Light adaptation of oscillatoria agardhii at different time scales

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Pergamon

0273-1223(95)00677-X

War. Sci. Tech. Vol. 32. No.4, PP 3s-4S. 1995. CopYflSbrC I99SIAWQ Pnnled in Oreal Bntain. All ngbl$ reserved. 0273-1223195 $9-$0 + 0-00

LIGHT ADAPTATION OF OSCILLATORIA AGARDHII AT DIFFERENT TIME SCALES Elisabeth H. S. van Duin*, R. Hans Aalderink and Lambertus Lijklema Department of Water Quality Management and Aquatic Ecology, Agricultural University. P.O. Box 8080. 6700 DD Wageningen. The Netherlands

ABSTRACT The Markermeer IS a eutropbic sbaJlow wmd exposed lake. In contrast to other eutropbic lakes in the area. persistent blooms of lhe cyanobacterium Osci/Ia/oria agardhii do not occur. The severe variations in lhe available ligbt energy. caused by an excessive resuspension of sedlffienl, are beld respon.~ible for this absence. Field experiments were conducted in the Markermeer. to investigate the relations between O. agardhii and lhe specific Iigbt climate in the Mastermeer. empbasizing the adaptation rate and extent to Iigbt energy level variations. In experiments wilh traditional ligbt and dark bottles. and bottles moving up and down the water column It was observed that venical mixing tended to increase lhe net production of oxygen. as !be exposure lime near the water surface is too sbort to cause light inhibiuon. From experiments with a vertical perspex tube it was concluded that during days with maximum hourly Iigbt energy levels above 200 l!E·m·2.s·l. lhe light utilization efficiency was mucb bigher in lhe morning hours than during lhe afternoon. This phenomenon did usually not occur at days wilh lower mean UT3thance levels. After prolonged periods of low energy levels (below SO l!E.m'2.s,1 l. the light utilization effiCiency increases significantly but lhe maximum producuon level does nOI increase.

KEYWORDS Adaptation; field experiments; growth: light inhibition: limitation: Oscillataria agardhii; primary production: vertical mixing. INTRODUCTION In many lakes in the Netherlands, blooms of Oscillatoria species occur regularly. In the Usselmeer and in particular in the string of smaller lakes surrounding the polder Flevoland (Fig. I), phytoplankton composition is generally dominated by blooms of Oscillatoria agardhii. The Markermeer (lake Marken) is a large shallow lake linked to these lakes, but with a remarkable absence of persistent blooms of O. agardhii. The often high and fluctuating suspended solids concentration and the related characteristic light field combined with the high degree of vertical mixing in the Markermeer are held responsible for this. Extensive management measures for the lake. which would reduce the size and fetch and accordingly the resuspension•

• Present address: Hoogheemraadscbap van Rijnland. P.O. Box IS6. 2300 AD Leiden. The Netherlands 3S NST 32·4·0

E. H. S. van DUIN el aL

36

were under consideration. The result of these measures would probably favour the conditions for blooms of

O. agardhii.

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To study this problem an extensive study has been conducted. including field experiments and the modelling of sediment transport. light field and algal growth. In these experiments both the adaptation and inhibition of OscillalOria agardhii cultures to various light climates was studied. In this paper the response of the primary production of O. agardhii to a number of time scales in light variations is described. using the Markermeer field data obtained by different experimental techniques. TIME SCALES IN LIGHT ADAPTAnON Phytoplankton in natural waters experiences various fluctuations in light regimes. In the farst place the incident irradianee is changing due to seasonal and diurnal variations. Furthermore the vertical displacement and variations in wind induced resuspension. superimpose short term variations upon the energy levels experienced by algae. All factors affecting the energy level have different time scales and amplitudes and the response of algae to these variations will differ accordingly. both in extent and rate. These factors are listed in Table 1. As various factors are superimposed on each another, this result.. in many pos."ible combined responses of photosynthesis to light variations. The fact that different algal species will react differently and that memory effects may occur, makes the light-production relationship extremely complex and probably contributes to the possible co-existence of many species in one single system.

Ligbt adapultion of Oscillaloria agardhii

37

Table I. Various factors affecting the light energy experienced by algae and their time scales factor

period

time scale

season

year

month

important for algal succession and production levels but not for individuals, considering the generation time (Marra, 1978)

diurnal photo period

day

hours

day-night pattern, very important for both maximum production level and efficiency (Falkowski, 1980; Neal & Richardson, 1987; Post tt ai, 1985)

auenuation

hours! days

hours! days

in shallow lakes with silty sediments, reflection and absorption by resuspended particles may be considerable (Kirk, 1983; Van Duin tt ai, 1992). Affects the decrease across the water column, (vertical attenuation).

waves (reflectance)

hours! days

hours! days

Increase in wave height results in a decrease in reflectance. Effect is only sigmficant at low solar elevation (Kirk, 1983) bUI in thaI case dwarfed by low total energy level.

c1oudiness

minutes! hours

minutesl hours

Though time scale may differ, effect is comparable with attenuation effects but affects the incident level.

vertical mixing

seconds! minutes

hours! days

Effect on individual cells may be considerable (Marra, 1978; Falkowski, 1980)

Most experimental research on light-photosynthesis relationships and adaptation has been done in steady• state turbidostat cultures or in field experiments without vertical mixing (Harris and Lott. 1973; Vollenweider. 1974; Post et al. 1985). However in nature a steady state is never reached and the rate at which light-adaptation occurs may be much more important than the final equilibrium. Harris and Lott (1973) suggested that vertical mixing by turbulence and Langmuir cells. will ensure that no cells are exposed to high light conditions for more than a few minutes continuously. It would thus seem possible that the fluctuating light conditions such as would be found in mixed water columns. best suit the algae for maintenance of continuous high light photosynthetic rates as inhibition is prohibited. Harris and Piccinin (1977) remarked that the static in situ photosynthetic profiles obtained from light and dark bottle experiments. underestimate the maximum net photosynthesis rate under vertically mixed conditions by 25 to 80% due to the appearance of inhibition in the experiments. Although in a number of studies attempts were made to simulate vertical motion in incubation experiments. the effects on the primary productivity estimates were equivocal (Jewson and Wood. 1975; Marra. 1978; Gallegos and Platt. 1981). The simulation of vertical motion in practical experiments is difficult. Gallegos and Platt (1985) distinguished three mixing situations and their implications for field experiments: moderate mixing. strong enough to keep the mixed layer well stirred. The population will be uniformly adapted to near-surface conditions; strong mixing. strong enough to deepen the mixed-layer. Static incubations underestimate the productivity. weak mixing, gradients in photosynthetic parameters will occur. Forced mixing in experiments may overestimate the production because no photoinhibition will occur. Simulation models using various vertical mixing rates and adaptation times suggest that light-shade adaptation does not significantly affect integrated water column photosynthesis (Falkowski. 1980). However simulation model parameters are often obtained from experiments in which phytoplankton cultures are fixed at a certain depth (light and dark bottle experiment) or a steady state is obtained (turbidostat). Platt and Gallegos (1980) and Neal and Marra (1985) found effects of vertical mixing on modelled integrated photosynthetic responses. however general conclusions did not yet emerge.

38

E. H. S. van DUIN el al.

Even if light-shade adaptations may not be important for the integrated water column, productivity in vertically mixed systems, still may control the succession of species. This is influenced by the local circumstances of mixing, light and phytoplankton succession (Neal and Richerson, 1987). OSCILLATORIA AGARDHII

O. agardhii is a solitary filamentous cyanobacterium. It has been known to adapt as a shade plant and is particularly favoured by conditions of low irradiance and short day length (Vermij and Janissen, 1991). Inhibition at high energy levels is less pronounced when nutrient levels or temperature are high (Berger and Sweers, 1986). Therefore under highly eutrophic conditions it can be envisaged that a dense O. agardhii population will dominate in shallow wind mixed lakes. Due to the resuspension of sediment the light climate in the Markermeer varies from very clear with high energy levels to very turbid with low energy levels. As O. agardhii favours low energy levels and grows slowly. the extreme fluctuations in the Markermeer are supposed to be the cause of the absence of persistent blooms. Adaptation of growth parameters has been studied in experiments in continuous cultures, of O. agardhii with a periodic supply of light energy (Post et ai, 1985; Post, 1986). From the results of these experiments it was deduced that the pigment content increased with shorter light periods as did the growth yield. EXPERIMENTAL During two years, 1989 and 1990, primary production experiments have been conducted at a site in the Markermeer. Primary production was measured with -traditional light and dark bottle experiments; -a modification thereof in which bottles moved up and down the water column; -a closed perspex tube placed vertically in the lake under different mixing regimes. In this study, the absence of O. agardhii has been studied. Hence, to conduct field experiments in the lake itself O. agardhii suspensions had to be obtained from other lakes and transported to the Markermeer field site (Van Duin, 1992). The O. agardhii samples were obtained from lake Nijkerkemauw. in which blooms of O. axardhii had been observed for several years. In the samples phytoplankton biomass consisted of at least 90% O. agardhii. To eliminate the effect of nutrient limitation. a solution containing nutrients and macro-ions was added. This suspension was stored in a container and used to fill the light and dark bottles and to supply the suspension in the tube. O. agardhii biomass was measured every two days. Both chlorophyll-a content, ash free dry weight and filament numbers were measured. The filament counts are subject to errors, hence these values have an indicative value only. Several factors may cause variations in chlorophylV cell ratios. for example adaptation to light fluctuations. As this is one of the phenomena of interest, expressing biomass in chlorophyll may complicate the data interpretation. Ash free dry weight (AFDW) may also be used as a measure for biomass, but does not discriminate between living and dead algae. The chlorophylVAFDW ratio was reasonably constant for the O. agardhii suspensions for both years. The average ratio is 0.0068 gchla·gAFDW-1 with a standard deviation of 0.0020. All in all chlorophyll-a seemed the biomass measure with the least disadvantages and is used in this paper. PrimjlQ' production in mOving light and dark bottles. description of experiments Classical light and dark bottles experiments (Vollenweider, 1974) were conducted from a platform at a measurement site in the lake using twelve light and six dark bottles. Six bottles were fixed to a long string at distances of one metre and six to a short string at 0.5 metre intervals. Halfway between two bottles a loop of rope was made. With these loops the strings were placed asymmetrically on a hook, such that all twelve bottles were fixed at a different depth (see Fig. 2). A long string with six bottles covered in aluminium foil wa.'l placed in a hook as well, representing the dark bottles. All bottles were one litre glass bottles.

Light adaPlatioo of Oscillatorla agardhli

39

o

-,

-2

-3

depth(m)

Figure 2. Layout of !be light and dark bottle experiments.

Besides the traditional experiments with bottles at fixed positions, movement through the water column was simulated. For this two long strings with six bottles each and two similar short strings were also placed on hooks but rotated, by hanging the strings on the next loop at specified time intervals. After six movements. the strings are back on their original loop. By changing the time interval between movemenl~. the migration of algae across the water column can be slackened or accelerated. The experiments were performed on II days, six days scattered over the summer of 1989 and five days in June in 1990. The time in which the bottles made a full trip up and down the water column was varied from 15 minutes to 2 hours. Thus the bottles were moved every 2.5. 5. 10 or 20 minutes. In all experiments a string made at least one full trip, and preferably two or three before dissolved oxygen was measured. With an excursion of 2.3 metres for the long strings and 1.17 for the short strings. rotation velocity was either 4.8 m·hour-\ or 9.2 m·hour-\. The number of experiments was limited by frequent high waves on the lake. At wind speeds of 5 Beaufort and more. the bottles smashed each other. Due precautions were taken to prevent exposure to high light intensities near or above the water surface during handling, but some exposure could not be prevented. The accuracy of the experiments was dependent on several factors, e.g., the accuracy of the oxygen measure• ments. the carefulness in the manipulation of the bottles. From measurements with duplicate bottles. an error of 10% in the primary production was estimated. Bacterial contamination was not considered important for the time span of the experiments: less than three hours. The measured net production was integrated over the depth and then averaged for all experiments in order to make comparison between short and long strings possible. The results are presented in Fig. 3. In the experiments of 1989 the specific production rates in September are much higher than those in July. The

40

E. H. S. v.. DUIN tt ilL

production in rotated bottles is higher than that in rUled bottles in 9 out of II experiments. "The n:verse is observed on 15 September 1989 and 20 June 1990 only. Considering the experimental error and the generally limited diffen:nce between the fixed and rotating bottles, these diffen:nces an: not always signifICant.

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Primary production in a perspex wbe. description of experiments A perspex tube of 2.8 metn: height and 0.3 metn: diameter was constructed. see Fig. 4. Within the tube three thin plastic tubes wen: placed. with a length of 0.9. 1.8 and 2.7 metn:s. The tubes wen: connected through the top of the tube jacket to thin hoses leading to a switchboard. With this system of pumps and hoses. the water in the tube was circulated. By shutting one or two of the inlet hoses on the switchboard. the water circulation in the tube could be changed. from circulating the top third of the tube. the top two thirds or the entire content of the tube. By opening the lower plastic tube or all three tubes. the entire tube content was circulated. but with the second method the top third of the tube was n:circulated mon: intensively than the lower third. Because the turbulence was highest near the top of the tube. an oxygen-temperatun: sensor was placed hen:. opposite the water inlet. During the experiment. the sensors wen: connected to a data logger on the platfonn. Oxygen concentration and temperatun: wen: n:gisten:d every 15 minutes. A fifth hose was connected to a hole in the top of the tube. to pn:vent significant over or under pn:ssun:. At the switch board a tap was placed to take samples from the water in the tube. These samples could be withdrawn from either of the three depths. At the start of each experiment the tube was filled with the O. agardhii suspension and lowen:d into the lake. In general for each experiment. the tube was operated for a week. with samples taken every second day. If the O. agardhii population inside the tube seemed unhealthy or seriously injun:d. the tube was cleaned and filled with a fn:sh phytoplankton suspension. and the membrane of the oxygen sensor n:placed. Generally. after a week the experiment had to be interrupted for maintenance. After three weeks the experiments had to be stopped for some time anyway. to clean aU the instruments and the plastic tubes 8.'\ well.

Ligbt adaplatioo of Oscillatoria agardhii

41

1 IntIow 2 outfloW 3 oxygen electrode (1989)

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In 1989 the tube was operated during two two-week periods; 89-2 and 89-3. A membrane pump was used to circulate the water. During period 89-2. only the top hose was opened. Therefore. only the top third of the tube was circulated and a partly stratified situation was simulated. During the period 89-3. only the lower hose was opened to simulate a completely mixed situation. Samples were taken every two days and analyzed for biomass. In the experiments of 1990 the operation of the switches was similar to that of 89-3. The oxygen temperature sensor was placed in a small vessel in the connector hose on the switchboard to improve maintenance possibilities. The tube was operated from June 25 till July 18 and functioned mostly well. The measured oxygen concentration and under water irradiance are for both years presented in Fig. 5. The total under water irradiance is rather different for all three periods. except for 89-3. The temperature was slightly higher in the period 89-2 than in the other periods. Although 89-2 simulated a partly stratified situation and 89-3 a totally mixed situation. the maximum production rates of 89-2 and 89-3 are similar. Detailed data interpretation is described in the following paragraphs.

42

E. H. S. v.. DUIN " aL

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OBSERVED TIMES-SCALES IN LIGHT ENERGY-PRODUCTIVITY RELATIONS Adaptation within an hour

1be effect of fluctuations in light energy by turbulent mixing was studied with the light and dark bottle experiments. However. differences in production vary much more between days iban between fixed and rotating bottles. Small differences between fIXed and rotating bottles are observed and generally rotation of the bottles tends to enhance the production. This observation is in agreement with that of Harris and Piccinin (1977) that fixation of bottles leads to underestimation of the primary production. Apparently the build-up in inhibition is slow compared to the length of exposure near the water surface. 1be rate of build-up of inhibition can not be deduced from these experiments. Adaptation within a day To assess the adaptation of growth parameters of O. agardhii to the light field within hours the production data of the tube experiments were studied. From both years together. 30 days were selected with data sets that were not or hardly affected by tube maintenance or malfunctioning problems. In agreement with the

43

Upt adapcatioa of Ose/tlolanG GgardJljj

method presented by Harris and Lon (1973), the gross production per hour was related to the total under water irradiance during the same hour for all 30 days. The respiration in the tube at night is estimated as the average of the net production values betwUn two hours after sunset until two hours before sunrise. No corrections are made for bacterial effects, including bacterial respiration. If adaptation of growth parameters to available energy occurs within hours, production will be more efficient during hours with increasing irradiance (morning) than during hours with decreasing irradiance (afternoon), i.e. a hysteresis effect Each day has been judged on the occurrence of this phenomenon. Based on an estimation of the accuracy of the production values, a threshold difference of 2 g02·gChla-l·h-1 is defined. If the gross production in the morning was more than 2 g~·gChla-l.h-1 greater than the gross production in the evening, that particular day was labelled to the category on which adaptation of growth parameters occurred (PPinc:reasc > PPdecrease)' If a data set was not conclusive, it was added to the category PPinc:reasc PPdecrease' Six examples are presented in Fig. 6. >t>tetf'Oer

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E. H. S. van DUIN tl al.

44

From the examples in Fig. 6. September 7. 1989 and July 12 and 13. 1990, are considered to demonstrate a positive hysteresis effect. Data are presented in Table 2. Table 2. Occurence of hysteresis effect in the tube Emean> 200 /LE·m· 2·s· 1

Emean < 200 /LE·m·2·s· 1

total

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11

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The expected hysteresis is observed in 14 of the 30 daily sets, the reverse has never been observed. From the 16 data sets without conclusive adaptation. the maximum mean under water irradiance values remained well below 200 IlE.m-2·s-1 for 12 days (75%). From the data sets with adaptation, during only three out of the 14 days the maximum mean under water irradiance values stayed below 200 IlE·m-2·s-1 (21%). Therefore. it may be concluded that adaptation of growth parameters of O. agardhii to the under water light field is observed particularly during days with maximum mean under water irradiance values over 200 IlE·m-Z.s-l. At days with maximum values below 200 IlE·m-2·s·l. adaptation usually does not occur or is imperceptible. This hysteresis effect is referred to as fast adaptation. These observations agree with the results of Harris and Lon (1973). In their experiments. the hysteresis effect occured only if the maximum light intensity experienced by the algae. reached at least the satuf'.ltion intensity. In that case cells became adapted to high light intensities in less than two hours. Harris and Lon (1973) and Harris and Piccinin (1977) expected that with vertical movement the hysteresis effect would be removed as a short exposure time to high light intensities would not cause photoinhibition. However. in our experiments in which we induced vertical mixing, the hysteresis effect was still observed in 14 out of 30 days. Marra (1978) found in his experiments that vertical movement by algae removed the hysteresis effect. However, he worked with laboratory turbidostat experiments with Lauderia borealis. This difference may be caused by a different response of L borealis compared to the response of O. agardhii or maybe the saturation intensity of L. borealis is higher than the maximum intensity used. The occurrence of hysteresis may be either due to state transitions (Post. 1986). diurnal changes or photorespiration. Harris and Lott (1973) thought photo-respiration the probable cause of the hysteresis effect. because they found it to be dependent on the oxygen concentration and the phenomenon was rapidly reversed in the dark. Pahl-Wostl (1992) discussed the importance of the hysteresis effect and used a dynamic model including the build up related to light excess and a first order decay of inhibition to explain these phenomena (Pahl-Wostl and Imboden. 1990). As the inhibition decay rate is relatively low. a significant inhibition can build up during the day, resulting in a severe afternoon dip in the production. Eilers and Peeters (1993) use a similar concept to explain hysteresis. In their mechanistic model they dynamically describe the transition between the so called open. activated and inhibited states. The slow recovery rate from the inhibited state explains the hysteresis observed during a daily light cycle. In our data no explanatory relationship between the oxygen concentration and the hysteresis effect could be detected. If photorespiration is the cause of the hysteresis effect, the representation of the net primary production instead of the gross primary production in the curves of Fig. 6 would have been preferable. because in the computation of the gross production a constant daily respiration has been assumed. However. in this study. we were more interested in the quantification of the light field causing the adaptation than in the precise physiological background.

Ughl adIptIIiOll of OscilllltoritJ agardhii

45

Adaptation within a few dm Figure 5 reveals that no net production occurs at days with mean (averaged over the water column) under water irradiance values of 100 ~E·m-2·s-1 or less (July 9. September 9-11. 1989 and July ~. 1990). but that after prolonged periods of low maximum irradiance values (> 2 days) the production efficiency increases and the net production may become positive (September 12-13. 1989 and July 8-10. 1990). Therefore. adaptation to low maximum energy levels does occur within a few days. This is referred to as slow adaptation. This is studied in more detail in Figs 7 and 8. 89-2

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In Fig. 7 the mean light utilization efficiency (averaged per day) and the mean available light energy (averaged the water column and over the day) are presented. In the period in September 1989 the light utilization efficiency decreases initially. but after prolonged periods of energy levels below SO ~E·m-l.s·l. the light utilization efficiency increases. During the measurement of July 1990 the light utilization efficiency increases initially with prolonged energy levels below SO ~E·m·l.s-l. At 10 July 1990. as the available light energy slowly increases. the light utilization efficiency in tum decreases. Both episodes suggest that the mean light utilization acclimates within a few days. This phenomenon is referred to as slow adaptation. This is not confirmed by the results of the measurements of July 1989. This may be due to the fact that during this period the available light energy was much higher (mostly above 100 ~E·m-2.s-I). The period of June 1990 is too short to observe trends.

E. H. S. VIII DUIN et al.

46 8 -2 Pma<

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In Fig. 8 the maximum hourly net primary production for one day is presented with the same mean available light energy. In aU periods the trend in the maximum production rate seems to follow the trend in the available light energy. The observed trend in adaptation of the efficiency and the maximum productivity reached by the cells is conftrming the conclusions of Falkowski (1980). He remarked that shade adapted algae are often capable of using low light intensities with a higher photosynthetic efficiency than light adapted cells. but their Iight• saturated photosynthetic capacity remains unchanged or is even decreased. If hysteresis effects occur the daily averaged value for the light utilization efficiency is smaller. As hysteresis effects do only occur at days with high energy levels. the hysteresis effect may be responsible for the observed trends of Fig. 7. Thus. the phenomena of slow and fast adaptation may actually be the same.

CONCLUSIONS The mean net production of a natural phytoplankton population dominated by O. agardhii as measured in light and dark bottles. varied between less than I and 14 g02·gChla-l.hr-l. As to short term adaptation to varying light intensities caused by vertical mixing. simulated by rotating bottles. there is a tendency for rotating bottles to exhibit higher primary production values. This effect is obscured by experimental errors.

Light adaptation of Oscil/atoria agardhii

47

Adaptation within a diurnal cycle occurs notably at light intensities above 200 !!E.m-2·s- l • when gross production during morning hours is higher than in the afternoon. Vertical movement in the water column did not remove this effect. This inhibition is generally absent at lower irradiances. Adaptation within a few days was observed at low light intensities. The efficiency of the primary production (in g02·gChla-Lhr-L(!!E.m-2·s-lrl) increased at prolonged intensities below 50 !!E·m-2·s- l . As predicted by Falkowski. alfa increases and Pmax does not increase. Such adaptation may play a role in phytoplankton succussion and selection. Their systematic analysis eventually may support lake management strategies. In the experiments. the light conditions of the Markermeer do not prevent O. agardhii from temporary net growth. The experiments are not conclusive whether the light climate is responsible for the absence of blooms of O. agardhii. ACKNOWLEDGMENTS This research was financed by Rijkswaterstaat. Directorate Flevoland. We would like to thank all student,> and coworkers who spend many hot days in the summers of 1989 and 1990 at the Markermeer. In particular we would like to thank Henk de Grote who made many improvements in both the design and the operation of the field experiments. Furthermore we would like to thank Steven Vermij and Kees Berger for their suggestions and scepticism. which improved the quality of the field work. REFERENCES Berger. C. and Sweers. H. E. (1988). The Ijsselmeer and its phytoplankton with special attention to the suitability of the lake as a habilal for Oscillatoria agardhii Gom.. J. Plankton Res.. 10. 579-599. Duin. E. H. S. van. (1992). Sediment transport, light and algal growth in the Markermeer; A two- dimensional model for a shallow lake. PhD thesis. Agricultural University Wageningen. The Netherlands. Duin. E. H. S. van. G. Blom. L. LiJklenta and Scholten. M. J. M. (1992). Aspects of modelling sediment transport and light attenuation in Lake Marken (Markermeer). Hydrobiologia. 235/236. 167-176. In: B. T. Han and P. G. Sly (eds). SedimentJWater Interactions. Eilers. P. H. C. and Peeters. J. C. H. (1993). Dynamic behaviour of a model for photosynthesis and photoinhibition. Ecological Modelling. 69, 113-133. Falkowski, P. G. (1980). Light-shade adaptation in marine phytoplankton. In: P. G. Falkowski (ed.). Primary Productivity in the Sea. Plenum Press, New York. 99-120. Gallegos, C. L. and Platt, T. (1981>' Photosynthesis measurements on natural populations of phytoplankton: numencal analysis. Can. BulL Fish. Aquat. SCI.• 210. 103-112. Gallegos. C. L. and Platt, T. (1985). Vertical advection of phytoplankton and productivity estimates. Mar. £Col. Prog. Ser.. 26, 125-134 Harris. G. P. (1973). Diel and annual cycles of net phytoplankton photosynthesis in lake Ontario. J. Fish. Res. Bd. Canada. 30. 1779-1787 Harris. G. P. and Loll. J. N. A. (1973). Light intensity and photosynthetic rates in phytoplankton. J. Fish. Res. Bd. Canada. 30. 1771-1778 Hams. G. P. and Piccinin. B. B. (1977). Photosynthesis by natural phytoplankton populations. Arch. Hydrobiology. 59. 405-457 Jewson, D. H. and Wood. R. B. (1975). Some effects on IOtegral photosynthesis of artificial circulation of phytoplankton through light gradients. Verh. Int. Verem. Limnol.• 19. 1037-1044. Kirk. J. T. O. (1983). Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press. Cambridge. USA. Marra, J. (1978). Vertical mixing and primary production. In: P. G. Falkowski (ed.). Przmary ProductIVity in the Sea. Plenum Press. New York. 121-137. Neal. P. J. and Marra. J. (1985). Shon term variations of Pmax under natural irradiance conditions: a model and its implications. Mar. Ecol. Prog. Ser.• 26. 113-124. Neal. P. J. and Richerson, P. J. (1987). Photoinhibition and diurnal variation of phytoplankton photosynthesis -I Development ora photosynthesis irradiance model from studies of in situ response. J. Plankton Res.• 9. 167-193. Pahl·Wostl. C. and Imboden. D. M. (1990). DYPHORA. a dynamic model for the rate of photosynthesis of algae. J. Plankton Res.• 12. 1207-1221. Pahl·Wostl. C. (1992). Dynamic versus static models for photosynthesis. Hydrobiologia. 238.189-196. Platt, T. and Gallegos. C. L. (1980). Modelling primary productivity. In: P. G. Falkowski (ed.). Primary Productivity in the Sea. Plenum Press. New York. 339-362. Post, A. F.• Loogman J. G. and Mur. L. R. (1985). Regulation of growth and photosynthesis of Oscillatoria agardhii grown with a light/dark cycle. FEMS Microbiology Ecology. 31. 97-102.

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Post, A. F. () 986). Transient state characteristics of adaptation to changes in light conditions for the cyanobacterium Oscillatoria agardhii. Arch. Microbiology. 145.353-357. Vermij. S. and Janlssen. R. (1991). Analyse van de habitat van OscUlatoria agardhii.lnJern rapport 1991· 17lio. Rijkswaterstaa/, direc/ie Flevoland. Lelystad (In Dutch). Vermij. S. ()992). ModeUering van de groei van Oscilla/aria agardhii. Intern rapport 1992·1 lio. Rijkswaterstaat, Directie Flevoland. Lelystad (In Dutch). Vollenweider. R. A. ()974). A manual on methods for measuring primary production in aquatic environments.1BP Handbook 110 12. Blackwell Scientific Publications. Oxford.