• Is nonliving organic matter, both dissolved and particulate, an important link in oceanic food webs?

• Do protist grazers such as ciliates and flagellates play a major role in grazing the autotrophic and heterotrophic microbes?

• Is leakage during feeding an important source of new dissolved organic material for heterotrophic microbes?

• Do microbes carry out the bulk of the respiration in the oceanic food web?

• Is recycling by the microbial food web a significant fate for newly produced organic matter?

At the time he asked them, Pomeroy's questions were unanswerable because of technical constraints. The saga of the microbial loop tells how one after another methodological advance allowed Pomeroy's questions to be answered. Hobbie et al. (1977) developed the fluorescent staining technique that permitted rapid counting and discrimination of bacteria, protozoa, and phytoplankton. The bacteria numbers found were high, but relatively constant. Bacterial production measured by Azam et al. (1983) was surprisingly high. Landry and Hassett (1982) and Fenchel (1982) found that protistan micrograzers provided the grazing mortality that held bacteria and picoautotrophs to relatively constant values. Rapidly growing micrograzers keep up with increases in growth rate of their bacterial and phytoplankton prey but never "overgraze" the prey because of threshold effects that make it unprofitable for micrograzers to feed when prey density drops below a given value.

The next step was to identify the source and magnitude of organic substrates for the heterotrophs. Measurement of dissolved organic carbon (DOC) was in disarray in 1974 when these questions were posed, but with a strong community effort supported by NSF, the DOC problem was painstakingly solved (Williams and Druffel, 1988; Peltzer and Brewer, 1993; Sharp, 1993). The presence of rapid DOC recycling was confirmed and other questions relative to DOC and bacterial production were rapidly solved (Ducklow and Carlson, 1992; Hansell et al., 1993).

In the mid-1980s, the new technology of flow cytometry enabled Chisholm et al. (1988, 1992) to discover a novel picoplankter that is now considered the most abundant autotroph in the world. How could we have overlooked these abundant organisms for so long?

Further work on micrograzer rates (Landry and Hassett, 1982; Landry et al., 1997) showed that grazer control of the pica-and nanophytoplankton was the norm and recycling by the microbial food web is a significant fate for primary production in the open ocean. Hard work and technical breakthroughs have confirmed most of the suggestions of Pomeroy (1974). Plate 3a shows how Steele (1998) entrained these ideas into a model of the pelagic food web; Plate 3b shows another representation of the concept. The Biological Oceanography Program at NSF was the major patron of the work that led this revolution. The response of NSF to the microbial revolution showed that this agency could adapt rapidly to a changing paradigm.

1971 Malone, T. 1971. The relative importance of nanoplankton and netplankton as primary producers in tropical oceanic and neritic phytoplankton communities. Limnol. Oceanogr. 16:633-639.

1974 Pomeroy, L.R. 1974. The ocean's food web, a changing paradigm. BioScience 24:499-504.

1977 Hobbie, J.E., R. I. Daley, and J. Jasper. 1977. Use of nucleopore filters for counting bacteria by fluorescence microscopy. Appl. Env. Microbial. 33:1225-1228.

1980 Fuhrman, J.A., J.W. Ammerman, and F. Azam. 1980. Bacterioplankton in the coastal euphotic zone: Distribution, activity and possible relationships with phytoplankton. Mar. Biol. 60:201-207.

1981 Williams, P.J. Le B. 1981. Incorporation of microheterotrophic processes into the classical paradigm of the planktonic food web. Kieler Meeresforschung 5:1-28.

1982 Fenchel, T. 1982. Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as bacterial consumers. Mar. Ecol. Prog. Ser. 9:35-42.

1982 Fuhrman, J.A., and F. Azam. 1982. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: Evaluation and field results. Mar. Biol. 66:109-120.

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

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

1988 Chisholm, S.W., R.J. Olson, E.R. Zettler, R. Goericke, J.B. Waterbury, and N.A. Welschmeyer. 1988. A novel free-living prochlorophyte abundant in the oceanic euphotic zone . Nature 334:340-343.

1992 Chisholm, S.W. et al. 1992. Prochlorococcus marinus nov. gen. nov. sp.: An oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Arch. Microbial. 157:297-300.

1992 Ducklow, H.W., and C.A. Carlson. 1992. Oceanic bacterial production. Advances in Microbial Ecology 12:113-181.

1995 Landry, M.R., J. Kirshtein, and J. Constantinou 1995. A refined dilution technique for measuring the community grazing impact of microzooplankton, with experimental tests in the central equatorial Pacific. Mar. Ecol. Prog. Ser. 120:53-63

1997 Landry, M.R., R.T. Barber, R.R. Bidigare, F. Chai, K.H. Coale, H.G. Dam, M.R. Lewis, S.T. Lindley, J.J. McCarthy, M.R. Roman, D.K. Stoecker, P.G. Verity, and R.T. White. 1997. Iron and grazing constraints on primary production in the central equatorial Pacific: An EqPac synthesis. Limnol. Oceanogr. 42:405-418.

1998 Azam, F. 1998. Microbial control of oceanic :arbon flux: The plot thickens. Science 280:694-696.

1998 Steele, J.H. 1998. Incorporating the microbia loop in a simple plankton model. Proc. Roy. Sac. Land. B 265:1771-1777.

1988 Williams, P.M., and E.R.M. Druffel. 1988. Dissolved organic matter in the ocean: Comments on a controvers. Oceanography 1:14-17.

1993 Hansell, D.A., P.M. Williams, and B.B. Ward. 1993. Comparative analyses of DOC and DON in the Southern, California Bight using oxidation by high temperature combustion. Deep-Sea Res. 40:219-234.