Do top-down and bottom-up controls interact to exclude nitrogen-fixing cyanobacteria from the plankton of estuaries? An exploration with a simulation model

Biogeochemistry

Volumn 46, Issue 1-3, 1999, Pages 203-231

  Howarth, Robert W ^a   Chan, Francis ^a   Marino, Roxanne ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Baltic Sea; Cyanobacteria; Estuaries; Grazing; Iron; Lakes; Molybdenum; Nitrogen; Nitrogen fixation; Nitrogen limitation; Zooplankton

Indexed keywords

BOTTOM UP APPROACH; CYANOBACTERIUM; ESTUARINE ECOSYSTEM; NITROGEN FIXATION; PLANKTON; TOP-DOWN CONTROL;

EID: 0032771276     PISSN: 01682563     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF01007580     Document Type: Article

References (85)

1. 2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol. Rev. 19: 139-185
2. Bothe H (1982) Nitrogen fixation. In: Carr NG & Whitton BA (Eds) The Biology of Cyanobacteria (pp 87-104). University of California Press, Berkeley, U.S.A.
3. Brand LE (1991) Minimum iron requirements of marine phytoplankton and the implications for the biogeochemical control of new production. Limnol. Oceanogr. 36: 1756-1771
4. Burns CW & Xu Z (1990) Calanoid copepods feeding on algae and filamentous cyanobacteria: Rates of ingestion, defecation and effects on trichome length. J. Plank. Res. 12: 201-213
5. Burns CW & Hegarty B (1994) Diet selection by copepods in the presence of cyanobacteria. J. Plank Res. 16: 1671-690
6. Canfield TJ & Jones JR (1996) Zooplankton abundance, biomass, and size-distribution in selected midwestern waterbodies and relation with trophic state. J. Fresh. Ecol. 11: 171-181
7. Cardin CJ & Mason J (1976) Molybdate and tungstate transfer by rat ileum: competitive inhibition by sulphate. Biochim. Biophys. Acta 455: 937-946
8. Carpenter EJ & Capone DG (1992) Nitrogen fixation in Trichodesmium blooms. In: Carpenter EJ, Capone DG & Rueter JG (Eds) Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs (pp 211-218). Kluwer, Dordrecht, The Netherlands
9. Cole JJ, Lane JM, Marino R & Howarth RW (1993) Molybdenum assimilation by cyanobacteria and phytoplankton in freshwater and salt water. Limnol. Oceanogr. 38: 25-35
10. D'Elia CF, Sanders JG & Boynton WR (1986) Nutrient enrichment studies in a coastal plain estuary; phytoplankton growth in large-scale, continuous cultures. Can. J. Fish. Aquat. Sci. 43: 397-406
11. Doremus C (1982) Geochemical control of dinitrogen fixation in the open ocean. Biol. Oceanogr. 1: 429-435
12. Durbin AE & Durbin EG (1981) Standing stock and estimated production rates of phytoplankton and zooplankton in Narragansett Bay, Rhode Island. Estuaries 4: 24-41
13. Elliott BB & Mortenson LE (1975) Regulation of molybdate transport by Clostridium pasteurianum. J. Bacteriol. 127: 770-779
14. Elmgren R & Larsson U (1997) Himmerfjarden: Forandringar i ett naringsbelastat kustekyosystem i Ostersjon. Rapport 4565. Naturvardsverket Forlag
15. Epp GT (1995) Herbivory in the freshwater plankton: interactions of Daphnia pulicaria and filamentous cyanobacteria. PhD dissertation, Cornell University, NY, U.S.A.
16. Falconer IR, Choice A & Hosja W (1992) Toxicity of edible mussels Mytilus edulis growing naturally in an estuary during a water bloom of the blue-green algae Nodularia spumigena. Environ. Toxicol. Water. Qual. 7: 119-123
17. 2 in the ocean. Nature 387: 272-275
18. Flett RJ, Schindler DW, Hamilton RD & Campbell NER (1980) Nitrogen fixation in Canadian precambrian shield lakes. Can. J. Fish. Aquat. Sci .37: 494-505
19. Fogg GE (1987) Marine planktonic cyanobacteria. In: Fay P & Baalen CV (Eds) The Cyanobacteria (pp 393-414). Elsevier, Amsterdam, The Netherlands
20. Fulton RS (1988) Grazing on filamentous algae by herbivorous zooplankton. Fresh. Biol. 20: 263-271
21. 2. New Phytol 122: 571-609
22. 2 fixation in non-heterocystous cyanobacteria: An overview. In: Carpenter EJ, Capone DG & Rueter JG (Eds) Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs (pp 115-140). Kluwer, Dordrecht, The Netherlands
23. Gibson CE & Smith RV (1982) Freshwater plankton. In: Carr NG & Whitton BA (Eds) The Biology of Cyanobacteria (pp 463-489). Univ. of California Press, Berkeley, U.S.A.
24. Gliwicz ZM & Lampert W (1990) Food thresholds in Daphnia species in the absence and presence of blue-green filaments. Ecology 71: 691-702
25. Grobbelaar JU and House WA (1995) Phosphorus as a limiting resource in inland waters: interactions with nitrogen. In: Tiessen H (Ed.) Phosphorus in the Global Environment (pp 255-273). Wiley, Chichester
26. Gronlund L, Kononen K, Lahdes E and Makela K (1996) Community development and modes of phosphorus utilization in a late summer ecosystem in the central Gulf of Finland, the Baltic Sea. Hydrobiol. 331: 97-108
27. Haney JF (1987) Field studies on zooplankton-cyanobacteria interactions. New Zeal. J. Mar. Fresh. Res. 21: 467-475
28. Hansson L-A, Bergman E & Cronberg G (1998) Size structure and succession in phytoplankton communities: the impact of interactions between herbivory and predation. Oikos 81: 337-345
29. Hearn CJ & Lukatelich RJ (1990) Dynamics of Peel-Harvey Estuary, Southwest Australia. In: Cheng, RT (Ed.) Residual Currents and Long-term Transport. Coastal and Estuarine Studies 38 (pp 431-450). Springer-Verlag, New York, U.S.A.
30. Holm NP, Ganf GG & Shapiro J (1983) Feeding and assimilation rates of Daphnia pulex fed Aphanizomenon flos-aquae. Limol. Oceanogr. 28: 677-687
31. Horne AJ (1977) Nitrogen fixation - a review of this phenomenon as a polluting process. Prog. Water Technol. 8: 359-372
32. Horne AJ & Goldman CR (1972) Nitrogen fixation in Clear Lake, California. I. Seasonal variation and the role of heterocysts. Limnol. Oceanogr. 17: 678-692
33. Horne AJ, Dillard JE, Fujita DK & Goldman CR (1972) Nitrogen fixation in Clear Lake, California. II. Synoptic studies on the autumn Anabaena bloom. Limnol. Oceanogr. 17: 693-703
34. Horne AJ, Sandusk JC & Carmiggelt CJW (1979) Nitrogen fixation in Clear Lake, California. 3. Repetitive synoptic sampling of the spring Aphanizomenon blooms. Limnol. Oceanogr. 24: 316-328
35. Howarth RW (1988) Nutrient limitation of net primary production in marine ecosystems. Ann. Rev. Ecol. Syst. 19: 89-110
36. Howarth RW & Cole JJ (1985) Molybdenum availability, nitrogen limitation, and phytoplankton growth in natural waters. Science 229: 653-655
37. Howarth RW, Marino R, Lane J & Cole JJ (1988a) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance. Limnol. Oceanogr. 33: 669-687
38. Howarth RW, Marino R & Cole JJ (1988b) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnol. Oceanogr. 33: 688-701
39. Howarth RW & Marino R (1990) Nitrogen-fixing cyanobacteria in the plankton of lakes and estuaries: A reply to the comment by Smith. Limnol. Oceanogr. 35: 1859-1863
40. Howarth RW, Butler T, Lunde K, Swaney D & Chu CR (1993) Turbulence and planktonic nitrogen fixation: a mesocosm experiment. Limnol. Oceanogr. 38: 1696-1711
41. Howarth RW, Swaney D, Marino R, Butler TJ & Chu CR (1995) Turbulence does not prevent nitrogen fixation by plankton in estuaries and coastal seas (reply to the comment of Paerl et al). Limnol. Oceanogr. 40: 639-643
42. Howarth RW & Marino R (1998) A mechanistic approach to understanding why so many estuaries and brackish waters are nitrogen limited. In: Effects of Nitrogen in the Aquatic Environment, KVA Report 1998: 1 (pp 117-136). Kungl. Vetenskapsakademien (Royal Swedish Academy of Sciences), Stockholm
43. Huber AL (1986) Nitrogen fixation by Nodularia spumigena Mertens (Cyanobacteriaceae). 1: Field Studies and the contribution of blooms to the nitrogen budget of the Peel-Harvey Estuary, Western Australia. Hydrobiologia 131: 193-203
44. Huising J & Matrone G (1975) Biological interactions of sulfate and molybdate. Environ. Health Perspect. 10: 265
45. James MR & Forsyth DJ (1990) Zooplankton-phytoplankton interactions in a eutrophic lake. J. Plank. Res. 12: 455-472
46. Jones GS, Blackburn SI & Parker NS (1994) A toxic bloom of Nodularia spumigena Mertens in Orielton Lagoon, Tasmania. Aust. J. Mar. Fresh. Res. 45: 787-800
47. Karentz D & Smayda TJ (1998) Temporal patterns and variations in phytoplankton community organization and abundance in Narragansett Bay during 1959-1980. J. Plank Res. 20: 145-168
48. Kling HJ, Findlay DL & Komárek J (1994) Aphanizomenon schindleri sp. nov.: a new nostocacean cyanoprokaryote from the Experimental Lakes Area, northwestern Ontario. Can. J. Fish. Aquat. Sci. 51: 2267-2273
49. Lehtimaki J, Moisander P, Sivonen K & Kononen K (1997) Growth, nitrogen fixation, and nodularin production by two Baltic Sea cyanobacteria. Appl. Environ. Microbiol. 63: 1647-1656
50. Leibold MA, Chase JM, Shurin JB & Downing AL (1997) Species turnover and the regulation of trophic structure. Ann. Rev. Ecol. Syst. 28: 467-494
51. Lindahl G & Wallstrom K (1985) Nitrogen fixation (acetylene reduction) in planktonic cyanobacteria in Oregrundsgrepen, SW Bothnian Sea. Arch. Hydrobiol. 104: 193-204
52. Lukatelich RJ & McComb AJ (1986) Nutrient levels and the development of diatom and blue green algal blooms in a shallow Australian estuary. J. Plank. Res. 8: 597-618
53. Lynch M & Shapiro J (1981) Predation, enrichment, and phytoplankton community structure. Limnol. Oceanogr. 26: 86-102
54. Marino R, Howarth RW, Shamess J & Prepas EE (1990) Molybdenum and sulfate as controls on the abundance of nitrogen-fixing cyanobacteria in saline lakes in Alberta. Limnol. Oceanogr. 35: 245-259
55. Martin, JH, Coale KM, Johnson, KS, Fitzwater, SE, Gordon RM, Tanner SJ, Hunter CN, Elrod VA, Nowicki JL, Coley TL, Barber RT, Lindly S, Watson AJ, van Scoy K, Law CS, Liddicoat MI, Ling R, Stanton T, Stockelt J, Collins C, Anderson A, Bidigare R, Ondruske M, Latasa M, Millero FJ, Lee K, Yao W, Zhang JZ, Friederich G, Sakamoto C, Chavez F, Buck K, Kolber Z, Green R, Falkowski P, Chisholm SW, Hoge F, Swift R, Yungel J, Turner S, Nightingale P, Hatton A, Liss P & Tindale NW (1994) Testing the iron hypothesis in ecosystems of the equatorical Pacific Ocean. Nature 371: 123-129
56. Michaels AF, Olson D, Sarmiento JL, Ammerman JW, Fanning K, Jahnke R, Knap AH, Lipschultz F & Prospero JM (1996) Inputs, losses and transformations of nitrogen and phosphorus in the pelagic North Atlantic Ocean. Biogeochemistry 35: 181-226
57. 2 and acetylene reduction methods for the measurement of nitrogen fixation by Baltic Sea cyanobacteria. Phycologia 35: 140-146
58. Morel FMM & Hudson RJ (1985) The geobiological cycle of trace elements in aquatic systems: Redfield revisited. In: Stumm W (Ed.) Chemical Processes in Lakes (pp 251-282). Wiley, New York, U.S.A.
59. Nalewajio C & Lean DRS (1978) Phosphorus kinetics - algal growth relationships in batch cultures. Mitt int. Verein. theor. angew. Limnol. 21: 184-192
60. Niemisto L, Rinne I, Melsvasalo T, Niemei Å (1989) Blue-green algae and their nitrogen fixation in the Baltic Sea in 1980, 1982, and 1984. Meri 17: 1-59
61. Nixon SW & Pilson MEQ (1983) Nitrogen in estuarine and coastal marine ecosystems. In: Carpenter EJ & Capone DG (Eds) Nitrogen in the Marine Environment (pp 565-648). Academic, New York, U.S.A.
62. NRC (1993) Managing wastewater in coastal urban areas. National Research Council, Washington, DC, U.S.A.
63. Ogawa FE & Carr JF (1969) The influence of nitrogen on heterocyst production in blue-green algae. Limnol. Oceanogr. 14: 342-351
64. Pace ML (1986) An empirical analysis of zooplankton community size structure across lake trophic gradients. Limnol. Oceanogr. 31: 45-55
65. Pace ML, Findlay SEG & Lints D (1992) Zooplankton in advective environments: the Hudson River community and a comparative analysis. Can. J. Fish. Aquat. Sci. 49: 1060-1069
66. 2 fixation. Limnol. Oceanogr. 30: 1246-1252
67. 2 fixation in natural waters. In: Marshall KC (Ed.) Advances in Microbial Ecology (pp 305-343). Plenum, NY, U.S.A.
68. Rowell A & Kerby NW (1991) Cyanobacteria and their symbionts. In: Dilworth MJ & Glenn AR (Eds) Biology and Biochemistry of Nitrogen Fixation. Studies in Plant Science 1 (pp 373-407). Elsevier, New York, U.S.A.
69. 2 fixation in the oceans. EOS 63: 945
70. Schaffner WR, Hairston NG, jr & Howarth RW (1994) Feeding rates and filament clipping by crustacean zooplankton consuming cyanobacteria. Verb. Internat. Verein. Limnol. 25: 2375-2381
71. Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195: 260-262
72. Sellner KG, Olson MM & Kononen K (1994) Copepod grazing in a summer cyanobacteria bloom in the Gulf of Finland. Hydrobiologia 292/293: 249-254
73. Stout PR & Meagher WR (1948) Studies of the molybdenum nutrition of plants with radioactive molybdenum. Science 108: 471-473
74. Tackx MLM, Bakker C & Van Rijswijk P (1990) Zooplankton grazing pressure in the Oosterschelde (The Netherlands). Neth. J. Sea Res. 25: 405-415
75. Turpin DH, Layzell DB & Elrifi IR (1985) Modeling the C economy of Anabaena flos-aquae. Plant. Physiol. 78: 746-752
76. Uitto A (1996) Summertime herbivory of coastal mesozooplankton and metazoan microplankton in the northern Baltic. Mar. Ecol. Prog. Ser. 132: 47-56
77. Valiela I (1991) Ecology of coastal ecosystems. In: Barnes RSK & Mann DH (Eds) Fundamentals of Aquatic Ecology (pp 57-76). Blackwell Scientific, Oxford
78. Varmo R, Viljamaa H, Pesonen L & Rinne I (1989) Two manipulated inner bays in the Helsinki Sea area, Northern Gulf of Finland. Aqua. Fenn. 19: 67-74
79. Vitousek PM & Field CB (this volume) Ecosystem constraints to symbiotic nitrogen fixers: A simple model and its implications. Biogeochemistry: in press
80. Vitousek PM & Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13: 87-115
81. Wallstrom K (1988) The occurrence of Aphanizomenon flos-aquae (Cyanophyceae) in a nutrient gradient in the Baltic. Kieler Meeresforschungen Sonderheft 6: 210-220
82. Wallstrom K (1991) Ecological studies on nitrogen fixing blue-green algae and on nutrient limitation of phytoplankton in the Baltic Sea. PhD thesis, Uppsala University. Uppsala, Sweden
83. Wallstrom K, Johansson S & Larsson U (1992) Effects of nutrient enrichment on planktonic blue-green algae in the Baltic Sea. Acta. Phytogeogr. Suec. 78: 25-31
84. White JR & Roman MR (1992) Seasonal study of grazing by metazoan zooplankton in the mesohaline Chesapeake Bay. Mar. Ecol. Prog. Ser. 86: 251-261
85. Zevenboom W & Mur LR (1978) Nitrogen uptake and pigmentation of N-limited chemostat cultures and natural populations of Oscillatoria agardhii. Mitt int. Verein. theor. angew. Limnol. 21: 261-274