Estuaries and Coasts

, Volume 32, Issue 5, pp 958–974 | Cite as

Nutrient Limitation on Phytoplankton Growth in the Upper Barataria Basin, Louisiana: Microcosm Bioassays

  • Ling Ren
  • Nancy N. Rabalais
  • R. Eugene Turner
  • Wendy Morrison
  • Warren Mendenhall
Article

Abstract

The Davis Pond Diversion (DPD) was constructed to divert Mississippi River (MR) water into the Barataria Basin to reduce the salinity in support of wetland restoration on the Louisiana coast. To assess the phytoplankton nutrient limitation in adjacent water systems and potential impacts of DPD, 12 seasonal nutrient-phytoplankton bioassay experiments were conducted from October 2003 to July 2004 using the natural phytoplankton assemblages from freshwater and brackish-water lakes, Cataouatche and Salvador, LA (USA), which receive Mississippi River water from the DPD, and from a nearby freshwater lake, Lac des Allemands, that does not. Dissolved inorganic nitrogen (N), phosphorus (P), and silicate (Si) were added with different combinations at Redfield ratios in 10-l microcosms. Nitrogen was found to be the sole or primary limiting nutrient in all 12 experiments. N and P colimitations were found in seven of 12 experiments, but N was always the stronger limiting factor. P limitation was never observed to be the sole limiting nutrient. The results showed that a low concentration of P and a relatively high concentration of N do not necessarily indicate only P limitation in these lakes. Lake Cataouatche and Lake Salvador were dominated by centric diatoms, and Anabaena spp. were detected at high levels, particularly in summer. Lac des Allemands was generally dominated by N-fixing Anabaena spp. and other cyanobacteria, and their biomass responded significantly to N addition but not to P addition, indicating that nitrogen fixation in Lac des Allemands may be inhibited by other factors such as iron. Our bioassay results demonstrate that whether a water body is N- or P-limited is the consequence of the nutrient status and not the salinity regime. The results suggest that the addition of nutrient-rich waters via diversions of Mississippi River water into these lakes might increase the frequency of algal blooms, including noxious and toxic freshwater cyanobacteria.

Keywords

Nutrient limitation Microcosm bioassays Phytoplankton growth Cyanobacteria Harmful algal blooms Barataria estuary Eutrophication Mississippi River 

References

  1. Bode, A. and Q. Dortch. 1996. Uptake and regeneration of inorganic nitrogen in coastal waters influenced by the Mississippi River: Spatial and seasonal variations. Journal of Plankton Research 18: 2251–2268. doi:10.1093/plankt/18.12.2251.CrossRefGoogle Scholar
  2. Boesch, D.F., M.N. Josselyn, A.J. Mehta, J.T. Morris, W.K. Nuttle, C.A. Simenstad, and D.J.P. Swift. 1994. Scientific assessment of coastal wetland loss, restoration and management in Louisiana. Journal of Coastal Research 20: 1–103. Special Issue.Google Scholar
  3. Carlson, R.E. 1977. A trophic state index for lakes. Limnology and Oceanography 22: 361–369.Google Scholar
  4. Chorus, I. and J. Bartram (eds). 1999. Toxic Cyanobacteria in Water. A Guide to Their Public Health Consequences, Monitoring and Management, 407. London: E & FN Spon (an imprint of Routledge).Google Scholar
  5. Conley, D.J., H.W. Paerl, R.W. Howarth, D.F. Boesch, S.P. Seitzinger, K.E. Havens, C. Lancelot, and G.E. Likens. 2009. Controlling eutrophication: Nitrogen and phosphorus. Science 323: 1014–1015. doi:10.1126/science.1167755.CrossRefGoogle Scholar
  6. Connors, S.D., M.T. Auer, and S.W. Effler. 1996. Phosphorus pools, alkaline phosphatase activity, and phosphorus limitation in hypereutrophic Onondaga Lake. Lake and Reservoir Management 12: 47–57.CrossRefGoogle Scholar
  7. Diaz, M.M. and F.L. Pedrozo. 1996. Nutrient limitation in Andean-Patagonian Lake at latitude 40–41°S. Archiv für Hydrobiologie 138: 123–143.Google Scholar
  8. Dodds, W.K. 2003. The misuse of inorganic N and soluble reactive P to indicate nutrient status of surface waters. Journal of the North American Benthological Society 22: 171–181. doi:10.2307/1467990.CrossRefGoogle Scholar
  9. Dodds, W.K. 2006. Nutrients and the “dead zone”: The link between nutrient ratios and dissolved oxygen in the northern Gulf of Mexico. Frontiers in Ecology and the Environment 4: 211–217. doi:10.1890/1540-9295(2006)004[0211:NATDZT]2.0.CO;2.CrossRefGoogle Scholar
  10. Dodds, W.K., A.J. López, W.B. Bowden, S. Gregory, N.B. Grimm, S.K. Hamilton, A.E. Hershey, E. Martí, W.B. McDowell, J.L. Meyer, D. Morrall, P.J. Mulholland, B.J. Peterson, J.L. Tank, H.M. Vallet, J.R. Webster, and W. Wollheim. 2002. N uptake as a function of concentration in streams. Journal of the North American Benthological Society 21: 206–220. doi:10.2307/1468410.CrossRefGoogle Scholar
  11. Dortch, Q. and T.E. Whitledge. 1992. Does nitrogen or silicon limit phytoplankton production in the Mississippi River plume and nearby regions? Continental Shelf Research 12: 1293–1309. doi:10.1016/0278-4343(92)90065-R.CrossRefGoogle Scholar
  12. Dortch, Q., R. Robichaux, S. Pool, D. Milsted, G. Mire, N.N. Rabalais, T.M. Soniat, G.A. Fryxell, R.E. Turner, and M.L. Parsons. 1997. Abundance and vertical flux of Pseudo-nitzschia in the northern Gulf of Mexico. Marine Ecology Progress Series 146: 249–264. doi:10.3354/meps146249.CrossRefGoogle Scholar
  13. Dortch, Q., M.L. Parson, N.N. Rabalais, and R.E. Turner. 1999. What is the threat of harmful algal blooms in Louisiana coastal waters. In Recent Research in Coastal Louisiana, 3–5 Feb. 1998, ed. L.O. Rozas, J.A. Nyman, C.E. Proffitt, N.N. Rabalais, D.J. Reed, and R.E. Turner, 134–144. Lafayette: Louisiana Sea Grant.Google Scholar
  14. Dzialowski, A.R., S.H. Wang, N.C. Lim, W.W. Spotts, and D.G. Huggins. 2005. Nutrient limitation of phytoplankton growth in central plains reservoirs, USA. Journal of Plankton Research 27: 587–595. doi:10.1093/plankt/fbi034.CrossRefGoogle Scholar
  15. Elmgren, R. 2001. Understanding human impact on the Baltic ecosystem: Changing view in recent decades. Ambio 30: 222–231.Google Scholar
  16. Elser, J.J., E.R. Marzolf, and C.R. Goldman. 1990. Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America: A review and critique of experimental enrichments. Canadian Journal of Fisheries and Aquatic Science 47: 1468–1477.Google Scholar
  17. Falkwoski, P.G. 1997. Evolution of the nitrogen cycle and its influence of the biological sequestration of CO2 in the ocean. Nature 387: 272–275. doi:10.1038/387272a0.CrossRefGoogle Scholar
  18. Fisher, T.R., J.M. Melack, J.U. Brobbelaar, and R.W. Howarth. 1995. Nutrient limitation of phytoplankton and eutrophication of inland, estuarine, and marine waters. In Phosphorus in the Global Environment, ed. H. Tiessen, 301–322. Chichester: Wiley.Google Scholar
  19. Fu, F.-X., Y. Zhang, S.A. Sanudo-Wilhelmy, and D.A. Hutchins. 2005. The biological and biogeochemical consequences of phosphate scavenging on phytoplankton cell surfaces. Limnology and Oceanography 50: 1459–1472.Google Scholar
  20. Fujiki, T., T. Toda, T. Kikuchi, H. Aono, and A.N.D.S. Taguchi. 2004. Phosphorus limitation of primary productivity during the spring–summer blooms in Sagami Bay, Japan. Marine Ecology Progress Series 283: 29–38. doi:10.3354/meps283029.CrossRefGoogle Scholar
  21. Gobler, C.J., N.J. Buck, M.E. Sieracki, and S.A. Sañudo-Wilhelmy. 2006. Nitrogen and silicon limitation of phytoplankton communities across an urban estuary: The East River-Long Island Sound system. Estuarine Coastal and Shelf Science 68: 127–138. doi:10.1016/j.ecss.2006.02.001.CrossRefGoogle Scholar
  22. Groeger, A.W. 2007. Nutrient limitation in Crater Lake, Oregon. Hydrobiologia 574: 205–216. doi:10.1007/s10750-006-0353-3.CrossRefGoogle Scholar
  23. Guildford, S.J. and R.E. Hecky. 2000. Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: Is there a common relationship? Limnology and Oceanography 45: 1213–1223.CrossRefGoogle Scholar
  24. Havens, K.E., E.J. Philips, M.F. Cichra, and B.L. Li. 1998. Light availability as a possible regulator of cyanobacteria species composition in a shallow subtropical lake. Freshwater Biology 39: 547–556. doi:10.1046/j.1365-2427.1998.00308.x.CrossRefGoogle Scholar
  25. Hecky, R.E. and P. Kilham. 1988. Nutrient limitation of phytoplankton in freshwater and marine environments: A review of recent evidence on the effects of enrichments. Limnology and Oceanography 33: 796–822.CrossRefGoogle Scholar
  26. Hillebrand, H., C.D. Dürselen, D. Kirschtel, U. Pollingher, and T. Zohary. 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424. doi:10.1046/j.1529-8817.1999.3520403.x.CrossRefGoogle Scholar
  27. Howarth, R.W., R. Marino, and J. Lane. 1988. Nitrogen fixation in freshwater, estuarine and marine ecosystems. 1. Rates and importance. Limnology and Oceanography 33: 669–687.Google Scholar
  28. Hyenstrand, P., E. Rydin, and M. Gunnerhed. 1999. Response of pelagic cyanobacteria to iron additions—enclosure experiment from Lake Erken. Journal of Plankton Research 22: 1113–1126. doi:10.1093/plankt/22.6.1113.CrossRefGoogle Scholar
  29. SAS Institute Incorporated. 2003. The SAS system for Windows, version 9.1. Cary, North Carolina, USA.Google Scholar
  30. Istvanovics, V., J. Padisak, K. Pettersson, and D.C. Pierson. 1994. Growth and phosphorus uptake of summer phytoplankton in Lake Erken (Sweden). Journal of Plankton Research 16: 1167–1196. doi:10.1093/plankt/16.9.1167.CrossRefGoogle Scholar
  31. James, C., J. Fisher, and B. Moss. 2003. Nitrogen driven lakes: The Shropshire and Cheshire Meres? Archiv für Hydrobiologie 158: 249–266. doi:10.1127/0003-9136/2003/0158-0249.CrossRefGoogle Scholar
  32. Klug, J.L. 2006. Nutrient limitation in the Lower Housatonic River Estuary. Estuaries and Coast 29: 831–840.Google Scholar
  33. Lee, D.Y. and G.Y. Rhee. 1999. Kinetics of growth and death in Anabaena flos-aquae (cyanobacteria) under light limitation and supersaturation. Journal of Phycology 35: 700–709. doi:10.1046/j.1529-8817.1999.3540700.x.CrossRefGoogle Scholar
  34. Levine, S.N. and D.W. Schindler. 1999. Influence of nitrogen to phosphorus supply ratios and physicochemical conditions on cyanobacteria and phytoplankton species composition in the Experimental Lake Area, Canada. Canadian Journal of Fishery and Aquatic Science 56: 451–466. doi:10.1139/cjfas-56-3-451.CrossRefGoogle Scholar
  35. Levine, M.A. and S.C. Whalen. 2001. Nutrient limitation of phytoplankton production in Alaskan Arctic foothill lakes. Hydrobiologia 455: 189–201. doi:10.1023/A:1011954221491.CrossRefGoogle Scholar
  36. Lohrenz, S.E., G.L. Fahnenstiel, D.G. Redalje, G.A. Lang, M.J. Dagg, T.E. Whitledge, and Q. Dortch. 1999. Nutrient, irradiance, and mixing as factors regulating primary production in coastal waters impacted by the Mississippi River plume. Continental Shelf Research 19: 1113–1141. doi:10.1016/S0278-4343(99)00012-6.CrossRefGoogle Scholar
  37. Maberly, S.C., L. King, M.M. Dent, R.I. Jones, and C.E. Gibson. 2002. Nutrient limitation of phytoplankton and periphyton growth in upland lakes. Freshwater Biology 47: 2136–2152. doi:10.1046/j.1365-2427.2002.00962.x.CrossRefGoogle Scholar
  38. Madden, C.R., J.W. Day Jr., and J.M. Randall. 1988. Freshwater and marine coupling in estuaries of the Mississippi River deltaic plain. Limnology and Oceanography 33: 982–1004.CrossRefGoogle Scholar
  39. Maestrini, S.Y., M. Rochet, L. Legendre, and S. Demers. 1986. Nutrient limitation of the bottom-ice microalgal biomass (southeastern Hudson Bay, Canadian Arctic). Limnology and Oceanography 31: 969–982.Google Scholar
  40. Mateo, P., I. Douterelo, E. Berrendero, and E. Perona. 2006. Physiological differences between two species of cyanobacteria in relation to phosphorus limitation. Journal of Phycology 42: 61–66. doi:10.1111/j.1529-8817.2006.00180.x.CrossRefGoogle Scholar
  41. Morton, T. A., J. C. Bernier, J. A. Barras, and N. F. Ferina. 2005. Rapid subsidence and historical wetland loss in the Mississippi Delta Plain: Likely causes and future implications. USGS Open-File Report 2005-1215.Google Scholar
  42. Nelson, D.M. and Q. Dortch. 1996. Silicic acid depletion and silicon limitation in the plume of the Mississippi River: Evidence from kinetic studies in spring and summer. Marine Ecology Progress Series 136: 163–178. doi:10.3354/meps136163.CrossRefGoogle Scholar
  43. Nürnberg, G.K. 1988. Prediction of phosphorus release rates from total and reductant soluble phosphorus in anoxic lake sediments. Canadian Journal of Fishery and Aquatic Science 45: 574–580. doi:10.1139/f88-054.CrossRefGoogle Scholar
  44. Paerl, H.W., L. Valdes, A.R. Joyner, M. Piehler, and M.E. Lebo. 2004. Solving problems resulting from solutions: Evolution of a dual nutrient management strategy for the eutrophying Neuse River Estuary, North Carolina. Environmental Science and Technology 38: 3068–3074. doi:10.1021/es0352350.CrossRefGoogle Scholar
  45. Parslow, J.S., P.J. Harrison, and P.A. Thompson. 1984. Saturated uptake kinetics: Transient response of the marine diatom Thalassiosira pseudonana to ammonium, nitrate, silicate or phosphate starvation. Marine Biology 83: 51–59. doi:10.1007/BF00393085.CrossRefGoogle Scholar
  46. Parsons, T.R. 1982. The future of controlled ecosystem enclosure experiments. In Marine Mesocosms. Biological and Chemical Research in Experimental Ecosystems, ed. G.D. Grice and M.R. Reeve, 411–418. New York: Springer.Google Scholar
  47. Parsons, T.R., Y. Maita, and M. Lalli. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis, 173. New York: Pergamon.Google Scholar
  48. Peeters, J.C.H. and L. Peperzak. 1990. Nutrient limitation in the North Sea: A bioassay approach. Netherlands Journal of Sea Research 26: 61–73.CrossRefGoogle Scholar
  49. Portielje, R. and L. Lijklema. 1994. Kinetics of luxury uptake of phosphate by algae-dominated benthic communities. Hydrobiologia 275(276): 349–358.CrossRefGoogle Scholar
  50. Postgate, J. 1998. Nitrogen Fixation, 3rd ed. Cambridge: Cambridge University Press.Google Scholar
  51. Rabalais, N.N. 2002. Nitrogen in aquatic ecosystems. Ambio 31: 102–112.Google Scholar
  52. Redfield, A.C. 1958. The biological control of chemical factors in the environment. American Scientist 46: 205–221.Google Scholar
  53. Ren, L. 2002. Biogeochemical conversion of nitrogen in enclosed pelagic coastal ecosystems of the German Bight: Mesocosm and modeling studies. University Hamburg, http://www.sub.uni-hamburg.de/disse/775/dissertation.pdf.
  54. Reynolds, C.S. 1993. The Ecology of Freshwater Phytoplankton, 384. Cambridge: Cambridge University Press.Google Scholar
  55. Riegman, R., F. Colijn, J.F.P. Malschaert, H.T. Kloosterhuis, and G.C. Cadée. 1990. Assessment of growth rate limiting nutrients in the North Sea by the use of nutrient-uptake kinetics. Netherlands Journal of Sea Research 26: 53–60. doi:10.1016/0077-7579(90)90055-L.CrossRefGoogle Scholar
  56. Sanudo-Wilhelmy, S.A., A. Tovar-Sanchez, F.X. Fu, D.G. Capone, E.J. Carpenter, and D.A. Hutchins. 2004. The impact of surface-adsorbed phosphorus on phytoplankton Redfield stoichiometry. Nature 432: 897–901. doi:10.1038/nature03125.CrossRefGoogle Scholar
  57. Schindler, D.W. 1977. Evolution of phosphorus limitation in lakes. Science 195: 260–262. doi:10.1126/science.195.4275.260.CrossRefGoogle Scholar
  58. Schindler, D.W., R.E. Hecky, D.L. Findlay, M.P. Stainton, B.R. Parker, M.J. Paterson, K.G. Beaty, M. Lyng, and S.E.M. Kasians. 2008. Eutrophication of lakes cannot be controlled by reducing nitrogen input: Results of a 37-year whole-ecosystem experiment. Proceedings of the National Academy of Sciences USA 105: 11254–11258. doi:10.1073/pnas.0805108105.CrossRefGoogle Scholar
  59. Swenson, E.M., J.E. Cable, B. Fry, D. Justić, A. Das, G. Snedden, and C. Swarzenski. 2006. Estuarine flushing times influenced by freshwater diversions. In Coastal Hydrology and Processes. Proceedings of the AIH 25th anniversary meeting & international conference “Challenges in coastal hydrology and water quality”, ed. V.P. Singh and Y.J. Xu, 403–413. Highlands Ranch: Water Resources.Google Scholar
  60. Sylvan, J.B., Q. Dortch, D.M. Nelson, A.F.M. Brown, W. Morrision, and J.W. Ammerman. 2006. Phosphorus limits phytoplankton growth on the Louisiana shelf during the period of hypoxia formation. Environmental Science and Technology 40: 7548–7553. doi:10.1021/es061417t.CrossRefGoogle Scholar
  61. Teaumroong, N. and S. Innok. 2002. Diversity of nitrogen-fixing cyanobacteria under various ecosystems of Thailand: 1. Morphology, physiology and genetic diversity. World Journal of Microbiology and Biotechnology 18: 673–682. doi:10.1023/A:1016812116538.CrossRefGoogle Scholar
  62. Tilzer, M.M. 1988. Secchi disk–chlorophyll relationships in a lake with highly variable phytoplankton biomass. Hydobiologia 162: 163–171. doi:10.1007/BF00014539.CrossRefGoogle Scholar
  63. Turner, R.E., N.N. Rabalais, and Z.N. Chang. 1990. Phytoplankton biomass, production and growth limitations on the Huanghe (Yellow River) continental shelf. Continental Shelf Research 10: 545–571. doi:10.1016/0278-4343(90)90081-V.CrossRefGoogle Scholar
  64. Turner, R.E., Q. Dortch, and N.N. Rabalais. 2004. Inorganic nitrogen transformations at high loading rates in an oligohaline estuary. Biogeochemistry 68: 411–423. doi:10.1023/B:BIOG.0000031039.56794.29.CrossRefGoogle Scholar
  65. Turner, R.E., N.N. Rabalais, R.B. Alexander, G. McIsaac, and R.W. Howarth. 2007. Characterization of nutrient and organic carbon and sediment loads and concentrations from the Mississippi River into the northern Gulf of Mexico. Estuaries and Coasts 30: 773–790.Google Scholar
  66. Tyrrell, P. 1999. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400: 525–531. doi:10.1038/22941.CrossRefGoogle Scholar
  67. Vahtera, E., M. Laamanen, and J.-M. Rintala. 2007. Use of different phosphorus sources by bloom-forming cyanobacteria Aphanizomenon flos-aquae and Nodularia spumigena. Aquatic Microbial Ecology 46: 225–237. doi:10.3354/ame046225.CrossRefGoogle Scholar
  68. Walsby, A.E., P.K. Hayes, R. Boje, and L.J. Stal. 1997. The selective advantage of buoyancy provided by gas vesicles for planktonic cyanobacteria in the Baltic Sea. The New Phytologist 136: 407–417. doi:10.1046/j.1469-8137.1997.00754.x.CrossRefGoogle Scholar
  69. Wang, S., A. R. Dzialowski, W. W. Spotts, N. C. Lim, and D. G. Huggins. 2005. Variability of nutrient limitation on phytoplankton growth in small and medium Kansas lakes. Kansas Biological Survey Open-File Report No. 120.Google Scholar
  70. Wilkerson, F.P., R.C. Dugdale, F.P. Chavez, and R.M. Kudela. 2000. Biomass and productivity in Monterey Bay, CA: Contribution of the larger autotrophs. Deep Sea Research II 47: 1003–1022. doi:10.1016/S0967-0645(99)00134-4.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2009

Authors and Affiliations

  • Ling Ren
    • 1
    • 3
  • Nancy N. Rabalais
    • 1
  • R. Eugene Turner
    • 2
  • Wendy Morrison
    • 1
  • Warren Mendenhall
    • 1
  1. 1.Louisiana Universities Marine ConsortiumChauvinUSA
  2. 2.Dept of Oceanography and Coastal SciencesLouisiana State UniversityBaton RougeUSA
  3. 3.Patrick Center for Environmental ResearchAcademy of Natural SciencesPhiladelphiaUSA

Personalised recommendations