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K . Jurgens et al. J. Exp. Mar. Biol. Ecol. 245 2000 127 –147
1. Introduction
About 30 of the surface of the Earth is covered by oligotrophic oceanic waters in which prokaryotes are the dominant primary and secondary producers of organic matter
Whitman et al., 1998. Determining the controlling factors of planktonic bacteria and their ecological interactions within the microbial food web is essential for an understand-
ing of the biogeochemical oceanic fluxes. Most studies examining these issues are from coastal and estuarine waters and comparatively few data exist for the open ocean.
However, some consistent features of the most oligotrophic systems emerged from studies of recent years: Heterotrophic bacteria constitute the major carbon pool in the
euphotic zone and this biomass can be several fold greater than phytoplankton biomass Cho and Azam, 1988; Fuhrman et al., 1989, leading to a different biomass food web
structure in oligotrophic compared to eutrophic systems Dortch and Packard, 1989; Gasol et al., 1997. The implications are also that bacterioplankton contribute sig-
nificantly to the particulate pools of inorganic nutrients N, P and affect light scattering and absorption phenomena in the open ocean Morel and Ahn, 1990. In most of the
oligotrophic subtropical and tropical oceanic areas also the primary producers are dominated by prokaryotic autotrophic picoplankton belonging to the taxa Prochlor-
ococcus Chisholm et al., 1988; Olson et al., 1990 and Synechococcus Waterbury et al., 1979; Burkill et al., 1993. Grazing by heterotrophic protists is assumed to be the
main loss factor of both heterotrophic and autotrophic picoplankton Wikner and
¨ Hagstrom, 1988; Landry et al., 1995; Reckermann and Veldhuis, 1997.
Whereas solid data exist meanwhile for the biomass distribution, much less is known about the population dynamics of the respective organism groups and how trophic
coupling between dissolved organic matter DOM, phytoplankton, bacteria, viruses and protozoa controls the carbon flux and biomass production of bacteria Azam et al.,
1994. It is important to understand these ecological interactions as they form the bases of the biogeochemical fluxes in the ocean. One research goal is to reveal the importance
of inorganic and organic substrates bottom-up control or predation top-down control as limiting factors for bacterial biomass e.g. Wright and Coffin, 1984; Ducklow et al.,
1992; Shiah and Ducklow, 1995. Strong evidence for bottom-up control of hetero- trophic bacteria has accumulated from open ocean studies. One line of evidence comes
from the fact that the addition of DOM often in combination with inorganic nutrients usually results in a stimulation of bacterial productivity in short-term microcosm
experiments Kirchman, 1990, Kirchman and Rich, 1997. Another line of evidence is the significant positive correlation between phytoplankton and bacterial biomass Cole et
al., 1988; Ducklow and Carlson, 1992; Dufour and Torreton, 1996, and between bacterial production and bacterial biomass Ducklow, 1992. Both correlations point
towards resource limitation as a mechanism of bacterial biomass regulation and imply that mean levels of bacterial biomass reflect the substrate supply or richness of the
system Billen et al., 1990.
Evidence for the other important regulating factor, grazing by bacterivores, comes from another temporal and spatial scale, generally different types of short-term
incubation experiments Weisse, 1989; Wikner et al., 1990. Heterotrophic nanoflagel- lates HNF in the size range 2–5 mm have also been identified for the open ocean as the
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. Jurgens et al. J. Exp. Mar. Biol. Ecol. 245 2000 127 –147 129
main bacterivorous grazers Fenchel, 1982b; Fuhrman and McManus, 1984; Rassoul- ¨
zadegan and Sheldon, 1986; Wikner and Hagstrom, 1988. The relevance of predation control of bacteria in oligotrophic systems remains, however, controversial and the
coupling between bacteria and bacterivores is not fully understood yet. This is partly due to the difficulty in obtaining precise measurements of bacterivory and biomass of
heterotrophic nanoplankton as these rates and standing stocks are extremely low. Some comparative analysis from different aquatic systems suggest that top-down regulation of
bacteria is more important in eutrophic and bottom-up control in oligotrophic environ- ments, although grazing and bacterial production are generally balanced Sanders et al.,
1992.
After the development of the ‘Microbial Loop’ concept, the prevailing picture was that a highly active and efficient protist grazer community controls bacterial abundance
and consumes new bacterial production, which eventually results in the rather constant and homogenous low bacterial abundance observed in the open ocean e.g. Ducklow,
1983. Efficient grazing control was also supported by experimental microcosm studies which revealed a close coupling between bacteria and bacterivores Wikner and
¨ Hagstrom, 1988; Weisse, 1989 and by substrate addition experiments in which bacterial
abundance remained relatively constant despite strong increases in bacterial production Kirchman, 1990; Kirchman and Rich, 1997. Even less is known about the importance
of grazing as a shaping factor for the phenotypic and genotypic bacterial community composition in oligotrophic systems. Studies in more productive coastal or freshwater
environments have demonstrated that bacterial grazing has an important impact in this
¨ ¨
respect Jurgens and Gude, 1994. The purpose of the present study was to examine the bacteria–protozoan coupling in
warm oligotrophic to ultra-oligotrophic ocean sites in microcosm experiments. Ex- perimental manipulations with substrate additions and size-fractionations were aimed at
stimulating bacterial production and increasing predation pressure by small bacterivores. We were specially interested in 1 revealing the response time of bacterivores to
increases in bacterial production and bacterial biomass, and 2 analysing the impact of grazers on bacterial size distribution and the appearance of grazing-resistant mor-
photypes in response to increased predation.
2. Material and methods
