A Freshwater Red Tide on a Water Reservoir

Jap. J. Limnol. 36, 2, 55-64, 1975.

Nobutada NAKAMOTO

Abstract

A long-lived, heavy freshwater red tide of Peridinium occurred in a newly built water supply reservoir, between late February and late May, 1972 and 1973, starting and spreading from the entrance region. The densities of the alga reached at least 9.3 x 104 cells per ml and at least 2, 700 ƒÊg chlorophyll-ƒ¿ per liter at a winddrift. The red tide is attributed to the increase of solar radiation, the hardness of water and the sewage drains from towns and croplands. The water mass containing a dense algal bloom was an excellent receiver of the solar radiation. This flagellate acted as an accumulater of nutrients at the entrance region of the reservoir.

reservoir from late February to late May. Introduction A striking coffee brown color appearance A heavy freshwater red tide on a newly- of water was caused by a dense algal bloom made water supply reservoir was observed. of Peridinium sp. which has coffee brown In Japan a lot of dams have recently been pigments consisting of xanthophyll. The built for the purpose of mainly stocking dense Peridinium bloom produced several water. However, the changes of the water complaints of local inhabitants who thought quality while reserving water have largely the brown color of water to be due to raw been ignored in the planning and building sewage from a gas station, as occurred in of the reservoir. the case of Clear Lake, California (HoRNE In 1968 a fairly large reservoir was made et al. 1971). for the purpose of supplying water mainly The present report concerns a description for Tokyo City, by damming a tributary of the algal bloom and the possibilities of of the River To-ne which has the largest its occurrence. watershed in Japan. The area of the water- Method shed of this reservoir is 322.88 km2. The reservoir, Lake Kanna-ko, is made behind Chlorophyll Determination the Shimokubo Dam (36°37'N, 139°02'E) of Chlorophyll a was estimated spectrome- 129 meters high, and is located at the west trically by extraction of pigments with 90 edge of the Kanto plain. Lake Kanna-ko per cent aqueous acetone (STRICKLAND and is possible to hold 130, 000,000 tons of water, PARSONS, 1968). Chlorophyll was estimated and when its high water level is reached, in situ using an instrument (Variosense its surface level is 296.8 meters above the Type II, Impulsphysik GmbH) on a boat. sea. Its length is about 10 kilometers and The principle method of this instrument is is slender in shape. a fluorometric determination. The exitation In 1972 and 1973, a heavy phytoplankton of chlorophyll pigments is made by a flash bloom was seen for the first time in this beam through a broad band filter (Balzer 56 A Freshwater Red Tide on a Water Reservoir

450/530 nm) using a xenon lamp (Fx 134). The fluoresence radiation occurred is de- tected by a receiver through a narrow band filter (Schott Al 675 nm). Particle Size Distribution Particles in water such as phytoplankton and silt were measured and counted by an electric particle counter (COULTER Counter Model B). Chemical Analysis Total phosphorus content was determined by a wet digestion method (MENZEL and CORwIN, 1965). Particulate carbon and nitrogen were determined by a CHN ele- mentary analyzer (YANAGIMOTO, MT-2). The total carbon dioxide content was determined by an infra-red gas analyzer (SATAKE et al. 1972).

Results and Discussion Description of Peridinium Bloom

The red tide was observed for the first Fig. 1. Spreading pattern of Peridinium red tide time in late February 1972 as a clear patch in the surface layer of Lake Kanna-ko of a coffee brown coloration extending during late February to early May, 1973. some 20 to 40 meters off the entrance of the reservoir in spite of a water temperature sevreal strips of coffee brown coloration as low as 5°C. In April the coloration were seen on a windy day during the extended toward the dam site as the water blooming period. In April, in some places, temperature became warmer. Peridinium the heavy algal blooms were observed at disappeared in late May 1972. In 1973, the winddrif is of the inlets where the Peridinium was seen in almost the same transparency was only 5 centimeters deep. period as the spring overturn (Fig. 1), and At some heavy winddrifts fed by small the bloom always began at the entrance of streams which pass through a settlement, the reservoir. The coffee brown coloration the high cell density was recorded at 9.3 due to algae was always observed at this x104 cells per ml. Such a high density of region during the long blooming period. Peridinium may be the highest record in The cell density of Peridinium at this area a natural environment in the world. During was more than 104 cells per ml, and this heavy blooming period, other phyto- declined toward the dam site. The alga plankton and zooplankton were scarcely had a tendency to crowd beneath the found in net-samples, only a number of surface. It readily floated with the surface copepods being observed at the end of the water when blown by the wind. Thus the Peridinium bloom in May. NAKAMOTO 57

Fig, 2, A record of chlorophyll distribution in the surface layer using an in situ measurement instrument. This is a record of about 200 meters' run.

The strips of Peridinium patch on the time. The cells in resting or in a bad surface of the water were confirmed by a condition tend to remain further beneath recording from a chlorophyll in situ the surface. Therefore, the brown colora- measurement instrument on a boat. The tion in the layer was seen deeper in the result is shown in Fig. 2. The instrument afternoon than in the morning. This pheno- was placed on the side of a boat just menon was created by the vertical migra- beneath the surface (about 15 centimeters tion of this flagellate. Under natural deep). The boat then progressed across the conditions, the cell division of Peridinium patches. The patches were very remarkable. occurs only at night (SWEENY and HASTING, There were seen on the lake surface many 1962). The coffee brown coloration was streaks which might have been caused by also deeper in the afternoon on a fine and the wind on that day (LANGUMIR, 1.938). warm day. The vertical movement of this The highest value of chlorophyll concen- alga was clear in the middle of the reser- tration in Fig. 2 is about 300 ig of chloro- voir. This migration phenomenon became phyll a per liter and the minimum about indistinct toward the dam site. During the 20. This chart records approximately 200 heavy blooming period in late April the meters of the algal patches. The differences transparency was about 2 meters in the of more than 10 times in chlorophyll con- clearest area near the dam site, while the centrations at the center and the perimeter average transparency was about 1.5 meter of the patches were observed in some at this time. This Peridinium bloom began places. The size and length of patches to occur just at the early spring overturn, varied greatly. This alga shows phototaxis and was spreading with the increase of with an action spectrum that has a peak solar radiation. Fig. 3 shows the daily of 475nm (ROUND, 1965). The living cells means of the global solar radiation at about are apt to rise near the surface in the day 28 kilometers north of the dam site. These 58 A Freshwater Red Tide on a Water Reservoir

Fig. 3. Global solar radiation profiles. Fig. 4. Schematic pictures of water invasion at the entrance region. Hatched areas indicate the blooming water masses of data were obtained from the Japan Meteo- the reservoir, a : in the morning, rological Agency's monthly report. The b : in the afternoon radiation increases from January till the middle of May, while in June and July it turbidity of the water sample taken from rapidly decreases due to the rainy season. the deep layer beneath the blooming water, The decrease of radiation continues until the mass of which ran just over the December. inflowing water mass. The edge of coffee brown coloration of phtytoplankton was Diurnal Change at the inflow Region observed at the inflow mouth of the influx. A clear border at the inflowing region On April 13th, however, such a phenomenon was usually observed between the bloom- at this place was the same in the morning ing area and the inflow during a blooming (Fig. 4a), but the border did not clear in period. This border was clear all the day the afternoon (Fig. 4b). The border went except at the end of the blooming period. back some 50 meters toward the dam site. In April and May, however, this border It seems that the inflowing water streamed was not visible in the afternoon. It seemed under the blooming water in the morning to be caused by the difference of the specific and ran over the blooming water mass in gravity which depends on the difference in the afternoon (Fig. 4a and b). The tem- the temperatures of the inflowing water perature of inflowing water was 13°C in mass and the blooming water mass. This the morning and of the blooming area was phenomenon which is shown schematically 14°C. As the diurnal change in the tem- in Fig. 4 a and b was observed by insight perature of this inflow stream was greater and measuring the temperature. On March than that of the water mass of the reser- 2nd, the temperature difference of both voir, the stream water ran over the border water masses was observed from a boat of coffee brown coloration in the afternoon. while crossing the border between the In this manner the border drew back. inflowing water mass and the blooming water mass. The temperatures at noon Cell Size of Peridinium were 4°C and 5-7°C, respectively. The The cell size of Peridinium is 20 to 50 phenomenon was also confirmed by the microns in diameter. They tend to colonize, NAKAMOTO 59 form patches, and rise toward the lent to diameters of 2' or 1/3 ~b increments. surface in day time. The density of its The ordinate represents by an arbitrary cells in the surface layer is very high. A unit a linear scale of the concentration of surface water sample was taken from the particles in one size interval. There was bloom region in the evening of March 3rd, an abundance of colloidal particles which the water temperature being only 6°C. caused a milk-white color in the stream The size distribution of particles was water. There were also big particles of measured and counted with a COULTER Peridinium cells which were observed only Counter (SHELDON and PARSONS, 1967) microscopically. Some small ciliate swam, within 6 hours after collection. As this however, across the view of the microscope. instrument requires that the particles be The ordinate of Fig. 5 expresses the volume suspended in an electrolytic solution, one in intervals of one particle size. Fig. 5a gram of NaCI was added to one liter of the shows the abundance of smaller particles. sample. To prevent the cell destruction by Peridinium size range particles were not the change of osmotic pressure caused by so abundant in this water mass. This large the electrolyte, a small amount of formal- fraction of particle spectra was dependent dehyde solution was added as a fixer. on the white-milk colloidal substances. The results show in smoothed size- There was a slight shoulder in the range frequency polygons (Fig. 5). The size incre- of particles which were 10 to 16 microns ment (abscissa) is logarithmic and follows in diameter. There is also a peak in the a series of V, 2V, 4V, where V is an Peridinium population which ranges from individual particle volume, which is equiva- 20 to 50 microns. In the case of a natural

Fig. 5. Particle size distribution, a : The relative numbers of particles in the surface water. The hatched areas show the biological fractions. The samples was taken on March 3, 1973. The sampling site was indicated by x on the map. The water temperature was 6.0°C, b : The relative volume concentration in each size interval of particles. There are two peaks depended on biological substances (hatched areas). The large peak depends on Peridinium population which cell diameter is 20 to 50 microns. 60 A Freshwater Red Tide on a Water Reservoir

particle spectrum by number, a shoulder in Fig. 6a is from a winddrif t located usually depends on bio-particles such as about 2 kilometers down from the entrance. phytoplankton cells. Fig. 5b shows the In this patch the transparencey was astoni- particle spectrum by volume in each size shingly low. It was only 5 centimeters in interval, and is a fine expression of natural the afternoon (3 : 45 p. m.) on April 14th, particles pattern. There are two clear 1973. The surface temperature was 20°C. peaks of Peridinium cells, the large one Only 5 meters away from this patch the of which was confirmed by microscope. temperature was 17.2°C. At that time the The causes of the small peak were not temperature of the inflowing stream was clear. It may probably depend on the ciliate 15.6°C. This indicates that the alga acted or the discarded shell of the Peridinium's as a heat trap and that the water mass cell division. Anyway such a peak depends must have been fairly stable. Fig. 6b on living substances in an aquatic environ- shows another patch which was situated ment. It is clear that the Peridinium cells about 2 kilometers from the dam site on occupied a large portion of particles. the same day. In this patch the surface temperature was 15.7°C, and the trans- Peridinium Bloom as a Heat Trap parency was only one meter. These data The turbid water containing coffee brown seem to indicate that the water masses do colored Peridinium is as a solar radiation not mix easily with each other and are heat trap. A difference of 3°C in the patch fairly stable. There were just a lot of was observed in comparison to the water water masses. Furthermore, the fact that at a winddrif t. Fig. 6a and b show the Peridinium cells come together by photo- clear evidences of the heat trap. The data taxis near the surface makes the action of a heat trap likely.

Specific Nature of This Watershed

In Japan dams have been made in the mountains in the past. Shimokubo Dam (Lake Kanna-ko), however, is one of the first attempts to build under mountain villages. There are in the watershed three villages, the total population of which is about ten thousands. The croplands occupy only 2.4 percents of the watershed, while 90 percents are woodlands. The crop- Fig. 6. Temperature profiles of inside ( i) and lands and homesteads lie along the river. outside (o) of two patches on April 13, The farms cultivate mainly vegetables and 1973, a : one of the winddrifts near the mulberry trees which require much fer- entrance region. Arrow indicates the temperature of the inflow stream. The tilizer. They also rear domestic fowls and transparency in this patch was 0.05 m. pigs. The domestic wastes and the drainage b : one of the patches on the center of the reservoir. The transparency in this from the croplands flow into the reservoir patch was 0.9 m. through the river. Thus the watershed NAKAMOTO 61 appears to contain a great amount of are high in the stream water, showing the nutrients (NAKAM0T0, 1973). In fact, there EDTA hardness of the water about 100 ppm is enough nutrients to permit algal growth. as calcium carbonate. The total carbon Most of the man-made reservoirs hitherto dioxide concentration was 52 mg C02/l. built in Japan were situated among the The domestic waste and the cropland drains mountains. There were fed only by the are mineralized by bacterial activity in the drainage from woodlands, so that there hypolimnion of the reservoir during the were a lack of nutrients to bring about a long resident time. Calcium then contri- heavy algal bloom. Those reservoirs are butes to the formation of calcium phosphate considered as oligotrophic or mesotrophic. compounds which are easily precipitated. Further, Lake Kanna-ko has the large As this factor should also coprecipitate with capacity for the watershed. This region in the nutrients, various deposits drained from Japan has less precipitate, the annual rain the watershed such as silt, gravel and fall being recorded at about 1, 000 mm. organic debris are abundant at the entrance The annual drain is only about 1.5 to 2 region, and should decline toward the dam times of the reserve capacity (130, 000, 000 site. In contrast to an ordinary fan-shaped tons). Therefore, the resident time of water watershed, this watershed is very long and is very long, and the current speed of water slender. Since this area has only little rain in the reservoir is extremely slow. From fall, the temperature of the inflowing such evidences, this reservoir would appear stream is relatively higher than that of the to be an excellent nutrient trap (HYNES, streams flowing into other mountain reser- 1960). voirs. The temperature of the inflowing There are two big stalactite caves on stream is usually lower than the surface account of a lime stone zone crossing the temperature of a mountain reservoir during watershed. Therefore, the concentrations of most of the year. The stream flows into calcium ion and clacium carbonate particles the layer which has the same specific

Fig. 7. The iso-thermal profile of the dam site in 1972. A thick line indicates the depth of the same temperature as the inflow stream. The outlet of the reservoir is indicated by an arrow. 62 A Freshwater Red Tide on a Water Reservoir gravity as that. In the reservoir under water of an oligotrophic lake in Japan consideration, the stream has a tendency (SAKAMOTO, 1966). However, the chloro- to inflow the surface layer until May due phyll concentration in this spring outburst to its high temperature. Fig. 7 shows the was extremely high, comparable to the iso-thermal profile at the dam site indicating most polluted lake water. The maximum the varying temperatures of the inflowing concentration recorded was 2,700 pg chl.-a stream. An artificial water reservoir essen- /l at an inlet on April 14. Near the tially differs from a natural lake in that its entrance region the average concentration water exit is near the bottom. The surface was more than 110 pg chl.-a/l in the water is heated by solar radiation. A hori- surface water and that near the dam site zontal change in the surface temperature was about 20 ,ug chl.-a/l on April 23rd. was observed from the river mouth to the Fig. 8 shows the veritcal profiles of chloro- dam site. After the circulation of water, phyll concentrations and temperature. the algal bloom began to grow at the beginning of the thermal stratification. The bloom grew correspondingly to the rise in the water temperature and the increase in solar radiation (Fig. 3). Phytoplankton which can grow at low temperatures under natural conditions are Euglenophyta, Chry- sophyta and Bacillariophyta. The former two classes are usually able to utilize organic matter. Two kilometers up the river from the reservoir there is a town, the population of which is about 4,000. Therefore, organic wastes from the town will be also drained. The ecological evidence assembled by HALL (1928) suggests that within larger genera of Dinophyceae there are different species adapted to acidic, calcium-deficient and alkaline, and calcium-rich waters as well as crabonates to support a heavy photosynthetic algal bloom. Fig. 8. Vertical profiles of the chlorophyll Peridinium as a Nutrient Accumulator amount and the temperatures at two stations on April 23, 1973. There is no answer to the question why the algal bloom started at the entrance It is difficult to explain why only a dino- region in such a heavy state. On the other flagellate, Peridinium, may have been hand, the range of total phosphorus content credited with the ability to flourish in and in the inflowing water was 0 0078 - 0.10 utilize the extremely low concentration of mg/l. Such concentrations are equal to the nutrients. The water with 2, 700 ,ug chl.-a/l NAKAMOTO 63 contained 9.3 x 107 cells/l of Peridinium. flows over. After stratification is established The concentrations of C, N and P (mg/l) the cool stream water flows to the bottom or in the suspended matter of this water are into the layer which has the same specific 110, 8. 24, and 1. 5, respectively. Anyway gravity. Compared with a natural lake, the the atomic ratio of Peridinium cell is water in the surface layer of a man-made almost the same as other plankton (SVER- reservoir has a long resident time, and DRUP et al, 1942). The presence of motility accordingly the phytoplankton living in the in dinoflagellates, and its absence in diatoms, surface layer remains in that layer after may have an important bearing in the the completion of the thermal strati- relationship of these organisms with such fication. Near the entrance region, fresh environmental conditions as temperature nutrients are always supplied from the and the nutrient concentrations of water watershed. Therefore, the algae grow (RYTHER, 1955). RYTHER considered three rapidly in this region and the standing caces of the occurence of red tides in the stock of phytoplankton declines from the oceans. In Lake Kanna-ko, the bloom is entrance region to the dam site. Flagellate almost the same as the pattern of a red having a motility can easily collect the tide in the vicinity of a river mouth. The fresh nutrients. These phenomena seem to surface water at the entrance region of the be a general feature of man-made reservoirs. reservoir is heated by the solar radiation, The specific nature of the watershed of this its temperature being slightly warmer than reservoir would tend to promote the heavy the inflowing stream in late February. The algal bloom. water stratification began at this time. Acknowledgements Then Peridinium bloom was observed in the vicinity of the river mouth. There were The author should like to express his sincere also large quantities of floating materials thanks to Prof. K. HOGETSU and the members of in this vicinity. Ecological, Microbial Chemistry, and Analytical According to THRONDSEN (1973), the Chemistry Laboratories of Tokyo Metropolitan relative swimming speed of marine flage- University, and many members of the Environ- mental Research Group of Nomura Research llates varies from 25 to 50 cell length per Institute, for their kind assistance during the second. The diameter of Peridinium of work in the field and the laboratory. Thanks for Lake Kanna-ko is about 20 to 50 microns. help of various kinds are also due to Mr. A. If this flagellate could swim by the above MATSUBARA, head of the control office of speeds, the speed should be 1.8 to 9.0 Shimokubo Dam, the Public Corporation of Water meter per hour. Peridinium at this bound- Resources. ary can catch the nutrient by the migration which flows into the reservoir. It grows 摘要 rapidly and makes a heavy bloom. Its 神流湖における淡水赤潮の発生について motility is effective in collecting the nutrient. 東京都民のための水源池として,1968年に利根川 Peridinium acts as a collector of nutrients の支流を堰き止めて,神流湖という貯水池を造った. at this region. 貯水を始めて数年しかたっていないにもかかわらず, Inlets and outlets of natural lakes are 春先から夏にかけて,長期間にわたって,鞭毛藻類の near the surface, so that the surface water ペリディニウムの大発生による淡水赤潮現象が見られ 64 A Freshwater Red Tide on a Water Reservoir

た.ペリディニウムの発生は,流入口から始まり,だ water conditions, in F. H. JOHNSON(Ed.), んだんと,ダム湖に向って広がっていった.場所によ The Luminescence of Biological Systems. っては,細胞数は9.3×104cells/m1にも達し,また, SAKAMOTO,M. (1966) : Primary production by クロロフィル量は2,700μ9パ1にも達した.この大発 phytplankton community in some Japanese 生は,太陽の輻射の増加に伴って発達していった.こ lakes and its dependence on lake depth. の大発生は流入水が炭酸カルシウムが多いことや,町 Arch. Hydrobiol., 62: 1-28. や農耕地からの流入水に起因している.流入口に植物 SATAKE,K., Y, SAIJO and H. TOMINAGA(1972) : プランクトンが発生するためには,鞭毛を持つ生物の Determination of small quantities of carbon 方が,流入してくる栄養i塩の利用という面で有利であ dioxide in natural waters. Jap, J Limnol., ることが推測された. 33: 16-20. SHELDON,R. W. and T. R. PARSONS (1967) : A References Practical Manual on the else of the Coulter HORNS, A. J., P. JAVORNICKYand C. R. GOLDMAN Counter in Marine Science. Coulter Electronics (1971) : A freshwater `Red Tide' on Clear Toronto, 66pp, Lake, California. Limnol. Oceanogr., 16: STRICKLAND,J. D. H, and T. R. PARSONS(1968) : A 684-689. practical handbook of seawater analysis. BOLL, K. (1928) : Oekologie der Peridineen . Pflan- Bull. Fish Res. Bd. Can., 167: 311pp. zenforschung, Heft 11, 105pp. SVERDRUP,H. U., M, W. JOHNSONand R. H. FLEMING HYNES, H. B. N. (1960) : The Biology of Polluted (1942) : The Oceans., 1, 087pp. Prentice-Hall, Waters., Liverpool University Press, 216pp, Inc. LANGMUIR,I. (1938) : Surface motion of water SWEENY,B. M. and J. W. HASTING(1962) : Rhythms, induced by wind. Science, 87: 119-123. In K. A. LEWIN (Ed.), Physiology and Bioche- MENZEL, D. W. and N. CORWIN(1965) : The mea- mistry of Algae., Academic Press. 929pp. surement of total phosphorus in sea water THRONDSEN,J. (1973) : Motility in some marine based on the liberation of organically bound nanoplankton flagellates. Norw. J. Zool., 21: fractions by persulfate oxidation. Limnol. 193-200. Oceanogr., 10: 280-282.

NAKAMOTO,N. (Dec. 1973) : Multi-purpose dam (著者:中本信忠,東京都立大学理学部生物学教室,

and water pollution. A-o to Midori, 2 (12) : 東京都世田谷区深沢2-1-1;NobutadaNAKAMOTO,

25-29. (in Japanese) DepartmentofBiology,FacultyofScience,Tokyo

ROUND,F. E. (1965) : The Biology of the Algae . MetropolitanUniversity,Fukazawa,Setagaya-ku,

Edward Arnold. 269pp. Tokyo158,Japan) RYTHER, J. H. (1965) : Ecology of autotrophic marine Dinoflagellates with reference to red