Achievements in Biological Oceanography
Richard T. Barber and Anna K. Hilting
Duke University, NSOE Marine Laboratory
For the Ocean Studies Board's examination of achievements of the National Science Foundation (NSF) in ocean research, we have been asked "to focus on the landmark achievements in biological oceanography in the past 50 years, the individuals involved, the new technology and ideas that made these achievements possible, how one discovery built on the foundations of earlier ones, discoveries made at the intersections of disciplines, and the role that NSF programs and institutional arrangements had in making these achievements possible."
The period addressed, the first 50 years of the National Science Foundation, has been a heady time for biological oceanography, and identification of landmark achievements of this period is a fitting tribute for the 1998 International Year of the Ocean. The pace of biological investigation of the ocean quickened as this period began in the 1950s. To appreciate the magnitude of the acceleration, a brief look at biological oceanography in the first half of this century is useful.
Before World War II, biological oceanography had two main themes. The first and more important by far was as a handmaiden to fisheries science. Where were exploitable resources, why did they vary so in abundance, and how could more resources be found? These were the demanding questions asked of biological oceanography. These questions, particularly the old question of why recruitment to exploitable fish stocks varies so much from year to year and from place to place (Hjort, 1926), have proved to be profoundly complex questions that biological oceanography still struggles with today (cf. the current Global Ocean Ecosystems Dynamics [GLOBEC] program).
The second major theme was discovery per se. Exotic and strange animals, and to a lesser degree plants, commanded interest among scientists as well as the general public; they illustrated the marvels of adaptation and evolution. Exploration for its own sake has always motivated biological oceanographers, but as the discipline matured, this motivation became less fashionable. NSF has never supported biological oceanographers for the sole purpose of looking for strange new organisms, yet discovery is what makes biological oceanography so much fun.
After World War II the climate of oceanographic research was different. One of the authors (RTB) spent an undergraduate summer in Woods Hole in the mid-1950s, a time when the overriding impression was that there were many exciting questions and unlimited opportunities. Ideas newly aired then were the ecosystem constructs of the Odum brothers (Odum and Odum, 1955), the quantitative and predictive plankton studies of Riley (1946), and the elegant ecology and evolution theories of Hutchinson (1961); the brilliance of these ideas inspired students and researchers. The relative merits of applied versus basic research became a topic of frequent discussion. At the same time, the distance between biological oceanography and fisheries science widened here in the United States until, by the 1960s, there was little significant intellectual exchange between the two disciplines. A few iconoclastic individuals argued for studying ocean biology whether or not an application for the new knowledge could be envisioned, implying that knowledge per se was good.
In addition to knowledge for the sake of knowledge, there arose in the postwar period the specter of pollution and the notion that it was necessary to know how the ocean functioned to avoid inadvertently destroying it. All of these needs or objectives—food from the ocean, discovery, knowledge for its own sake, and the custodial sense arising from pollution concerns—provided motivations to expand and reshape the field. But by far the most important impetus driving the expansion of biological oceanography was the cornucopia of new resources available for science.
Financial resources that flowed to American science as a result of Sputnik, the scientific race with the Soviets, and the Cold War trickled down (or up) to biological oceanography. It should be noted that NSF made a conscious decision to support biological oceanography in the 1950s because it foresaw that biological oceanography was unlikely to receive support elsewhere, including the Office of Naval Research. These new resources drove the increase in basic, NSF-supported, research during this period. Responding to the increased supply of resources by recruiting young scientists in large numbers, biological oceanography became a discipline of its own and settled into a steady rate of progress and expansion. In this paper we identify nine landmark achievements of biological oceanography of the past 50 years and discuss who made them, their sequelae, and NSF's role in making them possible.
This review got its start in March 1998 at an NSF-sponsored retreat where a group of about 50 people pondered the future of biological oceanography; the exercise was called OEUVRE (Ocean Ecology: Understanding and Vision for Research). In considering what's exciting for the future of biological oceanography, there was a thorough and wide-ranging discussion of achievements of the past two or three decades. We have used the OEUVRE report liberally; its results are presented in the paper by Peter Jumars later in this volume.
Next we queried about 150 practicing biological oceanographers on their opinions of the landmark achievements of the past 50 years. Almost everyone responded to our query, and it was fascinating to see this thoughtful self-evaluation of our discipline. Organizing and collating the many replies was educational, but this informal survey did not lend itself to quantitative analysis. We also looked at citation indices (McIntosh, 1989; Parsons and Seki, 1995) but did not use this information because biological oceanography was not a specific category. In the end we made a subjective selection which was, for the most part, consistent with the suggestions provided by the community. We thank the respondents and acknowledge how much we learned from their replies, but we absolve them from responsibility for the following.
Because neither of the authors has formal training as a historian, we are in every sense amateurs at writing history. Our strongest, or perhaps weakest, characteristic is a passionate interest in biological oceanography and its history. Another important weakness is that we are practicing biological oceanographers. It is unrealistic to expect an objective history of baseball from players who are in the middle of a playoff game. Our paper is very subjective—interesting and informative, we hope, but not necessarily objective.
Selecting achievements to include was not difficult; the agonizing aspect was what to leave out. In biology there are many kinds of achievements. In this short paper we do not do justice to the diversity of biological oceanography. Also, as any NSF program manager in biological oceanography will tell you, there is no tidy framework for organizing the different parts of biological oceanography. Our list is therefore eclectic as well as subjective.
TWO WONDERFUL ACCIDENTS: VENTS AND OCEAN COLOR
We begin with two landmark achievements that more or less fell into the laps of biological oceanographers.
Chemosynthetic Hydrothermal Vent Communities (Plate 1)
This is an easy landmark to start with because it has all the dramatic elements of discovery. We may no longer set out on voyages of discovery, but in the past 50 years the pace of biological discovery has been awesome. In 1976, when geologists discovered the hydrothermal vents, biological oceanography received a much-appreciated jolt of intellectual stimulation (Corliss et al., 1979). The existence of a new kind of ecosystem with dramatic new biochemical adaptation fueled the imagination of everyone. The names associated with this pioneering work on chemosynthesis are a cross section of the gentry of biological oceanography. Cavenaugh, Childress, Grassle, Jannasch, Karl, Lutz, and Somero were early leaders in this work, but the list soon expanded to include several dozen individuals (see references below). From this work we learned how organisms adapt biochemically to temperature extremes and lack of oxygen, a line of investigation that has led to the discovery of active microbes deep in the Earth. This work also provides a rational organizing paradigm for the search for life on other celestial bodies.
What is amazing about the discovery of chemosynthetic ecosystems is that, once discovered, they have turned up everywhere in the ocean: on the continental shelves and slopes, in the deep sea, and at plate margins and ridge crests (Van Dover, 1990, 1998, 1999). They are hot vents or cold seeps; their reducing power comes from hydrogen sulfide or methane. Chemosynthetic ecosystems even exist on whale carcasses (Smith et al., 1989).
The mystery is how we overlooked these ubiquitous ocean ecosystems for so long, and we wonder what other surprises the ocean holds.
NSF's Biological Oceanography Program has been the lead agency in support of this work, and Alvin support by NSF made rapid progress possible. The disco, cry, response by scientists, and response by NSF provide a model of science at its best.
Chemosynthetic Hydrothermal Vent Communities References1
1979 Corliss, J.B., J. Dymond, L.I. Gordon, J.M. Edmond, R.P. van Herzen, R.D. Ballard, K. Green, D. Williams, A. Bainbridge, K. Crane, and T.H. van Andel. 1979. Submarine thermal springs on the Galapagos Rift. Science 203:1073-1083.
1979 Jannasch, H.W., and C.O. Wirsen. 1979. Chemosynthetic primary production at East Pacific sea floor spreading centers. BioScience 29:592-598.
1980 Karl, D.M., C.O. Wirsen, and H.W. Jannasch. 1980. Deep-sea primary production at the Galapagos hydrothermal vents. Science 207:1345-1347.
1981 Cavanaugh, C.M., S.L. Gardiner, M.L. Jones, H.W. Jannasch, and J.B. Waterbury. 1981. Procaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: Possible chemoautotrophic symbionts. Science 213:340-341.
1981 Felbeck, J., J.J. Childress, and G.N. Somero. 1981. Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphiderich habitats. Nature 293:291-293.
1983 Arp, A.J., and J.J. Childress. 1983. Sulfide binding by the blood of the hydrothermal vent tube worm Riftia pachyptila. Science 219:295-297.
1984 Lutz, R.A., R.D. Turner, and D. Jablonski. 1984. Larval development and dispersal at deep-sea hydrothermal vents. Science 226:1451-1454.
1985 Paull, C.K., B. Hecker, R. Cammeau, R.P. Freeman-Lynde, C. Neumann, W.P. Corso, S. Golubic, J.E. Hook, E. Sikes, and J. Curray. 1985. Biological communities at the Florida escarpment resemble hydrothermal vent taxa. Science 226:965-967.
1985 Grassle, J.F. 1985. Hydrothermal vent animals: Distribution and biology. Science 229:713-717.
1985 Okutani, T., and K. Egawa. 1985. The first underwater observation on living habitat and thanatocoenoses of Calyptogena soyoae in bathyal depth of Sagami Bay. Venus: Japanese Journal of Malacology 44:285-289.
1989 Smith, C.R., H. Kukert, R.A. Wheatcroft, P.A. Jumars, and J.W. Deming. 1989. Vent fauna on whale remains. Nature 341:27-28.
1990 Van Dover, C.L. 1990. Biogeography of hydrothermal vent communities along seafloor spreading centers. Trends in Ecology and Evolution 5:242-246.
1998 Van Dover, C.L. 1998. Vents at higher frequency. Nature 395:437-439.
1999 Van Dover, C.L. 1999. Deep-sea clams feel the heat. Nature 397:205-220.
Ocean Color—Seeing the Ocean for the First Time
The Coastal Zone Color Scanner (CZCS) launched in 1978 showed biological oceanographers the patterns, variability, complexity, and coherence of ocean biology for the first time. Biological oceanography became a global discipline in a single step. It is, of course, somewhat facetious to call this new satellite-based remote sensing capability an "accident." Far-sighted individuals such as Gift Ewing and Charlie Yentsch kept prodding the National Aeronautics and Space Administration (NASA) in the right direction; they provided an accurate vision of what could be. However, the real drivers in the early days were the spirit of NASA, its engineers, and their unquenchable drive to build whatever could be built and flown on satellites. Our reading of the event is that NASA was looking for challenges, and the quantitative assessment of ocean surface chlorophyll and related pigments by reflected light was a challenge they took on with enthusiasm. Ironically, biological oceanographers don't even know the names of these creative NASA engineers who built the CZCS, but that doesn't reduce our debt to them.
The first CZCS data of reflected light that became available in the late 1970s started a scramble to put together systems to process and interpret this new kind of data. The key algorithms produced at the University of Miami (Gordon and Clark, 1980; Gordon et al., 1983) were the "open sesame" that permitted biological oceanographers to see the ocean for the first time (see references below). As CZCS images flooded into our consciousness it became obvious that we needed to train a cohort of biological oceanographers who would know how to use the new technology. This hard work has paid off. When a new, much improved U.S. ocean color satellite Sea-Viewing Wide Field of View Sensor (Sea WiFS) (Plate 2) flew in August 1997, the community was ready. As a result, the pace of biological oceanography has quickened all around the globe.
The space-based analysis of chlorophyll concentration based on ocean color revealed (1) oceanography's chronic problem of undersampling; (2) dominance of mesoscale physical processes in determining the spatial distribution of phytoplankton; (3) effect of topography on biomass; (4) complexity of the seasonal progression of phytoplankton blooms; and (5) magnitude of interannual variability. Space-based analysis changed not only our perception of the ocean, but also our ideas of what constitutes good biological oceanography. Of the various landmark achievements mentioned here, this is one that profoundly affects all biological oceanographers and indeed each citizen of the planet. Having seen the totality of the oceans, mankind can no longer maintain the concept of discrete or isolated components of the ocean.
NASA, of course, was the major patron of this work, but NSF has been and remains an important supporter of the synthesis and interpretation of this exciting new way to view the ocean. This NASA-NSF cooperation is an example of science support at its best.
Ocean Color References
1980 Gordon, H., and D.K. Clark. 1980. Atmospheric effects in the remote sensing of phytoplankton pigments. Boundary-Layer Meteorol. 18:299-313.
1983 Gordon, H.R., D.K. Clark, J.W. Brown, O.B. Brown, R.H. Evans, and W.W. Broenkow. 1983. Phytoplankton pigment concentrations in the Middle Atlantic Bight: Comparison of ship determinations and CZCS estimates. Applied Optics 22:3929-3931.
1986 Esaias, W.E., G.D. Feldman, C.R. McClain, and J.A. Elrod. 1986. Monthly satellite-derived phytoplankton pigment distribution for the North Atlantic Ocean basin. Eos, Trans., AGU 67:835-837.
1987 Yoder, J.A, C. McClain, J. Blanton, and L. Oey. 1987. Spatial scales in CZCS-chlorophyll imagery of the southeastern U. S. continental shelf. Limnol. Oceanogr. 32:929-941.
1989 Feldman, G., N. Kuring, C. Ng, W. Esaias, C.R. McClain, J. Elrod, N. Maynard, D. Endres, R. Evans, J. Brown, S. Walsh, M. Carle, and G. Podesta. 1989. Ocean color, availability of the global data set. Eos, Trans., AGU 70:634-641.
1993 Sullivan, C.W., K.R. Arrigo, C.R. McClain, J.C. Comiso, and J. Firestone. 1993. Distributions of phytoplankton blooms in the Southern Ocean. Science 262:1832-1837.
1993 Yoder, J.A., C.R. McClain, G.C. Feldman, and W.E. Esaias. 1993. Annual cycles of phytoplankton chlorophyll concentrations in the global ocean: A satellite view. Global Biogeochem. Cycles 7:181-193.
Global Productivity and Productivity Regimes—The Stepchildren of Ocean Color
Soon after Steeman-Nielsen (1952) introduced the radioactive carbon tracer method to measure primary productivity, biological oceanographers began to use the new productivity observations to speculate about the existence of differing oceanic productivity regimes and to estimate global productivity (Ryther, 1959). Two signal achievements in the estimation of global productivity were Ryther's synthesis (1969) dealing with productivity in different oceanic regimes and the synthesis by Koblentz-Mishke et al. (1970) of all the available radiocarbon productivity data. Both contributions advanced biological oceanography, but under-sampling compromised both efforts.
Global CZCS chlorophyll coverage provided a way to break out of this sampling limitation using the productivity-chlorophyll-light relationship described first by Ryther and Yentsch (1957). High-resolution spatial and temporal patterns of phytoplankton biomass permitted objective estimates of global primary productivity (see references below) as well as the size and seasonal variability of the various productivity regimes or biogeochemical provinces of the world ocean (Longhurst, 1998). Arguably the most important scientific contributions of the satellite ocean color breakthrough to date have been improved estimates of global productivity and the birth of an objective ecological geography of the sea.
Global Productivity and Productivity Regimes References
1952 Steemann-Nielsen, E. 1952. The use of radioactive carbon (14C) for measuring organic production in the sea. J. Cons. Int. Explor. Mer 144:38-46.
1957 Ryther, J.H., and C.S. Yentsch. 1957. The estimation of phytoplankton production in the ocean from chlorophyll and light data. Limnol. Oceanogr. 2:281-286.
1959 Ryther, J.H. 1959. Potential productivity of the sea. Science 130: 602-608.
1969 Ryther, J.H. 1969. Photosynthesis and fish production in the sea. Science 166:72-76.
1970 Koblentz-Mishke, O.J., V.V. Volkovinsky, and J.G. Kabanova. 1970. Plankton primary production of the world ocean. Pp. 183-193 in W.S. Wooster (ed.), Scientific Exploration of the South Pacific . National Academy of Sciences, Washington, D.C.
1982 Smith, R.C., R.W. Eppley, and K.S. Baker. 1982. Correlation of primary production as measured aboard ship in southern California coastal waters and as estimated from satellite chlorophyll images. Mar. Biol. 66:281-288.
1985 Eppley, R.W., E. Stewart, M.R. Abbott, and V. Heyman. 1985. Estimating ocean primary production from satellite chlorophyll, introduction to regional differences and statistics for the Southern California Bight. J. Plankton Res. 7:57-70.
1988 Platt, T., and S. Sathyendranath. 1988. Oceanic primary production: Estimation by remote sensing at local and regional scales. Science 241:1613-1620.
1992 Balch, W.M., R. Evans, J. Brown, G. Feldman, C. McClain, and W. Esaias. 1992. The remote sensing of ocean primary productivity: Use of new data compilation to test satellite algorithms. J. Geophys. Res. 97:2279-2293.
1995 Longhurst, A., S. Sathyendranath, T. Platt, and C. Caverhill. 1995. An estimate of global primary production in the ocean from satellite radiometer data. J. Plankton Res. 17:1245-1271.
1996 Antoine, D., J.M. Morel, and A. Morel. 1996. Oceanic primary production. 2. Estimation at global scale from satellite (Coastal Zone Color Scanner chlorophyll). Global Biogeochem. Cycles 10:57-69.
1997 Behrenfeld, M.J., and P.G. Falkowski. 1997. Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr . 42:1-20.
1998 Longhurst, A. 1998. Ecological Geography of the Sea. Academic Press, San Diego, California. 398 p.
1999 Esaias, W.E., R.L. Iverson, and K. Turpie. 1999. Ocean province classification using ocean color data: Observing biological signatures of variations in physical dynamics. Global Change Biology, in press.
1999 Iverson, R.L., W.E. Esaias, and K. Turpie. 1999. Ocean annual phytoplankton carbon and new production, and annual export production estimated with empirical equations and CZCS data. Global Change Biology , in press.
FOUR SPECIFIC BREAKTHROUGHS
The discovery of high biological diversity in the deep sea in the late 1960s changed the way deep-sea biology was viewed, and sparked theoretical debates on how diversity is maintained in a large, monotonous environment such as the deep sea (see references below). The diversity analyses, set in motion in the 1960s by Howard Sanders and Bob Hessler, were followed up by Paul Dayton, Fred Grassle, Gil Rowe, and Pete Jumars. This work was enhanced by the availability of the submersible Alvin, which gave researchers direct observation and the ability to do in situ benthie experiments. The skill these early workers gained in using Alvin for diversity and metabolic studies made it possible for them to shift rapidly to work on the hydrothermal vents soon after their discovery in 1976.
Alvin changed our perception of the deep sea just as the CZCS satellite changed our perception of the surface ocean. Images of the seafloor—particularly the monotonous, soft-sediment abyssal regimes—documented how different the
deep-sea environment is from any other that ecologists have visited.
The discovery of high diversity in the deep sea was critically important to the evolution and maturation of biological oceanography because it provided scientific respectability to this expensive research. Deep-sea animals were found to be interesting and sometimes weird, as National Geographic articles frequently reminded us, but of what relevance was deep-sea ecology? The discussion of diversity thrust deep-sea research into a mainstream ecology debate that was important and exciting. This development was pivotal because NSF is most comfortable supporting hypothesis-driven research on questions that are significant to mainstream science. After Howie Sanders and Bob Hessler published on deep-sea diversity (Sanders, 1967; Hessler and Sanders, 1969; Sanders and Hessler, 1967; Dayton and Hessler, 1972; Grassle and Sanders, 1973), there were abundant hypotheses to be tested, and tested they were. The Biological Oceanography Program at NSF was, and still is, the major supporter of this work.
Deep-Sea Diversity References
1967 Hessler, R.R., and H.L. Sanders. 1967. Faunal diversity in the deep-sea. Deep-Sea Res. 14:65-78.
1968 Sanders, H.L. 1968. Marine benthic diversity: A comparative study. Am. Natur. 102:243-282.
1969 Rowe, G.T., and R.J. Menzies. 1969. Zonation of large benthic invertebrates in the deep-sea off the Carolinas. Deep-Sea Res. 16:531-537.
1969 Sanders, H.L., and R.R. Hessler. 1969. Ecology of the deep-sea benthos. Science 163:1419-1424.
1972 Dayton, P.K., and R.R. Hessler. 1972. Role of biological disturbance in maintaining diversity in the deep sea. Deep-Sea Res. 19:199-208.
1973 Grassle, J.F., and H.L. Sanders. 1973. Life histories and the role of disturbance. Deep-Sea Res. 20:643-659.
1976 Jumars, P.A. 1976. Deep-sea species diversity: Does it have a characteristic scale? J. Mar. Res. 34:217-246.
New and Regenerated Productivity
This landmark achievement had its origin in a Limnology and Oceanography publication by Dugdale and Goering (1967) that introduced a deceptively simple notion: primary productivity in the ocean can be divided into the portion that uses locally recycled nutrients (regenerated production) and the portion that uses nutrients newly transported into the euphotic zone (new production), usually by the physical processes of mixing and upwelling. Dugdale and Goering's exciting and powerful concept was presented in very basic terms and specifically included ''new" nutrients entering from the atmosphere, a process that was not considered important in 1967 but is now known to be significant.
The new production concept, together with the Dugdale (1967) paper on nutrient uptake dynamics in the same issue of Limnology and Oceanography , provided biological oceanography with the mathematical formalism needed for rigorous, quantitative modeling of ocean productivity and biogeochemical fluxes. (See also Eppley et al., 1969; MacIsaac and Dugdale, 1969.) This formalism fueled the explosive growth of modeling described in the modeling section later in this paper.
Eppley and Peterson (1979) further developed the concept by arguing that at steady state the magnitude of new production is equal to the export flux of particulate organic matter out of the euphotic zone to the ocean interior. Together, the Dugdale and Goering (1967) and Eppley and Peterson (1979) papers have impressive citation index scores. At the ages of 31 and 19 years, respectively, they are cited more now than they were in their first decades. They are like fine wines. Significantly, Eppley and Peterson (1979) estimated global new production to be about 4 petagrams per year and suggested for the first time that this number approximates the sinking flux of organic carbon and, hence, the rate at which the deep sea sequesters atmospheric carbon dioxide. This number has proved very durable; it is still used in global biogeochemical budgets.
As a consequence of the work of Dugdale and Goering (1967) and Eppley and Peterson (1979), a link was forged between physical and biological oceanography. The new concept required that physical processes of mixing and upwelling be an integral part of ecosystem models dealing with new production, fish production, or export of organic material from the surface layer. Ocean physics and biology were formally wed by this landmark achievement.
The technological advance that made progress on new production possible was the use of a stable isotope tracer 15N and a mass spectrometer to measure it precisely. The 15N tracer method was a logical development of Steemann-Nielsen's (1952) breakthrough use of 14C as a tracer of carbon fixation.
Dugdale and Goering's work was supported by the NSF International Indian Ocean Expedition and its successor program, the Southeastern Pacific Expedition, using the NSF ship Anton Bruun for focused biological oceanography. The NSF decision to fund this vessel specifically for biological oceanography was a decision that had positive long-range consequences for the field. In addition to expeditionary support from NSF, laboratory support came from the Atomic Energy Commission (AEC), now the Department of Energy (DOE). In the 1960s and 1970s, NSF and AEC had a productive partnership, with NSF providing focused investigator and expedition awards and AEC providing block grants to support research groups. Dugdale and Goering went to sea with John Ryther's AEC-supported research group at the Woods Hole Oceanographic Institution. Eppley was a member of J.D.H. Strickland's AEC group at Scripps Institution of Oceanography and headed this group later during its most productive years. However, NSF was the lead agency responsible for this breakthrough and the agency should take great pride in this landmark achievement.
New and Regenerated Productivity References
1967 Dugdale, R.C., and J.J. Goering. 1967. Uptake of new and regenerated forms of nitrogen in primary production. Limnol. Oceanogr. 12:196-206.
1967 Dugdale, R.C. 1967. Nutrient limitation in the sea: Dynamics, identification and significance. Limnol. Oceanogr. 12:655-695.
1969 MacIsaac, J.J., and R.C. Dugdale. 1969. The kinetics of nitrate and ammonia uptake by natural populations of marine phytoplankton. Deep-Sea Res. 16:47-58.
1969 Eppley, R.W., J.N. Rogers, and J.J. McCarthy. 1969. Half-saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnol. Oceanogr. 14:912-920.
1979 Eppley R.W., and B.J. Peterson. 1979. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282:677-680.
How Zooplankton Swim, Feed, and Breed
Zooplankton live in a medium that, to them, is viscous and structured (Koehl, 1993). The process of capturing food does not involve passive sieving as much as it involves purposeful ingestion of particular food targets (see references below). Phytoplankton and other tasty prey items leave a chemical trail in the viscous water, and zooplankton follow such trails to find and eat a particular victim. Data suggest that the same process is at work in finding mates (Howlett, 1998; Yen et al., 1998). This view of the zooplankton world strains our credulity: because of our size, we cannot easily comprehend the low Reynolds number world in which zooplankton—especially copepods and smaller—swim, feed, and breed. This work showed us a world that is very common on our planet, but beyond our ken.
This new understanding has come in large part from the intellectual prodding of a single individual, Rudy Strickler, although he has had some very capable collaborators such as Mimi Koehl, Gus Paffenhöfer, Holly Price, Jeanette Yen, and others. A fascinating thing about this breakthrough is that it was immediately adopted by the field and entrained into the mainstream ideas. Zooplankton "gurus" such as Bruce Frost, Charlie Miller, Mike Roman, Sharon Smith, and Peter Wiebe had prepared the way for rapid assimilation of these new ideas by arguing that zooplankton feeding is selective and purposeful. Miller, in particular, had long emphasized that copepods fed in a viscous medium. Strickler's innovative high-speed movies of live copepod feeding showed how selectivity is realized. The technical breakthrough that made this advance possible was microcinematography. In this case, live copepods superglued to a dog hair on a microscope slide were filmed with a high-speed, strobe movie camera focused on the tethered animal. Innovation has many faces. NSF was the major source of support for this innovative work, which is continuing at an accelerated pace, but the Office of Naval Research (ONR) has also been a significant patron.
How Zooplankton Swim, Feed, and Breed References
1977 Hamner, P., and W.M. Hamner. 1977. Chemosensory tracking of scent trails by the planktonic shrimp Acetes sibogae australis. Science 195:886-888.
1977 Rubenstein, D.I., and M.A.R. Koehl. 1977. The mechanisms of filter feeding: Some theoretical considerations. Amer. Nat. 111:981-994.
1980 Alcaraz, M., G.A. Paffenhöfer, and J.R. Strickler. 1980. Catching the algae: A first account of visual observations on filter feeding calanoids. Pp. 241-248 in W.C. Kerfoot (ed.), Evolution and Ecology of Zooplankton Communities. University Press of New England, Biddefort, Maine.
1981 Koehl, M.A.R., and J.R. Strickler. 1981. Copepod feeding currents: Food capture at low Reynolds number. Limnol. Oceanogr. 26:1062-1073.
1982 Paffenhöfer, G.A., J.R. Strickler, and M. Alcaraz. 1982. Suspension-feeding by herbivorous calanoid copepods: A cinematographic study. Mar. Biol . 67:193-199.
1982 Strickler, J.R. 1982. Calanoid copepods, feeding currents, and the role of gravity. Science 218:158-160.
1983 Price, J.J., G.A. Paffenhöfer, and J.R. Strickler. 1983. Modes of cell capture in calanoid copepods. Limnol. Oceanogr. 28:116-123.
1993 Koehl, M.A.R. 1993. Hairy little legs: Feeding, smelling, and swimming at low Reynolds number. Contemp Math. 141:33-64.
1998 Howlett, R. 1998. Sex and the single copepod. Nature 394:423-425.
1998 Yen, J., M.J. Weissburg, and M.H. Doall. 1998 The fluid physics of signal perception by mate-tracking copepods. Phil. Trans. R. Soc. Lond. 353:787-804.
The iron issue is an example of classic science progress:
There was a nagging question.
A tentative explanation was advanced.
Available data did not support the explanation.
The data, however, were suspect.
A technical (analytical) breakthrough was made.
The new data suggested an hypothesis.
The hypothesis was tested and confirmed.
Textbooks had to be revised.
For the iron issue the nagging question was: Why do excess plant nutrients persist in the surface ocean in certain regions such as the Antarctic, equatorial Pacific, and Northeast Pacific? For 50 years there had been speculation that iron limitation might be a factor, but measurements showed there was abundant iron in seawater.
John Martin set out to improve the analytical chemistry of iron, and when he had done so, he found that iron was much less abundant in the ocean than previously thought. Martin's innovations in iron chemistry alone would have earned him a place in history, but John Martin continued his quest with great zest. In a 1990 paper in Paleoceanography , he published the "Iron Hypothesis," which proposed that glacial-interglacial changes in atmospheric carbon dioxide were driven by variations in dryness, dust, and iron that forced
variations in new production and, hence, atmospheric carbon dioxide drawdown in Antarctic waters.
The rest of this story is well known. John Martin gained considerable media attention with the radical notion that iron addition in the Southern Ocean could be used to "engineer down" atmospheric carbon dioxide. This marked the first time that biological oceanography per se commanded prime-time media attention, and it was no surprise that Martin's proposed iron enrichment method to draw down atmospheric CO2 met with considerable negative publicity and was unpopular with biological oceanographers, environmentalists, and federal agencies. Martin himself kept his radical notion, which he always mentioned with a playful grin, separate from his serious determination to test the Iron Hypothesis. His critics did not or would not recognize this distinction.
John H. Martin died in June 1993, but his iron hypothesis was tested successfully in an in situ transient iron enrichment experiment in September 1993 (Martin et al., 1994) and again in May 1995 (Coale et al., 1996). It has now become evident that iron is a limiting or regulating nutrient in many marine and freshwater habitats for many organisms, not just primary producers. At a recent American Society of Limnology and Oceanography (ASLO) meeting on aquatic sciences more than 50 papers referred to iron effects. As with the ubiquity of chemosynthetic ecosystems, the question is, How could we have missed the importance of iron for so long?
Martin's proposed research to test the iron hypothesis with an in situ transient iron addition in the equatorial Pacific Ocean was controversial from the start (Chisholm, 1995). There was significant opposition because of worries that confirmation of the hypothesis would lead immediately to reckless climate engineering. Furthermore, no one had ever modified and marked a patch of open-ocean water, and many oceanographers were dead certain that it couldn't be done. Two courageous program managers, Ed Green of ONR and Neil Anderson of NSF, devised a Byzantine funding arrangement to get Martin's experiment done despite their agencies' aversion to controversy. Without heroic efforts by these two individuals, the rapid progress in testing the Iron Hypothesis would not have taken place. It is regrettable that at present there are no in situ iron experiment projects under way by U.S. investigators; fortunately, other countries are forging ahead boldly with work in the Antarctic and North Pacific oceans.
Iron Hypothesis References
1990 Martin, J.H. 1990. Glacial-interglacial CO2 change: The iron hypothesis. Paleoceanography 5:1-13.
1994 Martin, J.H., et al. 1994. Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 371:123-129.
1995 Chisholm, S.W. 1995. The iron hypothesis: Basic research meets environmental policy. Reviews of Geophysics 33:1277-1288.
1996 Coale, K.H. et al. 1996. A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial eastern Pacific Ocean. Nature 383:495-501.
INDIVIDUAL INVESTIGATORS VERSUS TEAMS
Work on the preceding achievements was set in motion and doggedly pursued by individual investigators: deep-sea diversity by Howard Sanders and Bob Hessler; new and regenerated productivity by Dick Dugdale and Dick Eppley; zooplankton milieu by Rudy Strickler; and the iron hypothesis by John Martin. Of course, science in general (and oceanography, in particular) is a team activity, and these individuals had important and essential collaborators, but for the breakthroughs described here, these individual investigators were key to the achievement. In this context, these achievements are quite unlike the first two—the discovery of vents and the gaining of a global perspective through satellite imagery—and the following three, all of which were set in motion by teams.
THE MOST FAR REACHING ACHIEVEMENT
Recognizing the Microbial Character of the Pelagic Food web
Over the past 25 years our vision of the pelagic food web structure has changed dramatically. We now view the traditional "diatom-copepod-fish" foodweb as a relatively minor component. The food web consistently present in all oceanic habitats is based on pico-and nanoplankton-sized autotrophs and heterotrophs, which are efficiently grazed by flagellates and ciliates. The pelagic food web is microbe-centric. ("Microbe" in this context means small autotrophs, heterotrophs, and mixotrophs, and refers to both prokaryotes and eukaryotes.) Pioneering work by Malone (1971) introduced these ideas regarding picoplankton productivity and micrograzer regulation, but it was not until the late 1970s that this revolution gathered momentum.
The microbial revolution was the easiest achievement to select. In our informal survey it was by far the first choice for inclusion as a landmark achievement, and it was the accomplishment that one of the authors (RTB) suggested at the OEUVRE meeting as the major advance of the past 20 years. There is wide consensus that the microbial revolution is of paramount importance for biological oceanography. It is a revolution still in progress and it appears to be different things to different people (Azam, 1998; Steele, 1998).
In 1974, Larry Pomeroy's paper titled "The Ocean's Food Web: A Changing Paradigm" foretold the microbial revolution by asking a logical sequence of questions:
Do small autotrophs carry out a major portion of oceanic primary production?
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.
Recognizing the Microbial Character of the Pelagic Food web References
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.
Dissolved Organic Carbon (DOC) References:
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.
1993 Peltzer, E.T., and P.G. Brewer. 1993. Some practical aspects of measuring DOC-sampling artifacts and analytical problems with marine samples. Marine Chemistry 41:243-252.
1993 Sharp, J. 1993. The dissolved organic carbon controversy: An update . Oceanography 6:45-50.
TWO NEW AVENUES TO UNDERSTANDING
The six achievements described above were revolutionary in that they each overturned an old consensus and forced a new reality suddenly onto center stage. Revolutions are fun, particularly for the young at heart, but they are not the only route to scientific progress. The achievements discussed next are evolutionary, rather than revolutionary, in that they consist of steady, stepwise increases in knowledge and understanding. In addition, they involve many individuals; the advance cannot be credited to any one person.
A subtle, but pervasive, achievement of biological oceanography is that modeling has become a mainstream activity; it permeates so much of our work that graduate students in the discipline assume it is integral to biological oceanography. Modeling was at one time an esoteric craft practiced by a gifted few; now it is the norm. Today's biological oceanography graduate student is more likely to have a model than a microscope.
The evolution from Gordon Riley's original models, which were "run" by hand calculation, according to one enduring myth of biological oceanography, to the numerous coupled global ocean-atmosphere-biota models now running is marked by steady advances. A select number of contributors after Riley made improvements, added complexity, and incorporated more sophisticated forcing. The line from Riley (1946) led through John Steele (1959 and 1974), whose slim volume The Structure of Marine Ecosystems (1974) enticed mathematicians, physicists, and physical oceanographers to try their hand at the new craft. Even today one usually finds Steele's volume on the shelves of individuals recruited to biological modeling from the physical sciences.
With new talent entering the field, modeling gathered momentum in the 1970s and 1980s (Walsh, 1975; Jamart et al., 1977; Steele and Frost, 1977; Wroblewski, 1977; Evans and Parslow, 1985; Hofmann, 1988). Genealogies of modeling accomplishments in biological oceanography, impossibly difficult to construct, would be marked by lots of branching and fusion. One important milestone, the Fasham Model (Fasham et al., 1990), was an upper-ocean ecosystem model that was widely distributed by its generous originators. Dozens, if not hundreds, of researchers adapted the Fasham Model to their own ends; this was the code that caused a bloom of biological oceanography models in small computers around the world. One particularly influential application of the Fasham Model that demonstrated the power of physical-biological models was a seasonal North Atlantic ecosystem study by Sarmiento et al. (1993).
Biological oceanography modeling is at the forefront of modeling in a number of areas: the use of data assimilation, coupled physical-biological models, single-species population models, ecosystem models, and the use of massively parallel supercomputers to simulate biogeochemical processes in general circulation models (Hofmann and Lascara, 1998).
The growth of modeling is aptly demonstrated in Brink and Robinson (1998), The Sea, Volume 10, which has three chapters dealing with various aspects of interdisciplinary modeling of the coastal ocean. Together, these three chapters have 371 references. The growth of this area of biological oceanography exceeds the assimilative capacity of a single individual.
NSF programs such as GLOBEC and the Joint Global Ocean Flux Study (JGOFS) are making a significant investment in modeling, but there persists some uncertainty about the best way to manage this powerful new research activity to ensure that the sum of its parts will be realized.
1946 Riley, G.A. 1946. Factors controlling phytoplankton populations on Georges Bank. J. Mar. Res. 6:54-73.
1949 Riley, G.A., H. Stommel, and D.F. Bumpus. 1949. Quantitative ecology of the plankton of the western North Atlantic. Bull. Bingham Oceanog. 12(3):1-169.
1959 Steele, J.H. 1959. The quantitative ecology of marine phytoplankton. Biol. Rev. 34:129-158.
1974 Steele, J.H. 1974. The Structure of Marine Ecosystems. Harvard University Press, Cambridge, Mass. 128 pp.
1975 Walsh, J.J. 1975. A spatial simulation model of the Peru upwelling ecosystem. Deep-Sea Res. 22:201-236.
1977 Jamart, B.B., D.F. Winter, K. Banse, G.C. Anderson, and R.K. Lam. 1977. A theoretical study of phytoplankton growth and nutrient distribution in the Pacific Ocean off the northwest U.S. coast. Deep-Sea Res. 24:753-773.
1977 Steele, J.H., and B.W. Frost. 1977. The structure of plankton communities. Phil. Trans. Roy. Soc. Lond. 280:485-534.
1977 Wroblewski, J.J. 1977. A model of phytoplankton plume formation during variable Oregon upwelling . J. Mar. Res. 35:357-394.
1985 Evans, G.T., and J.S. Parslow. 1985. A model of annual plankton cycles. Biological Oceanography 3:327-347.
1987 Frost, B.W. 1987. Grazing control of phytoplankton stock in the open subarctic Pacific Ocean: A model assessing the role of mesozooplankton, particularly the large calanoid copepods, Neocalanus spp. Mar. Ecol. Prog. Ser. 39:49-68.
1988 Hofmann, E.E. 1988. Plankton dynamics on the outer southeastern U.S. continental shelf. III. A coupled physical-biological model. J. Mar. Res. 46:919-946.
1990 Fasham, M.J.R., H.W. Ducklow, and S.M. McKelvie. 1990. A nitrogen-based model of plankton dynamics in the oceanic mixed layer. J. Mar. Res . 48:591-639.
1993 Sarmiento, J.L., R.D. Slater, M.J.R. Fasham, H.W. Ducklow, J.R. Toggweiler, and G.T. Evans. 1993. A seasonal three-dimensional ecosystem model of nitrogen cycling in the North Atlantic euphotic zone. Global Biogeochem. Cycles 7:417-450.
1998 Brink, K.H., and A.R. Robinson (eds.). 1998. The Sea, Vol. 10,
The Global Coastal Ocean Processes and Methods. John Wiley & Sons, Inc., New York, 604 pp.
1998 Hofmann, E.E., and C.M. Lascara. 1998. Overview of interdisciplinary modeling for marine ecosystems. Chapter 19, pp. 507-540 in K.H. Brink and A.R. Robinson (eds.), The Sea, Vol. 10, The Global Coastal Ocean Processes and Methods. John Wiley & Sons, Inc., New York.
1998 Steele, J.H. 1998. Incorporating the microbial loop in a simple plankton model. Proc. Roy. Soc. Lond. B 265:1771-1777.
In Situ Observations and Experiments
When Jacques Cousteau first lured people under the sea, marine biologists joined the activity with enthusiasm. Scientific advances from these new in situ observations remained modest until biologists ventured into the pelagic realm. Once there, they found a world that had no counterpart in the mangled samples harvested by nets or water collection bottles (Alldredge, 1972; Madin, 1974; Hamner, 1975). Transparent and iridescent organisms, large and small, were abundant (Hamner et al., 1978). Organic aggregates were ubiquitous, and these large, gossamer structures were found to have very high rates of microbial activity (Silver and Alldredge, 1981; Caron et al., 1982). The aggregates appear to be self-contained biospheres with populations of producers and consumers living together. In situ observations by divers, submersibles, and remotely operated vehicles (ROVs) revealed a great diversity of large plank-tonic organisms, particularly cnidaria, ctenophores, and salps (Robison, 1995) (Plate 4). Some of these are so delicate that they disintegrate in the wake of a swim fin; others are as tough as shoe leather. In situ observations showed that the pelagic realm is anything but barren or boring.
A characteristic that is very much a part of being a biologist is the inclination to give nature a gentle prod and watch the response. Connell (1961) and Paine (1966) used manipulation of intertidal communities to establish the hugely successful field of experimental marine ecology. From this work we have learned many rules about how communities are structured. Thirty years after Connell and Paine, Martin's successful in situ open-ocean experiment was carried out by adding iron to a 64-km2 patch of the equatorial Pacific and following the enriched patch for about 10 days (Martin et al., 1994). Interest in the confirmation of the Iron Hypothesis overshadowed the demonstration by this work that open-ocean experiments can be done. Just as in situ observations have revealed a biology that bottles and nets cannot capture, in situ experiments in the open ocean will reveal how intact, pelagic communities respond to environmental variations. When in situ ocean experimentation is coupled with in situ sensors and data assimilation (von Alt and Grassle, 1992), our discipline will have reached the end of its adolescence. Experimental intertidal marine ecology is very much a mainstream research activity; experimental biological oceanography is still only a glimmer in the eye of a few visionaries.
Both in situ ocean observations and in situ ocean experiments are unorthodox by the standards of traditional biological oceanography. However, the exciting new insights that resulted from work in both areas showed that NSF was wise to support this unconventional and risky research.
In Situ Observations References
1972 Alldredge, A.L. 1972. Abandoned larvacean houses: A unique food source in the pelagic environment. Science 177:885-887.
1974 Madin, L.P. 1974. Field observations on the feeding behavior of salps (Tunicata: Thaliacea). Mar. Biol. 25:143-148.
1975 Hamner, W.M. 1975. Underwater observations of blue-water plankton. Logistics, techniques, and safety procedures for divers at sea. Limnol. Oceanogr. 20:1045-1051.
1978 Hamner, W.M., L.P. Madin, A.L. Alldredge, R.W. Gilmer, and P.P. Hamner. 1978. Underwater observations of gelatinous zoo-plankton: Sampling problems, feeding biology and behavior. Limnol. Oceanogr. 20:907-917.
1981 Silver, M.W., and A.L. Alldredge. 1981. Bathypelagic marine snow: Vertical transport system and deep-sea algal and detrital community. J. Mar. Res. 39:501-530.
1982 Caron, D.A., P.G. Davis, L.P. Madin, and J. McN. Sieburth. 1982. Heterotrophic bacteria and bacterivorous protozoa in oceanic aggregates. Science 218:795-797.
1995 Robison, B.H. 1995. Light in the ocean's midwaters. Scientific American (July):60-65.
In Situ Experiments References
1961 Connell, J.H. 1961. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42:710-723.
1966 Paine, R.T. 1966. Food web complexity and species diversity. Am. Nat. 100:65-75.
1992 von Alt, C.J., and J.F. Grassle. 1992. LEO-15—An unmanned long term observatory. Proc. Oceans '92 2:829-854.
1994 Martin, J.H., et al. 1994. Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 371: 123-129.
1996 Coale, K.H., et al. 1996. A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization' experiment in the equatorial eastern Pacific Ocean. Nature 383 495-501.
Reading over our selection of landmark achievements, we note with chagrin that we have failed to cite the achievements of the one individual, Alfred Redfield. who was most responsible for the dramatic advance of biological oceanography in the past 50 years. His groundbreaking work gave biological oceanographers both the Redfield Ratio and Redfield's Rule (Redfield, 1958). We acknowledge that all of the biological oceanographers cited in thing paper had the advantage of standing on Redfield's broad shoulders.
We have also failed to cite the work of a series of exceptionally productive biological oceanographers who were multi-faceted leaders. Mikhail Vinogradov, [)avid Cushing, Gotthilf Hempel, Ramon Margalef, Akihiko Hattori, Achim Minas, André Morel, and Takahisa Nemoto are individuals whose overarching leadership left an indelible mark on bio
logical oceanography. These individuals all led expeditions, directed laboratories, made important scholarly contributions, and at the same time were mentors to a generation of talented biological oceanographers. The significant contributions of these individuals to biological oceanography will have to be recognized at a future opportunity.
References Not Mentioned Under Specific Landmarks
1926 Hjort, J. 1926. Fluctuations in the year classes of important food fishes. J. Cons. Int. Explor. Mer. 1:1-38.
1955 Odum, H.T., and E.P. Odum. 1955. Trophic structure and productivity at a windward coral reef community on Eniwetok Atoll. Ecol. Monogr. 25:291-320.
1958 Redfield, A.C. 1958. The biological control of chemical factors in the environment. Amer. Scientist 46:205-221.
1961 Hutchinson, G.E. 1961. The paradox of the plankton. Amer. Nat . 95:137-145.
1989 Cushing, D.H. 1989. A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified. J. Plankton Res. 11:1-13.
1989 McIntosh, R.P. 1989. Citation classics of ecology. The Quarterly Review of Biology 64:31-49.
1995 Parsons, T.R., and H. Seki. 1995. A historical perspective of biological studies in the ocean. Aquat. Living Resour. 8:113-122.