Abstract
The relationship between concentrations of chlorophyll a in an open water area and growing areas of the macrophytes Trapa spp. and Nelumbo nucifera was investigated to clarify the role of macrophytes in phytoplankton growth in summer in a eutrophic shallow sand lake, Lake Honsagata, Japan. The chlorophyll a concentrations formed peaks in June 2007 and July 2008 in summer with cyanobacterial blooms composed of mainly Microcystis, Anabaena, Phormidium, and Oscillatoria, which decreased toward August and were maintained at different annual levels. The decline of blooms in August was caused by the rapid growth of macrophytes. The composition of phytoplankton and the level of bloom development in summertime differed characteristically from year to year. Also the total vegetation area of N. nucifera and Trapa spp. showed annually marked changes. A significant negative correlation between the concentrations of chlorophyll a and the growth areas of Trapa spp. in August was detected, indicating that the floating-leaved plants, Trapa spp., produced irregular, clear and turbid water states in this shallow eutrophicated lake. These antagonistic relations are explained based on a likely scenario of allelopathic effects on the development of cyanobacteria by Trapa spp. vegetation and the nutrient absorption competition among them. Our study demonstrated the potential of Trapa spp. to control cyanobacterial blooms producing harmful toxins.
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References
Akiyama M, Kunii H (1989) Allelopathic effects of aquatic seed plants on algal plankton. Bull Water Plant Soc Jpn 37:11–16 (in Japanese)
Asaeda T, van Bon TV (1997) Modeling the effects of macrophytes on algal blooming in eutrophic shallow lakes. Ecol Model 104:261–287
Bauer N, Blaschke U, Beutler E, Gross EM, Jenett-Siems K, Siems K, Hilt S (2009) Seasonal and interannual dynamics of polyphenols in Myriophyllum verticillatum and their allelopathic activity on Anabaena variabilis. Aquat Bot 91:110–116
Bicudo DC, Fonseca BM, Bini LM, Crossetti LO, Bicudo CEM, Tachane A-J (2007) Undesirable side-effects of water hyacinth control in a shallow tropical reservoir. Freshw Biol 52:1120–1133
Brammer ES (1979) Exclusion of phytoplankton in the proximity of dominant water soldier (Stratites aloides). Freshw Biol 9:233–249
Canfield DE Jr, Shireman JV, Colle DE, Haller WT, Watkins CEII, Maceina MJ (1984) Prediction of chlorophyll a concentrations in Florida lakes: importance of aquatic macrophytes. Can J Fish Aquat Sci 41:497–501
Codd GA, Morrison LF, Meteaf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203:264–272
Cook CDK (1990) Aquatic plant book. SPB Academic Publishing, Hague
Figueiredo DR, Azeiteiro UM, Esteves SM, Gonçalves FJM, Pereira MJ (2004) Microcystin-producing blooms—a serious global public health issue. Ecotoxicol Environ Saf 59:151–163
Fonseca BM, Bicudo CEM (2010) How important can the presence/absence of macrophytes be in determining phytoplankton strategies in two tropical shallow reservoirs with different trophic status? J Plankton Res 32:32–46
Fukuhara H, Ushijima T (1998) Limnological studies of lakes in Niigata Prefecture X. Changes in the area of emerged and floating-leaved plants, estimated by using aerial photographs in Lake Sagata (Akatsuka, Niigata). Mem Fac Educ Human Sci (Nat Sci) Niigata Univ 1:1–15 (in Japanese)
Fukuhara H, Tanaka T, Izumi M (1997) Growth and turion formation of Ceratophyllum demersum in a shallow lake in Japan. Jpn J Limnol 58:335–347
Fukuhara H, Kawakami A, Shimogaito T (2003) Characteristics of nutrient dynamics in Lake Sagata, Japan, a shallow sand dune lake. Hydrobiologia 506–509:93–99
Fukuhara H, Nemoto F, Takeuchi Y, Toda N (2007) Nitrate dynamics in a reed belt of a shallow sand dune lake in Japan: analysis of nitrate retention using stable nitrogen isotope ratios. Hydrobiologia 584:49–58
Fukuhara H, Kimura N, Nemoto F, Toda H, Nohara S, Ohtaka A (2008) Sand dune lakes in Niigata, Japan. Bull Fac Educ (Nat Sci) Niigata Univ 1:13–29 (in Japanese)
Fukushima T, Takeda Y, Ozaki N (2000) Relationship between water quality and floating-leaved plant coverage in irrigation ponds. J Jpn Soc Water Environ 23:721–725 (in Japanese)
Gopal B, Goel U (1993) Competition and allelopathy in aquatic plant communities. Bot Rev 59:155–210
Gross EM (2003) Allelopathy of aquatic autotrophs. Crit Rev Plant Sci 22:313–339
Gross EM, Erhard D, Ivanyi E (2003) Allelopathic activity of Ceratophyllum demersum L. and Najas marina ssp. intermedia (Wolfgang) Casper. Hydrobiologia 506–509:583–589
Gross EM, Hilt S, Lombardo P, Mulderij G (2007) Searching for allelopathic effects of submerged macrophytes on phytoplankton-state of the art and open questions. Hydrobiologia 584:77–88
Havens KE, James RT, East TL, Smith VH (2003) N:P ratios, light limitation, and cyanobacterial dominance in a subtropical lake impacted by non-point source nutrient pollution. Environ Pollut 122:379–390
Hilt S, Gross EM (2008) Can allelopathically active submerged macrophytes stabilise clear-water states in shallow lakes? Basic Appl Ecol 9:422–432
Hogetsu K, Okanishi R, Sugawara H (1960) Studies on the antagonistic relationship between phytoplankton and rooted aquatic plants. Jpn J Limnol 21:124–130 (in Japanese)
Horn AJ, Goldman CR (1994) Limnology. McGraw-Hill, New York
Hosomi M, Sudo R (1986) Simultaneous determination of total nitrogen and total phosphorus in freshwater samples using persulfate digestion. Int J Environ Stud 27:267–275
Iamchaturapatr J, Yi SW, Rhee JS (2007) Nutrient removals by 21 aquatic plants for vertical free surface-flow (VFS) constructed wetland. Ecol Eng 29:287–293
Ishikawa K, Walker RF, Tsujimura S, Nakahara H, Kumagai M (2004) Estimation of Microcystis colony size in developing water blooms via image analysis. J Jpn Soc Water Environ 27:69–72 (in Japanese)
Japan Environmental Agency (1993) Report on the fourth fundamental survey on lakes—Hokuriku and Koushinetsu edition. Japan Environmental Agency, Tokyo (in Japanese)
Japan Meteorological Agency (2011) Climate Statistic, monthly climate reports (in Japanese). http://www.data.jma.go.jp/obd/stats/etrn/index.php. Accessed Feb 2011
Jarvis AC, Hart RC, Combrink S (1987) Zooplankton feeding on size-fractionated Microcystis colonies and Chlorella in a hypertrophic lake (Hartbeespoort Dam, South Africa): implications to resource utilization and zooplankton succession. J Plankton Res 9:1231–1249
Ke Z, Xie P, Guo L (2008) Controlling factors of spring-summer phytoplankton succession in Lake Taihu (Meiliang Bay, China). Hydrobiologia 607:41–49
Kimura K, Ishida T (2002) Environmental analysis and annual changes in Lake Sagata with surrounding areas using LANDSAT-TM data. In: Niigata City (ed) Report on researches of Sagata financially supported by Niigata City. Niigata City, Niigata, pp 45–68 (in Japanese)
Lampert W, Fleckner W, Rai H, Taylor BE (1986) Phytoplankton control by grazing zooplankton: a study on the spring clear-water phase. Limnol Oceanogr 31:478–490
Lurling M, van Geest G, Scheffer M (2006) Importance of nutrient competition and allelopathic effects in suppression of the green alga Scenedesmus obliquus by the macrophytes, Chara, Elodea and Myriophyllum. Hydrobiologia 556:209–220
Mjelde M, Faafeng BA (1997) Ceratophyllum demersum hampers phytoplankton development in some small Norwegian lakes over a wide range of phosphorus concentrations and geographical latitude. Freshw Biol 37:355–365
Mulderij G, Van Nes EH, Van Donk E (2007a) Macrophyte–phytoplankton interactions: the relative importance of allelopathy versus other factors. Ecol Model 204:85–92
Mulderij G, Mau B, Van Donk E, Gross EM (2007b) Allelopathic activity of Stratiotes aloides on phytoplankton-towards identification of allelopathic substances. Hydrobiologia 584:89–100
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chem Acta 27:31–36
Nakai S, Inoue S, Hosomi M, Murakami A (1999) Growth inhibition of blue-green algae by allelopathic effects of macrophytes. Water Sci Technol 39:47–53
Nemoto F, Takeuchi Y, Saito A, Niino E, Sato C, Maruyama T, Fukuhara H (2009) Decrease in nitrate concentrations in spring water through the reed zone around a sand dune lake. Verh Int Ver Limnol 30:1141–1147
Niigata City (1993) Report on natural environmental assessment of constructing the Sagata Park. Niigata City, Niigata (in Japanese)
Niigata City (1998) Technical report on groundwater around L. Sagata. Niigata City, Niigata (in Japanese)
Niigata City (2000) Technical report on fish, zoobenthos, plankton communities in L. Sagata. Niigata City, Niigata (in Japanese)
Niigata City (2008) Technical report on the natural environment around Lakes Sagata and Mitaraigata. Niigata City, Niigata (in Japanese)
Niigata Prefecture (1981) Technical report on groundwater around L. Sagata (1980). Niigata Prefecture, Niigata (in Japanese)
Nonaka M, Abe R, Kamura T (1996) Nitrate movement through soil profile and groundwater pollution by nitrogen fertilizer in sand dune upland soil. Jpn J Soil Sci Plant Nutr 67:633–639 (in Japanese)
Ohkubo N, Yagi O, Okada M (1991) Effects of temperature and illumination on the growth of blue-green alga Microcystis viridis. Jpn J Limnol 52:255–261
Okino T (1974) Studies on the blooming of Microcystis aeruginosa. Jpn J Bot 20:381–402
Okino T (1982) Urban–hinterland interrelation: urban wastes and the ecosystem of Lake Suwa. Rep Suwa Hydrobiol Stn Shinshu Univ 4:1–8
Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58
Paerl HW, Hall NS, Calandrino ES (2011) Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci Total Environ. doi:10.1016/j.scitotenv.2011.02.001
Paul VJ (2008) Global warming and cyanobacterial harmful algal blooms. In: Hudnell K (ed) Cyanobacterial harmful algal blooms: state of the science and research needs. Adv. Exp. Med. Assoc., vol 619, chap 11. Springer Press, New York, pp 239–258. http://www.epa.gov/cyano_habs_symposium/. Accessed 10 Mar 2009
Qiming X, Haldong C, Huxian Z, Daqiang Y (2006) Allelopathic activity of volatile substance from submerged macrophytes on Microcystis aeruginosa. Acta Ecologica Sinica 26:3549–3554
Rolland A, Bird DF, Giani A (2005) Seasonal changes in composition of the cyanobacterial community and the occurrence of hepatotoxic blooms in the eastern townships, Québec, Canada. J Plankton Res 27:683–694
Ruggiero A, Solimini AG, Carchini G (2003) Nutrient and chlorophyll a temporal patterns in eutrophic mountain ponds with contrasting macrophyte coverage. Hydrobiologia 506–509:657–663
Scheffer M (1998) Ecology of shallow lakes. Chapman & Hall, London
Scheffer M, Van Nes EH (2007) Shallow lake theory revised: various alternative regimes driven by climate, nutrients, depth and lake size. Hydrobiologia 584:455–466
Scheffer M, Hosper SH, Meijer M-L, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279
Scheffer M, Szabo S, Gragnani A, Van Nes EH, Rinaldi S, Kautsky N, Nonberg J, Rijackers RMM, Franken RJM (2003) Floating plant dominance as a stable state. Proc Natl Acad Sci USA 100:4040–4045
Schriver P, Bøgestrand J, Jeppesen E, Søndergaard M (1995) Impact of submerged macrophytes on fish–zooplankton–phytoplankton interactions: large-scale enclosure experiments in a shallow eutrophic lake. Freshw Biol 33:255–270
Smith VH (1983) Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Sci 221:669–671
Smith VH, Bierman VJ, Jones BL Jr, Havens K (1995) Historical trends in the Lake Okeechobee ecosystem IV. Nitrogen: phosphorus ratios, cyanobacterial dominance and nitrogen fixation potential. Arch Hydrobiol Suppl 107:71–88
Smith JL, Boyer GL, Zimba PV (2008) A review of cyanobacterial odorous and bioactive metabolites: impacts and management alternatives in aquaculture. Aquaculture 280:5–20
Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801
Strickland JDH, Parsons TR (1972) A practical handbook of sea water analysis. Bull Fish Res Board Can 167:207–211
Takamura N, Watanabe M (1987) Seasonal changes in the biomass of four species of Microcystis in Lake Kasumigaura. Jpn J Limnol 48:S139–S144
Takamura N, Otsuki A, Aizaki M, Nojiri Y (1992) Phytoplankton species shift accompanied with transition from nitrogen dependence to phosphorus dependence of primary production in Lake Kasumigaura, Japan. Arch Hydrobiol 124:129–148
Takamura N, Kadono Y, Fukushima M, Nakagawa M, Kim B-HO (2003) Effects of aquatic macrophytes on water quality and phytoplankton communities in shallow lakes. Ecol Res 18:381–395
Tanaka H, Hasegawa T, Kimura S, Okamoto I, Sakai Y (1996) The geohistory of the formation of the Niigata Sand Dunes. Quat Res 35:207–218 (in Japanese)
Tsuchiya T, Iwaki H (1979) Impact of nutrient enrichment in a waterchestnut ecosystem at Takahama-iri Bay of Lake Kasumigaura, Japan II. Role of waterchestnut in primary productivity and nutrient uptake. Water Air Soil Pollut 12:503–510
van Donk E, van de Bund WJ (2002) Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquat Bot 72:261–274
Watanabe M, Koyama T, Sasaki H (2010) The proposal for nutrient concentration control employing nutrient uptake and release by Trapa japonica inhabiting Lake Izunuma. J Jpn Soc Water Environ 33:57–61 (in Japanese)
Yamamoto Y, Nakahara H (2009) Seasonal variations in the morphology of bloom-forming cyanobacteria in a eutrophic pond. Limnology 10:185–193
Acknowledgments
We are indebted to the members of the Waterfowl and Wetland Center in Sakata for providing the facilities for the surveys, and to the Environmental Policy Division, Niigata City, for permitting surveys of the lake and the citation of data in relevant reports, especially in the Water Quality Data Report of Public Water Area in Niigata City. We are also indebted to Mr. Toru Yanagisawa of the Niigata Green Sigma Co., Ltd., for his helpful instructions on a method to measure vegetation areas from aerial photographs and to Dr. Tatsuyoshi Morita of the Faculty of Education of Niigata University for his extensive advice in connection with this study. Our thanks also go to Mrs. Ayao Kawakami and Takashi Shimogaito for generously providing the phytoplankton samples collected in 1997. This study was supported in part by a Grant-in-Aid for Scientific Research (C) (nos. 17510193 and 20510214) from the Japan Society for the Promotion of Science.
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Nemoto, F., Fukuhara, H. The antagonistic relationship between chlorophyll a concentrations and the growth areas of Trapa during summer in a shallow eutrophic lake. Limnology 13, 289–299 (2012). https://doi.org/10.1007/s10201-012-0376-6
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DOI: https://doi.org/10.1007/s10201-012-0376-6