Marine Biology

, Volume 121, Issue 2, pp 373–380 | Cite as

Feeding, growth and bioluminescence of the heterotrophic dinoflagellate Protoperidinium huberi

  • E. J. Buskey
  • C. J. Coulter
  • S. L. Brown
Article

Abstract

Feeding, growth and bioluminescence of the thecate heterotrophic dinoflagellate Protoperidinium huberi were measured as a function of food concentration for laboratory cultures grown on the diatom Ditylum brightwellii. Ingestion of food increased with food concentration. Maximum ingestion rates were measured at food concentrations of ∼600 μg C l-1 and were ∼0.7 μg C individual-1 h-1 (1.8 D. brightwelli cells individual-1 h-1). Clearance rates decreased asymptotically with increasing food concentration. Maximum clearance rates at low food concentration were ca. 23 μl ind-1 h-1, which corresponds to a volume-specific clearance rate of 5.9x105 h-1. Cell size of P huberi was highly variable, with a mean diameter of 42 μm, but no clear relationship between cell size and food concentration was evident. Specific growth rates increased with food concentration until maximum growth rates of ∼0.7 d-1 were reached at a food concentration of 400 μg C l-1 (∼1000 cells ml-1). Food concentrations as low as 10 μg C l-1 of D. brightwellii (∼25 cells ml-1) were able to support growth of P. huberi. The bioluminescence of P. huberi varied with its nutritional condition and growth rate. Cells held without food lost their bioluminescence capacity in a matter of days. P. huberi raised at different food concentrations showed increased bioluminescence capacity, up to food concentration that supported maximum growth rates. The bioluminescence of P. huberi varied over a diel cycle, and these rhythmic changes persisted during 48 h of continuous darkness, indicating that the rhythm was under endogenous control.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Baars JWM (1981) Autecological investigations on marine diatoms 2. Generation times of 50 species. Hydrobiol Bull 15:137–151Google Scholar
  2. Balech E (1988) Los dinoflagelados del Atlantic Sudoccidental. Publnes esp Inst españ Oceanogr, Madrid: 1:1–310Google Scholar
  3. Banse K (1982) Cell volumes, maximal growth rates of unicellular algae and ciliates, and the role of ciliates in the marine pelagial. Limnol Oceanogr 27:1059–1071Google Scholar
  4. Batchelder HP, Swift E (1989) Estimated near-surface mesoplanktonic bioluminescence in the western North Atlantic during July 1986. Limnol Oceanogr 34:113–128Google Scholar
  5. Burkill PH, Edwards ES, John AWG, Sleigh MA (1993) Microzooplankton and their herbivorous activity in the northeastern Atlantic Ocean. Deep-Sea Res 40:479–493Google Scholar
  6. Buskey EJ (1992) Epipelagic planktonic bioluminescence in the marginal ice zone of the Greenland Sea. Mar Biol 113:689–698Google Scholar
  7. Buskey EJ (1994) Bioluminescence and growth rates of heterotrophic dinoflagellates on varying alagal diets: implications for studies of bioluminescence in the Arabian Sea. In: Thompson MF, Tirmizi NM (eds) Arabian Sea living marine resources and the environment. Vanguard Press, Karachi (in press)Google Scholar
  8. Buskey EJ, Coulter CJ, Strom SL (1993) Locomotory patterns of microzooplankton: potential effects on food selectivity of larval fish. Bull mar Sci 53:29–43Google Scholar
  9. Buskey EJ, Mills L, Swift E (1983) The effects of dinoflagellate bioluminescence on the swimming behavior of a marine copepod. Limnol Oceanogr 28:575–579Google Scholar
  10. Buskey EJ, Strom SL, Coulter CJ (1992) Bioluminescence of heterotrophic dinoflagellates from Texas coastal waters. J exp mar Biol Ecol 159:37–49Google Scholar
  11. Buskey EJ, Swift E (1983) Behavioral responses of the coastal copepod Acartia hudsonica to simulated dinoflagellate bioluminescence. J exp mar Biol Ecol 72:43–58Google Scholar
  12. Caron DA, Goldman JC (1990) Protozoan nutrient regeneration, In: Capriulo GM (ed) Ecology of marine Protozoa, University Press, New York, Oxford, pp 283–306Google Scholar
  13. Elbrachter M (1991) Food uptake mechanisms in phagotrophic dinoflagellates and classification. In: Patterson DJ, Larsen J (eds) The biology of free-living heterotrophic dinoflagellates. Clarendon, New York, pp 303–312Google Scholar
  14. Esaias WE, Curl HC Jr (1972) Effect of dinoflagellate bioluminescence on copepod ingestion rates. Limnol Oceanogr 17:901–906Google Scholar
  15. Fritz L, Triemer RE (1985) A rapid, simple technique utilizing Calcofluor White M2R for the visualization of dinoflagellate thecal plates. J Phycol 21:662–664Google Scholar
  16. Furnas MJ (1990) In situ growth rates of marine phytoplankton: approaches to measurement, community and species growth rates. J Plankton Res 12:1117–1151Google Scholar
  17. Gaines G, Elbrachter M (1987) Heterotrophic nutrition. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell Scientific Publications, Palo Alto, pp 224–268 (Bot Monogr 21)Google Scholar
  18. Gaines G, Taylor FJR (1984) Extracellular digestion in marine dinoflagellates. J Plankton Res 6:1057–1061Google Scholar
  19. Gifford DJ (1985) Laboratory culture of marine planktonic oligotrichs (Ciliphora, Oligotricha). Mar Ecol Prog Ser 23:257–267Google Scholar
  20. Gifford DJ (1988) Impact of grazing by microzooplankton in the Northwest Arm of Halifax Harbour, Nova Scotia. Mar Ecol Prog Ser 47:249–258Google Scholar
  21. Goldman JC (1993) Potential role of large oceanic diatoms in new primary production. Deep-Sea Res 40:159–168Google Scholar
  22. Goldman JC, Dennett MR, Gordin H (1989) Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina. J Plankton Res 11:391–407Google Scholar
  23. Guillard RRL, Ryther RH (1962) Studies of marine planktonic diatoms I Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239Google Scholar
  24. Hamman JP, Seliger HH (1972) The mechanical triggering of bioluminescence in marine dinoflagellates: chemical basis. J cell Physiol 80:397–408Google Scholar
  25. Hansen PJ (1991) Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagic food web. Mar Ecol Prog Ser 55:217–227Google Scholar
  26. Hansen PJ (1992) Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale. Mar Biol 114:327–334Google Scholar
  27. Hasting JW, Sweeney BM (1958) A persistent diurnal rhythm of luminescence in Gonyaulax polyedra. Biol Bull mar biol Lab, Woods Hole 115:440–458Google Scholar
  28. Haxo FT, Sweeney BM (1955) Bioluminescence in Gonyaulax polyedra In: Johnson FH (ed) The luminescence of biological systems. American Association for the Advancement of Science, Washington, DC, pp 415–420Google Scholar
  29. Heinbokel JF (1978) Studies on the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar Biol 47:177–189Google Scholar
  30. Jacobson DM (1987) The ecology and feeding of thecate heterotrophic dinoflagellates. Ph.D. thesis. Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution, BostonGoogle Scholar
  31. Jacobson DM, Anderson DM (1986) Thecate heterotrophic dinoflagellates: feeding behavior and mechanisms. J Phycol 22:249–258Google Scholar
  32. Jacobson DM, Anderson DM (1993) Growth and grazing rates of Protoperidinium hirobis Abe, a thecate heterotrophic dinoflagellate. J Plankton Res 15:723–736Google Scholar
  33. Jeong HJ, Latz MI (1994) Growth and grazing rates of the heterotrophic dinoflagellates Protoperidinium spp on red tide dinoflagellates. Mar Ecol Prog Ser 106:173–185Google Scholar
  34. Lapota D, Geiger ML, Stiffey AV, Rosenburg DE, Young DK (1989) Correlations of planktonic bioluminescence with other oceanographic parameters from a Norwegian fjord. Mar Ecol Prog Ser 55:217–227Google Scholar
  35. Lessard EJ (1984) Oceanic heterotrophic dinoflagellates: distribution, abundance and role as microzooplankton. Ph.D. thesis. University of Rhode Island, KingstownGoogle Scholar
  36. Lessard EJ (1991) The trophic role of heterotrophic dinoflagellates in diverse marine environments. Marine Microb Fd Webs 5:49–58Google Scholar
  37. Lessard EJ, Swift E (1985) Species-specific grazing rates of heterotrophic dinoflagellates in oceanic waters, measured with a duallabel radioisotope technique. Mar Biol 87:289–296Google Scholar
  38. Miller CB, Frost BW, Booth B, Wheeler PA, Landry MR, Welschmeyer N (1991) Ecological processes in the subarctic Pacific: iron limitation cannot be the whole story. Oceanography, Wash 4:73–78Google Scholar
  39. Paasche E (1968) Marine plankton algae grown with light-dark cycles 2. Ditylum brightwellii and Nitzschia turgidula. Physiologia Pl 21:66–77Google Scholar
  40. Sherr EB, Sherr BF, Paffenhöfer G-A (1986) Phagotrophic protozoa as food for metaboans: a “missing” trophic link in marine pelagic food webs. Mar microb Fd Webs 1:61–80Google Scholar
  41. Smetacek V (1981) The annual cycle of protozooplankton in the Kiel Bight. Mar Biol 63:1–11Google Scholar
  42. Stoecker DK, Capuzzo JM (1990) Predation on protozoa: its importance to zooplankton. J Plankton Res 12:891–908Google Scholar
  43. Strom SL (1991) Growth and grazing rates of the hervivorous dinoflagellate Gymnodinium sp from the open subarctic Pacific Ocean. Mar Ecol Prog Ser 78:103–113Google Scholar
  44. Strom SL, Buskey EJ (1993) Feeding, growth and behavior of the thecate heterotrophic dinoflagellate Oblea rotunda. Limnol Oceanogr 38:965–977Google Scholar
  45. Strom SL, Welschmeyer NA (1991) Pigment-specific rates of phytoplankton growth and microzooplankton grazing in the open subarctic Pacific Ocean. Limnol Oceanogr 36:50–63Google Scholar
  46. Sweeney BM (1969) Transducing mechanisms between circadian clock and overt rhythms in Gonyaulax. Can J Bot 47:299–308Google Scholar
  47. Sweeney BM, Hastings JW (1957) Characteristics of the diurnal rhythm of luminescence in Gonyaulax polyedra. J cell comp Physiol 49:115–128Google Scholar
  48. Sweeney BM, Haxo FT, Hastings JW (1959) Action spectra for two effects of light on luminescence in Gonyaulax polyedra. J gen Physiol 43:285–299Google Scholar
  49. Swift E, Lessard EJ, Biggley WH (1985) Organisms associated with stimulated epipelagic bioluminescence in the Sargasso Sea and the Gulf Stream. J Plankton Res 7:831–848Google Scholar
  50. Swift E, Meunier VA (1976) Effects of light intensity on division rate, stimulable bioluminescence, and cell size of the oceanic dinoflagellates Dissodinium lunula, Pyrocystis fusiformis and P. noctiluca. J Phycol 12:14–20Google Scholar
  51. Swift E, Sullivan JM, Batchelder HP, Van Keuren J, Vaillancourt RD, Bidigare RR (1994) Bioluminescent organisms and bioluminescence measurements in the Northern Atlantic Ocean. J geophys Res (Sect Oceans) (in press)Google Scholar
  52. Verity PG, Stoecker DK, Sieracki ME, Burkill PH, Edwards ES, Tronzo CR (1993) Abundance, biomass and distribution of heterotrophic dinoflagellates during the North Atlantic spring bloom. Deep-Sea Res 40:227–244Google Scholar
  53. White HH (1979) Effects of dinoflagellate bioluminescence on the ingestion rates of herbivorous zooplankton. J exp mar Biol Ecol 36:217–224Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • E. J. Buskey
    • 1
  • C. J. Coulter
    • 1
  • S. L. Brown
    • 1
  1. 1.Marine Science InstituteThe University of Texas at AustinPort AransasUSA

Personalised recommendations