Journal of Paleolimnology

, Volume 42, Issue 2, pp 155–165 | Cite as

Sedimentary records of reduction in resting egg production of Daphnia galeata in Lake Biwa during the 20th century: a possible effect of winter warming

  • Narumi K. TsugekiEmail author
  • Seiji Ishida
  • Jotaro Urabe
Original Paper


To clarify long-term variations in the resting egg production of Daphnia galeata in Lake Biwa during the 20th century, we examined an abundance of plankton remains and ephippia in a 26-cm sediment core with a time resolution of approximately 2–6 years. Historical changes shown by these plankton remains indicated that the Daphnia population has not produced resting eggs since the 1980s, but it has remained the most abundant zooplankton species in the lake. Plankton monitoring data collected from 1966 to 2000 revealed that the overwintering individuals (January–March) of D. galeata plankters showed a significant increasing trend in recent years, such increase being negatively correlated with ephippial abundance in the sediment samples. Further analyses showed that the dominant phytoplankton in winter has changed from large inedible diatoms to edible flagellated algae, probably due to changes in vertical mixing regimes resulting from winter warming. These changes that occurred in the last several decades suggest that global warming has improved winter food conditions and thus enabled the Daphnia plankton to maintain its population without producing resting eggs in Lake Biwa.


Daphnia Resting eggs Winter warming 20th century Lake Biwa Zooplankton 



We wish to thank J. J. Elser, M. Kyle, W. Makino and two anonymous reviewers for comments, and J. Togari, T. Koitabashi and T. Miyano and Drs. T. Ishikawa and F. Hyodo for field assistance. This study was funded by a Grant-in-Aid for Scientific Research of 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 Research Fellowship from the Japan Society for the Promotion of Science for Young Scientists to NKT.


  1. Ahlgren G, Lundstedt L, Brett M, Forsberg CJ (1990) Lipid composition and food quality of some freshwater phytoplankton for cladoceran zooplankters. J Plankton Res 12:809–818CrossRefGoogle Scholar
  2. Alekseev V, Lampert W (2001) Maternal control of resting-egg production in Daphnia. Nature 414:899–901CrossRefGoogle Scholar
  3. Anneville O, Soussi S, Gammeter S, Straile D (2004) Seasonal and inter-annual scales of variability in phytoplankton assemblages: comparison of phytoplankton dynamics in 3 pre-alpine lakes over a period of 28 years. Freshw Biol 49:98–115CrossRefGoogle Scholar
  4. Battarbee RW (1986) Diatom analysis. In: Berglund BE (ed) Handbook of holocene palaeoecology and palaeohydrology. Wiley, Chichester, pp 527–570Google Scholar
  5. Cáceres CE (1997) Temporal variation, dormancy, and coexistence: a field test of the storage effect. Proc Natl Acad Sci USA 94:9171–9175CrossRefGoogle Scholar
  6. Cáceres CE (1998) Interspecific variation in the abundance, production, and emergence of Daphnia diapausing eggs. Ecology 79:1699–1710Google Scholar
  7. Cáceres CE, Tessier AJ (2004a) Incidence of diapause varies among populations of Daphnia pulicaria. Oecologia 141:425–431CrossRefGoogle Scholar
  8. Cáceres CE, Tessier AJ (2004b) To sink or swim: variable diapause strategies among Daphnia species. Limnol Oceanogr 49:1333–1340Google Scholar
  9. Cáceres CE, Christoff AN, Boeing WJ (2007) Variation in ephippial buoyancy in Daphnia pulicaria. Freshw Biol 52:313–318CrossRefGoogle Scholar
  10. Carpenter SR, Kitchell JF (1993) The trophic cascade in lakes. Cambridge University Press, CambridgeGoogle Scholar
  11. Ebert D, Haag C, Kirkpatrick M, Riek M, Hottinger JW, Pajunen VI (2002) A selective advantage to immigrant genes in a Daphnia metapopulation. Science 295:485–488CrossRefGoogle Scholar
  12. 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
  13. Frey DG (1986) Cladocera analysis. In: Berglund BE (ed) Handbook of holocene palaeoecology and palaeohydrology. Wiley, Chichester, pp 667–692Google Scholar
  14. Hairston NGJR (1998) Time travelers: what’s timely in diapause research. Archiv für Hydrobiol Adv Limnol 52:1–15Google Scholar
  15. Hairston NGJR, Lampert W, Cáceres CE, Holtmeier CL, Weider LJ, Gaedke U, Fischer JM, Fox JA, Post DM (1999) Dormant eggs record rapid evolution. Nature 401:446CrossRefGoogle Scholar
  16. 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
  17. Hikone Meteorological Observatory (1993–2000) Shigaken No Kisho. Hikone Meteorological Observatory, Shiga (in Japanese)Google Scholar
  18. 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
  19. Ichise S, Wakabayashi T, Matsuoka Y, Yamanaka S, Fujiwara N, Nomura K (1996) Succession of phytoplankton in northern basin of Lake Biwa, 1978–1995. Rep Shiga Pref Inst Public Health Environ Sci 31:84–100 (in Japanese)Google Scholar
  20. 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 Public Health Environ Sci 36:29–35 (in Japanese)Google Scholar
  21. Jankowski T (2002) From diapause to sexual reproduction: evolutionary ecology of the Daphnia hybrid complex from Lake Constance. PhD thesis. Univ of Konstanz, Konstanz, GermanyGoogle Scholar
  22. Jankowski T, Straile D (2003) A comparison of egg-bank and long-term plankton dynamics of two Daphnia species, D. hyalina and D. galeata: potentials and limits of reconstruction. Limnol Oceanogr 48:1948–1955Google Scholar
  23. Jeppesen E, Leavitt P, DeMeester L, Jensen JP (2001) Functional ecology and palaeolimnology: using cladoceran remains to reconstruct anthropogenic impact. Trends Ecol Evol 16:191–198CrossRefGoogle Scholar
  24. Keller B, Spaak P (2004) Nonrandom sexual reproduction and diapausing egg production in a Daphnia hybrid species complex. Limnol Oceanogr 49:1393–1400Google Scholar
  25. Keller B, Bürgi HR, Sturm M, Spaak P (2002) Ephippia and Daphnia abundances under changing trophic conditions. Verh Int Verein Limnol 28:851–855Google Scholar
  26. 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
  27. LaMontagne JM, McCauley E (2001) Maternal effects in Daphnia: what mothers are telling their offspring and do they listen? Ecol Lett 4:64–71CrossRefGoogle Scholar
  28. Lynch M (1983) Ecological genetics of Daphnia pulex. Evolution 37:358–374CrossRefGoogle Scholar
  29. 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
  30. Miura T, Cai QH (1990) Annual and seasonal occurrences of the zooplankters observed in the northern basin of Lake Biwa from 1965–1979. Lake Biwa Study Monogr 5:1–35Google Scholar
  31. Mori S, Yamamoto K, Negoro K, Horie S, Suzuki N (1967) First report of the regular limnological survey of Lake Biwa (Oct. 1965–Dec. 1966). I. General Remark. Mem Fac Sci Kyoto Univ (B) 1:36–40Google Scholar
  32. 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
  33. Nakanishi M, Sekino T (1996) Recent drastic changes in Lake Biwabio-communities, with special attention to exploitation of the littoral zone. GeoJournal 40:63–67CrossRefGoogle Scholar
  34. 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 46:1228–1236Google Scholar
  35. Rellstab C, Maurer V, Zeh M, Bürgi HR, Spaak P (2007) Temporary collapse of the Daphnia population in turbid and ultra-oligotrophic Lake Brienz. Aquat Sci 69:257–270CrossRefGoogle Scholar
  36. Reynolds CS (1984) Periodicity and change in phytoplankton composition. In: Reynolds CS (ed) The ecology of freshwater phytoplankton. Cambridge University Press, UK, pp 277–328Google Scholar
  37. 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
  38. 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
  39. Schindler DW (2006) Recent advances in the understanding and management of eutrophication. Limnol Oceanogr 51:356–363Google Scholar
  40. Schindler DW, Beaty KG, Fee EJ, Cruikshank DR, Bruyn ER, Findlay DL, Linsey GA, Shearer JA, Stainton MP, Turner MA (1990) Effects of climatic warming on lakes of the central boreal forest. Science 250:967–970CrossRefGoogle Scholar
  41. 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 41:1004–1017Google Scholar
  42. Sekino T (1998) Role of nutritional status in vertical distribution of Daphnia galeata. PhD thesis, Kyoto University, Kyoto, JapanGoogle Scholar
  43. Shiga Prefecture (1963–2000) The regular observation in Lake Biwa. Fisheries Experimental Station of Shiga Prefecture (in Japanese)Google Scholar
  44. Ślusarczyk M (2001) Food threshold for diapause in Daphnia under the threat of fish predation. Ecology 82:1089–1096Google Scholar
  45. Straile D (2002) North Atlantic Oscillation synchronizes food-web interactions in central European lakes. Proc R Soc Lond B 269:391–395CrossRefGoogle Scholar
  46. Straile D, Geller W (1998) Crustacean zooplankton in Lake Constance from 1920 to 1995: response to eutrophication and re-oligotrophication. Arch Hydrobiol Special Issues Adv Limnol 53:255–274Google Scholar
  47. Straile D, Jöhnk K, Rossknecht H (2003) Complex effects of winter warming on the physicochemical characteristics of a deep lake. Limnol Oceanogr 48:1432–1438Google Scholar
  48. The Shiga Prefectural Institute of Public Health and Environmental Science (1979–2000) Annual report of water quality in Lake Biwa, Shiga Prefecture, Otsu (in Japanese)Google Scholar
  49. 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
  50. Tsugeki NK (2005) A paleolimnological approach on phytoplankton and zooplankton dynamics in Lake Biwa during the 20th century. PhD thesis, Kyoto University, Kyoto, JapanGoogle Scholar
  51. 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
  52. Urabe J, Kawabata K, Nakanishi M, Shimizu K (1996) Grazing and food size selection of zooplankton community in Lake Biwa during BITEX ’93. Jpn J Limnol 57:27–37Google Scholar
  53. Urabe J, Ishida S, Nishmoto M, Weider LJ (2003) Daphnia pulicaria; a zooplankton species that suddenly appeared in 1999 in the offshore zone of Lake Biwa. Limnology 4:35–41CrossRefGoogle Scholar
  54. Verburg P, Hecky RE, Kling H (2003) Ecological consequences of a century of warming in Lake Tanganyika. Science 301:505–507CrossRefGoogle Scholar
  55. Winder M, Schindler DE (2004) Climatic effects on the phenology of lake processes. Glob Change Biol 10:1844–1856CrossRefGoogle Scholar
  56. Yoshida T, Kagami M, Gurung TB, Urabe J (2001) Seasonal succession of zooplankton in the north basin of Lake Biwa. Aquat Ecol 35:19–29CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Narumi K. Tsugeki
    • 1
    • 2
    Email author
  • Seiji Ishida
    • 3
  • Jotaro Urabe
    • 4
  1. 1.Center for Ecological ResearchKyoto UniversityOtsuJapan
  2. 2.Ecology and Evolutionary Biology, Graduate School of Life SciencesTohoku UniversiySendaiJapan
  3. 3.Department of Biological SciencesState University of New York at BuffaloNYUSA
  4. 4.Graduate School of Life ScienceTohoku UniversitySendaiJapan

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