Hydrobiologia

, Volume 796, Issue 1, pp 309–318 | Cite as

Vulnerability of rotifers and copepod nauplii to predation by Cyclops kolensis (Crustacea, Copepoda) under varying temperatures in Lake Baikal, Siberia

  • Michael F. Meyer
  • Stephanie E. Hampton
  • Tedy Ozersky
  • Olga O. Rusanovskaya
  • Kara H. Woo
ROTIFERA XIV

Abstract

As lakes warm worldwide, temperature may alter plankton community structure and abundance by affecting not only metabolism but also trophic interactions. Siberia’s Lake Baikal presents special opportunity for studying shifting trophic interactions among cryophilic zooplankton species in a rapidly warming lake. To understand how warming may affect trophic interactions among plankton, we studied predator–prey relationships of a copepod predator (Cyclops kolensis) with three prey types: two rotifer species (Gastropus stylifer and Keratella cochlearis) and copepod nauplii. We hypothesized that the less evasive Gastropus and Keratella would be more susceptible to predation than nauplii. We exposed a starved predator to individuals of each prey type and observed encounters, ingestions, and escapes. Contrary to our hypothesis, Keratella were consumed at lower rates than nauplii, due to higher probability of ingestion after encounter with nauplii. In a second experiment, we assessed how predation varied across a thermal gradient, confining all three prey types and one starved predator at 5° temperature increments (5–20°C). Predation outcomes mirrored observational feeding trials, and predation outcomes were independent of temperature. Rotifers’ relatively high reproductive rate may present a mechanism to withstand predation should copepod’s preferred nauplii prey become less abundant in a warmer Baikal.

Keywords

Freshwater food webs Rotifera Coldwater stenotherms Zooplankton 

References

  1. Afanasyeva, E. L., 1977. Biology of Epischura in Lake Baikal. Nauka, Novosibirsk, 144 pp.Google Scholar
  2. Allan, J. D., 1976. Life history patterns in zooplankton. American Naturalist 100: 165–180.CrossRefGoogle Scholar
  3. Bondarenko, N. A., A. Tuji & M. Nakanishi, 2006. A comparison of phytoplankton communities between the ancient Lakes Biwa and Baikal. Hydrobiologia 568: 25–29.CrossRefGoogle Scholar
  4. Brandl, Z., 2005. Freshwater copepods and rotifers: predators and their prey. Hydrobiologia 546: 475–489.CrossRefGoogle Scholar
  5. Dell, A. I., S. Pawar & V. M. Savage, 2011. Systematic variation in the temperature dependence of physiological and ecological traits. Proceedings of the National Academy of Sciences of USA 108: 10591–10596.CrossRefGoogle Scholar
  6. Dell, A. I., S. Pawar & V. M. Savage, 2014. Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. Journal of Animal Ecology 83: 70–84.CrossRefPubMedGoogle Scholar
  7. Devetter, M. & J. Seďa, 2006. Regulation of rotifer community by predation of Cyclops vicinus (Copepoda) in the Římov Reservoir in spring. International Review of Hydrobiology 91: 101–112.CrossRefGoogle Scholar
  8. Edmondson, W. T., 1946. Factors in the dynamics of rotifer populations. Ecological Monographs 16: 357.CrossRefGoogle Scholar
  9. Ekvall, M. K. & L.-A. Hansson, 2012. Differences in recruitment and life-history strategy alter zooplankton spring dynamics under climate-change conditions. PLoS One 7: e44614.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Elliott, J. A., I. D. Jones & S. J. Thackeray, 2006. Testing the sensitivity of phytoplankton communities to changes in water temperature and nutrient load, in a temperate lake. Hydrobiologia 559: 401–411.CrossRefGoogle Scholar
  11. George, D. G., 1976. Life cycle and production of Cyclops vicinus in a shallow eutrophic reservoir. Oikos 27: 101.CrossRefGoogle Scholar
  12. Gilbert, J. J. & C. E. Williamson, 1978. Predator–prey behavior and its effect on rotifer survival in associations of Mesocyclops edax, Asplanchna girodi, Polyarthra vulgaris, and Keratella cochlearis. Oecologia 37: 13–22.CrossRefPubMedGoogle Scholar
  13. Gilbert, J. J. & C. E. Williamson, 1983. Sexual dimorphism in zooplankton (Copepoda, Cladocera, and Rotifera). Annual Review of Ecology and Systematics 14: 1–33.CrossRefGoogle Scholar
  14. Gilbert, J. J. & R. S. Stemberger, 1984. Asplanchna-induced polymorphism in the rotifer Keratella slacki. Limnology and Oceanography 29: 1309–1316.CrossRefGoogle Scholar
  15. Gyllström, M., L. A. Hansson, E. Jeppesen, F. G. Criado, E. Gross, K. Irvine, T. Kairesalo, R. Kornijów, M. R. Miracle, M. Nykänen, & others, 2005. The role of climate in shaping zooplankton communities of shallow lakes. Limnology and Oceanography 50: 2008–2021.Google Scholar
  16. Halbach, U., 1973. Life table data and population dynamics of the rotifer Brachionus calyciflorus Pallas as influenced by periodically oscillating temperature. In Effects of Temperature on Ectothermic Organisms. Springer, Berlin: 217–228.Google Scholar
  17. Hambright, K. D., T. Zohary & H. Güde, 2007. Microzooplankton dominate carbon flow and nutrient cycling in a warm subtropical freshwater lake. Limnology and Oceanography 52: 1018–1025.CrossRefGoogle Scholar
  18. Hampton, S. E., L. R. Izmest’eva, M. V. Moore, S. L. Katz, B. Dennis & E. A. Silow, 2008. Sixty years of environmental change in the world’s largest freshwater lake – Lake Baikal, Siberia. Global Change Biology 14: 1947–1958.CrossRefPubMedCentralGoogle Scholar
  19. Hampton, S. E., D. K. Gray, L. R. Izmest’eva, M. V. Moore & T. Ozersky, 2014. The rise and fall of plankton: long-term changes in the vertical distribution of algae and grazers in Lake Baikal, Siberia. PLoS One 9: e88920.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Higgins, K. A., M. J. Vanni & M. J. González, 2006. Detritivory and the stoichiometry of nutrient cycling by a dominant fish species in lakes of varying productivity. Oikos 114: 419–430.CrossRefGoogle Scholar
  21. Huey, R. B., 1991. Physiological consequences of habitat selection. American Naturalist 137: 91–115.CrossRefGoogle Scholar
  22. Izmest’eva, L. R., E. A. Silow & E. Litchman, 2011. Long-term dynamics of Lake Baikal pelagic phytoplankton under climate change. Inland Water Biology 4: 301–307.CrossRefGoogle Scholar
  23. Izmest’eva, L. R., M. V. Moore, S. E. Hampton, C. J. Ferwerda, D. K. Gray, K. H. Woo, H. V. Pislegina, L. S. Krashchuk, S. V. Shimaraeva & E. A. Silow, 2016. Lake-wide physical and biological trends associated with warming in Lake Baikal. Journal of Great Lakes Research 42: 6–17.CrossRefGoogle Scholar
  24. Kostopoulou, V. & O. Vadstein, 2007. Growth performance of the rotifers Brachionus plicatilis, B.Nevada” and B.Cayman” under different food concentrations. Aquaculture 273: 449–458.CrossRefGoogle Scholar
  25. Kozhov, M. M., 1963. Lake Baikal and Its Life. W. Junk, The Hague: 344.CrossRefGoogle Scholar
  26. Kozhova, O. M. & L. R. Izmest’eva, 1998. Lake Baikal: Evolution and Biodiversity. Backhuys Publishers, Leiden: 447 pp.Google Scholar
  27. Kozhova, O. M., N. G. Mel’nik & G. I. Pomazkova (eds). 1978. Инcтpyкция пo oбpaбoткe пpoб плaнктoнa cчeтным мeтoдoм (Instructions for Processing and Counting Plankton Samples). Publications of Irkutsk State University: 1–50.Google Scholar
  28. Lehman, J. T., 1980. Release and cycling of nutrients between planktonic algae and herbivores. Limnology and Oceanography 25: 620–632.CrossRefGoogle Scholar
  29. Melnik, N. G., N. A. Bondarenko, O. I. Belykh, V. V. Blinov, V. G. Ivanov, I. V. Korovyakova, T. Y. Kostornova, M. I. Lazarev, N. F. Logacheva, G. I. Pomazkova, P. P. Sherstyankin, L. M. Sorokovikova, L. I. Tolstikova & E. P. Tereza, 2006. Distribution of pelagic invertebrates near a thermal bar in Lake Baikal. Hydrobiologia 568: 69–76.CrossRefGoogle Scholar
  30. Moore, M. V., C. L. Folt & R. S. Stemberger, 1996. Consequences of elevated temperatures for zooplankton assemblages in temperate lakes. Archiv für Hydrobiologie 135: 289–319.Google Scholar
  31. Moore, M. V., S. E. Hampton, L. R. Izmest’eva, E. A. Silow, E. V. Peshkova & B. K. Pavlov, 2009. Climate change and the world’s “sacred sea” – Lake Baikal, Siberia. Bioscience 59: 405–417.CrossRefGoogle Scholar
  32. Nandini, S., F. S. Zúñiga-Juárez & S. S. S. Sarma, 2014. Direct and indirect effects of invertebrate predators on population level responses of the rotifer Brachionus havanaensis (Rotifera): direct and indirect effects of invertebrate predators. International Review of Hydrobiology 99: 107–116.CrossRefGoogle Scholar
  33. O’Reilly, C. M., S. Sharma, D. K. Gray, S. E. Hampton, J. S. Read, R. J. Rowley, P. Schneider, J. D. Lenters, P. B. McIntyre, B. M. Kraemer, G. A. Weyhenmeyer, D. Straile, B. Dong, R. Adrian, M. G. Allan, O. Anneville, L. Arvola, J. Austin, J. L. Bailey, J. S. Baron, J. D. Brookes, E. de Eyto, M. T. Dokulil, D. P. Hamilton, K. Havens, A. L. Hetherington, S. N. Higgins, S. Hook, L. R. Izmest’eva, K. D. Joehnk, K. Kangur, P. Kasprzak, M. Kumagai, E. Kuusisto, G. Leshkevich, D. M. Livingstone, S. MacIntyre, L. May, J. M. Melack, D. C. Mueller-Navarra, M. Naumenko, P. Noges, T. Noges, R. P. North, P.-D. Plisnier, A. Rigosi, A. Rimmer, M. Rogora, L. G. Rudstam, J. A. Rusak, N. Salmaso, N. R. Samal, D. E. Schindler, S. G. Schladow, M. Schmid, S. R. Schmidt, E. Silow, M. E. Soylu, K. Teubner, P. Verburg, A. Voutilainen, A. Watkinson, C. E. Williamson & G. Zhang, 2015. Rapid and highly variable warming of lake surface waters around the globe: global lake surface warming. Geophysical Research Letters 42: 10773–10781.CrossRefGoogle Scholar
  34. Pavón-Meza, E. L., S. S. S. Sarma & S. Nandini, 2007. Combined effects of temperature, food (Chlorella vulgaris) concentration and predation (Asplanchna girodi) on the morphology of Brachionus havanaensis (Rotifera). Hydrobiologia 593: 95–101.CrossRefGoogle Scholar
  35. Plassmann, T., G. Maier & H. B. Stich, 1997. Predation impact of Cyclops vicinus on the rotifer community in Lake Constance in spring. Journal of Plankton Research 19: 1069–1079.CrossRefGoogle Scholar
  36. Pomazkova, G. I. & E. N. Kuzevanova, 1989. Динaмикa чиcлeннocти и cтpyктypa плaнктoнныx кoлoвpaтoк oзepa Бaйкaл пo мнoгoлeтним дaнным (1946–1985 гг.) (Dynamics and structure of planktonic rotifers of Lake Baikal according to long-term data (1946–1985)). Proceeding of the III Rotifer Symposium: 89–92.Google Scholar
  37. Pourriot, R. & P. Clement, 1981. Action de facteurs externes sur la reproduction et le cycle reproducteur de reitfè (External factors affecting reproduction and reproductive cycle of rotifers). Acta Ecologia: Ecologia Generalis 2: 135–151.Google Scholar
  38. Pourriot, R. & C. Rougier, 1997. Taux de reproduction en fonction de la concentration en nourriture et de la température chez trois espèces du genre Brachionus (Rotifères) (Reproduction rates in relation to food concentration and temperature in three species of the genus Brachionus (Rotifera)). Annales de Limnologie: International Journal of Limnology 33: 23–31.CrossRefGoogle Scholar
  39. R Core Team. 2016. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna [available on internet at http://www.R-project.org/].
  40. Richardson, T. L., C. E. Gibson & S. I. Heaney, 2000. Temperature, growth and seasonal succession of phytoplankton in Lake Baikal, Siberia. Freshwater Biology 44: 431–440.CrossRefGoogle Scholar
  41. Rigosi, A., P. Hanson, D. P. Hamilton, M. Hipsey, J. A. Rusak, J. Bois, K. Sparber, I. Chorus, A. J. Watkinson, B. Qin & others, 2015. Determining the probability of cyanobacterial blooms: the application of Bayesian networks in multiple lake systems. Ecological Applications 25: 186–199.Google Scholar
  42. Sarma, S. S. S., R. A. L. Resendiz & S. Nandini, 2011. Morphometric and demographic responses of brachionid prey (Brachionus calyciflorus Pallas and Plationus macracanthus (Daday)) in the presence of different densities of the predator Asplanchna brightwellii (Rotifera: Asplanchnidae). Hydrobiologia 662: 179–187.CrossRefGoogle Scholar
  43. Schabetsberger, R., M. S. Luger, G. Drozdowski & A. Jagsch, 2009. Only the small survive: monitoring long-term changes in the zooplankton community of an Alpine lake after fish introduction. Biological Invasions 11: 1335–1345.CrossRefGoogle Scholar
  44. Schmidt, S. N., M. J. Vander Zanden & J. F. Kitchell, 2009. Long-term food web change in Lake Superior. Canadian Journal of Fisheries and Aquatic Sciences 66: 2118–2129.CrossRefGoogle Scholar
  45. Seifert, L. I., G. Weithoff, U. Gaedke & M. Vos, 2015. Warming-induced changes in predation, extinction and invasion in an ectotherm food web. Oecologia 178: 485–496.CrossRefPubMedGoogle Scholar
  46. Shaw, R. G. & T. Mitchell-Olds, 1993. ANOVA for unbalanced data: an overview. Ecology 74: 1638–1645.CrossRefGoogle Scholar
  47. Shimaraev, M. N., L. N. Kuimova, V. N. Sinyukovich & V. V. Tsekhanovskii, 2002. Manifestation of global climate change in Lake Baikal during the 20th century. Doklady Earth Sciences 383A: 288–291.Google Scholar
  48. Silow, E. A., L. S. Krashchuk, K. A. Onuchin, H. V. Pislegina, O. O. Rusanovskaya & S. V. Shimaraeva, 2016. Some recent trends regarding Lake Baikal phytoplankton and zooplankton. Lakes and Reservoirs: Research and Management 21: 40–44.CrossRefGoogle Scholar
  49. Stemberger, R. S., 1985. Prey selection by the copepod Diacyclops thomasi. Oecologia 65: 492–497.CrossRefPubMedGoogle Scholar
  50. Stemberger, R. S. & J. J. Gilbert, 1984. Spine development in the rotifer Keratella cochlearis: induction by cyclopoid copepods and Asplanchna. Freshwater Biology 14: 639–647.CrossRefGoogle Scholar
  51. Tadonléké, R. D., J. Marty & D. Planas, 2012. Assessing factors underlying variation of CO2 emissions in boreal lakes vs. reservoirs. FEMS Microbiology Ecology 79: 282–297.CrossRefPubMedGoogle Scholar
  52. Thackeray, S. J., T. H. Sparks, M. Frederiksen, S. Burthe, P. J. Bacon, J. R. Bell, M. S. Botham, T. M. Brereton, P. W. Bright, L. Carvalho, T. Clutton-Brock, A. Dawson, M. Edwards, J. M. Elliott, R. Harrington, D. Johns, I. D. Jones, J. T. Jones, D. I. Leech, D. B. Roy, W. A. Scott, M. Smith, R. J. Smithers, I. J. Winfield & S. Wanless, 2010. Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments: phenological change across major environments. Global Change Biology 16: 3304–3313.CrossRefGoogle Scholar
  53. Williamson, C. E., 1980. The predatory behavior of Mesocyclops edax: predator preferences, prey defenses, and starvation-induced changes. Limnology and Oceanography 25: 903–909.CrossRefGoogle Scholar
  54. Zhang, H., M. K. Ekvall, J. Xu & L.-A. Hansson, 2015. Counteracting effects of recruitment and predation shape establishment of rotifer communities under climate change: counteracting effect and shape establishment. Limnology and Oceanography 60: 1577–1587.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Michael F. Meyer
    • 1
  • Stephanie E. Hampton
    • 2
  • Tedy Ozersky
    • 3
  • Olga O. Rusanovskaya
    • 4
  • Kara H. Woo
    • 2
  1. 1.School of the EnvironmentWashington State UniversityPullmanUSA
  2. 2.Center for Environmental Research, Education, and OutreachWashington State UniversityPullmanUSA
  3. 3.Large Lakes ObservatoryUniversity of Minnesota-DuluthDuluthUSA
  4. 4.Biological Research InstituteIrkutsk State UniversityIrkutskRussian Federation

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