, Volume 250, Issue 2, pp 105–117 | Cite as

Seasonal pattern of ammonium (methylamine) uptake by phytoplankton in an oligotrophic lake

  • Marolyn J. Parson
  • Bruce C. Parker


Our primary objective was to determine if a relationship existed between seasonal change in phytoplankton and high affinity for (Km) or uptake rates (VmaX) of ammonium which might explain seasonal phytoplankton succession in oligotrophic ecosystems. We measured ammonium uptake using [14C]-methylamine and estimatedKm andVmax using Hanes Plots at 2-week intervals during 6 months of thermal stratification in Mountain lake, Virginia (37° 22′ N, 80° 32′ W). Community composition, nutrient levels, and other variables were determined in all uptake experiments. A second objective was to determine if ammonium was preferentially utilized over nitrate and to characterize further the ammonium transport system.Vmax increased steadily from May until the end of July, each increase coinciding with major changes in the phytoplankton community. Cryptophyceans dominated in May, chlorophyceans in June and July, and cyanophyceans from the end of July to late October. With cyanophycean dominance,Vmax declined until chlorophyceans reestablished dominance in late October. By contrast,Km values increased from May to the end of July, but thereafter showed no correlation. Acetylene reduction experiments showed no nitrogen fixation during late summer and fall when blue-green algae were present. Preference for ammonium was implied also by negative nitrate reductase assays. Overall, the coincidence ofVmax andKm values for [14C]-methylamine uptake and changing phytoplankton community structure suggests the possibility that successive algal communities may be changing as a result of specific species differences in ammonium affinity and uptake rates.

Key words

ammonium lake methylamine phytoplankton seasonal succession 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. American Public Health Association, American Water Works Association and Water Pollution Control Federation (APHA), 1985. Standard methods for the examination of water and wastewater, 16th edn. Washington, D.C. 1268 pp.Google Scholar
  2. Axler, R. P., G. W. Redfield & C. R. Goldman, 1981. The importance of regenerated nitrogen to phytoplankton productivity in a subalpine lake. Ecology 62: 345–354.Google Scholar
  3. Balch, W. M., 1985. Lack of an effect of light on methylamine uptake by phytoplankton. Limnol. Oceanogr. 30: 665–674.Google Scholar
  4. Barnes, E. M., Jr., P. Zimmiak & A. Jayakumar, 1983. Role of glutamine synthetase in the uptake and metabolism of methylammonium byAzotobacter vinelandii. J. Bact. 156: 752–757.Google Scholar
  5. Berman, T., B. F. Sherr, E. Sherr, D. Wynne & J. J. McCarthy, 1984. The characteristics of ammonium and nitrate uptake by phytoplankton in Lake Kinneret. Limnol. Oceanogr. 29: 287–297.Google Scholar
  6. Boussiba, S., W. Dilling & J. Gibson, 1984. Methylammonium transport inAnacystis nidulans R-2. J. Bact. 160: 204–210.Google Scholar
  7. Brook, A. J., 1959. The waterbloom problem. Proc. Soc. Water Treat. Exam. 8: 133–137.Google Scholar
  8. Brower, J. E. & J. H. Zar, 1984. Field and laboratory methods for general biology. Wm. C. Brown Publishers, Dubuque, Iowa. 226 pp.Google Scholar
  9. Cochlan, W. P. & P. J. Harrison, 1991. Uptake of nitrate, ammonium, and urea by nitrogen-starved cultures ofMicromonas pusilla (Prasinophyceae): transient responses. J. Phycol. 27: 673–679.Google Scholar
  10. Dodds, W. K. & J. C. Priscu, 1989. Ammonium, nitrate, phosphate, and inorganic carbon uptake in an oligotrophic lake: seasonal variations among light response variables. J. Phycol. 25: 699–705.Google Scholar
  11. Eppley, R. W., 1978. Nitrate reductase in marine phytoplankton. In J. A. Hellebust & J. S. Craigie (eds), Handbook of Phycological Methods: Physiological and Biochemical Methods. Cambridge University Press, New York: 217–232.Google Scholar
  12. Eppley, R. W. & E. H. Renger, 1974. Nitrogen assimilation of an oceanic diatom in nitrogen-limited continuous culture. J. Phycol. 10: 15–23.Google Scholar
  13. Eppley, R. W. & J. N. Rogers, 1970. Inorganic nitrogen assimilation ofDitylum brightwellii a marine plankton diatom. J. Phycol. 6: 344–351.Google Scholar
  14. Eppley, R. W., J. L. Coatsworth & L. Solorzano, 1969a. Studies of nitrate reductase in marine phytoplankton. Limnol. Oceanogr. 14: 194–205.Google Scholar
  15. Eppley, R. W., J. N. Rogers & J. J. McCarthy, 1969b. Half-saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnol. Oceanogr. 14: 912–920.Google Scholar
  16. Eppley, R. W., T. T. Packard & J. J. Maclsaac, 1970. Nitrate reductase in Peru current phytoplankton. Mar. Biol. (Berl.) 6: 195–199.Google Scholar
  17. Fuhs, G. W., S. D. Demmerle, E. Canelli & M. Chen, 1972. Characterization of phosphorus-limited algae (with reflections on the limiting nutrient concept). Am. Soc. Limnol. Oceanogr. Spec. Symp. 1: 113–120.Google Scholar
  18. Goldman, J. C., J. J. McCarthy & D. G. Peavey, 1979. Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279: 210–215.Google Scholar
  19. Healey, F. P. & L. L. Hendzel, 1979. Indicators of phosphorus and nitrogen deficiency in five algae in culture. J. Fish. Res. Bd Can. 36: 1364–1369.Google Scholar
  20. Hellebust, J. A., C. Sotto & T. C. Hutchinson, 1985. The effect of naphthalene and aqueous crude-oil extracts on the green flagellateClamydomonas angulosa. VII. nitrate and methylamine uptake and retention. Can. J. Bot. 63: 834–840.Google Scholar
  21. Horne, A. J. & G. E. Fogg, 1970. Nitrogen fixation in some English lakes. Proc. R. Soc. B. 175: 351–366.Google Scholar
  22. Kleiner, D. & E. Fitzke, 1981. Some properties of new electrogenic transport system: the ammonium (methylammonium) carrier fromClostridium pasteurianum. Biochim. Biophys. Acta 641: 138–147.Google Scholar
  23. Koike, I., D. G. Redalje, J. W. Ammerman & O. Holm-Hansen, 1983. High-affinity uptake by an ammonium analogue by two marine microflagellates from the oligotrophic Pacific. Mar. Biol. 74: 161–168.Google Scholar
  24. Kristiansen, S., 1983. The temperature optimum of the nitrate reductase assay for marine phytoplankton. Limnol. Oceanogr. 28: 776–780.Google Scholar
  25. Lange, W., 1971. Limiting nutrient elements in filtered Lake Erie water. Wat. Res. 5: 1031–1048.Google Scholar
  26. La Roche, J., 1983. Ammonium regeneration: its contribution to phytoplankton nitrogen requirements in a eutrophic environment. Mar. Biol. 73: 231–240.Google Scholar
  27. La Roche, J. & W. G. Harrison, 1989. Reversible kinetic model for the short-term regulation of methylammonium uptake in two phytoplankton species,Dunaliella tertiolecta (Chlorophyceae) andPhaeodactylum tricornutum (Bacillariophyceae). J. Phycol. 25: 36–48.Google Scholar
  28. MacIsaac, J. J. & R. C. Dugdale, 1969. The kinetics of nitrate and ammonium uptake by natural populations of marine phytoplankton. Deep Sea Res. 16: 45–57.Google Scholar
  29. Mague, T. H., 1978. Nitrogen fixation. In J. A. Hellebust & J. S. Craigie (eds), Handbook of Phycological Methods: Physiological and Biochemical Methods. Cambridge University Press, New York: 369–372.Google Scholar
  30. Mazzucco, C. E. & D. R. Benson, 1984. [14C] methylammonium transport byFrankia sp. strain Cpll. J. Bact. 160: 636–641.Google Scholar
  31. McCarthy, J. J. & J. C. Goldman, 1979. Nitrogenous nutrition of marine phytoplankton in nutrient-depleted water. Science 203: 670–672.Google Scholar
  32. McCarthy, J. J., W. R. Taylor & J. L. Taft, 1977. Nitrogenous nutrition of the plankton in the Chesapeake Bay; 1. nutrient availability and phytoplankton preferences. Limnol. Oceanogr. 22: 996–1011.Google Scholar
  33. Munawar, M. & N. M. Burns, 1976. Relationships of phytoplankton biomass with soluble nutrients, primary production, and chlorophylla in Lake Erie. J. Fish. Res. Bd Can. 33: 601–611.Google Scholar
  34. Murphy, T. P., 1980. Ammonium and nitrate uptake in the lower Great Lakes. Can. J. Fish. aquat. Sci. 37: 1365–1372.Google Scholar
  35. Myers, J., 1951. Physiology of the algae. Annu. Rev. Microbiol. 5: 157–180.Google Scholar
  36. Parker, B. C., L. J. Wenkert & M. J. Parson, 1991. Cause of the metalimnetic oxygen maximum in Mountain Lake, Virginia. J. Freshw. Ecol. 6: 293–303.Google Scholar
  37. Parslow, J. S., P. J. Harrison & P. A. Thompson, 1984. Development of rapid ammonium uptake during starvation of batch and chemostat cultures of the marine diatomThalassioseira pseudonana. Mar. Biol. 83: 43–50.Google Scholar
  38. Parson, M. J. & B. C. Parker, 1989a. Mountain Lake, Virginia: an oligotrophic lake under increasing stress. Curr. Prac. Envir. Sci. Eng. 4: 1–24.Google Scholar
  39. Parson, M. J. & B. J. Parker, 1989b. Algal flora in Mountain Lake, Virginia: past and present. Castanea 54: 79–86.Google Scholar
  40. Pearsall, W. H. 1932. Phytoplankton in the English lakes; II. The composition of the phytoplankton in relation to dissolved substances. J. Ecol. 20: 241–262.Google Scholar
  41. Pelley, J. L. & T. T. Banister, 1979. Methylamine uptake in the green algaChlorella pyrenoidosa. J. Phycol. 15: 110–112.Google Scholar
  42. Procházková, L., P. Blâzka & M. Králová, 1970. Chemical changes involving nitrogen metabolism in water and particulate matter during primary production experiments. Limnol. Oceanogr. 15: 797–807.Google Scholar
  43. Sherr, E. B., B. F. Sherr, T. Berman & J. J. McCarthy, 1982. Differences in nitrate and ammonium uptake among components of a phytoplankton population. J. Plankton Res. 4: 961–965.Google Scholar
  44. Singh, R. N., 1955. Limnological relations of Indian inland waters with special reference to water blooms. Verb. int. Ver. theor. angew. Limnol. 12: 831–836.Google Scholar
  45. Smith, F. A. & N. A. Walker, 1978. Entry of methylammonium and ammonium ions intoChara internodal cell. J. exp. Bot. 29: 107–120.Google Scholar
  46. Sommer, U., 1988. Phytoplankton succession in microcosm experiments under simultaneous grazing pressure and resource limitation. Limnol. Oceanogr. 33: 1037–1050.Google Scholar
  47. Sridharan, N. & G. F. Lee, 1977. Algal nutrient limitation in Lake Ontario and tributary water. Wat. Res. 11: 849–858.Google Scholar
  48. Stewart, W. D. P., 1972. Algal metabolism and water pollution in the Tay Region. Proc. R. Soc. Edinb. 71: 209–224.Google Scholar
  49. Stewart, W. D. P., G. P. Fitzgerald & R. H. Burris, 1967.In situ studies on N2 fixation using the acetylene reduction techniques. Biochemistry 58: 2071–2078.Google Scholar
  50. Stewart, W. D. P., G. P. Fitzgerald & R. H. Burris, 1970. Acetylene reduction assay for determination of phosphorus availability in Wisconsin Lakes. Proc. natn. Acad. Sci. U.S.A. 66: 1104–1111.Google Scholar
  51. Stewart, W. D. P., T. H. Mague, G. P. Fitzgerald & R. H. Burris, 1971. Nitrogenase activity in Wisconsin Lakes of differing degrees of eutrophication. New Phytol. 70: 497–509.Google Scholar
  52. Suttle, C. A. & P. J. Harrison, 1988. Rapid ammonium uptake by freshwater phytoplankton. J. Phycol. 24: 13–16.Google Scholar
  53. Syrett, P. J., 1962. Nitrogen assimilation. In R. A. Lewin (ed.), Physiology and Biochemistry of Algae. Academic Press, New York, 171–188.Google Scholar
  54. Takahashi, M. & Y. Saijo, 1981. Nitrogen metabolism in Lake Kizaki, Japan; I. ammonium and nitrate uptake by phytoplankton. Arch. Hydrobiol. 91: 393–407.Google Scholar
  55. Tilman, D., 1982. Resource Competition and Community Structure. Princeton University Press, Princeton, New Jersey, 296Google Scholar
  56. Toetz, D. W., L. P. Varga & E. D. Loughran, 1973. Half-saturation constants for uptake of nitrate and ammonium by reservoir plankton. Ecology 54: 903–908.Google Scholar
  57. Turpin, D. H., J. S. Parslow & P. J. Harrison, 1981. On limiting nutrient patchiness and phytoplankton growth: a conceptual approach. J. Plankton Res. 3: 421–431.Google Scholar
  58. Vance, B. D., 1965. Composition and succession of cyanophycean water blooms. J. Phycol. 1: 81–86.Google Scholar
  59. Vincent, W., 1979. Uptake of [14C] methylammonium by phytoplankton communities: a comparative assay for ammonium transport systems in natural waters. Can. J. Microbiol. 25: 1401–1407.Google Scholar
  60. Vincent, W., 1981. Rapid physiological assays for nutrient demand by plankton; 1. nitrogen. J. Plankton Res. 3: 685–699.Google Scholar
  61. Vincent, W. F., W. Wurtbaugh, C. L. Vincent & P. J. Richerson, 1984. Seasonal dynamics of nutrient limitation in a tropical high-altitude lake (Lake Titicaca, Peru-Bolivia): application of physiological bioassays. Limnol. Oceanogr. 29: 540–552.Google Scholar
  62. Vymazal, J., 1987. Ammonium uptake and biomass interaction inCladophora glomerata (Chlorophyta). Br. Phycol. J. 22: 163–167.Google Scholar
  63. Wetzel, R. G., 1975. Limnology. W. B. Saunders Company, Philadelphia, Pennsylvania, 743 pp.Google Scholar
  64. Wheeler, P. A., 1980. Use of methylammonium as an analogue in nitrogen transport and assimilation studies withCyclotella cryptica (Bacillariophyceae). J. Phycol. 16: 328–334.Google Scholar
  65. Wheeler, P. A., P. M. Gilbert & J. J. McCarthy, 1982. Ammonium uptake and incorporation by Chesapeake Bay phytoplankton: short term uptake kinetics. Limnol. Oceanogr. 27: 1113–1128.Google Scholar
  66. White, E. & G. W. Payne, 1978. Chlorophyll products, in response to nutrient addition, by the algae in Lake Rotorua water, N. Z. J. Mar. Freshwat. Res. 12: 131–138.Google Scholar
  67. Wright, S. A. & P. J. Syrett, 1983. The uptake of methylammonium and dimethylammonium by the diatomPhaeodactylum tricornutum. Mar. Biol. 83: 43–50.Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • Marolyn J. Parson
    • 1
  • Bruce C. Parker
    • 1
  1. 1.Department of Biology, Virginia TechBlacksburgU.S.A.

Personalised recommendations