Advertisement

Hydrobiologia

, Volume 771, Issue 1, pp 131–150 | Cite as

Contrasting controls on phytoplankton dynamics in two large, pre-alpine lakes imply differential responses to climate change

  • Tina K. Bayer
  • Marc Schallenberg
  • Carolyn W. Burns
Primary Research Paper

Abstract

The effects of climate change on lake ecosystems are often complex. We examined how phytoplankton in two neighbouring, pre-alpine, large oligotrophic lakes with similar catchments and land uses are likely to respond to climate change. We hypothesised that (i) while their climates and landscape filters were relatively similar, differences in in-lake biological, physical and chemical filters would influence the phytoplankton responses to climate and (ii) direct effects of warming on phytoplankton dynamics and productivity would be relatively minor compared to indirect effects, especially those influencing the lakes’ mixing regimes. We combined (i) dynamic modelling of the physical forcing of the lakes under climate change, (ii) multi-year field sampling of relevant biological, physical and chemical variables and (iii) bioassay experiments, to test our hypotheses. Water temperatures have warmed over recent decades in one lake, but not in the other. The warming lake showed evidence of incomplete mixing and phytoplankton layering in winter 2009, while the other lake did not. Such changes influenced the phytoplankton phenology, and incomplete winter mixing is common in similar deep, temperate lakes. Inhibited winter mixing and related indirect effects of climate warming appear to be key early drivers of climate change effects on the phytoplankton of deep, temperate lakes.

Keywords

Nutrient limitation Cyclotella New Zealand Oligotrophic Incomplete mixing Daphnia 

Notes

Acknowledgments

We thank all who assisted with field and lab work, especially Nicky McHugh. We also appreciate the logistical assistance of the Otago Regional Council (ORC) and Fish and Game Otago; we thank the National Institute for Water and Atmospheric Research (NIWA Ltd) and the ORC for providing climate and lake monitoring data, respectively. We are grateful to two reviewers whose suggestions have been very helpful in improving our paper. The research was funded by the Department of Zoology, University of Otago, a University of Otago Doctoral Scholarship (to TKB), the Ministry of Business, Innovation and Employment and the National Institute of Water and Atmospheric Research (to MS and CWB).

References

  1. Adrian, R., S. Wilhelm & D. Gerten, 2006. Life-history traits of lake plankton species may govern their phenological response to climate warming. Global Change Biology 12: 652–661.CrossRefGoogle Scholar
  2. Ambrosetti, W. & L. Barbanti, 2001. Temperature, mixing, heat content and stability in Lake Orta: a pluriannual investigation. Journal of Limnology 60: 60–68.CrossRefGoogle Scholar
  3. Ambrosetti, W., L. Barbanti & N. Sala, 2003. Residence time and physical processes in lake. Journal of Limnology 62: 1–15.CrossRefGoogle Scholar
  4. Anneville, O., S. Souissi, F. Ibanez, V. Ginot, J. C. Druart & N. Angeli, 2002. Temporal mapping of phytoplankton assemblages in Lake Geneva: annual and interannual changes in their patterns of succession. Limnology and Oceanography 45: 1355–1366.CrossRefGoogle Scholar
  5. Anneville, O., S. Gammeter & D. Straile, 2005. Phosphorus decrease and climate variability: mediators of synchrony in phytoplankton changes among European peri-alpine lakes. Freshwater Biology 50: 1731–1746.CrossRefGoogle Scholar
  6. Arhonditsis, G. B., M. Winder, M. T. Brett & D. E. Schindler, 2004. Patterns and mechanisms of phytoplankton variability in Lake Washington (USA). Water Research 38: 4013–4027.CrossRefPubMedGoogle Scholar
  7. Baigún, C. & M. C. Marinone, 1995. Cold—temperate lakes of South America: do they fit Northern Hemisphere models? Archiv für Hydrobiolgie 135: 23–51.Google Scholar
  8. Bayer, T. K., 2013. Effects of climate change on two large, deep oligotrophic lakes in New Zealand. Ph.D thesis, University of Otago, Dunedin, 221.Google Scholar
  9. Bayer, T. K., C. W. Burns & M. Schallenberg, 2013. Application of a numerical model to predict impacts of climate change on water temperatures in two deep, oligotrophic lakes in New Zealand. Hydrobiologia 713: 53–71.CrossRefGoogle Scholar
  10. Berger, S. A., S. Diehl, H. Stibor, G. Trommer, M. Ruhenstroth, A. Wild, A. Weigert, C. G. Jager & M. Striebel, 2007. Water temperature and mixing depth affect timing and magnitude of events during spring succession of the plankton. Oecologia 150: 643–654.CrossRefPubMedGoogle Scholar
  11. Bleiker, W. & F. Schanz, 1997. Light climate as the key factor controlling the spring dynamics of phytoplankton in Lake Zürich. Aquatic Sciences 59: 135–157.CrossRefGoogle Scholar
  12. Blenckner, T., 2005. A conceptual model of climate-related effects on lake ecosystems. Hydrobiologia 533: 1–14.CrossRefGoogle Scholar
  13. Boehrer, B., R. Fukuyama & K. Chikita, 2008. Stratification of very deep thermally stratified lakes. Geophysical Research Letters 35: L16405. doi: 10.1029/2008GL034519.CrossRefGoogle Scholar
  14. Burns, C. W., 2013. Predictors of invasion success by Daphnia species: influence of food, temperature and species identity. Biological Invasions 15: 859–869.CrossRefGoogle Scholar
  15. Burns, C. W. & M. Schallenberg, 1998. Impacts of nutrients and zooplankton on the microbial food web of an ultra-oligotrophic lake. Journal of Plankton Research 20: 1501–1525.CrossRefGoogle Scholar
  16. Burns, C. W. & M. Schallenberg, 2001. Calanoid copepods versus cladocerans: consumer effects on protozoa in lakes of different trophic status. Limnology and Oceanography 46: 1558–1565.CrossRefGoogle Scholar
  17. Burns, N. M. & J. C. Rutherford, 1998. Results of monitoring New Zealand Lakes, 1992–1996. NIWA Client Report: MFE80216. Ministry for the Environment, Wellington.Google Scholar
  18. Callieri, C., B. Modenutti, C. Queimaliños, R. Bertoni & E. Balseiro, 2007. Production and biomass of picophytoplankton and larger autotrophs in Andean ultraoligotrophic lakes: differences in light harvesting efficiency in deep layers. Aquatic Ecology 45: 511–523.CrossRefGoogle Scholar
  19. Carrick, H., R. P. Barbiero & M. Tuchman, 2001. Variation in Lake Michigan Plankton: temporal, spatial and historical trends. Journal of Great Lakes Research 27: 467–485.CrossRefGoogle Scholar
  20. Chapman, M. A., J. D. Green & V. H. Jolly, 1975. Zooplankton. In Jolly, V. H. & J. M. A. Brown (eds), New Zealand Lakes. Auckland University Press, Auckland: 209–230.Google Scholar
  21. Coats, R., G. Sahoo, J. Riverson, M. Costa-Cabral, M. Dettinger, B. Wolfe, J. Reuter, G. Schladow & C. R. Goldman, 2013. Historic and likely future impacts of climate change on Lake Tahoe, California-Nevada, USA. In Goldman, C. R., M. Kumagai & R. D. Robarts (eds), Climate Change and Global Warming of Inland Waters: Impacts and Mitigation for Ecosystems and Societies. John Wiley & Sons, New York: 231–254.Google Scholar
  22. Davies-Colley, R. J., 1988. Mixing depths in New Zealand lakes. New Zealand Journal of Marine and Freshwater Research 22: 517–528.CrossRefGoogle Scholar
  23. De Los Ríos, P., E. Hauenstein & M. Romero, 2012. Use of null models to explain crustacean zooplankton assemblages in waterbodies of Alerce Andino National Park (41°S, Chile). Crustaceana 85: 713–722.CrossRefGoogle Scholar
  24. Diehl, S., 2002. Phytoplankton, light, and nutrients in a gradient of mixing depths: theory. Ecology 83: 386–398.CrossRefGoogle Scholar
  25. Dokulil, M. T., K. Teubner, A. Jagsch, U. Nickus, R. Adrian, D. Straile, T. Jankowski, A. Herzig & J. Padisak, 2010. The impact of climate change on lakes in Central Europe. In George, G. (ed.), The Impact of Climate Change on European Lakes, Vol. 4. Springer, Netherlands: 387–409.CrossRefGoogle Scholar
  26. Duggan, I., J. Green & D. Burger, 2006. First New Zealand records of three non-indigenous zooplankton species: skistodiaptomus pallidus, Sinodiaptomus valkanovi, and Daphnia dentifera. New Zealand Journal of Marine and Freshwater Research 40: 561–569.CrossRefGoogle Scholar
  27. Duggan, I., K. Robinson, C. W. Burns, J. Banks & I. Hogg, 2012. Identifying invertebrate invasions using morphological and molecular analyses: north American Daphnia ‘pulex’ in New Zealand fresh waters. Aquatic Invasions 7: 585–590.CrossRefGoogle Scholar
  28. Duthie, H. C. & V. Stout, 1986. Phytoplankton periodicity of the Waitaki Lakes, New Zealand. Hydrobiologia 138: 221–236.CrossRefGoogle Scholar
  29. Fahnenstiel, G., S. Pothoven, H. Vanderploeg, D. Klarer, T. Nalepa & D. Scavia, 2010. Recent changes in primary production and phytoplankton in the offshore region of southeastern Lake Michigan. Journal of Great Lakes Research 36: 20–29.CrossRefGoogle Scholar
  30. Feuchtmayr, H., S. J. Thackeray, I. D. Jones, M. De Ville, J. Fletcher, B. E. N. James & J. Kelly, 2011. Spring phytoplankton phenology–are patterns and drivers of change consistent among lakes in the same climatological region? Freshwater Biology 57: 331–344.CrossRefGoogle Scholar
  31. Findlay, D. L., S. E. M. Kasian, M. P. Stainton, K. Beaty & M. Lyng, 2001. Climatic influences on algal populations of boreal forest lakes in the Experimental Lakes Area. Limnology and Oceanography 46: 1784–4793.CrossRefGoogle Scholar
  32. Flint, E., 1975. Phytoplankton in some New Zealand lakes. In Jolly, V. & J. M. A. Brown (eds), New Zealand Lakes. Auckland University Press and Oxford University Press, Oxford: 161–192.Google Scholar
  33. Gallina, N., O. Anneville & M. Beniston, 2011. Impacts of extreme air temperatures on cyanobacteria in five deep peri-Alpine lakes. Journal of Limnology 70: 186–196.CrossRefGoogle Scholar
  34. Green, J. D., A. B. Viner & D. J. Lowe, 1987. The effects of climate on lake mixing patterns and temperatures. In Viner, A. B. (ed.), Inland Waters of New Zealand. Department of Scientific and Industrial Research, Bangalore: 65–96.Google Scholar
  35. Goldman, C., & A. D. Jassby, 1990. Spring mixing and annual primary production at Lake Tahoe, California-Nevada. Verhandlungen der Internationale Vereinigung für Theoretische und Angewandte Limnologie 24: 504.Google Scholar
  36. Goldman, C., A. Jassby & T. Powell, 1989. Interannual fluctuations in primary production: meteorological forcing at two subalpine lakes. Limnology and Oceanography 34: 310–323.Google Scholar
  37. Guildford, S. J., H. A. Bootsma, E. J. Fee, R. E. Hecky & G. Patterson, 2000. Phytoplankton nutrient status and mean water column irradiance in Lakes Malawi and Superior. Aquatic Ecosystem Health and Management 3: 35–45.CrossRefGoogle Scholar
  38. Hadley, K., A. M. Paterson, R. I. Hall & J. P. Smol, 2013. Effects of multiple stressors on lakes in south-central Ontario: 15 years of change in lakewater chemistry and sedimentary diatom assemblages. Aquatic Sciences 75: 349–360.CrossRefGoogle Scholar
  39. Hamill, K., 2006. Snapshot of Lake Water Quality in New Zealand. Ministry for the Environment, Wellington.Google Scholar
  40. Hamilton, D. P., C. R. O’Brien, M. A. Burford, J. D. Brooks & C. G. McBride, 2010. Vertical distributions of chlorophyll in deep, warm monomictic lakes. Aquatic Sciences 72: 295–307.CrossRefGoogle Scholar
  41. Hamilton, D. P., C. G. McBride, D. Özkundakci, M. Schallenberg, P. Verburg, M. D. Winton, D. Kelly, C. Hendy & W. Ye, 2013. Effects of climate change on New Zealand Lakes. In Goldman, C. R., M. Kumagai & R. D. Robarts (eds), Climate Change and Global Warming of Inland Waters: Impacts and Mitigation for Ecosystems and Societies. John Wiley & Sons, New York: 337–366.Google Scholar
  42. Hampton, S., L. Izemeteva, M. Moore, S. Katz, B. Dennis & E. Silow, 2008. Sixty years of environmental change in the world’s largest freshwater lake–Lake Baikal, Siberia. Global Change Biology 14: 1–12.CrossRefGoogle Scholar
  43. Hylander, S., T. Jephson, K. Lebret, J. Von Einem, T. Fagerberg, E. Balseiro, B. Modenutti, M. S. Souza, C. Laspoumaderes, M. Jonsson, P. Ljungberg, A. Nicolle, P. A. Nilsson, L. Ranaker & L. A. Hansson, 2011. Climate-induced input of turbid glacial meltwater affects vertical distribution and community composition of phyto- and zooplankton. Journal of Plankton Research 33: 1239–1248.CrossRefGoogle Scholar
  44. Irwin, A., 1972. Lake Wakatipu. Bathymetry. In, Lake Chart Series. Department of Scientific and Industrial Research, Wellington.Google Scholar
  45. Irwin, A., 1976. Lake Wanaka. Bathymetry. In, Lake Chart Series. Department of Scientific and Industrial Research, Wellington.Google Scholar
  46. Jäger, C. G., S. Diehl & G. M. Schmidt, 2008. Influence of water-column depth and mixing on phytoplankton biomass, community composition, and nutrients. Limnology and Oceanography 53: 2361–2373.CrossRefGoogle Scholar
  47. James, M. R., M. Schallenberg, M. Gall & R. Smith, 2001. Seasonal changes in plankton and nutrient dynamics and carbon flow in the pelagic zone of a large, glacial lake: effects of suspended solids and physical mixing. New Zealand Journal of Marine and Freshwater Research 35: 239–253.CrossRefGoogle Scholar
  48. Jolly, H. & M. Chapman, 1977. The comparative limnology of some New Zealand lakes. 2 Plankton. New Zealand Journal of Marine and Freshwater Research 11: 307–340.CrossRefGoogle Scholar
  49. Katz, S. L., S. E. Hampton, L. R. Izmesteva & M. V. Moore, 2011. Influence of long-distance climate teleconnection on seasonality of water temperature in the world’s largest lake–Lake Baikal,Siberia. PLoS One 6: e14688.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Kirk, J. T. O., 1994. Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  51. Kishimoto, N., S. Ichese, K. Suzuki & C. Yamamoto, 2013. Analysis of long-term variation in phytoplankton biovolume in the northern basin of Lake Biwa. Limnology 14: 117–128.CrossRefGoogle Scholar
  52. Leathwick, J. R., D. West, P. Gerbeaux, D. Kelly, H. Robertson, D. Brown, W. L. Chadderton & A.-G. Ausseil, 2014. Freshwater Ecosystems of New Zealand (FENZ) geodatabase. Department of Conservation, Wellington. http://www.doc.govt.nz/conservation/land-and-freshwater/freshwater/freshwater-ecosystems-of-new-zealand/
  53. Livingstone, M. E., B. J. Biggs & J. S. Gifford, 1986. Inventory of New Zealand lakes. Water and Soil miscellaneous publication: 80–81.Google Scholar
  54. Magnuson, J. J., B. J. Benson & T. K. Kratz, 1990. Temporal coherence in the limnology of a suite of lakes in Wisconsin. Freshwater Biology 23: 145–159.CrossRefGoogle Scholar
  55. Mida, J. L., D. Scavia, G. L. Fahnenstiel, S. A. Pothoven, H. A. Vanderploeg & D. M. Dolan, 2010. Long-term and recent changes in Southern Lake Michigan water quality with implications for present trophic status. Journal of Great Lakes Research 36: 42–49.CrossRefGoogle Scholar
  56. Modenutti, B., E. Balseiro, C. Queimalinos, D. A. Anon Suarez, M. C. Diegues & R. J. Albarino, 1998. Structure and dynamics of food webs in Andean Lakes. Lakes and Reservoirs: Research and Management 3: 179–186.CrossRefGoogle Scholar
  57. Modenutti, B., E. Balseiro, M. B. Navarro, C. Laspoumaderes, M. S. Souza & F. Cuassolo, 2013. Environmental changes affecting light climate in oligotrophic mountain lakes: the deep chlorophyll maxima as a sensitive variable. Aquatic Sciences 75: 361–371.CrossRefGoogle Scholar
  58. Moss, B. D., 2012. Cogs in the endless machine: lakes, climate change and nutrient cycles: a review. Science of the Total Environment 434: 130–142.CrossRefPubMedGoogle Scholar
  59. Moss, B., D. Mckee, D. Atkinson, S. E. Collings, J. W. Eaton, A. B. Gill, I. Harvey, K. Hatton, T. Heyes & D. Wilson, 2003. How important is climate? Effects of warming, nutrient addition and fish on phytoplankton in shallow lake microcosms. Journal of Applied Ecology 40: 782–792.CrossRefGoogle Scholar
  60. Mullan, B., D. Wratt, S. Dean, M. Hollis, S. Allan, T. Williams & G. Kenny, 2008. Climate Change Effects and Impacts Assessment: A Guidance Manual for Local Government 2nd edition. New Zealand Ministry for the Environment, Wellington. http://www.mfe.govt.nz/sites/default/files/climate-change-effect-impacts-assessment-may08.pdf
  61. Naismith, M. M., 1994. Phytoplankton distribution in a lake-river reservoir system, South Island, New Zealand. University of Otago, Dunedin. Post Graduate Diploma Thesis in Zoology.Google Scholar
  62. O’Reilly, C. M., S. R. Alin, P.-D. Plisnier, A. S. Cohen & B. A. Mckee, 2003. Climate change decreases aquatic ecosystem productivity of Lake Tanganyika, Africa. Nature 424: 766–768.CrossRefPubMedGoogle Scholar
  63. Palmer, M. E., N. D. Yan & K. M. Somers, 2014. Climate change drives coherent patterns in physics and oxygen content in North American lakes. Climatic Change 124: 285–299.CrossRefGoogle Scholar
  64. Peeters, F., D. Livingstone, G.-H. Goudsmit, R. Kipfer & R. Forster, 2002. Modeling 50 years of historical temperature profiles in a large central European lake. Limnology and Oceanography 47: 186–197.CrossRefGoogle Scholar
  65. Peeters, F., D. Straile, A. Lorke & D. M. Livingstone, 2007. Earlier onset of the spring phytoplankton bloom in lakes of the temperate zone in a warmer climate. Global Change Biology 13: 1898–1909.CrossRefGoogle Scholar
  66. Pickrill, R. & J. Irwin, 1982. Predominant headwater inflow and its control of lake-river interactions in Lake Wakatipu. New Zealand Journal of Marine and Freshwater Research 16: 201–213.CrossRefGoogle Scholar
  67. Rae, R., C. Howard-Williams, I. I. Hawes, A. M. Schwarz & W. Vincent, 2001. Penetration of solar ultraviolet radiation into New Zealand lakes: influence of dissolved organic carbon and catchment vegetation. Limnology 2: 79–89.CrossRefGoogle Scholar
  68. Reynolds, C. S., 1997. Vegetation processes in the pelagic: a model for ecosystem theory. Ecology Institute Nordbünte, Germany.Google Scholar
  69. Reynolds, C., 2006. The Ecology of Phytoplankton. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  70. Riley, G. A., 1957. Phytoplankton of the North Central Sargasso Sea, 1950–52. Limnology and Oceanography 2: 252–270.Google Scholar
  71. Rühland, K., A. Paterson & J. P. Smol, 2008. Hemispheric-scale patterns of climate-related shifts in planktonic diatoms from North American and European lakes. Global Change Biology 14: 2740–2754.Google Scholar
  72. Rühland, K., A. Paterson & J. P. Smol, 2015. Lake diatom responses to warming: reviewing the evidence. Journal of Paleolimnology 54: 1–35.CrossRefGoogle Scholar
  73. Salmaso, N., 2005. Effects of climatic fluctuations and vertical mixing on the interannual trophic variability of Lake Garda, Italy. Limnology and Oceanography 50: 553–565.CrossRefGoogle Scholar
  74. Salmaso, N., 2010. Long-term phytoplankton community changes in a deep subalpine lake: responses to nutrient availability and climatic fluctuations. Freshwater Biology 55: 825–846.CrossRefGoogle Scholar
  75. Salmaso, N., R. Mosello, L. Garibaldi, F. Decet, M. C. Brizzio & P. Cordella, 2003. Vertical mixing as a determinant of trophic status in deep lakes: a case study from two lakes south of the Alps (Lake Garda and Lake Iseo). Journal of Limnology 62: 33–41.CrossRefGoogle Scholar
  76. Schallenberg, M. & C. W. Burns, 2001. Tests of autotrophic picoplankton as early indicators of nutrient enrichment in an ultra-oligotrophic lake. Freshwater Biology 46: 27–37.CrossRefGoogle Scholar
  77. Schallenberg, M., M. D. de Winton, P. Verburg, D. J. Kelly, K. D. Hamill & D. P. Hamilton, 2013. Ecosystem services of lakes. In Dymond, J. R. (ed.), Ecosystem Services in New Zealand: Conditions and Trends. Manaaki Whenua Press, Lincoln: 203–225.Google Scholar
  78. Schallenberg, M., M. James, I. I. Hawes & C. Howard-Williams, 1999. External forcing by wind and turbid inflows on a deep glacial lake and implications for primary production. New Zealand Journal of Marine and Freshwater Research 33: 311–331.CrossRefGoogle Scholar
  79. Schindler, D. W., 1987. Detecting ecosystem responses to anthropogenic stress. Canadian Journal of Fisheries and Aquatic Sciences 44(Suppl. 1): 6–25.CrossRefGoogle Scholar
  80. Schneider, P. & S. J. Hook, 2010. Space observations of inland water bodies show rapid surface warming since 1985. Geophysical Research Letters 37: L22405.CrossRefGoogle Scholar
  81. Sommer, U. & A. Lewandowska, 2011. Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton. Global Change Biology 17: 154–162.CrossRefGoogle Scholar
  82. Sommer, U., R. Adrian, L. De Senerpont Domis, J. J. Elser, U. Gaedke, B. Ibelings, E. Jeppesen, M. Lürling, J. C. Molinero, W. M. Mooij, E. Van Donk & M. Winder, 2012. Beyond the plankton ecology group (PEG) model: mechanisms driving plankton succession. Annual Review of Ecology, Evolution, and Systematics 43: 429–448.CrossRefGoogle Scholar
  83. Sorvari, S., A. Korhola & R. Thompson, 2002. Lake diatom response to recent Arctic warming in Finnish Lappland. Global Change Biology 8: 171–181.CrossRefGoogle Scholar
  84. Soto, D., 2002. Oligotrophic patterns in southern Chilean lakes: the relevance of nutrients and mixing depth. Revista Chilena de Historia Natural 75: 377–393.CrossRefGoogle Scholar
  85. Soto, D. & L. Zuniga, 1991. Zooplankton assemblages of Chilean temperate lakes: a comparison with North American counterparts. Revista Chilena de Historia Natural 64: 569–581.Google Scholar
  86. Stich, H. B. & A. Brinker, 2010. Oligotrophication outweighs effects of global warming in a large, deep, stratified lake ecosystem. Global Change Biology 16: 877–888.CrossRefGoogle Scholar
  87. Straile, D., 2005. Food webs in lakes–seasonal dynamics and the impact of climate variability. In Belgrano, A. (ed.), Aquatic Food Webs–An Ecosystem Approach. Oxford University Press, Oxford: 41–50.Google Scholar
  88. Straile, D., D. Livingstone, G. Weyhenmeyer & D. George, 2003. The response of freshwater ecosystems to climate variability associated with the North Atlantic Oscillation. In Hurrell, Y. K. W., G. Ottersen & M. Visbeck (eds), The North Atlantic Oscillation–Climatic Significance and Environmental Impact. AGU Geophysical Monograph Series, Salt Lake: 263–279.CrossRefGoogle Scholar
  89. Tirok, K. & U. Gaedke, 2007. The effect of irradiance, vertical mixing and temperature on spring phytoplankton dynamics under climate change: long-term observations and model analysis. Oecologia 150: 625–642.CrossRefPubMedGoogle Scholar
  90. Verburg, P., R. Hecky & H. Kling, 2003. Ecological consequences of a century of warming in Lake Tanganyika. Science 301: 505–507.CrossRefPubMedGoogle Scholar
  91. Vincent, W., 1983. Phytoplankton production and winter mixing: contrasting effects in two oligotrophic lakes. Journal of Ecology 71: 1–20.CrossRefGoogle Scholar
  92. Viner, A. B., 1985. Thermal stability and phytoplankton distribution. Hydrobiologia 125: 47–69.CrossRefGoogle Scholar
  93. Walsby, A. E., 1997. Numerical integration of phytoplankton photosynthesis through time and depth in a water column. New Phytologist 136: 189–209.CrossRefGoogle Scholar
  94. Wetzel, R. G. & G. E. Likens, 1991. Limnological Analysis. Springer, New York.CrossRefGoogle Scholar
  95. Weyhenmeyer, G. A., 2001. Warmer winters: are planktonic algal populations in Sweden’s largest lakes affected? AMBIO 30: 565–571.CrossRefPubMedGoogle Scholar
  96. White, E., M. Downes, M. M. Gibbs, L. Kemp, L. Mackenzie & G. Payne, 1980. Aspects of the physics, chemistry, and phytoplankton biology of Lake Taupo. New Zealand Journal of Marine and Freshwater Research 14: 139–148.CrossRefGoogle Scholar
  97. Winder, M. & D. E. Schindler, 2004a. Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85: 2100–2106.CrossRefGoogle Scholar
  98. Winder, M. & D. E. Schindler, 2004b. Climatic effects on the phenology of lake processes. Global Change Biology 10: 1844–1856.CrossRefGoogle Scholar
  99. Winder, M. & D. Hunter, 2008. Temporal organization of phytoplankton communities linked to physical forcing. Oecologia 156: 179–192.CrossRefPubMedGoogle Scholar
  100. Winder, M., J. E. Reuter & S. G. Schladow, 2009. Lake warming favours small-sized planktonic diatom species. Proceedings of the Royal Society B 276: 427–435.CrossRefPubMedPubMedCentralGoogle Scholar
  101. Winder, M., S. Berger, A. Lewandowska, N. Aberle, K. Lengfellner, U. Sommer & S. Diehl, 2012. Spring phenological responses of marine and freshwater plankton to changing temperature and light conditions. Marine Biology 159: 2491–2501.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Tina K. Bayer
    • 1
  • Marc Schallenberg
    • 1
  • Carolyn W. Burns
    • 1
  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand

Personalised recommendations