, Volume 776, Issue 1, pp 85–97 | Cite as

Temporal changes in cladoceran assemblages subjected to a low calcium environment: combining the sediment record with long-term monitoring data

  • Laura E. Redmond
  • Adam Jeziorski
  • Andrew M. Paterson
  • James A. Rusak
  • John P. Smol
Primary Research Paper


Lakewater calcium (Ca) decline affects softwater lakes across the Canadian Shield. Ca decline is one consequence of acid deposition, and has impeded biological recovery in formerly acidified lakes. Reduced Ca availability may advantage taxa better adapted to low Ca waters. Crosson Lake in south-central Ontario (Canada) has an extensive monitoring record and has experienced strong Ca decline since the late 1970s, recently falling below 1.5 mg L−1, a threshold value for some large Daphnia O.F. Müller, 1785 taxa. Paleolimnological analysis of the sedimentary cladoceran assemblages revealed that changes associated with the Ca decline began in the early 1970s. Relative abundances of the jelly-clad Holopedium glacialis Rowe, 2007 and the Daphnia pulex complex increased while Ca-sensitive members of the Daphnia longispina complex decreased. Zooplankton net hauls (1981–2010) corroborate the paleolimnological analysis, revealing that increases in the D. pulex complex were due to Daphnia catawba Coker, 1926 (a taxon tolerant of low Ca). Lakewater Ca, dissolved organic carbon and total phosphorus explain a significant amount of variation within the cladoceran community; however, the relationship between Ca concentration and the daphniid community was most apparent. The Crosson Lake paleolimnological and direct monitoring data may describe ecological changes that are also occurring in many other softwater lakes across the Canadian Shield and elsewhere.


Cladocera Paleolimnology Acidification Calcium decline Holopedium Daphnia 


  1. Anderson, T. & D. O. Hessen, 1991. Carbon, nitrogen and phosphorus content of freshwater zooplankton. Limnology and Oceanography 36: 807–814.CrossRefGoogle Scholar
  2. Appleby, P. G., 2001. Chronostratigraphic techniques in recent sediments. In Last, W. M. & J. P. Smol (eds), Tracking Environmental Change Using Lake Sediments, Volume 1: Developments in Paleoenvironmental Research. Kluwer Academic Publishers, Springer, The Netherlands: 171–203.Google Scholar
  3. Ashforth, D. & N. D. Yan, 2008. The interactive effects of calcium concentration and temperature on the survival and reproduction of Daphnia pulex at high and low food concentrations. Limnology and Oceanography 53: 420–432.CrossRefGoogle Scholar
  4. Barrow, J. L., A. Jeziorski, K. M. Rühland, K. R. Hadley & J. P. Smol, 2014. Diatoms indicate that calcium decline, not acidification, explains recent cladoceran assemblage changes in south-central Ontario softwater lakes. Journal of Paleolimnology 52: 61–75.CrossRefGoogle Scholar
  5. Bennett, K. D., 1996. Determination of the number of zones in a biostratigraphic sequence. New Phytologist 132: 155–170.CrossRefGoogle Scholar
  6. Bottrell, H. H., 1975. Generation time, length of life, instar duration and frequency of moulting, and their relationship to temperature in eight species of Cladocera from the River Thames, Reading. Oecologia 19: 129–140.CrossRefGoogle Scholar
  7. Cairns, A., 2010. Field assessments and evidence of impacts of calcium decline on Daphnia (Crustacea, Anomopoda) in Canadian Shield lakes. M.Sc. thesis, Department of Biology, York University, Toronto.Google Scholar
  8. Cairns, A. & N. Yan, 2009. A review of the influence of low ambient calcium concentrations on freshwater daphniids, gammarids, and crayfish. Environmental Reviews 17: 67–79.CrossRefGoogle Scholar
  9. Cogbill, C. V. & G. E. Likens, 1974. Acid precipitation in the northeastern United States. Water Resource Research 10: 1133–1137.CrossRefGoogle Scholar
  10. Couture, R. M., H. de Wit, K. Tominaga, P. Kiuru & I. Markelov, 2015. Oxygen dynamics in a boreal lake responds to long-term changes in climate, ice phenology, and DOC inputs. Journal of Geophysical Research: Biogeosciences 120: 2441–2456.Google Scholar
  11. Davidson, T. A., C. D. Sayer, M. R. Perrow, M. Bramm & E. Jeppesen, 2007. Are the controls of species composition similar for contemporary and sub-fossil cladoceran assemblages? A study of 39 shallow lakes of contrasting trophic status. Journal of Paleolimnology 38: 117–134.CrossRefGoogle Scholar
  12. Dixit, S. S., A. S. Dixit & J. P. Smol, 1992. Assessment of changes in lake water chemistry in Sudbury area lakes since preindustrial times. Canadian Journal of Fisheries and Aquatic Sciences 49: 8–16.CrossRefGoogle Scholar
  13. Futter, M. N., 2003. Patterns and trends in Southern Ontario lake ice phenology. Environmental Monitoring and Assessment 88: 431–444.CrossRefPubMedGoogle Scholar
  14. Glew, J. R., 1988. A portable extruding device for close interval sectioning of unconsolidated core samples. Journal of Paleolimnology 1: 235–239.CrossRefGoogle Scholar
  15. Glew, J. R., 1989. A new trigger mechanism for sediment samplers. Journal of Paleolimnology 2: 241–243.CrossRefGoogle Scholar
  16. Gliwicz, Z. M., 1990. Food thresholds and body size in cladocerans. Nature 343: 638–640.CrossRefGoogle Scholar
  17. Grimm, E. C., 1987. CONISS: a FORTRAN 77 program for stratigraphically constrained cluster analysis by the method of incremental sum of squares. Computers and Geosciences 13: 13–35.CrossRefGoogle Scholar
  18. Hall, R. I. & J. P. Smol, 1996. Paleolimnological assessment of long-term water-quality changes in south-central Ontario lakes affected by cottage development and acidification. Canadian Journal of Fisheries and Aquatic Sciences 53: 1–17.CrossRefGoogle Scholar
  19. Hebert, P. D. N., 1995. The Daphnia of North America: an illustrated fauna—CD-ROM. Cyber Natural Software. University of Guelph.Google Scholar
  20. Hessen, D. O., B. A. Faafeng & T. Andersen, 1995. Competition or niche segregation between Holopedium and Daphnia; empirical light on abiotic key parameters. Hydrobiologia 307: 253–261.CrossRefGoogle Scholar
  21. Houle, D., R. Ouimet, S. Couture & C. Gagnon, 2006. Base cation reservoirs in soil control the buffering capacity of lakes in forested catchments. Canadian Journal of Fisheries and Aquatic Sciences 63: 471–474.CrossRefGoogle Scholar
  22. Jeffries, D. S., T. G. Brydges, P. J. Dillon & W. Keller, 2003. Monitoring the results of Canada/U.S.A. acid rain control programs: some lake Responses. Environmental Monitoring and Assessment 88: 3–19.CrossRefPubMedGoogle Scholar
  23. Jeziorski, A. & N. D. Yan, 2006. Species identity and aqueous calcium concentrations as determinants of calcium concentrations of freshwater crustacean zooplankton. Canadian Journal of Fisheries and Aquatic Sciences 63: 1007–1013.CrossRefGoogle Scholar
  24. Jeziorski, A., N. D. Yan, A. M. Paterson, A. M. DeSellas, M. A. Turner, D. S. Jeffries, B. Keller, R. C. Weeber, D. K. McNicol, M. E. Palmer, K. McIver, K. Arseneau, B. K. Ginn, B. F. Cumming & J. P. Smol, 2008. The widespread threat of calcium decline in fresh waters. Science 322: 1374–1377.CrossRefPubMedGoogle Scholar
  25. Jeziorski, A., A. M. Paterson & J. P. Smol, 2012. Changes since the onset of acid deposition among calcium-sensitive cladoceran taxa within softwater lakes of Ontario, Canada. Journal of Paleolimnology 48: 323–337.CrossRefGoogle Scholar
  26. Jeziorski, A., A. J. Tanentzap, N. D. Yan, A. M. Paterson, M. E. Palmer, J. B. Korosi, J. A. Rusak, M. T. Arts, W. Keller, R. Ingram, A. Cairns & J. P. Smol, 2015. The jellification of north temperate lakes. Proceedings of the Royal Society B 282: 20142449. doi:10.1098/rspb.2014.2449.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kattel, G. R., R. W. Battarbee, A. Mackay & H. J. B. Birks, 2007. Are cladoceran fossils in lake sediment samples a biased reflection of the communities from which they are derived? Journal of Paleolimnology 38: 157–181.CrossRefGoogle Scholar
  28. Keller, W., 2009. Limnology in northeastern Ontario: from acidification to multiple stressors. Canadian Journal of Fisheries and Aquatic Sciences 66: 1189–1198.CrossRefGoogle Scholar
  29. Keller, W. & J. R. Pitblado, 1989. The distribution of crustacean zooplankton in Northern Ontario. Canadian Journal of Biogeography 16: 249–259.CrossRefGoogle Scholar
  30. Keller, W. & M. Conlon, 1994. Crustacean zooplankton communities and lake morphometry in Precambrian Shield lakes. Canadian Journal of Fisheries and Aquatic Sciences 51: 2424–2434.CrossRefGoogle Scholar
  31. Keller, W., J. M. Gunn & N. D. Yan, 1999. Acid rain – perspectives on lake recovery. Journal of Aquatic Ecosystem Stress and Recovery 6: 2107–2216.Google Scholar
  32. Keller, W., N. D. Yan, K. M. Somers & J. H. Heneberry, 2002. Crustacean zooplankton communities in lakes recovering from acidification. Canadian Journal of Fisheries and Aquatic Sciences 59: 726–735.CrossRefGoogle Scholar
  33. Kim, N., B. Walseng & N. D. Yan, 2012. Will environmental calcium declines in Canadian Shield lakes help or hinder Bythotrephes establishment success? Canadian Journal of Fisheries and Aquatic Sciences 69: 810–820.CrossRefGoogle Scholar
  34. Korhola, A. & M. Rautio, 2001. Cladocera and other branchiopod crustaceans. In Smol, J. P., H. J. B. Birks & W. M. Last (eds), Tracking Environmental Change Using Lake Sediments. Volume 4: Zoological Indicators. Kluwer Academic Publishers, Dordrecht, The Netherlands: 4–41.Google Scholar
  35. Korosi, J. B. & J. P. Smol, 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. Journal of Paleolimnology 48: 571–586.CrossRefGoogle Scholar
  36. Korosi, J. B. & J. P. Smol, 2012b. An illustrated guide to the identification of cladoceran subfossils from lake sediments in northeastern North America: part 2 – the Chydoridae. Journal of Paleolimnology 48: 587–622.CrossRefGoogle Scholar
  37. Korosi, J. B., A. Jeziorski & J. P. Smol, 2011. Using morphological characters of subfossil daphniid postabdominal claws to improve taxonomic resolution within species complexes. Hydrobiologia 676: 117–128.CrossRefGoogle Scholar
  38. Kurek, J., J. B. Korosi, A. Jeziorski & J. P. Smol, 2010. Establishing reliable minimum count sizes for cladoceran subfossils sampled from lake sediments. Journal of Paleolimnology 44: 603–612.CrossRefGoogle Scholar
  39. Lundstedt, L. & M. T. Brett, 1991. Differential growth rates of three cladoceran species in response to mono- and mixed-algal cultures. Limnology and Oceanography 36: 159–165.CrossRefGoogle Scholar
  40. Malley, D. F. & P. S. S. Chang, 1986. Increase in the abundance of cladocera at pH 5.1 in experimentally-acidified lake 223, Experimental Lakes Area, Ontario. Water Air Soil Pollution 30: 629–638.CrossRefGoogle Scholar
  41. McQueen, D. J. & N. D. Yan, 1993. Metering filtration efficiency of freshwater zooplankton hauls: reminders from the past. Journal of Plankton Research 15: 57–65.CrossRefGoogle Scholar
  42. Michelutti, N., J. M. Blais, B. F. Cumming, A. M. Paterson, K. Rühland, A. P. Wolfe & J. P. Smol, 2010. Do spectrally-inferred determinations of chlorophyll a reflect trends in lake trophic status? Journal of Paleolimnology 43: 205–217.CrossRefGoogle Scholar
  43. Monteith, D. T., J. L. Stoddard, C. D. Evans, H. A. de Wit, M. Forsius, T. Høgåsen, A. Wilander, B. L. Skjelkvåle, D. S. Jeffries, J. Vuorenmaa, B. Keller, J. Kopácek & J. Vesely, 2007. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450: 537–540.CrossRefPubMedGoogle Scholar
  44. Molot, L. A. & P. J. Dillon, 2008. Long-term trends in catchment export and lake concentrations of base cations in the Dorset study area, central Ontario. Canadian Journal of Fisheries and Aquatic Sciences 65: 809–820.CrossRefGoogle Scholar
  45. Neary, B. P. & P. J. Dillon, 1988. Effects of sulphur deposition on lake-water chemistry in Ontario, Canada. Nature 333: 340–343.CrossRefGoogle Scholar
  46. Norberg, M., C. Bigler & I. Renberg, 2008. Monitoring compared with paleolimnology: implications for definition of reference condition in limed lakes in Sweden. Environmental Monitoring and Assessment 146: 295–308.CrossRefPubMedGoogle Scholar
  47. Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Michin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, & H. Wagner, 2014. vegan: Community Ecology Package. R package version 2.2-0. http://CRAN.R-project.org/package=vegan.
  48. Paterson, A. M., J. G. Winter, K. H. Nicholls, B. J. Clark, C. W. Ramcharan, N. D. Yan & K. M. Somers, 2008. Long-term changes in phytoplankton composition in seven Canadian Shield lakes in response to multiple anthropogenic stressors. Canadian Journal of Fisheries and Aquatic Sciences 65: 846–861.CrossRefGoogle Scholar
  49. Persaud, A. D., P. J. Dillon, D. Lasenby & N. D. Yan, 2009. Stable isotope variability of meso-zooplankton along a gradient of dissolved organic carbon. Freshwater Biology 54: 1705–1719.CrossRefGoogle Scholar
  50. Pichlová-Ptáčníková, R. & H. A. Vanderploeg, 2011. The quick and the dead: might differences in escape rates explain the changes in the zooplankton community composition of Lake Michigan after invasion by Bythotrephes? Biological Invasions 13: 2595–2604.CrossRefGoogle Scholar
  51. Prater, C., N. D. Wagner & P. C. Frost, 2016. Effects of calcium and phosphorus limitation on the nutritional ecophysiology of Daphnia. Limnology and Oceanography 61: 268–278.CrossRefGoogle Scholar
  52. R Development Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/.
  53. Riessen, H. P., R. D. Linley, I. Altshuler, M. Rabus, T. Sollradl, H. Clausen-Schaumann, C. Laforsch & N. D. Yan, 2012. Changes in water chemistry can disable plankton prey defences. Proceedings of the National Academy of Science USA 109: 15377–15382.CrossRefGoogle Scholar
  54. Rowe, C. L., S. J. Adamowicz & P. D. N. Hebert, 2007. Three new cryptic species of the freshwater zooplankton genus Holopedium (Crustacea: Branchiopoda: Ctenopoda), revealed by genetic methods. Zootaxa 1656: 1–49.Google Scholar
  55. Rusak, J. A. & P. K. Montz, 2009. Sampling requirements and the implications of reduced sampling effort for the estimation of annual zooplankton population and community dynamics in north temperate lakes. Limnology and Oceanography Methods 7: 535–544.CrossRefGoogle Scholar
  56. Schindler, D. W., P. J. Curtis, S. E. Bayley, B. R. Parker, K. G. Beaty & M. P. Stainton, 1997. Climate-induced changes in the dissolved organic carbon budgets of boreal lakes. Biogeochemistry 36: 9–28.CrossRefGoogle Scholar
  57. Shapiera, M., A. Jeziorski, N. D. Yan & J. P. Smol, 2011. Calcium content of littoral Cladocera in three softwater lakes of the Canadian Shield. Hydrobiologia 678: 77–83.CrossRefGoogle Scholar
  58. Shapiera, M., A. Jeziorski, A. M. Paterson & J. P. Smol, 2012. Cladoceran response to calcium decline and the subsequent inadvertent liming of a softwater Canadian lake. Water Air Soil Pollution 223: 2437–2446.CrossRefGoogle Scholar
  59. Smirnov, N. N., 1996. Cladocera: the Chydorinae and Sayciinae (Chydoridae) of the world. In Dumont, H. J. (ed.), Guide to the identification of the microinvertebrates of the continental waters of the world. SPB Academy Publishing, Amsterdam.Google Scholar
  60. Stoddard, J. L., D. S. Jeffries, A. Lukewille, T. A. Clair, P. J. Dillon, C. T. Driscoll, M. Forsius, M. Johnannessen, J. S. Kahl, J. H. Kellogg, A. Kemp, J. Mannio, D. T. Monteith, P. S. Murdoch, S. Patrick, A. Rebsdorf, B. L. Skjelkvale, M. P. Stainton, T. Traaen, H. van Dam, K. E. Webster, J. Wieting & A. Wilander, 1999. Regional trends in aquatic recovery from lake acidification in North America and Europe. Nature 401: 575–578.CrossRefGoogle Scholar
  61. Sweetman, J. N. & J. P. Smol, 2006. A guide to the identification of cladoceran remains (Crustacea: Branchiopoda) in Alaskan lake sediments. Archiv für Hydrobiologie (Supplement) 151: 353–394.Google Scholar
  62. Szeroczyńska, K. & K. Sarmaja-Korjonen, 2007. Atlas of Subfossil Cladocera from Central and Northern Europe. Friends of the Lower Vistula Society, Swiecie.Google Scholar
  63. Tan, Q. & W. Wang, 2010. Interspecific differences in calcium content and requirement in four freshwater cladocerans explained by biokinetic parameters. Limnology and Oceanography 55: 1426–1434.CrossRefGoogle Scholar
  64. Urabe, J., 1991. Effect of food concentration on growth, reproduction and survivorship of Bosmina longirostris (Cladocera): an experimental study. Freshwater Biology 25: 1–8.CrossRefGoogle Scholar
  65. Vinyard, G. L. & R. A. Menger, 1980. Chaoborus americanus predation on various zooplankters; functional response and behavioral observations. Oecologia 45: 90–93.CrossRefGoogle Scholar
  66. Waervågen, S. B., N. A. Rukke & D. O. Hessen, 2002. Calcium content of crustacean zooplankton and its potential role in species distribution. Freshwater Biology 47: 1866–1878.CrossRefGoogle Scholar
  67. Yan, N. D., K. M. Somers, R. E. Girard, A. M. Paterson, B. Keller, C. W. Ramcharan, J. A. Rusak, R. Ingram, G. E. Morgan & J. Gunn, 2008. Long-term trends in zooplankton of Dorset, Ontario lakes: the probable interactive effects of changes in pH, TP, DOC and predators. Canadian Journal of Fisheries and Aquatic Sciences 65: 862–877.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Laura E. Redmond
    • 1
  • Adam Jeziorski
    • 1
  • Andrew M. Paterson
    • 2
  • James A. Rusak
    • 2
  • John P. Smol
    • 1
  1. 1.Paleoecological Environmental Assessment and Research Laboratory, Department of BiologyQueen’s UniversityKingstonCanada
  2. 2.Dorset Environmental Science CentreOntario Ministry of the Environment and Climate ChangeDorsetCanada

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