Hydrobiologia

, Volume 785, Issue 1, pp 307–325 | Cite as

The effects of Bythotrephes longimanus and calcium decline on crustacean zooplankton communities in Canadian Shield lakes

Primary Research Paper

Abstract

Declining calcium concentrations and invasion by Bythotrephes longimanus are two important, often co-occurring, stressors affecting Canadian Shield lakes. However, there has been no experimental examination of how they might jointly influence zooplankton communities. We conducted a 6-week field mesocosm experiment in Havelock Lake, Haliburton, Ontario, Canada to examine the individual and joint effects of Bythotrephes and calcium along a gradient ranging from 1.2 to 2.6 mg/l on zooplankton communities. Although densities of Bythotrephes in our study are unknown, it significantly reduced total zooplankton abundance in invaded compared to uninvaded treatments by 46%, with the greatest impacts on small cladocerans and daphniids. Low calcium reduced total zooplankton and cladoceran abundances. Although Havelock Lake has the lowest calcium concentration among invaded lakes in the Muskoka–Haliburton region (1.2 mg Ca/l), an effect of calcium on individual species abundances was not detected. Additionally, we did not detect an interactive effect of both stressors. Our results suggest that lake calcium concentration may not yet be low enough to effect a strong response. However, as Bythotrephes continue to invade low calcium lakes, and as calcium concentrations further decline, we may see larger impacts on cladocerans as calcium thresholds for reproduction and growth are reached.

Keywords

Hardness Base cation Crustacea Invasive species Boreal lakes Multiple stressors 

Supplementary material

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Supplementary material 1 (DOCX 58 kb) Fig. S1 Plot showing distribution of invaded (grey-filled) and uninvaded treatments along our calcium gradient that ranged from 1.2 to 2.6 mg/L
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Supplementary material 2 (DOCX 1458 kb) Fig. S2 Plots of linear regression models for calcium through time for select species and functional groups (n = 30 enclosures). Significance of regression line is categorised as: *, 0.01 < P<0.05; **, P < 0.001
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Supplementary material 3 (DOCX 14 kb)
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Supplementary material 8 (DOCX 20 kb)

References

  1. Anderson, D. R., 2008. Model Based Inference in the Life Sciences: A Primer on Evidence. Springer, New York.CrossRefGoogle Scholar
  2. Ashforth, D. & N. D. Yan, 2008. The interactive and effects of calcium concentration and temperature on the survival of Daphnia pulex at high and low food concentrations reproduction. Limnology and Oceanography 53: 420–432.CrossRefGoogle Scholar
  3. Azan, S. S. E., S. E. Arnott & N. D. Yan, 2015. A review of the effects of Bythotrephes longimanus and calcium decline on zooplankton communities—can interactive effects be predicted? Environmental Reviews 23: 395–413.CrossRefGoogle Scholar
  4. Barbiero, R. P. & M. L. Tuchman, 2004. Changes in the crustacean communities of Lakes Michigan, Huron, and Erie following the invasion of the predatory cladoceran Bythotrephes longimanus. Canadian Journal of Fisheries and Aquatic Sciences 61: 2111–2125.CrossRefGoogle Scholar
  5. Bartoń, K. 2013. MuMIn: Multi-model inference. R package version 1.9.13 [available on internet at http://cran.r-project.org/web/packages/MuMIn/index.html from August 21, 2015].
  6. Bates, D., M. Maechler, B. Bolker, S. Walker, R. H. B. Christensen & H. Singmann, 2014. lme4: Linear mixed-effects model using Eigen and S4. R package version 1.1-5 [available on internet at http://cran.r-project.org/web/packages/lme4/index.html from August 21, 2015].
  7. Boudreau, S. & N. D. Yan, 2003. The differing crustacean zooplankton communities of Canadian Shield lakes with and without the nonindigenous zooplanktivore Bythotrephes longimanus. Canadian Journal of Fisheries and Aquatic Sciences 60: 1307–1313.CrossRefGoogle Scholar
  8. Bourdeau, P. E., K. L. Pangle & S. D. Peacor, 2011. The invasive predator Bythotrephes induces vertical migration in native copepods of Lake Michigan. Biological Invasions 13: 2533–2545.CrossRefGoogle Scholar
  9. Bourdeau, P. E., K. L. Pangle, E. M. Reed & S. D. Peacor, 2013. Finely tuned response of native prey to an invasive predator in a freshwater system. Ecology 94: 1449–1455.CrossRefPubMedGoogle Scholar
  10. Bungartz, B. & D. K. Branstrator, 2003. Morphological changes in Daphnia mendotae in the chemical presence of Bythotrephes longimanus. Archiv füer Hydrobiologie 158: 97–108.CrossRefGoogle Scholar
  11. Burnham, K. P. & D. R. Anderson, 2002. Model Selection and Multi-model Inference: A Practical Information Theoretical Approach. Springer, New York.Google Scholar
  12. Burnham, K. P., D. R. Anderson & K. P. Huyvaert, 2011. AIC model selection and multi-model inference in behavioural ecology: some background, observations, and comparisons. Behavioural Ecology and Sociobiology 65: 23–35.CrossRefGoogle Scholar
  13. Breitburg, D. L., J. W. Baxter, C. A. Hatfield, R. W. Howarth, C. G. Jones, G. M. Lovett & C. Wigand, 1998. Understanding effects of multiple stressors: ideas and challenges. In Pace, M. L. & P. M. Groffman (eds.), Successes, Limitations, and Frontiers in Ecosystem Science. Springer Science, LLC, New York: 416–431.CrossRefGoogle Scholar
  14. Cairns, A. 2010. Field assessments and evidence of impact of calcium decline on Daphnia (Crustacea, Anomopoda) in Canadian Shield lakes. MSc. Thesis, Department of Biology, York University, Toronto, Ontario, Canada.Google Scholar
  15. Cairns, A. & N. D. Yan, 2011. 135 lake survey: new reports of Bythotrephes, summary of methodology, and database design. Canadian Aquatic Invading Species Network Technical Report (CAISN) Project I.V Technical Report #3, Dorset Environmental Science Centre, Dorset, Ontario, Canada.Google Scholar
  16. Culp, J. M., C. L. Podemski, K. J. Cash & R. B. Lowell, 2000. A research strategy for using stream microcosms in ecotoxicology: integrating experiments at different levels of biological organization with field data. Journal of Aquatic Ecosystem Stress and Recovery 7: 167–176.CrossRefGoogle Scholar
  17. DeSellas, A. M., A. M. Paterson, J. N. Sweetman & J. P. Smol, 2008. Cladocera assemblages from the surface sediments of south-central Ontario (Canada) lakes and their relationships to measured environmental variables. Hydrobiologia 600: 105–119.CrossRefGoogle Scholar
  18. DeSellas, A. M., A. M. Paterson, J. N. Sweetman & J. P. Smol, 2011. Assessing the effects of multiple environmental stressors on zooplankton assemblages in Boreal Shield lakes since pre-industrial times. Journal of Limnology 70: 41–56.CrossRefGoogle Scholar
  19. Early Detection and Distribution Mapping System (EDDMaps) Ontario. 2015 Bythotrephes longimanus, Leydig, 1860, distribution map [available on internet at http://www.eddmaps.org/ontario/distribution/viewmap.cfm?sub=59823 from May 19, 2015].
  20. Ebert, D. 2005. Ecology, epidemiology, and evolution of parasitism in Daphnia. Bathesda, Maryland, USA: National Centre for Biotechnology Information [available on internet at http://www.ncbi.nlm.nih.gov/books/NBK2036/ from December 14, 2015].
  21. Elser, J. J., W. F. Fagan, R. F. Denno, D. R. Dobberfuhl, A. Folarin, A. Huberty, S. Interlandi, S. S. Kilham, E. McCauley, K. L. Schulz, E. H. Siemann & R. W. Sterner, 2000. Nutritional constraints in terrestrial and freshwater food webs. Nature 408: 578–580.CrossRefPubMedGoogle Scholar
  22. Fernandez, R. J., M. D. Rennie & W. G. Sprules, 2009. Changes in nearshore zooplankton associated with species invasions and potential effects on larval lake whitefish (Coregonus clupeaformis). International Review of Hydrobiology 94: 226–243.CrossRefGoogle Scholar
  23. Fleminger, A. & R. I. Clutter, 1965. Avoidance of towed nets by zooplankton. Limnology and Oceanography 10: 96–104.CrossRefGoogle Scholar
  24. Folt, C. L., C. Y. Chen, M. V. Moore & J. Burnaford, 1999. Synergism and antagonism among multiple stressors. Limnology and Oceanography 44: 864–877.CrossRefGoogle Scholar
  25. Frost, T. M., D. L. DeAngelis, S. M. Bartell, D. J. Hall & S. H. Hurlbert, 1988. Scale in the design and interpretation of aquatic community research. In Carpenter, S. R. (ed.), Complex Interactions in Lake Communities. Springer, New York: 229–260.CrossRefGoogle Scholar
  26. Global Invasive Species Database, 2005. Bythotrephes longimanus [available on internet at http://www.issg.org/database/species/distribution_display.asp?si=151&ri=18873&pc=*&sts=sss&status=Alien&lang=EN#Alien from February 26, 2016].
  27. Halpern, B. S., S. Walbridge, K. A. Selkoe, C. V. Kappel, F. Micheli, C. D’Agrosa, J. F. Bruno, K. S. Casey, C. Ebert, H. E. Fox, R. Fujita, D. Heinemann, H. S. Lenihan, E. M. P. Madin, M. T. Perry, E. R. Selig, M. Spalding, R. Steneck & Reg Watson, 2008. A global map of human impact on marine ecosystems. Science 319: 948–952.CrossRefPubMedGoogle Scholar
  28. Havens, K. E., N. D. Yan, W. Keller & W., 1993. Lake acidification: effects on crustacean zooplankton populations. Environmental Science and Technology 27: 1621–1624.CrossRefGoogle Scholar
  29. Hedin, L. O., L. Granat, G. E. Likens, T. A. Buishand, J. N. Galloway, T. J. Butler & H. Rodhe, 1994. Steep declines in atmospheric base cations in regions of Europe and North America. Nature 367: 351–354.CrossRefGoogle Scholar
  30. Hessen D. O. 1992. Nutrient element limitation of zooplankton production. American Naturalist: 799–814.Google Scholar
  31. 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
  32. Hessen, D. O., N. E. Alstad & L. Skardal, 2000. Calcium limitation in Daphnia magna. Journal of Plankton Research 22: 553–568.CrossRefGoogle Scholar
  33. Hooper, D. U., F. S. Chapin III, J. J. Ewel, A. Hector, P. Inchausti, S. Lavorel, J. H. Lawton, D. M. Lodge, M. Loreau, S. Naeem, B. Schmid, H. Setälä, A. J. Symstad, J. Vandermeer & D. A. Wardle, 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75: 3–35.CrossRefGoogle Scholar
  34. 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
  35. 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
  36. Jeziorski, A., A. M. Paterson & J. P. Smol, 2012. Crustacean zooplankton sedimentary remains from calcium-poor lakes: complex responses to threshold concentrations. Aquatic Sciences 74: 121–131.CrossRefGoogle Scholar
  37. 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
  38. Jokela, A. 2013. Factors mediating the distribution and impact of the non-native invertebrate predator Bythotrephes longimanus. PhD. Thesis, Department of Biology, Queen’s University, Kingston, Ontario, Canada.Google Scholar
  39. Keller, W., S. S. Dixit & J. Heneberry, 2001. Calcium declines in northeastern Ontario lakes. Canadian Journal of Fisheries and Aquatic Sciences 58: 2011–2020.CrossRefGoogle Scholar
  40. Kim, N., B. Walseng & N. D. Yan, 2012. Will environmental calcium declines hinder Bythotrephes establishment success in Canadian Shield lakes? Canadian Journal of Fisheries and Aquatic Sciences 69: 810–820.CrossRefGoogle Scholar
  41. Korosi, J. B. & J. P. Smol, 2012. A comparison of present-day and pre-industrial cladoceran assemblages from soft water Nova Scotia (Canada) lakes with different regional acidification histories. Journal of Paleolimnology 47: 43–54.CrossRefGoogle Scholar
  42. Kuznetsova, A., P. B. Brockhoff & R. H. B. Christensen, 2012. lmerTest: Tests in linear mixed effects models. R package version 2.0-6 [available on internet at http://cran.r-project.org/web/packages/lmerTest/index.html from August 21, 2015]
  43. Lehman, J. T., 1988. Algal biomass unaltered by food web changes in Lake Michigan. Nature 32: 537–538.CrossRefGoogle Scholar
  44. Ministry of Environment and Climate Change (MOECC). 2015. The determination of cations in water and precipitation by atomic absorption spectrophotometry (AAS) version 5.0. Catalogue code: DoFLAME-E3249.Google Scholar
  45. 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
  46. Paine, R., M. J. Tegner & E. A. Johnson, 1998. Compounded perturbations yield ecological surprises. Ecosystems 1: 535–545.CrossRefGoogle Scholar
  47. Pangle, K. L. & S. D. Peacor, 2006. Non-lethal effect of the invasive predator Bythotrephes longimanus on Daphnia mendotae. Freshwater Biology 51: 1070–1078.CrossRefGoogle Scholar
  48. Pangle, K. L., S. D. Peacor & O. E. Johannsson, 2007. Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88: 402–412.CrossRefPubMedGoogle Scholar
  49. 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
  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 & C. P. Frost, 2015. Effects to calcium and phosphorus limitation on the nutritional ecophysiology of Daphnia. Limnology and Oceanography 16: 268–278.Google Scholar
  52. R Development Core Team. 2014. R: A language and environment for statistical computing, Version 3.1.2. R Foundation for Statistical Computing, Vienna.Google Scholar
  53. Reid, C. & S. A. Watmough, 2016. Spatial patterns, trends, and the potential long-term impacts of tree harvesting on lake calcium levels in the Muskoka River Watershed, Ontario, Canada. Canadian Journal of Fisheries and Aquatic Sciences 73: 1–12.CrossRefGoogle Scholar
  54. Riessen, H. P., R. D. Linley, I. Altshuler, M. Rabus, T. Söllradl, H. Clausen-Schaumann, C. Laforsch & N. D. Yan, 2012. Changes in water chemistry can disable plankton prey defences. Proceedings of the National Academy of Sciences of the United States of America 109: 15377–15382.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Ross, A. 2015. Assessing the role of declining calcium in biological recovery on zooplankton in historically acidified lakes. MSc. Thesis, Department of Biology, Queen’s University, Kingston, Ontario, Canada.Google Scholar
  56. Rukke, N. E. W. 2002. Tolerance to low ambient calcium shows inter-population differences in Daphnia galeata. Journal of Plankton Research 24: 527–531.CrossRefGoogle Scholar
  57. Sala, O. E., F. S. Chapin III, J. J. Armesto, E. Berlow, J. Bloomfield, R. Dirzo, E. Huber-Sanwald, L. F. Huenneke, R. B. Jackson, A. Kinzig, R. Leemans, D. M. Lodge, H. A. Mooney, M. Oesterheld, N. L. Poff, M. T. Sykes, B. H. Walker, M. Walker & D. H. Wall, 2000. Global biodiversity scenarios for the year 2100. Science 287: 1770–1774.CrossRefPubMedGoogle Scholar
  58. Schindler, D. W., 1998. Replication versus realism: the need for ecosystem-scale experiments. Ecosystems 1: 323–334.CrossRefGoogle Scholar
  59. Shapiera, M., A. Jeziorski, N. D. Yan & J. P. Smol, 2011. Calcium content of littoral Cladocera in three soft water lakes of the Canadian Shield. Hydrobiologia 678: 77–83.CrossRefGoogle Scholar
  60. Skaug, H., D. Fournier, A. Nielsen, A. Magnusson & B. Bolker, 2013. glmmadmb. R package version 0.7.7 [available on internet at http://glmmadmb.r-forge.r-project.org/ from August 21, 2015].
  61. Sterner, R. W. & D. O. Hessen, 1994. Algal nutrient limitation and the nutrition of aquatic herbivores. Annual Review of Ecology and Systematics 25: 1–29.CrossRefGoogle Scholar
  62. Strecker, A. L. & S. E. Arnott, 2005. Impact of Bythotrephes invasion on zooplankton communities in acid-damaged and recovered on the Boreal Shield. Canadian Journal of Fisheries and Aquatic Sciences 62: 2450–2462.CrossRefGoogle Scholar
  63. Strecker, A. L., S. E. Arnott, N. D. Yan & R. Girard, 2006. Variation in the response of crustacean zooplankton species richness and composition to the invasive predator Bythotrephes. Canadian Journal of Fisheries and Aquatic Sciences 63: 2126–2136.CrossRefGoogle Scholar
  64. Strecker, A. L. & S. E. Arnott, 2008. Invasive predator, Bythotrephes, has varied effects on ecosystem function in freshwater lakes. Ecosystems 11: 490–503.CrossRefGoogle Scholar
  65. Strecker, A. L. & S. E. Arnott, 2010. Complex interactions between regional dispersal of native taxa and an invasive species. Ecology 91: 1035–1047.CrossRefPubMedGoogle Scholar
  66. Stoddard, J. L., D. S. Jeffries, A. Lükewille, T. A. Clair, P. J. Dillon, C. T. Driscoll, M. Forsius, M. Johannessen. J. S. Kahl, J. H. Kellogg, A. Kemp, J. Mannio, D. T. Monteith, P. S. Murdoch, S. Patrick, A. Rebsdorf, B. L. Skjelkvåle, M. P. Stainton, T. Traaen, H. van Dam, K. E. Webster, J. Wieting & A. Wilander, 1999. Regional trends in aquatic recovery from acidification in North America and Europe. Nature 401: 575–578.CrossRefGoogle Scholar
  67. Tan, Q. & W. Wang, 2010. Interspecies differences in calcium content and requirement in four freshwater cladocerans explained by biokinetic parameters. Limnology and Oceanography 55: 1426–1434.CrossRefGoogle Scholar
  68. Tessier, A. J. & R. J. Horwitz, 1990. Influence of water chemistry on size structure of zooplankton assemblages. Canadian Journal of Fisheries and Aquatic Sciences 47: 1937–1943.CrossRefGoogle Scholar
  69. Vanderploeg, H. A., J. R. Liebig & M. Omair, 1993. Bythotrephes predation on Great Lakes zooplankton measured by an in situ method implication for zooplankton community structure. Archiv füer Hydrobiologie 127: 1–8.Google Scholar
  70. Vinebrooke, R. D., K. L. Cottingham, J. Norberg, M. Scheffer, S. I. Dodson, S. C. Maberly & U. Sommer, 2004. Impacts of multiple stressors on biodiversity and ecosystem functioning: the role of species co-tolerance. Oikos 104: 451–457.CrossRefGoogle Scholar
  71. Wærvågen, S. B., N. E. W. Rukke & D. O. Hessen, 2002. Calcium content of crustacean zooplankton and its potential role in species distribution. Freshwater Biology 47: 1866–1878.CrossRefGoogle Scholar
  72. Wahlström, E. & E. Westman, 1999. Planktivory by the predacious cladoceran Bythotrephes longimanus: effects on zooplankton size structure and abundance. Canadian Journal of Fisheries and Aquatic Sciences 56: 1865–1872.CrossRefGoogle Scholar
  73. Walsh, J. R., S. R. Carpenter & M. J. Vander Zanden, 2016. Invasive triggers a massive loss of ecosystem services through a trophic cascade. Proceedings of the National Academy of the United States of America 113: 4081–4085.CrossRefGoogle Scholar
  74. Watmough, S. A. & J. Aherne, 2008. Estimating calcium weathering rates and future lake calcium concentrations in the Muskoka–Haliburton region of Ontario. Canadian Journal of Fisheries and Aquatic Sciences 65: 821–833.CrossRefGoogle Scholar
  75. Watmough, S. A., J. Aherne & P. J. Dillon, 2003. Potential impact of forest harvesting on lake chemistry in south-central Ontario at current levels of acid deposition. Canadian Journal of Fisheries and Aquatic Sciences 60: 1095–1103.CrossRefGoogle Scholar
  76. Weisz, E. J. & N. D. Yan, 2010. Relative value of limnological, geographic and human use variables as predictors of the presence of Bythotrephes longimanus in Canadian Shield lakes. Canadian Journal of Fisheries and Aquatic Sciences 67: 462–472.CrossRefGoogle Scholar
  77. Welschmeyer, N. A., 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and phaeopigments. Limnology and Oceanography 39: 1985–1992.CrossRefGoogle Scholar
  78. Yan, N. D. & T. W. Pawson, 1997. Changes in the crustacean zooplankton community of Harp Lake, Canada, following the invasion by Bythotrephes cederstroemi. Freshwater Biology 37: 409–425.CrossRefGoogle Scholar
  79. Yan, N. D., G. L. Mackie & D. Boomer, 1989. Seasonal patterns in metal levels of the net plankton of three Canadian Shield lakes. The Science of the Total Environment 87(88): 439–461.CrossRefGoogle Scholar
  80. Yan, N. D., A. Blukacz, W. G. Sprules, P. K. Kindy, D. Hackett, R. E. Girard & B. J. Clark, 2001. Changes in the zooplankton and the phenology of the spiny water flea, Bythotrephes, following its invasion of Harp Lake, Ontario, Canada. Canadian Journal of Fisheries and Aquatic Sciences 58: 2341–2350.CrossRefGoogle Scholar
  81. Yan, N. D., R. Girard & S. Boudreau, 2002. An introduced predator (Bythotrephes) reduces zooplankton species richness. Ecology Letters 5: 481–485.CrossRefGoogle Scholar
  82. Yan, N. D., K. M. Somers, R. E. Girard, A. M. Paterson, W. Keller, C. W. Ramcharan, J. A. Rusak, R. Ingram, G. E. Morgan & J. M. Gunn, 2008a. Long-term trends in zooplankton of Dorset, Ontario lakes: the probable interactive effects of changes in pH, total phosphorus, dissolved organic carbon, and predators. Canadian Journal of Fisheries and Aquatic Sciences 65: 862–877.CrossRefGoogle Scholar
  83. Yan, N. D., A. M. Paterson, K. M. Somers & W. A. Scheider, 2008b. An introduction to the Dorset special issue: transforming understanding of factors that regulate aquatic ecosystems on the southern Canadian Shield. Canadian Journal of Fisheries and Aquatic Sciences 65: 781–785.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of BiologyQueen’s UniversityKingstonCanada

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