Abstract
Long-term changes in diatom community composition provided important insights into how multiple stressors affected shallow, macrophyte-dominated Lake Opinicon, Ontario (Canada) over the past ~ 200 years. A previous paleolimnological study of a sediment core collected in 1995 found that diatom responses to numerous large-scale cultural disturbances since the early nineteenth century were moderate in comparison to pronounced diatom responses to similar disturbances in nearby deeper lakes within the Rideau Canal system. The abundance of macrophytes in shallow and previously polymictic Lake Opinicon likely played an important role in maintaining a stable, clear-water equilibrium state. We examined diatom assemblages from a sediment core collected in 2019 to re-assess whether Lake Opinicon maintained its resistance to change over the past ~ 25 years. Despite numerous, intense early nineteenth and twentieth century cultural disturbances in Lake Opinicon’s catchment (complete deforestation, flooding with the construction of the Rideau Canal), the highest rate of diatom compositional change occurred only in the past ~ 25 years, when planktonic diatoms became prevalent for the first time in the lake’s postglacial history. This recent shift in assemblage composition is not explained by nutrient enrichment, as total phosphorus concentrations, measured since the 1970s, have declined significantly. The first appearance of zebra mussels (~ 1990s) and significant increases in Secchi depth broadly co-occurred with the diatom assemblage shift, but precipitous declines in mussel populations since 2013 and a continued increase in planktonic diatom taxa suggest the impact of this invasive species was modest. Instead, changes in diatom assemblage composition were strongly related to increasing regional air temperatures. Limnological monitoring indicated that, over the past few decades, previously polymictic Lake Opinicon has experienced increasingly longer and more stable periods of thermal stratification that are consistent with observed trends in regional warming and reduced wind speed. These water column changes, which accompanied reduced ice cover duration, would have provided favourable conditions for planktonic diatom growth. We conclude that the nature and high rate of diatom compositional change over the past ~ 25 years signifies that an ecological threshold was crossed in response to warming and changes in lake thermal structure.
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References
Agbeti MD (1993) Comparison of seasonal succession of phytoplankton in two lakes with different mixing regimes. PhD thesis. Queen’s University, Kingston
Agbeti MD, Kingston JC, Smol JP, Watters C (1997) Comparison of phytoplankton succession in two lakes of different mixing regimes. Arch Hydrobiol 140:37–69
Agbeti MD, Smol JP (1995a) Chrysophyte population and encystment patterns in two Canadian lakes. J Phycol 31:70–78
Agbeti MD, Smol JP (1995b) Winter limnology: a comparison of physical, chemical and biological characteristics in two temperate lakes during ice cover. Hydrobiologia 304:221–234
Appleby PG (2001) Chronostratigraphic techniques in recent sediments. In: Last WM, Smol JP (eds) Tracking environmental change using lake sediments. Basin analysis, coring, and chronological techniques, vol 1. Kluwer Academic Publishers, Dordrecht, pp 171–203
Battarbee RW, Jones VJ, Flower RJ, Cameron NG, Bennion H, Carvalho L, Juggins S (2001) Diatoms. In: Smol JP, Birks HJ, Last W (eds) Tracking environmental change using lake sediments. Terrestrial, algal, and siliceous indicators, vol 3. Kluwer Academic Publishers, Dordrecht, pp 155–202
Bennett KB (1996) Determination of the number of zones in a biostratigraphical sequence. New Phytol 132:155–170
Bennett KD, Humphry RW (1995) Analysis of late-glacial and Holocene rates of vegetational change at two sites in the British Isles. Rev Palaeobot Palynol 85:263–287
Birks HJB (2012) Introduction and overview part II. In: Birks HJB, Lotter AF, Juggins S, Smol JP (eds) Volume 5: tracking environmental change using lake sediments: data handling and numerical techniques. Springer, Dordrecht, pp 101–121
Bramburger AJ, Reavie ED (2016) A comparison of phytoplankton communities of the deep chlorophyll layers and epilimnia of the Laurentian Great Lakes. J Great Lakes Res 42:1016–1025
Budd JW, Drummer TD, Nalepa TF, Fahnenstiel GL (2001) Remote sensing of biotic effects: Zebra mussels (Dreissena polymorpha) influence on water clarity in Saginaw Bay, Lake Huron. Limnol Oceanogr 46:213–223
Bush E, Lemmen DS (2019) Canada's changing climate report. Government of Canada, Ottawa, ON
Cahill KL, Gunn JM, Futter MN (2005) Modelling ice cover, timing of spring stratification, and end-of-season mixing depth in small Precambrian Shield lakes. Can J Fish Aquat Sci 62:2134–2142
Camburn KE, Charles DF (2000) Diatoms of low alkalinity lakes in the Northeastern United States. Scientific Publications, Philadelphia, USA
Caraco NF, Cole JJ, Strayer DL (2006) Top down control from the bottom: regulation of eutrophication in a large river by benthic grazing. Limnol Oceanogr 51:664–670
Christie CE, Smol JP (1996) Limnological effects of 19th century canal construction and other disturbances on the trophic state history of Upper Rideau Lake, Ontario. Lake Reserv Manage 12:448–454
Conboy MA, English P (2010) Freeze up and thaw dates for Lake Opinicon, 1985–2010. https://opinicon.wordpress.com/2010/12/06/freeze-up-and-thaw-dates-for-lake-opinicon-1985-2010/#:~:text=The%20mean%20duration%20of%20ice%20cover%20on%20Lake%20Opinicon%20is%20119%20days. Accessed 5 Mar 2021
Coops H, Beklioglu M, Crisman TL (2003) The role of water-level fluctuations in shallow lake ecosystems–workshop conclusions. Hydrobiologia 506:23–27
Crowder A, Conboy MA (2010) History of QUBS forests: trees at QUBS point in the 1940s and 1970s. https://opinicon.wordpress.com/2010/07/21/history-of-qubs-forests-trees-at-qubs-point-in-the-1940s-and-1970s/. Accessed 15 May 2020
Crowder A, Topping KEJ, Topping JC (1996) Plants of the Kingston Region. The Fowler Herbarium, Queen’s University, Kingston
Crowder AA, Bristow JM, King MR, Vanderkloet S (1977) Distribution, seasonality, and biomass of aquatic macrophytes in Lake Opinicon (Eastern Ontario). Nat Can 104:441–456
Cumming BF, Laird KR, Gregory-Eaves I, Simpson KG, Sokal MA, Nordin R, Walker IR (2015) Tracking past changes in lake-water phosphorus with a 251-lake calibration dataset in British Columbia: tool development and application in a multiproxy assessment of eutrophication and recovery in Osoyoos Lake, a transboundary lake in Western North America. Front Ecol Evol 3:1–18
Cumming BF, Wilson SE, Smol JP (1993) Paleolimnological potential of chrysophyte cysts and scales and of sponge spicules as indicators of lake salinity. Int J Salt Lake Res 2:87–92
Curran HW, Bardach J, Bowman RI, Lawler HG (1947) A biological survey of Lake Opinicon: progress report, Queen’s University Biological Station, Chaffey’s Lock, Ontario
Fishman DB, Adlerstein SA, Vanderploeg HA, Fahnenstiel GL, Scavia D (2010) Phytoplankton community composition of Saginaw Bay, Lake Huron, during the zebra mussel (Dreissena polymorpha) invasion: a multivariate analysis. J Great Lakes Res 36:9–19
Fleming L (1981) Hearth and heritage: history of Chaffey’s Lock and area, 1800–1980. Brown and Martin Ltd., Kingston, Canada
Forrest F, Reavie ED, Smol JP (2002) Comparing limnological changes associated with 19th century canal construction and other catchment disturbances in four lakes within the Rideau Canal system, Ontario, Canada. J Limnol 61:183–197
Futter MN (2003) Patterns and trends in Southern Ontario lake ice phenology. Environ Monit Assess 88:431–444
Genkai-Kato M (2007) Macrophyte refuges, prey behaviour and trophic interactions: consequences for lake water clarity. Ecol Lett 10:105–114
Glew JR (1988) A portable extruding device for close interval sectioning of unconsolidated core samples. J Paleolimnol 1:235–239
Glew JR (1989) A new trigger mechanism for sediment samplers. J Paleolimnol 2:241–243
Grimm EC (1991) TILIA v2. 0. b. 4 and TGView v2. 0 (computer software). Illinois State Museum, Research and Collections Center, Springfield, United States
Hadley KR, Paterson AM, Hall RI, Smol JP (2013) Effects of multiple stressors on lakes in south-central Ontario: 15 years of change in lakewater chemistry and sedimentary diatom assemblages. Aquat Sci 75:349–360
Hadley KR, Paterson AM, Rühland KM, White H, Wolfe BB, Keller W, Smol JP (2019) Biological and geochemical changes in shallow lakes of the Hudson Bay Lowlands: a response to recent warming. J Paleolimnol 61:313–328
Harrell FE (2022) Hmisc: Harrell Miscellaneous, R package version 4.7-0. Available at: https://cran.r-project.org/web/packages/Hmisc/index.html
Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432
Hilt S, Brothers S, Jeppesen E, Veraart AJ, Kosten S (2017) Translating regime shifts in shallow lakes into changes in ecosystem functions and services. Bioscience 67:928–936
Ingram RG, Girard RE, Paterson AM, Sutey P, Evans D, Xu R, Rusak J, Thomson C, Masters C (2013) Lake sampling methods. Ontario Ministry of the Environment, Dorset Environmental Science Centre, Dorset
Janssen CR, Birks HJB (1994) Recurrent groups of pollen types in time. Rev Palaeobot Palyno 82:165–173
Karst TL, Smol JP (1998) Tracking the cultural eutrophication history of Collins Lake (southeastern Ontario, Canada) using paleolimnological techniques. Lake Reserv Manage 14:456–465
Karst TL, Smol JP (2000) Paleolimnological evidence of limnetic nutrient concentration equilibrium in a shallow, macrophyte-dominated lake. Aquat Sci 62:20–38
King JR, Shuter BJ, Zimmerman AP (1997) The response of the thermal stratification of South Bay (Lake Huron) to climatic variability. Can J Fish Aquat Sci 54:1873–1882
Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15:259–263
Krammer K, Lange-Bertalot H (1986–1991) Bacillariophyceae. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) Süßwasserflora von Mitteleuropa, Volume 2 (1–4). Gustav Fischer Verlag, Stuttgart
Laird K (2017) Lake fact sheet (2017) Opinicon Lake. https://www.crca.ca/wp-content/uploads/PDFs/LakeReports/2017-FactSheet-OpiniconLake.pdf. Accessed 2 March 2020
Larouche P, Galbraith PS (2016) Canadian coastal seas and Great Lakes sea surface temperature climatology and recent trends. Can J Remote Sens 42:243–258
Le Bagousse-Pinguet Y, Liancourt P, Gross N, Straile D (2012) Indirect facilitation promotes macrophyte survival and growth in freshwater ecosystems threatened by eutrophication. J Ecol 100:530–538
Lindenschmidt KE, Chorus I (1998) The effect of water column mixing on phytoplankton succession, diversity, and similarity. J Plankton Res 20:1927–1951
Little JL, Smol JP (2000) Changes in fossil midge (Chironomidae) assemblages in response to cultural activities in a shallow, polymictic lake. J Paleolimnol 23:207–212
Lotter AF, Bigler C (2000) Do diatoms in the Swiss Alps reflect the length of ice-cover? Aquat Sci 62:125–141
Madsen JD, Chambers PA, James WF, Koch EW, Westlake DF (2001) The interaction between water movement, sediment dynamics and submersed macrophytes. Hydrobiologia 444:71–84
Mason LA, Riseng CM, Gronewold AD, Rutherford ES, Wang J, Clites A, Smith SD, McIntyre PB (2016) Fine-scale spatial variation in ice cover and surface temperature trends across the surface of the Laurentian Great Lakes. Clim Change 138:71–83
McGucken W (1989) The Canadian federal government, cultural eutrophication, and the regulation of detergent phosphates, 1970. Environ Rev 13:155–166
McLeod AI (2016) Package ‘Kendall’, R Package Version 2.2. Available at: https://cran.r-project.org/web/packages/Kendall/index.html
Meerhoff M, Iglesias C, De Mello FT, Clemente JM, Jensen E, Lauridsen TL, Jeppesen E (2007) Effects of habitat complexity on community structure and predator avoidance behaviour of littoral zooplankton in temperate versus subtropical shallow lakes. Freshwater Biol 52:1009–1021
Meerhoff M, Teixeira-de Mello F, Kruk C, Alonso C, Gonzalez-Bergonzoni I, Pacheco JP, Lacerot G, Arim M, Beklioğlu M, Brucet S, Goyenola G, Iglesias C, Mazzeo N, Kosten S, Jeppesen E (2012) Environmental warming in shallow lakes: a review of potential changes in community structure as evidenced from space-for-time substitution approaches. Adv Ecol Res 46:259–349
Michelutti N, Blais JM, Cumming BF, Paterson AM, Rühland KM, Wolfe AP, Smol JP (2010) Do spectrally inferred determinations of chlorophyll a reflect trends in lake trophic status? J Paleolimnol 43:205–217
Michelutti N, Smol JP (2016) Visible spectroscopy reliably tracks trends in paleo-production. J Paleolimnol 56:253–265
Mulderij G, Van Nes EH, Van Donk E (2007) Macrophyte–phytoplankton interactions: the relative importance of allelopathy versus other factors. Ecol Model 204:85–92
Nelligan C, Jeziorski A, Rühland KM, Paterson AM, Meyer-Jacob C, Smol JP (2020) A multibasin comparison of historical water quality trends in Lake Manitou, Ontario, a provincially significant lake trout lake. Lake Reserv Manage 36:243–259
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin RP, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) Vegan: community ecology package. R package version 2.2–1. http://CRAN.Rproject.org/package=vegan. Accessed 10 Dec 2019
Paerl HW, Hall NS, Peierls BL, Rossignol KL, Joyner AR (2014) Hydrologic variability and its control of phytoplankton community structure and function in two shallow, coastal, lagoonal ecosystems: the Neuse and New River Estuaries, North Carolina, USA. Estuar Coast 37:31–45
Pasciak WJ, Gavis J (1974) Transport limitation of nutrient uptake in phytoplankton. Limnol Oceanogr 19:881–888
Peierls BL, Hall NS, Paerl HW (2012) Non-monotonic responses of phytoplankton biomass accumulation to hydrologic variability: a comparison of two coastal plain North Carolina estuaries. Estuar Coast 35:1376–1392
Poister D, Kurth A, Farrell A, Gray S (2012) Seasonality of Aulacoseira ambigua abundance and filament length: biogeochemical implications. Plankton Benthos Res 7:55–63
Ptacnik R, Diehl S, Berger S (2003) Performance of sinking and nonsinking phytoplankton taxa in a gradient of mixing depths. Limnol Oceanogr 48:1903–1912
Quinlan R, Hall RI, Paterson AM, Cumming BF, Smol JP (2008) Long-term assessments of ecological effects of anthropogenic stressors on aquatic ecosystems from paleoecological analyses: challenges to perspectives of lake management. Can J Fish Aquat Sci 65:933-944
R Core Team (2018) R: a language and environment for statistical computing. http://www.R-project.org/. Accessed 5 March 2020
Reavie ED, Kireta AR (2015) Centric, araphid and eunotioid diatoms of the coastal Laurentian Great Lakes. Sampling, taxonomic descriptions and environmental characteristics. In: Lange-Bertalot H, Kociolek P (eds) Volume 62: Bibl Diatomol, Stuttgart
Reavie ED, Sgro GV, Estepp LR, Bramburger AJ, Shaw Chraïbi VL, Pillsbury RW, Cai M, Stow CA, Dove A (2017) Climate warming and changes in Cyclotella sensu lato in the Laurentian Great Lakes. Limnol Oceanogr 62:768–783
Round FE, Crawford RM, Mann DG (1990) Diatoms: biology and morphology of the genera. Cambridge University Press, Cambridge
Rühland KM, Paterson AM, Keller W, Michelutti N, Smol JP (2013) Global warming triggers the loss of a key Arctic refugium. Proc R Soc B 280:20131887
Rühland KM, Paterson AM, Smol JP (2008) Hemispheric-scale patterns of climate-related shifts in planktonic diatoms from North American and European lakes. Glob Chang Biol 14:2740–2754
Rühland KM, Paterson AM, Smol JP (2015) Lake diatom responses to warming: reviewing the evidence. J Paleolimnol 54:1–35
Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279
Schelske CL, Peplow A, Brenner M, Spencer CN (1994) Low-background gamma counting: applications for 210Pb dating of sediments. J Paleolimnol 10:115–128
Schindler DW, Beaty KG, Fee EJ, Cruikshank DR, DeBruyn ER, Findlay DL, Linsey GA, Shearer JA, Stainton MP, Turner MA (1990) Effects of climatic warming on lakes of the central boreal forest. Science 250:967–970
Simpson GL (2018) Modelling palaeoecological time series using generalised additive models. Front Ecol Evol 6:149
Smol JP (1985) The ratio of diatom frustules to chrysophycean statospores: a useful paleolimnological index. Hydrobiologia 123:199–208
Sorvari S, Korhola A, Thompson R (2002) Lake diatom response to recent arctic warming in Finnish Lapland. Glob Chang Biol 8:171–181
Spaulding SA, Bishop IW, Edlund MB, Lee S, Furey P, Jovanovska E, Potapova M (2019) Diatoms of North America. https://diatoms.org/. Accessed 15 Jan 2020
Stainsby EA, Winter JG, Jarjanazi H, Paterson AM, Evans DO, Young JD (2011) Changes in the thermal stability of Lake Simcoe from 1980 to 2008. J Great Lakes Res 37:55–62
Stockner JG (1971) Preliminary characterization of lakes in the Experimental Lakes Area, Northwestern Ontario, using diatom occurrences in sediments. J Fish Res Board Can 28:265–275
Stoermer EF, Emmert G, Julius ML, Schelske CL (1996) Paleolimnologic evidence of rapid recent change in Lake Erie’s trophic status. Can J Fish Aquat Sci 53:1451–1458
Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshwater Biol 55:152–174
Talbot CJ, Bennett EM, Cassell K, Hanes DM, Minor EC, Paerl H, Raymond PA, Vargas R, Vidon PG, Wollheim W, Xenopoulos MA (2018) The impact of flooding on aquatic ecosystem services. Biogeochemistry 141:439–461
Ter Braak CJ, Šmilauer P (2002) CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). http://canoco.com/. Accessed 10 Dec 2019
Van Dam H, Mertens A, Sinkeldam J (1994) A coded checklist and ecological indicator values of freshwater diatoms from the Netherlands. Neth J Aquat Ecol 28:117–133
Vincent LA, Hartwell MM, Wang XL (2020) A third generation of homogenized temperature for trend analysis and monitoring changes in Canada’s climate. Atmos Ocean 58:173–191
Walker IR, Reavie ED, Palmer S, Nordin RN (1993) A palaeoenvironmental assessment of human impact on Wood Lake, Okanagan Valley, British Columbia, Canada. Quat Int 20:51–70
Warren S (1997) Hub of the Rideau: a history of South Crosby township. The Local Architectural Conservation Advisory Committee, Township of South Crosby, Leeds County, Ontario
Watson K (2000) Rideau Canal Waterway—zebra mussel sightings. http://www.rideau-info.com/local/zebra.html. Accessed 5 Apr 2020
Watson K (2019) Paddling the Rideau Canal- Jones Falls Locks to Chaffeys Lock (includes Sand and Opinicon lakes). http://www.rideau-info.com/canal/paddling/watson-paddling-guide-05.html. Accessed 5 Apr 2020
Werner P, Chaisson M, Smol JP (2005) Long-term limnological changes in six lakes with differing human impacts from a limestone region in southwestern Ontario, Canada. Lake Reserv Manage 21:436–452
Winder M, Reuter JE, Schladow SG (2009) Lake warming favours small-sized planktonic diatom species. Proc R Soc B 276:427–435
Wolfe AP, Vinebrooke RD, Michelutti N, Rivard B, Das B (2006) Experimental calibration of lake-sediment spectral reflectance to chlorophyll a concentrations: methodology and paleolimnological validation. J Paleolimnol 36:91–100
Woolway RI, Merchant CJ (2019) Worldwide alteration of lake mixing regimes in response to climate change. Nat Geosci 12:271–276
Woolway RI, Sharma S, Smol JPS (2022) Lakes in hot water: the impacts of a changing climate on aquatic ecosystems. Bioscience. https://doi.org/10.1093/biosci/biac052
Zeeb B, Smol JP (2001) Chrysophyte cysts and scales. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments. Terrestrial, algal, and siliceous indicators, vol 3. Kluwer Academic Publishers, Dordrecht, pp 202–223
Zohary T, Gasith A (2014) The littoral zone. In: Zohary T, Sukeni A, Berman T, Nishri A (eds) Lake Kinneret, ecology and management. Springer, Dordrecht, pp 517–532
Acknowledgements
This research was funded by the Natural Sciences and Engineering Research Council of Canada and the Rideau Lakes Environmental Foundation (RLEF). We thank the staff at the Queen’s University Biological Station (QUBS) for logistical support, and the Ontario Ministry of the Environment, Conservation and Parks and Dr. Shelley Arnott for sharing their historical limnological data, and Dr. David Phillipp for sharing his knowledge of historical zebra mussel abundances in Lake Opinicon. We thank Dr. Mark Brenner and two anonymous reviewers for providing valuable comments that helped us improve our paper considerably.
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Balasubramaniam, K., Rühland, K.M. & Smol, J.P. A diatom-based paleolimnological re-assessment of previously polymictic Lake Opinicon, Ontario (Canada): crossing an ecological threshold in response to warming over the past 25 years. J Paleolimnol 69, 37–55 (2023). https://doi.org/10.1007/s10933-022-00261-w
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DOI: https://doi.org/10.1007/s10933-022-00261-w