The effect of phosphorus removal from sewage on the plankton community in a hypertrophic reservoir
© The Author(s) 2016
Received: 11 November 2015
Accepted: 24 June 2016
Published: 24 October 2016
When developing water quality improvement strategies for eutrophic lakes, questions may arise about the relative importance of point sources and nonpoint sources of phosphorus. For example, there is some skepticism regarding the effectiveness of partial reductions in phosphorus loading; because phosphorus concentrations are too high in hypertrophic lakes, in-lake phosphorus concentrations might still remain within typical range for eutrophic lakes even after the reduction of phosphorus loading. For this study, water quality and the phytoplankton and zooplankton communities were monitored in a hypertrophic reservoir (Lake Wangsong) before and after the reduction of phosphorus loading from a point source (a sewage treatment plant) by the installation of a chemical phosphorus-removal process.
Before phosphorus removal, Lake Wangsong was classified as hypertrophic with a median phosphorus concentration of 0.232 mg L−1 and a median chlorophyll-a concentration of 112 mg L−1. The dominant phytoplankton were filamentous cyanobacteria for the most of the ice-free season. Following the installation of the advanced treatment process, phosphorus concentrations were reduced to 81 mg L−1, and the N/P atomic ratio increased from 42 to 102. Chlorophyll-a concentrations decreased to 42 μg L−1, and the duration of cyanobacterial dominance was confined to the summer season. Cyanobacteria in spring and autumn were replaced by diatoms and cryptomonads. Filamentous cyanobacteria in summer were replaced by colony-forming unicellular Microcystis spp. It was remarkable that zooplankton biomass increased despite the decrease in phytoplankton biomass, and especially cladoceran zooplankton which increased drastically. These responses to the reduction of point source P loading to Lake Wangsong imply that reducing the point source P loading can have a big impact even when nonpoint sources account for a large fraction of the total annual phosphorus loading.
Our results also show that the phytoplankton community can shift to decreased cyanobacterial dominance and the zooplankton community can shift to higher cladoceran dominance, even when phosphorus concentrations remain within the typical range for eutrophic lakes following the reduction of phosphorus loading.
Eutrophication is the most common water quality problem in lakes and reservoirs (Azevedo et al. 2015; Reed-Andersen et al. 2000), and phosphorus is the major limiting factor of eutrophication (Schindler 1977; Withers and Jarvie 2008). Phosphorus (P) comes mostly from animal excretion and fertilizer, and the sources are classified as point sources or nonpoint sources (Kundu et al. 2015; Carson et al. 2015). In most rural watersheds, nonpoint P sources such as agricultural fields and forest are the major sources of the total P load. However, if there is significant urban development within the watershed, sewage discharge can contribute a considerable portion of P loading (Neal et al. 2000; Jarvie et al. 2006). In watersheds consisting of complex terrain with urban and rural land use, P loading from agricultural fields is usually larger than the P loading from sewage. However, the export of P from nonpoint sources is exported mostly on rainy days in the form of storm runoffs (Li et al. 2015). On the contrary, P loading from point sources have uniform flow rates, and on dry days, their contribution can be larger than those of nonpoint sources.
Hydraulic residence time can be another factor that determines the relative importance of storm runoff in lakes and reservoirs (Dillon 1975; Brett and Benjamin 2008). Shock loading from agricultural nonpoint sources can be very large during a storm event, but a large portion of the P loading can be flushed out of reservoirs with short residence times. Therefore, there are still many important questions remaining concerning the relative importance of point and nonpoint P loading. There might be some skepticism regarding the effectiveness of reductions in point source P loading which result in only a partial reduction of the annual P loading (Mainstone and Parr 2002).
Point sources of P include raw sewage discharge or effluent from sewage treatment plants which do not have chemical phosphorus-removal processes. The sewage treatment process can be divided into three phases: primary treatment, secondary treatment, and tertiary treatment (or advanced treatment). Commonly, in developed countries, sewage is treated using secondary treatment processes, biological treatment processes designed mainly for biological oxygen demand (BOD) removal (Cullen and Forsberg 1988). Because P concentrations in the effluent from secondary treatment (1–2 mg P L−1) is 30–60 times higher than the typical criterion for eutrophication (typically 0.03 mg P L−1), advanced P treatment using chemical precipitation has been incorporated in some sewage treatment plants in Korea that discharge effluent into sensitive surface waters. The legal standards for P concentrations in effluent from treatment plants are between 0.2 and 0.5 mg P L−1, still substantially higher than the criterion for eutrophication.
In hypertrophic lakes where P concentrations are too high even after a reduction of point source P loading, the in-lake P concentrations may still remain in the typical range for eutrophic lakes (Schindler 2006). As part of efforts to provide a scientific basis for decision-making and developing strategies for water quality management, detailed information on the consequences of a reduction in P loading and especially the effects on water quality and the phytoplankton and zooplankton communities is required.
Morphological characteristics of Lake Wangsong
Watershed area (km2)
Mean depth (m)
Total water storage capacity (103 m3)
Maximum surface area (km2)
Hydraulic residence time (days)
Land use (ha)
Agriculture (upland field)
290 (18.6 %)
Agriculture (paddy field)
320 (20.6 %)
685 (44.1 %)
182 (11.7 %)
78 (5.0 %)
Population density (pop. km−2)
The phytoplankton and zooplankton communities and water quality were surveyed before the advanced treatment operation (2003 and 2004) and after the advanced treatment (2008 and 2009). Water samples were collected from the center of the lake at 0, 2, and 5-m depths. Two main inflowing streams were surveyed in order to assess P loading from the watershed in the dry season. In this study, water quality measurements of the STP effluent were measured and, also, the data from the STP management office were employed together for calculating the P loading from the STP effluent.
Water samples were collected using an inflatable boat and a horizontal Van Dorn water sampler. The water samples were transported in a cooler and stored in a refrigerator until analysis. Dissolved oxygen was measured in situ with a DO meter (YSI, USA). All water quality measurements were conducted according to standard methods (American Public Health Association 2005) except chemical oxygen demand (COD). Total phosphorus (TP) concentration was measured using the ascorbic acid method following persulfate digestion. Chlorophyll-a concentration was measured by the trichromatic spectrophotometric method. Total nitrogen (TN) was measured by the cadmium reduction method following persulfate digestion. Suspended solids (SS) was measured gravimetrically after filtration by GF/F filter. Biological oxygen demand (BOD) was measured by using a DO meter. COD measurements used the permanganate method, the official standard method in Korea (MOE 2009).
Water quality data collected at the surface of the lake by the Gyeonggido local province was also employed in addition to the data collected by this study in order to increase statistical significance in the comparison of water quality before and after the advanced treatment. Stream discharge of inflowing streams was measured using a magnetic flow velocity meter and the current cross-section method. P loading from nonpoint sources in the watershed was estimated by multiplying the unit export coefficients of phosphorus by the area of each land use type as suggested by the Korean Ministry of the Environment (MOE 2014).
Phytoplankton samples were collected in 500-mL polyethylene bottles at 0.5-m depth and preserved with Lugol’s solution. Cell densities were measured using a Sedgewick-Rafter counting chamber and an X300 microscope (Olympus BX50). Zooplankton samples were collected with a plankton net (63-μm mesh) using a slow vertical tow from the bottom (typically 5–6-m depth) to the surface of the lake. Zooplankton samples were preserved with 4 % sucrose formalin (Steedman 1976). The volume of water filtered by a zooplankton net was calculated by multiplying the aperture area of the net by the towing distance, assuming there is no significant loss of filtering efficiency through a 5-m towing.
Nutrient loading and water quality
Water quality of inflowing streams and lake surface (median, mg L-1; Chl.a, ug L-1, (25th–75th percentile))
(May 1999–Jun. 2007)
(Aug. 2007–Nov. 2009)
Comparison of daily phosphorus loading on dry days from the watershed (St.1 and St.2) and sewage treatment plant effluent (STP)
25 Sep. 2008
31 Oct. 2008
In August of 2007, the advanced P removal treatment started operation. With the reduction of P loading, TP concentrations in the surface have decreased from 0.232 to 0.081 mg P L−1 (median), a reduction of 65 % (Table 2). But even after the advanced treatment, TP concentrations in the STP effluent were ten times higher than the typical criterion for eutrophic conditions (0.03 mg P L−1). Consequently, TP in Lake Wangsong also exceeded the threshold of eutrophication by a factor of 2.5.
Because the advanced treatment was focused on the chemical removal of P, which has a lower removal efficiency than nitrogen, TN concentrations did not decrease as much as TP concentrations. With the higher removal efficiency of P than N, the atomic N/P ratio in the lake increased from 68 to 154 following the start of the advanced treatment. Thus, the atomic N/P was much higher than the Redfield ratio (16) (Redfield 1958) implying P limitation of algal growth in Lake Wangsong.
Suspended solids (SS) in the lake did not change after the advanced treatment. The median SS was 19 mg L−1, suggesting that the seston is composed of mostly inorganic particles, possibly arising from the bottom sediment in this shallow reservoir. Assuming that the chlorophyll-a content of algal cells is commonly 1 % of dry weight and the median chlorophyll-a concentration of 42.2 ug L m−1 in Lake Wangsong, algal cells would account for an algal biomass of approximately 4 mg L−1, much lower than the SS. Therefore, inorganic particles would account for 15 mg L−1 in the SS. In Lake Wangsong, resuspension of sediment is likely common on windy days. The decrease in BOD following the reduction in P loading affected the hypolimnetic DO concentrations, a common criterion for eutrophication (Horne and Goldman 1994). Anoxic conditions in the hypolimnion clearly developed below 4-m depth in September 2003 and May to August 2004, whereas the hypolimnion was oxic in 2009.
Phytoplankton and zooplankton
Cell densities of three major phytoplankton taxa and dominant species before and after advanced sewage treatment
Cell density (cells mL−1)
(by biomass, μgC L−1)
Advanced treatment start
Standing crop and dominant zooplankton species
Standing crop (ind. L−1)
Advanced treatment start
The annual P loading to lakes from point sources and nonpoint sources is commonly comprised mostly of agricultural nonpoint P sources in watersheds with mixed land uses. However, in reservoirs with short hydraulic residence time, storm runoff from nonpoint sources is not stored for a long time within the reservoir, especially in the rainy season. Because Korea is located in the summer monsoon region, most of the annual rainfall occurs in summer. Short hydraulic residence times in reservoirs can be a critical factor affecting nutrient concentrations in reservoirs. In the dry season, the relative importance of point sources is larger than nonpoint sources, because nonpoint sources do not export nutrients during periods with minimum stream flow. In this study, the importance of P removal in the STP effluent was obviously manifested in the water quality improvement after the advanced treatment.
Even after the advanced treatment, Lake Wangsong remained eutrophic. TP and chlorophyll-a concentrations were higher than the criteria for eutrophic lakes (Wetzel 2001), mainly because TP in the STP effluent was still much higher than the typical criterion for eutrophication. TP can be reduced to as low as 0.01 mg P L−1 in STP effluent with advanced chemical treatment. In Korea, the phosphorus standards for STP effluent are in the range of 0.2 to 2.0 mg L−1, still much higher than the eutrophication criterion. Therefore, even if sewage is treated according to the government standard for P concentration in the effluent, sewage can be a main cause of eutrophication and further reductions in P in STP effluent are strongly needed for the control of eutrophication.
Importantly, we observed that the dominance of cyanobacteria decreased with P concentrations, even though P concentrations remained in the eutrophic level. The N/P ratio increased due to the P removal in the STP effluent, which might have provided favorable conditions for algae other than cyanobacteria. A low N/P ratio is known to be favorable for cyanobacteria, because N can be a temporary limiting factor and N-fixing cyanobacteria can take advantage of this (Gu and Alexander 1993). Temporary nitrogen depletion during algal blooms can be a controlling factor in the competition among phytoplankton species; that is, decreases in P can provide favorable conditions for other algal species and inhibit the dominance of filamentous cyanobacteria (Fulton 1988). Before the start of the advanced treatment, most of the dominant phytoplankton were filamentous cyanobacteria with many species having the potential to carry out N-fixation, whereas filamentous cyanobacteria were dominant only in 1 sample out of 12 monthly samples after the advanced treatment.
The reduction of phosphorus from STP effluent resulted in a significant reduction of in-lake P concentrations in Lake Wangsong, which in turn effected a shift in the phytoplankton community. Even though P concentrations remained within the typical range for eutrophic conditions following the reduction in P loading, all the indicators of water quality and aquatic ecosystem health showed improvements: decreased phytoplankton density, decreased hypoxia in the hypolimnion, a shift from cyanobacteria to diatoms in cold seasons, a shift from filamentous cyanobacteria to colony-forming unicellular cyanobacteria, and increased cladoceran zooplankton populations which can improve water clarity and facilitate the transfer of energy through the grazing food chain. This implies that P removal from STP effluent can be important for improving water quality in hypertrophic reservoirs even if the annual P loading from nonpoint sources is larger than the P loading from sewage effluent.
This study was supported by a 2013 Research Grant from Kangwon National University (no. 120131194). This study was supported by the Center for Aquatic Ecosystem Restoration (CAER) of the Eco-STAR Project from the Ministry of Environment, Republic of Korea (MOE: EW 42-08-10). Support from the Environmental Research Institute at Kangwon National University is also acknowledged.
Availability of data and materials
Please contact the author for data requests.
All authors contributed extensively to the work presented in this paper. BK and SJ designed the study and wrote the main paper. YL and JL collected the zooplankton data and analyzed the results. SJ, JK, and YC collected and analyzed the phytoplankton data and conducted the data analysis. KK, JO, and AR analyzed the water quality data. All authors discussed the results and implications and commented on the manuscript at all stages.
The authors declare that they have no competing interests.
Consent for publication
Ethics approval and consent to participate
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- American Public Health Association, American Water Works Association, Water Environment Federation. (2005). Standard methods for the examination of water and wastewater (21st ed.). Washington, D.C.: American Public Health Association.Google Scholar
- Azevedo, L. B., van Zelm, R., Leuven, R. S., Hendriks, A. J., & Huijbregts, M. A. (2015). Combined ecological risks of nitrogen and phosphorus in European freshwaters. Environmental Pollution, 200, 85–92.View ArticlePubMedGoogle Scholar
- Bomi, C., Misun, S., Jong, I. K., & Woongghi, S. (2013). Taxonomy and phylogeny of the genus Cryptomonas (Cryptophyceae, Cryptophyta) from Korea. Algae, 28, 307–330.View ArticleGoogle Scholar
- Brett, M. T., & Benjamin, M. M. (2008). A review and reassessment of lake phosphorus retention and the nutrient loading concept. Freshwater Biology, 53, 194–211.Google Scholar
- Carson, A., Jennings, E., Linnane, S., & Jordan, S. N. (2015). Clearing the muddy waters: using lake sediment records to inform agricultural management. Journal of Paleolimnology, 53, 1–15.View ArticleGoogle Scholar
- Cullen, P., & Forsberg, C. (1988). Experiences with reducing point sources of phosphorus to lakes. Hydrobiologia, 170, 321–336.View ArticleGoogle Scholar
- Dillon, P. (1975). The phosphorus budget of Cameron Lake, Ontario: the importance of flushing rate to the degree of eutrophy of lakes. Limnology and Oceanography, 20, 28–39.View ArticleGoogle Scholar
- Fulton, R. S. (1988). Grazing on filamentous algae by herbivorous zooplankton. Freshwater Biology, 20, 263–271.View ArticleGoogle Scholar
- Gu, B., & Alexander, V. (1993). Estimation of N2 fixation based on differences in the natural abundance of 15N among freshwater N2-fixing and non-N2-fixing algae. Oecologica, 96, 43–48.View ArticleGoogle Scholar
- Gyeonggi Research Institute (2011). Water quality management and implementation: alternatives for Wangsong Reservoir.Google Scholar
- Horne, A. J., & Goldman, C. R. (1994). Limnology (2nd ed.). New York: McGraw-Hill Co.Google Scholar
- Jarvie, H. P., Neal, C., & Withers, P. J. (2006). Sewage-effluent phosphorus: a greater risk to river eutrophication than agricultural phosphorus? Science of the Total Environment, 360, 246–253.View ArticlePubMedGoogle Scholar
- Krevš, A., Koreivienė, J., & Mažeikaitė, S. (2010). Plankton food web structure during cyanobacteria bloom in the highly eutrophic Lake Gineitiškės. Ekologija, 56, 47–54.View ArticleGoogle Scholar
- Kundu, S., Coumar, M. V., Rajendiran, S., & Rao, A. S. (2015). Phosphates from detergents and eutrophication of surface water ecosystem in India. Current Science, 108, 1320–1325.Google Scholar
- Li, D., Wan, J., Ma, Y., Wang, Y., Huang, M., & Chen, Y. (2015). Stormwater runoff pollutant loading distributions and their correlation with rainfall and catchment characteristics in a rapidly industrialized city. PloS One. doi:10.1371/journal.pone.0118776.Google Scholar
- Mainstone, C. P., & Parr, W. (2002). Phosphorus in rivers-ecology and management. Science of the Total Environment, 282, 25–47.View ArticleGoogle Scholar
- Ministry of Environment. (2009). Standard methods of water sampling and analysis. Korea: Ministry of Environment.Google Scholar
- Ministry of Environment. (2014). Total maximum daily load program. Korea: Ministry of Environment.Google Scholar
- Neal, C., Jarvie, H. P., Howarth, S. M., Whitehead, P. G., Williams, R. J., Neal, M., Harrow, M., & Wickham, H. (2000). The water quality of the River Kennet: initial observations on a lowland chalk stream impacted by sewage inputs and phosphorus remediation. Science of the Total Environment, 251, 477–495.View ArticlePubMedGoogle Scholar
- Redfield, A. C. (1958). The biological control of chemical factors in the environment. American Scientist, 46, 205–221.Google Scholar
- Reed-Andersen, T., Carpenter, S. R., & Lathrop, R. C. (2000). Phosphorus flow in a watershed-lake ecosystem. Ecosystems, 3, 561–573.View ArticleGoogle Scholar
- Schindler, D. W. (1977). Evolution of phosphorus limitation in lakes. Science, 195, 260–262.View ArticlePubMedGoogle Scholar
- Schindler, D. W. (2006). Recent advances in the understanding and management of eutrophication. Limnology and Oceanography, 51, 356–363.View ArticleGoogle Scholar
- Schrage, L. J., & Downing, J. A. (2004). Pathways of increased water clarity after fish removal from Ventura Marsh; a shallow, eutrophic wetland. Hydrobiologia, 511, 215–231.View ArticleGoogle Scholar
- Sinistro, R. (2009). Top-down and bottom-up regulation of planktonic communities in a warm temperate wetland. Journal of Plankton Research. doi:10.1093/plankt/fbp114.Google Scholar
- Sommer, U., Sommer, F., Santer, B., Jamieson, C., Boersma, M., Becker, C., & Hansen, T. (2001). Complementary impact of copepods and cladocerans on phytoplankton. Ecology Letters, 4, 545–550.View ArticleGoogle Scholar
- Steedman, H. F. (1976). Zooplankton fixation and preservation. Paris: UNESCO Press.Google Scholar
- Wetzel, R. G. (2001). Limnology: lake and river ecosystems (3rd ed.). San Diego: Academic.Google Scholar
- Withers, P., & Jarvie, H. (2008). Delivery and cycling of phosphorus in rivers: a review. Science of the Total Environment, 400, 379–395.View ArticlePubMedGoogle Scholar