Questions for the futureINTRODUCTIONWe have reviewed the dynamics of marine ecosystems from three perspectives.In Chapter 2 we concentrated on the turbulent flow of the water surrounding theorganisms to understand better how algae obtain inorganic nutrients and microscopicanimals obtain their food. Chapters 3 to 8 reviewed the biological and physicalprocesses associated with the formation of phytoplankton concentrations inspring blooms, at fronts, in coastal upwelling areas, at shelf edges, in rings, andin estuaries. The final perspective, in Chapters 9 and 10, was of long-term variationsin biological productivity due to decadal-scale variations in weather patterns.In all of these discussions we reviewed information on consumer dynamics whereit was available, but by far the greater part of the text concerns phytoplankton.There are two reasons for this bias. One is that phytoplankton production is aprerequisite for almost all other kinds of biological production, and is in its turnalmost totally dependent on the transport of nutrients from deep water by physicalprocesses. The other is that for many years we have been able to measurechlorophyll continuously by means of a fluorometer, and this has served as a usefulindex of phytoplankton biomass, albeit a rough one. The ratio of chlorophyllto carbon varies five-fold, so our estimates of phytoplankton biomass are atbest approximate. Instruments for the continuous measurement of zooplanktonbiomass were devised more recently and are still under development.As marine ecology emerges as an integrated discipline concerned with the physics,chemistry, and biology of the oceans, there is a search for generalities around whichto organize the multiplicity of observations. We see this search revolving aroundfour questions:1 Is there a common mechanism to account for the occurrence of high biologicalproductivity in a variety of physical environments?2 To what extent are events in marine ecosystems determined by physical processes,and to what extent are the outcomes modified by interactions withinthe biological community?3 How can we develop concepts and models that span the enormous range ofscales in marine ecology, from the microscopic to the global and from secondsto geological ages?4 How do we explain an apparent synchrony in the variations in the biomassesof fish stocks worldwide?IS THERE A COMMON MECHANISM TO ACCOUNT FOR THE OCCURRENCE OFHIGH BIOLOGICAL PRODUCTIVITY IN A VARIETY OF PHYSICALENVIRONMENTS?A widely accepted generalization is that phytoplankton production is limited primarilyby the supply of nitrate and that global primary production is a functionof the various physical mechanisms making nitrate available in the photic zone.Evidence in support of this hypothesis is summarized below. However, the discoverythat large elements of the phytoplankton are limited by the availability oftrace elements such as iron and silicon means that work is needed to generatemore complex models of global primary production. Furthermore, the discoveryof the widespread abundance of extremely small photosynthetic cells, many ofwhich are unable to use nitrate, requires a radical reshaping of concepts aboutthe control of primary production in the sea.It was pointed out by Legendre (1981), and is amply confirmed by our review,that there is one sequence of events that occurs in a variety of physical settingsand on time scales ranging from a few hours to a year, and that normally leadsto an increase in phytoplankton production. The essence of it is strong verticalmixing followed by stratification of the water column. As first described by Gran(1931) and presented as a quantitative model by Sverdrup (1953), it was offeredas the explanation of the spring bloom in temperate waters. The vertical mixingbrings nutrients from depth to surface waters, and the formation of stratificationconfines the phytoplankton to a well-lit zone in which daily photosynthesis exceedsdaily respiration. The driving forces for vertical mixing are convective cooling andwind stress at the surface. The chief agent of stratification is solar heating.In estuaries and parts of the continental shelf vertical mixing may be drivenby tidal currents interacting with the bottom, and stratification may be mainly afunction of freshwater run-off, but the effect on the phytoplankton is the same.The major difference is the time scale. The strength of tidal currents varies witha diurnal rhythm and with the fortnightly cycle of spring and neap tides. Whentidal currents are strong, vertical mixing is also strong, and when tidal currentsare weak stratification is more marked. We have reviewed examples of highphytoplankton productivity corresponding with each period of stratification.At tidally mixed fronts, the area of tidal mixing increases with the spring tidesand decreases on the neap tides, causing the front to move back and forth horizontally.At some geographical locations there is an alternation of tidal mixingand stratification that leads to enhanced phytoplankton production and biomass.Similarly, in areas noted for their coastal upwelling, the prevailing wind bringscool nutrient-rich water to the surface and a relaxation of that wind permitssurface warming and stratification. The high productivity is associated with therelaxation of the winds, as the phytoplankton utilizes the upwelled nutrients. Evenin areas of more or less continuous winds, a horizontal succession of events canbe detected. Close to the coast, nutrients are abundant in the freshly upwelledwater, but as it streams away from the area of upwelling stratification sets in andphytoplankton biomass increases. Still further from the coast is a zone in whichthe zooplankton become more abundant as they feed on the phytoplankton.A similar zonation is found in relation to equatorial upwelling.Here, then, is a mechanism of biological productivity that is found in situationsas diverse as a temperate estuary and a mid-ocean band of upwelling runningparallel with the equator. The alternation of vertical mixing and stratificationis surely one of the most important sequences in marine ecology. In Chapter 3,we referred to examples that appeared to contradict the Gran/Sverdrup model namely, instances where a phytoplankton bloom was initiated in the apparentabsence of stratification. A bloom (i.e., an accumulation of phytoplanktonbiomass) is the result of the growth term for a phytoplankton population beingsignificantly larger than the loss term. Platt et al. (1994) pointed out that the lossterm is usually either grazing or sinking, so if these processes were unusuallylow, biomass could accumulate and a bloom could form. If light increasedrapidly due to increasing day length, or if the actual depth of the mixed layerwas less than that indicated by profiles of conductivity or temperature, thegrowth term could increase while the loss terms remained unchanged. The lastsituation is thought to occur when a body of water is subject to an unusuallylow level of wind mixing for a protracted period. The phytoplankton are movedvertically at such a slow rate that they are able to grow and multiply in the absenceof a clearly defined shallow thermocline. Because in the examples on record ofblooms forming before the onset of stratification, the critical parameters for thetest of these mechanisms were not measured, no conclusive evidence has beengathered for violation of the Gran/Sverdrup model.Making a clear distinction between changes in phytoplankton productivity andthe accumulation of biomass (i.e., bloom formation) has enabled oceanographersto begin the development of a global classification of pelagic ecosystems (Banseand English 1944; Longhurst 1995, 1998) that embodies the Gran/Sverdrup modelin conjunction with other physical and biological mechanisms. For example,Longhurst calls the areas exhibiting the classical pattern of spring bloom and subsidiaryautumn bloom the Westerlies Biome. A variant of this pattern is found inthe North Pacific, where the formation of a deep mixed layer in winter is limitedby the low salinity of the surface waters (see Section 3.3.8). Poleward of this area,where spring comes very late but the days of summer are very long, the mainbloom takes place in summer. A subsidiary fall bloom in that locale may bemediated by reduced grazing pressure as the zooplankton sink to overwinteringdepths. Areas exhibiting this pattern are called the Polar Biome. The Trades Biomeis the area that is permanently stratified and in which the biomass of phytoplanktonfluctuates with small amplitude in response to seasonal variations in trade winds.Finally, Longhurst (1998) recognizes a Coastal Boundary Zone Biome in which awide range of mechanisms, including tidal mixing, internal waves, wind stress,river run-off, or topography, cause periodic upwelling that is interspersed withstratification caused by either surface warming or reduced salinity. These mechanismsare analyzed in Chapters 47 of this textbook. All are consistent with theGran/Sverdrup model.Just as oceanographers were beginning to think that they had a grasp onseasonal cycles of phytoplankton production worldwide, two new observationssuddenly made the whole picture much more complex. One was the finding thatlarge areas of the ocean appear to have their primary production limited by theavailability of micronutrients such as iron and silicon. The second was that perhapsmore than half of the biomass of primary producers in the oligotrophic gyresis made up of cyanobacteria, Prochlorococcus, etc. These organisms may be unableto utilize nitrate. Both findings require that current production models based onthe vertical transport of nitrate-rich water will need to be supplemented bytotally different kinds of models. This is an important area for future research.TO WHAT EXTENT ARE EVENTS IN MARINE ECOSYSTEMS DETERMINED BYTHE PHYSICAL PROCESSES? TO WHAT EXTENT ARE THE OUTCOMES MODIFIEDBY INTERACTIONS WITHIN THE BIOLOGICAL COMMUNITY?Most of the text of this book deals with situations in which physical factors stronglyinfluence biological events in predictable ways. However, there are some situationsin which the course of events is strongly influenced by the biology, and theconsequences of physical events are not predictable without taking the biologyinto account. Examples are given below, but much remains to be done to understandhow interactions such as competition, predation, or adaptation within thebiological communities modify the expected consequences of a physical process.Does the concept of auxiliary energy help clarifyphysicalbiological relations?In our review we have seen that physically the ocean is controlled by heatingand cooling, freshwater run-off, wind-driven currents, eddies, turbulence, andvertical stratification. The solar energy that provides the heating is also capturedby phytoplankton, passed from one organism to the other through the feedingprocess, and finally dissipated in the heat of respiration. Physical oceanographydeals with the first of these pathways and biological oceanography with thesecond. In marine ecology we become concerned with both, and we then noticethat the two pathways are interrelated. Water movement breaks down theboundary layers around organisms, transports nutrients and waste products, andinfluences the rate of encounter between planktonic predators and their prey.Organisms use currents to assist their migrations and sessile organisms occupysites with a range of current speeds appropriate to their way of life. These physicalenergies assist the transfer of energy in the biological food web without themselvestaking part in the process. From a biological point of view they have beenlabeled auxiliary energy.The concept was first elucidated by Odum (1967a, 1967b), who drew attentionto the way in which the ebb and flow of the tide assists the productivity of a saltmarsh, and the way in which agricultural productivity (as measured by energyflow) is enhanced by the use of auxiliary energy to prepare the ground, removeweeds, spread fertilizers, and so on. In the history of agriculture the auxiliary energyhas changed from being human labor (the farmer and his family) through the useof domestic animals to the present-day use of fossil fuels. Odum drew attentionto the fact that the auxiliary energy for a salt marsh is provided free by nature,while the auxiliary energy of a farm is costly.Margalef (1974, 1978b) pointed out that the physical energy that upwellsnutrient-rich water in the ocean is an energy subsidy to the phytoplankton. Heshowed that a model relating photosynthesis to energy of upwelling is, in manysituations, a better predictor of phytoplankton production than the more complexcontemporary models involving light, nutrients, and temperature. He alsodeveloped detailed explanations of the morphology and physiology of variousphytoplankton species in terms of their adaptations to high or low levels ofauxiliary energy. For example, diatoms tend to be characteristic of turbulentwater in which nutrients are being upwelled vigorously, while flagellates arebetter suited to low-turbulence, low-nutrient waters.The topic was further explored by Legendre (1981; Legendre and Demers 1984,1985; Legendre et al. 1986). He and his colleagues pointed out that high biologicalproductivity often occurs at places where there is a sudden change of auxiliaryenergy, such as fronts, thermoclines, sedimentwater interfaces, and the undersideof ice. They also pointed out that for there to be an effective physicalbiological interaction there must be a matching of scales in time and space. Forexample, since the doubling time for phytoplankton cells is in the range of hoursto days, favorable physical conditions must persist for at least a few days forthere to be a marked increase in phytoplankton populations. A good example ofthe importance of matching time scales was reviewed in Chapter 6. High phytoplanktonproductivity on tidally mixed fronts is stimulated by changes in thestrength of tidal mixing and has a periodicity of 14 days, whereas high productivityat the shelf break is stimulated by internal waves that form on the ebbingtides with a semi-diurnal rhythm. Since the generation time of mesozooplanktonis of the order of weeks, they cannot reproduce fast enough to use the pulses ofprimary production occurring at fortnightly intervals on the tidally mixed fronts,but they are able to build their populations by using the more continuous supplyof phytoplankton generated in association with the internal lee waves at theshelf break.One of the problems inherent in trying to build the concept of auxiliary energyinto numerical models is that it is difficult to determine what proportion of theenergy of physical processes impinges on biological processes. Margalef (1978a)made some rough estimates and developed comparative plots of the regressionsof primary production in the plankton and in agriculture on auxiliary energy(Fig. 11.01). The diagram shows that a given amount of primary production inthe plankton requires about 10 times more auxiliary energy than the same productionon land. This finding is not surprising when we recall that in the oceannutrient regeneration often occurs at great depth, far removed from the euphoticzone, whereas on land nutrients are regenerated in the soil, close to the roots ofthe plants.It will be interesting to see whether the concept of auxiliary energy leads tobetter models of primary production. Now that it is possible to obtain verticalprofiles of turbulence (see Section 3.3.3), data on primary production as a functionof turbulent energy may begin to accumulate. Lande et al. (1989) used dataon the vertical distribution of cell concentrations and turbulence to calculate thepopulation growth rates at different depths of those phytoplankton cells that couldbe regarded as nonmotile and neutrally buoyant. These cells were all in the sizerange known as ultraphytoplankton, and consisted of prochlorophytes (