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Seasonal variations in abundance, growth and mortality of heterotrophic bacteria in Kagoshima Bay

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Abstract

Seasonal changes in abundance, growth and mortality of heterotrophic bacteria were investigated monthly from collections and dilution experiments in Kagoshima Bay, the southernmost of Japan. Bacteria occurred abundantly with considerable variation in the surface layers where chlorophyll a concentrations were high, whereas seasonal variations were obscure below 100 m. Especially, bacteria showed a decline of cell density toward summer when heterotrophic nano-flagellates increased their abundance. Seasonal and vertical variations in bacterial cell number during the study period were positively correlated with those of water temperature and pico-sized chlorophyll a concentration. Maximum growth and mortality rates showed positive correlations with water temperature but no positive relationships to size-fractionated chlorophyll a. Net increase rate (i.e. in situ rate if abundance changes) was negatively correlated with cell density of heterotrophic nano-flagellates. It is concluded that bacterial abundance is controlled by the resultant (i.e. net growth rate) of the balance between maximum growth and predatory mortality by heterotrophic nano-flagelllates which are both dependent on ambient temperature.

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References

  • Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil and F. Thingstad (1983): The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser., 10, 257–263.

    Article  Google Scholar 

  • Campbell, L., H. Liu, H. A. Nolla and D. Vaulot (1997): Annual variability of phytoplankton and bacteria in the subtropical North Pacific Ocean at Station ALOHA during the 1991–1994 ENSO event. Deep-Sea Res. I, 44, 167–192.

    Article  Google Scholar 

  • Cole, J. J., S. Findlay and M. L. Pace (1988): Bacterial production in fresh and saltwater ecosystem; a cross-system overview. Mar. Ecol. Prog. Ser., 43, 1–10.

    Article  Google Scholar 

  • Egli, T. (1995): The ecological and physiological significance of the growth of heterotrophic microorganisms with mixtures of substrates. p. 305–386. In Advances in Microbial Ecology, ed. by J. G. Jones, Plenum Press, New York.

    Google Scholar 

  • Fukami, K., N. Murata, Y. Morio and T. Nishijima (1996): Distribution of heterotrophic nanoflagellates and their importance as the bacterial consumer in an eutrophic coastal seawater. J. Oceanogr., 52, 399–407.

    Article  Google Scholar 

  • Haas, L. W. (1982): Improved epifluorescence microscopy for observing planktonic micro-organisms. Ann. Inst. Oceanogr., 58, 261–266.

    Google Scholar 

  • Hold, G. L., E. A. Smith, M. S. Rappé, E. W. Maas, E. R. B. Moore, C. Stroempl, J. R. Stephen, J. I. Prosser, T. H. Birkbeck and S. Gallacher (2001): Characterization of bacterial communities associated with toxic and non-toxic dinoflagellates. FEMS Microbiol. Ecol., 37, 161–173.

    Article  Google Scholar 

  • Imai, I. (1984): Size distribution and biomass of bacteria in Suo-Nada, western Seto Inland Sea. Bull. Nansei Reg. Fish. Res. Lab., 17, 183–196.

    Google Scholar 

  • Imai, I. and K. Ito (1984): Distribution of heterotrophic microflagellates in Suo-Nada, western Seto Inland Sea. Bull. Nansei Reg. Fish. Res. Lab., 17, 219–233.

    Google Scholar 

  • Imai, I. and M. Yamaguchi (1997): Abundance and productivity of bacteria in Osaka Bay, eastern Seto Inland Sea, Japan. Bull. Nansei Reg. Fish. Res. Lab., 30, 173–181.

    Google Scholar 

  • Ishizaka, J., K. Harada, K. Ishikawa, H. Kiyosawa, H. Furusawa, Y. Watanabe, H. Ishida, K. Suzuki, N. Honda and M. Takahashi (1997): Size and taxonomic plankton community structure and carbon flow at the equator, 175°E during 1990–1994. Deep-Sea Res. II, 44, 1927–1949.

    Article  Google Scholar 

  • Iwamoto, N., I. Imai and S. Uye (1993): Numerical fluctuation of bacteria and heterotrophic microflagellates in Hiroshima Bay of the Inland Sea of Japan in summer 1990. Bull. Plankton Soc. Japan, 40, 55–66.

    Google Scholar 

  • Iwamoto, N., I. Imai and S. Uye (1994): Seasonal fluctuation in abundance of bacteria, heterotrophic nanoflagellates, autotrophic nanoflagellates and nanodiatoms in Hiroshima Bay, the Inland Sea of Japan. Bull. Plankton Soc. Japan, 41, 31–42.

    Google Scholar 

  • Kirchman, D. L. (2000): Microbial Ecology of the Oceans. Wiley-Liss, New York, 542 pp.

    Google Scholar 

  • Kirchner, M., G. Sahling, G. Uhlig, W. Gunkel and K. W. Klings (1996): Does the red tide-forming dinoflagellate Noctiluca scintillans feed on bacteria? Sarsia, 81, 45–55.

    Google Scholar 

  • Kobari, T., A. Habano and T. Ichikawa (2002): Seasonal variations in phyto- and zooplankton biomass in Kagoshima Bay. Mem. Fac. Fish. Kagoshima Univ., 51, 19–25.

    Google Scholar 

  • Kobari, T., Y. Kobari, T. Ichikawa, Y. Kugita, T. Yoshida, T. Fujii, S. Furuhashi, T. Yamamoto, A. Habano and R. Fukuda (2009): Seasonal dynamics of microbial plankton community in Kagoshima Bay. Aquabiol., 31, 37–44 (in Japanese with English abstract).

    Google Scholar 

  • Kobari, T., K. Mitsui, T. Ota, M. Ichinomiya and Y. Gomi (2010): Response of heterotrophic bacteria to the spring phytoplankton bloom in the Oyashio region. Deep-Sea Res. II, 57, 1671–1678.

    Article  Google Scholar 

  • Landry, M. R. and P. P. Hassett (1982): Estimating the grazing impact of marine micro-zooplankton. Mar. Biol., 67, 283–288.

    Article  Google Scholar 

  • Landry, M. R., J. Constantinou and J. Kirshtein (1995): Microzooplankton grazing in the central equatorial Pacific during February and August, 1992. Deep-Sea Res. II, 42, 657–671.

    Article  Google Scholar 

  • McManus, G. B. and J. A. Fuhrman (1988): Clearance of bacteria sized particles by natural populations of nanoplankton in the Chesapeake Bay outflow plume. Mar. Ecol. Prog. Ser., 42, 199–206.

    Article  Google Scholar 

  • Naganuma, T. (1997): Abundance and production of bacterioplankton along a transect of Ise Bay, Japan. J. Oceanogr., 53, 579–583.

    Google Scholar 

  • Naganuma, T. and S. Miura (1997): Abundance, production and viability of bacterioplankton in the Seto Inland Sea, Japan. J. Oceanogr., 53, 435–442.

    Google Scholar 

  • Naganuma, T. and H. Seki (1993): Abundance and productivity of bacterioplankton in a eutrophication gradient of Shimoda Bay. J. Oceanogr., 49, 657–665.

    Article  Google Scholar 

  • Nakamura, Y., K. Fukami, S. Sasaki and J. Hiromi (1994): Population dynamics of bacteria and heterotrophic nanoflagellates following the summer diatom bloom in the Seto Inland Sea. Bull. Plankton Soc. Japan, 41, 1–8.

    Google Scholar 

  • Nomura, H., Y. Ishido, T. Ishimaru and M. Murano (2007): Temporal and spatial variation in abundance of heterotrophic bacteria in a eutrophic inlet, Tokyo Bay, of the temperate Pacific coast of Japan. Oceanogr. Japan, 16, 349–360 (in Japanese with English abstract).

    Google Scholar 

  • Nozawa, K. and T. Saisyo (1980): Plankton in Kagoshima Bay. Kaiyo Kagaku, 12, 654–672 (in Japanese).

    Google Scholar 

  • Pinhassi, J. and T. Berman (2003): Differential growth response of colonyforming α- and γ-proteobacteria in dilution culture and nutrient addition experiments from Lake Kinneret (Israel), the eastern Mediterranean Sea, and the Gulf of Eilat. Appl. Environ. Microbiol., 69, 199–211

    Article  Google Scholar 

  • Pinhassi, J., M. M. Sala, H. Havskum, F. Peters, Ò. Guadayol, A. Malits and C. Marrasé (2004): Changes in bacterioplankton composition under different phytoplankton regimens. Appl. Environ. Microbiol., 70, 6753–6766.

    Article  Google Scholar 

  • Pomeroy, L. R. and W. J. Wiebe (1993): Energy sources for microbial food webs. Mar. Microb. Food Webs, 7, 101–118.

    Google Scholar 

  • Sanders, R. W., K. G. Porter, S. J. Bennett and A. E. DeBiase (1989): Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol. Oceanogr., 34, 673–687.

    Article  Google Scholar 

  • Sanders, R. W., D. A. Caron and U.-G. Berninger (1992): Relationship between bacteria and heterotrophic nanoplankton in marine and fresh waters: an inter-ecosystem comparison. Mar. Ecol. Prog. Ser., 86, 1–14.

    Article  Google Scholar 

  • Schäfer, H., B. Abbas, H. Witte and G. Muyzer (2002): Genetic diversity of “satellite” bacteria present in cultures of marine diatoms. FEMS Microbiol. Ecol., 42, 25–35.

    Google Scholar 

  • Sherr, B. F., E. B. Sherr, T. L. Andrew, R. D. Fallon and S. Y. Newell (1986): Trophic interactions between heterotrophic protozoa and bacterioplankton in estuarine water analyzed with selective metabolic inhibitors. Mar. Ecol. Prog. Ser., 32, 169–179.

    Article  Google Scholar 

  • Shiah, F. K. and H. W. Ducklow (1994): Temperature regulation of heterotrophic bacterioplankton abundance, production, and specific growth rate in Chesapeake Bay. Limnol. Oceanogr., 39, 1243–1258.

    Article  Google Scholar 

  • Simon, M., B. C. Cho and F. Azam (1992): Significance of bacterial biomass in lakes and the ocean: comparison to phytoplankton biomass and biogeochemical implications. Mar. Ecol. Prog. Ser., 86, 103–110.

    Article  Google Scholar 

  • Steinberg, D. K., B. A. S. Van Mooy, K. O. Buesseler, P. W. Boyd, T. Kobari and D. M. Karl (2008): Bacterial vs. zooplankton control of sinking particle flux in the ocean’s twilight zone. Limnol. Oceanogr., 53, 1327–1338.

    Article  Google Scholar 

  • Suzuki, R. and T. Ishimaru (1990): An improved method for the determination of phytoplankton chlorophyll using N,Ndimethylformamide. J. Oceanogr. Soc. Japan, 46, 190–194.

    Article  Google Scholar 

  • Tada, K., K. Monaka, M. Morishita and T. Hashimoto (1998): Standing stocks and production rates of phytoplankton and abundance of bacteria in the Seto Inland Sea, Japan. J. Oceanogr., 54, 285–295.

    Article  Google Scholar 

  • Tada, K., M. Morishita, S. Montani, J. Hamada and M. Yamada (2002): Bacterial distribution in hypertrophic surface waters, Dokai Bay, Japan. Umi to Sora, 78, 1–6 (in Japanese).

    Google Scholar 

  • Tanaka, T., N. Fujita and A. Taniguchi (1997): Predatory prey eddy in heterotrophic nanoflagellate-bacteria relationships in a coastal marine environment: a new scheme for predator-prey associations. Aquat. Microb. Ecol., 13, 249–256.

    Article  Google Scholar 

  • Turley, C. M. (1993): Direct estimates of bacterial numbers in seawater samples without incurring cell loss due to sample storage. p. 143–147. In Aquatic Microbial Ecology, ed. By P. F. Kemp, B. F. Sherr, E. B. Sherr and J. J. Cole, Lewis Publishers, New York.

    Google Scholar 

  • Valiela, I. (1995): Marine Ecological Processes. Springer-Verlag, New York, 686 pp.

    Google Scholar 

  • Vaque, D., M. L. Pace, S. Findlay and D. Lints (1992): Fate of bacterial production in a heterotrophic ecosystem: grazing by protists and metazoans in the Hudson Estuary. Mar. Ecol. Prog. Ser., 89, 155–163.

    Article  Google Scholar 

  • Vaque, D., J. M. Gasol and C. Marrase (1994): Grazing rates on bacteria: the significance of methodology and ecological factors. Mar. Ecol. Prog. Ser., 109, 263–274.

    Article  Google Scholar 

  • Welschmeyer, N. A. (1994): Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and phaeopigments. Limnol. Oceanogr., 39, 1985–1992.

    Article  Google Scholar 

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Kobari, T., Fujii, T., Kobari, Y. et al. Seasonal variations in abundance, growth and mortality of heterotrophic bacteria in Kagoshima Bay. J Oceanogr 66, 845–853 (2010). https://doi.org/10.1007/s10872-010-0068-y

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