, Volume 138, Issue 4, pp 603–612 | Cite as

Damaging UV radiation and invertebrate predation: conflicting selective pressures for zooplankton vertical distribution in the water column of low DOC lakes

  • Wiebke J. BoeingEmail author
  • Dina M. Leech
  • Craig E. Williamson
  • Sandra Cooke
  • Lisette Torres
Community Ecology


In nature most organisms have to manage conflicting demands of food gathering, predator avoidance, and finding a favorable abiotic environment (oxygen, temperature, etc.) in order to maximize their fitness. In the vertical water column of lakes with high solar ultraviolet radiation (UV) and invertebrate predators, zooplankton face two particularly strong and conflicting selective pressures. During daylight hours invertebrate predators often induce an upward vertical migration of zooplankton prey while potentially damaging UV forces a downward migration. We used 2.2 m long columns suspended vertically in a lake to conduct 2×2 factorial experiments to examine patterns of depth selection behavior by zooplankton in the presence and absence of both the invertebrate predator Chaoborus and UV. We hypothesized that Chaoborus and UV both affect the distribution of zooplankton and a combination of both factors would lead to a narrowing of depth distribution. We found that when Chaoborus were present zooplankton tended to be distributed at shallower depths in the columns, while in the presence of UV they exhibited a deeper distribution. Chaoborus themselves were always found near the bottom of the columns regardless of the UV treatment. Simultaneous exposure to predators and UV resulted in a peak of zooplankton (especially Daphnia catawba) distribution at intermediate depths. In a significant number of cases, depth range was narrowed in response to Chaoborus, UV, or both.


Ultraviolet  Chaoborus Vertical distribution Vertical migration Predator-prey overlap 



We thank Lacawac Sanctuary and Janice Poppich for accommodations and access to Lake Lacawac and Blooming Grove Hunting and Fishing Club and Robin Wildermuth for access to Lake Giles. We are grateful for the constructive comments by David Post, Paige Hopper and anonymous reviewers to this manuscript. This work was supported by NSF grants DEB 9973938 and DEB 0210972, NOAA’s Fisheries-Oceanography Coordinated Investigations contribution FOCI-0480 and the Joint Institute for the Study of the Atmosphere and Ocean (JISAO) under NOAA Cooperative Agreement No. NA17RJ1232, Contribution #1000.


  1. Bakker JP, Berendse F (1999) Constraints in the restoration of ecological diversity in grassland and heathland communities. Trends Ecol Evol 14:63–68CrossRefPubMedGoogle Scholar
  2. Band LE, Mackay DS, Creed IF, Semkin R, Jeffries D (1996) Ecosystem processes at the watershed scale: Sensitivity to potential climate change. Limnol Oceanogr 41:928–938Google Scholar
  3. Bayly IAE (1986) Aspects of diel vertical migration in zooplankton, and its enigma variations. In: Deckker P, Williams WD (eds) Limnology in Australia. Junk, Dordrecht, The Netherlands, pp 349–368Google Scholar
  4. Benndorf J, Wissel B, Sell AF, Hornig U, Ritter P, Böing W (2000) Food web manipulation by extreme enhancement of piscivory: an invertebrate predator compensates for the effects of planktivorous fish on a plankton community. Limnologica 30:235–245Google Scholar
  5. Berendonk TU, O’Brien WJ (1996) Movement responses of Chaoborus to chemicals from a predator and prey. Limnol Oceanogr 41:1829–1832Google Scholar
  6. Bottrell HH (1975) The relationship between temperature and duration of egg development in some epiphytic Cladocera and Copepoda from the river Thames. Reading, with a discussion of temperature functions. Oecologia 18:63–68Google Scholar
  7. Caldwell MM, Ballare CL, Bornman JF, Flint SD, Bjorn LO, Teramura AH, Kulandaivelu G, Tevini M (2003) Terrestrial ecosystems increased solar ultraviolet radiation and interactions with other climatic change factors. Photochem Photobiol Sci 2:29–38CrossRefPubMedGoogle Scholar
  8. Carruthers RI (2003) Invasive species research in the United States Department of Agriculture—Agricultural Research Service. Pest Manage Sci 59:827–834CrossRefGoogle Scholar
  9. Chen M, Pollard D, Barron EJ (2003) Comparison of future climate change over North America simulated by two regional models. J Geophys Res Atmos 108:4348Google Scholar
  10. Clair TA, Ehrman J, Kaczmarska I, Locke A, Tarasick DW, Day KE, Maillet G (2001) Will reduced summer UV-B levels affect zooplankton populations of temperate humic and clearwater lakes? Hydrobiologia 462:75–89CrossRefGoogle Scholar
  11. Connell AD (1978) Reversed vertical migration of planktonic crustaceans in a eutrophic lake of high pH. J Limnol Soc S Afr 4:101–104Google Scholar
  12. Corfield J (2000) The effects of acid sulphate run-off on a subtidal estuarine macrobenthic community in the Richmond River, NSW, Australia. J Mar Sci 57:1517–1523CrossRefGoogle Scholar
  13. Day TA, Neale PJ (2002) Effects of UV-B radiation on terrestrial and aquatic primary producers. Annu Rev Ecol Syst 33:371–396CrossRefGoogle Scholar
  14. Dawidowicz P, Loose CJ (1992) Metabolic costs during predator-induced diel vertical migration of Daphnia. Limnol Oceanogr 37:665–669Google Scholar
  15. Dawidowicz P, Pijanowska J, Ciechomski K (1990) Vertical migration of Chaoborus larvae is induced by the presence of fish. Limnol Oceanogr 37:1631–1637Google Scholar
  16. De Meester L, Dawidowicz P, Van Gool E, Loose C (1999) Ecology and evolution of predator-induced behavior of zooplankton: depth selection behavior and diel vertical migration. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, New Jersey, pp 160–176Google Scholar
  17. Dodson SI (1972) Mortality in a population of Daphnia rosea. Ecology 53:1011–1023Google Scholar
  18. Dodson SI (1988) The ecological role of chemical stimuli for zooplankton: predator-avoidance behavior in Daphnia. Limnol Oceanogr 33:1431–1439Google Scholar
  19. Driscoll CT, Driscoll KM, Mitchell MJ, Raynal DJ (2003) Effects of acidic deposition on forest and aquatic ecosystems in New York State. Environ Pollut 123:327–336CrossRefPubMedGoogle Scholar
  20. Fedorenko AY (1975) Instar and species-specific diets in two species of Chaoborus. Limnol Oceanogr 20:238–249Google Scholar
  21. Harvell CD (1990) The ecology and evolution of inducible defenses. Q Rev Biol 65:323–340PubMedGoogle Scholar
  22. Hessen DO, Van Donk E (1994) Effects of UV-Radiation of humic water on primary and secondary production. Water Air Soil Pollut 75:325–338Google Scholar
  23. Hurtubise RD, Havel JE, Little EE (1998) The effects of ultraviolet-B radiation of freshwater invertebrates: experiments with a solar simulator. Limnol Oceanogr 43:1082–1088Google Scholar
  24. Jones AG, Chown SL, Ryan PG, Gremmen NJM, Gaston KJ (2003) A review of conservation threats on Gough Island: a case study for terrestrial conservation in the Southern Oceans. Biol Conserv 113:75–87CrossRefGoogle Scholar
  25. Kajak Z, Rybak J (1979) The feeding of Chaoborus flavicans Meigen (Diptera, Chaoboridae) and its predation on lake zooplankton. Int Rev Ges Hydrobiol 64:361–378Google Scholar
  26. Kennedy AD (1995) Antarctic terrestrial ecosystem response to global environmental change. Annu Rev Ecol Syst 26:683–704CrossRefGoogle Scholar
  27. Kerfoot WC (1985) Adaptive value of vertical migration: comments on the predation hypothesis and some alternatives. Contrib Mar Sci 27:91–113Google Scholar
  28. Kerr JB, McElroy CT (1993) Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion. Science 262:1032–1034Google Scholar
  29. Lamontagne S, Donald DB, Schindler DW (1994) The distribution of 4 Chaoborus species (Diptera, Chaoboridae) along an elevation gradient in Canadian Rocky Mountain lakes. Can J Zool 72:1531–1537Google Scholar
  30. Leech DM, Johnsen S (2003) Behavioral responses: UV avoidance and vision. In: Helbling W, Zagarese H (eds) UV effects in aquatic organisms and ecosystems. Royal Society of Chemistry, Cambridge, pp 455–481Google Scholar
  31. Leech DM, Williamson CE (2000) Is tolerance to UV radiation in zooplankton related to body size, taxon, or lake transparency? Ecol Appl 10:1530–1540Google Scholar
  32. Leech DM, Williamson CE (2001) In situ exposure to ultraviolet radiation alters the depth distribution of Daphnia. Limnol Oceanogr 46:416–420Google Scholar
  33. Lin ZS (2003) Simulating unintended effects restoration. Ecol Model 164:169–175CrossRefGoogle Scholar
  34. Luecke C (1986) A change in the pattern of vertical migration of Chaoborus flavicans after the introduction of trout. J Plankton Res 8:649–657Google Scholar
  35. Morris DP, Hargreaves BR (1997) The role of photochemical degradation of dissolved organic carbon in regulating the UV transparency of three lakes on the Pocono Plateau. Limnol Oceanogr 42:239–249Google Scholar
  36. Morris DP, Zagarese H, Williamson CE, Balseiro EG, Hargreaves BR, Modenutti B, Moeller RE, Queimalinos C (1995) The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnol Oceanogr 40:1381–1391Google Scholar
  37. Neill WE (1990) Induced vertical migration in copepods as a defense against invertebrate predation. Nature 345:524–526CrossRefGoogle Scholar
  38. Nesbitt LM, Riessen HP, Ramcharan CW (1996) Opposing predation pressures and induced vertical migration responses in Daphnia. Limnol Oceanogr 41:1306–1311Google Scholar
  39. Ohman MD (1990) The demographic benefits of diel vertical migration by zooplankton. Ecol Monogr 60:257–281Google Scholar
  40. Ohman MD, Frost BW, Cohen EB (1983) Reverse diel vertical migration: an escape from invertebrate predators. Science 220:1404–1407Google Scholar
  41. Persaud AD, Yan ND (2003) UVR sensitivity of Chaoborus larvae. Ambio 32:219–224PubMedGoogle Scholar
  42. Post DM (2002) The long and short of food-chain length. Trends Ecol Evol 17:269–277Google Scholar
  43. Ramcharan CW, Dodson SI, Lee J (1992) Predation risk, prey behavior, and feeding rate in Daphnia pulex. Can J Fish Aquat Sci 49:159–165Google Scholar
  44. Ramcharan CW, Yan ND, McQueen DJ, Perez-Fuentetaja A, Demers E, Rusak JA (2001) Dynamics of zooplankton productivity under two different predatory regimes. Arch Hydrobiol Spec Iss Advanc Limnol 56:151–169Google Scholar
  45. Rautio M, Korhola A (2002) Effects of ultraviolet radiation and dissolved organic carbon on the survival of subarctic zooplankton. Polar Biol 25:460–468Google Scholar
  46. Resh VA, Barnby MA (1987) Distribution of the Wilbur springs shorebug (Hemiptera, Saldidae)–a product of abiotic tolerances and biotic constraints. Environ Entomol 16:1087–1091Google Scholar
  47. Rhode SC, Pawlowski M, Tollrian R (2001) The impact of ultraviolet radiation on the vertical distribution of zooplankton of the genus Daphnia. Nature 412:69–72CrossRefPubMedGoogle Scholar
  48. Rouse WR, Douglas MSV, Hecky RE, Hershey AE, Kling GW, Lesack L, Marsh P, McDonald M, Nicholson BJ, Roulet NT, Smol JP (1997) Effects of climate change on the freshwaters of arctic and subarctic North America. Hydrol Process 11:873–902CrossRefGoogle Scholar
  49. Saether OA (1970) Nearctic and palearctic Chaoborus (Diptera, Chaoboridae). Bull Fish Res Bd Can 174:57Google Scholar
  50. Schindler DW, Curtis PJ, Parker BR, Stainton MP (1996) Consequences of climate warming and lake acidification for UV-B penetration in North American boreal lakes. Nature 379:705–708Google Scholar
  51. Scully NM, Lean DRS (1994) The attenuation of ultraviolet radiation in temperate lakes. Arch Hydrobiol Beih Ergeb Limnol 43:135–144Google Scholar
  52. Smith KC, Macagno ER (1990) UV photoreceptors in the compound eye of Daphnia magna (Crustacea, Branchiopoda)–a 4th spectral class in single ommatidia. J Comp Physiol A 166:597–606PubMedGoogle Scholar
  53. StatSoft Inc. (2003) STATISTICA (data analysis software system), version 6. (www. Scholar
  54. Stibor H, Lampert W (2000) Components of additive variance in life-history traits of Daphnia hyalina: seasonal differences in the response to predator signals. Oikos 88:129–138Google Scholar
  55. Stich HB, Lampert W (1981) Predator evasion as an explanation of diurnal vertical migration by zooplankton. Nature 293:396–398Google Scholar
  56. Swift MC (1976) Energetics of vertical migration in Chaoborus trivittatus larvae. Ecology 57:900–914Google Scholar
  57. Tjossem SF (1990) Effects of fish chemical cues on vertical migration behavior of Chaoborus. Limnol Oceanogr 35:1456–1468Google Scholar
  58. Tollrian R, Dodoson SI (1999) Inducible defenses in Cladocera: Constraints, costs, and multipredator environments. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 177–202Google Scholar
  59. Van Donk E, Hessen DO (1995) Reduced digestibility of UV-B stressed and nutrient-limited algae by Daphnia magna. Hydrobiologia 307:147–151Google Scholar
  60. Voss S, Mumm H (1999) Where to stay by day and night: Size-specific and seasonal differences in horizontal and vertical distribution of Chaoborus flavicans larvae. Freshwater Biol 42:201–213CrossRefGoogle Scholar
  61. Wichmann MC, Jeltsch F, Dean WRJ, Moloney KA, Wissel C (2003) Implication of climate change for the persistence of raptors in arid savanna. Oikos 102:186–202Google Scholar
  62. Williams JW, Post DM, Cwynar LC, Lotter AF, Levesque AJ (2002) Rapid and widespread vegetation responses to past climate change in the North Atlantic region. Geology 30:971–974CrossRefGoogle Scholar
  63. Williamson CE (1996) Effects of UV radiation on freshwater ecosystems. Int J Environ Stud 51:245–256Google Scholar
  64. Williamson CE, Zaragese HE, Schulze PC, Hargreaves R, Seva J (1994) The impact of short-term exposure of UV-B radiation on zooplankton communities in north temperate lakes. J Plankton Res 16:205–218Google Scholar
  65. Williamson CE, Stemberger RS, Morris DP, Frost TM, Paulsen SG (1996) Ultraviolet radiation in North American Lakes: attenuation estimates from DOC measurements and implications for plankton communities. Limnol Oceanogr 41:1024–1034Google Scholar
  66. Williamson CE, Metzgar SL, Lovera PA, Moeller RE (1997) Solar ultraviolet radiation and the spawning habitat of yellow perch, Perca flavescens. Ecol Appl 7:1017–1023Google Scholar
  67. Williamson CE, Hargreaves BR, Orr PS, Lovera PA (1999) Does UV radiation play a role in changes in predation and zooplankton community structure in acidified lakes Limnol Oceanogr 44:774–783Google Scholar
  68. Williamson CE, Neale PJ, Grad G, De Lange HJ, Hargreaves BR (2001a) Beneficial and detrimental effects of UV on aquatic organisms: Implications of spectral variation. Ecol Appl 11:1843–1857Google Scholar
  69. Williamson CE, Olson OG, Lott SE, Walker ND, Engstrom DR, Hargreaves BR (2001b) Ultraviolet radiation and zooplankton community structure following deglaciation in Glacier Bay, Alaska. Ecology 82:1748–1760Google Scholar
  70. Wissel B (2001) Effects of water color on food web structure in freshwater lakes. Dissertation, Louisiana State UniversityGoogle Scholar
  71. Woodward FI, Rochefort L (1991) Sensitivity analysis of vegetation diversity to environmental change. Global Ecol Biogeogr 1:7−23Google Scholar
  72. Yan ND, Nero RW, Keller W, Lasenby DC (1985) Are Chaoborus larvae more abundant in acidified than in non-acidified lakes in central Canada? Holarct Ecol 8:93–99Google Scholar
  73. Yan ND, Keller W, McIsaac HJ, Lasenby DC (1991) Regulation of zooplankton community structure of an acidified lake by Chaoborus. Ecol Appl 1:52–65Google Scholar
  74. Yan ND, Keller W, Scully NM, Lean DRS, Dillon PJ (1996) Increased UV-B penetration in a lake owing to drought-induced acidification. Nature 381:141–143CrossRefGoogle Scholar
  75. Zaret TM, Suffern JS (1976) Vertical migration in zooplankton as a predator avoidance mechanism. Limnol Oceanogr 21:804–813Google Scholar
  76. Zellmer ID (1996) The impact of food quantity on UV-B tolerance and recovery from UV-B damage in Daphnia pulex. Hydrobiologia 319:87–92Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Wiebke J. Boeing
    • 1
    • 3
    Email author
  • Dina M. Leech
    • 2
  • Craig E. Williamson
    • 2
  • Sandra Cooke
    • 2
  • Lisette Torres
    • 2
  1. 1.Department of Biological SciencesLouisiana State UniversityBaton RougeUSA
  2. 2.Department of Earth and Environmental SciencesLehigh UniversityBethlehemUSA
  3. 3.Alaska Fisheries Science CenterNOAASeattleUSA

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