Comparison of measured primary production, by radioactive carbonate incorporation or oxygen production, with diel variations of oxygen, inorganic carbon and particulate carbon, shows that the net in situ production often exceeds the measured activity, especially in deeper marine ecosystems. In vitro incubations under fluctuating light conditions provide higher values of primary production at low light intensities, both with cultures and with natural populations. The same results are obtained with in situ incubations, by varying the depth of incubation. This method allows reevaluation of primary productivity at low light intensities and provides results in agreement with the in situ variations of oxygen, inorganic carbon and particulate carbon. It can explain why primary productivity in the ocean is higher than previously calculated

Bertels, A.

Joiris, C.R.

Open Marine Archive

BULLETIN OF MARINE SCIENCE, 37(2): 62~25, 1985
INCUBATION UNDER FLUCTUATING LIGHT CONDITIONS
PROVIDES VALUES MUCH CLOSER TO REAL
IN SITU PRIMARY PRODUCTION
C. Joiris and A. Bertels
ABSTRACT
Comparison of measured pIimary production, by radioactive carbonate incorporation or
oxygen production, with diel variations of oxygen, inorganic carbon and particulate carbon,
shows that the net in situ production often exceeds the measured activity, especially in deeper
marine ecosystems. In vitro incubations under fluctuating light conditions provide higher
values of primary production at low light intensities, both with cultures and with natural
populations. The same results are obtained with in situ incubations, by varying the depth of
incubation. This method allows reevaluation of primary productivity at low light intensities
and provides results in agreement with the in situ variations of oxygen, inorganic carbon and
particulate carbon. It can explain why primary productivity in the ocean is higher than
previously calculated.
In the framework of a team approach to the ecological structure in the Southern
North Sea (C cycling: Joiris et al., 1982), a contradiction became evident between
the measured primary production and the determination of the activities con-
suming organic matter. This means that the primary production has been under-
estimated and/or the consumption rate over-estimated (Joiris, 1977). This is why
the measured activities [primary production: radioactive bicarbonate method and
Vollenweider (1965)-type of model; planktonic respiration: dark oxygen con-
sumption rate] were compared with the in situ variations of oxygen and carbonates
concentration during 24-h cycles (Joiris and Hecq, submittedl; Joiris and Bou-
quegneau, unpubl.). These results show that the respiration is correctly evaluated,
but that the primary production is often underestimated by the methods used.
Not only the gross, but even the net primary productions were underestimated.
Since these discrepancies are more important in deep marine systems than in
shallow ones (Joiris, 1977), it seemed interesting to reevaluate the primary pro-
duction methodology especially at low light intensities. One of the main differences
between the natural conditions and the measurements even under in situ con-
ditions seems to be the stability of the light conditions during the measurements,
while in nature, turbulence causes the displacement of phytoplankton within the
water column. This is the reason why we have compared estimates of integral
photosynthesis in natural populations of phytoplankton between samples provid-
ed with vertical movement in a mixed layer and samples incubated at fixed light
depths. Similar experiments have been performed by Marra (1978).
Conclusions reached from these field studies are supported by laboratory ex-
periments on a Dunaliella and a Skeletonema culture. Comparison of the pho-
tosynthesis-light intensity relationship and primary production kinetics has been
worked out under constant and fluctuating light conditions.
MATERIALS AND METHODS
Field experiments were performed in the English Channel (SOON,04°W) on 29 April 1983 at an
euphotic depth of 24 m and a total depth of 50 m. Similar experiments were conducted in the Southern
I Joiris, C. and J. H. Hecq. Planktonic metabolism and diel oxygen curves during FLEX 76, Northern North Sea. Submitted.
620
JOIRIS AND BERTELS: PRIMARY PRODUCTIVITY MEASUREMENTS 621
5
15
3
13
7
8 ••~ ••
10
''4'".
••.•••J..
.'..'
.'.'.p .
.....
........
f'
....
1
3
7
9
15
E
.J:: 20a.
4>
" 25
30
A.
Figure I. In situ primary production determination under constant and fluctuating light intensities
(0---0 constant light, 8" ...8 fluctuating light). A. (Left) English Channel; B. (Right) Southern
North Sea.
Bight of the North Sea (Station Ostend 51°24'N, 02°48'E) on 4 May 1983 at an euphotic depth of 10
m and a total depth of 15 m.
A seawater sample taken at one single depth (- 3 m) from the mixed layer with a polyethylene
Nyskin bottle was used for all incubations. For each depth two bottles (lena Glass), 50 ml each, were
inoculated wtih 10 /lCi NaH'4C03• The bottles were fixed in a transparent plastic rack, attached to a
line and distributed at various depths in the mixed layer. One line had fixed depths of constant light
at depths of - 5, -10, - IS and - 20 m for example. The second line was moved up or down 5 m
every 15 min (fluctuating light). Each experiment lasted 4 to 5 h. The samples were incubated in the
English Channel from 1200-1630, for Station Ostend from 1400-1700. After the incubation we filtered
the samples on Whatman GF/C filters, using a gentle vacuum « 100 mm Hg). Filters were rinsed 3
times with 5 ml filtered seawater. The radioactivity retained on the filter was counted by liquid
scintillation.
In the laboratory, similar experiments were performed with cultures of Duna/iel/a tertiolecta and
Skeletonema costatum. Photosynthesis experiments were performed using a light incubator. Winkler
bottles were inoculated with 400 /lCi NaH14C03 and incubated in light-bags under different light
intensities. Samples remained in their light-bags to prevent a light shock during the whole incubation.
During the fluctuating light incubation a second bag was added every IS min.
Also photosynthesis in the laboratory culture experiments was determined by the classical oxygen
method. Depending on the long respectively short altering of the fluctuating light, the light intensities
were changed every 2 hours respectively every 30 min.
In all the laboratory experiments, filtrations (5-ml aliquots) and radioactive determinations took
place as mentioned above.
RESULTS
Natural phytoplankton, in situ incubations. -In the English Channel an important
difference in primary production is noted between the "constant- and fluctuating
light" incubation measurements. The production measured under fluctuating light
intensities is a factor 2.2 higher than those obtained under constant light conditions
622 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.2, 1985
-I
.t:.
M
I
E
U 300
Cl
..§~~~
200
100
---T'
1.9 3 1 12 11 21
J cm-2h-1 (Ph AR.h-1)
../f·········· -......", ..it.
i
I
f
Figure 2. Primary production -light curves for a culture of Dunaliella under fluctuating and constant
light conditions: typical examples A. (Left) 02.02.1983: 3 h incubation, I4C bicarbonate method; B.
(Right) 31.08.1983: 3 h incubation, oxygen method (0---0 constant light intensities, 8...... 8.fluc-
tuating light intensities).
(Fig. 1A, Table 1). This difference is essentially to be attributed to the low light
intensities corresponding with the deeper incubation depths. Note the slightly
lower or comparable maximal primary production values. These experiments can
be seen as representive for the primary production results obtained during the
same period. In the Southern Bight of the North Sea the difference between both
types pfincubations are very low, if any (factor 1.1). This factor results from two
effects, fluctuating light being the cause of a slightly, lower maximal production,
but higher values at low light intensities (Fig. IB, Table 1).
Cultures, In vitro Incubation.- The effects of fluctuating light intensities on the
photosynthesis-light curves on a Dunaliella tertiolecta culture was worked out
using the radio-active bicarbonate method and the oxygen method. (Fig. 2A-B).
The results of both methods reflect a clear tendency to provide comparable or
slightly lower maximal production under fluctuating light, but higher values at
the low light intensities. As an example, typical kinetics done with cultures in the
laboratory are shown for Dunaliella and for Skeletonema (Fig. 3), both with long
(A, C) and short (B, D) fluctuating periods. The variations of primary production
under fluctuating light are as a rule clearly smaller than the expected values for
kinetics realized under constant light of the same intensities. In the extreme
situation (Fig. 3A, B, D), no difference can be detected between the two light
intensities after an adaptation period, where more than a factor two is observed
for comparable constant light intensities.
DISCUSSION
Incubations under fluctuating light clearly show a tendency to provide com-
parable or slightly lower values of maximal primary production, but higher values
JOIRIS AND BERTELS: PRIMARY PRODUCTIVITY MEASUREMENTS 623
3
4
e
."ci'
'c
./
./
~
3
e
!
4 ~
4
5;10/"
/
1 •• A
7'
TIME min
1eo e40
o 1eo e40
3B
o 1eo e40
TIME mQ1
3
Figure 3. In vitro primary production kinetic of Dunaliella (A, B) and Skeletonema (C, D) under
fluctuating light intensities. A, C: long fluctuations (on the 2 h) -: 30% I, -14% I. B, D: short
fluctuations (on the 30 min) -: 21% I, -13% I. 100% I = 26,000 lux.
than constant light incubations at low light intensities. As a consequence, in deep
systems, this provides higher integrated primary production values for the whole
water column (per surface unit). Not only is this a qualitative difference in the
expected direction, but the observed difference can even quantitatively explain
the discrepancy between measured and natural primary production: during the
diel cycle of 28-29 April 1983 in the English Channel, a net production of 2,500
mg Cm-2·d-1 is to be expected from the natural variations of O2 and CO2
concentrations (Joiris and Bouquegneau, unpubl.); constant light incubation pro-
vides 860 mg C·m-2·d-1 and fluctuating light incubations 1,940 mg Cm-2·d-1
(Table 1).During the diel cycle of 4 May 1983 at Station Ostend, a net production
of500 mg Cm-2·d-1 is to be expected from the variations of O2 and CO2 (ibidem);
in situ constant light incubation provides 350 mg C·m-2·d-1 (Table 1). This
fluctuating experiment provides the confirmation that no discrepancy between
measured and real primary production is to be expected in shallow systems. In
the same circumstances, no important difference between constant and fluctuating
light incubations is detected.
For these reasons, we suggest that incubations under conditions of light inten-
sities fluctuating at a rhythm of 15 min to two hours provide values of primary
production much closer to the real in situ values than incubations under constant
light intensity. The deeper the ecosystem, the bigger the discrepancy between
constant light values of production, on the one hand, and fluctuating light values
and real production, on the other hand.
624 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.2, 1985
Table I. Comparison between the in situ primary productions of a shallow and a deeper biotope ['I:
extinction coefficient, I.: saturation light intensity, Pmax: maximum production, PPP: particulate pri-
mary production, calculated from the modified Vollenweider formula (Mommaerts, 1982)]
It p~ ppp
(J·cm-l (mgC'm-' (mgC'm-l
Incubation time h-') h-') d-')
English Channel (SOON,04°W) 29.04.83
Constant light incubation 1200-1630 0.19 34 10 856
Auctuating light incubation 7 12 1,939
Southern North Sea (51°24'N, 02°48'E) 04.05.83
Constant light incubation 1400-1700 0.50 24 8 317
Auctuating light incubation 8 6 348
Within a more general discussion on the validity of the actual evaluations of
primary production in the ocean, these results suggest that both the 14Cbicar-
bonate and the oxygen methods could be basically correct especially at high light
intensities, both in the laboratory and in shallow systems (for the North Sea
biotopes: see Joiris, 1977). The main problem seems to lie in the extrapolation
of such results to the deeper systems where low light intensities play a very
important role. This is why, for instance, important difficulties for determining
a correct primary production are located in the Central Pacific Ocean (Shulenber-
ger and Reid, 1981; Kerr, 1983). In this situation, incubation under fluctuating
light conditions seems to provide a better picture of the dependence of primary
production on the light intensity and thus a possible answer to the problem.
This approach to the effects of fluctuating light is very different from-but
complementary to-the study ofits physiological effects to be noticed on a much
shorter time scale (Frechette and Legendre, 1978; Legendre, 1981). It must indeed
be noted that both types of experiments with fluctuating light concern entirely
different time scales, and thus probably different phenomena: the very short fluc-
tuations (sec) can correspond to the effect of surface waves. Such effects are
however already integrated in our experiments at least for the in situ measure-
ments. The time scale we used (fluctuation periods from 15 min to 2 h) concerns
another phenomenon, in addition to the effects of short time variations. It cor-
responds probably much more to the vertical water movements (turbulence and/
or internal waves, for instance) within the mixed layer. Other results concerning
the same time scale can easily be incorporated in our interpretation (Harris and
Lott, 1973; Jewson and Wood, 1975; Marra, 1980). A possible mechanism for
explaining the effects of fluctuating light could be found by establishing a link
with the light or shade adaptation of algae. Marine phytoplankton does indeed
respond to decreasing light intensities by increasing its photosynthetic pigments
content (Falkowski, 1980). On the other hand, the potential photosynthetic ac-
tivity per chlorophyll unit is dependent on the previous light intensities (Demers
and Legendre, 1981). Finally, a relation exists between photosynthetic capacity
and the stability of the water column (Legendre, 1981). This allows us to formulate
the following hypothesis: the differences between constant and fluctuating incu-
bations could be that the phytoplankton cells are respectively light- and shade-
adapted. The effect of fluctuating light on primary production is thus clearly
dependent on the depth of the mixed layer: no important effect was detected in
the Southern North Sea (15 m). This could explain why other authors came to
the conclusion that vertical mixing has little or no effect on primary production
(Falkowski and Wirrick, 1981; Gallegos and Platt, 1982).
JOIRIS AND BERTELS: PRIMARY PRODUCTIVITY MEASUREMENTS
ACKNOWLEDGMENTS
625
This is a contribution to the Belgian National Programme on Oceanography, Prime Ministry's office
for Science Policy. Part of the experimental work was realized by J. Nijs and R. Vanthomme.
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DATEACCEPTED:June 25, 1985.
ADDRESS: Laboratory for Ecology, Free University of Brussels (V. U.B.), Pleinlaan, 2, B- 1050 Brussels,
Belgium.


Incubation under fluctuating light conditions provides values much closer to real <i>in situ</i> primary production

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