of 500 ~1 were analyzed with an ACR-1400-SP
flow cytometer (Bruker
Spectrospin, Wissembourg, France). By using criteria from
previous studies (Chretiennot-Dinet
et al. 1995), we identified three groups of phytoplanktonic
cells: eucaryotic
picophytoplankton
(PEUC), picocyanobacteria (CYAN),
and phytoplanktonic
cells between 2 and 50 pm (which
was the upper boundary set by the instrument sample
injector) that we called NAN cells, even when microphytoplanktonic cells (see below) were included in this group.
For each group, forward and wide-angle light scatters and
red and(or) green fluorescences and abundances were recorded, but here we report only on the dynamics of group
abundances. Classification of PEUC and CYAN as picoplankters was occasionnally checked (~2= 6) from filtration experiments, which showed that on average 98.3%
of these cells passed through 2-pm and 93% through 1.2pm Nuclepore membranes. The cells classified as PEUC
exhibited the same flow cytometric signature as 0. tauri
cells isolated in the Thau Lagoon and described previously (Chretiennot-Dinet
et al. 1995). For NAN, the most
frequently observed (microscopic observation) cells were
diatoms (Chaetoceros, Skeletonema, Ditylum, Thalassiosira), Cryptophyceae (Cryptomonas), Dinophyceae (Peridinium, Gymnodinium, Prorocentrum), Euglenophyceae
(Eutrepsiella), Chlorella-like cells, and phytoflagellates.
For Chl a determinations, 20-ml samples were extracted in 90% acetone solution and analyzed by fluorometry
(Holm-Hansen
et al. 1965). Carbon fixation was mea-
Notes
sured according to Riemann and Jensen (199 1). Chl a
and production of picophytoplankton
were measured by
means of 2-pm Nuclepore polycarbonate filtrates.
Temperature (“C) and irradiance (J cm-2) were obtained from the automatic records of a meteorological
station (CIMEL Electronique, Paris) near ZBS station.
The temperature probe was immersed 50 cm under the
water’s surface.
For study of phytoplanktonic
time series, we used the
contingency periodogram method (Legendre et al. 198 1)
to search for periodic phenomena. To obtain a constant
sampling interval, we averaged raw data on a monthly
basis. R software (P. Legendre pers. comm.) has been
used to perform this analysis. Statview software (Abacus
Concept) was used for other statistical analysis.
Monthly evolution of PEUC, NAN, and CYAN cell
abundances in the Thau Lagoon are illustrated in Fig. 2.
Table 1 shows the most significant period for each station
as detected by contingency periodograms. CYAN data
were submitted to contingency periodogram analysis only
for ROQS and PSM stations. Other stations were not
analyzed because of the high frequency of zero values in
the data set. A significant period of almost 1 yr was clearly
detected at all stations for the PEUC and NAN series.
For CYAN data recorded at stations ROQS and PSM, a
shorter periodicity of 8-9 months was detected. The annual cycle is obvious in the PEUC and NAN data series,
but not in the case of CYAN (Fig. 2). The lowest numbers
of PEUC and NAN were found in winter and the highest
in summer. At least two peaks of very high abundances
of PEUC (up to 1.8 x 1O5 cells ml-l; TBS station) were
detected during the warm season, and a lower peak was
detected in fall. This annual cycle is similar to the annual
succession described in temperate sea areas (e.g. Andersson et al. 1994).
The simultaneous evolution of PEUC abundances in
the Thau Lagoon has been confirmed by correlation
(Pearson’s r) computations among temporal series obtained at the different stations. PEUC densities at these
stations are all significantly correlated (P I 0.0001). The
same results were obtained for NAN (0.000 1 5 P I 0.0 1).
PEUC and NAN evolutions are not correlated (ZAS and
PSM, P > 0.05) or are weakly correlated (ROQS and
ZBS, P I 0.05), except for station TBS (P I 0.001).
Correlations among CYAN series recorded at each station
were also significant (P I 0.05) except for station PSM,
but CYAN abundances are not correlated with PEUC or
NAN abundances.
The simultaneous annual evolution of PEUC or NAN
groups in the different areas of the lagoon indicates that
only environmental
factors with seasonal variation and
that act at the ecosystem scale (e.g. temperature, solar
radiation) may regulate the dynamic of these phytoplanktonic groups. Mean values of picophytoplankton
monthly
abundances (n = 23; log-transformed data) were significantly correlated with temperature or irradiance values.
Correlations were stronger for PEUC (r = 0.740, P I
0.0001 for temperature, r = 0.692, P 5 0.0001 for irra-
1823
diance) than for NAN (r = 0.624, P = 0.0014 for temperature, r = 0.485, P = 0.0188 for irradiance). These
results indicate that PEUC abundances are more closely
related to temperature or solar irradiance than are NAN
abundances. Correlation values also show that PEUC and
NAN abundances are more strongly related to temperature than to solar irradiance. Andersson et al. (1994) have
shown that the biomass-specific production of the picoplankton fraction in natural seawater phytoplanktonic
assemblage exhibits the strongest seasonal temperature response when compared with larger cells. However, shortterm temporal variations may be superimposed on this
annual cycle, especially during warm months. PEUC
abundances show large short-term variations that cannot
be explained by factors that exhibit seasonal variations,
such as temperature. For instance, data obtained for 5
consecutive days (data not shown) at ZBS station indicated that it took 3 d for PEUC cells to reach a 3.5-fold
(16-19 July 1991) or a 3-fold (14-17 October 1991) increase in density, which led to a net doubling time estimate of 1.6 d. In such cases, short-term variations of
nutrients, light conditions, or grazing pressure have to be
tested to explain short-term dynamics of PEUC. For instance, large daily variations of nutrients in Thau Lagoon
have been already demonstrated (Legendre et al. 1989).
The mean abundances of PEUC, CYAN, and NAN
cells detected by flow cytometry are shown in Table 2 for
each sampling station. Percentages of PEUC relative to
total phytoplanktonic
cells (PEUC + CYAN + NAN),
also reported in Table 2, show that in Thau Lagoon the
phytoplankton community is clearly dominated by PEUC
cells. By contrast, the Mediterranean
seawater samples
(MERS station) showed higher CYAN and lower PEUC
and NAN abundances than in lagoon waters. If picophytoplankton
exceed NAN in Mediterranean
seawater
(MERS station), PEUC and CYAN show similar mean
abundances. There is an inverse relationship
between
PEUC and CYAN overall mean abundances estimated
at each sampling station (Y = -0.94 1, P I 0.0001; n =
5), but not between PEUC and NAN or CYAN and NAN
mean abundances. The spatial evolution of the mean
abundances of these phytoplanktonic
groups is illustrated
in Fig. 3.
It is difficult to compare mean values of picophytoplankters from this study with published values because
of differences in sampling strategies. Nearly all oceanographic studies on picoplankters are based on intensive
spatial (vertical or horizontal) sampling. In our case, the
temporal variability was more extensively sampled than
the spatial variability.
This sampling choice is clearly
justified for the type of ecosystem studied in light of the
large differences between seasonal densities and the simultaneous evolution of picoplankton abundances at the
different stations.
If we accept that temporal variability in oceans is lower
than it is in shallow coastal marine waters (i.e. that ponctual values recorded in other studies are representative
of picophytoplankton
mean concentrations), mean values
Notes
1824
PEUC
r-=~~~
--o-
Fig. 2. Monthly evolution of PEUC, NAN,
the Thau Lagoon and at the MERS station.
of picophytoplankton
abundances in Thau Lagoon are in
the range of upper values found in the literature (Weisse
1993). The mean value of total picophytoplankton
in
Thau Lagoon (3.5 x 1O4cells ml-l) is close to that reported
NAN
and CYAN
-a--
CYAN
j
cell abundances at five stations in
for eutrophic coastal waters
(3.8 x lo4 cells ml-r; Vanucci
those reported for surface
(1.9 x lo4 cells ml- ‘; Vaulot
of the
et al.
waters
et al.
northern Adriatic Sea
1994) but higher than
in the northwestern
1990) or eastern (0. l-
1825
Notes
Table 1. Most significant period (number of months in interval) of each contingency periodogram. Asterisks: *P I 0.10,
**P I 0.05, ***P I 0.01. PEUC-picoeucaryotes;
NAN-nanophytoplanktonic
cells.
Station
Group
ZAS
ROQS
ZBS
TBS
PSM
PEUC
NAN
11**
11**
12*
12*
12”“”
12**
12*
13**
12*
12**
MERS
1.O x 1O4 cells ml- l; Li et al. 19933) Mediterranean Sea,
or in the Golfe du Lion upwelling area (1.1 x 1O4 cells
ml-l; this study, station MERS).
A reason for the higher numbers of picophytoplankton
in Thau Lagoon than in sea areas probably relates to
higher nutrient content, as illustrated by data in Table 3.
However, in nutrient-rich coastal waters, researchers have
observed a decrease in the proportion that picoplankton
forms of the total phytoplankton
number (Weisse 1993).
This decrease was not observed in Thau Lagoon, where
picophytoplankton
represents 73-93% of the total phytoplanktonic
cells detected by flow cytometry, but the
contribution
of the <2qrn size fraction to total phytoplankton Chl a biomass and primary production (Table
4) was estimated to be 29.8 and 38.3%, respectively. These
values are in the upper range reported for coastal water
(Iriarte and Purdie 1994). As reported by De Madariaga
and Joint (1994), mean (+ SD) photosynthetic activity of
the ~2 pm cells [6.6 + 4.7 pg C (pugChl a)-’ h-l] was
clearly higher than it was for the largest fraction (2.5 x).
This high level of activity can be related to the physiological advantages of small cells (higher efficiency of nutrient uptake).
The lower contribution
of picophytoplankton
to total
phytoplankton
biomass than to total abundance can be
explained, at least partly, by their lower size. However,
one can ask if, by using a sample volume of 500 ~1 and
recording particles ~50 pm, our FCM data permit accurate estimation
of the proportion
that picophytoplankton forms of the total phytoplankton abundance. It is clear
that mean abundances of species with low numbers (e.g.
< 100 cells ml-l) cannot be estimated accurately, as is
Table 2. Mean abundances ( x 1O3 cells ml- *) of picoeucaryotes (PEUC), cyanobacteria (CYAN), and nanophytoplanktonic (NAN) cells detected by flow cytometry for each sampling
station. SD-standard
deviation.
Sta.
ZAS
ROQS
TBS
ZBS
PSM
MERS
No.
samples
62
61
63
63
53
26
PEUC
CYAN
NAN
(SD)
29.9(33.4)
27.5(27.7)
38.4(40.7)
39.6(37.6)
34.6(41.2)
5.15(2.86)
0.033(0.070)
0.192(0.19 1)
0.024(0.059)
0.019(0.05 1)
0.071(0.102)
5.57(4.70)
2.58(3.43)
4.08(4.45)
3.03(3.04)
2.75(3.04)
12.8(5.26)
1.9 l( 1.OS)
PSM
TBS
ZBS
ZAS
Thau Lagoon
Fig. 3. Distribution of the mean abundances of PEUC, NAN,
and CYAN cells from the Mediterranean
Sea to the lagoon
center.
the case for the largest microplanktonic
species when referring to allometric relationships. This also seems to be
the case for CYAN cells in the Thau Lagoon (see Fig. 2j.
However, if we refer only to abundances, there is no
significant contribution
of these cells to overall phytoplankton concentration, and even large (- 100%) errors
in CYAN or NAN estimations might not significantly
affect the PEUC proportion estimation.
If our data are representative of picophytoplankton
proportions, we must consider why picoplankton exceed
the numbers of larger cells in the nutrient-rich
waters of
the Thau Lagoon, leading to a ratio of picophytoplanktonic vs. larger phytoplanktonic
cell numbers approximating that in the open ocean. The mean phosphate and
nitrogen concentrations (Table 3) show that growth rates
of large cells would not be diffusion limited (Chisholm
1992). Trace elements in low concentrations, such as iron,
are supposed to play a role in regulating the size of phytoplankton in nutrient-rich marine ecosystems (Chisholm
1992), but they seem to be irrelevant in Thau Lagoon.
The iron surface sediment concentrations are 5-33.3 mg
g-l (Pena 1989) for th e fi ne fraction (~63 pm) and they
may be easily resuspended with wind speed > 5 m s-l;
such conditions occur -50% of the time (Troussellier et
al. 1993).
In fact, a more comprehensive explanation for the dominance of large phytoplankton
(>2 pm) over picophytoplankton in eutrophic areas is given by Riegman et al.
Table 3. Nutrient concentrations
goon and Mediterranean waters.
PEUC/
total
(O/o>
9 1.9
86.5
92.6
93.4
72.9
40.8
RWS
Med. Sea Exchange Zone
(pm01 liter-l)
in Thau La-
Golfe du Liont
N03NH,+
PO,3-
Thau
Lagoon*
Offshore
6.95
3.86
1.29
0.02
0.06
0.02
* From Picot et al. 1990.
t From Sayed et al. 1994.
Coastal
upwelling
1.5
0.17
1.10
Sea referencet
0.04
0.09
0.01
1826
Notes
Table 4. Average values (n = 48) of Chl a biomass and production of picophytoplanktonic
cells (~2 pm) and average percentage of the total contributed by picophytoplankton
for the
same variables. Values in parentheses represent standard deviations.
Chl a biomass
Picophytoplankton
O/oPicophytoplankton
0.35 pg liter-l
29.8 (16.8)
(1993). These authors showed that although smaller algae
are better competitors for nutrients than are larger algae,
which could lead to the dominance of pica- over nanoand microphytoplankton,
the high reproduction rate of
their predators makes small algae more susceptible to
grazing control than larger algae.
Apparently, the main trophic feature of Thau Lagoon
is the large-scale mollusc farming (oyster’s biomass of
- 35,000 t). This biomass has a potential filtering rate of
106-lo7 m3 h-l (Outin 1990) (i.e. the overall water volume of the lagoon, 250x lo6 m3, in l-10 d). Because
oysters have a retention efficiency > 50% for > 3-pm particles and < 10% for 5 1-pm particles (Deslous-Paoli 1987),
they may considerably limit the development of large
phytoplanktonic
cells. They can also eliminate small zooplanktonic organisms (e.g. ciliates and flagellates) that are
able to graze on picoplanktonic
cells.
To explore the differential potential effect of filter feed-
Production
(0.17)
3.3 yg C liter-l
38.3 (18.7)
ers on the two phytoplanktonic groups, we compared mean
abundances obtained from daily sampling inside and outside the shellfish-breeding
area (TBS and ZBS stations)
at four different seasons. There were no significant differences between ZBS and TBS mean abundances of PEUC
(t-test, P 2 0.05), but NAN abundances were significantly
higher (P 5 0.05) at TBS than at ZBS station for April,
July, and October campaigns. For the January campaign,
the lack of significant difference (P = 0.5 932) in NAN
abundances between the two stations may be due to low
filter feeder activity and(or) to low phytoplanktonic
productivity as a consequence of the decrease in water temperature and irradiance.
These data from inside and outside shellfish-breeding
area stations suggest that filter feeders may impose a differential grazing pressure on PEUC and NAN populations. However, to quantify the grazing effect, field data
need to be augmented by experiments. Another point to
Table 5. Picoeucaryote abundances from different geographical
following decreasing mean (range) abundances values.
Location
Mediterranean lagoon
Western North Atlantic
Ocean
West coast of New Zealand
Northern Baltic Sea (Gulf
of Finland)
West coast of New Zealand
Northwest Atlantic (Halifax shore)
Northeast Atlantic
Northern Adriatic Sea
Northwest Mediterranean
Sea
Southampton Water
Skagerrak (North Sea)
Danish coastal waters
Northern Baltic Sea (Gulf
of Finland)
North Pacific Ocean (Hawaii Island)
Sargasso Sea
Cells
(X lo3 ml-l)
mean and(or)
min-max
h-l (2.67)
locations. Data are ranked
Method*
Reference
33.2(0.78-260)
FCM
This study
26-33
FCM
Li et al. 1993a
6.8-58
EFM
Hall and Vincent
6-30
EFM
Kuosa 1991
EFM
Hall and Vincent
4.48-l 2.5
8.1(2.5-13.5)
2.65-4.62
FCM
FCM
EFM
Longhurst et al. 1992
Li 1994
Vanucci et al. 1994
3.0(0.0 l-l 6)
0.08-l 3
14.0 (max)
0.2-9.1
FCM
EFM
EFM
EFM
Vaulot and Partensky 1992
Iriarte and Purdie 1994
Kuylenstierna and Karlson 1994
Sondergaard et al. 199 1
EFM
Kuuppo-Leinikki
FCM
FCM
Campbell and Vaulot
CHLOMAX
1992
12.8(3-2 1)
2.0-4.0
1.75t
0.48(0.003-l
* EFM - epifluorescence microscopy;
t Mean of maximum values.
.39)
FCM - flow cytometry.
1994
1990
et al. 1994
1993
Notes
evaluate is the effective role of oysters and epibionts such
as ascidians, which develop on oysters. It is necessary to
experimentally control for filter feeder community composition to obtain specific grazing rates on PEUC and
NAN populations. These points are under study by our
team.
Even if picoplankton dominance can be explained by
a relatively low grazing pressure, a more unusual result
of our study is the high concentration of an eucaryotic
picophytoplankter
(which, to our knowledge, is the highest reported in the literature; Table 5) and its large dominance over procaryotic picophytoplankton
(PROC), such
as CYAN cells (see Fig. 3). Average abundance values of
PEUC in the northwest Mediterranean Sea (Vaulot and
Partensky 1992) or north Adriatic Sea (Vanucci et al.
1994) are 1O-fold lower than in Thau Lagoon. A PROC :
PEUC ratio of - 1 has been reported only in upwelling
areas or at times in estuarine areas, whereas large PROC :
PEUC ratios are generally observed (Hall and Vincent
1990; Iriarte and Purdie 1994; Vanucci et al. 1994).
To date, little is known about the factors that can explain the dominance of picoplankton
communities by
eucaryotic species. From the data set listed in Table 5, it
seems that higher abundances of PEUC are generally found
in coastal waters. Data from Vaulot and Partensky (1992)
on spatial distribution of PEUC abundances also showed
maxima in the vicinity of the Rhone River, which contributes large amounts of inorganic nutrients (Sayed et al.
1994). A link between low PROC : PEUC ratios and high
nitrate and phosphate concentrations was suggested by
Hall and Vincent (1990). When compared with offshore
waters of the Mediterranean
Sea, N03- is the nutrient
with the greatest increase in Thau Lagoon (Table 3). However, to our knowledge, no clear causal relationship has
emerged in the literature to support the idea that neither
picoeucaryotic nor large eucaryotic cells preferentially assimilate N03- (e.g. see Chisholm 1992).
Another way to explain the dominance of one picoplanktonic species over another concerns pigment composition and related light use efficiency. The pigment
composition of 0. tauri (Chretiennot-Dinet
et al. 1995),
which is the main component of Thau Lagoon picoplankton, differs greatly from those of typical picoplanktonic
species (e.g. Prochlorococcus and Synechococcus). It contains Chl a, Chl b, Chl c-like, and at least eight carotenoid
pigments. Among the large number of carotenoids detected in 0. tauri, violaxanthin cellular concentration represents -50% of the Chl a cellular concentration. Violaxanthin is a major light-harvesting
pigment, but like
other carotenoids, it has also the function of dissipating
energy and excitated states of O2 (Lawlor 1993). The large
amount of this carotenoid could give 0. tauri cells the
ability to use solar radiation efficiently and to limit photodestruction when light levels are as high as may occur
in the shallow and transparent Thau Lagoon waters (mean
depth, 4.5 m; light attenuation coefficient, 0.30-0.50 m-l)
Finally, one can also hypothesize that some chemical
factors variably limit the development of procaryotic picoalgae, such as cyanobacteria, which seemed to be more
numerous in Mediterranean waters (MERS station) than
1827
in Thau waters. Brand et al. (1986) indicated that cyanobacteria are lo-fold more sensitive to copper than are
eucaryotic algae. The study of heavy metal concentrations
in the sediment of the Thau Lagoon has shown (Pena
1989) that copper concentrations are very high (up to 100
Pg Is-’ in the northeast part of the lagoon). Copper originates from agricultural practices in the watershed (i.e.
copper is used as an anticryptogamic
in vineyards). It is
therefore possible that eucaryotic picoplankton are more
numerous than procaryotic picoplankton because of their
better resistance to copper.
The effect of increasing nutrient availability
in lagoon
waters is modulated by the effect of filter feeding macrofauna leading to the dominance of picoplanktonic
size
classes. In this group we hypothesized that the dominance
of eucaryotic forms and the simultaneous disappearance
of procaryotic forms were based on the lower efficiency
of the latter group to adapt to adverse conditions, such
as high trace metal (copper) levels.
Thus, a better understanding of the physiological and
ecological characteristics of picoplanktonic
species, especially of eucaryotic forms, is needed to obtain a more
comprehensive view of the dynamics and dominance of
such species in such an ecosystem.
And& Vaquer
Marc Troussellier
Claude Courties
Bertrand Bibent
Laboratoire d’Hydrobiologie
UMR CNRS 5556 and URM IFREMER
Universite Montpellier II
F-34095 Montpellier Cedex 05, France
No. 5
References
ANDERSSON, A.,P.
HAECKY,AND
A. HAGSTR~M.
1994. Effect
of temperature and light on the growth of micro- nano- and
pica-plankton:
Impact on algal succession. Mar. Biol. 120:
51 l-520.
198 6.
BRAND, L. E., W. G. SUNDA, AND R. R. L. GUILLARD.
Reduction of marine phytoplankton
reproduction rates by
copper and cadmium. J. Exp. Mar. Biol. Ecol. 96: 225-250.
CAMPBELL, L., AND D. VAULOT.
1993. Photosynthetic picoplankton community structure in the subtropical North Pacific Ocean near Hawaii (station ALOHA). Deep-Sea Res.
40: 2043-2060.
CHISHOLM, S. W. 1992. Phytoplankton
size, p. 213-237. In
P. G. Falkowski and A. D. Woodhead [eds.], Primary productivity and biogeochemical cycles in the sea. Plenum.
1992. Les maximums profonds de Chl a en mer
CHLOMAX,
des Sargasses - Don&es physiques, chimiques et biologiques. Camp. Oceanogr. Fr. 17. IFREMER, Brest.
CHR~TIENNOT-DINET,
M.J., ANDOTHERS. 1995. Anewmarine
picoeucaryote: Ostreococcus tauri gen. et sp. nov. (Chlorophyta, Prasinophyceae). Phycologia 34: 285-292.
Acknowledgments
This research has been supported by grants from PNOCOxythau and URM IFREMER No. 5 programs financed by
CNRS, IFREMER, MESR, and Region Languedoc-Roussillon.
1828
Notes
DE MADARLAGA, I., AND I. JOINT. 1994. Phtotosynthesis and
carbon metabolism by size-fractionated phytoplankton
in
the southern North Sea in early summer. Cont. Shelf Res.
14: 295-3 11.
DESLOUS-PAOLI, J. M. 1987. Assessment of energetic requirements of reared molluscs and of their main competitors, p.
3 19-346. In Aquaculture. Shellfish Culture Develop. Manage. Ifremer, Paris.
HALL, J. A., AND W. F. VINCENT. 1990. Vertical and horizontal
structure in the picoplankton communities of a coastal upwelling system. Mar. Biol. 106: 465-47 1.
-,
AND W. F. VINCENT.
1994. Vertical and horizontal
structure of the picophytoplankton
community in a stratified coastal system of New Zealand. N.Z. J. Mar. Freshwater Res. 28: 299-308.
HOLM-HANSEN,
O., C. J. LORENZEN, R. W. HOLMES, AND J. D.
H STRICKLAND.
196 5. Fluorometric
determination
of
chlorophylls. J. Cons. Int. Explor. Mer 30: 3-15.
IRIARTE, A., AND D. A. PURDIE.
1994. Size distribution
of
chlorophyll a biomass and primary production in a temperate estuary (Southampton Water): The contribution of
photosynthetic
picoplankton.
Mar. Ecol. Prog. Ser. 115:
283-297.
KUOSA, H. 199 1. Picoplanktonic
algae in the northern Baltic
Sea: Seasonal dynamics and flagella grazing. Mar. Ecol.
Prog. Ser. 73: 269-276.
KUUPPO-LEINIKKI,
P., AND OTHERS. 1994. Trophic interactions
and carbon flow between picoplankton
and protozoa in
pelagic enclosures manipulated with nutrients and a top
predator. Mar. Ecol. Prog. Ser. 107: 89-102.
KUYLENSTIERNA, M., AND B. KARLSON. 1994. Seasonality and
composition of pica- and nanoplanktonic cyanobacteria and
protists in the Skagerrak. Bot. Mar. 37: 17-33.
LA-R,
D. W. 1993. Photosynthesis, 2nd ed. Longman.
LEGENDRE, L., M. F~~CHETTE, AND P. LEGENDRE.
198 1. The
contingency periodogram: A method of identifying rhythms
in series of nonmetric ecological data. J. Ecol. 69: 965-979.
LEGEND=,
P., M. TROUSSELLIER, V. JARRY, AND M. J. FORTIN.
1989. Design for simultaneous sampling of ecological variables: From concepts to numerical solutions. Oikos 55: 3042.
LI, W. K. W. 1994. Primary production of prochlorophytes,
cyanobacteria, and eucaryotic ultraphytoplankton:
Measurements from flow cytometry sorting. Limnol. Oceanogr.
39: 169-175.
P. M. DICKIE, W. G. HARRISON, AND B. D. IRWIN.
19$3a. Biomass and production of bacteria and phytoplankton during the spring bloom in western North Atlantic
Ocean. Deep-Sea Res. 40: 307-327.
T. ZOHARY,
Y. Z. YACOBI, AND A. M. WOOD.
19b3b. Ultraphytoplankton
in the eastern Mediterranean
Sea: Towards deriving phytoplankton
biomass from flow
cytometric measurements of abundance, fluorescence and
light scatter. Mar. Ecol. Prog. Ser. 102: 79-87.
A. R., AND OTHERS. 1992. Sub-micron particles
in northwest Atlantic shelf water. Deep-Sea Res. 39: l-7.
OUTIN, V. 1990. Ecophysiologie de l’huitre Crassostrea gigas
(Thunberg) en milieu naturel. D.S. thesis, Univ. Paris 6,
130 p.
PI?NA, G. 1989. Sels nutritifs et micropolluants
metalliques
dans un ecosysteme lagunaire: l’etang de Thau. D.S. thesis,
Univ. Montpellier II. 143 p.
PICOT, B., G. P~NA, C. CASELLAS, D. BONDON, AND J. BONTOUX.
1990. Interpretation of the seasonal variations of nutrients
in a Mediterranean lagoon: Etang de Thau. Hydrobiologia
207: 105-l 14.
RIEGMAN, R., B. R. KUIPERS, A. A. M. NOORDELOOS, AND H.
J. WITTE. 1993. Size-differential control of phytoplankton
and the structure of plankton communities. Neth. J. Sea
Res. 31: 255-265.
RIEMANN, B., AND L. M. JENSEN. 199 1. Measurements of phytoplankton primary production by means of the acidification and bubbling method. J. Plankton Res. 13: 853-862.
SAYED, M. A., A. AMINOT, AND R. KEROUEL. 1994. Nutrients
and trace metals in the northwestern Mediterranean. Cont.
Shelf Res. 14: 507-530.
SBNDERGAARD, M., L. M. JENSEN, AND G. AERTEBJERG. 199 1.
Picoalgae in Danish coastal waters during summer stratification. Mar. Ecol. Prog. Ser. 79: 139-149.
TROUSSELLIER, M., G. CAHET, P. LEBARON, AND B. BALEUX.
1993. Distribution
and dynamics of bacterial production
in relation to wind perturbations in a Mediterranean lagoon.
Limnol. Oceanogr. 38: 19 3-20 1.
-,
C. COURTIES, AND S. ZETTELMAIER.
1995. Flow cytometric analysis of coastal lagoon bacterioplankton
and
picophytoplankton:
Fixation and storage effects. Estuarine
Coastal Shelf Sci. 40: 62 l-633.
VANUCCI, S., M. L. C. ACOSTA POMAR, AND T. L. MAUGERI.
1994. Seasonal pattern of phototrophic picoplankton
in
the eutrophic coastal waters of the northern Adriatic Sea.
Bot. Mar. 37: 57-66.
VAULOT, D., AND F. PARTENSKY.
1992. Photosynthetic picoplankton of the north west Mediterranean Sea in summer:
Comparison with the winter situation, p. 173-l 8 1. In J. H.
Martin and H. Barth [eds.], Eros 2000 (European river ocean
system). Water Pollut. Res. Rep. 28. CEC.
-,
AND OTHERS. 1990. Winter presence of prochlorophytes in surface waters of the northwestern Mediterranean
Sea. Limnol. Oceanogr. 35: 1156-l 164.
WEISSE, T. 1993. Dynamics of autotrophic
picoplankton
in
marine and freshwater ecosystems. p. 327-370. In J. G.
Jones [ed.], Advances in microbial ecology. Plenum.
LONGHURST,
Submitted: 3 August 1995
Accepted: 29 April 1996
Amended: 25 September 1996