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Anti-predator behaviour of native prey (Daphnia) to an invasive predator (Bythotrephes longimanus) is influenced by predator density and water clarity

  • Sarah S. HasnainEmail author
  • Shelley E. Arnott
Primary Research Paper

Abstract

Bythotrephes longimanus is an invasive zooplankton predator, negatively impacting zooplankton abundance and diversity in North American lakes. Previous studies have shown that Daphnia populations in lakes move to deeper waters during the day, in the presence of Bythotrephes, a visual predator occupying well-lit regions. However, Daphnia vertical position can be influenced by a variety of biotic and abiotic factors. We conducted a survey to determine (1) if Daphnia daytime vertical position differed between invaded and uninvaded lakes and (2) if Daphnia vertical position in invaded lakes was affected by water chemistry variables linked to water clarity, UV exposure, and phytoplankton production, and Bythotrephes density. Invaded lakes had a lower proportion of epilimnetic Daphnia as compared to uninvaded lakes. Daphnia vertical position was species-dependent, and with a lower proportion of epilimnetic Daphnia mendotae and greater proportion of epilimnetic D. longiremis observed in invaded lakes. D. mendotae were deeper in the water column in high Bythotrephes density lakes with low dissolved organic carbon levels. Our results show Daphnia vertical position response to Bythotrephes is species specific, dependent on Bythotrephes density and influenced by local abiotic conditions, with important implications for community structure and ecosystem function in invaded lakes.

Keywords

Freshwater zooplankton Vertical migration Light availability Non-native Vertical distribution Dissolved organic carbon Daphnia mendotae 

Notes

Acknowledgements

Funding for this project was provided by the Canadian Aquatic Invasive Species Network (CAISN) II and an Ontario Graduate Scholarship. Support was also provided through the Queen’s University Summer Work Experience Program (SWEP). We thank the Dorset Environmental Science Centre (DESC) and its staff, especially James Rusak, Ron Ingram and Tim Field for providing logistical support during field sampling. We thank Norman Yan for providing access to physical, water chemistry data from the CAISN field surveys and P. Anderson and S. Azan for their field assistance. Finally, we thank the anonymous reviewers whose comments greatly improved our manuscript.

Supplementary material

10750_2019_3983_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 20 kb)

References

  1. Banks, P. B. & C. R. Dickman, 2007. Alien predation and the effects of multiple levels of prey naiveté. Trends in Ecology & Evolution 22: 229–230.CrossRefGoogle Scholar
  2. Beeton, A. M. & J. A. Bowers, 1982. Vertical migration of Mysis relicta Loven. Hydrobiologia 93: 53–61.CrossRefGoogle Scholar
  3. Benfield, M. C. & T. J. Minello, 1996. Relative effects of turbidity and light intensity on reactive distance and feeding of estuarine fish. Environmental Biology of Fishes 46: 126–211.CrossRefGoogle Scholar
  4. Blumstein, D. T., 2006. The multipredator hypothesis and the evolutionary persistence of antipredator behaviour. Ethology 112: 209–217.CrossRefGoogle Scholar
  5. Boeing, W. J., D. M. Leech & C. E. Williamson, 2004. Damaging UV radiation and invertebrate predation: conflicting selective pressures for zooplankton vertical distribution in the water column of low DOC lakes. Oecologia 138: 603–612.CrossRefPubMedGoogle Scholar
  6. Boeing, W. J., C. W. Ramcharan & H. P. Riessen, 2006. Clonal variation in depth distribution of Daphnia pulex in response to predator kairomones. Archiv fur Hydrobiologie 166: 241–260.CrossRefGoogle Scholar
  7. Boersma, M., P. Spaak & L. De Meester, 1998. Predator-mediated plasticity in morphology, life history, and behavior of Daphnia: the uncoupling of responses. American Naturalist 152: 237–248.PubMedGoogle Scholar
  8. Boudreau, S. A. & N. D. Yan, 2003. The differing crustacean zooplankton communities of Canadian Shield lakes with and without the non indigenous zooplanktivore Bythotrephes longimanus. Canadian Journal of Fisheries and Aquatic Sciences 60: 1307–1313.CrossRefGoogle Scholar
  9. Boudreau, S. A. & N. D. Yan, 2004. Auditing the accuracy of a volunteer based surveillance program for an aquatic invader, Bythotrephes. Environmental Monitoring and Assessment 91: 17–26.CrossRefPubMedGoogle Scholar
  10. Bourdeau, P. E., K. L. Pangle & S. D. Peacor, 2011. The invasive predator Bythotrephes induces changes in the vertical distribution of native copepods in Lake Michigan. Biological Invasions 13: 2533–2545.CrossRefGoogle Scholar
  11. 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
  12. Branstrator, D. K., M. E. Brown, L. J. Shannon, M. Thabes & K. Heimgartner, 2006. Range expansion of Bythotrephes longimanus in North America: evaluating habitat characteristics in the spread of an exotic zooplankter. Biological Invasions 8: 1367–1379.CrossRefGoogle Scholar
  13. Browman, H. L., S. Kruse & W. J. O’Brien, 1989. Foraging behavior of the predaceous cladoceran, Leptodora kindtii and escape responses of their prey. Journal of Plankton Research 11: 1078–1088.CrossRefGoogle Scholar
  14. Bruno, J. F., J. D. Fridley, K. D. Bromberg & M. D. Bertness, 2005. Insights into Biotic interactions from studies of species invasions. In Sax, D., J. Stachowicz & S. Gaines (eds), Insights into Ecology, Evolution, and Biogeography. Sinauer Associates, Sunderland: 13–40.Google Scholar
  15. Cairns, A. & N. D. Yan, 2011. CAISN Project I.V Technical Report #3. 135 Lake survey – new reports of Bythotrephes, summary of methodology and database design. CAISN Technical Report: 19 pp.Google Scholar
  16. Cairns, A., M. Elliott, N. D. Yan & E. Weisz, 2006. Operationalizing CAISN project 1.V, Technical Report No. 1: lake selection. Dorset Environmental Research Centre, Dorset: 51 pp.Google Scholar
  17. Cairns, A., N. D. Yan, E. Weisz, J. Petruniak & J. Hoare, 2007. Operationalizing CAISN Project 1.V, Technical Report No. 2: the large inland lake Bythotrephes survey – limnology, database design, and presence of Bythotrephes in 311 south-central Ontario lakes. Dorset Environmental Science Centre, Dorset: 66 pp.Google Scholar
  18. Carthey, A. J. R. & P. B. Banks, 2014. Naïvete in novel ecological interactions: lessons from theory and experimental evidence. Biological Reviews 89: 932–949.CrossRefPubMedGoogle Scholar
  19. Černý, M. & P. D. N. Hebert, 1999. Intercontinental allozyme differentiation among four holarctic Daphnia species. Limnology and Oceanography 6: 1381–1387.CrossRefGoogle Scholar
  20. Chow-Fraser, P., D. O. Trew, D. Findlay & M. Stanton, 1994. A test of hypotheses to explain the sigmoidal relationship between total phosphorus and chlorophyll a concentrations in Canadian lakes. Canadian Journal of Fisheries and Aquatic Sciences 51: 2052–2056.CrossRefGoogle Scholar
  21. Cousyn, C., L. De Meester, J. K. Colbourne, L. Brendock, D. Verschuren & F. Volkaert, 2001. Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proceedings of the National academy of Sciences of the United States of America 98: 6256–6260.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Cox, G. W., 2004. Alien Species and Evolution. Island Press, Washington.Google Scholar
  23. Dawidowicz, P. & C. J. Loose, 1992. Metabolic costs during predator-induced diel vertical migration of Daphnia. Limnology and Oceanography 37: 1589–1595.CrossRefGoogle Scholar
  24. De Meester, L., 1996. Evolutionary potential and local genetic differentiation in a phenotypically plastic trait of a cyclical parthenogen, Daphnia magna. Evolution 50: 1293–1298.CrossRefPubMedGoogle Scholar
  25. De’ath, G. & K. E. Fabricius, 2000. Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81: 3178–3192.CrossRefGoogle Scholar
  26. Dillon, P. J. & F. H. Rigler, 1974. The phosphorus-chlorophyll relationship in lakes. Limnology and Oceanography 19: 767–773.CrossRefGoogle Scholar
  27. Dodson, S. I., 1988. The ecological role of chemical stimuli for the zooplankton: predator-avoidance behavior in Daphnia. Limnology and Oceanography 33: 1431–1439.Google Scholar
  28. EDDMapS, 2016, Early Detection and Distribution Mapping System. The University of Georgia – Center for Invasive Species and Ecosystem Health. Available online at http://www.eddmaps.org/; last accessed August 24, 2016.
  29. Elton, C. S., 1958. The Ecology of Invasions by Animals and Plants. University of Chicago Press, Chicago.CrossRefGoogle Scholar
  30. Fedorenko, A. Y., 1975. Feeding characteristics and predation impact of Chaoborus (Diptera, Chaoboridae) larvae in a small lake. Limnology and Oceanography 20: 250–258.CrossRefGoogle Scholar
  31. Field, K. M. & E. E. Prepas, 1997. Increased abundance and depth distribution of pelagic crustacean zooplankton during hypolimnetic oxygenation in a deep, eutrophic Alberta lake. Canadian Journal of Fisheries and Aquatic Sciences 54: 2146–2156.CrossRefGoogle Scholar
  32. Goldschmidt, T., F. Witte & J. Wanick, 1993. Cascading effects of the introduced Nile Perch on the detritivorous/phytoplanktivorous species in the sublittoral areas of Lake Victoria. Conservation Biology 7: 686–700.CrossRefGoogle Scholar
  33. Grad, G., C. E. Williamson & C. M. Karapelou, 2001. Zooplankton survival and reproduction responses to damaging UV radiation: a test of reciprocity and photoenzymatic repair. Limnology and Oceanography 4: 584–591.CrossRefGoogle Scholar
  34. Greene, C. H., 1983. Selective predation in freshwater zooplankton communities. Hydrobiologia 68: 297–315.Google Scholar
  35. Haney, J. F., M. A. Aliberti, E. Allan, S. Allard, D. J. Bauer, W. Beagen, S. R. Bradt, B. Carlson, S. C. Carlson, U. M. Doan, J. Dufresne, W. T. Godkin, S. Greene, A. Kaplan, E. Maroni, S. Melillo, A. L. Murby, J. L. Smith, B. Ortman, J. E. Quist, S. Reed, T. Rowin, M. Schmuck, R. S. Stemberger & B. Travers, 2013. An-Image-based Key to the Zooplankton of North America, version 5.0 released 2013. University of New Hampshire Center for Freshwater Biology. http://cfb.unh.edu.
  36. Hansson, L. A. & S. Hylander, 2009. Size-structured risk assessments govern Daphnia migration. Proceedings of the Royal Society of London (Biological Sciences) 276: 331–336.CrossRefGoogle Scholar
  37. Healey, M. C. & U. Reinhardt, 1995. Predator avoidance in naive and experienced juvenile Chinook and Coho salmon. Canadian Journal of Fisheries and Aquatic Sciences 52: 614–622.CrossRefGoogle Scholar
  38. Hothorn, T., K. Hornik & A. Zeileis, 2006. Unbiased recursive partitioning: a conditional inference framework. Journal of Computational and Graphical Statistics 15: 651–674.CrossRefGoogle Scholar
  39. Hoverman, J. T., J. R. Auld & R. A. Relyea, 2005. Putting prey back together again: integrating predator-induced behavior, morphology, and life history. Oecologia 144: 481–491.CrossRefPubMedGoogle Scholar
  40. Johnsen, G. H. & P. J. Jakobsen, 1987. The effect of food limitation on vertical migration in Daphnia longispina. Limnology and Oceanography 32: 873–880.CrossRefGoogle Scholar
  41. Jokela, A., S. E. Arnott & B. E. Beisner, 2011. Patterns of Bythotrephes longimanus distribution relative to native macroinvertebrates and zooplankton prey. Biological Invasions 13: 2573–2594.CrossRefGoogle Scholar
  42. Jokela, A., S. E. Arnott & B. E. Beisner, 2013. Influence of light on the foraging impact of an introduced predatory cladoceran, Bythotrephes longimanus. Freshwater Biology 58: 1946–1957.CrossRefGoogle Scholar
  43. Kasprzak, P. H., R. C. Lathrop & S. R. Carpenter, 1999. Influence of different sized Daphnia species on chlorophyll concentration and summer phytoplankton community structure in eutrophic Wisconsin lakes. Journal of Plankton Research 21: 2161–2174.CrossRefGoogle Scholar
  44. Kessler, K. & W. Lampert, 2004. Fitness optimization of Daphnia in a trade-off between food and temperature. Oecologia 140: 381–387.CrossRefPubMedGoogle Scholar
  45. Kessler, K., R. S. Lockwood, C. E. Williamson & J. E. Saros, 2008. Vertical distribution of zooplankton in subalpine and alpine lakes: ultraviolet radiation, fish predation, and the transparency-gradient hypothesis. Limnology and Oceanography 53: 2374–2382.CrossRefGoogle Scholar
  46. Knapp, R. A. & K. R. Matthews, 2000. Non native fish introductions and the decline of the Mountain Yellow-Legged Frog. Conservation Biology 14: 428–437.CrossRefGoogle Scholar
  47. Knapp, R. A., C. P. Hawkins, J. Ladau & J. G. McClory, 2005. Fauna of Yosemite National Park lakes has low resistance but high resilience to fish introductions. Ecological Applications 15: 835–847.CrossRefGoogle Scholar
  48. Laforsch, C., L. Beccara & R. Tollrian, 2006. Inducible defenses: the relevance of chemical alarm cues in Daphnia. Limnology and Oceanography 51: 1466–1472.CrossRefGoogle Scholar
  49. Larsson, P. & W. Lampert, 2012. Finding the optimal vertical distribution: behavioural responses of Daphnia pulicaria to gradients of environmental factors and the presence of fish. Freshwater Biology 57: 2514–2525.CrossRefGoogle Scholar
  50. Lehman, J. T. & C. E. Cáceres, 1993. Food-web responses to species invasion by a predatory invertebrate: Bythotrephes in Lake Michigan. Limnology and Oceanography 38: 879–891.CrossRefGoogle Scholar
  51. Lehman, J. T., D. M. Bilkovic & C. Sullivan, 1997. Predicting development, metabolism and secondary production of the invertebrate predator Bythotrephes. Freshwater Biology 38: 101–110.CrossRefGoogle Scholar
  52. Leibold, M. A., 1990. Resources and predators can affect the vertical distributions of zooplankton. Limnology and Oceanography 35: 938–944.CrossRefGoogle Scholar
  53. Leibold, M. A., 1991. Trophic interactions and habitat segregation between competing Daphnia species. Oecologia 86: 510–520.CrossRefPubMedGoogle Scholar
  54. Longhi, M. L. & B. E. Beisner, 2009. Environmental factors controlling the vertical distribution of phytoplankton in lakes. Journal of Plankton Research 31: 1195–1207.CrossRefGoogle Scholar
  55. Loose, C. J. & P. Dawidowicz, 1994. Trade-offs in diel vertical migration by zooplankton: the costs of predator avoidance. Ecology 75: 2255–2263.CrossRefGoogle Scholar
  56. Lynch, M., 1979. Predation, competition and zooplankton community structure: an experimental study. Limnology and Oceanography 24: 253–272.CrossRefGoogle Scholar
  57. MacIsaac, H. J., A. M. Ketelaars, I. A. Grigorovich, C. W. Ramcharan & N. D. Yan, 2000. Modeling Bythotrephes longimanus invasions in the Great Lakes basin based on its European distribution. Archiv fur Hydrobiologie 149: 1–21.CrossRefGoogle Scholar
  58. Mack, R., D. Simberloff, M. Lonsdale, H. Evans, M. Clout & F. A. Bazzaz, 2000. Biotic invasions: causes, epidemiology, global consequences and control. Ecological Applications 10: 689–710.CrossRefGoogle Scholar
  59. Mitchell, D. L. & D. Karentz, 1993. The induction and repair of DNA photodamage in the environment. In Young, A. R., L. O. Bjorn, J. Moan & W. Nultsch (eds), Environmental UV Photobiology. Plenum Press, New York: 345–377.CrossRefGoogle Scholar
  60. Morris, D. P., H. Zagarese & C. E. Williamson, 1995. The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnology and Oceanography 40: 1381–1391.CrossRefGoogle Scholar
  61. NASA Langley Atmospheric Science Data Center, 2016. Surface Meterology and Solar Energy: a renewable energy resource website (release 6.0). Accessed June 1, 2016, from http://power.larc.nasa.gov/cgi-bin/cgiwrap/solar/hirestimeser.cgi?.
  62. Nesbitt, L. M., H. P. Reissen & C. W. Ramcharan, 1996. Opposing predation pressures and induced vertical migration responses in Daphnia. Limnology and Oceanography 41: 1306–1311.CrossRefGoogle Scholar
  63. O’Brien, W. J., 1979. The predator–prey interaction of planktivorous fish and zooplankton. American Scientist 67: 572–581.Google Scholar
  64. Olden, J. D., J. J. Lawler & N. L. Poff, 2008. Machine learning methods without tears: a primer for ecologists. The Quarterly Review of Biology 83: 171–192.CrossRefPubMedGoogle Scholar
  65. 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
  66. Pangle, K. L. & S. D. Peacor, 2009. Light-dependent predation by the invertebrate planktivore Bythotrephes longimanus. Canadian Journal of Fisheries and Aquatic Sciences 66: 1748–1757.CrossRefGoogle Scholar
  67. Pangle, K. L., S. D. Peacor, O. E. Johannsson & E. Field, 2007. Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88: 402–412.CrossRefPubMedGoogle Scholar
  68. Pastorok, R. A., 1981. Prey vulnerabilities and size selection by Chaoborus larvae. Ecology 62: 1311–1324.CrossRefGoogle Scholar
  69. Pothoven, S. A., G. L. Fahnensteil & H. A. Vanderploeg, 2008. Population dynamics of Bythotrephes cederstroemii in south-east Lake Michigan 1995–1998. Freshwater Biology 46: 1491–1501.CrossRefGoogle Scholar
  70. Preisendorfer, R. W., 1986. Secchi disk science: visual optics of natural waters. Limnology and Oceanography 31: 909–926.CrossRefGoogle Scholar
  71. Ramcharan, C. W., N. D. Yan, D. J. McQueen, A. Perez-Fuentetaja, E. Demers & J. A. Rusak, 2001. Complex responses of Chaoborus to changes in fish populations. Archiv fur Hydrobiologie 56: 81–100.Google Scholar
  72. Rautio, M., A. Korhola & I. D. Zellmer, 2003. Vertical distribution of Daphnia longispina in a shallow subarctic pond: does the interaction of ultraviolet radiation and Chaoborus predation explain the pattern? Polar Biology 26: 659–665.CrossRefGoogle Scholar
  73. R Core Team, 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
  74. Reissen, H., 1992. Cost benefit model for the induction of an anti-predator defense. American Naturalist 140: 349–362.CrossRefGoogle Scholar
  75. Relyea, R. A., 2004. Fine-tuned phenotypes: tadpole plasticity under 16 combinations of predators and competitors. Ecology 85: 172–179.CrossRefGoogle Scholar
  76. Rennie, M. D., A. L. Strecker & M. E. Palmer, 2011. Bythotrephes invasion elevates trophic position of zooplankton and fish: implications for contaminant biomagnification. Biological Invasions 13: 2621–2634.CrossRefGoogle Scholar
  77. Rodriguez, L. F., 2006. Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biological Invasions 8: 927–939.CrossRefGoogle Scholar
  78. Rose, K. C., C. E. Williamson, J. M. Fischer, S. J. Connelly, M. Olson, A. J. Tucker & J. Noe, 2012. The role of ultraviolet radiation and fish in regulating the vertical distribution of Daphnia. Limnology and Oceanography 56: 1867–1876.CrossRefGoogle Scholar
  79. Rothhaput, K. O., 1997. Nutrient turnover by freshwater bacterivorous flagellates: differences between a heterotrophic and a mixotrophic chrysophyte. Aquatic Microbial Ecology 12: 65–70.CrossRefGoogle Scholar
  80. Rozenberg, A., P. Mrutunjaya, F. Leese, L. C. Weiss, R. Tollrian & J. Manak, 2015. Transcriptional profiling of predator-induced phenotypic plasticity in Daphnia pulex. Frontiers in Zoology 12: 18.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Salo, P., E. Korpimäki, P. B. Banks, M. Nordstrom & C. R. Dickman, 2007. Alien predators are more dangerous than native predators to prey populations. Proceedings of the Royal Society of London (Biology) 274: 1237–1243.CrossRefGoogle Scholar
  82. Saros, J. E., S. J. Interlandi, S. Doyle, T. J. Michel & C. E. Williamson, 2005. Are the deep chlorophyll maxima in alpine lakes primarily induced by nutrient availability, not UV avoidance? Arctic, Antarctic, and Alpine Research 37: 557–563.CrossRefGoogle Scholar
  83. Schindler, D. W., 1978. Factors regulating phytoplankton production and standing crop in the world’s freshwaters. Limnology and Oceanography 23: 478–486.CrossRefGoogle Scholar
  84. Schulz, K. L. & P. M. Yurista, 1999. Implications of an invertebrate predator’s (Bythotrephes cederstroemi) atypical effects on a pelagic zooplankton community. Hydrobiologia 380: 179–193.CrossRefGoogle Scholar
  85. Sih, A., G. Englund & D. Wooster, 1998. Emergent impacts of multiple predators on prey. Trends in Ecology & Evolution 13: 350–355.CrossRefGoogle Scholar
  86. Sih, A., D. I. Bolnick, B. Luttbeg, J. L. Orrock, S. D. Peacor, L. M. Pintor, E. Preisser, J. S. Rehage & J. R. Vonesh, 2010. Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119: 610–621.CrossRefGoogle Scholar
  87. Stabell, O. B., F. Ogbebo & R. Primecerio, 2003. Inducible defences in Daphnia depend on latent alarm signals from conspecific prey activated in predators. Chemical Senses 28: 141–153.CrossRefPubMedGoogle Scholar
  88. Stahl, J. B., 1966. The ecology of Chaoborus in Myers Lake, Indiana. Limnology and Oceanography 11: 177–183.CrossRefGoogle Scholar
  89. Stirling, G. & D. A. Roff, 2000. Behavioural plasticity without learning: phenotypic and genetic variation of naive Daphnia in an ecological trade-off. Animal Behaviour 59: 929–941.CrossRefPubMedGoogle Scholar
  90. Straile, D. & A. Hälbich, 2000. Life history and multiple antipredator defenses of an invertebrate pelagic predator, Bythotrephes longimanus. Ecology 81: 150–163.CrossRefGoogle Scholar
  91. Strauss, S. Y., J. A. Lau & S. P. Carroll, 2006. Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecology Letters 9: 354–371.CrossRefGoogle Scholar
  92. Strecker, A. L. & S. E. Arnott, 2005. Impact of Bythotrephes invasion on zooplankton communities in acid-damaged and recovered lakes on the Boreal Shield. Canadian Journal of Fisheries and Aquatic Sciences 62: 2450–2462.CrossRefGoogle Scholar
  93. 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
  94. 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
  95. Strecker, A. L., S. E. Arnott, N. D. Yan & R. Girard, 2006a. Variation in the response of crustacean zooplankton species richness and composition to the invasive predator Bythotrephes longimanus. Canadian Journal of Fisheries and Aquatic Sciences 63: 2126–2136.CrossRefGoogle Scholar
  96. Strecker, A. L., S. E. Arnott, N. D. Yan & R. Girard, 2006b. Variation in the response of crustacean zooplankton species richness and composition to the invasive predator Bythotrephes longimanus. Canadian Journal of Fisheries and Aquatic Sciences 63: 2126–2136.CrossRefGoogle Scholar
  97. Strobl, C., T. Hothorn & A. Zeilis, 2009. Party on! A new, conditional variable-importance measure for random forests available in the party package. Technical Report 050. University of Munich, Department of Statistics.Google Scholar
  98. Thrane, J. E., D. O. Hessen & T. Andersen, 2014. The absorption of light in lakes: negative impact of dissolved organic carbon on primary productivity. Ecosystems 17: 1040–1052.CrossRefGoogle Scholar
  99. Tollrian, R., 1995. Chaoborus crystallinus predation on Daphnia pulex: can induced morphological changes balance effects of body size on vulnerability? Oecologia 101: 151–155.CrossRefPubMedGoogle Scholar
  100. Vanderploeg, H., J. R. Leibig & M. Omair, 1993. Bythotrephes predation on Great Lakes zooplankton measured by an in situ method: implications for zooplankton community structure. Archiv fur Hydrobiologie 127: 1–8.Google Scholar
  101. Vanderploeg, H. A., S. A. Ludsin, J. F. Cavaletto, T. O. Höök, S. A. Pothoven, S. B. Brandt, J. R. Liebig & G. A. Lang, 2009. Hypoxic zones as habitat for zooplankton in Lake Erie: refuges from predation or exclusion zones? The Journal of Experimental Marine Biology and Ecology 381: S108–S120.CrossRefGoogle Scholar
  102. Von Elert, E. & G. Pohnert, 2000. Predator specificity of kairomones in diel vertical migration of Daphnia: a chemical approach. Oikos 88: 119–128.CrossRefGoogle Scholar
  103. Walsh, J. R., S. R. Carpenter & M. Vander Zanden, 2016. Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proceedings of the National academy of Sciences of the United States of America 113: 4081–4085.CrossRefPubMedPubMedCentralGoogle Scholar
  104. Ward, H. B. & G. C. Whipple, 1959. In Edmondson, W. T. (eds), Fresh Water Biology, 2nd edn. Wiley, London.Google Scholar
  105. Watt, P. J. & S. Young, 1994. Effect of predator chemical cues on Daphnia behavior in both horizontal and vertical planes. Animal Behaviour 48: 861–869.CrossRefGoogle Scholar
  106. Williamson, C. E., 2009. UV Lakes project: Water Transparency and UV attenuation. Accessed June 1, 2016, from http://www.orgs.miamioh.edu/uvlakes/UVecology/Intro/intro.html.
  107. Williamson, C. E., H. E. Zagarese, P. C. Schluze, B. R. Hargreaves & J. Seva, 1994. The impact of short-term exposure to UV-B radiation on zooplankton communities in north temperate lakes. Journal of Plankton Research 16: 205–218.CrossRefGoogle Scholar
  108. Williamson, C. E., R. S. Stemberger, D. P. Morris, T. M. Frost & S. G. Paulsen, 1996. Ultraviolet radiation in North American lakes: attenuation estimates from DOC measurements and implications for plankton communities. Limnology and Oceanography 41: 1024–1034.CrossRefGoogle Scholar
  109. Williamson, C. E., J. M. Fischer, S. M. Bollens, E. P. Overholt & J. K. Breckenridge, 2011. Toward a more comprehensive theory of zooplankton diel vertical migration: integrating ultraviolet radiation and water transparency into the biotic paradigm. Limnology and Oceanography 56: 1603–1623.CrossRefGoogle Scholar
  110. Wissel, B. & C. W. Ramcharan, 2003. Plasticity of vertical distribution of crustacean zooplankton in lakes with varying levels of water colour. Journal of Plankton Research 25: 1047–1057.CrossRefGoogle Scholar
  111. Witty, L. M., 2004. Practical Guide to Identifying Freshwater Crustacean Zooplankton. Laurentian University, Cooperative Freshwater Ecology Unit, Department of Biology, Sudbury: 57 pp.Google Scholar
  112. Yan, N. D. & T. W. Pawson, 1998. Seasonal variation in the size and abundance of the invading Bythotrephes in Harp Lake, Ontario, Canada. Hydrobiologia 8: 157–168.Google Scholar
  113. Yan, N. D., R. W. Nero, W. Keller & D. C. Lasenby, 1991. Are Chaoborus larvae more abundant in acidified than in non-acidified lakes in central Canada? Holarctic Ecology 8: 93–99.Google Scholar
  114. Yan, N. D., A. Blukacz, W. G. Sprules, P. K. Kindy, D. Hackett, R. D. Girard & B. J. Clark, 2001. Changes in 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
  115. Yan, N. D., R. Girard & S. Boudreau, 2002. An introduced invertebrate predator (Bythotrephes) reduces zooplankton species richness. Ecology Letters 5: 481–485.CrossRefGoogle Scholar
  116. Young, J. D. & N. D. Yan, 2008. Modification of the diel vertical migration of Bythotrephes longimanus by the cold-water planktivore, Coregonus artedi. Freshwater Biology 53: 981–995.CrossRefGoogle Scholar
  117. Zagarese, H. E., C. E. Williamson, M. Mislivets & P. Orr, 1994. The vulnerability of Daphnia to UV-B radiation in the Northeastern United States. Archiv fur Hydrobiologie 43: 207–216.Google Scholar

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Authors and Affiliations

  1. 1.Department of BiologyQueen’s UniversityKingstonCanada

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