Advertisement

Hydrobiologia

, Volume 596, Issue 1, pp 251–267 | Cite as

Planktonic nitrogen fixation in Lake Malawi/Nyasa

  • Mangaliso J. Gondwe
  • Stephanie J. Guildford
  • Robert E. Hecky
Primary Research Paper

Abstract

Nitrogen (N2) fixation has been identified as possibly an important source of “new” nitrogen (N) to the epilimnion of Lake Malawi but studies in 1999–2000 and 2002 (September–December) estimated that the contribution of N2-fixation by heterocystous Anabaena filaments to the N budget of the lake’s epilimnion is only 3–4% of total N input. N2-fixation rates in Lake Malawi, as estimated by the acetylene reduction assay were higher during the stratified season (September–March) than during the rest of the year. Planktonic N2-fixation in Lake Malawi can be monitored by measuring heterocyst biovolume concentrations because a significant correlation (r 2 = 0.945, P < 0.0001) was observed between the two parameters. Heterocyst density cannot be used to estimate N2-fixation because heterocyst sizes in the lake change continuously as at least two Anabaena species with different heterocyst dimensions are present. During September–October 2002, a species similar to A. maxima, contained larger heterocysts (16.34 ± 2.46 and 13.25 ± 1.89 μm in cross and apical section dimensions, respectively). In November–December of 2002, A. discoidea dominated and had smaller sized heterocysts (8.92 ± 1.13 and 7.25 ± 0.95 μm in cross and apical section dimensions). Since planktonic N2-fixation is higher near shore than offshore, its contribution to the N budget in the littoral zone where high densities of grazing benthic fish occur may be more critical to maintaining the high rates of benthic algal productivity observed.

Keywords

Lake Malawi N2-fixation Heterocyst biovolume Littoral Pelagic 

Notes

Acknowledgements

This project was funded by the SADC/GEF Lake Malawi Biodiversity Conservation Project and by the Natural Sciences and Engineering Research Council of Canada (NSERC) through an individual research grant to Dr. Stephanie J. Guildford. The authors would like to sincerely thank Dr. Harvey Bootsma for his many contributions and support of this project when he was at the SADC/GEF Project and even after he moved to the University of Wisconsin, Milwaukee. We also thank Dr. Ralph E. Smith and Dr. Kistern Müller of the University of Waterloo also for their many contributions to the success of this project. We also thank the Director of the Department of Fisheries in Malawi for allowing us to use their facilities and equipment at Salima in 2002.

References

  1. Bootsma, H. A., R. E. Hecky, R. H. Hesslein & G. F. Turner, 1996. Food partitioning among Lake Malawi nearshore fishes as revealed by stable isotope analyses. Ecology. 77: 97–101.CrossRefGoogle Scholar
  2. Bootsma, H. A. & R. E. Hecky, 1999. Nutrient cycling in Lake Malawi/Nyasa. In Bootsma, H. A. & R. E. Hecky (eds), Water Quality Report: Lake Malawi/Nyasa Biodiversity Conservation Project, 215–241.Google Scholar
  3. Carr, N. G. & B. A. Whitton, 1982. The Biology of Cyanobacteria. Blackwell Scientific Publications, Oxford, 688 pp.Google Scholar
  4. Fay, P., 1981. Photosynthetic micro-organisms. In Broughton, W. J. (ed.), Nitrogen Fixation Volume 1: Ecology. Clarendon Press, Oxford, 1–29.Google Scholar
  5. Fee E. J., 1990. Computer programs for calculating in situ phytoplankton photosythesis. Canadian Technical Report of Fisheries and Aquatic Sciences 1740.Google Scholar
  6. Findlay, D. L., R. E. Hecky, L. L. Hendzel, M. P. Stainton & G. W. Regehr, 1994. Relationship between N2-fixation and heterocyst abundance and its relevance to the nitrogen budget of Lake 227. Canadian Journal of Fisheries and Aquatic Sciences 51: 2254–2266.Google Scholar
  7. Flett, R. J., R. D. Hamilton & N. E. Campbell, 1976. Aquatic acetylene reduction techniques: solutions to several problems. Canadian Journal of Microbiology 22: 43–51.PubMedCrossRefGoogle Scholar
  8. Flett, R. J., D. W. Schindler, R. D. Hamilton & N. E. R. Campbell, 1980. Nitrogen fixation in Canadian Precambrian Shield lakes. Canadian Journal of Fisheries and Aquatic Sciences. 37: 494–505.Google Scholar
  9. Flynn, K. J., 1991. Algal carbon-nitrogen metabolism: a biochemical basis for modelling the interactions between nitrate and ammonium uptake. Journal of Plankton Research 13: 373–387.CrossRefGoogle Scholar
  10. Fogg, G. E., 1974. Nitrogen fixation. In Stewart, W. D. P. (ed.), Algal Physiology and Biochemistry. Blackwell, Oxford, 560–582.Google Scholar
  11. Ganf, G. G. & R. L. Oliver, 1982. Vertical separation of light and available nutrients as a factor causing replacement of green algae by blue-green algae in the plankton of a stratified lake. Journal of Ecology 70: 829–844.CrossRefGoogle Scholar
  12. Gondwe, M. J., 2004. Planktonic and benthic N2-fixation in the sandy shores of Lake Malawi, Central Africa. MSc Thesis. University of Waterloo. Waterloo, Ontario, Canada, 157.Google Scholar
  13. Guildford, S. J., W. D. Taylor, H. A. Bootsma, L. L. Hendzel & L. Barlow-Busch, 1999. Factors controlling pelagic algal abundance and composition in Lake Malawi/Nyasa. In Bootsma, H. A. & R. E. Hecky (eds), Water Quality Report-Lake Malawi/Nyasa Biodiversity Conservation Project, 143–182.Google Scholar
  14. Guildford, S. J. & 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
  15. Guildford, S. J., H. A. Bootsma, E. J. Fee, R. E. Hecky & G. Patterson, 2000. Phytoplankton nutrient status and mean water column irradiance in Lakes Malawi and Superior. Aquatic Ecosystem Health and Management 3: 35–45.CrossRefGoogle Scholar
  16. Guildford, S. J., R. E. Hecky, W. D. Taylor, R. Mugidde & H. A. Bootsma, 2003. Nutrient enrichment experiments in tropical Great Lakes Malawi/Nyasa and Victoria. Journal of Great Lakes Research 29: 89–106.Google Scholar
  17. Guildford, S. J., H. A. Bootsma, W. D. Taylor, R. E. Hecky, 2007. High variability of phytoplankton photosynthesis in response to environmental forcing in oligotrophic Lake Malawi/Nyasa. Journal of Great Lakes Research 33: 170–185.Google Scholar
  18. Hansson, L.-A., 1992. Factors regulating periphytic algal biomass. Limnology and Oceanography 37: 322–328.Google Scholar
  19. Hardy, R. W. F., R. D. Holsten, E. K. Jackson & R. C. Burns, 1968. The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiology 43: 1185–1207.PubMedGoogle Scholar
  20. Hecky, R. E., H. A. Bootsma, R. Mugidde & F. W. B. Bungenyi, 1996. Phosphorus pumps, nitrogen sinks, and silicon drains: Plumbing nutrients in the African Great Lakes. In Johnson, T. C. & E. Odada (eds), The Limnology, Climatology and Paleolimnology of the East African Lakes. Gordon and Breach, Toronto, 205–224.Google Scholar
  21. Hecky, R. E., H. A. Bootsma & M. Kingdon, 2003. Impact of land use on sediment and nutrient yields of Lake Malawi/Nyasa (Africa). Journal of Great Lakes Research 29: 139–158.Google Scholar
  22. Hendzel, L. L., R. E. Hecky & D. L. Findlay, 1994. Recent changes of N2-fixation in Lake 227 in response to reduction of the N/P loading ratio. Canadian Journal of Fisheries and Aquatic Sciences 51: 2247–2253.Google Scholar
  23. Higgins, S. N., 1999. Epilithic nitrogen fixation in the rocky littoral zones of Lake Malawi, Africa. MSc Thesis. University of Waterloo. Waterloo, Ontario, Canada, 69.Google Scholar
  24. Higgins, S. N., R. E. Hecky & W. D. Taylor, 2001. Epilithic nitrogen fixation in the rocky littoral zones of Lake Malawi, Africa. Limnology and Oceanography 46: 976–982.CrossRefGoogle Scholar
  25. Hillebrand, H., C.-D. Durselen, D. Kirschtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.CrossRefGoogle Scholar
  26. Holl, C. M. & J. P. Montoya, 2005. Interactions between nitrate uptake and N2-fixation in Trichodesmium. Journal of Phycology 41: 1178–1183.CrossRefGoogle Scholar
  27. Horne, A. J. & G. E. Fogg, 1970. Nitrogen fixation in some English lakes. Proceedings of the Royal Society of London. Series B 175: 351–366.Google Scholar
  28. Horne, A. J. & C. R. Goldman, 1972. Nitrogen fixation in Clear Lake, California. 1. Seasonal variation and the role of heterocysts. Limnology and Oceanography 17: 678–692.Google Scholar
  29. Horne, A. J., J. E. Dillard, D. K. Fugita & C. R. Goldman, 1972. Nitrogen fixation in Clear Lake, California. II. Synoptic studies on the autumn Anabaena bloom. Limnology and Oceanography 17: 693–703.Google Scholar
  30. Howarth, R. W., R. Marino, J. Lane & J. J. Cole, 1988a. Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance. Limnology and Oceanography 33: 669–687.Google Scholar
  31. Howarth, R. W., R. Marino & J. J. Cole, 1988b. Nitrogen fixation in freshwater, estuarine and marine ecosystems. 2. Biogeochemical controls. Limnology and Oceanography 33: 688–701.CrossRefGoogle Scholar
  32. John C., Meeks J. C. & J. Elhai, 2002. Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiology and Molecular Biology Reviews 66: 94–121.CrossRefGoogle Scholar
  33. Konopka, A., T. D. Brock & A. E. Walsby, 1978. Buoyancy regulation by planktonic blue-green algae in Lake Mendota, Wisconsin. Archiv fur Hydrobiologie 83: 524–537.Google Scholar
  34. Lang, N. & P. Fay, 1971. The heterocysts of blue-green algae. 2. Details of ultrastructure. Proceedings of the Royal Society of London. Series B 178: 193–203.CrossRefGoogle Scholar
  35. Levine, S. N. & W. M. Lewis, 1985. The heterogeneity of nitrogen fixation in Lake Valencia, Venezuela. Limnology and Oceanography 30: 1240–1245.Google Scholar
  36. Levine, S. N. & W. M. Lewis, 1987. A numerical model of nitrogen fixation and its application to Lake Valencia, Venezuela. Freshwater Biology 17: 265–274.CrossRefGoogle Scholar
  37. Lomas M. W., P. M. Glibert, F.-K. Shiah & E. M. Smith, 2002. Microbial processes and temperature in Chesapeake Bay: current relationships and potential impacts of regional warming. Global Change Biology 8: 51–70.CrossRefGoogle Scholar
  38. Lund, J. W. G., C. Kipling & E. D. Le Cren, 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11: 143–170.CrossRefGoogle Scholar
  39. Moisander, P. H., J. L. Hench, K. Kononen & H. W. Paerl, 2002. Small-scale shear effects on heterocystous cyanobacteria. Limnology and Oceanography 47: 108–119.CrossRefGoogle Scholar
  40. Mugidde, R., R. E. Hecky, L. L. Hendzel & W. D. Taylor, 2003. Pelagic nitrogen fixation in Lake Victoria (East Africa). Journal of Great Lakes Research 29: 76–88.Google Scholar
  41. Mugidde, R., 2001. Nutrient status and planktonic nitrogen fixation in Lake Victoria, Africa. Ph.D. Thesis, University of Waterloo, Waterloo, Ontario, Canada, 196.Google Scholar
  42. Nicholls, K. H., L. Heintsch, E. Carney, J. Beaver & D. Middleton, 1986. Some effects of phosphorus loading reductions on phytoplankton in the Bay of Quinte, Lake Ontario. In Minns, C. K., D. A. Hurley & K. H. Nicholls (eds), Project Quinte: Point source phosphorus control and ecosystem response in the Bay of Quinte, Lake Ontario. Canadian Special Publication of Fisheries and Aquatic Sciences 86, 145–158.Google Scholar
  43. Paerl, H. W., P. T. Bland, 1982. Localised tetrazolium reduction in relation to N2 fixation, CO2 fixation and H2 uptake in aquatic filamentous cyanobacteria. Applied and Environmental Microbiology 43: 218–226.PubMedGoogle Scholar
  44. Paerl, H. W., 1988. Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnology and Oceanography 33: 823–847.Google Scholar
  45. Paerl, H. W., 1996. A comparison of cyanobacterial bloom dynamics in freshwater, estuarine and marine environments. Phycologia 35: 25–35.CrossRefGoogle Scholar
  46. Patterson, G. & O. Kachinjika, 1993. Effects of wind-induced mixing on the vertical distribution of nutrients and phytoplankton in Lake Malawi. Proceedings-International Association of Theoretical and Applied Limnology 25: 872–876.Google Scholar
  47. Patterson, G. & O. Kachinjika, 1995. Limnology and phytoplankton ecology. In Menz, A (ed.), The Fishery Potential and Ecology of the Pelagic Zone of Lake Malawi/Niassa. Natural Resources Institute, Chatham, Kent, UK, 1–67.Google Scholar
  48. Reynolds, C. S. & A. E. Walsby, 1975. Water blooms. Biological Reviews 50: 437–481.Google Scholar
  49. Reynolds, C. S., 1987. Cyanobacterial water-blooms. Advances in Botanical Research 13: 67–143.Google Scholar
  50. Ribbink, A. J., B. A. Marsh, A. C. Marsh, A. C. Ribbink & B. J. Sharp, 1983. A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi. South African Journal of Zoology 18: 149–310.Google Scholar
  51. Smith, V. H., 1985. Predictive models for the biomass of blue-green algae in lakes. Water Resources Bulletin 21: 433–439.Google Scholar
  52. Snoeks, J., 2000. How well known is the ichthyodiversity of large East African lakes? Advances in Ecological Research 31: 17–38.CrossRefGoogle Scholar
  53. Stewart, W. D. P., G. P. Fitzgerald & R. H. Burris, 1967. In situ studies on N2-fixation using the acetylene reduction technique. Proceedings of the National Academy of Science USA 58: 2071–2078.CrossRefGoogle Scholar
  54. Stewart, W. D. P., 1973. Nitrogen fixation by photosynthetic microorganisms. Annual Reviews of Microbiology 27: 283–316.CrossRefGoogle Scholar
  55. Thiel, T & B. Pratte, 2001. Effects of heterocysts differentiation of nitrogen fixation in vegetative cells of the cyanobaterium Anabaena variabilis ATCC 29413. Journal of Bacteriology 183: 280–286.PubMedCrossRefGoogle Scholar
  56. Walsby, A. E., 1994. Gas vesicles. Microbiology and Molecular Biology Reviews 58: 94–144.Google Scholar
  57. Wetzel, R., 1983. Attached algal-substrata interactions: fact or myth, and when and how? In Wetzel, R. (ed.), Periphyton of Freshwater Ecosystems. Dr W. Junk Publishers, The Hague, Netherlands, 207–215.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Mangaliso J. Gondwe
    • 1
    • 2
  • Stephanie J. Guildford
    • 2
  • Robert E. Hecky
    • 2
  1. 1.SADC/GEF Lake Malawi Biodiversity Conservation ProjectSalimaMalawi
  2. 2.Department of BiologyUniversity of WaterlooWaterlooCanada

Personalised recommendations