Journal of Paleolimnology

, Volume 44, Issue 1, pp 69–83 | Cite as

Phytoplankton dynamics in Lake Biwa during the 20th century: complex responses to climate variation and changes in nutrient status

  • Narumi K. Tsugeki
  • Jotaro Urabe
  • Yuichi Hayami
  • Michinobu Kuwae
  • Masami Nakanishi
Original paper


We examined algal remains and fossil pigments in 210Pb-dated sediment cores from Lake Biwa to explore historical changes in the phytoplankton community of the lake over the past 100 years and to identify environmental factors that caused those changes. Fluxes of fossil pigments and algal remains were very low before the 1960s, but increased through the 1960s and 1970s, indicating that the lake had eutrophied in the 20 years since 1960. After 1980, however, fluxes of all fossil pigments and algal remains decreased or stabilized. Redundancy analysis with meteorological and limnological variables explained more than 70% of the variation of these fluxes and showed that the decrease in fluxes of most algal taxa that occurred in the 1980s was related to changes in meteorological variables such as wind velocity, rather than changes in the lake’s trophic state. Sedimentary records of algal remains also revealed that Aulacoseira nipponica, an endemic diatom species that grows in winter, decreased dramatically after 1980, while Fragilaria crotonensis, a cosmopolitan spring diatom species, became dominant. Replacement of one dominant diatom species by another could not be explained simply by changes in the lake trophic state, but was reasonably strongly related with an increase in winter water temperature. These results suggest that the phytoplankton community in Lake Biwa was influenced by changes in local environmental conditions (nutrient loading) through the 1960s and 1970s, but more so by regional (meteorological) and global (climate warming) factors since 1980.


Phytoplankton dynamics 20th century Climate warming Wind velocity Eutrophication Lake Biwa 



We thank Mr. T. Koitabashi, T. Miyano and J. Togari for shipboard assistance, and appreciate Drs. F. Hyodo, T. Ishikawa, and M. Kagami for helpful discussions. This study was funded by a Grant-in-Aid for Scientific Research B (No. 12440218) and Research A (No. 19207003) from the MEXT Japan to JU and by a grant to NM as a part of the FS studies by RIHN Japan, and partly supported by a JSPS postdoctoral fellowship to NKT.


  1. Anneville O, Gammeter S, Straile D (2005) Phosphorus decrease and climate variability: mediators of synchrony in phytoplankton changes among European peri-alpine lakes. Freshw Biol 50:1731–1746CrossRefGoogle Scholar
  2. Battarbee RW (1986) Diatom analysis. In: Berglund BE (ed) Handbook of Holocene palaeoecology and palaeohydrology. Wiley, Chichester, pp 527–570Google Scholar
  3. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
  4. Berman T, Shteinman B (1998) Phytoplankton development and turbulent mixing in Lake Kinneret (1992–1996). J Plankton Res 20:709–726CrossRefGoogle Scholar
  5. Birks HJB (1995) Quantitative palaeoenvironmental reconstructions. In: Maddy D, Brew JS (eds) Statistical modelling of quaternary science data. Technical guide 5. Quaternary Research Association, Cambridge, pp 161–254Google Scholar
  6. Endo S, Yamashita S, Kawakami M, Okumura Y (1999) Recent warming of Lake Biwa water. Jpn J Limnol 60:223–228 (in Japanese with English abstract)Google Scholar
  7. Findlay DL, Kasian SEM, Stainton MP, Beaty K, Lyng M (2001) Climatic influences on algal populations of boreal forest lakes in the Experimental Lakes Area. Limnol Oceanogr 46:1784–1793Google Scholar
  8. Frenette J-J, Vincent WF, Legendre L, Nagata T (1996) Size-dependent changes in phytoplankton C and N uptake in the dynamic mixed layer of Lake Biwa. Freshw Biol 36:221–236CrossRefGoogle Scholar
  9. Gontcharov AA, Kasai F, Watanabe M (1999) Morphology and taxonomy of two planktic species of [Staurastrum] (Desmidiaceae, Chlorophyta) in Lake Biwa, Japan. Arch Hydrobiol Suppl 93:79–90Google Scholar
  10. Gurung TB, Urabe J, Nozaki K, Yoshimizu C, Nakanishi M (2002) Bacterioplankton production in a water column of Lake Biwa. Lakes Res 7:317–323CrossRefGoogle Scholar
  11. Hall RI, Leavitt PR, Quinlan R, Dixit AS, Smol JP (1999) Effects of agriculture, urbanization, and climate on water quality in the northern great plains. Limnol Oceanogr 44:739–756Google Scholar
  12. Hayami Y, Fujiwara T (1999) Recent warming of the deep water in Lake Biwa. Oceanogr Jpn 8:197–202 (in Japanese with English abstract)Google Scholar
  13. Hecky RE (1993) The eutrophication of Lake Victoria. Verh Int Ver Theor Angew Limnol 25:39–48Google Scholar
  14. Hikone Meteorological Observatory (1993–2000) Shigaken no kisho. Shiga (in Japanese)Google Scholar
  15. Huisman J, Jonker RR, Zonneveld C, Weissing FJ (1999) Competition for light between phytoplankton species: experimental tests of mechanistic theory. Ecology 80:211–222CrossRefGoogle Scholar
  16. Hyodo F, Tsugeki N, Azuma J-I, Urabe J, Nakanishi M, Wada E (2008) Changes in stable isotopes, lignin-derived phenols, and fossil pigments in sediments of Lake Biwa, Japan: implications for anthropogenic effects over the last 100 years. Sci Total Environ 403:139–147CrossRefGoogle Scholar
  17. Ichise S, Wakabayashi T, Fujiwara N, Mizushima K, Ito M (2001) Long-term changes of biomass of phytoplankton in Lake Biwa. Rep Shiga Pref Inst Pub Hlth Environ Sci 36:29–35 (in Japanese)Google Scholar
  18. Interlandi SJ, Kilham SS (1998) Assessing the effects of nitrogen deposition on mountain waters: a study of phytoplankton community dynamics. Water Sci Technol 38:139–146Google Scholar
  19. Interlandi SJ, Kilham SS, Theriot EC (1999) Responses of phytoplankton to varied resource availability in large lakes of the greater yellowstone ecosystem. Limnol Oceanogr 44:668–682CrossRefGoogle Scholar
  20. Interlandi SJ, Kilham SS, Theriot EC (2003) Diatom-chemistry relationships in Yellowstone Lake (Wyoming) sediments: implications for climatic and aquatic processes research. Limnol Oceanogr 48:79–92CrossRefGoogle Scholar
  21. Jöhnk K, Huisman D, Sharples J, Sommeijer J, Visser B, Stroom PM, Summer JM (2008) Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biol 14:495–512CrossRefGoogle Scholar
  22. Kadota S (1973) A quantitative study of microfossils in the core sample from Lake Biwa-ko. Jpn J Limnol 34:103–110 (in Japanese with English abstract)Google Scholar
  23. Kagami M, Gurung TB, Yoshida T, Urabe J (2006) To sink or to be lysed: contrasting fate of two large phytoplankton species in Lake Biwa. Limnol Oceanogr 51:2775–2786CrossRefGoogle Scholar
  24. Kalff J (2002) Limnology―inland water ecosystems. Prentice Hall, Upper Saddle River (592 pp)Google Scholar
  25. Kawabata K (1987) Ecology of large phytoplankton in Lake Biwa: population dynamics and food relations with zooplankters. Bull Plankton Soc Jpn 34:165–172Google Scholar
  26. Kilham P (1990) Ecology of Melosira species in the Great lakes of Africa. In: Tilzer MM, Serruya C (eds) Large lakes: ecological structure and function. Springer, New York, pp 414–427Google Scholar
  27. Kohata K, Watanabe M, Yamanaka K (1991) Highly sensitive determination of photosynthetic pigments in marine in situ samples by high-performance liquid chromatography. J Chromatogr 558:131–140CrossRefGoogle Scholar
  28. Kuwae M, Yoshikawa S, Tsugeki N, Inouchi Y (2004) Reconstruction of a climate record for the past 140 kyr based on diatom valve flux data from Lake Biwa, Japan. J Paleolimnol 32:19–39CrossRefGoogle Scholar
  29. Leavitt PR (1993) A review of factors that regulate carotenoid and chlorophyll deposition and fossil pigment abundance. J Paleolimnol 9:109–127CrossRefGoogle Scholar
  30. Leavitt PR, Findlay DL (1994) Comparison of fossil pigment with 20 years of phytoplankton data from eutrophic Lake 227, experimental lakes area, Ontario. Can J Fish Aquat Sci 51:2286–2299CrossRefGoogle Scholar
  31. Leavitt PR, Findlay DL, Hall RI, Smol JP (1999) Algal responses to dissolved organic carbon loss and pH decline during whole-lake acidification: evidence from paleolimnology. Limnol Oceanogr 44:757–773CrossRefGoogle Scholar
  32. Lund JW (1971) An artificial alteration of the seasonal cycle of the plankton diatom Melosira italica subsp. subarctica in an English lake. J Ecol 59:521–533CrossRefGoogle Scholar
  33. Maberly SC (1996) Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshw Biol 35:579–598Google Scholar
  34. Magnuson JJ, Webster KE, Assel RA, Bowser CJ, Dillon PJ, Eaton JG, Evans HE, Fee EJ, Hall RI, Mortsch LR, Schindler DW, Quinn FH (1997) Potential effects of climate changes on aquatic systems: Laurentian great lakes and Precambrian shield region. Hydrol Process 11:825–871CrossRefGoogle Scholar
  35. Meyers PA, Takemura K, Horie S (1993) Reinterpretation of Late Quaternary sediment chronology of Lake Biwa, Japan, from correlation with marine glacial-interglacial cycles. Quat Res 39:154–162CrossRefGoogle Scholar
  36. Miyajima T, Nakano S, Nakanishi M (1995) Planktonic diatoms in pelagic silicate cycle in Lake Biwa. Jpn J Limnol 56:211–220Google Scholar
  37. Mori S, Horie S (1975) Diatoms in a 197.2 meters core sample from Lake Biwa-ko. Proc Jpn Acad 51:675–679Google Scholar
  38. Nakamura M (2002) Lake Biwa watershed transformation and the changed water environments. Verh Internat Verein Limnol 28:69–83Google Scholar
  39. Nakanishi M (1976) Seasonal variations of chlorophyll-a amounts, photosynthesis and production rates of macro- and microphytoplankton in Shiozu Bay. Lake Biwa. Physiol Ecol Jpn 17:535–549Google Scholar
  40. Negoro K (1968) Phytoplankton of Lake Biwa. In: Kitamura S (ed) Flora ohmiensis. Hoikusya, Osaka, pp 275–330 (in Japanese)Google Scholar
  41. O’Reilly CM, Alin SR, Plisnier P-D, Cohen AS, McKee BA (2003) Climate change decreases aquatic ecosystem productivity of Lake Tanganyika, Africa. Nature 424:766–768CrossRefGoogle Scholar
  42. Ogawa NO, Koitabashi T, Oda H, Nakamura T, Wada E (2001) Fluctuations of nitrogen isotope ratio of gobiid fish (Isaza) specimens and sediments in Lake Biwa, Japan, during the 20th century. Limnol Oceanogr 46:1228–1236CrossRefGoogle Scholar
  43. Passarge J, Hol S, Escher M, Huisman J (2006) Competition for nutrients and light: stable coexistence, alternative stable states, or competitive exclusion? Ecol Monogr 76:57–72CrossRefGoogle Scholar
  44. Petersen J, Chen C-C, Kemp WM (1997) Scaling aquatic primary productivity: experiments under nutrient and light limited conditions. Ecology 78:2326–2338CrossRefGoogle Scholar
  45. Ravens TM, Koscis O, Wuest A, Granin N (2000) Small-scale turbulence and vertical mixing in Lake Baikal. Limnol Oceanogr 45:159–173CrossRefGoogle Scholar
  46. Reuss N, Leavitt PR, Hall RI, Bigler C, Hammarlund D (2009) Development and application of sedimentary pigments for assessing effects of climatic and environmental changes on subarctic lakes in northern Sweden. J Paleolimnol 32:19–39Google Scholar
  47. Reynolds CS (1984) The ecology of freshwater phytoplankton. Cambridge University, New York, p 384Google Scholar
  48. Rhew K, Baca RM, Ochs CA, Threlkeld ST (1999) Interaction effects of fish, nutrients, mixing and sediments on autotrophic picoplankton and algal composition. Freshw Biol 42:99–109CrossRefGoogle Scholar
  49. Robbins JA, Edington DN (1975) Determination of recent sedimentation rates in Lake Michigan using Pb-210 and Cs-137. Geochim Cosmochim Acta 39:285–304CrossRefGoogle Scholar
  50. Roberts N (1998) The Holocene: an environmental history. Blackwell, Oxford, p 344Google Scholar
  51. Scheffer M, Rinaldi S, Gragnani A, Mur LR, Vannes EH (1997) On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology 78:272–282CrossRefGoogle Scholar
  52. Schindler DW (1978) Factors regulating phytoplankton production and standing crop in the world’s freshwaters. Limnol Oceanogr 23:478–486CrossRefGoogle Scholar
  53. Schindler DW (2006) Recent advances in the understanding and management of eutrophication. Limnol Oceanogr 51:356–363CrossRefGoogle Scholar
  54. Schindler DW, Beaty K, Fee EJ, Cruikshank D, de Bruyn E, Findlay D, Linsey G, Shearer JA, Stainton M, Turner MA (1990) Effects of climatic warming on lakes of the western Boreal forest. Science 250:967–970CrossRefGoogle Scholar
  55. Schindler DW, Bayley SE, Parker BR, Beaty KG, Cruikshank DR, Fee EJ, Schindler EU, Stainton MP (1996) The effects of climatic warming on the properties of boreal lakes and streams at the Experimental Lakes Area, northwestern Ontario. Limnol Oceanogr 41:1004–1017CrossRefGoogle Scholar
  56. Shiga Prefecture (1963–2000) Annual report of the regular observation in Lake Biwa. Fisheries Experimental Station of Shiga Prefecture (in Japanese)Google Scholar
  57. Straile D, Jöhnk K, Rossknecht H (2003) Complex effects of winter warming on the physicochemical characteristics of a deep lake. Limnol Oceanogr 48:1432–1438CrossRefGoogle Scholar
  58. Sugawara K (1938) The seasonal variation of the occurrence of phytoplankton and the circulation of silicon in Lake Biwa. Jpn J Limnol 8:434–445 (in Japanese)Google Scholar
  59. Talling JF (1966) The annual cycle of stratification and phytoplankton growth in Lake Victoria (East Africa). Int Rev Hydrobiol 51:545–621CrossRefGoogle Scholar
  60. ter Braak CJF (1995) Ordination. In: Jongman RHG, ter Braak CJF, van Tongeren OFR (eds) Data analysis in community and landscape ecology. Cambridge University Press, Cambridge, pp 91–173CrossRefGoogle Scholar
  61. ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca (500 pp)Google Scholar
  62. Tezuka Y (1984) Seasonal variations of dominant phytoplankton, chlorophyll a and nutrient levels in the pelagic regions of Lake Biwa. Jpn J Limnol 45:26–37Google Scholar
  63. The Shiga Prefectural Institute of Public Health and Environmental Science (1978–2000) White paper on the environment of Shiga Prefecture. Shiga Prefecture, Japan (in Japanese)Google Scholar
  64. The Shiga Prefectural Institute of Public Health and Environmental Science (1984-1986, 1991, 1995, 2000) Compilation report of phytoplankton data in Lake Biwa. Shiga Prefecture, Otsu (in Japanese)Google Scholar
  65. Tsugeki N, Oda H, Urabe J (2003) Fluctuation of the zooplankton community in Lake Biwa during the 20th century: a paleolimnological analysis. Limnology 4:101–107CrossRefGoogle Scholar
  66. Tsugeki NK, Ishida S, Urabe J (2009) Sedimentary records of reduction in resting egg production of Daphnia galeata in Lake Biwa during the 20th century: a possible effect of winter warming. J Paleolimnol 42:155–165CrossRefGoogle Scholar
  67. Tuji A, Houki A (2001) Centric diatoms in Lake Biwa. Lake Biwa Study Monogr 9:1–90Google Scholar
  68. Urabe J, Sekino T, Nozaki K, Tsuji A, Yoshimizu C, Kagami M, Koitabashi T, Miyazaki T, Nakanishi M (1999) Light, nutrients and primary productivity in Lake Biwa. Ecol Res 14:233–242CrossRefGoogle Scholar
  69. Verburg P, Hecky RE, Kling H (2003) Ecological consequences of a century of warming in Lake Tanganyika. Science 301:505–507CrossRefGoogle Scholar
  70. Yamada Y, Nakanishi M (1999) Regional development, urbanization and water, and changes in material cycling. In: Wada E, Yasunari T (eds) Changes in systems of water and material cycling. Iwanami-Shoten, Tokyo, pp 89–113 (in Japanese)Google Scholar
  71. Yamamoto K, Nakamura M (2004) An examination of land use controls in the Lake Biwa watershed from the perspective of environmental conservation and management. Lakes Res 9:217–228CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Narumi K. Tsugeki
    • 1
    • 5
  • Jotaro Urabe
    • 1
  • Yuichi Hayami
    • 2
  • Michinobu Kuwae
    • 3
  • Masami Nakanishi
    • 4
  1. 1.Graduate School of Life ScienceTohoku UniversitySendaiJapan
  2. 2.Ariake Sea Research ProjectSaga UniversitySagaJapan
  3. 3.Senior Research Fellow CenterEhime UniversityMatsuyamaJapan
  4. 4.Research Institute for Humanity and NatureKyotoJapan
  5. 5.Centre for Marine Environmental Studies (CMES)Ehime UniversityMatsuyamaJapan

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