Advertisement

Climate variability promotes unprecedented cyanobacterial blooms in a remote, oligotrophic Ontario lake: evidence from paleolimnology

  • Elizabeth J. FavotEmail author
  • Kathleen M. Rühland
  • Anna M. DeSellas
  • Ron Ingram
  • Andrew M. Paterson
  • John P. Smol
Original paper

Abstract

Dickson Lake, located in Algonquin Provincial Park, Ontario, is a remote, oligotrophic lake, where cyanobacterial blooms of the genus Dolichospermum (Ralfs ex Bornet & Flahault) P. Wacklin, L. Hoffmann and J. Komárek were reported for the first time in the fall of 2014, and subsequently in the late spring of 2015. To investigate the potential environmental triggers of these bloom events, we assessed long-term trends in water quality using a multi-proxy paleolimnological approach, examining sedimentary diatoms, chironomids, cladocerans, spectrally inferred chlorophyll a, and cyanobacterial akinetes preserved in a 210Pb-dated sediment core. Assemblage changes were modest in all biological proxies. A subtle increase in the abundance of warm-water chironomid taxa (Topt > 15 °C) commences in the year ~ 2000, with further increases in the most recent years of the sediment record (~ 2013–2015). End-of-summer volume-weighted hypolimnetic oxygen concentrations (CI-VWHO), inferred from chironomid remains, reveal a decline in oxygen concentrations over the last two decades coincident with the highest levels of sedimentary chlorophyll a and cyanobacterial akinetes in the sediment record. These paleolimnological findings corroborate observed reports of the onset of cyanobacterial blooms in Dickson Lake in late 2014 and are consistent with increasingly favourable bloom-forming conditions over the past few decades that are related to warmer air temperatures, sharp declines in wind speed, and a lengthening of the ice-free season by 2 weeks since 1975. It is plausible that late ice-out and a quick onset to stratification in 2014 may have resulted in incomplete spring mixing, early onset of hypolimnetic anoxia, and increased internal nutrient loading, that, occurring during a period when climate conditions were particularly ideal for cyanobacterial proliferation, may have fueled the unprecedented algal blooms in this remote lake. Collectively, the factors causing algal blooms in remote lakes such as Dickson Lake are not yet fully understood, and it is worrisome that with continued warming the triggering conditions may become a more common feature of Algonquin Park and other minimally impacted Boreal Shield lakes in the coming years.

Keywords

Blue-green algae Cyanobacteria Climate change Primary production Hypoxia Akinetes 

Notes

Acknowledgements

We thank two anonymous reviewers for their constructive comments on the manuscript. Ontario Ministry of Natural Resources and Forestry staff are thanked for assistance with field work, and Alison Lake and Glenn Forward in particular. We also thank Ann St. Amand and PhycoTech, Inc. staff for conducting the akinete analysis, Ron Tozer for lake-ice records from Lake of Two Rivers, Trevor Middel and the Harkness Laboratory of Fisheries Research for bathymetric data, and Rory MacKay for information on the logging history around Dickson Lake. This work was funded by a Natural Sciences and Engineering Research Council CREATE grant awarded to J.P.S, a Discovery Grant awarded to A.M.P., and a CGS-M awarded to E.J.F.

Supplementary material

10933_2019_74_MOESM1_ESM.jpg (5.4 mb)
Trends for mean annual and seasonal air temperatures taken for daily minimum, mean, and maximum air temperatures over the last ~100 years at the Madawaska climate station showing a greater rate of increase in minimum than mean or maximum temperatures. Thick lines represent LOESS trends and dashed lines represent time series means (JPEG 5535 kb)
10933_2019_74_MOESM2_ESM.jpg (1.5 mb)
Down-core (with secondary axis of estimated 210Pb dates) Principal Component Analysis (PCA) Axis 1 and Axis 2 sample scores for cladocerans (Clad), diatoms (Dia), and chironomids (Chiro) (JPEG 1504 kb)

References

  1. 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. Springer, Dordrecht, pp 171–203CrossRefGoogle Scholar
  2. Battarbee RW, Jones VJ, Flower RJ, Cameron NG, Bennion H, Carvalho L, Juggins S (2001) Diatoms. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments, terrestrial, algal, and siliceous indicators, vol 3. Kluwer Academic Publishing, Dordrecht, pp 155–202CrossRefGoogle Scholar
  3. Bennett KB (1996) Determination of the number of zones in a biostratigraphical sequence. New Phytol 132:155–170CrossRefGoogle Scholar
  4. Bergström A-K (2010) The use of TN:TP and DIN:TP ratios as indicators for phytoplankton nutrient limitation in oligotrophic lakes affected by N deposition. Aquat Sci 72:277–281CrossRefGoogle Scholar
  5. Bláha L, Babica P, Maršálek B (2009) Toxins produced in cyanobacterial water blooms—toxicity and risks. Interdiscip Toxicol 2:36–41CrossRefGoogle Scholar
  6. Brodin YW (1986) The postglacial history of Lake Flarken, southern Sweden, interpreted from subfossil insect remains. Int Rev Hydrobiol 71:371–432CrossRefGoogle Scholar
  7. Brooks SJ, Langdon PG, Heiri O (2007) The identification and use of Palaearctic Chironomidae larvae in paleoecology. Technical guide no 10. Quaternary Research Association, London, p 10Google Scholar
  8. Brundin L (1949) Chironomiden und andere Bodentiere der südschwedischen Urgebirgsoon. Ein Beitrag zur Kenntnis der bodenfaunistischen Charakterzüge schewedischer oligotropher Seen. Rep Inst freshw res Drottningholm 30:1–914Google Scholar
  9. Bunting L, Leavitt PR, Gibson CE, McGee EJ, Hall VA (2007) Degradation of water quality in Lough Neagh, Northern Ireland, by diffuse nitrogen flux from a phosphorus-rich catchment. Limnol Oceanogr 52:354–369CrossRefGoogle Scholar
  10. Bunting L, Leavitt PR, Simpson GL, Wissel B, Laird KR, Cumming BF, St. Amand A, Engstrom DR (2016) Increased variability and sudden ecosystem state change in Lake Winnipeg, Canada, caused by 20th century agriculture. Limnol Oceanogr 61:2090–2107CrossRefGoogle Scholar
  11. Camburn KE, Charles DF (2000) Diatoms of low-alkalinity lakes in the Northeastern United States. The Academy of Natural Sciences of Philadelphia: Special Publication 18, PhiladelphiaGoogle Scholar
  12. Cottingham KL, Ewing HA, Greer ML, Carey CC, Weathers KC (2015) Cyanobacteria as biological drivers of lake nitrogen and phosphorus cycling. Ecosphere 6:1–19CrossRefGoogle Scholar
  13. Crins WJ, Gray PA, Uhlig PWC, Wester MC (2009) The ecosystems of Ontario, part 1: ecozones and ecoregions. Ontario Ministry of Natural Resources, Peterborough, Ontario, Inventory, Monitoring, and Assessment, SIB TER IMA TR-01Google Scholar
  14. Crumpton WG (1987) A simple and reliable method for making permanent mounts of phytoplankton for light and fluorescence microscopy. Limnol Oceanogr 32:1154–1159CrossRefGoogle Scholar
  15. Cumming G (2010) Algonquin Park forest management plan 2010–2020. Algonquin Forestry AuthorityGoogle Scholar
  16. Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci U S A 106:12788–12793.  https://doi.org/10.1073/pnas.0902080106 CrossRefGoogle Scholar
  17. Eimers MC, Watmough SA, Paterson AM, Dillon PJ, Yao H (2009) Long-term declines in phosphorus export from forested catchments in south-central Ontario. Can J Fish Aquat Sci 66:1682–1692.  https://doi.org/10.1139/F09-101 CrossRefGoogle Scholar
  18. Ellegaard M, Ribeiro S (2017) The long-term persistence of phytoplankton resting stages in aquatic ‘seed banks’. Biol Rev 93:166–183CrossRefGoogle Scholar
  19. Fallu MA, Allaire N, Pienitz R (2000) Freshwater diatoms from northern Québec and Labrador (Canada): species-environment relationships in lakes of boreal forest, forest-tundra and tundra regions. Bibl Diatomol 45:1–200Google Scholar
  20. Fay P (1983) The blue-greens (Cyanophyta-Cyanobacteria) (Studies in biology/Institute of Biology; no. 160). Edward Arnold (Publishers) Ltd., LondonGoogle Scholar
  21. Flett R (2012) Flett research—understanding lead-210 (Pb-210). http://www.flettresearch.ca/UnderstandingPb210.html. Accessed 1 Dec 2017
  22. Frey DG (1959) The taxonomic and phylogenetic significance of the head pores of the Chydoridae (Cladocera). Int Rev Hydrobiol 44:27–50CrossRefGoogle Scholar
  23. Frey DG (1986) Cladocera analysis. In: Berglund BE (ed) Handbook of Holocene palaeoecology and palaeohydrology. Wiley, New York, pp 667–692Google Scholar
  24. Futter MN (2003) Patterns and trends in Southern Ontario lake ice phenology. Environ Monit Assess 88:431–444CrossRefGoogle Scholar
  25. Gannon JE (1971) Two counting cells for the enumeration of zooplankton micro-crustacea. Trans Am Microsc Soc 90:486–490CrossRefGoogle Scholar
  26. Glew JR (1988) A portable extruding device for close interval sectioning of unconsolidated core samples. J Paleolimnol 1:235–239CrossRefGoogle Scholar
  27. Glew JR (1989) A new trigger mechanism for sediment samplers. J Paleolimnol 2:241–243CrossRefGoogle Scholar
  28. Grimm EC (1987) CONISS: A Fortran 77 program for stratigraphically constrained cluster analysis by the method of incremental sum of squares. Comput Geosci 13:13–35CrossRefGoogle Scholar
  29. Hadley KR, Paterson AM, Stainsby EA, Michelutti N, Yao H, Rusak JA, Ingram R, McConnell C, Smol JP (2014) Climate warming alters thermal stability but not stratification phenology in a small north-temperate lake. Hydrol Process 28:6309–6319.  https://doi.org/10.1002/hyp.10120 CrossRefGoogle Scholar
  30. Hawkins E, Ortega P, Suckling E, Schurer A, Hegerl G, Jones P, Joshi M, Osborn TJ, Masson-Delmotte V, Mignot J, Thorne P, Van Oldenborgh GJ (2017) Estimating changes in global temperature since the preindustrial period. Bull Am Meteorol Soc 98:1841–1856CrossRefGoogle Scholar
  31. Huisman J, Codd GA, Paerl HW, Ibelings BW, Verspagen JMH, Visser PM (2018) Cyanobacterial blooms. Nat Rev Microbiol 16:471–483CrossRefGoogle Scholar
  32. Jeziorski A, Smol JP (2017) The ecological impacts of lakewater calcium decline on softwater boreal ecosystems. Environ Rev 25:245–253CrossRefGoogle Scholar
  33. Jeziorski A, Paterson AM, Watson S, Cumming BF, Smol JP (2014) The influence of calcium decline and climate change on the cladocerans within low calcium, circumneutral lakes of the experimental lakes area. Hydrobiologia 722:129–142.  https://doi.org/10.1007/s10750-013-1691-6 CrossRefGoogle Scholar
  34. Jeziorski A, Keller B, Dyer RD, Paterson AM, Smol JP (2015) Differences among modern-day and historical cladoceran communities from the “Ring of Fire” lake region of northern Ontario: identifying responses to climate warming. Fundam Appl Limnol 186:203–216.  https://doi.org/10.1127/fal/2015/0702 CrossRefGoogle Scholar
  35. Jeziorski A, Yan ND, Paterson AM, DeSellas AM, Turner MA, Jeffries DS, Keller W, Weeber RC, McNicol RC, Palmer ME, McIver K, Arseneau K, Ginn BK, Cumming BF, Smol JP (2008) The widespread threat of calcium decline in fresh waters. Science 322:1374–1377CrossRefGoogle Scholar
  36. Juggins S (2017) Rioja: analysis of Quaternary science data, R package version (0.9-15.1). http://cran.r-project.org/package=rioja. Accessed 1 Dec 2017
  37. Kansanen PH (1985) Assessment of pollution history from recent sediments in Lake Vanajavesi, southern Finland. II. Changes in Chironomidae, Chaoboridae and Ceratopogonidae (Diptera) fauna. Ann Zool Fenn 22:57–90Google Scholar
  38. King JR, Shuter BJ, Zimmerman AP (1999) Signals of climate trends and extreme events in the thermal stratification pattern of multibasin Lake Opeongo, Ontario. Can J Fish Aquat Sci 56:847–852CrossRefGoogle Scholar
  39. Komárek J (2013) Cyanoprokaryota 3. Teil/3rd part: heterocystous genera. In: Büdel B, Gärtner G, Krienitz L, Schagerl M (eds) Süßwasserflora von Mitteleuropa, vol 19. Springer, Berlin, pp 1–1130CrossRefGoogle Scholar
  40. Korhola A, Rautio M (2001) Cladocera and other brachiopod crustaceans. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments: zoological indicators, vol 4. Kluwer Academic Publishers, Dordrecht, pp 5–41CrossRefGoogle Scholar
  41. Korosi JB, Smol JP (2012a) An illustrated guide to the identification of cladoceran subfossils from lake sediments in northeastern North America: part 1—the Daphniidae, Leptodoridae, Bosminidae, Polyphemidae, Holopedidae, Sididae, and Macrothricidae. J Paleolimnol 48:571–586CrossRefGoogle Scholar
  42. Korosi JB, Smol JP (2012b) An illustrated guide to the identification of cladoceran subfossils from lake sediments in northeastern North America: part 2—the Chydoridae. J Paleolimnol 48:587–622CrossRefGoogle Scholar
  43. Korosi JB, Burke SM, Thienpont JR, Smol JP (2012) Anomalous rise in algal production linked to lakewater calcium decline through food web interactions. Proc R Soc Lond B Biol Sci 279:1210–1217.  https://doi.org/10.1098/rspb.2011.1411 CrossRefGoogle Scholar
  44. Kothwala DN, Watmough SA, Futter MN, Zhang L, Dillon PJ (2011) Stream nitrate responds rapidly to decreasing nitrate deposition. Ecosystems 14:274–286CrossRefGoogle Scholar
  45. 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, StuttgartGoogle Scholar
  46. Kurek J, Korosi JB, Jeziorski A, Smol JP (2010) Establishing reliable minimum count sizes for cladoceran subfossils sampled from lake sediments. J Paleolimnol 44:603–612CrossRefGoogle Scholar
  47. Laroque I, Rolland N (2006) A visual guide to sub-fossil chrionomids from Quebec to Ellesmere Island. Université du Québec. Institut national de la recherche scientifique. Eau, Terre et Environnement. Rapport de recherche No. R-900Google Scholar
  48. LeBlanc S, Pick FR, Hamilton PB (2008) Fall cyanobacterial blooms in oligotrophic-to-mesotrophic temperate lakes and the role of climate change. Verh Internat Verein Limnol 30:90–94Google Scholar
  49. Matthews-Bird F, Gosling WD, Coe AL, Bush M, Mayle FE, Axford Y, Brooks SJ (2016) Environmental controls on the distribution and diversity of lentic Chironomidae (Insecta: Diptera) across an altitudinal gradient in tropical South America. Ecol Evol 6:91–112CrossRefGoogle Scholar
  50. McDermid J, Fera S, Hogg A (2015) Climate change projections for Ontario: An updated synthesis for policymakers and planners. Ontario Ministry of Natural Resources and Forestry, Science and Research Branch, Peterborough, Ontario. Climate change research report CCRR-44Google Scholar
  51. McGowan S, Britton G, Haworth E, Moss B (1999) Ancient blue-green blooms. Limnol Oceanogr 44:436–439CrossRefGoogle Scholar
  52. McKenney DW, Pedlar JH, Lawrence K, Gray PA, Colombo SJ, Crins WJ (2010) Current and projected future climatic conditions for ecoregions and selected natural heritage areas in Ontario. Ontario Ministry of Natural Resources, Applied Research and Development Branch, Sault Ste. Marie, ON. Climate change research report CCRR-16Google Scholar
  53. Merel S, Walker D, Chicana R, Snyder S, Baurès E, Thomas O (2013) State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ Int 59:303–327CrossRefGoogle Scholar
  54. Michelutti N, Smol JP (2016) Visible spectroscopy reliably tracks trends in paleo-production. J Paleolimnol 56:253–265CrossRefGoogle Scholar
  55. Michelutti N, Wolfe AP, Vinebrooke RD, Rivard B, Briner JP (2005) Recent primary production increases in arctic lakes. Geophys Res Lett 32:L19715CrossRefGoogle Scholar
  56. Michelutti N, Blais JM, Cumming BF, Paterson AM, Rühland K, Wolfe AP, Smol JP (2010) Do spectrally inferred determinations of chlorophyll a reflect trends in lake trophic status? J Paleolimnol 43:205–217CrossRefGoogle Scholar
  57. Minns CK, Shuter BJ, Fung S (2012) Regional projections of climate change effects on ice cover and open-water duration for Ontario Lakes. Ontario Ministry of Natural Resources, Applied Research and Development Branch, Sault St. Marie, ON. Climate change research report CCRR-27Google Scholar
  58. Molot LA (2017) The effectiveness of cyanobacteria nitrogen fixation: review of bench top and pilot scale nitrogen removal studies and implications for nitrogen removal programs. Environ Rev 25:292–295CrossRefGoogle Scholar
  59. Molot LA, Watson SB, Creed IF, Trick CJ, McCabe SK, Verschool MJ, Sorichetti RJ, Powe C, Venkiteswaran JJ, Schiff SL (2014) A novel model for cyanobacteria bloom formation: the critical role of anoxia and ferrous iron. Freshw Biol 59:1323–1340CrossRefGoogle Scholar
  60. O’Beirne MD, Werne JP, Hecky RE, Johnson TC, Katsev S, Reavie ED (2017) Anthropogenic climate change has altered primary productivity in Lake Superior. Nat Commun 8:15713.  https://doi.org/10.1038/ncomms15713 CrossRefGoogle Scholar
  61. O’Neil JM, Davis TW, Burford MA, Gobler CJ (2012) The rise of harmful cyanobacterial blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334CrossRefGoogle Scholar
  62. Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58CrossRefGoogle Scholar
  63. Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1:27–37CrossRefGoogle Scholar
  64. Paerl HW, Fulton RS, Moisander PH, Dyble J (2001) Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Sci World 1:76–113CrossRefGoogle Scholar
  65. Pal S, Gregory-Eaves I, Pick FR (2015) Temporal trends in cyanobacteria revealed through DNA and pigment analyses of temperate lake sediment cores. J Paleolimnol 54:87–101CrossRefGoogle Scholar
  66. Palmer ME, Yan ND, Paterson AM, Girard RE (2011) Water quality changes in south-central Ontario lakes and the role of local factors in regulating lake response to regional stressors. Can J Fish Aquat Sci 68:1038–1050CrossRefGoogle Scholar
  67. Paterson AM, Rühland KM, Anstey CV, Smol JP (2017) Climate as a driver of increasing algal production in Lake of the Woods, Ontario, Canada. Lake Reserv Manag 33:403–414CrossRefGoogle Scholar
  68. Pick FR (2016) Blooming algae: a Canadian perspective on the rise of toxic cyanobacteria. Can J Fish Aquat Sci 73:1149–1158CrossRefGoogle Scholar
  69. Quinlan R, Smol JP (2001a) Setting minimum head capsule abundance and taxa deletion criteria in chironomid-based inference models. J Paleolimnol 26:327–342CrossRefGoogle Scholar
  70. Quinlan R, Smol JP (2001b) Chironomid-based inference models for estimating end-of-summer hypolimnetic oxygen from south-central Ontario lakes. Freshw Biol 46:1529–1551CrossRefGoogle Scholar
  71. Quinlan R, Smol JP (2010) Use of subfossil Chaoborus mandibles in models for inferring past hypolimnetic oxygen. J Paleolimnol 44:43–50CrossRefGoogle Scholar
  72. Quinn NWS, Korver RM, Hicks FJ, Monroe BP, Hawkins RH (1994) An empirical model of lentic brook trout. N Am J Fish Manag 14:692–709CrossRefGoogle Scholar
  73. R Core Team (2015) R: A language and environment for statistical computing. R foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 1 Dec 2017
  74. Rampone J (2018) A paleolimnological and modeling investigation of water quality and biological changes in Algonquin Park lakes in response to multiple stressors. MSc thesis, Queen’s University, Kingston, Ontario, CanadaGoogle Scholar
  75. Reynolds SK, Benke AC (2005) Temperature-dependent growth rates of larval midges (Diptera: Chironomidae) from a southeastern U.S. stream. Hydrobiologia 544:69–75CrossRefGoogle Scholar
  76. Rühland KM, Paterson AM, Hargan K, Jenkin A, Clark BJ, Smol JP (2010) Reorganization of algal communities in the Lake of the Woods (Ontario, Canada) in response to turn-of-the-century damming and recent warming. Limnol Oceanogr 55:2433–2451CrossRefGoogle Scholar
  77. Rühland KM, Paterson AM, Smol JP (2015) Lake diatom responses to warming: reviewing the evidence. J Paleolimnol 54:1–35CrossRefGoogle Scholar
  78. Schelske CL, Peplow A, Brenner M, Spence CN (1994) Low-background gamma counting applications for 210Pb dating of sediments. J Paleolimnol 10:115–128CrossRefGoogle Scholar
  79. Sivarajah B, Rühland KM, Labaj AL, Paterson AM, Smol JP (2016) Why is the relative abundance of Asterionella formosa increasing in a Boreal Shield lake as nutrient levels decline? J Paleolimnol 55:357–367CrossRefGoogle Scholar
  80. Smirnov NN (1996) Cladocera: the Chydorinae and Sayciinae (Chydoridae) of the world. SPB Academic Publishing, AmsterdamGoogle Scholar
  81. Smol JP (2008) Pollution of lakes and rivers: a paleoenvironmental perspective. Wiley, ChicesterGoogle Scholar
  82. 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.R-project.org/package=vegan. Accessed 1 Dec 2017
  83. Sorichetti RJ, Creed IF, Trick CG (2014) Evidence for iron-regulated cyanobacterial predominance in oligotrophic lakes. Freshw Biol 59:679–691CrossRefGoogle Scholar
  84. 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 37:55–62CrossRefGoogle Scholar
  85. Sweetman JN, Smol JP (2006) A guide to the identification of cladoceran remains (Crustacea, Branchipoda) in Alaskan lake sediments. Archiv für Hydrobiologie (Supplementbände) Monogr Stud 151:353–394Google Scholar
  86. Szeroczyńska K, Sarmaja-Korjonen K (2007) Atlas of subfossil Cladocera from central and northern Europe. Friends of the Lower Vistula Society, ŚwiecieGoogle Scholar
  87. Taranu ZE, Gregory-Eaves I, Leavitt PR, Bunting L, Buchaca T, Catalan J, Domaizon I, Guilizzoni P, Lami A, McGowan S, Moorhouse H, Morabito G, Pick FR, Stevenson MR, Thompson PL, Vinebrooke RD (2015) Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the Anthropocene. Ecol Lett 18:375–384CrossRefGoogle Scholar
  88. Taylor DJ, Ishikane CR, Haney RA (2002) The systematics of Holarctic bosminids and a revision that reconciles molecular and morphological evolution. Limnol Oceanogr 47:1486–1495CrossRefGoogle Scholar
  89. ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CANOdraw for Windows user’s guide: software for canonical community ordination, version 5. Microcomputer Power, IthacaGoogle Scholar
  90. van Geel B, Mur LR, Ralska-Jasiewiczowa M, Goslar T (1994) Fossil akinetes of Aphanizomenon and Anabaena as indicators for medieval phosphate-eutrophication of Lake Gosciaz (Central Poland). Rev Palaeobot Palyno 83:97–105CrossRefGoogle Scholar
  91. Vet R, Artz RS, Carou S, Shaw M, Ro C-U, Aas W, Baker A, Bowersox VC, Dentener F, Galy-Lacaux C, Hou A, Pienaar JJ, Gillett R, Forti MC, Gromov S, Hara H, Khodzher T, Mahowald NM, Nickovic S, Rao PSP (2014) A global assessment of precipitation chemistry and deposition of sulfur, nitrogen, sea salt, base cations, organic acids, acidity and pH, and phosphorus. Atmos Environ 93:3–100CrossRefGoogle Scholar
  92. Vincent LA, Wang XL, Milewska EJ, Wan H, Yang F, Swail V (2012) A second generation of homogenized Canadian monthly surface air temperature for climate trend analysis. J Geophys Res 117:D18110Google Scholar
  93. Walker IR (2001) Midges: Chironomidae and related Diptera. 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 155–202Google Scholar
  94. Walker IR, Smol JP, Engstrom DR, Birks HJB (1991) An assessment of Chironomidae as quantitative indicators of past climatic change. Can J Fish Aquat Sci 48:875–987CrossRefGoogle Scholar
  95. Wang XF (2010) fANCOVA: Nonparametric analysis of covariance. R package version 0.5-1. https://cran.r-project.org/web/packages/fANCOVA/index.html. Accessed 1 Dec 2017
  96. Weyhenmeyer GA, Broberg N (2014) Increasing algal biomass in Lake Vänern despite decreasing phosphorus concentrations: A lake-specific phenomenon? Aquat Ecosyst Health Manag 17:341–348CrossRefGoogle Scholar
  97. Wiederholm T (1983) Chironomidae of the Holarctic region. Keys and diagnoses, Part 1: Larvae. In: Andersen T, Cranston PS, Epler JH (eds) Insect systematics & evolution, vol 66. Scandinavian Entomology, Lund, Sweden, p 573Google Scholar
  98. Winter JG, DeSellas AM, Fletcher R, Heintsch L, Morley L, Nakamoto L, Utsumi K (2011) Algal blooms in Ontario, Canada: increases in reports since 1994. Lake Reserv Manag 27:107–114CrossRefGoogle Scholar
  99. 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 36:91–100CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Paleoecological Environmental Assessment and Research Laboratory (PEARL), Department of BiologyQueen’s UniversityKingstonCanada
  2. 2.Dorset Environmental Science Centre (DESC)Ontario Ministry of the Environment, Conservation and Parks (MECP)DorsetCanada

Personalised recommendations