Annual phytoplankton cycle in a meromictic anoxic basin of a Rhode Island (USA) estuarine river

  • Theodore J. Smayda
  • Boyce Thorne-Miller
  • Carmelo TomasEmail author
Primary Research Paper


Estuarine Pettaquamscutt River is a unique habitat 10 km in length with physical and biogeochemical characteristics analogous to a miniature fjord. Its meromictic upper basins are characterized by a permanent oxic–anoxic vertical gradient in which a well-oxygenated upper layer overlies a deeper, anoxic reservoir, with persistent blooms of phototrophic anoxygenic bacteria (Chromatium, Chlorobium) at the oxic–anoxic transition layer. A diverse assemblage of nanoplanktonic, centric diatoms (Cyclotella caspia, Thalassiosira pseudonana, cf. Cyclotella cryptica) dominated the seasonal phytoplankton cycle in the aerobic layer, similar to comparable meromictic habitats elsewhere. This assemblage of nano-centric diatoms appears to be trait-separated from other species clusters and is potentially useful as a functional group flora with ecophysiology diagnostic of marine estuarine rivers and meromictic habitat niche structure. The most conspicuous phytoplankton feature, however, was the year-round occurrence of the photoautotrophic euglenid Euglenaformis (Euglena) proxima, restricted in its upper water column distribution to the O2–H2S boundary layer where it formed a consortium with the photosynthetic green and purple sulfur bacteria community. The association of E. proxima with meromixis, H2S, and phototrophic anoxygenic bacteria is similar to that reported previously in a brackish Norwegian oyster poll and a brackish loch in Scotland.


Meromixis H2Photosynthetic bacteria Phytoplankton Nano-diatoms Euglenaformis proxima H2S tolerant micro-alga consortia 



This study was aided by the Environmental Protection Agency’s Science to Achieve Results (STAR) Program funded by EPA Grant No. R83-2443. The STAR program is managed by the EPA’s Office of Research and Development (ORD), National Center for Environmental Research and Quality Assurance (NCERQA). STAR research supports the Agency’s mission to safe guard human health and the environment. We thank Dr. Paul Hargraves for his assistance in identifying the nano-centric diatoms.


  1. Bennett, M. S., K. E. Wiegert & R. E. Triemer, 2014. Characterization of Euglenaformis gen. nov. and the chloroplast genome of Euglenaformis [Euglena] proxima Euglenophyta). Phycologia 53: 66–73.CrossRefGoogle Scholar
  2. Boothroyd, J. C., 1991. The geologic history of Narrow River. Maritimes 35: 3–5.Google Scholar
  3. Braarud, T. & B. Føyn, 1958. Phytoplankton observations in a brackish water locality of southeast Norway. Nytt Magasin for Botanikk 6: 47–73.Google Scholar
  4. Broenkow, W. W. & J. D. Cline, 1969. Colorimetric determination of dissolved oxygen at low concentrations. Limnology and Oceanography 14: 450–454.CrossRefGoogle Scholar
  5. Carritt, D. E. & J. H. Carpenter, 1965. Accuracy of the Winkler method for dissolve oxygen analysis. Limnology and Oceanography 10: 135–143.CrossRefGoogle Scholar
  6. Cline, J. D., 1969. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnology and Oceanography 14: 454–458.CrossRefGoogle Scholar
  7. Cloern, J. E., B. E. Cole & R. S. Oremland, 1983. Autotrophic processes in meromictic Big Soda Lake, Nevada. Limnology and Oceanography 28: 1049–1061.CrossRefGoogle Scholar
  8. de Madariaga, I., 1995. Photosynthetic characteristics of phytoplankton during the development of a summer bloom in Urdaibai Estuary, Bay of Biscay. Estuarine, Coastal and Shelf Science 40: 559–575.CrossRefGoogle Scholar
  9. Durbin, A. G., S. W. Nixon & C. A. Oviatt, 1979. Effects of the spawning migration of the alewife, Alosa pseudoharengus, on freshwater ecosystems. Ecology 60: 8–17.CrossRefGoogle Scholar
  10. Fanning, K. A. & M. E. Q. Pilson, 1972. A model for the anoxic zone of the Cariaco Trench. Deep-Sea Research 19: 847–863.Google Scholar
  11. Fenchel, T. & B. J. Finlay, 1995. Ecology and Evolution in Anoxic Worlds. Oxford Series in Ecology and Evolution, Oxford Univ. Press, Oxford.Google Scholar
  12. Fenchel, T., C. Bernard, G. Esteban, et al., 1955. Microbial diversity and activity in a Danish fjord with anoxic deep water. Ophelia 43: 45–100.CrossRefGoogle Scholar
  13. Furnas, M. J., T. J. Smayda & C. R. Tomas, 1989. Persistent dinoflagellate blooms in a small marine cove. I. Effect of wind and tidal currents. Marine Nature 2: 79–93.Google Scholar
  14. Furnas, M. J., T. J. Smayda & C. R. Tomas, 1990. Persistent dinoflagellate blooms in a small marine cove. II. Tidal fluxes of nutrients and phytoplankton. Marine Nature 3: 9–28.Google Scholar
  15. Gaines, A.G. Jr., 1975. Papers on the geomorphology, hydrography, and geochemistry of the Pettaquamscutt River. Ph.D. Thesis. University of Rhode Island, 278.Google Scholar
  16. Gaines, A. G. & M. E. Q. Pilson, 1972. Anoxic water in the Pettaquamscutt River. Limnology and Oceanography 17: 42–49.CrossRefGoogle Scholar
  17. Genovese, S., 1963. The distribution of the H2S in the Lake of Faro (Messina) with particular regard to the presence of “red water”. In Oppenheimer, C. H. (ed.), Symposium on Marine Microbiology. C.C Thomas Publisher, Springfield: 194–204.Google Scholar
  18. Goldberg, E. G., E. Gamble, J. J. Griffin & M. Koide, 1977. Pollution history of Narragansett Bay as recorded in its sediments. Estuarine, Coastal and Shelf Science 5: 549–561.CrossRefGoogle Scholar
  19. Guerrero, R., E. Montesinos, C. Pedrós-Alió, et al., 1985. Phototrophic sulfur bacteria in two Spanish lakes: vertical distribution and limiting factors. Limnology and Oceanography 30: 919–931.CrossRefGoogle Scholar
  20. Guillard, R. R. L. & S. Myklestad, 1970. Osmotic and ionic requirements of the marine centric diatom Cyclotella nana. Helgoländer wissenschaftliche Meeresuntersuchun 20: 104–110.CrossRefGoogle Scholar
  21. Hargraves, P. E. & B. Thorne Miller, 1974. The ebridian flagellate Hermesinum adriaticum Zach. Archive für Protistenkunde 116: 280–284.Google Scholar
  22. Hasle, G. R., 1978. Some freshwater and brackish species of the diatom genus Thalassiosira Cleve. Phycologia 17: 263–292.CrossRefGoogle Scholar
  23. Hasle, G. R. & B. R. Heimdal, 1970. Some species of the centric diatom genus Thalassiosira studied in the light and electron microscopes. Beihefte zur Nova Hedwigia 31: 543–581.Google Scholar
  24. Hasle, G. R. & G. A. Fryxell, 1977. The genus Thalassiosira: some species with a linear areola array. Beihefte zur Nova Hedwigia 54: 15–66.Google Scholar
  25. Holmes, R. W., 1970. The Secchi disk in turbid coastal waters. Limnology and Oceanography 15(688–554): 694.Google Scholar
  26. Hulburt, E. M., 1956. The phytoplankton of Great Pond, Massachusetts. Biological Bulletin 110: 157–168.CrossRefGoogle Scholar
  27. Hulburt, E. M., 1963. The diversity of phytoplanktonic populations in oceanic, coastal, and estuarine regions. Journal of Marine Research 21: 81–93.Google Scholar
  28. Iizuka, S., 1972. Gymnodinium-’65 red tide occurring in anoxic environment of Omura Bay. Bay. Bulletin of the Plankton Society of Japan 19: 13–21.Google Scholar
  29. Iizuka, S. & H. Irie, 1969. Anoxic status of bottom waters and occurrences of Gymnodiniium red water in Omura Bay. Bulletin of the Plankton Society of Japan 16: 99–115.Google Scholar
  30. Iizuka, S. & T. Nakashima, 1975. Response of red tide organisms to sulphide. Bulletin of the Plankton Society of Japan 22: 27–32.Google Scholar
  31. Jackson, R. H., P. J. Lebour Williams Jr. & I. R. Joint, 1987. Freshwater phytoplankton in the low salinity region of the River Tamar estuary. Estuarine, Coastal and Shelf Science 25: 299–311.CrossRefGoogle Scholar
  32. Johnson, P. W., P. L. Donaghay, E. B. Small & J. M. Sieburth, 1995. Ultrastructure and ecology of Perspira ovum (Ciliophora: Litostomatea): an aerobic, planktonic ciliate that sequesters the chloroplasts, mitochondria, and paramylon of Euglena proxima in a micro-oxic habitat. Journal of Eukaryotic Microbiology 42: 323–335.CrossRefGoogle Scholar
  33. Karentz, D. & T. J. Smayda, 1984. Temperature and the seasonal occurrence pattern of 30 dominant phytoplankton species in Narragansett Bay over a 22-year period (1959–1980). Marine Ecology Progress Series 18: 277–293.CrossRefGoogle Scholar
  34. Kennett, D. M., 1983. Benthic subtidal diatom flora and sulfide fluctuations in the upper basin of Pettaquamscutt River. M.S. Thesis, University of Rhode Island, 121.Google Scholar
  35. Kennett, D. M. & P. E. Hargraves, 1984. Subtidal benthic diatoms from a stratified estuarine basin. Botanica Marina 27: 169–183.CrossRefGoogle Scholar
  36. Kennett, D. M. & P. E. Hargraves, 1985. Benthic diatoms and sulfide fluctuations: upper basin of Pettaquamscutt River, Rhode Island. Estuarine, Coastal and Shelf Science 21: 577–586.CrossRefGoogle Scholar
  37. Klavestad, N., 1957. An ecological study of the vegetation in Hunnebunnen, an old oyster poll in south-eastern Norway. Nytt Magasin for Botanikk 5: 63–100.Google Scholar
  38. Lindholm, T. & X. Weppling, 1997. Blooms of phototrophic bacteria and phytoplankton in a small brackish lake on Aaland, SW Finland. Acta Academiae Aboensis 47: 45–53.Google Scholar
  39. Marshall, S. M., 1947. An experiment in marine fish cultivation. III. The plankton of a fertilized loch. The Proceedings Royal Society of Edinburgh Series B 63: 21–33.CrossRefGoogle Scholar
  40. Marshall, S. M. & A. P. Orr, 1948. Further experiments on the fertilization of a sea loch (Loch Craiglin). The effect of different plant nutrients on the phytoplankton. Journal of the Marine Biological Association of the Marine Biological Association of the United Kingdom 27: 360–379.CrossRefGoogle Scholar
  41. Moncrieff, R. W., 1967. The Chemical Senses. Leonard Hill, London.Google Scholar
  42. Noland, L. E. & M. Gojdics, 1967. Ecology of free-living protozoa. In Chen, T. (ed.), Research in Protozoology, Vol. 2. Pergamon Press, Oxford: 215–266.Google Scholar
  43. Orive, E., A. Iriarte, I. de Madariaga & M. Revilla, 1998. Phytoplankton blooms in the Urdaibai estuary during summer: physico-chemical conditions and taxa involved. Oceanologica Actga 21: 293–305.CrossRefGoogle Scholar
  44. Orr, A. P., 1947. An experiment in marine fish cultivation: II. Some physical and chemical conditions in a fertilized sea-loch (Loch Craiglin, Argyll). Proceedings Royal Society of Edinburgh Series B 63: 3–20.CrossRefGoogle Scholar
  45. Orr, W. L. & A. G. Gaines Jr., 1974. Observations on the rate of sulfate reduction and organic matter oxidation in the bottom waters of an estuarine basin: the upper basin of the Pettaquamscutt River (Rhode Island). In Tisson, B. & F. Bienner (eds), Advances in Organic Geochemistry. Editions Technics, Paris: 791–812.Google Scholar
  46. Paasche, E., 1971. A simple method for establishing bacteria-free cultures of photoautrophic flagellates. Journal du Conseil International pour l’Exploration de la Mer 33: 509–511.CrossRefGoogle Scholar
  47. Pedrós-Alió, C., J. M. Gaso & R. Guerrero, 1987. On the ecology of a Cryptomonas phaseolus population forming a meta-limnetic bloom in Lake Cisco, Spain. Annual distribution and loss factors. Limnology and Oceanography 32: 285–298.CrossRefGoogle Scholar
  48. Requejo, A. G., J. G. Quinn, J. N. Gearing & P. Gearing, 1984. C25 and C30 biogenic alkenes in a sediment core from the upper anoxic basin of the Pettaquamscutt River (Rhode Island, U.S.A.). Organic Geochemistry 7: 1–10.CrossRefGoogle Scholar
  49. Reynolds, C. S., V. L. Huszar, V. L. Kruk, L. Naselli-Flores & S. Melo, 2002. Towards a functional classification of freshwater phytoplankton. Journal of Plankton Research 24: 417–428.CrossRefGoogle Scholar
  50. Richards, F. A., 1965. Anoxic basins and fjords. In Riley, J. P. & G. Skirrow (eds), Chemical Oceanography, Vol. 1. Academic Press, New York: 611–645.Google Scholar
  51. Rines, J. E. B. & P. E. Hargraves, 1987. The seasonal distribution of the marine diatom genus Chaetoceros Ehr. in Narragansett Bay, Rhode Island (1981–1982). Journal of Plankton Research 9: 917–933.CrossRefGoogle Scholar
  52. Scranton, M. I., P. Crill, M. A. deAngelis, et al., 1993. The importance of episodic events in controlling the flux of methane from an anoxic basin. Global Biogeochemical Cycles 7: 491–507.CrossRefGoogle Scholar
  53. Sieburth, J. M. & P. L. Donaghay, 1993. Planktonic methane production and oxidation within the algal maximum of the pycnocline: seasonal fine-scale observations in an anoxic estuarine basin. Marine Ecology Progress Series 100: 3–15.CrossRefGoogle Scholar
  54. Smayda, T. J., 1970. The suspension and sinking of phytoplankton in the sea. Oceanography and Marine Biology 8: 353–414.Google Scholar
  55. Smayda, T. J., 1973. A survey of phytoplankton dynamics in the coastal waters from Cape Hatteras to Nantucket. In Coastal and Offshore Environmental Inventory, Cape Hatteras to Nantucket Shoals. Marine Publication Series No. 2, University of Rhode Island: 3.1–3.100.Google Scholar
  56. Smayda, T. J., 1998. Patterns of variability characterizing marine phytoplankton, wit examples from Narragansett Bay. ICES Journal of Marine Science 55: 562–573.CrossRefGoogle Scholar
  57. Sørensen, K., 1988. The distribution and biomass of phytoplankton and phototrophic bacteria in Framvaren, a permanently anoxic fjord in Norway. Marine Chemistry 23: 229–241.CrossRefGoogle Scholar
  58. Strickland, J. D. H. & T. R. Parsons, 1968. A practical handbook of seawater analysis. Bulletin of the Fishery Research Board of Canada 167: 1–203.Google Scholar
  59. Takahashi, M. & S. Ichimura, 1968. Vertical distribution and organic matter production of photosynthetic sulfur bacteria in Japanese lakes. Limnology and Oceanography 13: 644–655.CrossRefGoogle Scholar
  60. Takahashi, M. & S. Ichimura, 1970. Photosynthetic properties and growth of photosynthetic sulfur bacteria in lakes. Limnology and Oceanography 15: 929–944.CrossRefGoogle Scholar
  61. Throndsen, J., G. R. Hasle & K. Tangen, 2007. Phytoplankton of Norwegian coastal waters. Almater Forlag, Oslo: 343.Google Scholar
  62. Tomas, C. R. & T. J. Smayda, 2008. Red tide blooms of Cochlodinium polykrikoides in a coastal cove. Harmful Algae 7: 308–317.CrossRefGoogle Scholar
  63. Trigueros, J. M. & E. Orive, 2000. Tidally driven distribution of phytoplankton blooms in a shallow, macrotidal estuary. Journal of Plankton Research 22: 969–986.CrossRefGoogle Scholar
  64. Trüper, H. G., 1970. Culture and isolation of phototrophic sulfur bacteria from the marin environment. Helgoländer wissenschaftliche Meeresuntersuchungen 20: 6–16.CrossRefGoogle Scholar
  65. Trüper, H. G. & S. Genovese, 1968. Characterization of photosynthetic sulfur bacteria causing red water in Lake Faro (Messina, Sicily). Limnology and Oceanography 13: 225–232.CrossRefGoogle Scholar
  66. Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplankton Methodik. Mitteilungen der Internationale Vereinigung für Theoretische und Angewandte Limnologie 9: 1–39.Google Scholar
  67. Vargo, S. L. & A. N Sastry, 1977. Interspecific differences in tolerance of Eurytemora affinis and Acartia tonsa from an estuarine anoxic basin to low dissolved oxygen and hydrogen sulfide. In D. S. McLusky & A. J. Berry (eds), Physiology and Behavior of Marine Organisms. Proceedings 12th European Symposium on Marine Biology. Pergamon Press, Oxford. 219–226.Google Scholar
  68. Whelan, J. K., M. A. Blanchette & J. M. Hunt, 1983. olatile C1–C7 organic compounds in an anoxic sediment core from the Pettaquamscutt River (Rhode Island). Organic Geochemistry 5: 29–33.CrossRefGoogle Scholar
  69. Wood, E. D., F. A. J. Armstrong & F. A. Richards, 1967. Determination of nitrate in sea water by cadmium copper reduction to nitrite. Journal of the Marine Biological Association of the United Kingdom 47: 23–31.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Graduate School of OceanographyUniversity of Rhode IslandKingstonUSA
  2. 2.DickersonUSA
  3. 3.Center for Marine ScienceUniversity of North Carolina WilmingtonWilmingtonUSA

Personalised recommendations