temporal changes in biomass specific photosynthesis during the summer: regulation by environmental...

Hydrobiologia 2431244: 1 19- 135, 1992. V. Ilmavirta & R.Z. Jones (eds), The Dynamics and Use of Lacustrine Ecosystems. O 1992 Kluwer Academic Publishers. Printed in Belgium.

Temporal changes in biomass specific photosynthesis during the summer: regulation by environmental factors and the importance of phytoplankton succession

Donald C. Pierson,' Kurt Pettersson ' & Vera Istvanovics 1 Institute of Limnology, Uppsala University, Box 557, S-751 22 Uppsala, Sweden; * ~ a l a t o n Limnological Research Institute, H-8237, Tihany, Hungary

Abstract

Measurements of phytoplankton photosynthesis vs. irradiance relationships have been made at 3-7 day intervals in Lake Erken (central Sweden) for three years during summer stratification. Both the rate of light-limited (aB) and light-saturated (PE,) photosynthesis per unit chlorophyll a showed distinct and similar temporal trends in each year. Seasonal trends were especially evident for P:,,, which increased in value for several weeks following the onset of thermal stratification, and then declined in the presence of the large colonial blue-green alga, Gloeotrichia echinulata. By late summer, when the biomass of G. echinulata had decreased, P:,, again rose to its early summer value. The covariation of biomass- specific photosynthesis with the blooming of G. echinulata was the one clear seasonal (week-month) pattern which emerged in each of 3 years. Over short (day-week) time scales, changes in aB were related to changes in irradiance exposure on the day of sampling. However, the relationship between these two parameters was variable in time, since it was superimposed upon longer term trends controlled by changes in phytoplankton species composition. Increases in G. echinulata biomass corresponded with a deepening of the thermocline, which both increased internal phosphorus loading and the transport of resting G. echinulata colonies into the epilimnion. The timing and magnitude of the yearly G . echinulata bloom was as a result related to the seasonal development of thermal stratification. These results illustrate the importance of seasonal changes in the phytoplankton community as a factor regulating rates of biomass specific photosynthesis, particularly when the successional changes involve species with very different life strategies.

Introduction

Biomass specific rates of both light-limited (aB) and light-saturated (P:,,) photosynthesis are measures of phytoplankton physiology, which have received wide attention, both as indicators of phytoplankton growth and adaptation, and be- cause of their use as parameters in models of algal photosynthesis. Over the past 3 years (1987- 1989), we have monitored biomass-specific photosynthesis, phytoplankton phosphorus status,

and the thermal structure in Lake Erken (Central Sweden), from late spring to early fall. Such data have allowed us to examine the vertical variability in rates of biomass-specific photosynthesis, and the impact of this variability on estimates of integral primary production (Pierson, 1989. In addition to the vertical inhomogeneity of biomass- specific photosynthesis, distinct temporal variations in both PE, and aB are also evident during each of the three years. In this paper these temporal variations in biomass specific photosynthe-

sis are examined, and related to algal adaptation to light, temperature, and available nutrients.

Factors regulating biomass spec& photosynthesis

The rate of light-limited, biomass-specific photosynthesis (aB) can be considered to be a function of two factors (Bannister, 1974; Platt & Jassby, 1976).

- aB = $ , (1)

where:

aB = The slope of the initial light limited portion of the photosynthesis vs. irradiance relationship i.e. [mg C (mg Ch1)- ' h - ') (pmole quanta m - 2 - 1

- s > - ' I a;, = The absorption cross section of

cellular chlorophyll a i.e. (m2 mg Chl- ') (Morel, 1978; Kishino et al., 1986)

@ = The quantum efficiency of carbon assimilation i.e. [mg C (mole quanta)- '1

Kiefer & Mitchell (1983) suggest that @ is relatively independent of nutrient limitation, but does vary as an inverse function of irradiance with maximum values occurring at low irradiances. Sakshaug et al. (1989) define the relationship between @ and irradiance as a function of absorption cross section and turnover time of photosystem 11, such that @ decreases when the incident photon flux saturates the processing capacity of the photosystem. The value of varies as a result of changes in the packaging of the intercellular chlorophyll a. In general, will be maxi- mal when the intercellular chlorophyll a is highly dispersed, so that increases in Chl/cell, cell size, and cell sphericity, will all tend to decrease the value of (Kirk, 1975, 1976, 1983; Morel & Bricaud, 1981). Also since a* is normalized to chlorophyll a, the presence of%ther light harvesting pigments and changes in their relative composition can lead to changes in qh .

The rate of light-saturated photosynthesis (P:,) is independent of light harvesting capacity, but is instead a measure of the dark reaction in photosynthesis (Platt & Jassby, 1976; Harris, 1978). From a biochemical standpoint, there is reason to believe that these reactions, which are enzyme mediated, would be temperature dependent. A number of studies suggest that P:,, will vary as a function of temperature in terms of in- dividual species (Tailing, 1957; Eppley, 1972). However, this is not always the case, particularly in regards to natural phytoplankton populations (Harris et al., 1980; Heyman, 1986; Fee et al., 1987). Therefore, while temperature sets and upper limit on P:,,, a variety of other environmental factors seem to limit it to less than this upper value (Eppley, 1972).

That nutrient availability would regulate rates of biomass specific photosynthesis is expected, since empirical models do show a hyperbolic relationship between specific growth rate and cellular nutrient concentration (Droop, 1973). Senft (1978) and Smith (1983a) have shown that a similar relationship also exists between p:,, and cellular phosphorus. The relationship between nutrient limitation and aB is not considered by either Senft (1978) or Smith (1983a), and parameters directly describing nutrient limitation are absent from mechanistic descriptions of photosynthesis such those presented by Kiefer & Mitchell (1983) and Sakshaug et al. (1989). However, it seems reasonable to expect aB to be related to nutrient availability, if nutrient availability affects light harvesting capacity. Both Kiefer & Mitchell (1983) and Sakshaug et al. (1989) show the ratio of cellular chlorophyll a to carbon to be related to nutrient availability, supporting this contention.

Methods

Water samples were taken at a sampling station 700 m offshore above the deepest point of the lake (Z,,, = 21 m). Sampling began just prior to (1987 and 1989) or just after (1988) the onset of thermal stratification, and continued until late Sep- tember, by which time the lake was isothermal.

On each sampling date one sample was always collected from 0.5 m, and a second was collected from just above the seasonal thermocline when it existed, or from 12 m when the lake was isothermal. During thermally stratified conditions sarn- ples were collected from the hypolimnion at a depth of 15 m. In 1988 and 1989 samples were also regularly collected from a depth of 3 m. The data presented in this paper are averages of the measurements made within the epilimnion during stratification or between 0.5 m and 12 m during isothermal periods. In 1987 and 1988 samples were usually collected twice weekly, while in 1989 the sampling frequency was decreased to once a week. The more frequent sampling interval in 1987 and 1988 more adequately recorded short term changes in the parameters examined, and as a result these data appear more variable. To bring out the long term trends in the 1987 and 1988 data, and make these data visually comparable with the 1989 data, we therefore occasionally smoothed the 1987 and 1988 data with a 3 point (approximately 1 week) running mean.

Photosynthesis vs. Irradiance (PI) relationships were determined using the 14C incubation method of Lewis & Smith (1983). The measured photosynthesis (pB) and irradiance (I) data were used with the empirical relationship (eq. 4), suggested by Jassby & Platt (1976) to estimate the values of PEax and aB.

PB (I) = Pga, tan h (aBI/PE,) . (2)

A more detailed description of the photosynthesis methods is presented by Pierson (1989). In Pierson (1989) a term representing the Y intercept of the PI relationship (RB) was added to equation 2. This term, which in theory represents the phytoplankton dark respiration and should therefore be slightly negative, could rarely be statisti- cally differentiated from zero, and was occasionally positive. For this reason R* was eliminated from equation 2. In this work, the 1987 Pgax and aB values were re-estimated on the basis of equation 2, as were the 1988 and 1989 values.

Dissolved nutrient concentrations (SRP, NO;, NO, and NH,' ) were determined by standard methods described in Ahlgren & Ahlgren

(1976) and APHA (1975). To measure particulate phosphorus, seston was first collected on 0.45 pm membrane filters which were first leached with distilled water. The filters were then digested by persulfate oxidation in an autoclave (Menzel & Corwin, 1965). Total phosphorus was measured using the same digestion procedure on aliquots of whole lake water. For particulate nitrogen and carbon, seston was collected on precombusted Whatman GF/F glass fiber filters which were later analysed using a Carlo-Erba CHN analyzer. Sur- plus phosphorus and alkaline phosphatase activity were measured using the methods described in Pettersson (1980). Seston for chlorophyll a analysis was filtered on Whatman GF/F filters, which were extracted in 90% acetone. In 1987 and 1988 the acetone extracts were fluorometrically analysed by the method in Strickland & Parsons (1972). In 1989 chlorophyll a was spectrophoto- metrically measured using the method described in Ahlgren & Ahlgren (1976). Occasionally in 1988 and consistently in 1989 chlorophyll a size fractionation experiments were performed in which the filtrates passing through 3.0 pm and 12 pm membrane filters, and a 200 pm net were also collected on Whatman GF/F filters and analysed for chlorophyll a as described above. A more detailed description of the size fraction experiments is given by Pettersson et al. (in prep.).

Underwater PAR (400-700 nm) irradiance profiles were usually measured at the time of sampling. From these measurements the mean extinction coefficient of downwelling irradiance (Kd) was calculated as described in Pierson (1989). Water temperatures were measured automatically at 16-25 depths at 1 minute intervals using ther- mocouple sensors having a 0.05 "C resolution. Mean temperature profiles were saved at 30 min. intervals, and later used to estimate the depth of vertical mixing and the magnitude of the metalimnetic temperature gradient. A similar data log- ging system was used to record surface irradiance, with measurements being made at 1 minute intervals, and mean values saved at hourly intervals. In 1987 total incoming radiation (watts m - between 300-3000 nm) was measured with a pyr- anometer, and these data were subsequently con-

verted to PAR as described by Tilzer (1983). Be- ginning in 1988, surface PAR was measured directly using a Li-Cor sensor.

Yearly variations in thermal structure, nutrient limitation, and biomass

Variations in the thermal structure of Lake Erken are shown by the isotherm plots in Fig. 1, and some relevant statistics regarding the thermal structure are summarized in Table 1. Of the three years, 1988 stands out as having an exceptionally stable and long period of stratification, which was established approximately two weeks earlier, and lasted nearly a month longer when compared to 1987 and 1989. Furthermore, the temperature gradient across the metalimnion was much greater in 1988, on average, by a factor of more than two (Table 1). While the mean epilimnion depth (Ta-

ble 1) was similar in all years, inspection of Fig. 1 shows that between late June and late July of 1988 the epilimnion was shallow relative to the other years, varying between 4 and 7 meters.

After the onset of thermal stratification in each year hypolimnetic water temperatures rose by several degrees during the stratified period (Fig. 2). Since the bottom of the euphotic zone (1 % PAR) was usually between 7-8 meters, while the hypolimnion was usually deeper (Fig. I), direct warming can not be responsible for this temperature increase. In fact, less than 0.05% of the surface radiation could penetrate to the 15 meter depth. The occasional step-like rises in temperature must therefore, be the result of large individ- ual mixing events, while the more gradual rises are likely the combined effects of a number of smaller events. These data indicate that there is considerable hypolimnion-epilimnion exchange during thermally stratified conditions.

In Table 1 the mean July-August concentrations of phosphorus, nitrogen and chlorophyll a,

Table 1. Mean epilimnetic nutrient concentrations and indices of nutrient deficiency for July to August of each year. Values in parentheses are the coefficient of variation. Data which characterizes the lake's thermal structure is given in the bottom of the table. The thermal data are calculated over the entire period of thermal stratification during each year. -

Parameter

Chlorophyl a * * (mg m - 3,

Soluble reactive phosphorus (mg m - 3,

Total phosphorus ** (mg m - 3,

Particulate phosphorus ** (mg y - ') Particulate nitrogen ** (mg m - ) Specific phosphatase activity (n mole pgChl- Particulate PIC** (weight) Particulate N/C * (weight) Particulate N/P * (weight)

Onset of thermal stratification (1) Loss of thermal stratification (2) Total days of thermal stratification Mean depth of epilimnion (m) (3) Mean metalimnion temperature Gradient ("C/m) (4)

24 June 17 Aug. 54 8.6 1.39

4.43 (66.0) 1.64 (68.1)

15.0 (30.2) 6.82 (38.3)

90.7 (23.4) 0.133 (72.8) 0.014 (29.6) 0.185 (16.4)

14.1 (22.5)

9 June 12 Sept. 95 9 3.08

9.28 (95.1) 5.78 (96.8)

23.8 (30.3) 10.4 (40.9)

111.8 (46.6) 0.257 (120) 0.019 (23.1) 0.175 (20.9) 9.46 (21.0)

22 June 5 Aug.

44 9.6 1 .14

** ANOVA showed significant differences to p < 0.0001. * ANOVA showed significant differences to p t 0.005.

Time after which there was a temperature gradient greater than 1 "C/m somewhere between 4 m and 12 m. Time after which a temperature of at least 1 "C/m did not exist anywhere between 4 m and 12 m. Depth to the first measured temperature gradient that was at least 1 "C/m. The metalimnetic temperature gradient is considered to be the maximum gradient found between 4 and 12 m.

1987 Water Temperature isopleths

0 V I d

1988 Water Temperature Isopleths

1989 Water Temperature Zsopleths

Fig. 1. The summer thermal structure of Lake Erken as shown by 2 "C isotherms. Note the differences in the time scales. Instrument failure in 1989 prevented data from being collected after the second week in August.

along with several measurements of phosphorus status are presented. We have limited this comparison to these months in which we have ade- quate sampling coverage in all years, and since

17 15 Meter Water Temperatures T ("C)

12000

15 Meter SRP Concentrat~ons IOOOO ( ~ r ' I . t

: 8

80 00 . ,

I-May 22-May 12-Jun 3-Jul 24-Jul 14 Aug

Fig. 2. Seasonal variations in hypolimnetic temperature, and soluble reactive phosphorus concentrations. All measurements were made at the 15 meter depth. The increases in hypolimnetic temperatures during stratification suggests epilimnion - hypolimnion exchange.

thermal stratification was always established by July. Thermal stratification had a predicable effect on epilimnion SRP concentrations. Concen- trations were lowest in 1988 largely since the prolonged period of stratification limited autoch- thonous inputs of hypolimnetic SRP, particularly those that followed the breakdown of thermal stratification in the other two years (Fig. 3). The increase in SRP in August 1989 was particularly large due to higher hypolimnetic SRP concentrations (Fig. 2), which were completely mixed into the water column, once the lake turned over on 5 August (Table 1). Significant increases in epilimnetic SRP occurred in late July of 1987 and 1989, and in mid August of 1988. In each year these increases began several weeks before the complete breakdown of thermal stratification.

There were two phytoplankton blooms during

I ~ M a y 22-May 12-June 3 ~ J u l y 24-July I 4 Aug 4 Sept 25-Sept

Fig. 3. Seasonal variations in epilimnetic soluble reactive phosphorus concentrations. The large increase in 1989 results from the greater hypolimnetic concentrations shown in the previous figure. 1987 and 1988 data are smoothed with a 3 point running mean. The arrows correspond to the times at which the depth of the epilimnion became greater than 10 meters.

1989 (Fig. 4). The large blue-green alga Gloeo- trichia echinulata, dominated during the first peak. The second bloom corresponded in time with a rapid increase in epilimnion SRP (Fig. 3), and consisted of large diatoms (Stephanodiscus hantzschii, Stephanodiscus astraea var. intermedia, and Melosira granulata). In 1988 there was an increase in biomass which occurred between mid July and mid August, and consisted of two distinct peaks. The first peak was largely of diatoms (Asterionella fonnosa and Stephanodiscus sp.) and the dinoflagellate Ceratium hirudinella, but G. echinulata and Anabaena spp. were also present. During the second peak there was an increase in G. echinulata, which then accounted for over 50% of the biomass, and a decline in the importance of C. hirudinella. G. echinulata obtained a greater dominance in 1989 as is indicated from chlorophyll a size fractionation experiments. In 1989, when over 90% of the phytoplankton composition (by biomass) was G. echinulata, more than 70 % of the chlorophyll a was retained by a 200 pm nitex net. In 1988 however, only 30% to 47% of the chlorophyll a was in the >200 pm size fraction during early August. In 1987, a much smaller biomass peak occurred in August. Unfortunately, we lack data on the phytoplankton composition during this year. How- ever, G. echinulata colonies were clearly visible in the collected samples, and at the lake's surface during August of 1987.

Mean July-August P/C and NIP, ratios (Ta- ble 1) show 1989 to be least phosphorus deficient as would be expected from the greater SRP transport to the epilimnion during this year. Addition- ally, the particulate N/P ratios, suggest that 1987 was less phosphorus limited than 1988, a conclusion also corroborated by the SRP data. None of the measures, however, suggest severe phosphorus limitation to have occurred during July and August of any of the years for which measurements were made. Using the classification suggested by Healey & Hendzel(l980) both the N/P and P/C ratios suggest no phosphorus limitation in 1989, and only moderate limitation in 1987 and 1988. Specific alkaline phosphatase activities were not significantly different between years, and were in a range that Pettersson (1980) found to be indicative of low - moderate phosphorus limitation in Lake Erken. Since 1988 was clearly the year with the most stable and persistent thermal stratification, it is surprising that more severe phosphorus limitation was not detected. Earlier in the year, between June and mid July, a number of indices of phosphorus deficiency (Istvanov- ics et al., in press.) did, however, suggest the phytoplankton were phosphorus limited. Further- more, Bell et al. (in prep.) suggest that phosphorus deficiency during June-July of 1988 was reduced as a result of grazing induced epilimnetic phosphorus cycling. In all years phosphorus deficiency was decreased by the appearance of G. echinulata, which migrates from the sediments (Roelofs & Oglesby, 1970) bringing with it stores of surplus phosphorus (U16n, 1971; Pettersson et al., 1990; Welch & Barbiero, 1990).

The temporal variability of biomass speczfi photosynthesis

In Fig. 5 volumetric rates of light-saturated (P,,,) and light-limited (a) photosynthesis are plotted against chlorophyll a. The slope of these plots, which were made using pooled data from all depths (within the epilimnion) and all years, therefore represent an overall mean of the biomass-specific photosynthetic rates. These data

Mean Ep~lmnet~c Chlorophylla

l.May 22-May 12-June 3 July 24 July 14 Aug 4-Sept 25~Sepl

I

Fig. 4. Temporal variations in epilimnetic chlorophyll a concentration. 1987 and 1988 data are smoothed with a 3 point running mean. The arrows correspond to the times at which the depth of the epilimnion became greater than 10 meters.

1 Pmax =2 871 Chl + 3 071

r2 =0435 2 Pmax = 1 36 Ch l t6 736

r2 = 0 469

0 5 10 15 20 25

Chlorophyll (mg m )

8 0 5 10 15 20 25

Chlorophyll (mg m .3 )

Fig. 5. Regression analyses between chlorophyll a and non normalized measurements of light limited (u ) and light saturated (P,,,) photosynthesis. The line with the steepest slope in each diagram was calculated using only data with chlorophylla concentrations that were less than or equal to 5 mg m-3.

show considerable scatter about the regression lines as a result of the rates of biomass specific photosynthesis being temporally and spatially variable, but as would be expected, there is a relationship between biomass and photosynthesis. The slopes of these relationships are steeper at low biomasses, indicating a negative relationship between chlorophyll a and rates of biomass-

specific photosynthesis. For example, regression analysis of the entire PE, vs. chlorophyll a data set yields a slope of 1.36 mg C(mg Ch1)- ' h- ' (r2 0.469, p < 0.0001), while restricting the analysis to chlorophylla concentrations of less than 5 mg m-3 yields a slope of 2.87 mg C (mg Ch1)-'h-' ( r 2 0.435, p<0.0001).

To examine the temporal variability in biomass specific photosynthesis, seasonal variations in PE, and aB are plotted in Fig. 6. In this figure, by averaging all epilimnetic values associated with a given sampling date, and by smoothing the 1987 and 1988 data with a running average, we largely eliminate small-scale temporal and vertical differences in photosynthesis which would be associated with short term photoadaptation. The re- maining seasonal trends represent the effects of long term successional adaptation to changing levels of light, temperature and nutrient limitation. Two general trends can be seen from these data. First, the values of PE,, consistently increase from the pre-stratified or early stratified period to a maximum summer value which is usually reached at a period corresponding to maxi-

m 1-May 22-May 12-June 3-July 24-July 14 Aug 4 Sept 25~Sepl

Fig. 6. Seasonal variations in the photosynthetic parameters ctB and Pg,,. The 1987 and 1988 data are smoothed with a 3 point running mean.

mum epilimnion water temperatures (compare Figs. 6 and 1). Secondly, there is a distinct decline in the values of both P;,, and aB, that corresponds to the biomass increase associated with the G. echinulata bloom in each year.

Phytoplankton size and biomass-specljic photosynthesis

In 1989 chlorophyll a size fractionation experiments allowed the influence of phytoplankton size on aB to be examined. In Fig. 7 both the propor- tion of total chlorophyll a that was greater than 12 pm in size, and the value of aB, which was determined using unfiltered whole water, are plotted. When temporal variations in these parameters are examined together (Fig. 7), a negative relationship between them is evident. Evidence that the temporal variations in aB are similarly, influ- enced by changes in size composition of the phytoplankton in 1987 and 1988 can be obtained from Figure 8, in which the data from Fig. 6 are transformed so that values on the vertical axis are a percentage of the yearly maximum for each parameter, and time is relative to the maximum blue-green algal biomass in 1988 and 1989, or what we assume to be maximum blue-green algal biomass (maximum surface chlorophyll a and G. echinulata colonies visibly present) in 1987. The data when expressed in this manner, clearly show that both P:,, and aB reached their seasonal minima at times corresponding to the dominance of large blue-green algae. Further-

: t 1 0 0 4 N ~

A W - -

950 - - - . ' 0 0 3 7 C

; 40 ' 30 0 0 2 5

,*- .- -- 48 p 20 0 0 1 i" 10 0 0 E - !-May 22 May 12-June 3 July 24-July 14 Aug 4-Sepl 25 Sepl ,

t(

Fig. 7. Temporal variations in the percentage of total chlorophyll a greater than 12 pm (------), and light limited photosynthesis (aB) ( ) . Detailed chlorophyll a size fractionation data were only available in 1989.

-60 -40 2 0 0 20 40

Day Relative lo Maxlrnurn Blue~Gieen Blornass

+87 - - A - - 8 8 *89

Fig. 8. Normalized plots of PE,,, aB and the ratio of chlorophyll a to particulate carbon. The value of these parameters are expressed as a percentage of the maximum value measured in each year. Time in days is expressed relative to the maximum measured blue-green algal biomass. This maximum (day 0) corresponded with the maximum surface chlorophyll a concentrations in 1987 and 1988, and the first major chlorophyll a peak in 1989.

more, the range in variation is greatest in 1989, which is consistent with a greater dominance of the large colonial G. echinulata. Blue-green algae may contain phycobilins which also act as light harvesting pigments. Consequently, in the presence of blue-green algae, normalizing rates of photosynthesis to chlorophyll a may be particularly dubious. Such variations in pigmentation would, however, increase not decrease the value of aB so that the decline of aB in the presence of blue-green algae (Fig. 8) is, if anything, an under- estimation of the true decline in light-limited photosynthesis. In Fig. 8 the ratio of chlorophyll a to

particulate carbon is also plotted. While the carbon quotient is clearly affected by bacterial and detrital material (Banse, 1977; Pettersson, 1980) there is none the less, a consistent trend of increasing Chl/C that corresponds with the peak in the blue-green algal biomass, and the decline in biomass specific photosynthesis.

Irradiance exposure - biomass specrficphotosynthe- sis

In order to examine the relationship between light exposure and changes in the rate of biomass- specific photosynthesis, temporal variations in aB were compared with changes in effective irradiance exposure. This measure of irradiance is based on the irradiance at the surface (I,), the depth of mixing (Z,), and the vertical extinction coefficient of downwelling irradiance (Kd). It is simply, the mean irradiance calculated through- out the epilimnion.

1 1 eff = - J I. e - KdZ dZ .

z, (3)

Equation 3 can be simplified to equation 4, which was used for the calculations made here.

In our calculations Z, was estimated from 1 "C isotherm plots calculated from the automated temperature records. In 1989 underwater light measurements, from which Kd is calculated, were not made after 8 August, so only data up to this time are considered. Variations in aB and the effective irradiance calculated over the entirety of the sampling day, up to the time of sampling, are shown in Fig. 9. Examination of these data shows a correspondence between changes in aB and changes in I , , with increases in aB resulting from increased irradiance exposure.

1 1 ioo4 , 1

8 .__---._ I ~, 0 03

0 02 4

. -.--. -. 0 01

0 0 19-May 29-May %June 18-June 28 June 8-July 18-July 28 July 7 Aug 17-Aug

Fig. 9. Variations in effective irradiance exposure, and aB. In all years I,, was calculated by varying the value of both Kd and Zm over time (dashed line). In 1989, I,, was also calculated and by holding Kd constant at the years mean value (dashed and dotted line).

Relationship between PEax and 8

Figure 8 shows a positive correspondence between seasonal variations in aB and P:,,, which is also seen from the variations in IK (pEaX/aB) shown in Fig. 10. The value of IK was relatively constant, considering the magnitude of the variations in Pzax and aB. Its value ranged between 100 and 150 pE m- s - ' except during July 1988 when values of up to 250 pE m - s - ' were measured. These values of IK are within the range found by Harris (1978) who compiled IK data from a large number of published investigations, and found that values between 50 pE m - s - ' and 120 pE m-* s- ' were most common. The increases in IK were a result of increases in PEax that occurred, while a' remained relatively unchanged (Fig. 6), and correspond to a decline in epilimnion depth (Fig. 1) and an increase in I,,

0 4 1-May 22~May 12~June 3 July 24-July 14~Aug 4-Sept 25 Sepl

0 l L l oo 10-June 24-June &July 22-July 5Aug 19-Aug X e p t 16-Sept 30Sept

Fig. 10. Temporal changes in IK for all years (top) and only for 1988 (bottom). In the top portion ofthe figure the 1987 and 1988 data are smoothed with a 3 point running mean. In the bottom portion of the figure nonsmoothed IK data from 1988 are plotted with calculated values of I,,

(Fig. 10). It is significant that only during 1988, when thermal stability was unusually high and the mixed layer was unusually shallow, did shifts in IK occur, which were in accordance with large increases in I,, (Fig. 10).

Nutrient defiiency and biomass-speczfic photosynthesis

The relationship between nutrient deficiency and the measured rates of biomass specific photosynthesis is examined by plotting P:,, as a function of particulate P/Chl and particulate N/Chl (Fig. 11). While there is some suggestion of a hyperbolic relationship between nutrient quota and P:,,, such as previously found by Senft (1978) and Smith (1983a), the relationship is poor and of no statistical significance. Similar plots using surplus phosphorus normalized to chlorophyll a or phosphatase activity normalized to chlorophyl-

Fig. 1 1 . Scatter plots of Pg,, plotted against particulate phosphorus normalized to chlorophyll a and particulate nitrogen normalized to chlorophyll a. The solid symbols represent data collected before the dominance of blue-green algae, the open symbols represent data collected after the dominance of blue- green algae.

1 a gave similarly poor results. Bell et al. (in prep.) show that bacterial-algal competition for phosphorus was highest from June to mid July of 1988, and that the amount of phosphorus contained within bacterial and algal biomass was approximately equal during this period. Bacterial production declined dramatically during the G. echinulata bloom, at which time declining inorganic nitrogen concentrations and increasing 3 2 ~ turnover times suggest a switch from phosphorus to nitrogen deficiency (Pettersson et al., 1990; Ist- vhovics et al., 1990; Istvhnovics et al., in press.). Considering the above, it is possible that bacterial interference would have affected the N/Chl and P/Chl relationship, and that N/Chl would be a better measure of nutrient limitation following the dominance of blue-green algae. Consequently, there were reasons to believe that a better relationship between nutrient quota and P:,, would be obtained if the data were divided into pre- bloom and post-bloom periods using the same criteria as in Fig. 8. Dividing the data in this man-

ner (Fig. 11) did not, however, reveal an improved relationship between nutrient quota and P:,. Lastly, the relationship between P:,, and the maximum 3 2 ~ uptake velocity per chlorophyll a (V:,,) was also examined. This measurement of phosphorus deficiency would be free of detrital interferences that might affect particulate phosphorus and particulate nitrogen determination. Again, no relationship could be found between P:,, and this measurement of phosphorus deficiency either using the entire data set or pre-bloom and post-bloom subperiods.

Temperature and biomass-speczfi photosynthesis

A regression analysis between water temperature and P:,, revealed no direct relationship between these two parameters, and there was little evidence of a temperature-dependent upper limit on P:,, such as that suggested by Eppley (1972).

4 24-June 8~July 22~July 5 Aug 19.Aug 2 Sept 16-Sepl 30 Sepl

Fig. 12. Seasonal variations in Pz,, and the mean water temperature between 0 and 5 meters. The data from 1987 and 1988 are smoothed with a 3 point running mean.

Seasonal trends in epilimnetic water temperature and P:, are plotted for 1987-1989 in Fig. 12. When the data are expressed in this manner there does appear to be a positive relationship between P:,, and temperature in 1987 and 1988, with both parameters increasing from low values at the onset of stratification, to maximum values at approximately the time of maximum temperature. Such a clear correspondence between water temperature and p:,, is not seen in 1989. After the seasonal peak in P;,, is reached, the variability in this parameter is more strongly related to seasonal trends in biomass, and the succession of blue-green algae, than to variations in temperature. It is this fact that largely explains the lack of a significant P:,, vs. temperature relationship when all the data are pooled and used for a sin- gle regression analysis.

Discussion

Of all of the factors examined, changes in cell/ colony size (and the corresponding changes in species composition) were of greatest importance in regulating rates of biomass-specific photosynthesis. The most convincing data in support of this contention is the comparison of the 1989 temporal variations in aB with the variations in > 12 pm chlorophyll a (Fig. 7). Time series plots of P:,, and > 12 pm chlorophyll a revealed a similar result. Further evidence of the importance of algal size as a regulator of biomass-specific photosynthesis, can be found in the normalized time series of aB and P:,, (Fig. 8). Here there is a clear correspondence between the decline in both photosynthetic parameters and the dominance of the large colonial blue-green alga, G. echinulata. Finally, regression relationships between (non chlorophyll a specific) measurements of P,,, or ct and chlorophyll a (Fig. 5) show that inclusion of high biomass data significantly reduces the regression slope.

A mechanistic explanation for the relationship between size and rates of biomass-specific photosynthesis is most obvious for aB, due to the effect of pigment packaging on (Kirk, 1975,

1976, 1983; Morel & Bricaud, 1981, see also eq. 1). Since maximum Chl/C ratios also occur at times of G. echinulata dominance (Fig. 8), it can be ascertained that reductions in aB result from reductions in a* , both due to increasing cell/ colony size, an8Lcreases in the concentration of cellular chlorophyll a. In the case of PE,,, cell size and its effect on surface area/volume, are suggested to lead to the observed negative PE,, vs. size relationship by influencing nutrient or CO, uptake (Taguchi, 1976; Cote & Platt, 1983). Large colonial algae such as G. echinulata, may have low values of both PE,, and aB as a result their physical size and structure. The cells in these colonies are so closely packed that it is possible that a significant portion of the internal cells are shaded and have no chance to photosynthesize. Under such circumstances increasing dominance of G. echinulata would lead to reductions in both B a and P:,,, since some chlorophyll a extracted

from the colonies would be from shaded cells that were not capable of photosynthesizing. Paerl (1983) made a similar argument in regard to carbon limited photosynthesis. He demonstrated, by autoradiographic methods, that only the outer layers of large (100 pm-200 pm) Microcystis aeruginosa colonies actively photosynthesize under ambient carbon concentrations, and that the addition of either CO, or HC0,-increased the rate of photosynthesis in the inner portions of the colonies. A similar mechanism could also explain the reduced rates of aB and PE,, in Lake Erken when G. echinulata dominate the phytoplankton. However, this effect would be less pronounced since the alkalinity in Lake Erken is much higher (20 mg C 1- ') than was the case in Paerl's experiments (alkalinity = 1-5 mg C 1- I).

Changes in irradiance exposure also appear to have played a role in regulating short-term variations in biomass-specific photosynthesis, particularly in the case of aB (Fig. 9). Such a relationship is in accordance with equation 1, since increases in irradiance will lead to increases in < (Platt & Jassby, 1976), as a result of decreases in cellular chlorophyll a, changes in pigmentation (e.g. Falkowski, 1980; Richardson et al., 1983), or other factors affecting light harvesting capac-

ity, such as changes in the size and distribution of chloroplasts within the cell (Kiefer, 1973). Ap- parently such adaptation occurs over hourly times scales, as attempts to relate aB to I,, calculated over a 2-4 day interval prior to sampling, rather than on the day of sampling as was done in Fig. 9, were less successful.

The relationship between aB and I,, is not in- variant, or in other words, the relative difference~ between the magnitudes of the two parameters changes through time, even though the timing in their variations correspond (see also Cote & Platt, 1983). Comparison of the 1989 temporal variations in aB with the variations in I,, (Fig. 9) and > 12 pm chlorophyll a (Fig. 7), show short term (daily) variations in aB to be most closely coupled to changes in I , , while longer term (weekly- monthly) changes in aB are more dependent on changes in > 12 pm chlorophyll a. Therefore, the longer term variations in aB resulting from changes in phytoplankton size largely account for the variable nature of the relationship between aB and I,,. Since aB, phytoplankton size, and I,, all tend to covary, the relative importance of variations in irradiance and size, in determining changes in photosynthesis, is difficult to deter- mine. As an example, in 1989 a major decrease in aB and increase in > 12 pm chlorophyll a (Fig. 7) occurred during a decrease in I,, (4-19 July, Fig. 9). This suggests that the correspondence between aB and I,, may at least partly be due to the effect of biomass on I,,. Between 11 and 19 July mean epilimnion chlorophyll a concentrations increased from 5.4 mg rn-, to 21.2 mg m- 3, and at the same time Kd also increased from 0.57 m - ' to 0.8 1 m - ', suggesting the decrease in I,, might be due to the biomass- related increase in Kd. To examine this possibility I,, was recalculated holding Kd constant at its yearly mean value (0.59 m - I ) . These recalculated I,, data (Fig. 9) are little changed from the orig- inal values. The decline in I,, can in fact, be best related to first low surface irradiances (9 E m - d - ' on 1 1 July), and then a decline in Z , from 7 to 12 meters between 11 and 19 July. Changes in the biomass and size distribution of the phytoplankton community may therefore, re-

spond to changes in I , , or some other factor associated with increases in mixing depth or decrease in surface irradiance, but a biomass effect on Kd is not sufficient to explain the aB-I,, relationship.

The relative consistency of IK (Fig. 10) is the result of a number of factors which would lead to a covariation between PE,, and aB. One such factor would be irradiance exposure. As discussed above, aB is expected to be related to changes in irradiance as a result of changes in the absorption cross section of chlorophyll a. PE,,, on the other hand, is not directly dependent on the absorption cross section of chlorophyll a (Platt & Jassby, 1976), but it is clear that changes in PE,, can occur as a positive function of irradiance exposure (Steemann Nielsen et al., 1962; Beardall & Morris, 1976; Cullen & Lewis, 1988). Variations in PE,, are related to factors such as changes in enzyme activities responsible for catalyzing the dark reactions of photosynthesis, changes in the number of photosynthetic units (PSU) or changes in the ratio of photosystem I to photosystem I1 reaction centers (Beardall & Morris, 1976; Falkowski, 1980). Therefore, it is clear that as a result of a number of differing physiological pro- cesses changes in both p:,, and aB are positively related to increasing irradiance exposure. The mechanism that would bring these differing pro- cesses in balance, so as to maintain the consistency of IK is, however, not well understood. The simplest explanation for the covariation of PE, and aB would be the dependence of both of these parameters on changes in algal size and species composition. Indeed, since change in phytoplankton size is a major factor regulating the changes in aB in Lake Erken, it also seems that correla- tions between cell size aB and PE,, may be largely responsible for the consistency of IK. Similar conclusions have been reached by Cote & Platt (1983), and Tilzer & Beese (1988).

The results obtained here do not suggest that changes in the rates of biomass-specific photosynthesis are easily predictable from measurements of temperature or nutrient limitation. While there was an apparent relationship between temperature and photosynthesis in the early summer

of two of the three years studied, the relationship broke down by mid-summer, and the relationship between PEaX and temperature was poorer than others reported in the literature (Jones, 1977; Cote & Platt, 1983; Heyman, 1983; Fee et al., 1987). It was also impossible to find any strong relationship between measurements of biomass-specific nutrient quotas and biomass-specific photosynthesis. This was true both in terms of simple scatter plots (Fig. l l) , or time series plots. The potential relationships between photosynthesis and temperature, nutrients, or light are greatly com- plicated by temporal changes in the composition of the phytoplankton community. The PE,, temperature relationship is masked by the strong seasonal variation in PE,, that corresponds with the G. echinulata bloom in each year. In terms of nutrient limitation, the dominance of G . echinulata coincides with: increases in the transport of inorganic phosphorus to the epilimnion, which leads to a shift from phosphorus to nitrogen limitation (Pettersson, 1980; Bostrbm, 198 1; Istvanovics et al., in press); increased transport of phosphorus to the epilimnion by the G. echinulata colonies themselves (Welsh & Barbiero, 1990; Istvhnovics et al., in press); and a reduction in bacterial production (Bell et al., in prep.). All of the above factors will conceal any simple nutrient quota to photosynthesis relationship, despite the fact that such relationships would be expected to exist, and have been found both in phytoplankton cul- tures (Senft, 1978; Smith, 1983a), and in other lakes (Senft, 1978; Heyman, 1986).

The strongest predictor of either PE,, or aB was biomass. Increases in biomass which corresponded to the blooming of G . echinulata led to significant decreases in both photosynthetic parameters in each year. In fact, this is the one clear pattern that emerges when examining the inter- annual variations in PE,, and aB. Any attempt to improve predictions of biomass-specific photosynthesis in Lake Erken should therefore, take into account the onset and decline of the yearly G. echinulata bloom. To do so, our data indicate that the seasonal development of the lakes thermal structure should be considered.

In 1989 the water warmed to a greater extent

prior to stratification, as a result of clear but windy weather, and this led to higher hypolimnetic temperatures (Fig. 2). Pettersson et al. (1990) suggest that the hypolimnetic SRP concentration of Lake Erken is sensitive to hypolimnetic water temperatures, since the warmer hypolimnetic temperatures in 1989 led to much higher hypolimnetic SRP concentrations (Fig. 2). It appears, however, that a temperature threshold must be passed before sediment SRP loss greatly increases. For example, the 1989 SRP increase was largest, while in 1987 and 1988 there were similar hypolimnetic SRP concentrations in spite of warmer 1987 temperatures. The formation of an anaerobic micro- layer at the sediment surface is one process which could account for such a threshold.

The gradual warming of the hypolimnion (Fig. 2) indicates that there was an exchange of water and nutrients between the hypolimnion and epilimnion during thermal stratification in all years. The magnitude of this exchange increased with time as a result of increasing hypolimnetic SRP concentrations (Fig. 2), and internal SRP loading was greatest in 1989 due to higher hypolimnetic SRP concentrations. The seasonal deepening of the epilimnion allows epilimnetic water to come in direct contact with a greater area of lake sediment (Fig. 13), and the SRP rich water overlying the sediments. In terms of epilimnion- sediment contact it is important to distinguish

Hypsograph~c Curve Lake Erken

Percent Cumulat~ve Area 0 0 200 400 600 800 1000

2 0 4 ! : I ! I 98 85 70 20 1 0

Percent Exposed Accumulation Sedments

Fig. 13. Hypsographic curve for Lake Erken. The top horizontal scale shows the cumulative area of the entire lake basin. The lower horizontal scale shows the cumulative area of exposed accumulation sediments.

between erosion-transportation sediments, and accumulation sediments (HAkanson, 198 1,1982). It is the latter type of sediments which are depos- ited in the deepest parts of the lake basin, and would be of importance in regards to SRP loading, since these are rich in organic matter and nutrients. H&kanson (1982) gave a relationship from which the accumulation sediment area may be estimated. Applying this relationship to Lake Erken suggests that 40 % of the basin area would contain accumulation sediments. From the hypsographic curve (Fig. 13) it can be seen that the deepest 40% of the lake basin, containing the accumulation sediments, would be found at depths of greater than 10.5 meters; therefore, increases in the mixing depth to below this level, would lead to increased transport of SRP and resting G. echinulata cells to the epilimnion. Com- parison of the temperature isotherms (Fig. 1) with the SRP and chlorophyll a data (Figs 3 and 4) shows that decline in mixing depth to below 10.5 meters corresponds to the onset of increasing epilimnetic SRP concentrations, and the blooming of G. echinulata.

The more extensive bloom of G. echinulata which occurred in 1989, can be related to the poorly developed and short lived period of thermal stratification in this year. This resulted in greater levels of internal SRP loading, and a greater transport of resting G. echinulata colonies into the epilimnion. Both of these factors would favour the blooming of G. echinulata. The increased SRP loading resulted in decreases in particulate NIP ratios (Table I), to levels which have been suggested to favour the succession of blue- green algae (Schindler, 1977; Smith, 1983b, 1986). The earlier episodes of deep vertical mixing, may have inoculated the epilimnion with G. echinulata colonies, at a time when conditions were particularly favorable for their growth.

Concerning the role of blue-green algal succession in affecting seasonal variations in PE,, and aB, it is perhaps worthwhile to consider the importance of differing phytoplankton life strategies. Blue-green algae through their buoyancy regulating abilities, are often considered to dominate stable stratified systems, where they can optimize

their vertical position in regard to nutrients and light (Paerl, 1988). Lake Erken, being located near the Baltic coast, is wind exposed. The longest axis of the lake is aligned in the direction of the pre- vailing winds, and the surrounding topography is low. As a result, the lake is susceptible to periodic events of wind induced turbulent mixing, and we suggest that the physiology of the prevalent blue-green algae is largely determined by adaptation to this intermittently turbulent environment. Humphries & Lyne (1988) demonstrated the ad- vantages to be obtained by buoyant species in such an environment, and showed buoyant species to have a greater relative growth rate as a result of their ability to remain in the upper euphotic zone. We concur with this conclusion, and suggest that the large colony size of G. echinulata is an adaptation which allows it to move rapidly (Stoke's Law) to the surface during periods of low turbulence, and may allow it to remain on average higher in the euphotic zone even during mixing (calculations for dinoflagellates show this to be the case, Yamazaki & Kamyowski, 1990). In support of this idea it can be pointed out that G. echinulata never dominated the Erken phytoplankton community until after the period of greatest water column stability when the mixing depth was greater than 10 meters. Thus, at least in this lake, major changes in biomass-specific photosynthesis may not be directly related to light adaptation, but instead driven by the need to maximize size and floating velocity. Large colony size, while advantageous in terms of floating, leads to reductions in rates of biomass-specific photosynthesis. Presumably, however, reduced rates of biomass specific photosynthesis are compensated for by a greater light exposure, and greater cellular chlorophyll concentrations. The role of G. echinulata in regulating rates of biomass-specific photosynthesis in Lake Erken therefore illustrates a potential shortfall in attempts to model algal photoadaptation: namely that adaptation associated with one aspect of the life strategy of a phytoplankton species may affect other aspects (i.e. light adaptation) in a manner that might not be predictable by theories which consider light adaptation in isolation from total life strategy.

Acknowledgements

This work was carried out at the Erken Labora- tory of Uppsala University. Financial support was given by the Swedish Natural Science Re- search Council. Vera Istvanovics visited the Erken Laboratory as a guest researcher on a fel- lowship from Uppsala University. For technical and analytical work we thank Ineke Barten, Rima Abu Middain, and Ulf Lindqvist. The comments and suggestions of Lars Bengtsson and Russell Bell greatly improved an earlier draft of this manuscript.

References

Ahlgren, I. & G. Ahlgren, 1976. Analytical methods for water chemistry (in Swedish) Institute of Limnology, Uppsala University.

APHA, American Public Health Association, 1975. Standard Methods For the Examination of Water and Wastewater. 14'h edn. APHA Washington, D.C.

Bannister, T. T., 1974. Production equations in terms of chlorophyll concentration quantum yield and upper limit to production. Limnol. Oceanogr. 19: 1-12.

Banse, K., 1977. Determining the carbon to chlorophyll ratio of natural phytoplankton. Mar. Biol. 41: 199-212.

Beardall, J. & I. Morris, 1976. The concept of light intensity adaptation in marine phytoplankton. Some experiments with Phaeodactylum tricornutum. Mar. Biol. 37: 377-387.

Bell, R.T., U. Stensdotter, V. Istvinovics, D. C. Pierson & K. Pettersson. Microbial dynamics and nutrient turnover in Lake Erken. Limnol. Oceanogr. (in press).

BostrOm, B., 1981. Factors Controlling the Seasonal Varia- tion of Nitrate in Lake Erken. Int. Revue ges. Hydriolbiol. 66: 821-836.

Cote, B. & T. Platt, 1983. Day-to-day variations in spring- summer photosynthetic parameters of coastal marine phytoplankton. Limnol. Oceanogr. 28: 320-344.

Cullen, J. J. & M. R. Lewis, 1988. The kinetics of algal photoadaptation in the context of vertical mixing. J. Plankton Res. 10: 1039-1063.

Droop, M. R., 1973. Some thoughts on nutrient limitation in algae. J. Phycol. 9: 264-272.

Eppley, R. W., 1972. Temperature and phytoplankton growth in the sea. Fish. Bull. 70: 1063-1085.

Falkowski, P. G., 1980. Light and shade adaption in marine phytoplankton. In P. G. Falkowski (ed.), Primary Produc- tivity of the Sea. Plenum Press, New York: 99-119.

Fee, E. J., R. E. Hecky & H. A. Welch, 1987. Phytoplankton photosynthesis parameters in central Canadian lakes. J . Plankton Res. 9: 305-316.

Harris, G. P., 1978. Photosynthesis, productivity and growth: The physiological ecology of phytoplankton. Arch. Hydro- biol. Beih. Ergebn. Limnol. 10: 1-171.

Harris, G. P., G. D. HafTner & B. B. Piccinin, 1980. Physical variability and phytoplankton communities. 11. Primary production by phytoplankton in a physically variable environment. Arch. Hydrobiol. 88: 393-425.

Healey, F. P. & L. L. Hendzel, 1980. Physiological indicators of nutrient deficiency in lake phytoplankton. Can. J. Fish. aquat. Sci. 37: 442-453.

Heyman, U., 1983. Relationships between production and biomass of phytoplankton in four Swedish lakes of different tropic status and humic content. Hydrobiologia 101: 89-104.

Heyman, U., 1986. The response of photosynthetic parameters to environmental factors in Siggeforasjbn, Sweden. Arch. Hydrobiol. 106: 155-175.

Humphries, S. E. & V. D. Lyne, 1988. Cyanophyte blooms: The role of cell buoyancy. Limnol. Oceanogr. 33: 79-91.

Hikanson, L., 1981. Determination of characteristic values for physical and chemical lake sediment parameters. Wat. Resour. Res. 17: 1625-1640.

H&anson, L., 1982. Lake bottom dynamics and morphom- etry: The dynamic ratio. Wat. Resour. Res. 18: 144-1450.

Istvinovics, V., K. Pettersson & D. Pierson, 1990. Partition- ing of phosphate uptake between different size groups of planktonic microorganisms in Lake Erken. Verh. int. Ver. Limnol. 24: 231-235.

IstvBnovics, V., K. Pettersson, D. C. Pierson & R. Bell, 1992. Phosphorus deficiency as an indicator of algal phosphorus status in Lake Erken during the summer. Limnol Oceanogr. (in press).

Jassby, A. D. & T. Platt, 1976. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol. Oceanogr. 21: 540-547.

Jones, R. I., 1977. Factors Controlling phytoplankton production and succession in a highly eutrophic lake (Kinnego Bay, Lough Neagh). 11. Phytoplankton production and its chief determinates. J. Ecol. 65: 561-577.

Kiefer, D. A,, 1973. Chlorophyll a fluorescence in marine cen- tric diatoms: Responses of chloroplasts to light and nutrient stress. Mar. Biol. 23: 39-46.

Kiefer, D. A. & B. C. Mitchell, 1983. A simple steady state description of phytoplankton growth based on absorbtion cross spectra and quanta efficiency. Limnol. Oceanogr. 28: 770-776.

Kirk, J. T. O., 1975. A theoretical analysis of the contribution of algal cells to the attenuation of light in natural waters 11. Sperical cells. New Phytol. 75: 21-36.

Kirk, J. T. O., 1976. A theoretical analysis of the contribution of algal cells to the attenuation of light in natural waters 111. Cylindrical and spheroidal cells. New Phytol. 77: 341- 358.

Kirk, J. T. O., 1983. Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, New York. 401 pp.

Lewis, M. R. & C. R. Smith, 1983. A small volume, short incubation-time method for the measurement of photosynthesis as a function of incident irradiance. Mar. Ecol. Prog. Ser. 13: 211-221.

Menzel, D. W. & N. Convin, 1965. The measurement of total phosphorus based on the liberation of organically bound fractions by persulphate oxidation. Limnol. Oceanogr. 10: 280-282.

Morel, A., 1978. Available, usable, and stored radiant energy in relation to marine photosynthesis. Deep-sea Res. 25: 673-688.

Morel, A. & A. Bricaud, 1981. Theoretical results concerning light absorption in a discrete medium, and application to specific absorption of phytoplankton. Deep Sea Res. 28A: 1375-1393.

Paerl, H. W., 1983. Partioning of carbon dioxide fixation in the colonial cyanobacterium Microcystis aeruginosa: Mech- anism promoting formation of surface scums. Appl. envir. Microbiol. 1: 252-259.

Paerl, H. W., 1988. Nuisance phytoplankton blooms in cos- tal, estuarine, and inland waters. Limnol. Oceanogr. 33: 823-847.

Pettersson, K., 1980. Alkaline phosphatase activity and algal surplus phosphorus as phosphorus-deficiency indicators in Lake Erken. Arch. Hydrobiol. 89: 54-87.

Pettersson, K., V. Istvanovics & D. Pierson, 1990. Effects of vertical mixing on phytoplankton phosphorus supply during summer in Lake Erken. Verh. int. Ver. Limnol.: 24: 236-241.

Pettersson, K., R. Bell, V. Istvanovics, J. Padisak & D.C. Pierson. Phosphorus status of nano-, ultra-, and bacteri- oplankton in Lake Erken (in prep.).

Pierson, D. C., 1989. The importance of phytoplankton photoadaptation in influencing estimates of integral photosynthesis. Nordic Hydrol. 20: 53-72.

Platt, T. & A. D. Jasby, 1976. The relationship between photosynthesis and light for natural assemblages of coastal marine phytoplankton. J. Phycol. 12: 421-430.

Richardson, K., J. Beardall & J. A. Raven, 1983. Adaptation of unicellular algae to irradiance: an analysis of strategies. new Phytol. 93: 157-191.

Roelofs, T. D. & R. T. Oglesby, 1970. Ecological observa- tions on the planktonic cyanophyte Gloeotrichia echinulata. Limnol. Oceanogr. 15: 224-229.

Sakshaug, E., K. Andresen & D. A. Kiefer, 1989. A steady state description of growth and light absorption in the marine planktonic diatom Skeletonema costatum. Limnol. Oceanogr. 34: 198-205.

Schindler, D. W., 1977. Evolution of phosphorus limitation in lakes. Science 195: 260-262.

Senft, W. H., 1978. Dependence of light-saturated rates of algal photosynthesis on intracellular concentrations of phosphorus. Limnol. Oceanogr. 23: 709-718.

Smith, V. H., 1983a. Light and nutrient dependence of photosynthesis by algae. J. Phycol. 19: 306-313.

Smith, V. H., 1983b. Low nitrogen to phosphorus ratios favor

dominance by blue-green algae in lake phytoplankton. Sci- ence 221: 669-671.

Smith, V. H., 1986. Light and nutrient effects on the relative biomass of blue-green algae in lake phytoplankton. Can. J. Fish. aquat. Sci. 43: 148-153.

Steemann-Nielsen, E., V. K. Hansen & E. G. Jorgensen, 1962. The adaptation to different light intensities in Chlo- rella vulgaris and the time dependence on the transfer to a new light intensity. Physiol. Plant. 15: 505-517.

Strickland, J. D. & T. R. Parsons, 1972. A Practical Hand- book of Seawater Analysis. Bull. 167 Fisheries Res. Bd Ottawa, Canada. 310 pp.

Taguchi, S., 1976. Relationship between photosynthesis and cell size of marine diatoms. J. Phycol. 12: 185-189.

Talling, J. F., 1957. The photosynthetic characteristics of some freshwater plankton diatoms in relation to underwater radiation. New Phytol. 56: 29-50.

Tilzer, M. M., 1983. The importance of fractional light ab-

sorbtion by photosynthetic pigments for phytoplankton photosynthesis in Lake Constance. Limnol. Oceanogr. 28: 833-846.

Tilzer, M. M. & B. Breese, 1988. The seasonal productivity cycle of phytoplankton and controlling factors in Lake Constance. Schweiz. Z. Hydrol. 50: 1-39.

UlBn, B., 1971. Chemical composition of freshwater phytoplankton. (In Swedish). Scripta Limnologica Uppsalien- sia. 270. 12 pp.

Welch, E. B. & R. P. Barbiero, 1990. Sediment to water transport of phosphorus via blue-green algae (abstract only). In The Interactions between sediments and water. Proceed- ings of the 5th Symposium. International Association for Sediment Water Science.

Yamazaki, H. & D. Karnykowski, 1991. The vertical trajec- tories of motile phytoplankton in a wind mixed water column. Deep Sea Res: 38: 219-241.

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