JOURNAL OF PLANKTON RESEARCH
j
VOLUME 29
j
NUMBER
11
j
PAGES
999 – 1014
j
2007
Typology of environmental conditions at
the onset of winter phytoplankton
blooms in a shallow macrotidal coastal
ecosystem, Arcachon Bay (France)
CORINE GLÉ1*, YOLANDA DEL AMO1*, BÉATRICE BEC1, BENOÎT SAUTOUR1, JEAN-MARIE FROIDEFOND2, FRANCIS GOHIN3,
DANIÈLE MAURER4, MARTIN PLUS4, PIERRE LABORDE2 AND PIERRE CHARDY1
1
CNRS, UNIVERSITÉ BORDEAUX
1, UMR 5805-EPOC, ECOBIOC, STATION MARINE, D’ARCACHON, 2 RUE DU PROFESSEUR JOLYET, 33120 ARCACHON, FRANCE,
1, UMR 5805-EPOC, ECOBIOC, AVENUE DES FACULTÉS, 33405 TALENCE CEDEX, FRANCE, 3IFREMER CENTRE DE BREST,
4
BP 70 29280 PLOUZANE, FRANCE AND IFREMER DEL/AR, QUAI DU COMMANDANT SILHOUETTE, 33120 ARCACHON, FRANCE
2
CNRS, UNIVERSITÉ BORDEAUX
*CORRESPONDING AUTHOR: c.gle@epoc.u-bordeaux1.fr (G.C.) or y.delamo@epoc.u-bordeaux1.fr (D.A.Y.)
Received April 4, 2007; accepted in principle June 27, 2007; accepted for publication August 4, 2007; published online October 8, 2007
Communicating editor: K.J. Flynn
Phytoplankton dynamics were assessed in the macrotidal ecosystem of Arcachon Bay through highfrequency surveys over a 5-year period in order to characterize typology of environmental conditions
at the onset of the productive period. Temporal variations of hydrological and biological parameters
were examined in external and internal waters of the lagoon, during the winter –spring periods
from 1999 to 2003. An additional survey was performed during winter – spring 2005 in order
to study the vertical structure of the water column. The occurrence of winter phytoplankton blooms
between January and March emerged as a recurrent event. The early onset of the productive period
is influenced by the biological functioning of adjacent Bay of Biscay oceanic waters. It is hypothesized that under a propitious hydrodynamic regime, phytoplankton inocula from the Bay of Biscay
enter in the Arcachon Bay where cells presumably find favourable conditions for their fast development. The timing of the onset of those winter blooms in Arcachon Bay seems to be mainly influenced by the presence of anticyclonic weather conditions (associated with an increase in incident
irradiance) during late winter (i.e. by February), while the water column does not show any particular stabilization nor stratification liable to facilitate the onset of these blooms. Moreover, these
winter blooms dominated by diatoms led to an early nutrient depletion which could have inevitable
consequences on the structuration of the food web during spring and summer.
I N T RO D U C T I O N
In coastal temperate ecosystems, the basic scheme of
the plankton dynamics shows a productive period with
an important initial phytoplankton bloom during spring
(Margalef, 1958) based on new production and characterized by large cells (.20 mm) on which the classical
herbivorous food chain reposes. These spring blooms
are a characteristic feature of temperate North Atlantic
open waters (Harrison et al., 1993; Waniek, 2003), as
well as coastal and estuarine waters in temperate
latitudes (Cloern, 1996). However, over recent decades,
the increasing quantities of nutrients produced by
anthropogenic activities on the edges of coastal areas
(Howarth et al., 1996) as well as the climatic variability
(Edwards et al., 2002) have strongly modified the
primary production calendar, its extent, and the nature
of the phytoplankton communities (Cloern, 2001;
Edwards and Richardson, 2004).
In a few coastal ecosystems, the phytoplankton
dynamics pattern occasionally or recurrently shifts on the
doi:10.1093/plankt/fbm074, available online at www.plankt.oxfordjournals.org
# The Author 2007. Published by Oxford University Press. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org
JOURNAL OF PLANKTON RESEARCH
j
VOLUME 29
seasonal scale with early blooms starting by late winter
(Herbland et al., 1998; Labry et al., 2001; Townsend and
Thomas, 2001; Winder and Schindler, 2004). This is the
situation observed in coastal waters of the Bay of Biscay
and specially in the plumes of the Gironde and Loire estuaries where late winter phytoplankton blooms are
observed by February (Labry et al., 2001; Lunven et al.,
2005). Those early blooms have been observed within
hydrographic fronts during the establishment of halostratification and/or decrease of light vertical attenuation coefficient (Labry et al., 2001). The major consequence of the
early phytoplankton development in the Bay of Biscay is a
precocious nutritive limitation (Labry et al., 2002) leading
to a spring phytoplankton community dominated by small
cells (Herbland et al., 1998) and thus mainly grazed by
microzooplankton (Sautour et al., 2000). The timing of the
onset of the productive period is therefore one of the
essential factors determining its duration as well as
the total annual primary production rate. Moreover, as
phytoplankton represents the first step of the food chain,
the timing of bloom initiation has inevitable effects on the
trophodynamic fate of bloom products, including life
cycle of grazers (Edwards and Richardson, 2004).
Arcachon Bay (France) is a semi-enclosed embayment, situated on the east coast of the Bay of Biscay
below the Gironde estuary (100 km). This bay sustains a
high exploitation of Crassostrea gigas and the phytoplankton community structure affects the success of oyster
larvae recruitment (Maurer et al., 2003). In such
systems, it appears essential to understand the ecosystem
functioning and to specify under what conditions the
productive period starts and its chronology. More fundamentally, the main objective of this paper is to
characterize the phytoplankton dynamics in this coastal
lagoon during the winter– spring period. In this paper,
we address the following questions: (i) What is the
pattern of the phytoplankton dynamics in Arcachon
Bay during this period: do early blooms exist in this
system, as they do in the Bay of Biscay and if so, is this
a recurrent phenomenon?; (ii) Is there any coupling link
between the adjacent Bay of Biscay winter blooms and
phytoplankton dynamics within Arcachon Bay? And (iii)
What are the climatic and hydrological conditions that
characterize the onset of the productive period?
METHOD
Study area
Arcachon Bay (448400 N 018100 W; Fig. 1) is a semienclosed embayment of 174 km2 on the southwest coast
of France, connected to the Bay of Biscay (Atlantic
j
NUMBER
11
j
PAGES
999 – 1014
j
2007
Ocean) by a large opening (3 km wide). In the inner
lagoon (156 km2), channels (41 km2) penetrate between
large intertidal areas (115 km2), mostly covered by seagrass beds. This shallow lagoon is a macrotidal environment (maximum tidal range 4.35 m) characterized by
semi-diurnal tides enabling important water exchanges
with the ocean through the southwest entrance of the
lagoon. Those are estimated at 384106 m3 for an
average spring tide and 264106 m3 for an average
neap tide. Continental inputs also participate to the
distribution of the water masses but to a lesser degree as
the volume of seawater exchange with Bay of Biscay
waters during one single tide is higher than the total
annual river discharge to the Bay. Annual freshwater
inputs average 1.25106 m3 with a major part (4/5)
coming from the Leyre estuary located in the southeastern part of the bay. The remaining one-fifth is provided by secondary canals, e.g. the Lège Canal, at the
northeast area (Carruesco, 1989).
The influence of both oceanic inputs derived from
the Bay of Biscay and freshwater runoff due to the river
Leyre and secondary canals permits us to distinguish
clearly two distinct geographical areas in the bay
according to hydrological parameters (Vincent, 2002):
(i) the external waters, directly influenced by the
oceanic waters; (ii) the internal waters, particularly influenced by continental inputs. The bay is therefore a
heterogeneous ecosystem according to its hydrology.
Arcachon Bay is subjected to a typical oceanic temperate climate where prevailing winds were westerly
(Manaud et al., 1997).
Sampling strategy
Two sampling locations were chosen in order to
compare external and internal part of the bay: the first
one is located in the external waters (EW; station
“Bouée 13”; 44838 N, 1814 W; Fig. 1), characterized by
a flushing time of about 4 days in winter (Plus et al.,
2006). This station is situated in a channel 17 m deep,
characterized by neritic coastal water masses at high
tide. It is therefore considered as representative of the
Bay of Biscay waters entering the bay at high tide
(Guillocheau, 1988).
A second sampling site is located in the internal
waters (IW; station “Comprian”; 44840 N, 1805 W;
Fig. 1), near continental inputs (i.e. river Leyre), and is
characterized by a flushing time of about 13 days in
winter (Plus et al., 2006). This station is situated in the
south-eastern channel of the bay and is characterized
by a depth of 7 m.
Sampling was performed at the two stations during
the winter– spring periods (from January to May)
1000
C. GLÉ ET AL.
j
WINTER PHYTOPLANKTON BLOOMS
Fig. 1. Sampling locations in Arcachon Bay: External waters (EW) (“Bouée 13”) and Internal waters IW (“Comprian”).
during five consecutive years, from 1999 to 2003.
Samples were collected three times a week from 1999 to
2002 and two times a week in 2003. Each sampling was
performed in sub-surface (21 m) and centred on the
high tide, providing the best chances to sample neritic
water masses entering the bay. In order to study the vertical structure of the water column, an additional study
was performed in 2005 at both stations, during high
tide and with a monthly sampling strategy from January
to April.
Climatic and physical environment
Data on daily-integrated irradiance (i.e. incident irradiance) were provided by the meteorological station of
Arcachon Bay (Météo France).
Seawater salinity and temperature measurements
were obtained with a thermosalinometer (WTW
Tetracon 325). Discrete sampling was carried out at
subsurface (1 m below the surface) by using 5 L Niskin
samplers, fitted with non-toxic silicone tubing. In 2005,
temperature and salinity profiles were measured in the
whole water column with a CTD probe (Sea Bird,
SBE-19). The system was also equipped with light
sensors (Biospherical/Licor) to measure photosynthetically available radiation (PAR; 400 –700 nm). Density
vertical distribution was determined from temperature,
salinity and pressure profiles.
The vertical attenuation coefficient K for PAR was
calculated from the relation between irradiance (Ez),
surface irradiance (Eo) and depth z using PAR data:
Ez¼Eo* e2KZ. K is the slope of the linear regression
between ln Ez and depth Z. Depth of the euphotic
1001
JOURNAL OF PLANKTON RESEARCH
j
VOLUME 29
layer, Ze, was assumed to be the depth of 1% of surface
irradiance and was determined by Ze¼ – (ln 0.01)/K.
Chemical and biological variables
All seawater samples were collected in subsurface waters
(1 m below the surface) by using 5-L Niskin samplers
and kept on a l0 L polypropylene (PP) carboy. Nutrient
and phytoplankton subsamples were performed on
board and the remaining water was kept in an icebox
until return to the laboratory for chlorophyll a (Chl a)
filtrations and primary production incubations.
For nutrient measurements, seawater was directly filtered either on glass fibre filters (Whatman GF/C for
nitrateþnitrite and phosphate) or on cellulose acetate
filters (for silicic acid) with a syringe filtration system,
and stored in 100 mL glass bottles (nitrateþnitrite and
phosphate) or in 100 mL PP bottles (silicic acid).
Nutrient samples were then either stored at 48C for
silicic acid or frozen (2208C) for nitrateþnitrite and
phosphate. Ammonium was immediately fixed by the
addition of working reagents (Koroleff, 1969) and kept
in the dark. Phosphate (Murphy and Riley, 1962),
nitrateþnitrite (Bendschneider and Robinson, 1952)
and silicic acid (Mullin and Riley, 1955) concentrations
were measured on a Technicon Auto Analyser II.
Ammonium was analysed according to Koroleff (1969).
For chlorophyll a (Chl a) and phaeopigment determinations, 0.5 L of seawater were filtered through
Whatman GF/F filters. Filters were immediately frozen
(2208C) until further analysis by the fluorimetric
method (Yentsch and Menzel, 1963), using a Turner
Design 700 fluorometer calibrated with a standard solution of purified chlorophyll a (Sigma Chemical Co.).
Samples for the identification of phytoplankton
species composition were preserved immediately on the
collection with an acid lugol solution. Phytoplankton
species were identified and counted by microscopic
examination on an inverted microscope (ZEISS) in
accordance with Utermöhl method (Utermöhl, 1958)
for the years 2000, 2001 and 2003. A minimum of 400
cells were counted leading to an accuracy range of 10%
(Lund et al., 1958).
Primary production rates were also measured in
sub-surface during winter–spring 2003 in the EW and
IW. The experimental design was based on the measurement of C incorporation with the 14C method of
Steeman–Nielsen (Steeman Nielsen, 1952) and using in
situ simulated incubations. Unprefiltered seawater was
dispensed into 250 mL translucent polycarbonate bottles
and inoculated with 1 mL (ca. 5.6 mCi–1.85105 Bq) of
NaH14CO3 solution (Carbon 14 Centralen, Denmark).
Dark incubations were periodically performed for
j
NUMBER
11
j
PAGES
999 – 1014
j
2007
control. Bottles were then incubated in an outdoor tank
filled by a continuous flow of seawater directly pumped
from Arcachon Bay in order to maintain ambient water
temperature. This outdoor tank received during the incubation time the natural incident daylight irradiance (i.e.
solar radiation). After 24 h incubation, samples were
filtered onto 0.4 mm Nucleopore filters which were
immediately covered with 250 mL of 0.5 M HCl and
scintillation vials were stored at room temperature until
counting. Initial specific activities of each sample were
counted from 250 mL of sample collected from incubation bottles and stored in a vial with 100 mL of NaOH
(1 N). Before counting, 10 mL of liquid scintillation cocktail (Ultima Gold Packard) was added to each vial and
activity was counted after 24 h in the dark with a
Beckmann LS 6500 liquid scintillation counter. Primary
production rates were calculated using usual equations
converting DPM values to daily production rates, assuming 25 000 mg C m23 for DIC concentration following
the JGOFS protocol (JGOFS, 1988). As incubations were
rarely dawn-to-dawn due to the tide-dependent sampling
times, daily primary production rates (mg C m23 day21)
were corrected according to Moutin’s model (Moutin
et al., 1999) which accounts for geographical position,
length of sunshine and incubation timing.
Chlorophyll-specific primary productivity (P/B,
mg C mg Chl a 21 h21) was calculated as the carbon fixation rate (P) per unit of Chl a (B).
In order to verify how hydrodynamism can affect
particle dispersion ( phytoplankton cells) within the
lagoon, we have tested the hypothesis that a given Chl a
concentration present in the external waters can attain
the internal waters of the bay by using a bi-dimensional
hydrodynamic mathematical model. Phytoplankton
biomass dispersion was calculated by the MARS model
(horizontal
resolution:
235 m)
developed
by
IFREMER—French Research Institute for Exploitation
of the Sea—(Salomon et al., 1995) and calibrated for
Arcachon Bay (Plus and Durand, 2004). Briefly, the
algorithm calculates surface elevation and barotropic
currents, as well as dissolved and suspended elements
transported by currents. In this model, Chl a concentrations are assimilated to a passive tracer, i.e. mortality,
sedimentation and growth rates are not taken into
account. The simulation is forced by real conditions of
tide, river run-off and wind using 2003 data.
For a larger assessment of phytoplankton dynamics in
the adjacent oceanic waters, ocean colour data were
used. Daily maps of Chl a concentrations of the Bay of
Biscay surface waters, during February 2003, have been
provided by IFREMER (MarCoast project) from
SeaWiFS data. Briefly, the SeaWiFS radiances have
been processed by an empirical algorithm adapted to
1002
C. GLÉ ET AL.
j
WINTER PHYTOPLANKTON BLOOMS
coastal waters (i.e. modifications of the SeaWiFS Ocean
Colour 4 band algorithm¼OC4 by including the 412
and 555 channels) to avoid overestimations of Chl a
concentration due to yellow substances and suspended
matter. The complexity of the parameterization of the
relationship between the OC4 ratio and the 412 and
555 bands led to the creation of a “look up table” that
was applied to SeaWiFS data, to provide realistic chlorophyll concentration maps in the mixed coastal-clear
water area (Gohin et al., 2002). For a full description of
the algorithms, see Gohin et al. (2002).
R E S U LT S
Physical and climatic environments
The general pattern of the Leyre river flow rates
recorded during the five study periods (i.e. winter–
spring; Table I) reveals a high interannual variability.
The winter– spring 2001 exhibited the highest mean
flow rates (45 m3 s21). On the contrary, the winter–
spring 2002 was especially dry and river flow rates
remained very low (8 m3 s21).
As evidenced by salinities (Table I), the EW (external
waters) behaves as a typical marine ecosystem with salinity
mean values generally .33. In the IW (internal waters),
due to its geographical position near to freshwater inputs,
salinities were lower than those of the EW but generally
.25. In these two water masses, lower mean salinities
were observed in 2001 when high river discharges led
punctually to important decreases (down to 29.9 in the
EW and 20.3 in the IW). Conversely, the very dry 2002
winter–spring exhibited the highest mean salinities
(average .34.6 and 32.7 in the EW and IW, respectively).
Table I: Average and range salinities and
temperatures (8C) in the External (EW) and
Internal waters (IW) of Arcachon Bay and
average Leyre flow rates for the five study
periods (from January to May)
1999
2000
2001
2002
2003
EW
IW
EW
IW
EW
IW
EW
IW
EW
IW
Salinity mean
(range)
Temperature (88 C)
mean (range)
33.7
28.9
33.8
29.3
33.3
26.5
34.6
32.7
34.0
30.7
12.2
12.4
11.6
11.5
12.6
12.4
12.5
12.6
12.3
12.4
(31.5 –34.7)
(24.9 –30.6)
(32.3 –34.7)
(26.7 –33.1)
(29.9 –36.5)
(20.3 –32.8)
(33.8 –35.1)
(30.1 –33.7)
(31.1 –35.0)
(20.3 –33.3)
(9.5 –15.8)
(8.0 –18.9)
(6.3 –16.8)
(6.1 –19.3)
(8.6 –17.4)
(7.2 –21.5)
(10.6 – 16.5)
(8.2 –17.8)
(8.8 –15.9)
(6.0 –18.7)
Average
Leyre flow
rates (m3s21)
Average temperatures of the five winter– spring
periods (Table I) did not show great differences between
the EW and IW. A comparison of the five years showed
slightly lower temperatures during the 2000 study
period (,128C) than during the other years in the two
water masses. Seasonal variations of water temperatures
in the EW and IW followed the usual seasonal cycle,
characterized by minimal winter values in January –
February and maximal values during May (Table I,
Fig. 2). Temperatures in the IW (Fig. 2) were generally
lower than those recorded in the EW during January –
February (mean difference¼1.38C) and higher from
March to May (mean difference¼0.78C). These two
water masses were at the same temperature (homothermous period) during a short period observed generally
in March (from 5th to 12th March 1999, 25th February
to 18th March 2000, 14th March to 2nd April 2001,
15th to 20th March 2002 and 6th to 20th March 2003).
Based on this seasonal pattern of temperature differences between the EW and IW, two periods have been
distinguished (Fig. 2): (i) the winter period (22nd
January – 5th March 1999, 17th January – 25th February
2000, 19th January – 14th March 2001, 21st January –
15th March 2002 and 16th January – 6th March 2003)
marked by higher temperatures in the EW than in the
IW and (ii) the spring period until the end of the
studied period, when temperatures in the EW were generally lower than in the IW.
In order to assess the influence of incident irradiance
on phytoplankton and considering our 3-days interval
sampling strategy, we have summed the daily-integrated
irradiance for the 3 days before each sampling date
(Fig. 2). The 3-days cumulated irradiance followed the
classical seasonal evolution of temperate areas with
lowest values in January and maximum values in May.
During winter, some periods were characterized by
anticyclonic weather conditions (i.e. anticyclonic
window is equal to consecutive days with relatively high
irradiance), especially during February when 3-days
cumulated irradiance exceeded 3000 J cm22. During
spring periods, a clear step-like increase was observed
during March for the years 1999, 2000, 2002 and 2003,
while for the year 2001, irradiance raised in a more
progressive way from January to May.
21
28
45
8
17
Structure of the water column and light
conditions
The vertical structure of temperature and salinity was
studied during the winter–spring 2005. In both water
masses, temperature and salinity differences between
surface and bottom waters (Fig. 3) were weak during the
2005 winter–spring period, generally less than 0.88C and
1003
JOURNAL OF PLANKTON RESEARCH
j
VOLUME 29
j
NUMBER
11
j
PAGES
999 – 1014
j
2007
Fig. 2. Time course variations of temperatures (8C) in the External waters (EW) and Internal waters (IW) and 3-days cumulated incident
irradiance (J cm22) from January to May during 1999– 2003. Vertical dashed lines delimit the winter and spring periods (see text for details).
with variations in salinity of 0.5. The corresponding vertical gradient of density shows that from January to April,
the Arcachon Bay waters exhibited a homogeneous vertical structure. The maximal vertical density difference,
reaching 0.23, was observed in the IW on 31st March.
Values of the vertical attenuation coefficient (K,
Table II) do not show pronounced spatial variability
between the EW and IW except in April 2005 when K
was higher in the IW (0.55 m21) than in the EW
(0.29 m21). In the two water masses, values of K
1004
C. GLÉ ET AL.
j
WINTER PHYTOPLANKTON BLOOMS
masses during 2002, silicic acid concentrations reached
their lowest values (2 mM in the EW and 4 mM in the
IW), as a consequence of low Leyre River flow rates.
Average phosphate concentrations were generally low in
the two water masses (,1 mM) except in 2001 when
they reached 1.3 mM in the EW.
During the productive period (from February to
May), the start of the productive period coupled with
weaker freshwater inputs led to a drastic decrease of
nutrient concentrations in both stations, except during
March when freshwater inputs, following spring rainfalls, led to pulsed nutrient enrichments.
Fig. 3. Vertical structure of temperature, salinity and density during
winter–spring 2005 in the External waters (EW) and Internal waters
(IW) of Arcachon Bay.
decreased from January to April, affecting the euphotic
layer depth (Ze). In the EW, Ze was shallower than the
maximum water depth during January, and became
deeper (or equal) to the maximum water depth from
February to April. In the IW, Ze was always deeper than
the maximum water depth.
Nutrients
For the five study years, just before the productive
period beginning, the average DIN (nitrateþnitriteþ
ammonium) and Si concentrations in the ENW were
the highest (ranges from 3.7 to 9.1 mM for DIN and
from 2 to 7.1 mM for Si; Table III) but remained nevertheless low value for a typical coastal embayment.
Similarly, in the INW, average DIN and Si levels were
maximal before the start of the productive period and
due to the proximity of the Leyre River, levels were
higher than in the ENW (ranges from 4.2 to 30 mM for
DIN and from 4 to 22.5 mM for Si). In the two water
Table II: Mean value of the vertical
attenuation coefficient K (m – 1) and the depth
of the euphotic layer Ze (m) in the External
waters (EW) and Internal waters (IW) of
Arcachon Bay during winter-spring 2005
Dates
Stations
K (m21)
Ze (m)
31/01/2005
EW
IW
EW
IW
EW
IW
EW
IW
0.50
0.46
0.30
0.30
0.19
0.15
0.29
0.55
9.2
10.0
15.4
15.4
24.2
30.7
15.8
8.4
03/02/2005
31/03/2005
14/04/2005
Seasonal plankton cycle and biomass
parameters
In order to facilitate the study of the productive period
onset, we have split the Chl a series between two
periods: the first termed the “winter bloom” and the
second “spring blooms”. The distinction of “winter”
and “spring” periods was based on the seasonal pattern
of temperature differences between the EW and IW as
described previously.
In the two water masses, Chl a concentrations were
generally ,2 mg L21 by mid January (Fig. 4). Afterwards,
the seasonal pattern of Chl a concentrations showed an
early start of the productive period (.2 mg L21) with a
rapid increase of the phytoplankton biomass (excepted in
2000) as early as February. Globally, the winter Chl a
maxima were higher in the EW than in the IW (5-years
average of Chl a winter maxima¼5.6 and 4.2 mg L21 in
the EW and IW, respectively). In the two water masses, the
lowest winter blooms were observed during 2000
(2.5 mg L21 in the EW and IW) and the greatest in 2002
(9.4 mg L21 in the EW and 7.4 mg L21 in the IW). The
onset of winter blooms in the EW and in the IW are either
delayed in time (earlier in the EW, in 1999 and 2003) or
synchronous (2000, 2001 and 2002). The spring period
was then evidenced by successive Chl a peaks showing
variable intensities in the two water masses. Chl a concentrations remained low during 1999 (below 2.5 mg L21 in
the EW and IW), whereas they reached their maximum
during 2002 spring (14.9 mg L21 in the EW and
7.1 mg L21 in the IW). Phaeopigment concentrations
were generally lower than Chl a values and their temporal
evolution was close to that of Chl a (data not shown).
Phytoplankton species determinations showed that winter
blooms were dominated by diatoms (60%) and abundant
autotrophic nanoflagellates (.30%) as Cryptophyceae
and Prymnesiophyceae in both stations. The dominant
diatom populations during the winter bloom were the
same in the EW and IW, and mainly composed of
Lauderia spp., Skeletonema costatum and Thalassiosira spp. in
1005
JOURNAL OF PLANKTON RESEARCH
j
VOLUME 29
j
NUMBER
11
j
PAGES
999 – 1014
j
2007
Table III: Average nutrient concentrations (in mM) in the External waters (EW) and Internal waters
(IW) of Arcachon Bay for the 1999, 2000, 2001, 2002 and 2003 study periods
DIN (mM)
Silicic acid (mM)
Phosphate (mM)
Year
Periods
EW
IW
EW
IW
EW
IW
1999
Before productive period
During productive period
Before productive period
During productive period
Before productive period
During productive period
Before productive period
During productive period
Before productive period
During productive period
5.9
2.9
4.9
5.2
4.6a
3.1a
3.7
3.1
9.1
2.4
10.3
5.3
–
–
20.2a
11.1a
4.2
3.2
30.0
7.7
4.3
2.1
4.2
2.6
7.1
1.9
2.0
1.4
6.4
2.2
–
–
–
–
20.9
10.6
4.0
3.6
22.5
7.7
1.0
0.8
0.2
0.4
1.3
0.5
0.3
0.2
0.3
0.2
0.5
0.7
–
–
0.3
0.2
0.2
0.1
0.3
0.2
2000
2001
2002
2003
The average nutrient concentrations observed before the beginning of the productive period have been calculated from 22nd January to 12th February
1999, from 17th January to 2nd February 2000, from 19th January to 21st February 2001, from 21st January to 13th February 2002 and from 16th
January to 20th February 2003. The average concentrations during the productive period have been calculated from the onset of the winter blooms to
the end of the study periods (i.e. May). DIN¼nitrateþnitriteþammonium.
a
Ammonium not available.
winter 2000, Chaetoceros spp. and Asterionella glacialis in
winter 2001 and A. glacialis in winter 2003. During the
spring period, in the two water masses, diatoms
accounted for as much as 80% of the total phytoplankton abundances and were essentially represented by
Leptocylindrus danicus, Pseudonitzschia spp., Chaetoceros spp.
and A. glacialis.
In 2003, the pattern of P/B (carbon fixation rates per
unit of biomass based upon Chl a) shows several
increases starting from mid-February in both water
masses (Fig. 5). During the 2003 winter bloom, P/B of
1.1 mg C mg Chl a 21 h21 were observed in the EW (on
27th February) and of 1.8 mg C mg Chl a 21 h21 in the
IW (on 6th March). The maximum P/B values were
reached during the spring period: on 31st March in the
EW (2.8 mg C mg Chl a 21 h21) and on 22nd April in
the IW (4.9 mg C mg Chl a 21 h21).
For the 2003 winter– spring period, P/B and levels
of daily-integrated incident irradiance (Fig. 5) show a
significant correlation in the EW (r ¼ 0.63, P , 0.001,
n ¼ 37; Pearson test) and IW (r ¼ 0.66, P ¼ 0.001,
n ¼ 37; Pearson test).
Dispersion of chlorophyll biomass in the
lagoon
We have chosen to simulate the Chl a biomass dispersion in the lagoon during the winter 2003 when Chl
a concentrations show the clearest delay (7 days)
between winter peaks in the EW (on 27th February) and
IW (on sixth March; Fig. 4). Phytoplankton biomass dispersion was modelled from 27th February to 6th March
2003, under real (i.e. in situ) tide, river run-off and wind
conditions. Figure 6A presents the initial conditions of
the simulation in Arcachon Bay on 27th February 2003:
Chl a concentrations attributed to the EW and IW at the
start of the simulation correspond to in situ Chl a
measured in these water masses (7 and 1.3 mg L21,
respectively). The simulation shows that in 7 days, the
main part of the initial phytoplankton biomass present
in the EW was ejected towards the ocean (Fig. 6B).
Nevertheless, a part of this initial phytoplankton
biomass is transported towards the internal part of the
lagoon, reaching by 6th March 2003 concentrations
ranging from 3 to 4 mg L21 in the IW, i.e. lower than
those measured in these water masses (5 mg L21).
Chl a concentrations derived from SeaWiFs
data
Chl a images from SeaWiFS data showed an increase of
surface Chl a in the Bay of Biscay coastal waters by
mid-February 2003 (Fig. 7), i.e. simultaneously to the
EW winter bloom. From 18th to 21st of February, the
Chl a concentrations increase in time and from South
to North along the Biscay east coast, in the direction of
Arcachon Bay. The 21st February 2003, the Chl a concentrations derived from satellite data reached up to
10 mg m23 (10 mg L21) along the Biscay coast while
during early March, the Chl a concentrations dropped
down to ,2 mg m23 (2 mg L21; data not shown).
DISCUSSION
Oceanic influence on the onset of winter
phytoplankton bloom in Arcachon Bay
In Arcachon Bay waters, the increase of Chl a concentrations between January and February from 1999 to
1006
C. GLÉ ET AL.
j
WINTER PHYTOPLANKTON BLOOMS
Fig. 5. Time course variations of the Chl a-specific primary
productivity (P/B in mg C mg Chl a 21 h21) in the External waters
(EW) and Internal waters (IW) and incident irradiance in
(J cm22 day21) in Arcachon Bay during winter–spring 2003.
Fig. 4. Time course variations of chlorophyll a (in mg L21) in the
External waters (EW) and Internal waters (IW) of Arcachon Bay
during winter–spring 1999, 2000, 2001, 2002 and 2003.
2003 shows the occurrence of a late winter phytoplankton bloom, which appears as a recurrent seasonal event
(Fig. 4). Winter blooms were initiated as early as
February for the five study years and usually persist over
periods of several weeks (from 2 to 5 weeks) in
Arcachon Bay. Although winter phytoplankton blooms
are now recognized as a common feature of the annual
phytoplankton cycle in the adjacent Bay of Biscay
waters (Herbland et al., 1998; Beaufort and Heussner,
2001; Labry et al., 2001; Lampert, 2001; Gohin et al.,
2003) and in faraway systems as the Massachusetts Bay
(Kelly and Doering, 1997; Keller et al., 2001), the Gulf
of Maine (Durbin et al., 2003), the Narragansett Bay
(Oviatt et al., 2002) or the Chesapeake Bay (Glibert
et al., 1995), this is the first high frequency monitoring
which permits to observe them within Arcachon Bay
waters.
A well more significant result of our study concerns
the relationships that can be evidenced among a macrotidal coastal lagoon and the adjacent oceanic waters in
terms of combined phytoplankton dynamics. Winter
phytoplankton species dominating in Arcachon Bay
were essentially composed of diatoms larger than
20 mm (Lauderia spp., Thalassiosira spp., Chaetoceros spp., S.
costatum) and large colonies (A. glacialis), typical of spring
phytoplankton populations (Margalef, 1958) that grow
under rich nutrient conditions. These populations correspond to those blooming during late winter and early
spring in the Bay of Biscay waters and more generally
along the French coasts e.g. Thalassiosira spp, A. glacialis,
1007
JOURNAL OF PLANKTON RESEARCH
j
VOLUME 29
j
NUMBER
11
j
PAGES
999 – 1014
j
2007
Fig. 7. Daily Chl a concentrations estimated by SeaWiFS maps along
the Biscay coast for 18th and 21st February 2003. The spot (A) is
located 50 km South from the Arcachon Bay.
Fig. 6. Phytoplankton cell dispersion calculated by the hydrodynamic
model MARS-2D developed by IFREMER (Salomon et al., 1995) and
calibrated for Arcachon Bay (Plus and Durand, 2004) with a
horizontal resolution of 235 m from 27th February 2003 (A) to sixth
March 2003 (B). See text for details.
Chaetoceros danicus (Beliaeff et al., 2001; Labry et al., 2001;
Gailhard et al., 2002; Gohin et al., 2003). Satellite estimates of surface Chl a in the oceanic waters adjacent to
the lagoon, at the timing of the 2003 winter bloom in
the EW (i.e. February), corroborated the existence of
great phytoplankton developments (10 mg L21) during
early winter on the continental shelf waters (Bay of
Biscay), close to Arcachon Bay (Fig. 7). This observation
is consistent with the hypothesis that the biological functioning of adjacent oceanic waters may influence the
timing and the chronology of the productive period in
Arcachon Bay. The hypothesis made here is that horizontal transport of water masses at each high tide can
be a source of phytoplankton (i.e. phytoplankton
inocula) when oceanic adjacent blooms are advected
into the lagoon (the flushing time is approximately 4
and 13 days for the EW and IW, respectively).
In terms of internal functioning of Arcachon Bay, the
comparison of temporal variations of Chl a concentrations between the EW and IW (Fig. 4) showed that
some years, under some particular conditions (i.e. tidal
coefficient, wind, oceanic phytoplankton dynamics), the
winter bloom started first in the EW and secondarily in
the IW (in 1999 and 2003; Fig. 4). Additionally, the
intensity of winter blooms in the EW was always higher
than those of the IW and the dominant phytoplankton
species characterizing these winter blooms are similar in
the two water masses. The simulation of the Chl a
biomass advection within the lagoon (for the 2003 scenario; Fig. 6) has shown that the dispersion and advection of phytoplankton from the EW towards the IW
could be in part responsible of the winter bloom
observed in the inner part of the bay and could explain
the decreasing gradient of Chl a observed every year
from the EW to the IW. However, these single hydrodynamic processes do not seem sufficient to explain the
5 mg L21 of Chl a measured in the IW. The increase of
the biomass-specific primary productivity (P/B) at the
time of the winter bloom in the IW (1.8 mg C mg Chl
1008
C. GLÉ ET AL.
j
WINTER PHYTOPLANKTON BLOOMS
a 21 h21) proved that Chl a levels observed in the IW
during the winter bloom were not only the result of
cells advection but were also originated from local phytoplankton production (Fig. 5). This local production
could be supported by phytoplankton inoculum from
EW finding favourable conditions for blooming in the
inner part of the bay, as well as by autochthonous phytoplankton, which could explain that some years winter
bloom was synchronous in the two water masses.
To conclude, horizontal transport can be a source of
phytoplankton when outer blooms are advected into
macrotidal coastal systems by a propitious hydrodynamic regime. The occurrences of these phenomena
may vary seasonally and spatially with hydrodynamic
forcing such as wind, freshwater flow and tidal currents
(Lucas et al., 1999) and could also explain that some
years, delay between the onset of winter bloom in the
EW and IW has not be evidenced. Finally, phytoplankton inocula that enter into Arcachon Bay necessarily
finds favourable climatic (light, wind regime) and hydrological (nutrients, temperature, turbulence) conditions in
this bay for their fast development.
Typology of environmental conditions
at the onset of the winter bloom
In coastal ecosystems, the conditions that determine the
timing of the onset of the productive period are the
result of the conjunction of several favourable factors as
temperature, nutrient and light availability, as well as
low grazing pressure (Thórdardóttir, 1986).
Nutrient concentrations in the two water masses were
at their highest levels before the start of the productive
period. Compared to typical French coastal embayment
(Wafar et al., 1983; Del Amo et al., 1997; Struski et al.,
2006), ranges of concentrations (Table III) appeared
to be low for the ENW (ranges: 3.7 – 9.1 mM for DIN,
2 –7.1 mM for Si, 0.2– 1.3 mM for P) and moderate in
the INW (ranges: 4.2– 30 mM for DIN, 4 – 22.5 mM for
Si, 0.2– 0.5 mM for P). However, in the two water
masses, nutrient levels were well above half-saturation
constants for nutrient uptake (Ks) reported by Fisher
et al. (Fisher et al., 1988) for natural populations in
coastal temperate ecosystems (DIN¼1 – 2 mM, silicic
acid¼1 – 5 mM, phosphate¼0.1 – 0.5 mM). Moreover,
amongst the five study periods, the greater winter bloom
was observed when nutrient concentrations were at their
lowest levels (i.e. 2002). These observations support the
idea that winter nutrient stocks were sufficient to sustain
a fast development of phytoplankton cells at this period
but not a triggering factor acting on the early onset of
the productive period in Arcachon Bay as shown in the
Gironde plume estuary (Labry et al., 2001).
In Narragansett Bay, the onset of the winter bloom
has been shown to be the result of grazing pressure relaxation (Pratt, 1965; Martin, 1970). In Arcachon Bay,
planktonic metazoa abundances are usually at their
lowest levels during winter (Castel and Courties, 1982;
D’Elbée and Castel, 1991; Vincent, 2002), and increase
only by March after the decline of winter blooms.
However, grazer abundances can definitely play a major
role on the magnitude of those winter blooms, as shown
by the minor winter bloom recorded in 2000 (Fig. 4).
Higher mesozooplankton abundances than other years
and an atypical Noctitula scintillans bloom were indeed
observed in 2000 (data not shown). This top–down
control of winter blooms, already reported in some
coastal areas (Keller et al., 1999; Keller et al., 2001; Oviatt
et al., 2002; Oviatt, 2004), could have important consequences on trophic levels, and more specially on benthicpelagic coupling, by reducing the detrital carbon supply
available for benthic organisms (Townsend and
Cammen, 1988; Oviatt et al., 2002; Oviatt, 2004).
The most important factor affecting the onset of the
productive period in coastal temperate areas is usually
depth-integrated solar radiation as a function of stratification, vertical attenuation coefficient and incident irradiance (Thórdardóttir, 1986). In Arcachon Bay, no
vertical density stratification was observed during the
2005 winter– spring (Fig. 3). In such well-mixed waters,
more influenced by tidal stirring than by freshwater discharges, the mixed layer corresponds to the whole water
column. Consequently, the increase of light availability
in the water column does not depend on the establishment of a persistent density stratification of the water
column as shown in numerous coastal and estuarine
systems (Cloern, 1984; Levasseur et al., 1984; Ingram
et al., 1985; Thórdardóttir, 1986; Pennock and Sharp,
1994; Yin et al., 1996; Labry et al., 2001).
Despite a perpetual well-mixed water column, light
seems to be sufficient to sustain photosynthesis as
early as February as the water column was entirely
euphotic. Two major factors are liable to control the
depth-averaged quantity of light available for phytoplankton: the vertical attenuation coefficient K and
surface irradiance levels (Riley, 1957).
In macrotidal shallow systems poorly influenced by
freshwater inputs such Arcachon Bay, K essentially
depends on cyclic tidal currents and punctual wind
events that provoke sediment re-suspension (Allen et al.,
1980; De Jonge and van Beusekom, 1995). This high
variability of K controlled by short-term fluctuations
and punctual events cannot therefore be the triggering
factor of recurrent winter blooms whose onset is periodically observed by February. The prevailing factor in
this case is obviously a seasonal-fluctuating factor such
1009
JOURNAL OF PLANKTON RESEARCH
j
VOLUME 29
as the incident irradiance level. Anticyclonic weather
conditions (i.e. high incident irradiance) were observed
during the 3 days preceding the onset of the winter
blooms in the EW (Fig. 2). The 3-days cumulated incident irradiance before the onset of the winter bloom
range from 3794 to 2263 J cm22. The minimum value
was observed in 2000 and can also explain the minor
winter bloom observed this year (,2.5 mg L21). On the
contrary, the highest 3-days cumulated incident irradiance (.3000 J cm22) lead to well developed winter
blooms as such observed in 1999, 2001, 2002 and
2003.
The Riley (Riley, 1957) equation allows the calculation of the depth-averaged irradiance (I) received by
phytoplankton in the water column during February –
March (at the onset of winter blooms): I¼(Io—Io
*e2KZ)/KZ where Io is the total surface incident irradiance (in W m – 2), Z is water depth (in m) and K is the
vertical attenuation coefficient (in m21). Using a 3-days
irradiance value of 3000 J cm22 as a threshold for
biomass accumulation, a daily value of Io¼1000 J cm22
day21 (¼116 W m22) can be calculated; K¼0.25 (corresponding to the average of K measured during
February – March 2005 in Arcachon Bay), then
I¼27 W m22. This value is higher than the empirical
critical irradiance suggested by Riley (Riley, 1957) of
0.03 g cal cm – 2 min – 1 (¼20.9 W m – 2) required for
blooming in temperate coastal waters. Inversely, this
empirical value of 20.9 W m – 2 would led to a 3-days
cumulated incident irradiance of 2330 J cm22 with our
conditions, that explains the quasi-absence of winter
bloom in 2000 (coupled with high zooplankton
abundances).
We could conclude that in Arcachon Bay, initiation of
winter blooms seems to be triggered when incident irradiance reaches a threshold value as observed in other
coastal systems characterized by relatively clear waters
(Hitchcock and Smayda, 1977; Båmstedt, 1985;
Townsend et al., 1992; Townsend et al., 1994; Townsend
and Thomas, 2001). Under such conditions, incident
irradiance seems to prevail upon vertical attenuation
coefficient in the initiation processes of winter phytoplankton bloom. The correlation between the biomassspecific primary productivity (P/B) and daily-averaged
incident irradiance observed in 2003 corroborates this
hypothesis. This situation, typical of clear waters, is
different to that of the dilution plume of the Gironde
estuary and other turbid coastal ecosystems affected by
freshwater inputs where the onset of the productive
period is typically associated with an increase of
depth-averaged quantity of light available due to a
decrease of the vertical attenuation coefficient and a
vertical density stratification/gradient induced by
j
NUMBER
11
j
PAGES
999 – 1014
j
2007
freshwater runoff (Thórdardóttir, 1986; Cloern, 1991;
Ragueneau et al., 1996; Labry et al., 2001).
Finally, although the increase of light availability is
one of the main factors controlling the outburst of phytoplankton bloom during winter, water temperature
could also play an important role during this season, by
influencing the P/B (Eppley, 1972; Harrison and Platt,
1980). From 1999 to 2003, winter blooms were generally initiated when temperatures ranged from 9.5 to
11.58C in the EW and from 8.2 to 10.38C in the IW
(Fig. 2). These lowest temperatures characterizing the
IW could explain the delay of the onset of winter
blooms observed between the outer and inner water
masses in 1999 and 2003 (considering that
depth-integrated irradiance is similar in the two water
masses, i.e. same incident irradiance and identical seasonal variations of K). For the years 1999 and 2003,
when winter blooms were initiated in the EW but not
yet in the IW, water temperature were inferior to 88C in
the IW while they were above 98C in the EW,
suggesting that the overtaking of a temperature
threshold of 8 – 98C could be necessary for an increase
of phytoplankton growth. Obviously, this temperature
threshold needs to be clarified and used with some
caution as temperature optima are highly variable and
species specific (Goldman and Ryther, 1976). Moreover,
some diatoms are known to be eurythermal species and
therefore are able to develop in a large range of temperatures. For instance, A. glacialis (that dominated the
2003 winter blooms) are present from 0.8 to 238C in
Narragansett Bay (Karentz and Smayda, 1984). By consequence, this temperature threshold is also considered
as region-dependent.
Trophic consequences of the early
phytoplankton blooms
In Arcachon Bay, a major consequence of the presence
of phytoplankton blooms early in the year was a nutrient
depletion that occurred as early as March–April
(Table III) and led to nutrient limitations of phytoplankton primary production rates by spring (Glé et al., 2007).
The consequences of these precocious nutrient limitations could be similar to those observed in the dilution
plume of the Gironde Estuary, which means the structuring of the planktonic food web tends towards the dominance of small phytoplankton cells (Herbland et al.,
1998) and grazing mainly realized by microzooplankton
(Sautour et al., 2000). The size-class structure of summer
phytoplankton developments appears to be specially
determinant for the success of the development and
recruitment of bivalves larvae as C. gigas which are particularly demanding as regards of food (Robert and
1010
C. GLÉ ET AL.
j
WINTER PHYTOPLANKTON BLOOMS
Trintignac, 1997). Indeed, in Arcachon Bay, low abundances of nanoplankton in summer could limit the food
supply to bivalves larvae and thus could be a cause of
weak settlement as observed some years (D. Maurer,
IFREMER, personal communication).
In shallow coastal ecosystem rich in suspension
feeders as Arcachon Bay, early phytoplankton blooms
could sustain a great pelagic –benthic coupling. Indeed,
in Arcachon Bay, there is typically a mismatch between
the winter– spring diatom bloom and the mesozooplankton abundance peak which occurs by March –
April (data not shown) when water temperatures are
favourable (Castel and Courties, 1982; Vincent, 2002).
In consequence, phytoplankton could not be efficiently
consumed by the zooplankton but instead sinks, providing a large supply of organic matter which serves as a
rich food source for benthic organisms as shown in
Narragansett Bay (Townsend and Cammen, 1988;
Keller et al., 2001; Oviatt, 2004), in the North Sea
(Nielsen and Richardson, 1989) or in Northern Baltic
Sea (Lignell et al., 1993).
Moreover, the massive sedimentation of spring diatom
blooms could also impact the Si cycle, with potential
implications on the summer functioning of the bay.
Indeed, it has been shown recently in the Bay of Brest
that the activity of suspension feeders during early spring
(filtration and subsequent production of quantities of biodeposits) led to temporary retention of biogenic silica
(BSi) in the sediments of the Bay (Ragueneau et al., 2002;
Ragueneau et al., 2005). The subsequent BSi dissolution
during late spring and summer, enhanced by increasing
temperature and elevated bacterial activity, would
provide the necessary dissolved silicon required by
diatoms to maintain their dominance throughout the
productive period (Chauvaud et al., 2000).
CONCLUSION
This study has shown that winter blooms, initiated as
early as February, are a recurrent pattern observed in
Arcachon Bay. In this macrotidal system, the beginning
of the productive period seems to be highly influenced
by the phytoplankton dynamics of the adjacent oceanic
waters. This oceanic influence, by affecting firstly the
external waters of the lagoon, led to an uncoupling of
the biological functioning between the external and
internal waters of the lagoon at the start of the productive period, evidenced by the recurrent lowest magnitude of winter blooms in the IW and by the delayed
onset of the winter bloom observed in the IW.
The essential environmental condition for the onset
of winter blooms in Arcachon Bay seems to be an
increase of light availability. Due to the low turbidity of
these water masses, incident irradiance seems to prevail
upon any particular vertical structure of the water
masses (e.g. stratification, decrease of extinction coefficient) in the initiation process of winter phytoplankton
bloom. However, the influence of temperature on phytoplankton growth during winter should not be underestimated, especially in the cooler internal waters.
As seen in most early-year blooms, winter blooms in
Arcachon Bay are dominated by diatoms that thrive
under the relatively rich nutrient environment.
However, the early nutrient depletion that will encompass the winter bloom collapse by spring could have
inevitable consequences on the structuration of the food
web during spring and summer as shown in the dilution
plume of the Gironde estuary (Herbland et al., 1998;
Sautour et al., 2000). Further studies are therefore
needed to characterize such consequences on nutrient
dynamics and consequently, on the following community and size structure of plankton in Arcachon Bay.
AC K N OW L E D G E M E N T S
We would like to express our deepest thanks to
P. Marraco and P. Lebleu (our sailors). Many thanks are
due to Sophie Dargelos, Damien Devault, Emilie
Hoogland, Yoann Larré, Marie-Claude Lécart, Rija
Samsera, Julie Simounet, Marie-Laure Valvason, Benoı̂t
Gouilleux, Elise Thomas and Cédric Fanchamps for
their valuable sea and laboratory assistance during
these five study years.
Ocean colour data used in this study were produced
by the SeaWiFS Project at Goddard Space Flight
Center. The data were obtained from the Goddard
Earth Sciences Distributed Active Archive Center under
the auspices of the National Aeronautics and Space
Administration.
FUNDING
This investigation was supported for the most part by
the CNRS/INSU (PNEC Chantier Littoral Atlantique
and a Action Thématique Innovante 2001 grant). This
work is UMR CNRS 5805 contribution 1674.
REFERENCES
Allen, G. P., Salamon, J. C., Bassoullet, P. et al. (1980) Effects of tides
on mixing and suspended sediment transport in macrotidal estuaries. Sedimentary Geol., 26, 69–90.
1011
JOURNAL OF PLANKTON RESEARCH
j
VOLUME 29
j
NUMBER
11
j
PAGES
999 – 1014
j
2007
Båmstedt, U. (1985) Spring-bloom dynamics in Kosterfjorden, western
Sweden: variation in phytoplankton production and macrozooplankton characteristics. Sarsia, 70, 69– 82.
Gailhard, I., Gros, P. h., Durbec, J. P. et al. (2002) Variability patterns
of microphytoplankton communities along the French coasts. Mar.
Ecol. Progr. Ser., 242, 39–50.
Beaufort, L. and Heussner, S. (2001) Seasonal dynamics of calcareous
nannoplankton on a West European continental margin: the Bay of
Biscay. Mar. Micropaleontol., 43, 27– 55.
Glé, C., Del Amo, Y., Sautour, B. et al. (2007) Variability of nutrients and
phytoplankton primary production in a shallow macrotidal coastal
ecosystem (Arcachon Bay, France). Estuar. Coast. Shelf Sci, in press.
Beliaeff, B., Gros, P., Belin, C. et al. (2001) ‘Phytoplankton events’ in
French coastal waters during 1987–1997. Oceanol. Acta, 24,
425–433.
Glibert, P. M., Conley, D. J., Fisher, T. R. et al. (1995) Dynamics of the
1990 winter/spring bloom in Chesapeake Bay. Mar. Ecol. Progr. Ser.,
122, 27–43.
Bendschneider, K. and Robinson, R. J. (1952) A new spectrophotometric determination of nitrite in seawater. J. Mar. Res., 2, 87–96.
Gohin, F., Druon, J. N. and Lampert, L. (2002) A five channel chlorophyll concentration algorithm applied to SeaWiFS data processed
by SeaDAS in coastal waters. Int. J. Remote Sens., 23, 1639–1661.
Carruesco, C. (1989) Genèse et évolution de trois lagunes du littoral
atlantique depuis l’Holocène: Oualidia, Moulay Bousselham
(Maroc) et Arcachon (France). PhD Thesis. Université de
Bordeaux1, Bordeaux, unpublished.
Gohin, F., Lampert, L., Guillaud, J. F. et al. (2003) Satellite and in situ
observations of a late winter phytoplankton bloom, in the northern
Bay of Biscay. Cont. Shelf Res., 23, 1117–1141.
Castel, J. and Courties, C. (1982) Composition and differential distribution of zooplankton in Arcachon Bay. J. Plankton Res., 4,
417–433.
Goldman, J. C. and Ryther, J. H. (1976) Temperature-influenced
species competition in mass cultures of marine phytoplankton.
Biotechnol. Bioeng., 18, 1125– 1144.
Chauvaud, L., Jean, J., Ragueneau, O. et al. (2000) Long-term variation of the Bay of Brest ecosystem: benthic-pelagic coupling
revisited. Mar Ecol. Prog. Ser., 200, 35–48.
Guillocheau, N. (1988) Répartition spatio-temporelle du phytoplancton du bassin d’Arcachon. PhD Thesis. Université Aix Marseille II,
Marseille, Unpublished.
Cloern, J. E. (1984) Temporal dynamics and ecological significance of
salinity stratification in an estuary (South San Francisco Bay, USA).
Oceanol. Acta, 7, 137– 141.
Harrison, W. G. and Platt, T. (1980) Variations in assimilation number
of coastal marine phyto-phytoplankton: Effects of environmental
co-variates. J. Plankton Res., 2, 249– 260.
Cloern, J. E. (1991) Annual variations in river flow and primary production in the South San Francisco Bay estuary (USA). In Elliott,
M. and Ducrotoy, J. P. (eds), Estuaries and coasts: spatial and temporal
intercomparisons. Olsen and Olsen, Fredensborg, pp. 91–96.
Harrison, W. G., Head, E. J. H., Horne, E. P. W. et al. (1993) The
western North Atlantic bloom experiment. Deep-Sea Res. Part II, 40,
279 –305.
Cloern, J. E. (1996) Phytoplankton bloom dynamics in coastal ecosystems: a review with some general lessons from sustained investigation of San Francisco Bay, California. Rev. Geophys., 34, 127–168.
Cloern, J. E. (2001) Our evolving conceptual model of the coastal
eutrophication problem. Mar. Ecol. Progr. Ser., 210, 223– 253.
De Jonge, V. N. and Van Beusekom, J. E. (1995) Wind- and
tide-induced resuspension of sediment and microphytobenthos from
tidal flats in the Ems estuary. Limnol. Oceanogr., 40, 766– 778.
Del Amo, Y., Le Pape, O., Tréguer, P. et al. (1997) Impacts of highnitrate freshwater inputs on macrotidal ecosystems. I. Seasonal evolution of nutrient limitation for the diatom-dominated phytoplankton of the Bay of Brest (France). Mar Ecol. Prog. Ser., 161, 213– 224.
D’Elbée, J. and Castel, J. (1991) Zooplankton from the continental
shelf of the southern Bay of Biscay exchange with Arcachon Basin,
France. Ann. Inst. océanogr., 67, 35–48.
Durbin, E. G., Campbell, R. G., Casas, M. C. et al. (2003)
Interannual variation in phytoplankton blooms and zooplankton
productivity and abundance in the Gulf of Maine during winter.
Mar. Ecol. Progr. Ser., 254, 81–100.
Edwards, M., Beaugrand, G., Reid, P. C. et al. (2002) Ocean climate
anomalies and the ecology of the North Sea. Mar. Ecol. Progr. Ser.,
239, 1 –10.
Edwards, M. and Richardson, A. J. (2004) Impact of climate change
on marine pelagic phenology and trophic mismatch. Nature, 430,
881–884.
Herbland, A., Delmas, D., Laborde, P. et al. (1998) Phytoplankton
spring bloom of the Gironde plume waters in the Bay of Biscay:
early phosphorus limitation and food-web consequences. Oceanol.
Acta, 21, 279–291.
Hitchcock, G. L. and Smayda, T. J. (1977) The importance of light in
the initiation of the 1972–1973 winter-spring diatom bloom in
Narragansett Bay. Limnol. Oceanogr., 22, 126– 131.
Howarth, R. W., Billen, G., Swaney, D. et al. (1996) Regional N
budgets and riverine N & P fluxes for the drainages to the North
Atlantic Ocean: Natural and human influences. Biogeochemistry, 35,
75– 139.
Ingram, R. G., Legendre, L., Simard, Y. et al. (1985) Phytoplankton
response to freshwater runoff: the diversion of the Eastmain River,
James Bay. Can. J. Fish. Aquat. Sci., 42, 1216–1221.
JGOFS (1988) Core measurements protocols: report of the core
measurement working group. JGOFS report n86, Joint Global Ocean
Flux, Study SCOR, pp. 1 –40.
Karentz, D. and Smayda, T. J. (1984) Temperature and seasonal
occurrence patterns of 30 dominant phytoplankton species in
Narragansett Bay over a 22-year period (1959– 1980). Mar. Ecol.
Prog. Ser., 18, 277– 293.
Kelly, J. R. and Doering, P. H. (1997) Monitoring and modeling
primary production in coastal waters: Studies in Massachusetts Bay
1992–1994. Mar. Ecol. Progr. Ser., 148, 155– 168.
Eppley, R. W. (1972) Temperature and phytoplankton growth in the
sea. Fish. Bull, 70, 1063–1085.
Keller, A. A., Oviatt, C. A., Walker, H. A. et al. (1999) Predicted
impacts of elevated temperature on the magnitude of the winterspring phytoplankton bloom in temperate coastal waters: A mesocosm study. Limnol. Oceanogr., 44, 344–356.
Fisher, T. R., Harding, J. L. W., Stanley, D. W. et al. (1988)
Phytoplankton, nutrients, and turbidity in the Chesapeake,
Delaware, and Hudson estuaries. Estuar. Coast. Shelf Sci., 27, 61– 93.
Keller, A. A., Taylor, C., Oviatt, C. et al. (2001) Phytoplankton production patterns in Massachusetts Bay and the absence of the 1998
winter-spring bloom. Mar. Biol., 138, 1051– 1062.
1012
C. GLÉ ET AL.
j
WINTER PHYTOPLANKTON BLOOMS
Koroleff, F. (1969) Direct determination of ammonia in natural waters
as indophenol blue. J. Cons. Int. Expl. Mer, 9, 1 –6.
Labry, C., Herbland, A., Delmas, D. et al. (2001) Initiation of winter
phytoplankton blooms within the Gironde plume waters in the Bay
of Biscay. Mar. Ecol. Progr. Ser., 212, 117–130.
Pennock, J. R. and Sharp, J. H. (1994) Temporal alternation between
light-limitation and nutrient-limitation of phytoplankton production
in a coastal plain estuary. Mar. Ecol. Progr. Ser., 111, 275– 288.
Plus, M. and Durand, N. (2004) Le modèle hydrodynamique du
Bassin d’Arcachon. Ifremer/DEL, Arcachon.
Labry, C., Herbland, A. and Delmas, D. (2002) The role of phosphorus on planktonic production of the Gironde plume waters in
the Bay of Biscay. J. Plankton Res., 24, 97– 117.
Plus, M., Maurer, D., Stanisiere, J.-Y. et al. (2006) Caractérisation des
composantes hydrodynamiques d’une lagune mésotidale, le Bassin
d’Arcachon, Rapport Ifremer RST/LER/AR/06.007. 54.
Lampert, L. (2001) Dynamique saisonnière et variabilité pigmentaire
des populations phytoplanctoniques dans l’Atlantique Nord (Golfe
de Gascogne). PhD Thesis. Université de Bretagne Occidentale,
Brest, Unpublished.
Pratt, D. M. (1965) The winter-spring diatom flowering in
Narragansett Bay. Limnol. Oceanogr., 10, 173– 184.
Levasseur, M., Therriault, J. C. and Legendre, L. (1984) Hierarchical
control of phytoplankton succession by physical factors. Mar. Ecol.
Progr. Ser., 19, 211– 222.
Lignell, R., Heiskanen, A. S., Kuosa, H. et al. (1993) Fate of a phytoplankton spring bloom: sedimentation and carbon flow in the planktonic
food web in the northern Baltic. Mar. Ecol. Progr. Ser., 94, 239–252.
Lucas, L. V., Koseff, J. R., Monismith, S. G. et al. (1999) Processes governing phytoplankton blooms in estuaries. II: The role of horizontal
transport. Mar. Ecol. Progr. Ser., 187, 17–30.
Lund, J. W. G., Kipling, C. and Le Cren, E. D. (1958) The inverted
microscope method of estimating algal numbers and the statistical
basis of estimations by counting. Hydrobiologia, 11, 143 –170.
Lunven, M., Guillaud, J. F., Youénou, A. et al. (2005) Nutrient and
phytoplankton distribution in the Loire River plume (Bay of Biscay,
France) resolved by a new Fine Scale Sampler. Estuar. Coast. Shelf
Sci., 65, 94– 108.
Manaud, F., Bouchet, J. M., Deltreil, J. P. et al. (1997) Etude intégrée
du bassin d’Arcachon, Tome 1: Physique. Ifremer/DEL, Arcachon.
Margalef, R. (1958) Temporal succession and spatial heterogeneity in
phytoplankton. In Buzzati-Traverso, A. A. (ed.), Perspectives in Marine
Biology. University of California Press, Berkeley, pp. 323– 349.
Martin, J. H. (1970) Phytoplankton-zooplankton relationships in
Narragansett Bay. The seasonal importance of grazing. Limnol.
Oceanogr., 15, 413–418.
Maurer, D., Auby, I., Masson, N. et al. (2003) Etude de la reproduction
de l’huı̂tre creuse dans le Bassin d’Arcachon - Année 2002. Ifremer/
DEL, Arcachon.
Moutin, T., Raimbault, P. and Poggiale, J. C. (1999) Primary production in surface waters of the western Mediterranean sea.
Calculation of daily production. CR Acad. Sci. III Vie, 322, 651– 659.
Mullin, J. B. and Riley, J. P. (1955) The colorimetric determination of
silicate with special reference to sea and natural waters. Anal. Chim.
Acta, 12, 162– 176.
Murphy, J. and Riley, J. P. (1962) A modified single solution method
for the determination of phosphate in natural waters. Anal. Chim.
Acta, 27, 31–36.
Nielsen, T. G. and Richardson, K. (1989) Food chain structure of the
North Sea plankton communities: seasonal variations of the role of
the microbial loop. Mar. Ecol. Progr. Ser., 56, 75– 87.
Oviatt, C., Keller, A. and Reed, L. (2002) Annual Primary Production
in Narragansett Bay with no Bay-Wide Winter-Spring
Phytoplankton Bloom. Estuar. Coast. Shelf Sci., 54, 1013–1026.
Oviatt, C. A. (2004) The changing ecology of temperate coastal
waters during a warming trend. Estuaries, 27, 895–904.
Ragueneau, O., Queguiner, B. and Treguer, P. (1996) Contrast in biological responses to tidally-induced vertical mixing for two macrotidal ecosystems of Western Europe. Estuar. Coast. Shelf Sci., 42,
645–665.
Ragueneau, O., Chauvaud, L., Leynaert, A. et al. (2002) Direct evidence of a biologically active coastal silicate pump: ecological implications. Limnol. Oceanogr., 47, 1849– 1854.
Ragueneau, O., Chauvaud, L., Moriceau, B. et al. (2005)
Biodeposition by an invasive suspension feeder impacts the biogeochemical cycle of Si in a coastal ecosystem (Bay of Brest, France).
Biogeochemistry, 75, 19–41.
Riley, G. A. (1957) Phytoplankton of the North Central Sargasso Sea.
Limnol. Oceanogr., 2, 252– 270.
Robert, R. and Trintignac, P. (1997) Substitues for live microalagae in
mariculture: a review. Aquat. Living Resour., 10, 315–327.
Salomon, J. C., Breton, M. and Guegueniat, P. (1995) A 2D long term
advection-dispersion model for the Channel and Southern North Sea.
Special Issue MAST 52, part B and C. J. Marine Syst., 6, 495–528.
Sautour, B., Artigas, F. L., Delmas, D. et al. (2000) Grazing impact of
micro- and mesozooplankton during a spring situation in coastal
waters off the Gironde estuary. J. Plankton Res., 22, 531– 552.
Steeman Nielsen, R. (1952) The use of radioactive carbon (14C) for
measuring organic production in the sea. J. Cons. Int. Expl. Mer., 18,
117 –140.
Struski, C. and Bacher, C. (2006) Preliminary estimate of primary production by phytoplankton in Marennes-Oleron Bay, France. Estuar.
Coast. Shelf Sci., 66, 323–334.
Thórdardóttir, T. (1986) Timing and duration of spring blooming
south and southwest of Ireland. In Skrelet, S. (ed.). The role of freshwater outflow in coastal marine ecosystems. Springer, Berlin, pp. 345–360.
Townsend, D. W. and Cammen, L. M. (1988) Potential importance of
the timing of spring plankton blooms to benthic-pelagic coupling
and recruitment of juvenile demersal fishes. Biol. Oceanogr., 5,
215 –229.
Townsend, D. W., Keller, M. D., Sieracki, M. E. et al. (1992) Spring
phytoplankton blooms in the absence of vertical water column stratification. Nature, 360, 59–62.
Townsend, D. W., Cammen, L. M., Holligan, P. M. et al. (1994)
Causes and consequences of variability in the timing of spring phytoplankton blooms. Deep-Sea Res. Part I, 41, 747 –765.
Townsend, D. W. and Thomas, A. C. (2001) Winter-spring transition
of phytoplankton chlorophyll and inorganic nutrients on Georges
Bank. Deep-Sea Res. Part II, 48, 199–214.
Utermöhl, H. (1958) Zur Vervollkommnung der quantitative
phytoplankton-methodik. Mitt. Int. Verein. Theor. Angew. Limnol., 9,
1 –38.
1013
JOURNAL OF PLANKTON RESEARCH
j
VOLUME 29
Vincent, D. (2002) Dynamique et nutrition du zooplancton en milieu
lagunaire macrotidal (Bassin d’Arcachon): flux de carbone et d’azote
associés. Conséquences sur le pool nutritifs et les organismes. PhD
Thesis. Université de la Méditerranée, Marseille, Unpublished.
Wafar, M. V. M., Le Corre, P. and Birrien, J. L. (1983) Nutrients and
primary production in permanently well-mixed temperate coastal
waters. Estuar. Coast. Shelf Sci., 17, 431 –446.
Waniek, J. J. (2003) The role of physical forcing in initiation of spring
blooms in the northeast Atlantic. J. Marine Syst., 39, 57–82.
j
NUMBER
11
j
PAGES
999 – 1014
j
2007
Winder, M. and Schindler, D. E. (2004) Climate change uncouples
trophic interactions in an aquatic ecosystem. Ecology, 85,
2100–2106.
Yentsch, C. S. and Menzel, D. W. (1963) A method for the determination of phytoplankton chlorophyll and pheophytin by fluorescence. Deep-Sea Res., 10, 221– 231.
Yin, K., Harrison, P. J., Goldblatt, R. H. et al. (1996) Spring bloom in
the central Strait of Georgia: interactions of river discharge, winds
and grazing. Mar. Ecol. Progr. Ser., 138, 255–263.
1014