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Synergistic Effects of Warming and Internal Nutrient Loading Interfere with the Long-Term Stability of Lake Restoration and Induce Sudden Re-eutrophication

. 2023 Mar 07 ; 57 (9) : 4003-4013. [epub] 20230220

Language English Country United States Media print-electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Phosphorus (P) precipitation is among the most effective treatments to mitigate lake eutrophication. However, after a period of high effectiveness, studies have shown possible re-eutrophication and the return of harmful algal blooms. While such abrupt ecological changes were attributed to the internal P loading, the role of lake warming and its potential synergistic effects with internal loading, thus far, has been understudied. Here, in a eutrophic lake in central Germany, we quantified the driving mechanisms of the abrupt re-eutrophication and cyanobacterial blooms in 2016 (30 years after the first P precipitation). A process-based lake ecosystem model (GOTM-WET) was established using a high-frequency monitoring data set covering contrasting trophic states. Model analyses suggested that the internal P release accounted for 68% of the cyanobacterial biomass proliferation, while lake warming contributed to 32%, including direct effects via promoting growth (18%) and synergistic effects via intensifying internal P loading (14%). The model further showed that the synergy was attributed to prolonged lake hypolimnion warming and oxygen depletion. Our study unravels the substantial role of lake warming in promoting cyanobacterial blooms in re-eutrophicated lakes. The warming effects on cyanobacteria via promoting internal loading need more attention in lake management, particularly for urban lakes.

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Kraemer B. M.; Pilla R. M.; Woolway R. I.; Anneville O.; Ban S.; Colom-Montero W.; Devlin S. P.; Dokulil M. T.; Gaiser E. E.; Hambright K. D.; et al. Climate change drives widespread shifts in lake thermal habitat. Nat. Clim. Change 2021, 11 (6), 521–529. 10.1038/s41558-021-01060-3. DOI

Holgerson M. A.; Raymond P. A. Large contribution to inland water CO2 and CH4 emissions from very small ponds. Nat. Geosci. 2016, 9 (3), 222–226. 10.1038/ngeo2654. DOI

Harrison J. A.; Maranger R. J.; Alexander R. B.; Giblin A. E.; Jacinthe P.; Mayorga E.; Seitzinger S. P.; Sobota D. J.; Wollheim W. M. The regional and global significance of nitrogen removal in lakes and reservoirs. Biogeochemistry 2009, 93 (1–2), 143–157. 10.1007/s10533-008-9272-x. DOI

Seelen L. M.; Teurlincx S.; Bruinsma J.; Huijsmans T. M.; van Donk E.; Lürling M.; de Senerpont Domis L. N. The value of novel ecosystems: Disclosing the ecological quality of quarry lakes. Sci. Total Environ. 2021, 769, 144294.10.1016/j.scitotenv.2020.144294. PubMed DOI

Hou X.; Feng L.; Dai Y.; Hu C.; Gibson L.; Tang J.; Lee Z.; Wang Y.; Cai X.; Liu J.; Zheng Y.; Zheng C. Global mapping reveals increase in lacustrine algal blooms over the past decade. Nat. Geosci. 2022, 15, 130–134. 10.1038/s41561-021-00887-x. DOI

Ho J. C.; Michalak A. M.; Pahlevan N. Widespread global increase in intense lake phytoplankton blooms since the 1980s. Nature 2019, 574 (7780), 667–670. 10.1038/s41586-019-1648-7. PubMed DOI

Huisman J.; Codd G. A.; Paerl H. W.; Ibelings B. W.; Verspagen J. M.; Visser P. M. Cyanobacterial blooms. Nat. Rev. Microbiol. 2018, 16 (8), 471–483. 10.1038/s41579-018-0040-1. PubMed DOI

Qin B.; Paerl H. W.; Brookes J. D.; Liu J.; Jeppesen E.; Zhu G.; Zhang Y.; Xu H.; Shi K.; Deng J. Why Lake Taihu continues to be plagued with cyanobacterial blooms through 10 years (2007–2017) efforts. Sci. Bull. 2019, 64 (6), 354–356. 10.1016/j.scib.2019.02.008. PubMed DOI

Johnk K. D.; Huisman J.; Sharples J.; Sommeijer B.; Visser P. M.; Stroom J. M. Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biol. 2008, 14 (3), 495–512. 10.1111/j.1365-2486.2007.01510.x. DOI

Huser B. J.; Egemose S.; Harper H.; Hupfer M.; Jensen H.; Pilgrim K. M.; Reitzel K.; Rydin E.; Futter M. Longevity and effectiveness of aluminum addition to reduce sediment phosphorus release and restore lake water quality. Water Res. 2016, 97, 122–132. 10.1016/j.watres.2015.06.051. PubMed DOI

Teurlincx S.; Kuiper J. J.; Hoevenaar E. C.; Lurling M.; Brederveld R. J.; Veraart A. J.; Janssen A. B.; Mooij W. M.; de Senerpont Domis L. N. Towards restoring urban waters: understanding the main pressures. Curr. Opin. Environ. Sustain. 2019, 36, 49–58. 10.1016/j.cosust.2018.10.011. DOI

Søndergaard M.; Jensen J. P.; Jeppesen E. Internal phosphorus loading in shallow Danish lakes. Hydrobiologia 1999, 408/409, 145–152. 10.1023/A:1017063431437. DOI

Rönicke H.; Frassl M. A.; Rinke K.; Tittel J.; Beyer M.; Kormann B.; Gohr F.; Schultze M. Suppression of bloom-forming colonial cyanobacteria by phosphate precipitation: A 30 years case study in Lake Barleber (Germany). Ecol. Eng. 2021, 162, 106171.10.1016/j.ecoleng.2021.106171. DOI

Berkowitz J.; Anderson M. A.; Amrhein C. Influence of aging on phosphorus sorption to alum floc in lake water. Water Res. 2006, 40 (5), 911–916. 10.1016/j.watres.2005.12.018. PubMed DOI

Jensen H. S.; Andersen F. O. Importance of temperature, nitrate, and pH for phosphate release from aerobic sediments of four shallow, eutrophic lakes. Limnol. Oceanogr. 1992, 37 (3), 577–589. 10.4319/lo.1992.37.3.0577. DOI

Moss B.; Kosten S.; Meerhoff M.; Battarbee R. W.; Jeppesen E.; Mazzeo N.; Havens K.; Lacerot G.; Liu Z.; De Meester L. Allied attack: climate change and eutrophication. Inland waters 2011, 1 (2), 101–105. 10.5268/IW-1.2.359. DOI

Meerhoff M.; Audet J.; Davidson T. A.; De Meester L.; Hilt S.; Kosten S.; Liu Z.; Mazzeo N.; Paerl H.; Scheffer M.; et al. Feedback between climate change and eutrophication: revisiting the allied attack concept and how to strike back. Inland Waters 2022, 12 (2), 187–204. 10.1080/20442041.2022.2029317. DOI

Warszawski L.; Frieler K.; Huber V.; Piontek F.; Serdeczny O.; Schewe J. The inter-sectoral impact model intercomparison project (ISI-MIP): project framework. Proc. Natl. Acad. Sci. U.S.A. 2014, 111 (9), 3228–3232. 10.1073/pnas.1312330110. PubMed DOI PMC

Mooij W. M.; van Wijk D.; Beusen A. H.; Brederveld R. J.; Chang M.; Cobben M. M.; DeAngelis D. L.; Downing A. S.; Green P.; Gsell A. S.; Huttunen I.; Janse J. H.; Janssen A. B.; Hengeveld G. M.; Kong X.; Kramer L.; Kuiper J. J.; Langan S. J.; Nolet B. A.; Nuijten R. J.; Strokal M.; Troost T. A.; van Dam A. A.; Teurlincx S. Modeling water quality in the Anthropocene: directions for the next-generation aquatic ecosystem models. Curr. Opin. Environ. Sustain. 2019, 36, 85–95. 10.1016/j.cosust.2018.10.012. DOI

Soares L. M. V.; do Carmo Calijuri M. Deterministic modelling of freshwater lakes and reservoirs: Current trends and recent progress. Environ. Model. Software 2021, 144, 105143.10.1016/j.envsoft.2021.105143. DOI

Grant L.; Vanderkelen I.; Gudmundsson L.; Tan Z.; Perroud M.; Stepanenko V. M.; Debolskiy A. V.; Droppers B.; Janssen A. B.; Woolway R. I.; et al. Attribution of global lake systems change to anthropogenic forcing. Nat. Geosci. 2021, 14, 849–854. 10.1038/s41561-021-00833-x. DOI

Yindong T.; Xiwen X.; Miao Q.; Jingjing S.; Yiyan Z.; Wei Z.; Mengzhu W.; Xuejun W.; Yang Z. Lake warming intensifies the seasonal pattern of internal nutrient cycling in the eutrophic lake and potential impacts on algal blooms. Water Res. 2021, 188, 116570.10.1016/j.watres.2020.116570. PubMed DOI

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. Global Change Biol. 2014, 20 (3), 811–823. 10.1111/gcb.12371. PubMed DOI

Carey C. C.; Ibelings B. W.; Hoffmann E. P.; Hamilton D. P.; Brookes J. D. Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res. 2012, 46 (5), 1394–1407. 10.1016/j.watres.2011.12.016. PubMed DOI

Kong X.; Seewald M.; Dadi T.; Friese K.; Mi C.; Boehrer B.; Schultze M.; Rinke K.; Shatwell T. Unravelling winter diatom blooms in temperate lakes using high frequency data and ecological modeling. Water Res. 2021, 190, 116681.10.1016/j.watres.2020.116681. PubMed DOI

Hannappel S.; Strom A. Method to determine the amount of phosphorous entering Barleber See near Magdeburg via groundwater. Korrespondenz Wasserwirtschaft 2020, 13, 24–30. (in German).

Moore T.gotmtools: Tools to work with GOTM input data and also process the output data. R package version 0.1.0, 2021. https://github.com/aemon-j/gotmtools (accessed 14 Dec. 2022).

Boessenkool B.rdwd: Select and Download Climate Data from ‘DWD’ (German Weather Service). R package version 1.2.0, 2019. https://CRAN.R-project.org/package=rdwd (accessed 14 Dec. 2022).

Seewald M.Monitoring und Phosphorbilanz des Barleber Sees unter Einfluss einer Cyanophyceenmassenentwicklung. Master thesis, University of Applied Sciences Magdeburg-Stendal; (in German), 2019.

Beutler M.; Wiltshire K. H.; Meyer B.; Moldaenke C.; Lüring C.; Meyerhöfer M.; Hansen U.-P.; Dau H. A fluorometric method for the differentiation of algal populations in vivo and in situ. Photosynth. Res. 2002, 72 (1), 39–53. 10.1023/A:1016026607048. PubMed DOI

Dadi T.; Kong X.; Schultze M.; Seewald M.; Rinke K.; Friese K.. Sudden re-eutrophication of an alum-treated lake after three decades of mesotrophy due to abrupt increase of internal phosphorus loading. In revision. PubMed

Burchard H.; Bolding K.; Villarreal M. R.. GOTM, a general ocean turbulence model. Theory, implementation and test cases. European Commission, Space Applications Institute, 1999. https://op.europa.eu/en/publication-detail/-/publication/5b512e12-367d-11ea-ba6e-01aa75ed71a1/language-en/format-PDF/source-272420379 (accessed 14 Dec. 2022).

Schnedler-Meyer N. A.; Andersen T. K.; Hu F. R. S.; Bolding K.; Nielsen A.; Trolle D. Water Ecosystems Tool (WET) 1.0 - a new generation of flexible aquatic ecosystem model. Geosci. Model Dev. 2022, 15 (15), 3861–3878. 10.5194/gmd-15-3861-2022. DOI

Golub M.; Thiery W.; Marcé R.; Pierson D.; Vanderkelen I.; Mercado-Bettin D.; Woolway R. I.; Grant L.; Jennings E.; Kraemer B. M.; et al. A framework for ensemble modelling of climate change impacts on lakes worldwide: the ISIMIP Lake Sector. Geosci. Model Dev. 2022, 15 (11), 4597–4623. 10.5194/gmd-15-4597-2022. DOI

Janse J.Model studies on the eutrophication of shallow lakes and ditches. Doctoral dissertation, Wageningen Universiteit, 2005. http://edepot.wur.nl/121663 (accessed 14 Dec. 2022).

Hu F.; Bolding K.; Bruggeman J.; Jeppesen E.; Flindt M.; van Gerven L.; Janse J.; Janssen A.; Kuiper J.; Mooij W.; et al. FABM-1 PCLake-linking aquatic ecology with hydrodynamics. Geosci. Model Dev. 2016, 9 (6), 2271–2278. 10.5194/gmd-9-2271-2016. DOI

Bruggeman J.; Bolding K. A general framework for aquatic biogeochemical models. Environ. Model. Software 2014, 61, 249–265. 10.1016/j.envsoft.2014.04.002. DOI

Johnes P. J. Evaluation and management of the impact of land use change on the nitrogen and phosphorus load delivered to surface waters: the export coefficient modelling approach. J. Hydrol. 1996, 183 (3–4), 323–349. 10.1016/0022-1694(95)02951-6. DOI

Onderka M.; Wrede S.; Rodny M.; Pfister L.; Hoffmann L.; Krein A. Hydrogeologic and landscape controls of dissolved inorganic nitrogen (DIN) and dissolved silica (DSi) fluxes in heterogeneous catchments. J. Hydrol. 2012, 450, 36–47. 10.1016/j.jhydrol.2012.05.035. DOI

OECD . Eutrophication of Waters. Monitoring, Assessment and Control; Final Report; OECD Cooperative Program on Monitoring of Inland Waters (Eutrophication Control), Environment Directorate, OECD: Paris,1982, p 154.

Schröder W.; Holy M.; Pesch R.; Harmens H.; Fagerli H. Mapping background values of atmospheric nitrogen total depositions in Germany based on EMEP deposition modelling and the European Moss Survey 2005. Environ. Sci. Eur. 2011, 23, 18.10.1186/2190-4715-23-18. DOI

Andersen T. K.; Nielsen A.; Jeppesen E.; Bolding K.; Johansson L. S.; Søndergaard M.; Trolle D. Simulating shifting ecological states in a restored, shallow lake with multiple single-model ensembles: Lake Arreskov, Denmark. Environ. Model. Software 2022, 156, 105501.10.1016/j.envsoft.2022.105501. DOI

Bolding K.; Bruggeman J.. Parsac: parallel sensitivity analysis and calibration, 2020, 10.5281/zenodo.4280520 (accessed 14 Dec. 2022). DOI

Ayala A. I.; Moras S.; Pierson D. C. Simulations of future changes in thermal structure of Lake Erken: proof of concept for ISIMIP2b lake sector local simulation strategy. Hydrol. Earth Syst. Sci. 2020, 24 (6), 3311–3330. 10.5194/hess-24-3311-2020. DOI

Andersen T. K.; Nielsen A.; Jeppesen E.; Hu F.; Bolding K.; Liu Z.; Søndergaard M.; Johansson L. S.; Trolle D. Predicting ecosystem state changes in shallow lakes using an aquatic ecosystem model: Lake Hinge, Denmark, an example. Ecol. Appl. 2020, 30 (7), e0216010.1002/eap.2160. PubMed DOI PMC

Kong X.; Ghaffar S.; Determann M.; Friese K.; Jomaa S.; Mi C.; Shatwell T.; Rinke K.; Rode M. Reservoir water quality deterioration due to deforestation emphasizes the indirect effects of global change. Water Res. 2022, 221, 118721.10.1016/j.watres.2022.118721. PubMed DOI

Bennett N. D.; Croke B. F.; Guariso G.; Guillaume J. H.; Hamilton S. H.; Jakeman A. J.; Marsili-Libelli S.; Newham L. T.; Norton J. P.; Perrin C.; et al. Characterising performance of environmental models. Environ. Model. Software 2013, 40, 1–20. 10.1016/j.envsoft.2012.09.011. DOI

Arhonditsis G. B.; Brett M. T. Evaluation of the current state of mechanistic aquatic biogeochemical modeling. Mar. Ecol.: Prog. Ser. 2004, 271, 13–26. 10.3354/meps271013. DOI

Pohlert T.Non-parametric trend tests and change-point detection. R package version 1.1.4, 2020. https://CRAN.R-project.org/package=trend (accessed 14 Dec. 2022).

R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Austria, 2021. http://www.R-project.org (accessed 14 Dec. 2022).

Mollema P. N.; Antonellini M. Water and (bio) chemical cycling in gravel pit lakes: A review and outlook. Earth-Sci. Rev. 2016, 159, 247–270. 10.1016/j.earscirev.2016.05.006. DOI

Søndergaard M.; Lauridsen T. L.; Johansson L. S.; Jeppesen E. Gravel pit lakes in Denmark: Chemical and biological state. Sci. Total Environ. 2018, 612, 9–17. 10.1016/j.scitotenv.2017.08.163. PubMed DOI

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. 2016, 97, 153–161. 10.1016/j.watres.2015.06.052. PubMed DOI

Hupfer M.; Lewandowski J. Oxygen controls the phosphorus release from Lake Sediments-a long-lasting paradigm in limnology. Int. Rev. Hydrobiol. 2008, 93 (4–5), 415–432. 10.1002/iroh.200711054. DOI

Anderson H. S.; Johengen T. H.; Godwin C. M.; Purcell H.; Alsip P. J.; Ruberg S. A.; Mason L. A. Continuous in situ nutrient analyzers pinpoint the onset and rate of internal P loading under anoxia in Lake Erie’s Central Basin. ACS ES&T Water 2021, 1 (4), 774–781. 10.1021/acsestwater.0c00138. DOI

Pilla R. M.; Williamson C. E.; Adamovich B. V.; Adrian R.; Anneville O.; Chandra S.; Colom-Montero W.; Devlin S. P.; Dix M. A.; Dokulil M. T.; et al. Deeper waters are changing less consistently than surface waters in a global analysis of 102 lakes. Sci. Rep. 2020, 10 (1), 20514.10.1038/s41598-020-76873-x. PubMed DOI PMC

Jane S. F.; Hansen G. J.; Kraemer B. M.; Leavitt P. R.; Mincer J. L.; North R. L.; Pilla R. M.; Stetler J. T.; Williamson C. E.; Woolway R. I.; et al. Widespread deoxygenation of temperate lakes. Nature 2021, 594 (7861), 66–70. 10.1038/s41586-021-03550-y. PubMed DOI

Qin B.; Deng J.; Shi K.; Wang J.; Brookes J.; Zhou J.; Zhang Y.; Zhu G.; Paerl H. W.; Wu L. Extreme climate anomalies enhancing cyanobacterial blooms in eutrophic Lake Taihu, China. Water Resour. Res. 2021, 57 (7), e2020WR02937110.1029/2020WR029371. DOI

Hipsey M. R.; Gal G.; Arhonditsis G. B.; Carey C. C.; Elliott J. A.; Frassl M. A.; Janse J. H.; de Mora L.; Robson B. J. A system of metrics for the assessment and improvement of aquatic ecosystem models. Environ. Model. Software 2020, 128, 104697.10.1016/j.envsoft.2020.104697. DOI

Kong X.; He Q.; Yang B.; He W.; Xu F.; Janssen A. B. G.; Kuiper J. J.; van Gerven L. P.; Qin N.; Jiang Y.; Liu W.; Yang C.; Bai Z.; Zhang M.; Kong F.; Janse J. H.; Mooij W. M. Hydrological regulation drives regime shifts: evidence from paleolimnology and ecosystem modelling of a large shallow Chinese lake. Global Change Biol. 2017, 23 (2), 737–754. 10.1111/gcb.13416. PubMed DOI

Schauser I.; Hupfer M.; Brüggemann R. SPIEL—a model for phosphorus diagenesis and its application to lake restoration. Ecol. Model. 2004, 176 (3–4), 389–407. 10.1016/j.ecolmodel.2003.10.033. DOI

Liu C.; Du Y.; Zhong J.; Zhang L.; Huang W.; Han C.; Chen K.; Gu X. From macrophyte to algae: Differentiated dominant processes for internal phosphorus release induced by suspended particulate matter deposition. Water Res. 2022, 224, 119067.10.1016/j.watres.2022.119067. PubMed DOI

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