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.
Similar content being viewed by others
References
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.
Ambrosetti, W. & L. Barbanti, 2001. Temperature, mixing, heat content and stability in Lake Orta: a pluriannual investigation. Journal of Limnology 60: 60–68.
Ambrosetti, W., L. Barbanti & N. Sala, 2003. Residence time and physical processes in lake. Journal of Limnology 62: 1–15.
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.
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.
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.
Baigún, C. & M. C. Marinone, 1995. Cold—temperate lakes of South America: do they fit Northern Hemisphere models? Archiv für Hydrobiolgie 135: 23–51.
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.
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.
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.
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.
Blenckner, T., 2005. A conceptual model of climate-related effects on lake ecosystems. Hydrobiologia 533: 1–14.
Boehrer, B., R. Fukuyama & K. Chikita, 2008. Stratification of very deep thermally stratified lakes. Geophysical Research Letters 35: L16405. doi:10.1029/2008GL034519.
Burns, C. W., 2013. Predictors of invasion success by Daphnia species: influence of food, temperature and species identity. Biological Invasions 15: 859–869.
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.
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.
Burns, N. M. & J. C. Rutherford, 1998. Results of monitoring New Zealand Lakes, 1992–1996. NIWA Client Report: MFE80216. Ministry for the Environment, Wellington.
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.
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.
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.
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.
Davies-Colley, R. J., 1988. Mixing depths in New Zealand lakes. New Zealand Journal of Marine and Freshwater Research 22: 517–528.
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.
Diehl, S., 2002. Phytoplankton, light, and nutrients in a gradient of mixing depths: theory. Ecology 83: 386–398.
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.
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.
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.
Duthie, H. C. & V. Stout, 1986. Phytoplankton periodicity of the Waitaki Lakes, New Zealand. Hydrobiologia 138: 221–236.
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.
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.
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.
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.
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.
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.
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.
Goldman, C., A. Jassby & T. Powell, 1989. Interannual fluctuations in primary production: meteorological forcing at two subalpine lakes. Limnology and Oceanography 34: 310–323.
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.
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.
Hamill, K., 2006. Snapshot of Lake Water Quality in New Zealand. Ministry for the Environment, Wellington.
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.
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.
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.
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.
Irwin, A., 1972. Lake Wakatipu. Bathymetry. In, Lake Chart Series. Department of Scientific and Industrial Research, Wellington.
Irwin, A., 1976. Lake Wanaka. Bathymetry. In, Lake Chart Series. Department of Scientific and Industrial Research, Wellington.
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.
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.
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.
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.
Kirk, J. T. O., 1994. Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Cambridge.
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.
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/
Livingstone, M. E., B. J. Biggs & J. S. Gifford, 1986. Inventory of New Zealand lakes. Water and Soil miscellaneous publication: 80–81.
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.
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.
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.
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.
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.
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.
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
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.
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.
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.
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.
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.
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.
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.
Reynolds, C. S., 1997. Vegetation processes in the pelagic: a model for ecosystem theory. Ecology Institute Nordbünte, Germany.
Reynolds, C., 2006. The Ecology of Phytoplankton. Cambridge University Press, Cambridge.
Riley, G. A., 1957. Phytoplankton of the North Central Sargasso Sea, 1950–52. Limnology and Oceanography 2: 252–270.
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.
Rühland, K., A. Paterson & J. P. Smol, 2015. Lake diatom responses to warming: reviewing the evidence. Journal of Paleolimnology 54: 1–35.
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.
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.
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.
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.
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.
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.
Schindler, D. W., 1987. Detecting ecosystem responses to anthropogenic stress. Canadian Journal of Fisheries and Aquatic Sciences 44(Suppl. 1): 6–25.
Schneider, P. & S. J. Hook, 2010. Space observations of inland water bodies show rapid surface warming since 1985. Geophysical Research Letters 37: L22405.
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.
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.
Sorvari, S., A. Korhola & R. Thompson, 2002. Lake diatom response to recent Arctic warming in Finnish Lappland. Global Change Biology 8: 171–181.
Soto, D., 2002. Oligotrophic patterns in southern Chilean lakes: the relevance of nutrients and mixing depth. Revista Chilena de Historia Natural 75: 377–393.
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.
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.
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.
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.
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.
Verburg, P., R. Hecky & H. Kling, 2003. Ecological consequences of a century of warming in Lake Tanganyika. Science 301: 505–507.
Vincent, W., 1983. Phytoplankton production and winter mixing: contrasting effects in two oligotrophic lakes. Journal of Ecology 71: 1–20.
Viner, A. B., 1985. Thermal stability and phytoplankton distribution. Hydrobiologia 125: 47–69.
Walsby, A. E., 1997. Numerical integration of phytoplankton photosynthesis through time and depth in a water column. New Phytologist 136: 189–209.
Wetzel, R. G. & G. E. Likens, 1991. Limnological Analysis. Springer, New York.
Weyhenmeyer, G. A., 2001. Warmer winters: are planktonic algal populations in Sweden’s largest lakes affected? AMBIO 30: 565–571.
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.
Winder, M. & D. E. Schindler, 2004a. Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85: 2100–2106.
Winder, M. & D. E. Schindler, 2004b. Climatic effects on the phenology of lake processes. Global Change Biology 10: 1844–1856.
Winder, M. & D. Hunter, 2008. Temporal organization of phytoplankton communities linked to physical forcing. Oecologia 156: 179–192.
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.
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.
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).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: Judit Padisák
Rights and permissions
About this article
Cite this article
Bayer, T.K., Schallenberg, M. & Burns, C.W. Contrasting controls on phytoplankton dynamics in two large, pre-alpine lakes imply differential responses to climate change. Hydrobiologia 771, 131–150 (2016). https://doi.org/10.1007/s10750-015-2625-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-015-2625-2