Heterogeneous response of diatom assemblages since ca. 1945 in lakes from boreal regions of northern Alberta and Saskatchewan, Canada

Abstract

The degree to which climate variability and anthropogenic stressors have impacted the rich array of boreal lakes in northern Saskatchewan and Alberta was explored in a dataset of 42 lakes from previous paleolimnological investigations of this region. This dataset was used to evaluate the extent of change in diatom assemblages over the past ~ 60 to 70 years in relation to lake and watershed characteristics. Similarity analysis was used to define the degree of change in diatom composition in lake sediment cores from each lake with a focus on post ca. 1945 changes to establish a common time frame to compare across all lakes. This time frame incorporates pre- and post-development of the Athabasca Oil Sands Region and additionally integrates pre- and post-periods of distinct changes in temperature and precipitation. Beta regression analysis was used to identify potential links between diatom assemblage change and lake physical–chemical and landscape characteristics (limno and landscape models, respectively). Similarity analysis indicated nearly 80% of the lakes showed only a very low degree of change (0–25%) since ca. 1945. Lakes with larger percent change in similarity (> 25%) showed increases in planktonic diatoms, although the specific taxa that changed varied from oligotrophic Discostella spp. to meso-eutrophic taxa, such as Asterionella formosa and Stephanodiscus minutulus. Lake volume and percent peat in the catchment were the most important limno and landscape explanatory variables, respectively, albeit the models had low predictive power. The lakes with large diatom compositional change were dispersed across the region, located in various geological and ecological zones and varying degrees of human disturbance. The interplay of climate and morphometric features of lakes is likely an influential driver of these changes, with larger heat-storage capacity in higher-volume lakes that potentially increases the sensitivity to warming. The small surface areas and shallow morphometry of most lakes, a heterogeneous hydrological and geological landscape, and frequent dominance of diatom assemblages by benthic generalists may explain the minimal responses of diatom assemblages over the past ~ 70 years to anthropogenic influences and climate.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Alahuhta J, Kosten S, Akasaka M, Auderset D, Azzella MM, Bolpagni R et al (2017) Global variation in the beta diversity of lake macrophytes is driven by environmental heterogeneity rather than latitude. J Biogeogr 44:1758–1769. https://doi.org/10.1111/jbi.12978

    Article  Google Scholar 

  2. Allen L, Johnson JD, Vujnovic K (2006) Small patch communities of caribou mountains Wildland Provincial park. In: A report prepared for parks and protected areas. Alberta Community Development, Edmonton, Alberta

  3. Arp CD, Jones BM, Grosse G (2013) Recent lake ice-out phenology within and among lake districts of Alaska, USA. Limnol Oceanogr 58(6):2013–2028. https://doi.org/10.4319/lo.2013.58.6.2013

    Article  Google Scholar 

  4. Bansal S, Sheley RL (2016) Annual grass invasion in sagebrush steppe: the relative importance of climate, soil properties and biotic interactions. Oecologia 181:543–557. https://doi.org/10.1007/s00442-016-3583-3588

    Article  Google Scholar 

  5. Barton K (2018) MuMIn: multi-model inference. https://cran.r-project.org/web/packages/MuMIn/index.html

  6. Bennett KE (2006) Regional hydrological controls on acid-sensitivity lakes in Boreal Canada: an isotopic perspective. M.Sc Thesis University of Victoria

  7. Bennett KE, Gibson JJ, McEachern PM (2008) Water-yield estimates for critical loadings assessment: comparisons of gauging methods versus an isotopic approach. Can J Fish Aquat Sci 65:88–99. https://doi.org/10.1007/s00442-016-3583-8

    Article  Google Scholar 

  8. Bennion H, Sayer CD, Tibby J, Carrick HJ (2010) Diatoms as indicators of environmental change in shallow lakes. In: Smol JP, Stoermer EF (eds) The diatoms: applications for the environmental and earth sciences, 2nd edn. Cambridge University Press, New York, pp 152–173

    Google Scholar 

  9. Bennion H, Simpson GL, Goldsmith BJ (2015) Assessing degradation and recovery pathways in lakes impacted by eutrophication using the sediment record. Front Ecol Evol 3:94. https://doi.org/10.3389/fevo.2015.00094

    Article  Google Scholar 

  10. Bernhardt J, Engelhardt C, Kirillin G, Matschullat J (2012) Lake ice phenology in Berlin–Brandenburg from 1947–2007: observations and model hindcasts. Clim Change 112:791–817. https://doi.org/10.1007/s10584-011-0248-9

    Article  Google Scholar 

  11. Bicudo DC, Tremarin PI, Almeida PD, Zorzalalmeida S, Wengrat S, Faustino SB, Costa LF, Bartozek ECR, Rocha ACR, Bicudo CEM, Morales EA (2016) Ecology and distribution of Aulacoseira species (Bacillariophyta) in tropical reservoirs from Brazil. Diat Res 31:199–215. https://doi.org/10.1080/0269249X.2016.1227376

    Article  Google Scholar 

  12. Blenckner T (2005) A conceptual model of climate-related effects on lake ecosystems. Hydrobiologia 533:1–14. https://doi.org/10.1007/s10750-004-1463-4

    Article  Google Scholar 

  13. Burnham KP, Anderson DR (2002) Model selection and inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  14. Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD (2012) Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res 46:1394–1407. https://doi.org/10.1016/j.watres.2011.12.016

    Article  Google Scholar 

  15. Clark KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-e, Plymouth

    Google Scholar 

  16. Cobbaert Wong A, Bayley SE (2015) Resistance to drought affects persistence of alternative regimes in shallow lakes of the Boreal Plains (Alberta, Canada). Freshw Biol 60:2084–2099. https://doi.org/10.1111/fwb.12633

    Article  Google Scholar 

  17. Cribari-Neto F, Zeileis A (2010) Beta regression in R. J Stat Softw 34:1–24

    Article  Google Scholar 

  18. 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 multi-proxy assessment of eutrophication and recovery in Osoyoos Lake, a transboundary lake in Western North America. Front Ecol Evol 3:84. https://doi.org/10.3389/fevo.2015.00084

    Article  Google Scholar 

  19. Curtis CJ, Flower RJ, Pla S, Rose N, Shilland J, Simpson GL, Turner S, Yang H (2009) Paleolimnological study in selected lakes of wood buffalo region by University College London

  20. Curtis CJ, Flower RJ, Rose N, Shilland J, Simpson GL, Turner S, Yang H, Pla S (2010) Palaeolimnological assessment of lake acidification and environmental change in the Athabasca Oil Sands Region. Alberta J Limnol 69(Suppl. 1):92–104. https://doi.org/10.3274/JL10-69-S1-10

    Article  Google Scholar 

  21. Devito KJ, Hokanson KJ, Moore PA, Kettridge N, Anderson AE, Chasmer L, Hopkinson C, Lukenbach MC, Mendoza CA, Morissette J, Peters DL, Petrone RM, Silins U, Smerdon B, Waddington JM (2016) Landscape controls on long-term runoff in subhumid heterogeneous Boreal Plains catchments. Hydrol Process 31:2737–2751. https://doi.org/10.1002/hyp.11213

    Article  Google Scholar 

  22. Dong X, Bennion H, Maberly SC, Sayer CD, Simpson GL, Battarbee RW (2012) Nutrients exert a stronger control than climate on recent diatom communities in Esthwaite water: evidence from monitoring and palaeolimnological records. Freshw Biol 57:2044–2056. https://doi.org/10.1111/j.1365-2427.2011.02670.x

    Article  Google Scholar 

  23. Edlund MB, Almendinger JE, Fang X, Ramstack Hobbs JM, Vander Meulen DD, Key RL, Engstron DR (2017) Effects of climate change on lake thermal structure and biotic response in northern wilderness lakes. Water 9:678. https://doi.org/10.3390/w9090678

    Article  Google Scholar 

  24. Enache MD, Paterson AM, Cumming BF (2011) Changes in diatom assemblages since pre-industrial times in 40 reference lakes from the experimental lakes area (northwestern Ontario, Canada). J Paleolimnol 46:1–15. https://doi.org/10.1007/s10933-011-9504-2

    Article  Google Scholar 

  25. Evans M, Davies M, Janzen K, Muir D, Hazewinkel R, Kirk J, de Boer D (2016) PAH distributions in sediments in the oil sands monitoring area and western Lake Athabasca: concentration, composition and diagnostic ratios. Environ Pollut 213:671–687. https://doi.org/10.1016/j.envpol.2016.03.014

    Article  Google Scholar 

  26. Ferrari SL, Cribari-Neto F (2004) Beta regression for modelling rates and proportions. J Appl Stat 31:799–815. https://doi.org/10.1080/0266476042000214501

    Article  Google Scholar 

  27. Gibson CE, Anderson NJ, Haworth EY (2003) Review: Aulacoseira suharctica: taxonomy, physiology, ecology and palaeoecology. Eur J Phycol 38:83–101. https://doi.org/10.1080/0967026031000094102

    Article  Google Scholar 

  28. Håkanson L (2005) The importance of lake morphometry and catchment characteristics in limnology–ranking based on statistical analyses. Hydrobiologia 541:117–137. https://doi.org/10.1007/s10750-004-5032-7

    Article  Google Scholar 

  29. Hazewinkel RRO, Wolfe AP, Pla S, Curtis C, Hadley K (2008) Have atmospheric emissions from the Athabasca oil sands impacted lakes in northeastern Alberta, Canada? Can J Fish Aquat Sci 65:1554–1567. https://doi.org/10.1080/0967026031000094102

    Article  Google Scholar 

  30. Hobbs WO, Telford RJ, Birks HJB, Saros JE, Hazewinkel RRO, Perren BB, Saulnier-Talbot É, Wolfe AP (2010) Quantifying recent ecological changes in remote lakes of North America and Greenland using sediment diatom assemblages. PLoS ONE 5:e10026

    Article  Google Scholar 

  31. Ireson AM, Barr AG, Johnstone JF, Mamet SD, van der Kamp G, Whitfield CJ, Michel NL, North RL, Westbrook CJ, DeBeer C, Chun KP, Nazemi A, Sagin J (2015) The changing water cycle: the Boreal Plains ecozone of Western Canada. WIREs Water 2:505–521. https://doi.org/10.1002/wat2.1098

    Article  Google Scholar 

  32. Kelly EN, Schindler DW, Hodson PV, Short JW, Radmanovich R, Nielsen CC (2010) Oil sands development contributes elements toxic at low concentrations to the Athabasca River and its tributaries. Proc Natl Acad Sci 107:16178–16183. https://doi.org/10.1073/pnas.1008754107

    Article  Google Scholar 

  33. Kingsbury MV, Laird KR, Cumming BF (2012) Consistent patterns in diatom assemblages and diversity measures across water-depth gradients from eight Boreal lakes from north-western Ontario (Canada). Freshw Biol 57:1151–1165. https://doi.org/10.1111/j.1365-2427.2012.02781.x

    Article  Google Scholar 

  34. Kirillin G, Leppäranta M, Terzhevik A, Granin N, Bernhardt J, Engelhardt C, Efremova T, Golosov S, Palshin N, Sherstyankin P, Zdorovennova G, Zdorovennov R (2012) Physics of seasonally ice-covered lakes: a review. Aquat Sci 74:659–682. https://doi.org/10.1007/s00027-012-0279-y

    Article  Google Scholar 

  35. Kraemer BM, Anneville O, Chandra S, Dix M, Kuusisto E, Livingstone DM, Rimmer A, Schladow SG, Silow E, Sitoki LM, Tamatamah R, Vadeboncoeur Y, McIntyre PB (2015) Morphometry and average temperature affect lake stratification responses to climate change. Geophys Res Lett 42:4981–4988. https://doi.org/10.1002/2015GL064097

    Article  Google Scholar 

  36. Kurek J, Kirk JL, Muir DCG, Wang X, Evans MS, Smol JP (2013) The legacy of a half century of Athabasca oil sands development recorded by lake ecosytems. Proc Natl Acad Sci 110:1761–1766. https://doi.org/10.1073/pnas.1217675110

    Article  Google Scholar 

  37. Laird KR, Das B, Kingsbury M, Moos MT, Pla-Rabes S, Ahad JME, Wiltse B, Cumming BF (2013) Paleolimnological assessment of limnological change in 10 lakes from northwest Saskatchewan downwind of the Athabasca oils sands based on analysis of siliceous algae and trace metals in sediment cores. Hydrobiologia 720:55–73. https://doi.org/10.1007/s10750-013-1623-5

    Article  Google Scholar 

  38. Laird KR, Das B, Hesjedal B, Leavitt PR, Mushet GR, Scott KA, Simpson GL, Wissel B, Wolfe J, Cumming BF (2017) Paleolimnological assessment of nutrient enrichment on diatom assemblages in a priori defined nitrogen- and phosphorus-limited lakes downwind of the Athabasca Oil Sands. Can J Limnol 76(3):488–502. https://doi.org/10.4081/jlimnol.2017.159

    Article  Google Scholar 

  39. Leavitt PR, Fritz SC, Anderson NJ, Baker PA, Blenckber T, Bunting L, Catalan J, Conley DJ, Hobbs WO, Jeppensen E, Korhola A, McGowan S, Rühland K, Rusak JA, Simpson GL, Solovieva N, Werne J (2009) Paleolimnological evidence of the effects on lakes of energy and mass transfer from climate and humans. Limnol Oceanogr 54:2330–2348. https://doi.org/10.4319/lo.2009.54.6_part_2.2330

    Article  Google Scholar 

  40. Legendre P (1993) Spatial autocorrelation: Trouble or new paradigm? Ecology 74:1659–1673. https://doi.org/10.2307/1939924

    Article  Google Scholar 

  41. Magee MR, Wu CH (2017) Effects of changing climate on ice cover in three morphometrically different lakes. Hydrolog Process 31:308–323. https://doi.org/10.1002/hyp.10996

    Article  Google Scholar 

  42. Magnuson JJ, Benson BJ, Kratz TK (2004) Patterns of coherent dynamics within and between lake districts at local to intercontinental scales. Boreal Environ Res 9:359–369

    Google Scholar 

  43. Moos MT, Laird KR, Cumming BF (2009) Climate-related eutrophication of a small boreal lake in northwestern Ontario: a palaeolimnological perspective. Holocene 19:359–367. https://doi.org/10.1177/0959683608101387

    Article  Google Scholar 

  44. Mushet GR, Laird KR, Das B, Hesjedal B, Leavitt PR, Scott KA, Simpson GL, Wissel B, Wolfe J, Cumming BF (2017) Regional climate changes drive increased scaled chrysophyte abundance in lakes downwind of Athabasca Oil Sands nitrogen emissions. J Paleolimnol 58:419–435. https://doi.org/10.1007/s10933-017-9987-6

    Article  Google Scholar 

  45. Oksanen J, Guillaume Blanchet F, Friendly M, Kindt R., Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) Vegan: community ecology package. https://CRAN.R-project.org/package=vegan

  46. O’Reilly CM, Sharma S, Gray DK, Hampton SE, Read JS, Rowley RJ et al (2015) Rapid and highly variable warming of lake surface waters around the globe. Geophys Res Lett 42:10–773. https://doi.org/10.1002/2015GL066235

    Article  Google Scholar 

  47. Orihel DM, Baulch HM, Casson NJ, North RL, Parsons CT, Seckar DCM, Venkiteswaran JJ (2017) Internal phosphorus loading in Canadian fresh waters: a critical review and data analysis. Can J Fish Aquat Sci 74:2005–2029. https://doi.org/10.1139/cjfas-2016-0500

    Article  Google Scholar 

  48. Paradis E, Blomber S, Bolker B, Brown J, Claude J, Cuong HS et al. (2018) APE: analyses of phylogenetics and evolution. https://cran.r-project.org/web/packages/ape/index.html

  49. RAMP (2011) Regional aquatics monitoring program, 2011 final technical report. https://www.ramp-alberta.org/ramp/results/report.aspx

  50. Richardson DC, Melles SJ, Pilla RM, Hetherington AL, Knoll LB, Williamson CE, Kraemer BM, Jackson JR, Long EC, Moore K, Rudstam LG, Rusak JA, Saros JE, Sharma S, Strock KE, Weathers KC, Wigdahl-Perry CR (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

    Article  Google Scholar 

  51. Rühland K, Priesnitz A, Smol JP (2003) Paleolimnological evidence from diatoms for recent environmental changes in 50 lakes across Canadian Arctic treeline. Arct Antarct Alp Res 35(1):110–123. https://doi.org/10.1657/1523-0430(2003)035[0110:PEFDFR]2.0.CO;2

    Article  Google Scholar 

  52. Rühland KM, Pateron AM, Smol JP (2015) Lake diatom responses to warming: reviewing the evidence. J Paleolimnol 54:1–35. https://doi.org/10.1007/s10933-015-9837-3

    Article  Google Scholar 

  53. Saros JE, Anderson NJ (2015) The ecology of the planktonic diatom Cyclotella and its implications for global environmental change studies. Biol Rev 90:522–541. https://doi.org/10.1111/brv.12120

    Article  Google Scholar 

  54. Sass GZ, Creed IF, Devito KJ (2008) Spatial heterogeneity in trophic status of shallow lakes on the boreal plain: influence of hydrologic setting. Water Resour Res 44:W08444. https://doi.org/10.1029/2007WR006311

    Article  Google Scholar 

  55. Schindler DW (2013) Geoscience of climate and energy 12. Water quality issues in the oil sands region of the lower Athabasca river. Alberta Geosci Can 40:202–214. https://doi.org/10.12789/geocanj.2013.40.012

    Article  Google Scholar 

  56. Schindler DW, Donahue WF (2006) An impending water crisis in Canada’s western prairie provinces. Proc Natl Acad Sci 103:7210–7216. https://doi.org/10.1073/pnas.0601568103

    Article  Google Scholar 

  57. Scott KA, Wissel B, Gibson JJ, Birks SJ (2010) Chemical characteristics and acid sensitivity of boreal headwater lakes in northwest Saskatchewan. J Limnol 69(Suppl 1):33–44. https://doi.org/10.3274/JL10-69-S1-05

    Article  Google Scholar 

  58. Smol JP, Stoermer EF (2010) The diatoms: applications for the. In: Environmental and earth sciences, 2nd edn. University Press, Cambridge

  59. Summers JC, Kurek J, Kirk JL, Muir DCG, Wang X, Wiklund JA, Cooke CA, Evans MS, Smol JP (2016) Recent warming, rather than industrial emissions of bioavailable nutrients, is the dominant driver of lake primary production shifts across the Athabasca Oil Sands Region. PLoS ONE 11:e0153987. https://doi.org/10.1371/journal.pone.0153987

    Article  Google Scholar 

  60. Summers JC, Rühland KM, Kurek J, Smol JP (2019) A diatom-based paleolimnological survey of environmental changes since ~ 1850 in 18 shallow lakes of the Athabasca Oil Sands Region, Canada. J Paleolimnol 61:147–163. https://doi.org/10.1007/s10933-018-0050-z

    Article  Google Scholar 

  61. Taranu ZE, Köster D, Hall RI, Charette T, Forrest F, Cwynar LC, Gregory-Eaves I (2010) Contrasting responses of dimictic and polymictic lakes to environmental change: a spatial and temporal study. Aquat Sci 72:97–115. https://doi.org/10.1007/s00027-009-0120-4

    Article  Google Scholar 

  62. Verpoorter C, Kutser T, Seekell DA, Tranvik LJ (2014) A global inventory of lakes based on high-resolution satellite imagery. Geophys Res Lett 41:6396–6402. https://doi.org/10.1002/2014GL060641

    Article  Google Scholar 

  63. Watmough SA, Whitfield CJ, Fenn ME (2014) The importance of atmospheric base cation deposition for preventing soil acidification in the Athabasca Oil Sands Region of Canada. Sci Total Environ 493:1–11. https://doi.org/10.1016/j.scitotenv.2014.05.110

    Article  Google Scholar 

  64. Wetzel R (2001) Limnology lake and river ecosystems, 3rd edn. Academic Press, Cambridge

    Google Scholar 

  65. Weyhenmeyer GA, Livingstone DM, Meili M, Jensen O, Benson B, Magnuson JJ (2011) Large geographical differences in the sensitivity of ice-covered lakes and rivers in the Northern Hemisphere to temperature changes. Glob Change Biol 17:268–275. https://doi.org/10.1111/j.1365-2486.2010.02249.x

    Article  Google Scholar 

  66. Whitmore TJ, Riedinger-Whitmore MA, Lauterman FM, Curtis JH (2018) Cyanobacterial influence on diatom community lifeform dynamics in shallow subtropical lakes of Florida USA. J Paleolimnol 60:223–246. https://doi.org/10.1007/s10933-018-0018-z

    Article  Google Scholar 

  67. Williamson CE, Saros JE, Vincent WF, Smol JP (2009) Lakes and reservoirs as sentinels, integrators, and regulators of climate change. Limnol Oceanogr 54(6):2273–2282. https://doi.org/10.4319/lo.2009.54.6_part_2.2273

    Article  Google Scholar 

  68. Wiltse B, Paterson AM, Findlay D, Cumming BF (2016) Seasonal and decadal patterns in Discostella (Bacillariophyceae) species from bi-weekly records of two boreal lakes (Experimental Lakes Area, Ontario, Canada). J Phycol 52(5):817–826. https://doi.org/10.1111/jpy.12443

    Article  Google Scholar 

  69. Wolfe AP, Hobbs WO, Birks HH, Briner JP, Holmgren S, Ingólfsson O, Kaushal SS, Miller GH, Pagani M, Saros JE, Vinebrooke RD (2013) Stratigraphic expressions of the Holocene-Anthropocene transition revealed in sediments from remote lakes. Earth Sci Rev 116:17–34. https://doi.org/10.1016/j.earscirev.2012.11.001

    Article  Google Scholar 

  70. Wood SN (2018) mgcv: mixed GAM computation vehicle with automatic smoothness estimation. https://cran.r-project.org/web/packages/mgcv/index.html

  71. Zeileis A, Cribari-Neto F, Gruen B, Kosmidis I, Simas AB, and Rocha AV (2016) betareg: Beta Regression. https://cran.r-project.org/web/packages/betareg/index.html

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Kathleen R. Laird.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 2395 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Laird, K.R., Mushet, G.R., Flower, R.J. et al. Heterogeneous response of diatom assemblages since ca. 1945 in lakes from boreal regions of northern Alberta and Saskatchewan, Canada. J Paleolimnol 64, 137–153 (2020). https://doi.org/10.1007/s10933-020-00128-y

Download citation

Keywords

  • Diatom assemblages
  • Boreal lakes
  • Climate
  • Athabasca oil sands region