In Lake Biwa, restoration of water quality was achieved through the control of phosphorus discharges from the drainage basin. Recently, additional concerns have arisen regarding accelerating hypolimnetic deoxygenation and changes in the flora and seasonal periodicity of phytoplankton. Based on the analysis of the monitoring survey data, the effects of the changes in lake water mixing due to global warming on phytoplankton dynamics were examined using the seasonal [NO3] changes in surface water as a marker of the vertical mixing of water column. Autumnal increases in the surface water [NO3] started one month earlier after 1990. It was concluded that earlier onset of the fall overturn after 1990 was due to warming of the hypolimnion by warm winters after 1990. Because of diverse impacts of climate change and anthropogenic activities on lakes, and less predictability of their cumulative effects, increased knowledge of these effects is an urgent requirement for the progress of limnological science under global warming.
For the last half century, considerable advances have been made in the understanding and management of lake eutrophication. The development and application of the phosphorus loading model by Vollenweider (1976) to control lake eutrophication was especially important. Designation of phosphorus as the major target of eutrophication control after the intensive experimental studies by Schindler and his colleagues (Schindler et al., 1971, 1973) made an effective contribution to solving the problem of eutrophication in the world's lakes. There are still many cases where rehabilitation of eutrophied lakes has not occurred because of inffective control of nutrient supply from diffused sources and/or from sediments (Sondergaard et al., 2001). Recently, concern has been rising about the additional effects due to global warming on lake ecosystems (Schindler, 2006; Kumagai, 2008). Because of local variation in global warming and lake characteristics, the combined effects of eutrophication and global warming on a lake are currently less predictable. To increase our understanding of these effects, we need to increase the information of lake responses to the external impacts in a variety of lakes as indicated in Vollenweider's eutrophication studies. As a step toward this goal, this paper examines the effects of global warming on the pelagic system in Lake Biwa.
Study lake and data analysis
Lake Biwa is a representative large lake where eutrophication control by phosphorus reduction has been successfully achieved. The lake is located in central Japan and has a surface area of 670 km2, maximum depth of 104 m, volume of 27.5 km3 and water residence time of 5.5 yr. The lake comprises a large and deep North Basin (mesotrophic), and a small and shallow South Basin (eutrophic). The upper water column of deep North Basin is thermally stratified from early April to September and characteristic phytoplankton flora is developed.
Through 1960–1980, the lake suffered from increased eutrophication due to increasing discharge of sewage and polluted waters from the drainage basin. Massive development of freshwater red-tide by Uloglena americana in 1977 resulted in considerable impacts on the local societies around the lake and forced the government to take effective countermeasures to control eutrophication. In 1979, the government enacted the Ordinance for Prevention of Eutrophication of Lake Biwa including the legal regulation of nitrogen and phosphorus discharge from domestic and industrial sources. Considerable efforts have also been made to install sewage systems to reduce the waste water discharge from urban, industrial and agricultural communities. These actions were effective in reducing phosphorus discharge into the lake and resulted in a gradual recovery of lake water quality after the mid 1980s (Shiga Prefecture, 2008).
Despite a partial recovery from eutrophication, several unfavorable effects have been observed in Lake Biwa. The decreasing hypolimnetic dissolved oxygen concentration in the North Basin is one concern. Based on the intensive survey and data analysis, Kumagai (2008) reported that incomplete winter mixing of the whole water column due to global warming was largely responsible for increased deoxygenation in the hypolimnion of the North Basin. Considerable changes in the species composition and seasonal periodicity of phytoplankton are also of concern in Lake Biwa (Ichise et al., 1996, 2007). As part of the studies on the effects of global warming on phytoplankton dynamics in Lake Biwa, the author describes some outcomes from the analysis of the environmental monitoring survey data in Lake Biwa with a focus on the effect of global warming on the overturn of pelagic water. The analysis was performed with a focus on surface water at the depth of 0.5 m at the lake center (Station 17 B) of the North Basin, to represent the euphotic layer of the pelagic system of Lake Biwa. The analysis covered 33 years from 1975 to 2008. The meteorological record data at the Hikone Meteorological Station were also employed as the reference. All the data were available on web (see Lake Biwa Environmental Research Insititute, 2009 and Meteorological Agency, Japan, 2009).
Fall overturn of the pelagic water
In the surface waters of the North Basin, a noticeable seasonal change in [NO3] has been observed every year in association with the seasonal change of temperature and vertical mixing of the pelagic water. The peak values occurred on the full overturn of the whole water column in late February or early March after pronounced winter cooling of the lake water due to declining air temperatures, and were followed by a gradual decrease in concentration due to utilization by phytoplankton, reaching the lowest levels (frequently an undetectable level) in the summer. After the summer, there was a significant increase in [NO3] in the surface water associated with the start of a partial vertical mixing of water mass due to the autumn cooling of the lake surface (Sakamoto and Maeda, 2002).The inflowing supply of nitrogen and phosphorus by rivers as the major route of external nutrient supply into Lake Biwa is under influence of precipitation and a considerable discharge was recorded during rainy seasons from April to June but a less significant contribution was observed in fall season with less precipitation (Okubo and Azuma, 2005). These observations suggest that the seasonal increase of [NO3] in surface water layer reflects the nutrient supply associated with seasonal vertical turnover of the pelagic water and therefore can be used as a marker of the vertical mixing of water column.
According to Hsieh et al. (2010) who conducted the analysis on the monitoring data of Lake Biwa, Lake Biwa was impacted by global warming after 1990. In the present study, the long-term monitoring data were divided into four groups, two periods before 1990 and two periods after 1990, and the changes in the mean [NO3] in surface water for each month of the continued several years were plotted in Figure 1. Considering effect of the gradual increase of [NO3] standing stock in Lake Biwa with year (Kumagai, 2008) and the developing the annual peak [NO3] on the full overturn at the beginning of vegetation season, the relative rates of the mean [NO3] for each month to the annual peak value were employed for Figure 1.
There is a significant difference in the seasonality of relative [NO3] between the periods before and after 1990 (Figure 1 A). In 1990–2008, the increase of [NO3] after the summer began one month earlier than in 1975–1989. The earlier start of the fall increase in 1990–2008 suggests an earlier onset of the fall overturn after 1990. This earlier start is also known from the changes in water temperature at 0.5 m in Figure 2, showing the change of mean surface water temperature for consecutive four periods. After 1990, the water temperature reached to the peak value earlier than in the precedent periods, followed by earlier decline toward winter, suggesting earlier start of autumnal vertical mixing after 1990. The earlier start of vertical mixing at higher temperature of the surface water affected the later mixing of the deeper water. The higher surface water temperature at the start of fall overturn in 1990–2008 was associated with the later start of temperature decline at 20 m depth than in 1975–1989 as shown in the lower graph of Figure 2.
The autumnal surface water temperature at the given [NO3] concentration in 1990–2008 was consistently higher than in 1975–1989 (Figure 1-B). This suggests that autumnal overturn after 1990 must be beneficial for phytoplankton growth. Judging from density difference of the water at higher temperature, higher surface water temperature after 1990 is regarded as effective for vertical mixing of lake water and resultant upward nutrient supply.
According to the meteorological data recorded at the Hikone meteorological station beside Lake Biwa, the increase in annual mean air temperature per year was minor, 0.47°C in 10 years through 1980–2008. The annual lowest temperature in winter displayed considerable increase at 3.7°C in 5 years beginning in 1984, followed by relatively higher winter temperature of 4.2°C. The lake water exhibited a similar temperature change. Increase of the surface water temperature was minor, 0.6°C in 10 years through the survey period, but increase of the near bottom temperature was considerable, 2.1°C in 5 years beginning in 1984, followed by relatively higher temperature of 7.5°C afterward. Concerning wind velocity, there was an increase of around 20% in mean wind velocity during 33 years of 1975 to 2008. Although this increase in wind velocity could be of influence on the vertical mixing, evaluation on its real effect on the lake water mixing is a future task because of limited basic information.
In the North Basin of Lake Biwa through the 1980s, the winter overturn of the pelagic water was usually followed by the spring bloom of chrysophytes and the summer-fall propagation of chlorophytes (Ichise et al., 1996). After 1990, a considerable change was observed in the seasonal periodicity of phytoplankton community. The seasonal population was dominated by different seasonal species from those in the previous 10 years (Ichise et al., 2007). The representatives were the domination of the small cell sized species of chlorophytes and cyanobacteria in a colonial form covered with gelatinous sheath during the summer, the propagation of cryptophytes and dinophytes throughout the year, and the development of diatoms in higher density in winter. The progressive decline in the phosphorus concentration by eutrophication control could be largely responsible for the significant decline in phytoplanbkton biomass (Ichise et al., 2007). Generally, the seasonal succession of phytoplankton in pelagic system is affected by the turbulence of water column and associated change in nutrient supply from the hypolimnion (Reynolds, 1999). The present result and the published information suggest that the changes in the periodicity and species composition of phytoplankton in the North Basin were closely connected to the change of water temperature and vertical mixing of lake water, although the total phytoplankton biomass was controlled by the decline in phosphorus supply rate. Increasing information has been provided on diverse effects of global warming on lake water mixing and phytoplankton dynamics. These studies indicate the local differences in limnological characteristics of lakes, as well as climate, could account for the diverse responses (Simona, 2003; Salmaso, 2005).
Earlier onset of the fall overturn after 1990 was due to warming of the hypolimnion by warm winters after 1990. Because of diverse impacts of climate change and anthropogenic activities on lakes, further studies are needed on the cumulative effects of climate and other forcing on thermal, chemical, and biological processes in lakes.
This paper is dedicated to the late J. R. Vallentyne and the late R.A Vollenweider, whom the author gratefully acknowledges for their continuous stimulus and suggestions on his studies in Canada and on lake eutrophication control in Japan. The author also thanks the late Vollenweider for his deep consideration and discussions on Chl-TP relationship and nutrient dynamics through lake and watershed in Sakamoto's paper (1966), and two anonymous reviewers for their valuable comments which greatly improved this manuscript.