Spring bloom in a hypereutrophic lake, lake Kasumigaura, Japan—I Succession of phytoplankters with different accessory pigments

Water Res. Vol. 17, No. 4, pp. 441-445, 1983 Printed in Great Britain. All rights reserved

0043-1354/83/040441-05$03.00/0 Copyright © 1983 Pergamon Press Ltd

SPRING BLOOM IN A HYPEREUTROPHIC LAKE, LAKE KASUMIGAURA, JAPAN--I SUCCESSION

OF PHYTOPLANKTERS WITH ACCESSORY PIGMENTS

DIFFERENT

HUMITAKE SEKI and ERIKO TAKAHASHI Institute of Biological Sciences, University of Tsukuba, Sakuramura, Ibaraki, Japan 305 (Received March 1982)

Abstract--Phytoplankters appearing during the spring bloom of 1980 in Lake Kasumigaura were classified into three groups characterized by different accessory pigments. Phytoplankters of the first group possess phycocyanin, those of the second group possess chlorophyll b, and those of the third group possess chlorophyll c. Only eucaryotic phytoplankters, belonging to the second or third group, were predominantly present during the bloom. Predominance of the second and third groups alternated during the bloom as individual phytoplankton pulses. The relationship between the population density of all phytoplankters and the abundance of phytoplankters possessing chlorophyll c could be expressed as a highly significant regression curve (r = 0.7997) throughout the spring bloom in Tsuchiura Harbor: Y = 102.9 e -°'°slsax + 29.04, where X is the concentration of chlorophyll a in all phytoplankters in lake water, and Y is the percentage of chlorophyll a possessed by phytoplankters possessing also chlorophyll c.

INTRODUCTION Marked seasonal variation of phytoplankters has been reported for many years in all regions of Lake Kasumigaura (The National Institute for Environmental Studies, 1977, 1979, 1981). Each year, phytoplankters multiply actively in early spring to form a spring maximum in their biomass. This increase in the population density of phytoplankton, called spring bloom, has been known in a number of lakes since the work of Calkins in 1892 (Hutchinson, 1967). In Lake Kasumigaura, the spring bloom is usually smaller than a summer maximum that often merges with an autumnal maximum to form an extraordinarily large bloom. A winter minimum is clearly defined. An early summer minimum, on the other hand, is not always well marked because phytoplankton abundance in the spring and summer blooms are sometimes hardly separable, According to the fragmental data on blooms in Lake Kasumigaura (Fisheries Experiment Station, Ibaraki Prefecture, 1912; Freshwater Fisheries Experiment Station, Ibaraki Prefecture, 1973a, b, 1975, 1976, 1977, 1978, 1979), several pulses with different species of phytoplankters seem to appear alternately in high densities and to comprise apparently one spring bloom each year. The predominant groups of these phytoplankters are observed as diatoms and green algae, with on rare occasions a lesser abundance of blue-green algae at a later period of the bloom. These algae possess accessory pigments in different ratios which may possibly allow their differentiation from each other. A differentiation may be possible by classifying phytoplankters into three 44l

groups characterized by different possession of accessory pigments: Phytoplankters of the first group possess phycocyanin, those of the second group possess chlorophyll b, and those of the third group possess chlorophyll c. A great amount of secondary treated domestic sewage continuously discharged into Lake Kasumigaura in Tsuchiura Harbor (Fig. 1). More than 520 tons of nitrogen and 10 tons of phosphorus flow into the harbor annually as inorganic nutrients. These influxes of inorganic nutrients induce secondary organic pollution, in effect, making the harbor a large continuous culture system of phytoplankton. Tsuchiura Harbor is completely free from littoral vegetation due to the

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embankment. Thus direct impact of nutrient influxes upon the pelagic communities can be precisely studied during a spring bloom, as a typical model among hypereutrophic lakes of the temperate zone. In this report we examine the spring succession of phytoplankters with respect to their accessory pigments. MATERIALS AND METHODS One liter water samples were aseptically collected every 2 days with Hyroht sampling bottles from depths of 0, 10, 25, 50, 100 and 150cm. The lake bottom around the sampling station is flat with approx. 150 cm depth. Phytoplankters were collected onto a Whatman glass fiber filter GF/C by filtration of 200 ml each water sample. Chlorophyll a, b and c possessed by the phytoplankters were measured by the method of Strickland & Parsons (1968), using the formula of Jeffrey and Humphrey (Humphrey, 1976). Phycocyanin was measured by the method of Hattori & Fujita (1959). The same species of predominant phytoptankters could always be found for all samples from different depths at each observation day. Thus the fraction of chlorophyll a possessed in each phytoplankton group was determined using the following formula together with data on the respective concentrations of different accessory pigments in each phytoplankton sample: Chlorophyll a (#g 1 ~) = f t x phycocyanin (/~g I '~) +j2 x chlorophyll b (#gl ~) + .13 x chlorophyll c (pg 1- ~) where,t; is a conversion factor of phycocyanin into chlorophyll a possessed by the blue-green alqae yroup, ,[2 is a conversion factor of chlorophyll b into chlorophyll a possessed by the chlorophyll b 9roup, and f3 is a conversion factor of chlorophyll c into chlorophyll a possessed by the chlorophyll c 9roup. These factors were calculated by the method of least squares (Steel & Tome, 1960) using chlorophyll data from all the depths obtained each observation day. Feb 17 !

RESULTS The variation of chlorophyll concentrations (F'ig. 2) shows that the spring bloom in 1980 started on 24 March and terminated 6 June. During this spring bloom blue-green algal cells were scarcely detected (Hara et al., 1983), but phycocyanin was below the limit of detection. From the nature of chlorophyll variation, the spring bloom separated into four periods; the first period from 24 March to 3 April. the second period from 5 April to 29 April, the third period from 1 May to 17 May and the fourth period from 19 May to 6 June. Around June 6, blue-green algae started to appear and began to increase very quickly. These blue-green algae formed the first pulse of the summer bloom in 1980. Throughout these periods, the conversion factors for chlorophyll b (f2) or chlorophyll c (fa) into chlorophyll a possessed by the chlorophyll b 9roup or the chlorophyll c 9roup, respectively, was almost uniform, i.e. average value in each period of the factor J; was 3.4 (lst period), 2.8 (2nd period), 2.8 (3rd period) and 2.6 (4th period); and that of the factor f3 was 4.6 (lst period), 4.8 (2nd period), 5.0 (3rd period) and 4.0 (4th period). Each factor, J~ or f3, showed very similar values in all periods of the spring bloom. This means that the composition of photosynthetic pigments possessed by phytoplankters of the chlorophyll b 9roup or the chlorophyll c .qroup in the spring bloom was almost uniform. This is in contrast to what was seen in the winter season just before the bloom when .12 and f3 were 0.7 and 1,9, respectively. Phytoplankters in each of these groups, however, have different multiplication rates, thus the species composition of each pulse was various. In this particular case, the fraction of phytoplankton biomass belonging to the chloro-

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Fig. 2. Quantitative variation of phyt~ankton density as indicated by chlorophyll concentrations during the spring bloom in 1980.

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Fig. 3. Percentage of total chiorophylla in the lake water possessed by the chlorophyll c group of the phytoplankton community from 24 March to 3 April. Each circle shows the value measured for each sample. The direction of arrow shows variation of the percentage as the time elapsed from the beginning to the end of the period.

phyll b group and the chlorophyll c group was almost

uniform during each of the four periods. It was possible to subdivide each period further into shorter intervals of smaller phytoplankton pulses. This was apparent when phytoplankton maxima were indicated by the percentage of total chlorophy,ll a in the lake water possessed by the chlorophyll c group of the phytoplankton community in each period (Figs 3-6). The change in this percentage during the growth phase of phytoplankton pulse can be traced by the direction of an arrow which is drawn through the mean concentration for various sampling days. The circular movements of the arrow even within one period may be caused by two reasons: firstly, there could be more

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Fig. 5. Percentage of total chlorophyll a in the lake water possessed by the chlorophyll c group of the phytoplankton community from 1 May to 17 May. Symbols are as in Fig. 3.

than one phytoplankton pulse during the period; secondly the chlorophyll estimate was for samples collected from one geographic location whereas the phytoplankton bloom or patch may have been carried to and fro past the sampling site, thereby the samples could come from different parts of the same bloom. The percentage of the chlorophyll c group in the plankton community was greater during the first (average: 72~) and the third (average: 62%) periods, whereas it was smaller during the second (average: 58~) and the fourth (average: 42~o) periods. Statistical analysis shows that the chlorophyll c group was especially evident during the first period of the bloom (F = 26.47, F[35, 228: 0.01] = 1.7). The predominance during the third period, on the other hand, was as marked as that during the first period, but it was still highly significant (F = 6138). The abundance of the chlorophyll c group in the plankton community reveals that this group may be more predominant at a lower population density of the phytoplankton pulse. Thus a highly significant regression (r -- 0.7997) was obtained for the spring bloom in the relation of abundance of the chlorophyll c group in the population density of all phytoplankters (Fig. 7): Y = 102.9e -°'°31asx + 29.04

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Fig. 4. Percentage of total chlorophyll a in the lake water possessed by the chlorophyll c group of the phytoplankton community from 5 April to 29 April. Symbols are as in Fig. 3.

where X is the concentration of chlorophyll a possessed by all phytoplankters in lake water, and Y is the percentage of chlorophyll a possessed by the chlorophyll c group. This relationship could be possible only when the abundance of each phytoplankton group was at the same population density level of any plankton pulse during the spring bloom. DISCUSSION Phycocyanin is an accessory pigment possessed by

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Fig. 6. Percentage of total chlorophyll a in the lake water possessed by the chlorophyll c group of the phytoplankton community from 19 May to 6 June, Symbols are as in Fig. 3.

Cyanophyta, Cryptophyta and Rhodophyta in the biosphere. In Lake Kasumigaura, Cyanophyta is exclusively responsible for this pigment. Cyanophyta. i.e. blue-green algae, emerged early in the history of the evolution of creatures. Chlorophyll b is possessed by Chlorophyta and Euglenophyta. Both taxa are represented among the phytoplankters in Lake Kasumigaura. Chlorophyll c is possessed by Bacillariophyta, Phaeophyta, Pyrrophyta and Cryptophyta. The appearance of Bacillariophyta. i.e. diatoms, is believed to be the latest event among phytoplankters existing in the biosphere to be able to support the most energy requiring ecosystem IParsons. 19791. Thus, the transition from blue-green algae to diatoms

has involved the incorporation of new pigments which offer the plants high efficiency in gathering solar energy for photosynthesis, This in turn has led to ecological modification of an aquatic ecosystem from the energy-poor to the energy-rich level (Parsons, 1979l. On the other hand, Lake Kasumiguara has been an eutrophic lake for hundreds of years (Seki. 1974). This means that the phytoplankton communities in the lake have been exposed for hundreds of years to an energy-rich aquatic ecosystem. In recent decades, the process of eutrophication has been accelerating with additional enrichment of agricultural and domestic wastes by human activities to the lake (Seki et al.,

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Spring bloom in Lake Kasumigaura--I 1979). The phytoplankton community presently in Lake Kasumigaura might be expected to have acclimatized to an enriched environment and thus might be expected to exhibit a characteristic annual cycle in the succession of species from advanced to primitive. In the annual cycle of 1980, it was obvious that eucaryotic phytoplankters were exclusive components of the spring bloom. The population density of procaryotic phytoplankters, i.e. blue-green algae, was below the level of detection by traditional standard methods in biochemistry. In the earliest phase of the spring bloom in 1980, phytoplankters possessing chlorophyll c quickly appeared and became predominant. Although they persisted as the dominant taxa only for a very short time, the appearance of these advanced algae in the biosphere at the first phase of the bloom is provocative, especially at the environment of Lake Kasumigaura is referred as that of the final stage of life progress of a lake. The first phase of the bloom should be free from strong biotic interactions, and may be only regulated by abiotic factors. Once the environment becomes occupied by a high density of phytoplankters the environmental conditions become highly dynamic (Seki et al., 1980) and the phytoplankton community may have become composed of phytoplankters at various levels of biochemical evolution.

Acknowledgements--The authors wish to thank Drs T. R. Parsons and R. J. LeBrasseur for valuable comments. This work was partly supported by a special research project of the Ministry of Education of Japan (203012).

REFERENCES

Fisheries Experiment Station, Ibaraki Prefecture (1912) Report on fisheries in Lake Kasumigaura and Lake Kitaura 1, 1-259. Freshwater Fisheries Experiment Station, Ibaraki Prefecture (1973a) Report on limnological observation in Lake Kasumigaura and Lake Kitaura. 1-137. Freshwater Fisheries Experiment Station, Ibaraki Prefecture (1973b) Report of Freshwater Fisheries Experiment Station, Ibaraki Prefecture. 11, 1-40. Freshwater Fisheries Experiment Station, Ibaraki Prefecture (1975) Report of Freshwater Fisheries Experiment Station Ibaraki Prefecture. 12, 1-140.

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Freshwater Fisheries Experiment Station, Ibaraki Prefecture (1976) Report of Freshwater Fisheries Experiment Station, Ibaraki Prefecture. 13, 1-101. Freshwater Fisheries Experiment Station, Ibaraki Prefecture (1977) Report of Freshwater Fisheries Experiment Station, Ibaraki Prefecture. 14, 1-89. Freshwater Fisheries Experiment Station, Ibaraki Prefecture (1978) Report of Freshwater Fisheries Experiment Station, Ibaraki Prefecture. 15, 1-101. Freshwater Fisheries Experiment Station, Ibaraki Prefecture (1979) Report of Freshwater Fisheries Experiment Station, Ibaraki Prefecture. 16, 1-225. Hara Y., Tsuchida A. & Seki H. 0983) Spring bloom in a hypereutrophic lake, Lake Kasumigaura, Japan--II. Succession of phytoplankton species. Water Res. 17, 447-451. Hattori A. & Fujita Y. (1959) Crystalline phycobilin chromoproteids obtained from a blue-green alga, Tolypothrix tenuis. J. Biochem. 46, 633-644. Humphrey G. F. (1976) The concentration of phytoplankton pigments in Australian waters. CSIRO Marine Biochemistry Unit, Annual Report 1975-76, 16-21. Hutchinson G. E. (1967) A treatise on limnology. Introduction to Lake Biology and the Limnoplankton, Vol. 2, 1115 pp. Wiley, New York. Parsons T. R. (1979) Some ecological, experimental and evolutionary aspects of the upwelling ecosystem. South Af. J. Sci. 75, 536-540. Seki H. (1974) Lake Kasumigaura. Survey of lake rehabilitation techniques and experiences. Technical Bulletin. Department of Natural Resources, Madison, Wisconsin 75, 56. Seki H., Takahashi M. & Ichimura S. (1979) Impact of nutrient enrichment in a waterchestnut ecosystem at Takahama-iri Bay of Lake Kasumigaura, Japan. I. Nutrient influx and phytoplankton bloom. WASP 12, 383-391. Seki H., Takahashi M., Hara Y. & Ichimura S. (1980) Dynamics of dissolved oxygen during algal bloom in Lake Kasumigaura, Japan. Water Res. 14, 179-183. Steel R. G. D. & Torrie J. H. (1960) Principles and Procedures of Statistics, 481 pp. McGraw-Hill, New York. Strickland J. D. H. & Parsons T. R. (1968) A Practical Handbook of Seawater Analysis, 2nd Edition, pp. 1-311. Bulletin of the Fisheries Research Board of Canada. The National Institute for Environmental Studies (1977) Man activity and aquatic environment--with special references to Lake Kasumigaura. L R-1-'77, 1-145. The National Institute for Environmental Studies (1979) Man activity and aquatic environment--with special references to Lake Kasumigaura. II. R-6-'79, 1-420. The National Institute for Environmental Studies (1981) Man activity and aquatic environment--with special references to Lake Kasumigaura. III. R-19-'gl, 1 150.