Anoxia begets anoxia: A positive feedback to the deoxygenation of temperate lakes.
air temperature
anoxia
chlorophyll a
dissolved oxygen
feedback
hypolimnion
lake
oxygen demand
phosphorus
residence time
Journal
Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746
Informations de publication
Date de publication:
Jan 2024
Jan 2024
Historique:
revised:
01
11
2023
received:
18
07
2023
accepted:
05
11
2023
medline:
26
1
2024
pubmed:
26
1
2024
entrez:
26
1
2024
Statut:
ppublish
Résumé
Declining oxygen concentrations in the deep waters of lakes worldwide pose a pressing environmental and societal challenge. Existing theory suggests that low deep-water dissolved oxygen (DO) concentrations could trigger a positive feedback through which anoxia (i.e., very low DO) during a given summer begets increasingly severe occurrences of anoxia in following summers. Specifically, anoxic conditions can promote nutrient release from sediments, thereby stimulating phytoplankton growth, and subsequent phytoplankton decomposition can fuel heterotrophic respiration, resulting in increased spatial extent and duration of anoxia. However, while the individual relationships in this feedback are well established, to our knowledge, there has not been a systematic analysis within or across lakes that simultaneously demonstrates all of the mechanisms necessary to produce a positive feedback that reinforces anoxia. Here, we compiled data from 656 widespread temperate lakes and reservoirs to analyze the proposed anoxia begets anoxia feedback. Lakes in the dataset span a broad range of surface area (1-126,909 ha), maximum depth (6-370 m), and morphometry, with a median time-series duration of 30 years at each lake. Using linear mixed models, we found support for each of the positive feedback relationships between anoxia, phosphorus concentrations, chlorophyll a concentrations, and oxygen demand across the 656-lake dataset. Likewise, we found further support for these relationships by analyzing time-series data from individual lakes. Our results indicate that the strength of these feedback relationships may vary with lake-specific characteristics: For example, we found that surface phosphorus concentrations were more positively associated with chlorophyll a in high-phosphorus lakes, and oxygen demand had a stronger influence on the extent of anoxia in deep lakes. Taken together, these results support the existence of a positive feedback that could magnify the effects of climate change and other anthropogenic pressures driving the development of anoxia in lakes around the world.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e17046Subventions
Organisme : College of Science Roundtable at Virginia Tech
Organisme : Cornell Atkinson Center for Sustainability, Cornell University
Organisme : Deutsche Forschungsgemeinschaft
ID : GR1540/37-1
Organisme : EMALCSA Chair
Organisme : Institute for Critical Technology and Applied Science
Organisme : Leibniz-Institut für Gewässerökologie und Binnenfischerei
Organisme : LTSER Platform Tyrolean Alps (LTER-Austria)
Organisme : Ministry of Business, Innovation and Employment
ID : C01X2205
Organisme : Missouri Department of Natural Resources
Organisme : National Science Foundation
ID : 1737424
Organisme : National Science Foundation
ID : 1753639
Organisme : National Science Foundation
ID : 1754265
Organisme : National Science Foundation
ID : 1840995
Organisme : National Science Foundation
ID : 1933016
Organisme : National Science Foundation
ID : 2019528
Organisme : National Science Foundation
ID : 2048031
Organisme : Natural Environment Research Council
ID : NE/R016429/1
Organisme : Oak Ridge National Laboratory
Organisme : Svenska Forskningsrådet Formas
ID : 2020-01091
Organisme : Vetenskapsrådet
ID : 2020-03222
Organisme : Water Power Technologies Office
Informations de copyright
© 2023 Oak Ridge National Laboratory and The Authors. Global Change Biology published by John Wiley & Sons Ltd. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.
Références
Anderson, H. S., Johengen, T. H., Miller, R., & Godwin, C. M. (2021). Accelerated sediment phosphorus release in Lake Erie's central basin during seasonal anoxia. Limnology and Oceanography, 66, 3582-3595. https://doi.org/10.1002/lno.11900
Bartosiewicz, M., Przytulska, A., Lapierre, J.-F., Laurion, I., Lehmann, M. F., & Maranger, R. (2019). Hot tops, cold bottoms: Synergistic climate warming and shielding effects increase carbon burial in lakes. Limnology and Oceanography Letters, 4, 132-144. https://doi.org/10.1002/lol2.10117
Bates, D., Maechler, M., Bolker, B., Walker, S., Christensen, R. H. B., Singmann, H., Dai, B., Grothendieck, G., Green, P., Fox, J., Bauer, A., Krivitsky, P. N., & Tanaka, E. (2023). lme4: Linear mixed-effects models using “Eigen” and S4. CRAN.
Borchers, H. W. (2022). pracma: Practical numerical math functions. CRAN.
Breitburg, D., Levin, L. A., Oschlies, A., Grégoire, M., Chavez, F. P., Conley, D. J., Garçon, V., Gilbert, D., Gutiérrez, D., Isensee, K., Jacinto, G. S., Limburg, K. E., Montes, I., Naqvi, S. W. A., Pitcher, G. C., Rabalais, N. N., Roman, M. R., Rose, K. A., Seibel, B. A., … Zhang, J. (2018). Declining oxygen in the global ocean and coastal waters. Science, 359, eaam7240. https://doi.org/10.1126/science.aam7240
Burnham, K. P., & Anderson, D. R. (Eds.). (2002). Model Selection and Multimodel Inference. Springer. https://doi.org/10.1007/b97636
Burns, N. M. (1995). Using hypolimnetic dissolved oxygen depletion rates for monitoring lakes. New Zealand Journal of Marine and Freshwater Research, 29(1), 1-11. https://doi.org/10.1080/00288330.1995.9516634
Carey, C. C., Hanson, P. C., Thomas, R. Q., Gerling, A. B., Hounshell, A. G., Lewis, A. S. L., Lofton, M. E., McClure, R., Wander, H. L., Woelmer, W. M., Niederlehner, B. R., & Schreiber, M. E. (2022). Anoxia decreases the magnitude of the carbon, nitrogen, and phosphorus sink in freshwaters. Global Change Biology, 28, 4861-4881. https://doi.org/10.1111/gcb.16228
Carey, C. C., Lewis, A. S. L., Howard, D. W., Woelmer, W. M., Gantzer, P. A., Bierlein, K. A., Little, J. C., & WVWA. (2022). Bathymetry and watershed area for Falling Creek Reservoir, Beaverdam Reservoir, and Carvins Cove Reservoir. https://doi.org/10.6073/PASTA/352735344150F7E77D2BC18B69A22412
Carey, C. C., Lewis, A. S. L., McClure, R. P., Gerling, A. B., Breef-Pilz, A., & Das, A. (2022). Time series of high-frequency profiles of depth, temperature, dissolved oxygen, conductivity, specific conductance, chlorophyll a, turbidity, pH, oxidation-reduction potential, photosynthetic active radiation, and descent rate for Beaverdam Reservoir, Carvins Cove Reservoir, Falling Creek Reservoir, Gatewood Reservoir, and Spring Hollow Reservoir in Southwestern Virginia 2013-2021. https://doi.org/10.6073/PASTA/C4C45B5B10B4CB4CD4B5E613C3EFFBD0
Carey, C. C., Wander, H. L., Howard, D. W., Niederlehner, B. R., Woelmer, W. M., Lofton, M. E., Gerling, A. B., & Breef-Pilz, A. (2022). Water chemistry time series for Beaverdam Reservoir, Carvins Cove Reservoir, Falling Creek Reservoir, Gatewood Reservoir, and Spring Hollow Reservoir in Southwestern Virginia, USA 2013-2021. https://doi.org/10.6073/PASTA/7BD797155CDBB5F1ACDF0547C6BA9023
Carey, C. C., Wynne, J. H., Lofton, M. E., Hamre, K. D., Das, A. R., Bryant, C. E., Doubek, J. P., Niederlehner, B. R., Breef-Pilz, A., & Woelmer, W. M. (2022). Filtered chlorophyll a time series for Beaverdam Reservoir, Carvins Cove Reservoir, Claytor Lake, Falling Creek Reservoir, Gatewood Reservoir, Smith Mountain Lake, Spring Hollow Reservoir in Southwestern Virginia and Lake Sunapee in Sunapee, New Hampshire, USA during 2014-2021 [dataset]. Environmental Data Initiative. https://doi.org/10.6073/PASTA/6BA5BEED2869A05C854C34251144A76E
Carpenter, S. R. (2003). Regime shifts in lake ecosystems: Pattern and variation (Vol. 15). International Ecology Institute.
Carpenter, S. R., Cottingham, K. L., & Schindler, D. E. (1992). Biotic feedbacks in lake phosphorus cycles. Trends in Ecology & Evolution, 7, 332-336. https://doi.org/10.1016/0169-5347(92)90125-U
Carpenter, S. R., & Lathrop, R. C. (2008). Probabilistic estimate of a threshold for eutrophication. Ecosystems, 11, 601-613.
Cottingham, K. L., Ewing, H. A., Greer, M. L., Carey, C. C., & Weathers, K. C. (2015). Cyanobacteria as biological drivers of lake nitrogen and phosphorus cycling. Ecosphere, 6, art1. https://doi.org/10.1890/ES14-00174.1
Doig, L. E., North, R. L., Hudson, J. J., Hewlett, C., Lindenschmidt, K.-E., & Liber, K. (2017). Phosphorus release from sediments in a river-valley reservoir in the northern Great Plains of North America. Hydrobiologia, 787, 323-339. https://doi.org/10.1007/s10750-016-2977-2
Einsele, W. (1936). Über die Beziehungen des Eisenkreislaufs zum Phosphatkreislauf im eutrophen See. Archiv für Hydrobiologie, 29, 664-686.
Elser, J. J., Bracken, M. E. S., Cleland, E. E., Gruner, D. S., Harpole, W. S., Hillebrand, H., Ngai, J. T., Seabloom, E. W., Shurin, J. B., & Smith, J. E. (2007). Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters, 10, 1135-1142. https://doi.org/10.1111/j.1461-0248.2007.01113.x
Elshout, P. M. F., Dionisio Pires, L. M., Leuven, R. S. E. W., Wendelaar Bonga, S. E., & Hendriks, A. J. (2013). Low oxygen tolerance of different life stages of temperate freshwater fish species. Journal of Fish Biology, 83(1), 190-206. https://doi.org/10.1111/jfb.12167
Encinas Fernández, J., Peeters, F., & Hofmann, H. (2014). Importance of the autumn overturn and anoxic conditions in the hypolimnion for the annual methane emissions from a temperate lake. Environmental Science & Technology, 48, 7297-7304. https://doi.org/10.1021/es4056164
Feuchtmayr, H., Clarke, M. A., De Ville, M. M., Dodd, B. A., Fletcher, J., Guyatt, H., Hunt, A. G., James, J. B., Mackay, E. B., Rhodes, G., Thackeray, S. J., & Maberly, S. C. (2021). Surface temperature, surface oxygen, water clarity, water chemistry and phytoplankton chlorophyll a data from Blelham Tarn, 2014 to 2018. NERC Environmental Information Data Centre. https://doi.org/10.5285/ae8c850d-211e-4560-8b37-437b6e0e2a16
Filazzola, A., Mahdiyan, O., Shuvo, A., Ewins, C., Moslenko, L., Sadid, T., Blagrave, K., Gray, D., Quinlan, R., O'Reilly, C., & Sharma, S. (2020). A global database of chlorophyll and water chemistry in freshwater lakes. https://doi.org/10.5063/F1JH3JKZ
Finlayson, C. M., de Groot, R. S., Hughes, F. M. R., & Sullivan, C. A. (2018). Freshwater ecosystem services and functions. In J. Hughes (Ed.), Freshwater ecology and conservation: Approaches and techniques. Oxford University Press.
Foley, B., Jones, I. D., Maberly, S. C., & Rippey, B. (2012). Long-term changes in oxygen depletion in a small temperate lake: Effects of climate change and eutrophication. Freshwater Biology, 57, 278-289. https://doi.org/10.1111/j.1365-2427.2011.02662.x
Fox, J., Weisberg, S., Price, B., Adler, D., Bates, D., Baud-Bovy, G., Bolker, B., Ellison, S., Firth, D., Friendly, M., Gorjanc, G., Graves, S., Heiberger, R., Krivitsky, P., Laboissiere, R., Maechler, M., Monette, G., Murdoch, D., Nilsson, H., … R-Core. (2022). car: Companion to applied regression (3.1-0). CRAN. https://CRAN.R-project.org/package=car
Genkai-Kato, M., & Carpenter, S. R. (2005). Eutrophication due to phosphorus recycling in relation to lake morphometry, temperature, and macrophytes. Ecology, 86(1), 210-219. https://doi.org/10.1890/03-0545
Håkanson, L. (1982). Lake bottom dynamics and morphometry: The dynamic ratio. Water Resources Research, 18(5), 1444-1450. https://doi.org/10.1029/wr018i005p01444
Håkanson, L. (2005). The importance of lake morphometry for the structure and function of lakes. International Review of Hydrobiology, 90(4), 433-461. https://doi.org/10.1002/iroh.200410775
Haupt, F., Stockenreiter, M., Reichwaldt, E. S., Baumgartner, M., Lampert, W., Boersma, M., & Stibor, H. (2010). Upward phosphorus transport by Daphnia diel vertical migration. Limnology and Oceanography, 55(2), 529-534. https://doi.org/10.4319/lo.2010.55.2.0529
Hersbach, H., Bell, B., Berrisford, P., Biavati, G., Horányi, A., Muñoz Sabater, J., Nicolas, J., Peubey, C., Radu, R., Rozum, I., Schepers, D., Simmons, A., Soci, C., Dee, D., & Thépaut, J.-N. (2019). ERA5 monthly averaged data on single levels from 1979 to present [dataset]. Copernicus Climate Change Service (C3S) Climate Data Store (CDS). https://doi.org/10.24381/CDS.F17050D7
Hounshell, A. G., McClure, R. P., Lofton, M. E., & Carey, C. C. (2021). Whole-ecosystem oxygenation experiments reveal substantially greater hypolimnetic methane concentrations in reservoirs during anoxia. Limnology and Oceanography Letters, 6, 33-42.
Hupfer, M., & Lewandowski, J. (2008). Oxygen controls the phosphorus release from lake sediments-A long-lasting paradigm in limnology. International Review of Hydrobiology, 93, 415-432. https://doi.org/10.1002/iroh.200711054
Jagtman, E., Van der Molen, D. T., & Vermij, S. (1992). The influence of flushing on nutrient dynamics, composition and densities of algae and transparency in Veluwemeer, The Netherlands. Hydrobiologia, 233, 187-196. https://doi.org/10.1007/BF00016107
Jane, S. F., Hansen, G., Kraemer, B., Leavitt, P. R., Mincer, J. L., North, R. L., Pilla, R. M., Stetler, J. T., Williamson, C. E., Woolway, R. I., Arvola, L., Chandra, S., DeGasperi, C., Diemer, L., Dunalska, J., Erina, O., Flaim, G., Grossart, H. P., Hambright, K. D., … Rose, K. C. (2021). Widespread deoxygenation of temperate lakes. Nature, 594, 66-70. https://doi.org/10.1038/s41586-021-03550-y
Jane, S. F., Mincer, J. L., Lau, M. P., Lewis, A. S. L., Stetler, J. T., & Rose, K. C. (2023). Longer duration of seasonal stratification contributes to widespread increases in lake hypoxia and anoxia. Global Change Biology, 29, 1009-1023. https://doi.org/10.1111/gcb.16525
Jenny, J.-P., Francus, P., Normandeau, A., Lapointe, F., Perga, M.-E., Ojala, A., Schimmelmann, A., & Zolitschka, B. (2016). Global spread of hypoxia in freshwater ecosystems during the last three centuries is caused by rising local human pressure. Global Change Biology, 22, 1481-1489. https://doi.org/10.1111/gcb.13193
Jenny, J.-P., Normandeau, A., Francus, P., Taranu, Z. E., Gregory-Eaves, I., Lapointe, F., Jautzy, J., Ojala, A. E. K., Dorioz, J. M., Schimmelmann, A., & Zolitschka, B. (2016). Urban point sources of nutrients were the leading cause for the historical spread of hypoxia across European lakes. Proceedings of the National Academy of Sciences of the United States of America, 113, 12655-12660. https://doi.org/10.1073/pnas.1605480113
Jones, J. R., Argerich, A., Obrecht, D. V., Thorpe, A. P., & North, R. L. (2020). Missouri lakes and reservoirs long-term limnological dataset. https://doi.org/10.6073/PASTA/86D8D176E91410566B4DE51DF44C2624
Kamarainen, A. M., Yuan, H., Wu, C. H., & Carpenter, S. R. (2009). Estimates of phosphorus entrainment in Lake Mendota: A comparison of one-dimensional and three-dimensional approaches. Limnology and Oceanography: Methods, 7, 553-567. https://doi.org/10.4319/lom.2009.7.553
Kraemer, B. M., Kakouei, K., Munteanu, C., Thayne, M. W., & Adrian, R. (2022). Worldwide moderate-resolution mapping of lake surface chl-a reveals variable responses to global change (1997-2020). PLOS Water, 1, e0000051. https://doi.org/10.1371/journal.pwat.0000051
LaBrie, R., Hupfer, M., & Lau, M. P. (2023). Anaerobic duration predicts biogeochemical consequences of oxygen depletion in lakes. Limnology and Oceanography Letters, 8, 666-674. https://doi.org/10.1002/lol2.10324
Ladwig, R., Hanson, P. C., Dugan, H. A., Carey, C. C., Zhang, Y., Shu, L., Duffy, C. J., & Cobourn, K. M. (2021). Lake thermal structure drives interannual variability in summer anoxia dynamics in a eutrophic lake over 37 years. Hydrology and Earth System Sciences, 25, 1009-1032. https://doi.org/10.5194/hess-25-1009-2021
Leach, T. H., Winslow, L. A., Acker, F. W., Bloomfield, J. A., Boylen, C. W., Bukaveckas, P. A., Charles, D. F., Daniels, R. A., Driscoll, C. T., Eichler, L. W., Farrell, J. L., Funk, C. S., Goodrich, C. A., Michelena, T. M., Nierzwicki-Bauer, S. A., Roy, K. M., Shaw, W. H., Sutherland, J. W., Swinton, M. W., … Rose, K. C. (2018). Long-term dataset on aquatic responses to concurrent climate change and recovery from acidification. Scientific Data, 5, 180059. https://doi.org/10.1038/sdata.2018.59
Lentz, M., Schmidt, S., Woodhouse, J., Kasprzak, P., Wollrab, S., Berger, S. A., Beyer, U., Bodenlos, M., Degebrodt, M., Degebrodt, R., Gonsiorczyk, T., Huth, E., Uta, M., Elke, M., Nejstgaard, J. C., Papke, M., Pinnow, S., Roßberg, R., Sachtleben, M., … Koschel, R. (2023). Lake Stechlin vertical profiles of multiparameter probe data 1970-2020. IGB Leibniz-Institute of Freshwater Ecology and Inland Fisheries. Dataset. https://doi.org/10.18728/igb-fred-823.1
Lewis, A. S. L., Kim, B. S., Edwards, H. L., Wander, H. L., Garfield, C. M., Murphy, H. E., Poulin, N. D., Princiotta, S. D., Rose, K. C., Taylor, A. E., Weathers, K. C., Wigdahl-Perry, C. R., Yokota, K., Richardson, D. C., & Bruesewitz, D. A. (2020). Prevalence of phytoplankton limitation by both nitrogen and phosphorus related to nutrient stoichiometry, land use, and primary producer biomass across the northeastern United States. Inland Waters, 10. https://doi.org/10.1080/20442041.2019.1664233
Lewis, A. S. L., & Lau, M. P. (2023). Abbylewis/anoxia-begets-anoxia: Data analysis of biogeochemical dynamics in 656 lakes: v1.1.1. Zenodo. https://doi.org/10.5281/zenodo.10086950
Lewis, A. S. L., Lau, M. P., Jane, S. F., Beeri-Shlevin, Y., Burnet, S. H., Clayer, F., Feuchtmayr, H., Grossart, H., Howard, D. W., Mariash, H., Delgado-Martin, J., North, R. L., Oleksy, I., Pilla, R. M., Rose, K. C., Smagula, A. P., Sommaruga, R., Steiner, S. E., Verburg, P., … Carey, C. C. (2023). Dissolved oxygen, temperature, chlorophyll-a, total phosphorus, total nitrogen, and dissolved organic carbon at multiple depths in 822 lakes from 1921-2022 ver 1. Environmental Data Initiative. https://doi.org/10.6073/pasta/2cd6628a942de2a8b12d2b19962712a0
Lewis, W. M., Jr., & Wurtsbaugh, W. A. (2008). Control of lacustrine phytoplankton by nutrients: Erosion of the phosphorus paradigm. International Review of Hydrobiology, 93, 446-465. https://doi.org/10.1002/iroh.200811065
Livingstone, D. M., & Imboden, D. M. (1996). The prediction of hypolimnetic oxygen profiles: A plea for a deductive approach. Canadian Journal of Fisheries and Aquatic Sciences, 53, 924-932. https://doi.org/10.1139/f95-230
Lynch, A. J., Cooke, S. J., Arthington, A. H., et al. (2023). People need freshwater biodiversity. WIREs Water, 10, e1633. https://doi.org/10.1002/wat2.1633
Maberly, S. C., Brierley, B., Carter, H. T., Clarke, M. A., De Ville, M. M., Fletcher, J. M., James, J. B., Keenan, P., Kelly, J. L., Mackay, E. B., Parker, J. E., Patel, M., Pereira, M. G., Rhodes, G., Tanna, B., Thackeray, S. J., Vincent, C., & Feuchtmayr, H. (2017). Surface temperature, surface oxygen, water clarity, water chemistry and phytoplankton chlorophyll a data from Blelham Tarn, 1945 to 2013. NERC Environmental Information Data Centre. https://doi.org/10.5285/393a5946-8a22-4350-80f3-a60d753beb00
MacKeigan, P. W., Taranu, Z. E., Pick, F. R., Beisner, B. E., & Gregory-Eaves, I. (2023). Both biotic and abiotic predictors explain significant variation in cyanobacteria biomass across lakes from temperate to subarctic zones. Limnology and Oceanography, 68, 1360-1375. https://doi.org/10.1002/lno.12352
Magnuson, J. J., Robertson, D. M., Benson, B. J., Wynne, R. H., Livingstone, D. M., Arai, T., Assel, R. A., Barry, R. G., Card, V. V., Kuusisto, E., Granin, N. G., Prowse, T. D., Stewart, K. M., & Vuglinski, V. S. (2000). Historical trends in lake and river ice cover in the Northern Hemisphere. Science, 289, 1743-1746. https://doi.org/10.1126/science.289.5485.1743
Masson-Delmotte, V., Zhai, P., Pirani, A., Connors, S. L., Péan, C., Berger, S., Caud, N., Chen, Y., Goldfarb, L., Gomis, M. I., Huang, M., Leitzell, K., Lonnoy, E., Matthews, J. B. R., Maycock, T. K., Waterfield, T., Yelekçi, Ö., Yu, R., & Zhou, B. (2021). Climate change 2021: The physical science basis. In Contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change. Cambridge University Press. https://doi.org/10.1017/9781009157896
Matisoff, G., Kaltenberg, E. M., Steely, R. L., Hummel, S. K., Seo, J., Gibbons, K. J., Bridgeman, T. B., Seo, Y., Behbahani, M., James, W. F., Johnson, L. T., Doan, P., Dittrich, M., Evans, M. A., & Chaffin, J. D. (2016). Internal loading of phosphorus in western Lake Erie. Journal of Great Lakes Research, 42(4), 775-788. https://doi.org/10.1016/j.jglr.2016.04.004
Messager, M. L., Lehner, B., Grill, G., Nedeva, I., & Schmitt, O. (2016). Estimating the volume and age of water stored in global lakes using a geo-statistical approach. Nature Communications, 7, 13603. https://doi.org/10.1038/ncomms13603
Middelburg, J. J., & Levin, L. A. (2009). Coastal hypoxia and sediment biogeochemistry. Biogeosciences, 6, 1273-1293. https://doi.org/10.5194/bg-6-1273-2009
Mortimer, C. H. (1941). The exchange of dissolved substances between mud and water in lakes. Journal of Ecology, 29, 280-329. https://doi.org/10.2307/2256395
Mortimer, C. H. (1942). The exchange of dissolved substances between mud and water in lakes. Journal of Ecology, 30, 147-201. https://doi.org/10.2307/2256691
Moss, B. (2011). Allied attack: Climate change and eutrophication. Inland Waters, 1, 101-105. https://doi.org/10.5268/IW-1.2.359
Muggeo, V. M. R. (2023). Segmented: Regression models with break-points/change-points (with possibly random effects) estimation (1.6-3). https://CRAN.R-project.org/package=segmented
Müller, B., Bryant, L. D., Matzinger, A., & Wüest, A. (2012). Hypolimnetic oxygen depletion in Eutrophic Lakes. Environmental Science & Technology, 46, 9964-9971. https://doi.org/10.1021/es301422r
Müller, B., Steinsberger, T., Schwefel, R., Gächter, R., Sturm, M., & Wüest, A. (2019). Oxygen consumption in seasonally stratified lakes decreases only below a marginal phosphorus threshold. Scientific Reports, 9, 18054. https://doi.org/10.1038/s41598-019-54486-3
North, R. L., Barton, D., Crowe, A. S., Dillon, P. J., Dolson, R. M. L., Evans, D. O., Ginn, B. K., Håkanson, L., Hawryshyn, J., Jarjanazi, H., King, J. W., La Rose, J. K. L., León, L., Lewis, C. F. M., Liddle, G. E., Lin, Z. H., Longstaffe, F. J., Macdonald, R. A., Molot, L., … Young, J. D. (2013). The state of Lake Simcoe (Ontario, Canada): The effects of multiple stressors on phosphorus and oxygen dynamics. Inland Waters, 3(1), 51-74. https://doi.org/10.5268/IW-3.1.529
North, R. P., North, R. L., Livingstone, D. M., Köster, O., & Kipfer, R. (2014). 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 Biology, 20, 811-823. https://doi.org/10.1111/gcb.12371
Nürnberg, G., & Peters, R. H. (1984). The importance of internal phosphorus load to the eutrophication of lakes with anoxic hypolimnia. SIL Proceedings, 22, 190-194. https://doi.org/10.1080/03680770.1983.11897287
Nürnberg, G. K. (1984). The prediction of internal phosphorus load in lakes with anoxic hypolimnia. Limnology and Oceanography, 29, 111-124. https://doi.org/10.4319/lo.1984.29.1.0111
Nürnberg, G. K. (1988). A simple model for predicting the date of fall turnover in thermally stratified lakes. Limnology and Oceanography, 33, 1190-1195. https://doi.org/10.4319/lo.1988.33.5.1190
Nürnberg, G. K. (1995). Quantifying anoxia in lakes. Limnology and Oceanography, 40, 1100-1111. https://doi.org/10.4319/lo.1995.40.6.1100
Nürnberg, G. K. (2009). Assessing internal phosphorus load-Problems to be solved. Lake and Reservoir Management, 25, 419-432. https://doi.org/10.1080/00357520903458848
Nürnberg, G. K. (2019). Quantification of anoxia and hypoxia in water bodies. In Encyclopedia of water (pp. 1-9). John Wiley & Sons, Ltd. https://doi.org/10.1002/9781119300762.wsts0081
Nürnberg, G. K., Howell, T., & Palmer, M. (2019). Long-term impact of Central Basin hypoxia and internal phosphorus loading on north shore water quality in Lake Erie. Inland Waters, 9, 362-373. https://doi.org/10.1080/20442041.2019.1568072
Oleksy, I. A., & Richardson, D. C. (2021). Climate change and teleconnections amplify lake stratification with differential local controls of surface water warming and deep water cooling. Geophysical Research Letters, 48, e2020GL090959. https://doi.org/10.1029/2020GL090959
Orihel, D. M., Baulch, H. M., Casson, N. J., North, R. L., Parsons, C. T., Seckar, D. C. M., & Venkiteswaran, J. J. (2017). Internal phosphorus loading in Canadian fresh waters: A critical review and data analysis. Canadian Journal of Fisheries and Aquatic Sciences, 74, 2005-2029. https://doi.org/10.1139/cjfas-2016-0500
Pace, M. L., & Prairie, Y. T. (2005). Respiration in lakes. In P. Del Giorgio & P. Williams (Eds.), Respiration in aquatic ecosystems (pp. 103-121). Oxford University Press.
Paerl, H. W., & Huisman, J. (2008). Blooms like it hot. Science, 320, 57-58. https://doi.org/10.1126/science.1155398
Paerl, H. W., Scott, J. T., McCarthy, M. J., Newell, S. E., Gardner, W. S., Havens, K. E., Hoffman, D. K., Wilhelm, S. W., & Wurtsbaugh, W. A. (2016). It takes two to tango: When and where dual nutrient (N & P) reductions are needed to protect lakes and downstream ecosystems. Environmental Science & Technology, 50, 10805-10813. https://doi.org/10.1021/acs.est.6b02575
Parmesan, C., Morecroft, M. D., Trisurat, Y., et al. (2022). Terrestrial and freshwater ecosystems and their services. In H. O. Pörtner, D. C. Roberts, M. Tignor, E. S. Poloczanska, K. Mintenbeck, A. Alegría, M. Craig, S. Langsdorf, S. Löschke, V. Möller, A. Okem, & B. Rama (Eds.), Climate change 2022: Impacts, adaptation and vulnerability. Contribution of working group II to the sixth assessment report of the intergovernmental panel on climate change (pp. 197-378). Cambridge, UK and New York, NY, USA: Cambridge University Press. https://doi.org/10.1017/9781009325844.004
Pilla, R. M., & Williamson, C. E. (2023). Multidecadal trends in ultraviolet radiation, temperature, and dissolved oxygen have altered vertical habitat availability for daphnia in temperate Lake Giles, USA. Freshwater Biology, 68, 523-533. https://doi.org/10.1111/fwb.14044
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., Gaiser, E. E., Girdner, S. F., Hambright, K. D., Hamilton, D. P., Havens, K., Hessen, D. O., Higgins, S. N., Huttula, T. H., Huuskonen, H., … Zadereev, E. (2020). Deeper waters are changing less consistently than surface waters in a global analysis of 102 lakes. Scientific Reports, 10, 20514. https://doi.org/10.1038/s41598-020-76873-x
Quinlan, R., Paterson, A. M., Smol, J. P., Douglas, M. S. V., & Clark, B. J. (2005). Comparing different methods of calculating volume-weighted hypolimnetic oxygen (VWHO) in lakes. Aquatic Sciences, 67(1), 97-103. https://doi.org/10.1007/s00027-004-0717-6
R Core Team. (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
Read, J. S., Hamilton, D. P., Jones, I. D., Muraoka, K., Winslow, L. A., Kroiss, R., Wu, C. H., & Gaiser, E. (2011). Derivation of lake mixing and stratification indices from high-resolution lake buoy data. Environmental Modelling & Software, 26(11), 1325-1336. https://doi.org/10.1016/j.envsoft.2011.05.006
Reid, A. J., Carlson, A. K., Creed, I. F., Eliason, E. J., Gell, P. A., Johnson, P. T. J., Kidd, K. A., MacCormack, T., Olden, J. D., Ormerod, S. J., Smol, J. P., Taylor, W. W., Tockner, K., Vermaire, J. C., Dudgeon, D., & Cooke, S. J. (2019). Emerging threats and persistent conservation challenges for freshwater biodiversity. Biological Reviews, 94, 849-873. https://doi.org/10.1111/brv.12480
Reinl, K. L., Harris, T. D., North, R. L., et al. (2023). Blooms also like it cold. Limnology and Oceanography Letters, 8, 546-564. https://doi.org/10.1002/lol2.10316
Reynaud, A., & Lanzanova, D. (2017). A global meta-analysis of the value of ecosystem services provided by lakes. Ecological Economics, 137, 184-194. https://doi.org/10.1016/j.ecolecon.2017.03.001
Richardson, D. C., Melles, S. J., Pilla, R. M., Hetherington, A. L., Knoll, L. B., Williamson, C. E., Kraemer, B. M., Jackson, J. R., Long, E. C., Moore, K., Rudstam, L. G., Rusak, J. A., Saros, J. E., Sharma, S., Strock, K. E., Weathers, K. C., & Wigdahl-Perry, C. R. (2017). Transparency, geomorphology and mixing regime explain variability in trends in lake temperature and stratification across Northeastern North America (1975-2014). Water, 9, 442. https://doi.org/10.3390/w9060442
Rosenberg, R., Hellman, B., & Johansson, B. (1991). Hypoxic tolerance of marine benthic fauna. Marine Ecology Progress Series, 79, 127-131. https://doi.org/10.3354/meps079127
Sachs, J. (1874). Lehrbuch der botanik. Engelmann.
Schindler, D. E. (2017). Warmer climate squeezes aquatic predators out of their preferred habitat. Proceedings of the National Academy of Sciences of the United States of America, 114, 9764-9765. https://doi.org/10.1073/pnas.1712818114
Schindler, D. W. (1974). Eutrophication and recovery in experimental lakes: Implications for lake management. Science, 184, 897-899.
Schmidtko, S., Stramma, L., & Visbeck, M. (2017). Decline in global oceanic oxygen content during the past five decades. Nature, 542, 335-339. https://doi.org/10.1038/nature21399
Scott, J. T., McCarthy, M. J., & Paerl, H. W. (2019). Nitrogen transformations differentially affect nutrient-limited primary production in lakes of varying trophic state. Limnology and Oceanography Letters, 4, 96-104. https://doi.org/10.1002/lol2.10109
Shatwell, T., Thiery, W., & Kirillin, G. (2019). Future projections of temperature and mixing regime of European temperate lakes. Hydrology and Earth System Sciences, 23, 1533-1551. https://doi.org/10.5194/hess-23-1533-2019
Smith, V. H. (1982). The nitrogen and phosphorus dependence of algal biomass in lakes: An empirical and theoretical analysis. Limnology and Oceanography, 27, 1101-1111. https://doi.org/10.4319/lo.1982.27.6.1101
Solomon, C., Jones, S., Weidel, B. C., et al. (2022). MFE database: Data from ecosystem ecology research by Jones, Solomon, and collaborators on the ecology and biogeochemistry of lakes and lake organisms in the Upper Midwest, USA. https://doi.org/10.25390/caryinstitute.7438598.v6
Soranno, P. A., Carpenter, S. R., & Lathrop, R. C. (1997). Internal phosphorus loading in Lake Mendota: Response to external loads and weather. Canadian Journal of Fisheries and Aquatic Sciences, 54, 1883-1893. https://doi.org/10.1139/f97-095
Steinsberger, T., Schwefel, R., Wüest, A., & Müller, B. (2020). Hypolimnetic oxygen depletion rates in deep lakes: Effects of trophic state and organic matter accumulation. Limnology and Oceanography, 65, 3128-3138. https://doi.org/10.1002/lno.11578
Stetler, J. T., Jane, S. F., Mincer, J. L., Sanders, M. N., & Rose, K. C. (2021). Long-term lake dissolved oxygen and temperature data, 1941-2018. https://doi.org/10.6073/PASTA/C45EFE4826B5F615023B857DC59856F3
Thienemann, A. (1928). Der Sauerstoff im eutrophen und obligotrophen See. Stuttgart, Germany: E. Schweizerbart.
Vachon, D., Solomon, C. T., & del Giorgio, P. A. (2017). Reconstructing the seasonal dynamics and relative contribution of the major processes sustaining CO2 emissions in northern lakes. Limnology and Oceanography, 62, 706-722. https://doi.org/10.1002/lno.10454
Vaquer-Sunyer, R., & Duarte, C. M. (2008). Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences of the United States of America, 105, 15452-15457. https://doi.org/10.1073/pnas.0803833105
Wang, J., Guan, Y., Wu, L., Guan, X., Cai, W., Huang, J., Dong, W., & Zhang, B. (2021). Changing lengths of the four seasons by global warming. Geophysical Research Letters, 48, e2020GL091753. https://doi.org/10.1029/2020GL091753
Wang, M., Xu, X., Wu, Z., Zhang, X., Sun, P., Wen, Y., Wang, Z., Lu, X., Zhang, W., Wang, X., & Tong, Y. (2019). Seasonal pattern of nutrient limitation in a eutrophic lake and quantitative analysis of the impacts from internal nutrient cycling. Environmental Science & Technology, 53, 13675-13686. https://doi.org/10.1021/acs.est.9b04266
Wetzel, R. G. (2001). 13-The phosphorus cycle. In R. G. Wetzel (Ed.), Limnology (3rd ed., pp. 239-288). Academic Press.
Wetzel, R. G., & Likens, G. E. (2000). Estimates of whole lake metabolism: Hypolimnetic oxygen deficits and carbon dioxide accumulation. In R. G. Wetzel & G. E. Likens (Eds.), Limnological analyses (pp. 373-382). Springer.
Williamson, C. E. (2022). Three decades of limnological data from lakes in the Pocono Mountains region, Pennsylvania USA, 1988-2021. https://doi.org/10.6073/PASTA/0D764453DD98D7FA978D517E6787538F
Williamson, C. E., Overholt, E. P., Pilla, R. M., Leach, T. H., Brentrup, J. A., Knoll, L. B., Mette, E. M., & Moeller, R. E. (2015). Ecological consequences of long-term browning in lakes. Scientific Reports, 5, 1-10. https://doi.org/10.1038/srep18666
Winslow, L., Leach, T., & Hahn, T. (2018). adklakedata: Adirondack long-term lake data. CRAN.
Winslow, L., Read, J., Woolway, R., Brentrup, J., Leach, T., Zwart, J., Albers, S., & Collinge, D. (2019). rLakeAnalyzer: Lake physics tools. CRAN.
Woolway, R. I. (2023). The pace of shifting seasons in lakes. Nature Communications, 14, 2101. https://doi.org/10.1038/s41467-023-37810-4
Woolway, R. I., Sharma, S., Weyhenmeyer, G. A., Debolskiy, A., Golub, M., Mercado-Bettín, D., Perroud, M., Stepanenko, V., Tan, Z., Grant, L., Ladwig, R., Mesman, J., Moore, T. N., Shatwell, T., Vanderkelen, I., Austin, J. A., DeGasperi, C., Dokulil, M., la Fuente, S., … Jennings, E. (2021). Phenological shifts in lake stratification under climate change. Nature Communications, 12, 2318. https://doi.org/10.1038/s41467-021-22657-4
Zhao, L., Zhu, R., Zhou, Q., Jeppesen, E., & Yang, K. (2023). Trophic status and lake depth play important roles in determining the nutrient-chlorophyll a relationship: Evidence from thousands of lakes globally. Water Research, 242, 120182. https://doi.org/10.1016/j.watres.2023.120182
Zhi, W., Klingler, C., Liu, J., & Li, L. (2023). Widespread deoxygenation in warming rivers. Nature. Climate Change, 13(10), 1105-1113. https://doi.org/10.1038/s41558-023-01793-3