Control of Cyanobacteria (Microcystis aeruginosa) Blooms by Floating Aquatic Plant (Iris pseudoacorus): an in situ Mesocosm Experiment Using Stable ($^{13}C$, $^{15}N$) Isotope Tracers

$^{13}C$, $^{15}N$ 추적자 실험을 통한 부유 수생식물(Iris pseudoacorus)의 Cyanobacteria (Microcystis aeruginosa) 성장억제능력 평가

  • Received : 2011.08.11
  • Accepted : 2011.09.20
  • Published : 2011.09.30

Abstract

Bottom-up approaches to control of Microcystis aeruginosa blooms were comparatively investigated through an in situ mesocosm experiment using aquatic plants (Iris pseudoacorus). In the mesocosm experiments, floating I. pseudoacorus, seemed to be effective in controlling massive M. aeruginosa blooms in an agricultural reservoir, exhibiting a close coupling with temporal variations in Chl-a and DO concentration. Shading by floating I. pseudoacorus resulted in a reduced phytoplankton abundance inhibiting light energy availability. Moreover, I. pseudoacorus may suppress phytoplankton growth through the excretion of chemical substances, likes a allelopathy, that inhibit phytoplankton photosynthetic activity. The $^{15}N$ atom % of I. pseudoacorus showed higher values than POM, suggesting that I. pseudoacorus assimilates DIN predominantly compared to phytoplankton, which was mostly M. aeruginosa. This result strongly suggests that the M. aeruginosa bloom should be regulated by aquatic plants, like I. pseudoacorus, this approach can affect zooplankton composition. This is the first study that has used stable isotope tracers to evaluate the biomanipulation efficiency through floating I. pseudoacorus.

생물조절기법(Biomanipulation)을 이용한 수질개선 방법으로서, 인공식물섬을 이용한 부유성 수생식물(I. pseudoacorus)은 그 표면적에 따라서 수층으로의 광량 투과를 제어함으로써 미세조류의 광합성 효율을 저해한다. 또한, 수층에서 영양염을 흡수하여, 미세조류의 성장을 억제함으로서 남조류(M. aeruginosa) 대량발생을 제어할 수 있다는 것을 $^{13}C$, $^{15}N$ 추적자 실험을 통하여 정량적으로 확인하였다. 이와 같이 부유수생식물을 이용하여 저수지내 남조류 번성을 억제함으로서 수질 개선에 중요한 역할을 하지만, 동물플랑크톤의 종 조성 변화를 야기할 수 있다는 것을 고려해야 할 것이다. 본 연구 결과는 향후 인공 식물섬을 사용한 남조류 제어 기법에 중요한 자료로 활용될 것으로 사료된다.

Keywords

References

  1. An, K.G., J.Y. Lee, K. Hema, S.J. Lee, S.J. Hwang, B.H. Kim, S.K. Park and H.Y. Um. 2010. Control of algal scum using top-down biomanipulation approach and ecosystem health assessments for efficient reservoir management. Water Air Soil Pollutant 205: 3-24.
  2. Balls, H., B. Moss and K. Irvine. 1989. The loss of submerged plants with eutrophication I. Experimental design, water chemistry, aquatic plant and phytoplankton biomass in experiments carried out in ponds in the Norfolk Broadland. Freshwater Biology 22: 71-87. https://doi.org/10.1111/j.1365-2427.1989.tb01085.x
  3. Barko, J.W. and W.F. James. 1998. Effects of submerged aquatic macrophytes on nutrient dynamics, sedimentation, and resuspension, p. 197-217. In: The Structuring Role of Submerged Macrophytes in Lakes (Jeppesen, E., M. Sondergaard and K. Christoffersen, eds.). Springer, New York.
  4. Beklioglu, M. 1999. A review on the control of eutrophication in deep and shallow lakes. Turkish Journal of Zoology 23: 327-336.
  5. Benndorf, J. 1990. Conditions for effective biomanipulation: conclusions derived from whole-lake experiments in Europe. Hydrobiologia 200/201: 187-203.
  6. Bontes, B.M., A.M. Verschoo, L.M. Dionisio Pires, E. Van Donk and B.W. Ibelings. 2007. Functional response of Anodonta anatine feeding on a green algal and four strains of cyanobacteria, differing in shape, size and toxicity. Hydrobiologia 584: 191-204. https://doi.org/10.1007/s10750-007-0580-2
  7. Bunn, S.E., N.R. Loneragan and M.A. Kempster. 1995. Effects of acid washing samples on stable isotope ratios of C and N in penaeid shrimps and seagrass: implications for food web studies using stable isotopes. Limnology and Oceanography 40: 622-625. https://doi.org/10.4319/lo.1995.40.3.0622
  8. Caraco, J., J.C. Cole, S. Findlay and C. Wigand. 2006. Vascular plants as engineers of oxygen in aquatic systems. Bioscience 56: 219-225. https://doi.org/10.1641/0006-3568(2006)056[0219:VPAEOO]2.0.CO;2
  9. Carpenter, S.R., J.F. Kitchell and J.R. Hodgson. 1985. Cascading trophic interactions and lake productivity. Bioscience 35: 634-639. https://doi.org/10.2307/1309989
  10. DeMott, W.R. 1999. Foraging strategies and growth inhibition in 5 daphnids feeding on mixtures of a toxic cyanobacterium and a green alga. Freshw Biol 42: 263-274. https://doi.org/10.1046/j.1365-2427.1999.444494.x
  11. Dittmann, E. and C. Wiegand. 2006. Cyanobacterial toxinsoccurrence, biosynthesis and impact on human affairs. Molecular Nutrition & Food Research 50: 7-17. https://doi.org/10.1002/mnfr.200500162
  12. Engstrom, J., M. Viherluoto and M. Viitasalo. 2001. Effects of toxic and non-toxic cyanobacteria on grazing, zooplanktivory and survival of the mysid shrimp Mysis mixta. Journal of Experimental Marine Biology and Ecology 257: 269-280. https://doi.org/10.1016/S0022-0981(00)00339-7
  13. Fulton, R.S. 1988. Resistance to blue-green toxins by Bosmina longirostris. J Plankton Res 10: 771-778. https://doi.org/10.1093/plankt/10.4.771
  14. Gopal, B. and U. Goel. 1993. Competition and allelopathy in aquatic plant communities. Botanical Review 59: 155-210. https://doi.org/10.1007/BF02856599
  15. Gross, E.M. 1999. Allelopathy in benthic and littoral areas: case studies on allelochemicals from benthic cyanobacteria and submerged macrophytes. p. 179-199. In: Principles and Practices in Plant Ecology: Allelochemical Interactions (Inderjit Dakshini, K.M.M. and C.L. Foy, eds.). CRC Press, Boca Raton, FL.
  16. Hama, T., T. Miyazaki, Y. Ogawa, T. Iwakuma, M. Takahashi, A. Otsuki and S. Ichimura. 1983. Measurement of photosynthetic production of a phytoplankton population using a stable 13C isotope. Mar Biol 73: 31-36. https://doi.org/10.1007/BF00396282
  17. Hanazato, T. and M. Yasuno. 1984. Growth, reproduction and assimilation of Moina macropoda fed on Microcystis and/or Chlorella. Jpn J Ecol 34: 195-202.
  18. Hutchinson, G.E. 1975. A Treatise on Limnology. Vol. III. Limnological Botany. Wiley, New York.
  19. Hwang, S.J., H.S. Kim and J.K. Shin. 2001. Filter-feeding effect of a freshwater bivalve (Corbicula leana PRIME) on phytoplankton. Korean Journal of Limnology 34(4): 298-309.
  20. Infante, A. and W. Riehl. 1984. The effect of Cyanophyta upon zooplankton in a eutrophic lake. Hydrobiologia 113: 293-298. https://doi.org/10.1007/BF00026615
  21. Jasser, I. 1995. The influence of macrophytes on a phytoplankton community in experimental conditions. Hydrobiologia 306: 21-32. https://doi.org/10.1007/BF00007855
  22. Jeppesen, E., J.P. Jensen, M. Sondergaard, T.L. Lauridsen, L.J. Pedersen and L. Jensen. 1997. Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth. Hydrobiologia 342-343: 151-164. https://doi.org/10.1023/A:1017046130329
  23. Jeppesen, E., T.L. Lauridsen, T. Kairesalo and M.R. Perrow. 1998. Impact of submerged macrophytes on fish-zooplankton interactions in lakes, p. 91-114. In: The Structuring Role of Submerged Macrophytes in Lakes (Jeppesen, E., M. Sondergaard and K. Christoffersen, eds.). Springer, New York.
  24. Kononen, K., J. Kuparinen, K. Makela, J. Laanemets, J. Pavelson and S. Nommann. 1996. Initiation of cyanobacterial blooms in a frontal region at the entrance to the Gulf on Finland, Baltic Sea. Limnology and Oceanography 41: 98-112. https://doi.org/10.4319/lo.1996.41.1.0098
  25. Koski, M., M. Rosenberg and M. Viitasalo. 1999a. Reporduction and survivial of the calanoid copepod Eurytemora affinis fed with toxic and non-toxic cyanobacteria. Marine Ecology Progress Series 186: 187-197. https://doi.org/10.3354/meps186187
  26. Lampert, W. 1987. Laboratory studies on zooplankton-cyanobacteria interactions. NZ J Mar Freshw Res 21: 483-490. https://doi.org/10.1080/00288330.1987.9516244
  27. Large, A.R.G., G. Pabon and C. Amoros. 1996. Primary production and primary producers, p. 117-136. In: Fluvial Hydrosystems (Petts, G.E. and C. Amoros, eds.). Chapman & Hall, London.
  28. Magalhaes, V.F., R.M. Soares and S.M.F.O. Azevedo. 2001. Microcystin contamination in fish from the Hacarepagua Lagoon (Rio de Janeiro, Brazil): ecological implication and human health risk. Toxicon 39: 1077-1085. https://doi.org/10.1016/S0041-0101(00)00251-8
  29. Mehner, T., R. Arlinghaus, S. Berg, H. Dorner, L. Jacobsen, P. Kasprzak, R. Koschel, T. Schulze, C. Skov, C. Wolter and K. Wysujack. 2004. How to link biomanipulation and sustainable fisheries management: a step-by-step guideline for lakes of the European temperate zone. Fisheries Management and Ecology 11: 261-275. https://doi.org/10.1111/j.1365-2400.2004.00401.x
  30. Mohamed, Z.A., W.W. Carmichael and A.A. Hussein. 2003. Estimation of microcystins in the freshwater fish Oreochromis niloticus in an Egyptian fish farm containing a Microcystis bloom. Environmental Toxicology 18: 137-141. https://doi.org/10.1002/tox.10111
  31. O'Farrell, I., P. de Tezanos Pinto, P. Rodriguez, G. Chaparro and H. Pizarro. 2009. Experimental evidence of the dynamic effect of free-floating plankts on phytoplankton ecology. Freshwater Biology 54: 363-375. https://doi.org/10.1111/j.1365-2427.2008.02117.x
  32. Ozimek, T., R.D. Gulati, E. van Donk. 1990. Can macrophytes be useful in biomanipulation of lakes? The lake Zwemlust example. Hydrobiologia 200/201: 399-407.
  33. Paine, R.T. 1969. A note on trophic complexity and community stability. The American Naturalist 103: 91-93. https://doi.org/10.1086/282586
  34. Park, S.K., I.K. Cho, O.B. Kwon, J.S. Mun, H.Y. Um and S.J. Hwang. 2008. Algae and nutrient removal by vegetated artificial floating island. Korean J Limnol 41(Special issue): 93-98.
  35. Parker, P.L., R.K. Anderson and A. Lawrence. 1989. A $\delta^{13}C$ and $\delta^{15}N$ tracer study of nutrition in aquaculture: Penaeus vannamei ni an pond growout system, p. 288-303. In: Stable Isotopes in Ecological Research (Rundel, P.W., J.R. Ehleringer and K.A. Nagy, eds.). Springer-Verlag, New York.
  36. Peterson, B.J. and B. Fry. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology, Evolution, and Systematics 18: 293-320. https://doi.org/10.1146/annurev.es.18.110187.001453
  37. Piola, R.F., I.M. Suthers and D. Rissik. 2008. Carbon and nitrogen stable isotope analysis indicates freshwater shrimp Paratya australiensis Kemp, 1917 (Atyidae) assimilate cyanobacterial accumulations. Hydrobiologia 608: 121-132. https://doi.org/10.1007/s10750-008-9374-4
  38. Roman, M.R., A.L. Gauzens, W.K. Rhinehart and J.P. White. 1993. Effects of low oxygen waters on Chesapeake bay zooplankton. Limnology and Oceanography 38: 1603-1614. https://doi.org/10.4319/lo.1993.38.8.1603
  39. Sarnelle, O. 1993. Herbivore effects on phytoplankton succession in a eutrophic lake. Ecological Monographs 63: 129-149. https://doi.org/10.2307/2937177
  40. Scheffer, M., S.H. Hospe, M.L. Meijer, B. Moss and E. Jeppesen. 1993. Alternative equilibria in shallow lakes. Trends in Ecology & Evolution 8: 275-279. https://doi.org/10.1016/0169-5347(93)90254-M
  41. Shapiro, J. and D.I. Wright. 1984. Lake restoration by biomanipulation. Freshwater Biology 14: 371-383. https://doi.org/10.1111/j.1365-2427.1984.tb00161.x
  42. Sipia V.O., H.T. Kankaanpaa, J. Flinkman, K. Lahti and J.A.O. Meriluoto. 2001. Time-dependent accumulation of cyanobacterial hepatotoxins in flounders (Platichthys flesus) and mussels (Mytilus edulis) from the northern Baltic Sea. Environmental Toxicology 16: 330-336. https://doi.org/10.1002/tox.1040
  43. Strand, J.A. and S.E.B. Weisner. 2001. Dynamics of submerged macrophyte populations in response to biomanipulation. Freshwater Biology 46: 1397-1408. https://doi.org/10.1046/j.1365-2427.2001.00746.x
  44. Strickland, J.D.H. and T.R. Parsons. 1972. A Pratical Handbook of Seawater Analysis. Journal of the Fisheries Research Board of Canada. (Bull.). p. 167-311.
  45. Tester, P.A., J.T. Turner and D. Shea. 2000. Vectorial transport of toxins from the dinoflagellate Gymnodinium breve through copepods to fish. Journal of Plankton Research 22: 47-61. https://doi.org/10.1093/plankt/22.1.47
  46. Van Donk, E., R.D. Gulati, A. Iedema and J. Meulemans. 1993. Macrophyte-related shifts in the nitrogen and phosphorus contents of the different trophic levels in a biomanipulated shallow lake. Hydrobiologia 251: 19-26. https://doi.org/10.1007/BF00007160
  47. Wium-Andersen, S., C. Christophersen and G. Houen. 1982. Allelopathic effects on phytoplankton by substances isolated from aquatic macrophytes (Charales). Oikos 39: 187-190. https://doi.org/10.2307/3544484
  48. Xie, P. and J.C. Liu. 2001. Practical success of biomanipulation using filter-feeding fish to control cyanobacteria blooms. Sci World 1: 337-356. https://doi.org/10.1100/tsw.2001.67