Journal of Plankton Research Vol.20 no.2 pp.371-381, 1998
SHORT COMMUNICATION
Comparisons of primary production values estimated from
different incubation times in a coastal sea
F.Lizon and Y.Lagadeuc
Station Marine, Universite des Sciences et Technologies de Lille, CNRS-URA
1363, BP 80, 62930 Wimereux, France
Abstract. In shallow coastal systems dominated by vertical mixing, phytoplankton cells experience
light variations due to vertical excursions. Therefore, it would be unusual for phytoplankton to experience constant irradiance during 4 or 24 h, the standard incubation times used to estimate daily primary
production rates. The aim of this work was to determine conditions under which bias could occur in
long-term simulated in situ incubations (SIS). Values of primary production estimated from 4 and 24 h
SIS incubations have been compared with estimates of primary production based on photosynthetic
parameters, which were determined on short incubation times (40 min). Sampling was conducted
under different conditions of vertical mixing. It appears that daily primary production rates computed
from 24 h incubation times are the lowest at each sampling station, whereas differences between daily
production rates estimated from 4 h and 40 min incubation times depend on the sampling stations.
Vertical mixing and available light intensity could control differences between the computed daily
production rates on 4 h and 40 min incubation times. In fact, under conditions of non-Limiting light
intensity for photosynthesis, photoadaptation processes could occur in long-term SIS incubations,
which do not take into account vertical mixing, and enhance primary production estimates.
In recent years, evidence has been accumulated that, for several reasons, the deviations between true water column primary production and the measured bottle
rates are even more pronounced as samples are confined for a long time (Harris,
1980; Goldman etal, 1981; Goldman and Dennett, 1984; Gallegos and Platt, 1985;
Mallin and Paerl, 1992). In fact, in photosynthesis measurements, samples are
generally exposed under natural or artificial light for times varying from 2 to 4 h.
Some protocols (Lohrenz et ai, 1992) also recommend simulated in situ (SIS)
incubations of 24 h in order to estimate daily rates of primary production.
However, events such as water column mixing, attributed to tides and wind, can
take place in the field within 4 h or 24 h, and can significantly affect phytoplankton
productivity in aquatic systems (Eppley and Sharp, 1975; Harris and Piccinin,
1977; Harris, 1978,1980,1984; Marra, 1978; Harris et ai, 1989; Mallin and Paerl,
1992), making representations of bottle incubations questionable.
It is now recognized that photosynthesis is mediated by physiological adaptations of phytoplankton, according to the light-shade adaptation theory
(Falkowski, 1983,1981). Therefore, phytoplankton responses to vertical mixing,
which moves cells up and down in the water column, will depend primarily on the
intensity of mixing. When mixing is moderate, light conditions change at a slower
rate than the physiological adaptation time of phytoplankton. Cells, then, can
continuously adjust their activities to the new conditions (Vincent, 1980;
Falkowski, 1983; Demers et al, 1986). However, if vertical mixing is high and continuous, phytoplankton respond to the mean light condition in the mixed layer.
© Oxford University Press
371
F.Lizon and Y.Lagadenc
Furthermore, testing of the kinetics of algal photoadaptation for laboratory or
field studies has shown that phytoplankton effect significant photoadaptive
responses with a characteristic time much shorter than 4 h (Gallegos et al, 1983;
Lewis and Smith, 1983; Lewis et al., 1984; Cullen and Lewis, 1988; Lizon and
Lagadeuc, 1995). In fact, it would be somewhat unusual for phytoplankton to
experience constant irradiance during 2 or 4 h in the natural environment (Lewis
and Smith, 1983).
A number of workers have attempted to simulate vertical motion in incubation
experiments (Jewson and Wood, 1975; Marra, 1978; Gallegos and Platt, 1982;
Yoder and Bishop, 1985), but results of the effects on primary production estimates have been equivocal. Some of these studies showed a stimulation of
primary production with mixing, while others found that mixing had little effect,
or reduced productivity. Recently, Mallin and Paerl (1992) concluded that static
incubations may significantly underestimate phytoplankton production in
shallow, well-mixed aquatic systems. However, their study was conducted in a
very shallow (5 m depth) and turbid (Kd = 1.47 m"1) system.
The objective of our study was to estimate primary production with three
different incubation times, in a typical shallow coastal system (30-50 m depth)
and in different conditions of vertical mixing. We measured primary production
according to the photosynthetron technique of Babin et al. (1994) with 40 min
incubation time, and the conventional SIS method in which samples were incubated for 4 and 24 h. We did not use a vertical mixing simulator as in the previously mentioned studies. However, the advantage of the P-I curve and short-term
incubation methods, recommended by many investigators (Harrison et al., 1985;
Tilzer et al., 1993) in order to estimate in situ daily production rates, is that photosynthetic characteristic measurements from short-term incubations reflect the
physiological state of cells at the time of collection (Lewis and Smith, 1983). We
can hypothesize that the three methods would lead to different primary production rates according to the environmental conditions encountered, especially light
intensity and vertical mixing.
Sampling was conducted from 18 to 29 September 1994, in the eastern English
Channel. The tidal range in this system is one of the highest in the world (ranging
from 3 to 9 m). Tides generate a residual circulation parallel to the coast, drifting
nearshore coastal waters from the English Channel to the North Sea. Coastal
waters are influenced by freshwater run-off from the Seine estuary to the Strait
of Dover, and then separated from offshore waters by a tide-controlled frontal
area (Brylinski and Lagadeuc, 1990; Figure 1).
The three sampling stations (Figure 1) were chosen because their different
physical and hydrological properties are representative of the range found within
the eastern English Channel. Station 4 was located in the Bay of Seine where
freshwater inputs from the Seine river can induce stratifications of the water
column. Tidal currents at this station are lower (Salomon and Breton, 1993) than
at Stations 5 and 6, which are located near the Strait of Dover, in coastal and offshore waters, respectively.
Each station was occupied during 3 days. On the first 2 days, sampling was conducted at sunrise only, while on the third day it was conducted at sunrise, midday
372
Primary production values and incubation times
re
Fig. 1. The study area showing the three sampling stations, and the inshore and onshore waters of the
eastern English Channel.
and sunset, at a fixed station. Water samples were collected with Niskin bottles
from four depths selected to be within a range of 1-80% of surface incident irradiance. SIS primary production on 4 h incubation times, P-I relationships and
chlorophyll (Chi) a concentrations were then determined for each sampling. In
contrast, SIS incubations on 24 h started only at sunrise. A Sea-Bird 25 CTD
probe was used to measure temperature, salinity and photosynthetically active
radiation (PAR; 400-700 nm; QSP-200, Biospherical Instruments) during each
sampling period. Hourly measurements of surface irradiance (PAR) were made
using a Biospherical Instruments QSL-100.
Chlorophyll a analyses were performed after nitration of samples on Whatman
GF/F glass fibre filters and after 24 h extraction in 90% acetone at 5°C using the
spectrophotometric method. Primary production was estimated by the 14C
373
F.lizon and Y.Lagadeuc
incorporation method (Steeman Nielsen, 1952). For each sampling, P-I experiments (12 subsamples) were conducted in a radial 'photosynthetron' (Babin et al.,
1994) equipped with a halogen dysprosium lamp (Osram, HQI-T 250 W/D) that
provided a daylight spectrum from -850 oE m~2 s~2 in front of the first subsample to -10 uE m~2 s~2 at the last one. All subsamples (50 ml) were inoculated with
74 kBq NaH 14 CO 3 and incubated for 40 min (Lizon and Lagadeuc, 1995). A standard system of four deck boxes attenuated with different neutral-density nickel
screens (simulating the light level of sampling depths) was designed for SIS incubations under natural sunlight conditions (Harrison et al., 1982, 1985; Videau,
1987; Videau et al., 1994). SIS experiments were conducted in 125 ml bottles
injected with 148 and 444 kBq NaH14CO3 for 4 and 24 h incubation times, respectively. Samples were previously filtered in order to eliminate mesozooplankton
grazers. After incubation, samples were filtered on glass fibre filters (GF/F) which
were rinsed (three times) with filtered seawater (Harrison et al., 1985) before
being dropped in vials containing the scintillation cocktail. The activity was
measured later on a liquid scintillation counter (L.K.B. Wallac 12-14 Rackbeta),
the efficiency of which was determined by an external standard channels ratio
method.
Primary production was calculated according to Parsons et al. (1984). The
photosynthetic parameters P B (light-saturated uptake rate), a B (photosynthetic
efficiency at low irradiance) and 7k (light saturation parameter), whose resolution
is dependent on the number of irradiance, were derived from the equation of
optimal curve adaptation as presented by Platt et al. (1980). The superscript 'B'
denotes that these parameters have been normalized to Chi a concentrations. The
ratios of the average irradiance in the water column [7avg = 70 (1 - exp(-Kdz))/Kdz;
where z is water column depth] to 7k (Jellison and Melack, 1993) were also calculated to estimate whether cells were light limited in their natural environment.
The Kruskal-Wallis test (non-parametric analysis of variance) was used to
compare values of photosynthetic parameters, 7avg/7k ratios and Chi a concentrations between each sampling depth at each station.
In order to calculate depth-integrated primary production for each profile of
the third day, the water column was divided into four layers for which the exponential model of Platt et al. (1980) was adjusted to photosynthetic parameters
measured and to the decreasing irradiance (Harrison et al., 1985). In the same
way, each day was divided into three periods for which the measured light field
was adjusted to P-I parameters. Depth-integrated production was then obtained
by integration of linearly interpolated values from the sea surface to the bottom
of the euphotic layer (Legendre et al., 1993). Daily primary production was then
computed by adding together the time- and depth-integrated rates (Vandevelde
etal, 1989). In the same way, from SIS measurements on both 4 h (using the three
daily measurements) and 24 h incubation times, depth-integrated and daily production rates were also calculated.
The results of this study show that daily primary production rates computed
from 24 h incubation times were, as expected, the lowest at each station
(Figure 2). Such results are consistent with what the 14C technique measures. In
fact, net or gross primary production measurements depend on the incubation
374
Primary production values and incubation times
900
A
•
Met. 1
D
S3 Met. 2
O
450
225
a
Bel
-1r
MI
H
675
CO
Met. 3
1
.B
i
40
•
(Met2-Met1)/Met1
EB (Met3-Met1)/Met1
•
(Met3-Met2)/Met2
20
-60
2
Station
Fig. 2. (A) Daily primary production rates at the three stations, computed according to the three
methods: the P-I parameters determined on 40 min incubation times (1); SIS procedure on 4 h (2)
and 24 h (3) incubation times. (B) Per cent differences between methods 2 and 1,3 and 1 and 3 and
2.
time (Jackson, 1993; Langdon, 1993; Williams, 1993). As the total loss rates
increase with incubation times, long-term 14C incubations (as 24 h incubation
times) approximate net production. On the contrary, short incubation times minimize the loss of labelled organic materials and, therefore, approximate gross production rates. The typical rates of loss owing to excretion and respiration of
phytoplankton can be -10 and 60% of gross primary production rates, respectively (Lancelot and Mathot, 1985; Langdon, 1993). These substantial losses could
explain the lower level of production estimated with the SIS technique on 24 h
incubation times, as also reported by other studies (Eppley et ai, 1973; Eppley
and Sharp, 1975; Harrison et al, 1985). Furthermore, it can be noted that losses
of tracer, which can also be due to microzooplankton grazing (mesozooplankton
being eliminated by filtration), must be low during the sampling period. In September, the English Channel is dominated by large cells (Hedin-Bougard, 1980;
Martin-Jezequel, 1983), consistent with the concept of population succession of
Margalef (1978).
375
F.lizon and Y.Lagadeuc
However, differences between daily primary production rates estimated from
4 h and 40 min incubation times depended on the sampling stations (Figure 2A
and B). At Station 6, the daily primary production rate estimated from 4 h incubation times was lower (-20%) than that calculated from P-I parameters determined on 40 min incubation times. At Station 5, daily production estimated from
the SIS technique on 4 h incubation times exceeded by ~20% the daily rate calculated from P-I parameters. At Station 4, daily production estimated from the two
previously mentioned incubation times displayed nearly the same rates (Figure
1000
SL 6
SL 5
SL 4
~800
'a
"g 600
ui
5 400
a.
a 200
7
9.6
12.2
14.8
17.4
20
7
9.6
12.2
,B
14.8
17.4
20 7
9.6
12.2
14.8
17.4
20
Time (h)
St 6\
I
1
£15
a
Q20
25
30
25.55
•
25.65
25.7525.1
25.2
25.3
Density (ot)
25.424.6
24.7
0.25 0
50
24.8
24.9
25
0
0
0.05
0.1
0.15
0.2
100
150
200
250
Fig. 3. Time series of (A) photosyntetically active radiation (PAR) of the third sampling day, in subsurface waters at the three stations, and (B) density profiles measured the first day (
), the second
day (—) and the third day at sunrise ( ), midday ( ) and sunset (
) of sampling for each of
the three sites. (C) Typical vertical profiles of P°m (mg C m^ Chi a h"1), otB [mg C ing-1 Chi a h~'
(uE m-2 s"1)-1] and / k (uE nr 2 s~') obtained at midday at Station 6 (•), Station 5 (O) and Station 4
(•)•
376
Primary production values and incubation tunes
2A). The estimated rate on 4 h incubation times showed a very weak underestimation of 5% (Figure 2B). It appears that differences between daily rates estimated from 4 h and 40 min incubation times are consistent with earlier
considerations about net or gross primary production estimations, at Station 6
only. In order to explain such results, ecological considerations related to light,
vertical mixing conditions and photoadaptation of phytoplankton can be considered.
First, available light for photosynthesis was different between the three sampling periods (Figure 3A). Light intensity was in fact the highest at Station 4, the
lowest at Station 6 and intermediate at Station 5. Secondly, the stability of the
water columns was different between Stations 5-6 and Station 4. The very high
tidal ranges at Stations 5 and 6 (6.6 and 7.5 m, respectively) indicate that tidal
forces were of great importance during the sampling periods at these two stations,
in contrast to Station 4 (3.8 m) located in the Bay of Seine. There, the water
column was also characterized by more or less pronounced stratifications, as
shown by density profiles (Figure 3B). Thirdly, photosynthetic parameters displayed different vertical structures between Stations 5-6 and Station 4 (Figure
3C). At Stations 5 and 6, photosynthetic properties of surface and depth populations were nearly the same. On the contrary, at Station 4, photosynthetic parameters displayed pronounced vertical gradients, consistent with weak vertical
mixing intensity reported at this station, and with the iight-shade' adaptation
theory of phytoplankton to a vertical gradient of light (Falkowski and Owens,
1980). P%i and 7k indeed show significantly different means between the four
sampling depths, in Kruskal-Wallis analyses (Table I). Furthermore, values of the
vertical averaged / avg /4 ratios (/avg/Ik) indicate that light intensity was not limiting for photosynthesis at Stations 5 (0.85) and 4 (0.99), in contrast to Station 6
(0.50). In fact, at Stations 5 and 4, values of / avg /I k ratios are close to the standard
value of one, which is used to estimate whether photosynthesis was light limited
( W 7 k < 2 ) o r n o t ( W 7 * > 1) (Jellison and Melack, 1993).
Based on the previous ecological considerations, it can be suggested that at
Stations 5 and 4, high daily production rates obtained from 4 h incubation times,
compared to 40 min incubation times, could be due to pronounced photoadaptation
Table I. Results of the Kruskal-Wallis (K-W) analysis between each sampling depth of each station,
for each photosynthetic parameter and chlorophyll a concentration. P is the probability of error if
significant differences are accepted*
z>B
* m
aB
Chi a
K-W
P
K-W
P
K-W
P
K-W
P
K-W
P
Station 4
Station 5
Station 6
8.692*
0.033
5390
0.145
8.122*
0.040
0.864
0.834
1.739
0.398
5.615
0.154
0.282
0.963
5.820
0.097
2.711
0.438
0.256
0.919
2.282
0.515
1.461
0.691
1.932
0.412
2.692
0.441
0.312
0.951
377
F.lizon and Y.Lagadeuc
processes occurring in incubation bottles. At Station 5, this is consistent with the
non-limiting irradiance conditions, and the non-photoadapted state of in situ phytoplankton deduced from the vertical profiles of P-I parameters. The development
of photoadaptation processes in incubation bottles is also supported at Station 5 by
the absence of a correlation between production values estimated from P-I parameters (integrated over 4 h on the measured light field) and SIS incubations on 4
h (Figure 4A), whereas their per cent differences are highly correlated with integrated irradiance values (on 4 h) (Figure 4B). Incident light would be responsible
for the differences between primary production values estimated from the two
previous methods. Therefore, pronounced photoadaptation of phytoplankton
occurring in incubation bottles, but not in the water column at Station 5, could
explain why the daily primary production rate estimated from 4 h incubation times
was greater than the daily rate estimated from 40 min incubation times. As for
Station 4, photoadaptation processes occurring in incubation bottles, but also in the
water column, could explain the low difference between daily production rates
estimated from 4 h and 40 min incubation times. This is consistent with non-limiting light for photosynthesis noted at Station 4, and with the significant correlation
found between SIS and P-I calculated production values on 4 h (Figure 4A),
whereas their per cent differences were not correlated with integrated irradiance
values (Figure 4B).
With reference to our hypothesis, we can therefore conclude that vertical
mixing events and available light intensities could control differences between the
daily primary production rates estimated from short- and long-term incubations.
45
A
220
SL5
165
30
110
55
15
r = 0.339
p>0.05
E
si
r = 0.986
p< 0.001
H
St. 4
CU
1
h
—I
1—
St. 4
•
a. 30
55
15
n
1
-5
165
8
I
5
110
55
r = 0.569
p < 0.05
0
20
4 0 6 0 8 0
r = 0.414 p>0.05
100 0 2 0 0
Calculated P. P. (mgC.m-3.4h-1)
4 0 0 6 0 0 8 0 0
-5
-60
4 h integrated Irr. (/* Em- 2 .4h-')
Fig. 4. (A) Relationships between primary production values computed from P-l parameters integrated over 4 h on the measured light field, and SIS incubations on 4 h incubation times, for Stations
5 and 4. (B) Relationships between integrated irradiance over 4 h and the per cent differences
between P-I computed and SIS primary production estimates, for Stations 5 and 4. n = 12; r = Spearman correlation coefficients.
378
Primary production values and incubation times
In fact, under conditions of non-limiting irradiance for photosynthesis, photoadaptation occurring in long-term SIS incubations which do not take into account
light variations due to vertical excursions in the water column would enhance
primary production estimates. However, it would be premature to generalize
from our data set, as for the increase of primary production in SIS incubations.
In fact, some studies have found, under some conditions, that static SIS incubations could also underestimate primary production rates because of photoinhibition processes occurring under high light intensities (Harris, 1978, 1980, 1984;
Marra, 1978,1980). Nevertheless, our results are consistent with the recent work
done by Barkman and Woods (1996). They have shown by a simulation model
that static incubation measurements could overestimate phytoplankton production rates by up to 40% in continental shelf regions where vertical mixing due to
tidal flows is high.
However, it can be recommended to use short incubation times in order to estimate primary production measurements in a perturbed hydrodynamic system.
Furthermore, because light is changing on a daily time scale, primary production
estimations on short-term incubations must be conducted several times during
the day, especially when interactions between periodic vertical mixing events and
photoadaptation of phytoplankton occur (Lizon, 1997).
Acknowledgements
The authors thank S.L'helguen for the on-deck incubators, P.Sangiardi and the
'Noroit' crew for their assistance during the cruise. They are grateful to J.L.Sardin
for a revision of the English of this manuscript. The research support was provided by the PNOC (Programme National d'Oc^anographie Cotiere).
References
Babin.M., Morel,A. and GagnonJR. (1994) An incubator designed for extensive and sensitive
measurements of phytoplankton photosynthetic parameters. LimnoL Oceanogr., 39,694-702.
Barkmann.W. and Woods J.D. (1996) On using a Lagrangian model to calibrate primary production
determined from in vitro incubation measurements. /. Plankton Res., 17, 767-787. .
BrylinskiJ.M. and Lagadeuc.Y. (1990) L'interface eaux cdtieres/eaux du large dans le Pas-de-Calais
(Cote franc.aise): une zone frontale. C. R. Acad. Sci. Paris, 311,535-540.
CullenJJ. and Lewis,M.R. (1988) The kinetics of algal photoadaptation in the context of vertical
mixing. /. Plankton Res., 10,1039-1063.
Demers.S., LegendreJL and TherriaultJ.C. (1986) Phytoplankton responses to vertical tidal mixing.
In Bowmanjvl., Yentsch.C.M. and Peterson.W.T. (eds), Lecture Notes on Coastal and Estuarine
Studies. Springer-Verlag, Berlin, Vol. 17, pp. 1-40.
Eppley,R.W. and SharpJ.H. (1975) Photosynthetic measurements in the central North Pacific: the
dark loss of carbon in 24 h incubations. LimnoL Oceanogr., 20, 981-987.
Eppley,R.W., Renger, E.H., VenrickJE.L. and Mullin,M.M. (1973) A study of phytoplankton
dynamics and nutrient cycling in the central gyre of the North Pacific Ocean. LimnoL Oceanogr.,
18, 534-551.
Falkowski,P.G. (1981) Light-shade adaptation and assimilation numbers. / Plankton Res., 3,203-216.
Falkowski,P.G. (1983) light-shade adaptation and vertical mixing of marine phytoplankton: a
comparative field study. J. Mar. Res., 41,215-237.
Falkowski,P.G. and Owens.T.G. (1980) Light-shade adaptation: two strategies in marine phytoplankton. Plant Physiol., 66, 592-595.
Gallegos.C.L. and Platt.T. (1982) Phytoplankton production and water motion in surface mixed layer.
Deep-Sea Res., 29,65-76.
379
F.Iizon and YXagadeuc
Gallegos.GL. and Platt.T. (1985) Vertical advection of phytoplankton and productivity estimates: a
dimensional analysis. Mar. EcoL Prog. Ser., 26,125-134.
Gallegos.CL., Platt.T., Harrison,W.G. and IrwinJB. (1983) Photosynthetic parameters of artic marine
phytoplankton: Vertical variations and time scales of adaptation. LimnoL Oceanogr., 28, 698-708.
Goldman J.C. and Dennet,M.R. (1984) Effect of photoinhibition during bottle incubations on the
measurement of seasonal primary production in a shallow coastal water. Mar. EcoL Prog. Ser., 15,
169-180.
GoldmanJ.G, Taylor.C.D. and Glibert,P.M. (1981) Nonlinear time-course uptake of carbon and
ammonium by marine phytoplankton. Mar. EcoL Prog. Ser., 6,137-148.
Harris.G.P. (1978) Photosynthesis, productivity and growth: the physiological ecology of phytoplankton. Arch. HydrobioL Beih. Ergebn. Limnol., 10,1-171.
Harris.G.P. (1980) The relationship between chlorophyll afluorescence,diffuse attenuation changes
and photosynthesis in natural phytoplankton populations. /. Plankton Res., 2,109-127.
Harris,G.P. and Puccinin3-B. (1977) Photosynthesis by natural phytoplankton populations. Arch.
HydrobioL, 80, 405-457.
Harris.G.P. (1984) Phytoplankton productivity and growth measurements: past, present and future.
/. Plankton Res., 6, 219-237.
Harris,G.P., Griffiths.F.B. and ThomasJD.P. (1989) Light and dark uptake and loss of 14 C: methodological problems with productivity measurements in oceanic waters. Hydrobiologia, 173,95-105.
Harrison.W.G., Platt.T. and Irwin,B. (1982) Primary production and nutrient assimilation by natural
phytoplankton populations of the eastern Canadian Arctic. Can. J. Fish. Aquat. Scu, 39,335-345.
Harrison,W.G., Platt.T. and Lewis.M.R. (1985) The utility of light saturation models for estimating
marine primary productivity in the field: a comparison with conventional 'simulated' in situ
methods. Can. J. Fish. Aquat. Sci., 42,864-872.
Hedin-Bougard,M. (1980) Hydrobiologie littorale: phytoplancton. PhD Thesis, University of Sciences
and Technology of Lille, Lille, France.
Jackson,G.A. (1993) The importance of the DOC pool for primary production estimates. ICES Mar.
Sci. Symp., 197,141-148.
JellisonJR. and MelackJ.M. (1993) Algal photosynthetic activity and its response to meromixis in
hypersaline Mono Lake, California. LimnoL Oceanogr., 38,818-837.
Jewson J>.H. and Wood,R.B. (1975) Some effects on integral photosynthesis of artificial circulation
of phytoplankton through light gradients. Verh. Int. Ver. Limnol., 19,1037-1044.
Lancelot.C. and Mathot.S. (1985) Biochemical fractionation of primary production by phytoplankton
in Belgian coastal waters during short- and long-term incubations with 14C-bicarbonate. Mar. Biol.,
86, 219-226.
Langdon.C. (1993) The significance of respiration in production measurements based on oxygen.
ICES Mar. ScL Symp., 197,69-78.
Legendre,L., Gosselinjvl., Hirche,H.J., Kattner.G. and Rosenberg.G. (1993) Environmental control
and potential fate of size-fractionated phytoplankton production in the Greenland Sea (75°N). Mar.
EcoL Prog. Ser., 98,297-313.
Lewis,M.R. and SmithJ.C. (1983) A small volume, short incubation time method for measurement
of photosynthesis as a function of incident irradiance. Mar. EcoL Prog. Ser., 13, 99-102.
Lewis,M.R., CullenJJ. and Platt.T. (1984) Relationships between vertical mixing and photoadaptation of phytoplankton: similarity criteria. Mar. EcoL Prog. Ser., 15,141-149.
Lizon,F. (1997) Photoadaptation et Evaluation de la production photosynthe'tique du phytoplancton
en relation avec les caract£ristiques hydrodynamiques de la Manche Orientale. Thesis, Paris VI
University.
Lizon,F. and Lagadeuc.Y. (1995) Echelles temporelles et production primaire: considerations
m^thodologiques. /. Rech. Oceano., 20, 84-88.
Lohrenz,S.E., WiesenburgJXA., Rein.GR., Araone,R.A., Taylor.C.D., Knauer.G.A. and KnapA-H.
(1992) A comparison of in situ and simulated in situ methods for estimating oceanic primary production. /. Plankton Res., 14,201-221.
MaUin,M.A. and Paerl jl.W. (1992) Effects of variable irradiance on phytoplankton productivity in
shallow estuaries. LimnoL Oceanogr., 37,54-62.
MargalefJL (1978) Life-forms of phytoplankton as survival alternatives in an unstable environment.
OceanoL Acta, 1,493-509.
MarraJ. (1978) Effect of short-term variations in light intensity on photosynthesis of a marine phytoplankter: a laboratory simulation study. Mar. Biol., 46,191-202.
MarraJ. (1980) Vertical mixing and primary production. In Falkowski,P.G. (ed.), Primary Productivity in the Sea. Plenum Press, New York, pp. 121-137.
380
Primary production values and incubation times
Martin-Jezequel.V. (1983) Facteurs hydrologiques et phytoplancton en Baie de Morlaix (Manche
Occidentale). Hydrobiologia, 102,131-143.
Parsons.T.R., Takahashi,M. and Hargrave3- (1984) Biological Oceanographic Processes, 3rd edn.
Pergamon Press, 330 pp.
Platt.T., Gallegos.C.L. and Harrison.W.G. (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res., 38, 687-701.
SalomonJ.C. and Breton,M. (1993) An atlas of long-term currents in the Channel. OceanoL Acta, 16,
439-448.
Steemann Nielsen^. (1952) The use of radio-active carbon (14C) for measuring organic production
in the sea. J. Cons. Int. Explor. Mer, 18,117-140.
Tilzer,M.M., Hase.C. and ConredJ. (1993) Estimation of in situ primary production from parameters
of the photosynthesis-light curve obtained in laboratory incubators. ICES Mar. ScL Symp., 197,
181-195.
Vandevelde.T., Legendre,L., Demers.S. and TherriaultJ.C. (1989) Circadian variations in photosynthetic assimilation and estimation of daily production. Mar. Biol., 100,525-531.
Videau.C. (1987) Primary production and physiological state of phytoplankton at the Ushant tidal
front (west coast of Brittany, France). Mar. Ecol. Prog. Ser., 35,141-151
Videau.C, SourniaA-, Prieur,L. and Fiala,M. (1994) Phytoplankton and primary production characteristics at selected sites in the geostrophic Almeria-Oran front system (SW Mediterranean Sea).
J. Mar. Syst., 5,235-250.
Vincent.W.K (1980) Mechanisms of rapid photosynthetic adaptation in natural phytoplankton
communities. II. Capacity for non cyclic electron transport. J. Physiol., 16, 368-377.
Williams.PJ.LeB. (1993) Chemical and tracer methods of measuring plankton production. ICES Mar.
Sci. Symp., 197,20-36.
YoderJ.A. and Bishop.S.S. (1985) Effects of mixing-induced irradiancefluctuationson photosynthesis
of natural assemblages of coastal phytoplankton. Mar. Biol., 90, 87-93.
Received on February 9,1996; accepted on October 20,1997
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