Intermittent meromixis controls the trophic state of warming deep lakes
1.
Smith, V. H. & Schindler, D. W. Eutrophication science: where do we go from here?. Trends Ecol. Evol. 24, 201–207 (2009).
PubMed Google Scholar
2.
Steffen, W. et al. Planetary boundaries: guiding human development on a changing planet. Science 347, 1259855 (2015).
PubMed Google Scholar
3.
Carpenter, S. et al. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol. Appl. 8, 559–568 (1998).
Google Scholar
4.
Cohen, A. S. et al. Climate warming reduces fish production and benthic habitat in Lake Tanganyika, one of the most biodiverse freshwater ecosystems. Proc. Natl. Acad. Sci. 113, 9563–9568 (2016).
ADS CAS PubMed Google Scholar
5.
Fernández, J. E., Peeters, F. & Hofmann, H. Importance of the autumn overturn and anoxic conditions in the hypolimnion for the annual methane emissions from a temperate lake. Environ. Sci. Technol. 48, 7297–7304 (2014).
ADS Google Scholar
6.
Friedrich, J. et al. Investigating hypoxia in aquatic environments: diverse approaches to addressing a complex phenomenon. Biogeosciences 11, 1215–1259 (2014).
ADS Google Scholar
7.
Vollenweider, R. A. Advances in Defining Critical Loading Levels for Phosphorus in Lake Eutrophication (Mem. dell’Istituto Ital. di Idrobiol. Dott, Marco Marchi Verbania Pallanza, 1976).
Google Scholar
8.
Jenny, J.-P. et al. Inherited hypoxia: a new challenge for reoligotrophicated lakes under global warming. Glob. Biogeochem. Cycles 28, 1413–1423 (2014).
ADS CAS Google Scholar
9.
Matzinger, A. et al. Eutrophication of ancient Lake Ohrid: global warming amplifies detrimental effects of increased nutrient inputs. Limnol. Oceanogr. 52, 338–353 (2007).
ADS CAS Google Scholar
10.
Meire, L., Soetaert, K. E. R. & Meysman, F. J. R. Impact of global change on coastal oxygen dynamics and risk of hypoxia. Biogeosciences 10, 2633–2653 (2013).
ADS CAS Google Scholar
11.
Pachauri, R. K. et al. Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the fifth assessment report of the Intergovernmental Panel on Climate Change (IPCC, 2014).
12.
O’Reilly, C. M. et al. Rapid and highly variable warming of lake surface waters around the globe. Geophys. Res. Lett. 42, 10773–10781 (2015).
ADS Google Scholar
13.
Schmid, M., Hunziker, S. & Wüest, A. Lake surface temperatures in a changing climate: a global sensitivity analysis. Clim. Change 124, 301–315 (2014).
ADS Google Scholar
14.
Paerl, H. W. & Huisman, J. Blooms like it hot. Science 320, 57–58 (2008).
CAS Google Scholar
15.
Müller, B., Bryant, L. D., Matzinger, A. & Wüest, A. Hypolimnetic oxygen depletion in eutrophic lakes. Environ. Sci. Technol. 46, 9964–9971 (2012).
PubMed Google Scholar
16.
Adrian, R. et al. Lakes as sentinels of climate change. Limnol. Oceanogr. 54, 2283–2297 (2009).
ADS PubMed PubMed Central Google Scholar
17.
Butcher, J. B., Nover, D., Johnson, T. E. & Clark, C. M. Sensitivity of lake thermal and mixing dynamics to climate change. Clim. Change 129, 295–305 (2015).
ADS CAS Google Scholar
18.
Kirillin, G. Modeling the impact of global warming on water temperature and seasonal mixing regimes in small temperate lakes. Boreal Environ. Res. 15, 279–293 (2010).
Google Scholar
19.
Straile, D., Jöhnk, K. & Rossknecht, H. Complex effects of winter warming on the physicochemical characteristics of a deep lake. Limnol. Oceanogr. 48, 1432–1438 (2003).
ADS CAS Google Scholar
20.
Woolway, R. I. & Merchant, C. J. Worldwide alteration of lake mixing regimes in response to climate change. Nat. Geosci. 12, 271–276 (2019).
ADS CAS Google Scholar
21.
Boehrer, B., Fukuyama, R. & Chikita, K. Stratification of very deep, thermally stratified lakes. Geophys. Res. Lett. 35, 8–12 (2008).
Google Scholar
22.
Boehrer, B. & Schultze, M. Stratification of lakes. Rev. Geophys. 46, 1–27 (2008).
Google Scholar
23.
Boehrer, B., Rohden, C. Von & Schultze, M. Ecology of Meromictic Lakes. 228 (2017).
24.
Hall, K. J. & Northcote, T. G. Meromictic lakes. In Encyclopedia of Lakes and Reservoirs 519–524 (Springer, 2012).
25.
Søndergaard, M., Jensen, J. P. & Jeppesen, E. Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506–509, 135–145 (2003).
Google Scholar
26.
Hupfer, M. & Lewandowski, J. Oxygen controls the phosphorus release from lake sediments—a long-lasting paradigm in limnology. Int. Rev. Hydrobiol. 93, 415–432 (2008).
CAS Google Scholar
27.
Yankova, Y., Neuenschwander, S., Köster, O. & Posch, T. Abrupt stop of deep water turnover with lake warming: drastic consequences for algal primary producers. Sci. Rep. 7, 13770 (2017).
ADS PubMed PubMed Central Google Scholar
28.
Lehmann, M. et al. Powering up the “biogeochemical engine”: the impact of exceptional ventilation of a deep meromictic lake on the lacustrine redox, nutrient, and methane balances. Front. Earth Sci. 3, 45 (2015).
ADS Google Scholar
29.
Anneville, O., Gammeter, S. & Straile, D. Phosphorus decrease and climate variability: mediators of synchrony in phytoplankton changes among European peri-alpine lakes. Freshw. Biol. 50, 1731–1746 (2005).
CAS Google Scholar
30.
Posch, T., Köster, O., Salcher, M. M. & Pernthaler, J. Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming. Nat. Clim. Change 2, 809 (2012).
ADS CAS Google Scholar
31.
Winder, M. Lake warming mimics fertilization. Nat. Clim. Change 2, 771 (2012).
ADS CAS Google Scholar
32.
Coats, R., Perez-Losada, J., Schladow, G., Richards, R. & Goldman, C. The warming of Lake Tahoe. Clim. Change 76, 121–148 (2006).
ADS Google Scholar
33.
Kraemer, B. M. et al. Morphometry and average temperature affect lake stratification responses to climate change. Geophys. Res. Lett. 42, 4981–4988 (2015).
ADS Google Scholar
34.
Verburg, P., Hecky, R. E. & Kling, H. Ecological consequences of a century of warming in Lake Tanganyika. Science 301, 505–507 (2003).
ADS CAS PubMed Google Scholar
35.
North, R. P., North, R. L., Livingstone, D. M., Köster, O. & Kipfer, R. Long-term changes in hypoxia and soluble reactive phosphorus in the hypolimnion of a large temperate lake: consequences of a climate regime shift. Glob. Change Biol. 20, 811–823 (2014).
ADS Google Scholar
36.
Salmaso, N. Effects of climatic fluctuations and vertical mixing on the interannual trophic variability of Lake Garda, Italy. Limnol. Oceanogr. 50, 553–565 (2005).
ADS Google Scholar
37.
Kõiv, T., Nõges, T. & Laas, A. Phosphorus retention as a function of external loading, hydraulic turnover time, area and relative depth in 54 lakes and reservoirs. Hydrobiologia 660, 105–115 (2011).
Google Scholar
38.
Walker, K. F. & Likens, G. E. Meromixis and a reconsidered typology of lake circulation patterns. Int. Vereinigung für Theor. und Angew. Limnol. Verhandlungen 19, 442–458 (1975).
Google Scholar
39.
Rogora, M. et al. Climatic effects on vertical mixing and deep-water oxygen content in the subalpine lakes in Italy. Hydrobiologia https://doi.org/10.1007/s10750-018-3623-y (2018).
Article Google Scholar
40.
Valerio, G., Pilotti, M., Barontini, S. & Leoni, B. Sensitivity of the multiannual thermal dynamics of a deep pre-alpine lake to climatic change. Hydrol. Process. 29, 767–779 (2015).
ADS Google Scholar
41.
Rapuc, W. et al. Holocene-long record of flood frequency in the Southern Alps (Lake Iseo, Italy) under human and climate forcing. Glob. Planet. Change 175, 160–172 (2019).
ADS Google Scholar
42.
Gächter, R. & Müller, B. Why the phosphorus retention of lakes does not necessarily depend on the oxygen supply to their sediment surface. Limnol. Oceanogr. 48, 929–933 (2003).
ADS Google Scholar
43.
Katsev, S. & Dittrich, M. Modeling of decadal scale phosphorus retention in lake sediment under varying redox conditions. Ecol. Model. 251, 246–259 (2013).
CAS Google Scholar
44.
Garibaldi, L., Mezzanotte, V., Brizzio, M. C., Rogora, M. & Mosello, R. The trophic evolution of Lake Iseo as related to its holomixis. J. Limnol. 58, 10 (1999).
Google Scholar
45.
Leoni, B. et al. Long-term studies for evaluating the impacts of natural and anthropic stressors on limnological features and the ecosystem quality of Lake Iseo. Adv. Oceanogr. Limnol. https://doi.org/10.4081/aiol.2019.8622 (2019).
Article Google Scholar
46.
Wilhelm, S. & Adrian, R. Impact of summer warming on the thermal characteristics of a polymictic lake and consequences for oxygen, nutrients and phytoplankton. Freshw. Biol. 53, 226–237 (2008).
CAS Google Scholar
47.
Pilotti, M., Valerio, G. & Leoni, B. Data set for hydrodynamic lake model calibration: a deep prealpine case. Water Resour. Res. 49, 7159–7163 (2013).
ADS Google Scholar
48.
Hutchinson, G. E. Treatise on limnology; geography, physics of lakes. In Treatise on Limnology; Geography, Physics of Lakes (Wiley, New York, 1975).
49.
Livingstone, D. M. A change of climate provokes a change of paradigm: taking leave of two tacit assumptions about physical lake forcing. Int. Rev. Hydrobiol. 93, 404–414 (2008).
Google Scholar
50.
Livingstone, D. M. Impact of secular climate change on the thermal structure of a large temperate central European lake. Clim. Change 57, 205–225 (2003).
Google Scholar
51.
Peeters, F., Livingstone, D. M., Goudsmit, G.-H., Kipfer, R. & Forster, R. Modeling 50 years of historical temperature profiles in a large central European lake. Limnol. Oceanogr. 47, 186–197 (2002).
ADS Google Scholar
52.
Foley, B., Jones, I. D., Maberly, S. C. & Rippey, B. Long-term changes in oxygen depletion in a small temperate lake: effects of climate change and eutrophication. Freshw. Biol. 57, 278–289 (2011).
Google Scholar
53.
Salmaso, N., Boscaini, A., Capelli, C. & Cerasino, L. Ongoing ecological shifts in a large lake are driven by climate change and eutrophication: evidences from a three-decade study in Lake Garda. Hydrobiologia 824, 177–195 (2018).
CAS Google Scholar
54.
Vinçon-Leite, B., Lemaire, B. J., Khac, V. T. & Tassin, B. Long-term temperature evolution in a deep sub-alpine lake, Lake Bourget, France: how a one-dimensional model improves its trend assessment. Hydrobiologia 731, 49–64 (2014).
Google Scholar
55.
Livingstone, D. M. An example of the simultaneous occurrence of climate-driven “sawtooth” deep-water warming/cooling episodes in several Swiss lakes. SIL Proc. 1922–2010(26), 822–828 (1997).
Google Scholar
56.
Martin-Creuzburg, D., von Elert, E. & Hoffmann, K. H. Nutritional constraints at the cyanobacteria—Daphnia magna interface: the role of sterols. Limnol. Oceanogr. 53, 456–468 (2008).
ADS Google Scholar
57.
Zadereev, E. S., Boehrer, B. & Gulati, R. D. Introduction: meromictic lakes, their terminology and geographic distribution. In: Ecology of Meromictic Lakes, Vol. 228, 1–11 (Springer, 2017).
58.
Bryhn, A. C., Girel, C., Paolini, G. & Jacquet, S. Predicting future effects from nutrient abatement and climate change on phosphorus concentrations in Lake Bourget, France. Ecol. Model. 221, 1440–1450 (2010).
CAS Google Scholar
59.
Kourzeneva, E., Asensio, H., Martin, E. & Faroux, S. Global gridded dataset of lake coverage and lake depth for use in numerical weather prediction and climate modelling. Tellus A Dyn. Meteorol. Oceanogr. 64, 15640 (2012).
Google Scholar
60.
Downing, J. A. et al. The global abundance and size distribution of lakes, ponds, and impoundments. Limnol. Oceanogr. 51, 2388–2397 (2006).
ADS Google Scholar
61.
Cael, B. B., Heathcote, A. J. & Seekell, D. A. The volume and mean depth of Earth’s lakes. Geophys. Res. Lett. 44, 209–218 (2017).
ADS Google Scholar
62.
Brett, M. T. & Benjamin, M. M. A review and reassessment of lake phosphorus retention and the nutrient loading concept. Freshw. Biol. 53, 194–211 (2007).
Google Scholar
63.
Bryhn, A. C. A morphometrically based method for predicting water layer boundaries in meromictic lakes. Hydrobiologia 636, 413–419 (2009).
CAS Google Scholar
64.
Rempfer, J. et al. The effect of the exceptionally mild European winter of 2006–2007 on temperature and oxygen profiles in lakes in Switzerland: a foretaste of the future?. Limnol. Oceanogr. 55, 2170–2180 (2010).
ADS CAS Google Scholar
65.
Jenny, J. P. et al. Global spread of hypoxia in freshwater ecosystems during the last three centuries is caused by rising local human pressure. Glob. Change Biol. 22, 1481–1489 (2016).
ADS Google Scholar
66.
Kraemer, B. M., Mehner, T. & Adrian, R. Reconciling the opposing effects of warming on phytoplankton biomass in 188 large lakes. Sci. Rep. 7, 10762 (2017).
ADS PubMed PubMed Central Google Scholar
67.
Bonomi, G. & Gerletti, M. Lake Iseo: a first limnological survey (temperature, chemistry, plankton and benthos). Mem. 1st. Ital. Idrobiol. 22, 149–175 (1967).
Google Scholar
68.
Pilotti, M., Simoncelli, S. & Valerio, G. A simple approach to the evaluation of the actual water renewal time of natural stratified lakes. Water Resour. Res. 50, 2830–2849 (2014).
ADS Google Scholar
69.
Ambrosetti, W. & Barbanti, L. Evolution towards meromixis of Lake Iseo (Northern Italy) as revealed by its stability trend. J. Limnol. 64, 1 (2005).
Google Scholar
70.
Hupfer, M., Reitzel, K., Kleeberg, A. & Lewandowski, J. Long-term efficiency of lake restoration by chemical phosphorus precipitation: scenario analysis with a phosphorus balance model. Water Res. 97, 153–161 (2016).
CAS PubMed Google Scholar
71.
Hesslein, R. H. An in situ sampler for close interval pore water studies1. Limnol. Oceanogr. 21, 912–914 (1976).
ADS CAS Google Scholar
72.
Psenner, R., Pucsko, R. & Sage, M. Fractionation of Organic and Inorganic Phosphorus Compounds in Lake Sediments, An Attempt to Characterize Ecologically Important Fractions (Die Fraktionierung Organischer und Anorganischer Phosphorverbindungen von Sedimenten, Versuch einer Definition Okologisch Wichtiger Fraktionen). Arch. fur Hydrobiol. 1 (1984).
73.
Hupfer, M., Gächter, R. & Giovanoli, R. Transformation of phosphorus species in settling seston and during early sediment diagenesis. Aquat. Sci. 57, 305–324 (1995).
Google Scholar
74.
Reitzel, K., Hansen, J., Andersen, F. Ø, Hansen, K. S. & Jensen, H. S. Lake restoration by dosing aluminum relative to mobile phosphorus in the sediment. Environ. Sci. Technol. https://doi.org/10.1021/ES0485964 (2005).
Article PubMed Google Scholar
75.
Berg, P., Risgaard-Petersen, N. & Rysgaard, S. Interpretation of measured concentration profiles in sediment pore water. Limnol. Oceanogr. 43, 1500–1510 (1998).
ADS CAS Google Scholar
76.
Yuan-Hui, L. & Gregory, S. Diffusion of ions in sea water and in deep-sea sediments. Geochim. Cosmochim. Acta 38, 703–714 (1974).
ADS Google Scholar
77.
R Core Team. R: a language and environment for statistical computing (2013).
78.
Messager, M. L., Lehner, B., Grill, G., Nedeva, I. & Schmitt, O. Estimating the volume and age of water stored in global lakes using a geo-statistical approach. Nat. Commun. 7, 13603 (2016).
ADS CAS PubMed PubMed Central Google Scholar
79.
Håkanson, L. The importance of lake morphometry for the structure and function of lakes. Int. Rev. Hydrobiol. 90, 433–461 (2005).
Google Scholar More
