FISHERIES OCEANOGRAPHY Fish. Oceanogr. 2:314, 231-243, 1993

The North Atlantic turbine: views of production processes from a mainly North Atlantic perspective

T. WYATT1 AND I. R. JENKINSON2

1 Instituto de Investigaciones Marinas, Eduardo Cabello, 6,36208 Vigo, Spain1 Agrace de Conseil et de Recherche Océanographiques,Lavergne, 19320 La Roche Caniüac, France

“Perhaps no phenomenon in the natural economy of the gulf [of Maine) so arrests attention (certainly none is so spectacular) as the sudden appearance of enormous numbers of diatoms in early spring, and their equally sudden disappearance from most of its area after a brief flowering period."

(Henry Bigelow, 1926)

“The spring bloom in the North Atlantic is one of the most conspicuous events in the world ocean . . . a sudden explosion of colour that fills the basin north of about 40 degrees latitude in April and May each year . . . ."

(Ducklow and Harris, 1993)

ABSTRACT

A brief account is given of the ‘agricultural hypothesis’, the key studies which led to its replacement by the ‘grazing hypothesis’, and early models of the classical planktonic food chain. The budgetary problems posed by these views led to interest in the roles of dissolved and particulate components of planktonic ecosystems, and to discovery of the ‘microbial loop’. The balance between these alternative pathways is seen to reflect processes at the interface between hydrodynamics and ecology.

Key words: North Atlantic, production, turbulence, plankton

INTRODUCTION

At the time when plankton studies were being initiated in various laboratories, a widely recognized view con- ceming the source of agricultural productivity was in vogue, due largely to Justus von Liebig. This view gave

Received for publication 9 June 1993 Accepted for publication 30 June 1993 © 1993 Blackwell Scientific Publications, Inc.

rise to what we now call ‘Liebig’s law of the minimum’, and simply stated, maintains that production is limited by whichever essential nutrient is in shortest supply. Brandt (1899) and others were soon to argue that a similar principle must equally control the production of photosynthetic organisms in the sea. Liebig had empha­sized the importance of nitrogen, phosphorus and pot­assium in this equation. Brandt drew attention as well to silica, the main mineral component of diatom frustules, but concentrated on nitrogen. The idea that nutrients control production is known as the ‘agricultural hypoth­esis’. In combination with a persistent failure in many studies to properly distinguish between stock and pro­duction, the agricultural hypothesis has been a chronic source of misunderstanding in biological oceanography. Iron is a recent claimant to the role of nutrient limi­tation (Martin and Fitzwater, 1988; Martin et al., 1990), and in their introduction to a symposium addressing these problems, Chisholm and Morel ( 1991 ) described the debate as a “conceptual and experimental mire”.

Following the lead of the Kiel plankton school, plankton surveys using nets were widely undertaken, especially in European coastal waters, and in the Atlan­tic Ocean during the Plankton Expedition of 1899, led by Victor Hensen. The best material then available, and for a long time afterwards, for making plankton nets was silk, and the smallest mesh size was about 50 /um. Although the limitations of such nets were soon recog­nized, and it was not long before other collecting methods (bottles, pumps, the centrifuge) were being employed to collect the smaller fractions of plankton, nets continue to provide the mainstay of plankton surveys. The widespread deployment of nets soon led to descriptions of the annual cycles and interannual vari­ability of net phytoplankton in different localities, especially in European waters and the Atlantic Ocean.

Reliance on net collection initially gave an emphasis to diatoms at the expense of other organisms which was to last for several decades, but the distortions this emphasis may have generated were largely offset by the European context and by the special attention given to that most remarkable of phenomena, the ‘spring bloom’ (earlier called ‘vernal augmentation’), which in many areas is indeed formed predominantly by diatoms. It was with the search for the causes of the spring bloom that

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232 T. Wyatt and l.R. Jenkinson

many students then concerned themselves. The prob­lems are so interesting and so perplexing that almost a century later we share the same concerns.

Brandt (1899), although he shifted his position as new evidence and criticism accumulated, was long convinced that the agricultural hypothesis which he championed was unassailable. Other students of marine productivity were not, and in the early part of this century they laid the foundations of what was to become the classical paradigm of biological oceanography. The first serious cracks in the agricultural hypothesis were due to Gran (1902), who began his work on phyto­plankton in Norwegian coastal waters in 1900. But it was not until about 1930 that the cracks became obvious, and even as late as 1927 Gran was to lend qualified support to the agricultural hypothesis. In fact he never unequivocally rejected it, though his contri­butions to its ultimate demise were very important, and he was largely responsible for the two key concepts of compensation depth and mixing depth.

As already indicated, attention centred on the regu­lation of the spring diatom outburst, on its initiation and subsequent decline. The long delay in reaching a general model and a general consensus can be partly attributed to the small number of people involved in the enquiry and to technical limitations. But perhaps the main reason, a measure of the intrinsic difficulties posed by the spring bloom phenomenon, was a failure to define questions with sufficient clarity. This is hardly surprising because the production problem lies at the interface between two very intractable areas, hydro­dynamics on the one hand and ecosystem dynamics on the other.

Tire components available with which a general model of the spring bloom could be constructed were all known from the start: light, cloudiness, temperature, salinity, nutrient concentrations, the impacts of winds and tides on mixing, and so on. Initially each of these components was a candidate as a limiting factor in an extended sense of Liebig’s idea, and because the import­ance of each varies geographically, confusion reigned. It was of course obvious that light is critical, but it was found for example that the diatom outburst off western Norway coincided in time with that of South-west England 10° of latitude nearer the Equator. It was also argued that if light induced the spring bloom, it should equally favour its continuance through the subsequent summer. While the abundance of nanoplankton remained unknown and the impact of grazing was not stressed (except by Lohmann), these considerations led back to the agricultural hypothesis, at least so far as concerned the declining phase of the bloom. As we now know, it was not the growth season which ended, only

the predominance of diatoms, and the diatom bloom is usually over before nutrients are exhausted, as Brandt (1905) himself was aware.

Nathansohn suggested in 1906 that vertical mixing plays a role by maintaining adequate nutrient concen­trations in the upper layers. Gran and others immedi­ately recognized the significance of this, and the important step was made that vertical mixing caused by winds and tides followed by stabilization due to insola­tion and run-off were critical to the spring bloom. This process of alternate mixing and stabilization was not always expressed clearly at the time, but we can never­theless recognize the seeds of more sophisticated ideas developed later by Gran and Riley, and most recently by Margalef, Frontier, Lasker and Legendre. We now attach great importance to the depth of mixing and to the frequency of mixing events (see e.g. Legendre et al., 1986).

Several other early observations distracted attention from this line of enquiry. Amongst these were seasonal changes in the viscosity of seawater, first appreciated by Wolfgang Ostwald in 1902. Following logically from that appreciation was an interest in the problem of how diatoms maintain themselves in the photic zone, which has led to an extensive literature on the effect of shape, spines, selective excretion of heavy ions and so on, on the sinking rates of diatoms. Much of this literature treats diatoms as victims of the decay of turbulence. The first review of the topic was provided by Steuer in 1910. It was not until 1970 that Smayda pointed out that dead diatoms in settling chambers can hardly behave like live ones in the sea. It is now clear that the sinking (and suspension) of diatoms is in large measure under their own control, rather than an inadvertent response to environmental conditions, that sinking is a part of diatom life history strategies (e.g. Smetacek, 1985; Waite and Harrison, 1992).

Another early observation was that the spring diatom bloom begins first near land and at the ‘edge’ of deep water. Fpyn noted both phenomena in Norwegian coastal waters in 1929. It was supposed that coastal waters were fertilized by nutrients in freshwater run-off, and the stabilizing effect of run-off was not at first emphasized. But Sund, also in 1929, reported that there is no substantial increase in either phosphorus or nitro­gen in Norwegian coastal waters owing to run-off. This was confirmed by Braarud and Klem (1931), who conse­quently took the side of the emerging British school, Marshall and Orr working in the Clyde Sea, and Atkins in the Channel, who then regarded light as the critical factor. Bigelow (1926), working in the Gulf of Maine, also knew that run-off was not necessarily enriching. He nevertheless attributed the inshore diatom bloom to

Production processes in the North Atlantic 233

run-off, without pointing directly to its potentially stabilizing role. The lack of an archetypal framework or paradigm at that time was made very clear by Bigelow when he came to discuss the productivity of Georges Bank. He more or less admitted defeat.

THE CLASSICAL PARADIGM - MIXING DEPTHS AND THE DEVELOPMENT OF PRODUCTION MODELS

The confusion described in the preceding section was finally sorted out in the 1930s, and a synthesis was achieved which has provided a fertile source for many subsequent investigations of the production problem. Important contributions were made by Harvey and his colleagues working in the Channel and by Riley, who worked in a variety of environments including the Gulf of Mexico, the Sargasso, Long Island Sound, and Georges Bank. The arguments of these and others were synthesized by Sverdrup (1953).

A major development during these years was the introduction of chlorophyll estimates to assess phyto­plankton stock. This procedure was first used by E. Kreps and N. Verbinskaya (1930) in the Barents Sea. Harvey developed the idea into a routine and was the first to deploy it widely in the sea. Many early surveys of chlorophyll concentrations were expressed in Harvey plant pigment units (HPPU), which often related reasonably well to values obtained from more advanced techniques. Harvey also deployed a current meter (con­structed by E. J. Allen) when towing his nets, an idea first suggested by Nansen in 1915.

With these novelties, the Plymouth team was able to make more accurate assessments of changes in the phytoplankton, and to demonstrate that the production of particulate organic matter greatly exceeded the stock over the course of a year (Harvey, 1934). In a sub­sequent paper, Harvey etal. (1935) established that the amplitude and timing of the spring outburst is regulated by grazing, and that even in late summer when phyto­plankton stocks are very low, there is no evidence that herbivores suffer starvation; daily production is at all times sufficient for their metabolic needs. They also found that only part of the inorganic phosphorus used during phytoplankton growth is found in the plankton, and that it must therefore undergo a continuous process of recycling by being grazed. Nathansohn (1908) had made a similar point. These were early hints of the important distinction drawn much later between ‘new’ and ‘regenerated’ production (Dugdale and Goering,1967).

The Plymouth group noted, too, that when phyto­plankton stocks are high, herbivores consume more

than is necessary for their maintainence and growth, i.e. ‘overfeeding’ or superfluous feeding occurs. This behaviour must clearly have a significant impact on nutrient recycling rates, and thus shift the balance, in modem parlance, from new to regenerated production. It is not therefore necessarily superfluous. Finally, it was concluded that diatoms almost never die a ‘natural death’ other than by being eaten, and that their sinking rates are extremely slow and therefore unimportant. In brief, Harvey and his colleagues rejected the agricul­tural hypothesis, both in its general sense and in all important details, and in its place set up the ‘grazing hypothesis’.

These results were formalized by R. H. Fleming (1939) in a model as follows:

dP/dt = P [a - (b + ct)], (1)

where P is the phytoplankton stock per unit area of sea, a is its growth rate, b is the initial grazing rate, and c is the rate at which grazing increases. Fleming defined the yield as the amount of production removed by grazing, and obtained curves for production, yield, and stock of the form shown in Fig. 1.

This makes it clear that it is impossible to obtain any correlation between stock and changes in nutrient concentration unless the grazing rate is zero.

Harvey et al. (1935) did not at that time consider either the compensation depth or the depth of mixing to any extent when interpreting their data from the Chan­nel, though they thought the autumn outburst was terminated by declining light. But these two concepts, together with grazing, became the key issues of Riley’s contribution, who can thus be seen to have followed the work of Gran and Braarud (1935) more closely.

Riley had found on Georges Bank that there was no clear relationship between the rate of oxygen pro­duction and pigment concentrations, that the localiz­ation of the spring bloom was not therefore due to an increase in the photosynthetic rate. This turned his attention to the roles played by water depth and turbu­lence. He wrote (Riley, 1941):

Vertical turbulence has a two-fold effect on plankton productivity. By removing part of the crop from the zone of active growth, the growth rate of the entire population is reduced, and furthermore, any part of the population which remains isolated from the phototrophic zone suf­fers depletion through the normal process of res­piration. It follows that depth is an important factor when it limits the extent of vertical turbu­lence.

andIt seems most probable that. . . the rates of photo-

234 T. Wyatt and l. R. Jenkinson

Figure 1. Trends measured as chlorophyll in production, yield and stock using Fleming’s (1939) model.

Time

— Cumulative Production — Cumulative Yield - - - Stock

synthesis and respiration, and the degree of verti­cal turbulence, are the controlling influences on growth through the late autumn, winter, and early spring, when the quantities of nutrients and animals are such that they can have little effect on the phytoplankton crop.

But the critical test between the agricultural and grazing hypotheses must be made in late spring and summer in these waters, when nutrient availability might be more restricted, and when large herbivore populations develop. Riley considered a variety of con­trolling factors for this period, including self-shading (in April, when stocks were very high), high respiration rates caused by high temperatures and overstabilization, as well as nutrient limitation and grazing. With certain reservations, he favoured the view that the low standing stock of summer is caused by rapid removal by the grazers despite the high rate of production. He was more ambiguous about the role of nutrient limitation.

Later, Riley (1946) expressed these views in the form of a general equation, as follows:

dP/dt = P(Ph - R - G), (2)

where P is as in Fleming’s model, Ph is a photosynthetic coefficient, R is the coefficient of phytoplankton respir­ation, and G is a grazing coefficient: Ph — R is equival­ent to a in Fleming’s equation, but is now a variable rather than a constant. Riley restated his general equation by others containing the six environmental factors (photosynthetic coefficient, incident radiation, extinction coefficient, depth of euphotic zone, nutrient

concentration, and vertical turbulence) which he had thought to be important on Georges Bank. Riley was able to obtain an approximate integration over short time intervals, and hence simulate the seasonal cycle of phytoplankton on Georges Bank and elsewhere.

In a later review, Riley (1963) wrote that “few major events in the seasonal cycle were controlled by a single factor” and that the conclusion of Harvey et al. (1935) that blooms are controlled by grazing, might be true in British waters, but was not applicable to the New England area. There “the relative importance of grazing varies from one part of the area to another, suggesting that this is not a subject for broad generalization.” This was a curious statement in the light of his subsequent remarks in the same review, and most pertinently, that in constructing his equations, he had lost a most important part of the Volterra theory, the mutual dependence of predator and prey.

Steele (1956), working on the North Sea Fladen Ground, followed the approach of Riley. He estimated production directly from the decline of phosphorus (and thus ignored one of the clear messages of the Plymouth School, and of Fleming’s model), and the grazing coef­ficient and sinking rate of the diatoms from a pair of simultaneous equations. But if sinking did not occur, his grazing coefficients were under-estimated, and the dependence of algal growth on phosphorus therefore fictitious. Cushing (1958) pointed out that Riley’s grazing coefficient was based on the minimal needs of the herbivores, and thus ignored both their growth requirements and superfluous feeding. In Riley’s and

Production processes in the North Atlantic 235

Steele’s models, an increased value of G would reduce Ph as effectively as nutrient depletion. Subsequent arguments have suggested that nutrients only control algal growth when grazing has failed to do so. This may take place occasionally in shallow temperate waters in winter when herbivores are rare, and during some exceptional blooms at other seasons. But even in these special circumstances, evidence that nutrient limi­tation occurs is far from convincing, and the agricul­tural hypothesis must usually be rejected.

The last piece of the classical paradigm was due to Sverdrup (1953), who introduced the concept of'criti­cal depth’. Sverdrup assumed that production decreases logarithmically with depth (a result established by Penelope Jenkins (1936) at Plymouth), while respir­ation rate is independent of it. The two processes balance (over 24 h) at the compensation depth of Gran and Braarud (1935). The total population can only increase when production exceeds respiration, both integrated over depth, and “there must exist a critical depth such that blooming can occur only if the depth of the mixed layer is less than the critical value” (Sverdrup, 1953).

The critical depth is defined by the photosyntheti- cally active radiation (PAR) passing the surface, Ic, and the extinction coefficient. As Sverdrup pointed out, the level of 1c in the water column must be higher for a mixed population of both phytoplankton and zoo­plankton, since it is the net growth of the algae which contributes to the increase in stock. Thus the grazing coefficient is an integral part of Sverdrup’s model, and nutrient limitation is assumed not to occur. Nutrients might regulate the rate of which biomass accumulates, but not the final yield (Riebesell et al., 1993). This point is frequently misunderstood.

To summarize, by the 1950s, there was an approxi­mate consensus that the greater part of production is consumed by herbivores, and that rapid increases in algal stock are usually due to the time lag between the initiation of production and the development of herbi­vore grazing capacity (e.g. Wyatt, 1980). Thus the classical paradigm (unlike its basically chemical prede­cessors) points directly to the fundamental role of turbulence in the control of production; we turn to some aspects of turbulence later. The curtailment of such blooms is similarly the result of grazing. Production itself is initiated when the depth of mixing rises above the critical depth and is thereafter controlled by the ratio of compensation depth to depth of mixing (Dc/ Dm). One of the unexpected results of recent work in the Atlantic is that f-ratios (the ratio between new and regenerated production) are low, between 0.3 and 0.45 even at the beginning of the spring bloom, indicating

that grazing and microbial activity are then already important (Harrison et al., 1993; Sambrotto et al., 1993).

DISSOLVED AND PARTICULATE ORGANIC MATERIALS

As already indicated, Lohmann was the first planktono- logist to emphasize the importance of grazing, in 1908. He calculated from measurements of algal and zoo­plankton biomass in Kiel Bay that algal production must be of the order of 30% daily for the continued existence of the animals present. Putter (1909) measured the oxygen consumption of the animals and, on that basis, suggested that Lohman’s figure was too low. He turned to the dissolved organic matter (DOM) in seawater in an attempt to balance the budget, and proposed that it could be absorbed directly by the animals. Putter’s views were not widely accepted, but the budgetary problem remained. Early criticism was due to the fact that attempts to culture zooplankton on DOM alone were unsuccessful.

Many years later, Baylor and Sutcliffe (1963) showed that DOM could be made available to filter feeders by bubbles in the cultures. The DOM is adsorbed to bubble surfaces, and when they burst at the surface, the organic matter remains in micelles at the surface, and can subsequently mix into the water again as filterable particulate organic matter (POM). Bacteria are essen­tial to this process, at least for low molecular weight (<100000) compounds. It also became clear, as Riley had surmised, that the functional relation between zooplankton and its food is rather complex and variable (e.g. j0rgensen, 1955) so that oxygen consumption is a poor measure of grazing capacity (Anraku, 1964) and its rate cannot be used to estimate algal mortality.

We can now say, briefly, that DOM is abundant, and that it might provide food to the zooplankton in windy weather when breaking waves drive bubble clouds into the mixed layer. But the budgetary problem perceived by Putter is much more likely to be resolved by a better understanding of feeding behaviour. The real signifi­cance of DOM from an ecological viewpoint probably lies elsewhere. The dynamics and fate of DOM, and the factors which determine these, remain largely un­known.

The role of POM or detritus is less intractable. We know that animals can feed on detritus, and that these particles are colonized by bacteria and other organisms which enhance their food value. It is likely that this material is sometimes more important than phyto­plankton, especially where microalgae, sea-grasses, mangroves and sewage outfalls introduce large quan-

236 T. Wyatt and I. R. Jenkinson

titles. But the disappearance of Zostera beds from the Danish Limfjord in the 1930s did not lead to massive changes in upper trophic levels as was anticipated at the time on the basis of estimates of primary production then available (Rasmussen, 1973), and which were too low. The higher grazing rates required in some pro­duction models, such as that of Cushing (1959) can now be justified by the revised (upwards) estimates of pro­duction, made possible particularly by the introduction of the radiocarbon technique by Steeman Nielsen in 1952. In any case, the importance of detritus is now known to be more varied than economic food chain models imply.

Tire classical ‘grazing food chain’ model, whose roots were traced above, transfers mainly diatom production to zooplankton, and subsequently to planktonic and pelagic carnivores. Part of this production leaves the photic zone, either before (sinking cells in aggregates or marine snow) or after being eaten (as faecal pellets) to form a link in the biological pump.

The proportion of production which sinks directly is probably rather small, of the order of 1%, except under special conditions related to diatom life histories. The secretion of organic materials by plankton and the waste organic products of metabolism fuel the pools of DOM and POM, and are used by heterotrophic bacteria. These pathways support the ‘microbial food web’ or ‘microbial loop’ in which microflagellates, ciliates, amoebae and other organisms are engaged. Most, but not all, of this biota is associated with the POM. The upper trophic levels of this loop can re-enter the grazing food chain, but their economic contribution (as food items) to the latter is probably small (<10%) in most circumstances, especially where low temperatures (<5°C) inhibit bacterial activity. Perhaps the most important role of the microbial loop vis-à-vis the grazing food chain is remineralization, leading to regenerated production. The comment has been made that the classical paradigm, because it can incorporate these more recently discovered pathways, as well as the rediscovery of the picoplankton (Lohmann described components of this group from Oikopleura houses), is not of quantitative value. But this paradigm is specifi­cally linked to the grazing food chain, so the comment is not valid. The real limitations of the classical paradigm stem from its economic roots. It still maintains its potency in economic terms (i.e. in terms of production of potential human food) but is of more restricted value ecologically.

The grazing and microbial pathways of the food web are not only linked through the mutual supply of substrates. There are lower limits to the particle size spectrum which can be used by the herbivores of the

classical food chain, and autotrophic organisms below that threshold are directly available to some of the grazers of the microbial loop. The size spectrum of the phytoplankton is controlled partly by the input of turbulent energy. Thus changes in energy input can switch production between the two pathways. Ex­pressed in a useful though oversimplified way, moderate to high average mixing rates (on time scales of weeks or months) - as in eastern boundary current upwelling systems and tidally energetic shelf seas - will favour larger phytoplankton species, which will in turn sustain larger pelagic fish populations. Lower mixing rates will tip the balance towards the microbial loop.

At low rates of turbulence, particularly for grazers of low mobility, shear is positively related to grazing rate because the shear brings food into grazers’ reach (or perception zone) (Rothschild and Osborn, 1988). Above a certain threshold, however, different for each organism, turbulence sweeps an increasing fraction of the food out of reach again before the grazer can catch it, so the grazing rate then becomes negatively related to turbulence (Jenkinson and Wyatt, 1992). Low levels of turbulence allow larger and more marked microzones of nutrients to develop around heterotrophic particles (Lazier and Mann, 1989), facilitating nutrient uptake by motile phytoplankton.

By allowing nutrient uptake (at least for motile phytoplankton) and grazing to become progressively easier, periods of declining turbulence may be intervals of productive and trophic bounty (even if phyto­plankton standing stock declines). By contrast, in­creases in turbulence are usually experienced locally as sudden events: microzones are seriously eroded, tempor­ary or seasonal thermoclines are deepened, leading to reduced mean light levels in the surface mixed layer; aggregates (Alldredge et ai. , 1990), fragile feeding struc­tures (Barham, 1979) and organisms (Thomas and Gibson, 1992) are pulled apart; grazing may be rendered more difficult. Following such events, production and feeding may be seriously disrupted, particularly until levels of nutrients build- up again to permit uptake directly from the bulk field. Grazers may have to starve until prey becomes once again sufficiently abundant to counteract the effects of the greater turbulence. As for resultant changes in the phytoplankton community structure, more recent work has only managed to con­firm Margalefs mandata (Margalef et al., 1979), except by the addition of nano- and picoplankton.

The amplitude and frequency of individual mixing events (time scales of days) are also important and modulate these general trends. Mixing disperses the phytoplankton stock, and hence decreases grazing coef­ficients. During critical life history stages, persistent

Production processes in the North Atlantic 237

depression of feeding rates by such a mechanism could lead to year class failure in annual and perennial species. This is the essence of Lasker’s hypothesis (Lasker, 1975; Davis et al., 1991). There circumstances lead to an increase in phytoplankton stock without a concomitant increase in production. The obverse, that periods of low energy inputs allow contagious distributions to develop and grazing activities to reach their full potential - the prerequisites of good fish recruitment - are called ‘Lasker events’ (e.g. Cury and Roy, 1989). They lend support to the value of the classical paradigm.

Remineralization and other biochemical processes which provide the links between the grazing food chain and the microbial loop require a variety of different conditions. These must be provided by and under the control of the organisms themselves. The environment must be structured by biological activity. Thus processes like nitrogen fixation, nitrification, sulphur oxidation and methanogenesis need particular conditions which depend largely on oxygen concentrations and acidity. Sieburth (1983, 1988) has provided a provocative syn­thesis of these problems, as well as much information on which their understanding depends. The organic par­ticles with their associated microbial consortia provide the necessary microenvironments. Some, as already mentioned, are derived from the micelles which form from the surface skin, but most are created in situ. The interior regions of some of the larger particles are anoxic and acidic, and are surrounded by shells with intermedi­ate oxidation/reduction potential. The particles are suspended in the oxygenated and alkaline seawater with which we are familiar. The gradients between the oxygenated, alkaline seawater and the particle centres provide the suite of conditions necessary for the pro­cesses which maintain chemical homeostasis in the photic zone. The anoxic centres of these particles with their anaerobic procaryotic organisms are a survival of the Archaean world. Thus production depends on nutrients introduced by mixing processes, and on nutri­ents which are recycled in situ (i.e. without first disappearing into deep water) by the microbial loop. This important distinction between ‘new’ and ‘regener­ated’ production was first made explicit by Dugdale and Goering (1967). It is an important component of our understanding of how it is that productivity can be maintained at high levels in the absence of large stocks of ‘free’ nutrients.

MICROSTRUCTURE AND TURBULENCE

In the classical paradigm, the sea is considered as a two- layered system. The upper layer is assumed to be mixed down to the depth of the thermocline, and the phyto­

plankton to be randomly distributed within it. Turbu­lence is homogeneous, and the mixed layer is isotropic with respect to the distribution of velocity. This is reasonable in the inertial subrange, and these simplify­ing assumptions were justified at a time when the physical complexities of the upper ocean were not detectable by the instrumentation then in use. An interesting product of this view of the mixed layer was Hutchinson’s well known ‘paradox of the plankton’, which asked how so many different species could exist in a homogeneous niche.

It was not until the 1960s and 1970s that instruments and techniques became widely available with which to study the microstructure and dynamics of the water column. Physicists have now established that vertical profiles of temperature, velocity, and other properties have step-like structures with many inversions, and that turbulence in much of the ocean interior is concen­trated in thin elongated patches which occur intermit­tently in time and space. The turbulent patches occur sporadically within layers in which motion is otherwise laminar. Turner (1973) and Federov (1978) provide introductions to these topics.

The energy for the formation of these patches (see e.g. Woods and Wiley, 1972) propagates from:1. boundaries or fronts into the ocean interior as gravity waves. These boundaries can be created by wind mixing or by large-scale intrusions of one water mass into another. At such boundaries, internal waves of modest amplitude can interact with the mean shear rates due to the large-scale motion, and reduce Richardson numbers below about 0.25, thereby allowing Kelvin-Helmholz instabilities and associated turbulence to occur within pycnoclines.2. double-diffusive processes which draw on the potential energy of unstably distributed components. Patches gener­ated in these ways will initially be turbulent, but the turbulence decays as fluid is entrained from above and below. The passage of subsequent long internal waves produces further ‘splitting’ of the patches until the whole water column is filled with microstructure, which is comparatively stable in time relative to phyto­plankton doubling rates. The empirical scales of these features correspond to the theoretical predictions of Garrett and Munk (1972). Even in the open ocean, temperature changes of the order of tenths of a degree and salinity changes of about 1 (per mil) or more per kilometre occur horizontally and can be traced for 5 to 20 km. The layers are from tens of metres to a few centimetres thick. The degeneration times of tempera­ture inversions are of the order of tens of hours, those of salinity gradients slower unless convective phenomena

238 T. Wyatt and I. R. Jenkinson

intervene. In such complex systems, there are still very great technical difficulties in distinguishing spatio- temporal interaction of processes, particularly from the Lagrangian point of view (which is that experienced by perfectly suspended plankton and molecules). Layers as thin as 10 cm with horizontal scales of hundreds of metres, however, seem to be real. Internal waves raise and lower the microstructural features, at the same time compressing and stretching them in the vertical direc­tion. Current processing of Eulerian measurements of vertical shear, dWdt, would over-estimate the disper­sion associated with this motion. Thus the photic zone provides a great variety of different habitats, and the source of Hutchinson’s paradox disappears.

In the distribution of homogeneous turbulence, there is a range of eddy sizes in the inertial subrange (remote from the largest and smallest eddies) in which energy per unit volume (E) is related to wave-number (Jc) by

E °c k-5/3. (3)

The energy spectrum is defined as w2 E(k) where u2 is the mean square of velocity fluctuations. If m2 is a function of k and the eddy diffusivity ( e ) with dimensions veloc­ity2 X r \ then Kolmogorov’s (1941) expression

u2E(k) oc e 2nk - 5/i (4)

or

E(k) dk oc e2nk~$ndk (5)

provides a combination of k and £ with the correct dimensions. This expression has been modified in vari­ous ways to reflect the intermittent decay of turbulence described above. One such expression is

E(k)dk = £2/}k -3/5[kL(0)]-<3 " D>/3dk, (6)

where L(0) is the initial length scale and D is the fractal dimension. Experimentally determined values of D lie in the range 2.5 to 2.75. The important points in the present context are the increase in slope which the intermittency model dictates when log u2 is plotted on log k, and the increase in turbulent diffusion rates which the model implies (Kraichman, 1991).

Beginning at about the same time as these develop­ments in ocean physics, biologists began a renewed exploration of the plankton in terms of size categories and of spatial distributions (patchiness). In the 1960s and 1970s more attention was devoted to the nano­plankton (<10-20 /tm), which generally passes through the meshes of plankton nets, and somewhat later to the picoplankton (<2 /tm) (e.g. Pomeroy, 1974; Platt, 1983; Johnson and Sieburth 1979, 1982). More accurate estimates of bacterial abundance, now

accepted to fall in the range 105 to 107 ml-1 , also became available. This process has now been extended to the femtoplankton (<0.2 /um) or viruses (Bergh et al., 1989). Along with and beyond the femtoplankton in smallness lies the high-molecular-weight colloidal fraction of the DOM (<0.05 /im), an unknown pro­portion of which is present as aggregates.

In the 1960s, too, fluorometers began to be widely deployed in the sea, and the distribution of chlorophyll could be sampled much more rapidly and at smaller scales than previously. Platt (1972) used this tool to make the fundamental comparison between chlorophyll distributions and the decay of turbulence predicted by Kolmogorov’s theorem, and to highlight the signifi­cance of wavenumbers to phytoplankton ecology (see also Kierstead and Slobodkin, 1953). This brought the problems posed by phytoplankton patchiness into sharp focus. Platt (1978) gives an excellent account of these developments. The slopes of chlorophyll power spectra were found by Platt and others to lie between — 1 and — 3, a range which encompasses both the Kolmogorov prediction (5/3 or —1.67) and the intermittency value ( —1.78). In a theoretical treatment of this problem, Denman and Platt (1976) compared the time to transfer kinetic energy from eddies of length scale d (= L(0)) to eddies of 0.5 d with phytoplankton growth rate, r. They distinguished two regimes in terms of kinetic energy (r): r « r-1 and r » r-1 , separated by a reciprocal wavenumber Kc with a value of about 1 km. Below Kc, spatial pattern is dominated by r.

The variability of the results led Platt (1978) to conclude that the processes which determine the slopes of chlorophyll spectra “cannot be entirely physical, unless wq can rationalize a progressive change in the turbulence or internal wave field concomitant with the development of the spring bloom” and that “the feed­back between the biological system and the physical system cannot be ignored.” Furthermore, Koblentz- Mishke (pers. comm.) has suggested that phyto­plankton production is regulated in such a way as to control the amount of radiation which penetrates the water column to maintain values of about 100 cal cm-2 day-1 . When normalized by maximum photosynthetic rate, these P-I curves are all identical. Development of the phytoplankton bloom increases the optical attenua­tion coefficient, which in turn leads to increased verti­cal stability through stronger heating. Thus, unfolding of the seasonal biological cycle can, itself, lead to changes in the internal wave field (Lewis et al., 1983; Sathyendranath et al., 1991) and therefore affect the relative shapes of the chlorophyll and temperature spectra.

Margalef (1978, see also Margalef et al., 1979) pro­

Production processes in the North Atlantic 239

vided a very condensed and highly intuitive mandala in which turbulence (A) and growth rate, modelled as a function of nutrient concentration, define a space within which phytoplankton succession takes place. Rotation of these axes generates two new axes, (rA)1/2 representing production potential, and (r/A)1/2 with the dimensions of wavenumber. The r -K axis of McArthur (1962), which bisects this space, parallels both the trend from new to regenerated production and the axis of potential production (= nutrients X turbulence). This mandala provides a useful framework within which the problems raised by Platt can be discussed.

THE TURBULENCE/PLANKTON INTERFACE

The distribution of turbulence is generally measured as shear rate, but presented in terms of calculated dissipa­tion, e, so that such measurements tell us virtually nothing about the occurrence and distribution of small, low-shear zones in the oceans. Low-shear zones, how­ever, occupy the greater part of the volume fraction in turbulence fields (Kraichman, 1991), so they are at least as important to the biota as the high-shear zones, perhaps all the more so because they represent more stable (Frontier and Pichod-Viale, 1990) ‘oases’ (Gold­man, 1984), easier for their inhabitants to structure and manage (Wyatt, 1989; Margalef, 1992; Jenkinson and Wyatt, 1992). Understanding the interactions between biopolymeric structuring and turbulence distribution is necessary to comprehend the small-scale dynamics of productive processes. This problem is already well appreciated in industrial bioengineering (Allen and Robinson, 1989) and is beginning to be understood at the boundaries between soil science, terrestrial and aquatic ecology (Frontier and Pichod-Viale, 1990; Mar­galef, 1992). In oceanography it is likely to become an important research topic in the next decade or so.

There are two features of phytoplankton which appear to be particularly well adapted to planktonic life, and to interaction with the microstructure of the physi­cal environment. These are the shapes of many species and their ability to secrete polymers of high molecular weight.

Polymer secretion

The classical axis of succession, as represented by the r— K bisector of Margalefs mandala (see above), takes us from typical centric diatoms such as some species of Thaiassiosira which are characteristic of highly energetic environments, to the complex architecture of the flat­tened dinoflagellates with their lists and other bizarre morphological features, found in highly stratified

waters. It might be instructive to study the hydro­dynamic behaviour of the former in relation to that of kites designed to be flown in strong winds. These kites owe their dynamic stability to their multiplex designs (i.e. they form chains), and to the structural elasticity of their suspension systems. Some Thaiassiosira species have a complex system of extracellular mucilaginous secretions which may anchor them in the microvortices which surround them. The flexible linkages between the cells may integrate, hence damp, the disruptive forces which would otherwise break the chains, while large strings and networks, by straddling different turbu­lent structures (Davey and Crawford, 1986), may in­crease the water flow past their constituent cells.

Extracellular structures of this kind are known in a wide variety of phytoplankton. Castellvi (1971), for example, describes filamentous appendages in the ubi­quitous Skeletonema costatum. Reaching out in different directions are six to eight filaments, each 50,11m or more long and less than 0.1 ftm diameter, on each 5-20 /zm valve. Castellvi found that individuals without these filaments sink thirteen times faster than those which possess them. Most remarkably, these filaments are also present in auxospores. Perhaps an analogy is in order here, with spiders which disperse aerially using threads of gossamer suspended in turbulent air. Pickett-Heaps et al (1986) describe how the large centric diatom Odon- tella sinensis appears to be “held quite firmly in the invisible, elastic mucilage” which it secretes through special processes. Hasle (1983) describes colonies of Thaiassiosira “formed by extrusion of an enormous amount of threads”. There are a variety of descriptions of how such aquatic cobwebs trap bubbles, hence gain­ing even greater buoyancy.

Alldredge and Gotschalk (1989) has shown that extracellular secretions also lead to aggregation and rapid sinking. Thus both suspension and sinking may in some species depend on polymer secretion, and such factors as dispersion of the cells within these floes and the architecture of the threads assume great signifi­cance. There may be critical values of dispersion and packing density (volume fraction of cells) Which deter­mine whether a species floats or sinks, and these values may be reached before production is maximized in economic terms.

Jenkinson (1986, 1989, 1993) gives accounts of the significance of these findings to algal blooms in the sea and to aquaculture (see below). As both Hoyt (1986) and Jenkinson have stressed, changes in the properties of seawater caused by the presence of algae and their secretions can account for many curious observations made during red tides, such as the viscous or slimy character of the water, wave damping at the surface, the

240 T. Wyatt and ¡.R. Jenkinson

respiratory problems of caged fish and other animals, and the feeding difficulties of shellfish.

Heat transfer rates are also reduced in polymer solu­tions, which adds a second dimension to the problem raised by Platt. The associated surface phenomena alter the transfer of heat and gases between atmosphere and ocean, processes which are of crucial importance in relation to conjectured homeostatic mechanisms in geochemical cycles (Wyatt, 1989).

Phytoplankton form

It is well known to river engineers that turbid streams flow faster than clear ones (Zandi, 1967). This is due to the interaction of the suspended particles with the flow, which leads to reduction in both turbulence and turbu­lent drag, and is thus comparable with the impact of high-molecular-weight polymers on flow character­istics. Asbestos fibres are often used industrially to achieve the same effect, and at concentrations between 100 and 150 ppm and Reynolds numbers of 7 to 10, can provide 20% to 40% drag reduction. It is obvious that phytoplankton at adequate concentrations is likely to achieve similar effects (Wyatt et al., 1993) but most studies have dealt with inert particles - the original context was paper mill slurries - or with body fluids, especially blood, and food particles. These studies pro­vide some clues as to the likely impact of phytoplankton blooms on mixed layer dynamics, but there is a need for experimental and field observations to quantify it.

CONCLUSIONS

Costas et al. (1993) suggested that while procaryotes might theoretically be limited by nutrients in Liebig’s sense, eucaryotes are not, because their division rates are strictly regulated by oncogenes which encode growth factors and other components of the cellular signalling machinery, and thus control the onset of the M-phase of cell division. This machinery might control production of some dinoflagellate species during the vegetative phase (Yentsh and Mague, 1980), and deter­mine potential growth during bloom initiation by encystment (Anderson and Keafer, 1987), but is so far unknown in diatoms.

Freshwater phytoplankton populations are some­times infested with parasites which can reach epidemic proportions (e.g. Burning, 1991) and thus have a major impact on host population dynamics and production. It is not known in the sea whether such infestations ever rival grazing in importance for the control of phyto­plankton populations.

New production is frequently assessed from the rate of

nitrate removal, and the f-ratio obtained by calculating the ratio of new to total production. Carpenter and Romans (1991) have shown that nitrogen fixation in the tropical west Atlantic by the large cyanobacterium Trichodesmium exceeds the flux of nitrate through the thermocline, and cite a study of Villareal which indi­cates that nitrogen fixation by Richelia, an endosym- biont of large diatoms, is even higher than that of Trichodesmium.

It has recently been shown that sporadic blooms of large diatoms like Stephanopyxis palmeriana and Pseudo- guinardia recta, which form giant flocculent masses and which grow at low light levels in the pycnocline, can contribute significantly to new production (Goldman, 1993). Goldman (p. 165) points out that the “chances for these events to go unnoticed increase in proportion to the degree of aggregation, but also the aggregates themselves could sink. . . or be grazed by fish and invertebrates and become part of a short and simple food chain. . .”, as envisioned by the classical paradigm. Thus substantial fractions of new production can escape our attention due both to sampling difficulties and to a relative unconcern with sources of nitrogen other than nitrate. Both these poorly appreciated sources of new production depend on large cells, and should they eventually prove to be of general importance, will offset the current trend to emphasize the picoplankton contri­bution to production, at least in oligotrophic waters.

In the late 19th Century, political institutions in the northern countries of the North Atlantic set up corps of government scientists in laboratories, mainly to answer the following questions: ‘What is fish food, where does it come from, and how does it affect stocks and exploi­tation of fish?’ Within a few decades, these scientists had already provided'the wisdom of the classical para­digm as part of the answer. Later, the methods were extended to other oceanographic systems (the tropics, the Mediterranean, monsoon systems, the Antarctic). Then in the 1970s and 1980s, it seemed as if the rediscovery of the picoplankton and the discovery of the microbial loop would show the old paradigm to be too simplistic. Now, however, it is becoming clear that the new information, although adding interesting ecologi­cal details, is of little overall relevance to the fish-food question: the classical paradigm has survived essentially unscathed.

Over the last 30 years, people have become much more aware about how different modes of economic and ecological production and fluxes interact. As a result, political institutions are now asking the successors of these scientists new questions, such as ‘How, and how much, may coastal enrichment be changing DMS pro­duction, global warming and the occurrence of toxic

Production processes in the North Atlantic 241

and slimy blooms?’; ‘What is the role of the oceans in the draw-down of new CO2?’. The classical paradigm is largely irrelevant to such new questions, for which new paradigms are being extracted from both old and new data. Such new paradigms may generally have to in­clude some of the interesting ecological details (such as thepicoplankton, parasites, viruses, the microbial loop, DOM, aggregation and rheological modification of flow fields, toxins and telemediators, regulation of growth by grazing) that the economic paradigm could successfully ignore.

ACKNOWLEDGEMENTS

Our main title is borrowed from a poem of Edward Dorn. One message there was ‘buy or die’ which seems a fair precis of Malthusian models like the agricultural hypothesis; but he also wrote of cloth, slaves and molasses, which formed the golden trade of the 18th Century Atlantic, a trade which perhaps more closely approaches modem views of the production process. The notes on intermittency used here are taken from an unpublished seminar by David Jou at the University of Barcelona some years ago.

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