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Home , Isopycnal, Marine ecosystem, New production, Photic zone

MARINE PROGRESS SERIES Vol. 52: 77-88, 1989 Published February 16 l Mar. Ecol. Prog. Ser.

REVIEW

Biological production of the : the case for a consensus

Trevor platt1, William G. ~arrison',Marlon R. ~ewis~,William K. W. ~i',Shubha sathyendranath2, Ralph E. Smith1. 3, Alain F. ~ezina'.

' Biological Division, Bedford Institute of Oceanography, Dartmouth. Nova Scotia, Canada B2Y4A2 *Department of Oceanography, Dalhousie University, Halifax, Nova Scotia, Canada B3H 451 Biology Department, University of Waterloo, Waterloo, Ontario, Canada N2L 3G1 Universite du Quebec a Rimouski, Rimouski, Quebec, Canada G5L 3A1

ABSTRACT: Biological dynamics in the pelagic are intermittent rather than steady. In oceanic regimes, where nitrogen is limiting to growth, an important fraction of the annual, depends on transient episodes of increased supply: at such times the role of locally-regenerated nitrogen is correspondingly less. Proper averaging of these variable rates, in time and space, is the key to reconciliation of existing data on the biogenic fluxes of and carbon in the ocean. The magnitude of oceanic production supported by nitrate (the ) is higher than previously thought.

In the oceans, as on the land, the fundamental relates to the new production (sensu Dugdale & Goe- biological process is photosynthetic fixation of carbon. ring 1967) rather than the total primary production. In ecological terminology, the rate of is called the primary production. Notwithstanding that it is the principal source of organic carbon for the support CONCEPTUAL BACKGROUND of the entire marine , the magnitude of pri- mary production in the ocean is still disputed to within Components of the carbon cycle a factor of 10 (Eppley 1980, Shulenberger & Reid 1981, Jenkins 1982a, Williams et al. 1983, Platt 1984, Platt & The absolute fixation rate of inorganic carbon into Harrison 1985, Platt & Harrison 1986, Reid & Shulen- organic molecules is the gross primary production (P,). berger 1986). The disagreement is most acute for the When corrected for the respiration of the open ocean, which comprises 90 % of the surface area (R), P, reduces to the net primary production (P,): of the world ocean, and accounts for more than 80 O/O of P, R = P, marine biological production on a global scale. - (1) Although the debate has animated important research These formal distinctions have no exactoperational on the major biogeochemical cycles of the oceans counterparts in work on natural communities (Table 1). (National Academy of Sciences 1984), the uncertainty A major complication is that microheterotrophs coexist continues to confound speculation on such important with and share the same size range as autotrophs, and in questions as whether ocean phytoplankton will serve seeking to measure the or metabolism of the as a significant sink for the COz that is building up in one it is exceptionally difficult to discriminate the bio- the atmosphere (Sarmiento & Toggweiler 1984). It is mass or metabolism of the other (Li 1986). Another argued here that the divergent points of view can be complication is that it is often difficult, in respect of the reconciled within the resolution of the existing data: a autotrophs themselves, to specify, or control, the degree consensus is emerging. The common ground, however, to which R influences the measurement of P. The extent

G3 Inter-Research/Printed in F. R. Germany Mar. Ecol. Prog. Ser 52: 77-88, 1989

Table 1 Methods for estimating primary production in the ocean and the nominal time-scales on which the results apply. The components P,, P,,,and P, of primary production refer to a scheme based on carbon; PT and P,,, to one based on nitrogen. Sedimentation rate refers to the gravitational flux of organic particles leaving the , not the (much smaller) flux arriving at the sediment surface. See also Fig. 1

Method Nominal component of Nominal time-scale production

In vitro 14C assimilation PT ('p") Hours to 1 d (durabon of incubation) O2 evolution PT Hours to 1 d (duration of incubation) I5NO3 assimilation pnew Hours to 1 d (duration of incubation) Bulk property Sedimentation rate below photic zone P ( P) Days to months (duration of trap deployment) Oxygen utilization rate OUR pmw Seasonal to annual Net O2 accumulation in photic zone pnew Seasonal to annual NO3 flux to photic zone Pnew Hours to days Upper limit Optimal energy conversion of photons absorbed PT Instantaneous to annual by phytoplankton pigments Lower limit Depletion of winter accumulation of No3 above P~w Seasonal seasonal

of the resulting bias in particular cases will depend on production.) Other parts of the , such as the structure (topology) of the local and on the nitrification (a component of regenerated production) measurement techniques employed (Eppley 1980, and denitrification, are considered to be relatively Peterson 1980, Smith et al. 1984). If the respiration of all unimportant in the photic zone. The sum of P,,, and P, (both macroscopic and microscopic) in the is referred to as the total production PT. The ratio P,,,/ is subtracted from P,, the residual is called PT is called the £-ratio (Eppley & Peterson 1979). Total the net community production (Pc). production, PT, is the nitrogen-equivalent of P,, in the sense that it represents the sum total of nitrogen assimi- lation by the photoautotrophs. However, because there Components of the nitrogen cycle is no evidence that phytoplankton remineralise nitro- gen, a case could be made for equating PT with P,. The The limiting elemental for plant production distinction is of significance for calculations involving in most oceanic regions is believed to be nitrogen the interconversion of carbon and nitrogen. It is con- (Carpenter & Capone 1983), which may be supplied in ventional to convert between carbon and nitrogen various chemical forms from a variety of sources. using stoichiometric factors known as the Redfield Another way to partition the primary production then is ratios (Redfield et al. 1963, Takahashi et al. 1985). We according to the source and oxidation state of the follow the same convention in this paper, in which case nitrogen substrates utilised (Dugdale & Goering 1967). it is appropriate to consider PT equivalent to P, (Lan- Strictly, the partition depends on whether the nitrogen celot & Billen 1985). is supplied by regeneration from organisms within the Many of the arguments that follow rest on the (ideal- euphotic zone (regenerated production, P,) or from ised) premise that the of the ocean is in a outside the photic zone (new production, P,,,). In the biochemical steady state (Fig. 1). Then, the flux of open ocean, the dominant contribution to externally- nitrogen leaving the photic zone in sedimenting supplied nitrogen is the vertical flux in the form of biogenic particles is balanced by the vertical flux of nitrate (Eppley et al. 1973, Fogg 1982),whereas regen- nitrate into the zone. In principle, if there were no erated production depends only on reduced nitrogen leakage of nitrogen, the pelagic ecosystem could run compounds, in particular ammonia. It is therefore con- indefinitely on regenerated nitrogen alone. There is ventional to equate new production with nitrate-based always, however, a constant nitrogen loss through production. (Any nitrogen supplied by horizontal gravitational settling of organic material or otherwise. advection or terrestrial runoff, whether oxidized or (In areas subject to heavy exploitation of renewable reduced, or from the atmosphere by direct fixation or resources, a potentially significant loss is that associ- washout from rain, would be included in the new ated with the harvest of .) If the nitrogen losses Platt et al.: Biological production of the oceans 7 9

direct titration. Changes in the bulk properties of the give other indices of primary production. They include the change in dissolved O2 content of the phot~czone, the rate of sedimentation of organic parti- cles, the consumption of 0, below the photic zone by the of the sedimenting material (the oxygen utilization rate, OUR), and the vertical flux of nitrate into the photic zone (Platt et al. 1984). It is crucial to realize that these various methods do not all refer to the same component of primary produc- tion. Nor do they all refer to the same fundamental timescale (Table 1). That is to say, each method may be characterized by an intrinsic timescale to which its results apply, but outside of which they may be invalid. The reason is that primary production is very far from constant in space and time, so that the way it is aver- aged has a profound effect on the results (Platt & Harrison 1985). When incubations to determine PT are of duration less than 1 d, extrapolation of the results to daily rates is fraught with difficulty. Generally, meas- urements based on changes in the bulk properties of the water column refer to a longer timescale than do in vitro ones. They also depend more heavily on the Fig. 1. Schematic of principal fluxes for new and regenerated assumption of biochemical steady state for the photic production. The sole support for regenerated production is zone. A further complication is that the basic dimen- reduced nitrogen supplied within the photic zone by the sions of the results may differ. In vitro estimates refer to excretion of organisms. New production depends on nitrogen supplied from outside the photic zone, of which the dominant discrete depths and fluxes per unit volume, whereas flux is the delivery of nitrate from below. In the steady state bulk property methods require averaging over depth, this vertical flux is balanced by the downward flux of nitrogen and therefore refer to fluxes per unit area of sur- in the sedimenting particles. At the annual time-scale, current face. evidence is that in the open ocean, new production is very roughly from one third to one half of regenerated production, but may deviate considerably from this figure over short time- and space-scales COMPARING INDICES OF PRIMARY PRODUCTION were not replaced in the form of nitrate, the pool of Because the ocean is undersampled with respect to nitrogen available to run the regenerated production primary production measurements, we should attempt cycle would become depleted. The new production, to assemble all relevant data into a single data base, and its equivalent nitrate flux, may be thought of as the after intercomparison of different techniques. But the maximum rate at which organic compounds can be incompatibility of intrinsic timescales, and the difficulty extracted from the photic zone without jeopardy to the of extrapolating one component of primary production long-term integrity of the ecosystem contained therein. to estimate another, limit the resolving power of the In other words (Platt et al. 1984), for the long term, P,,, comparison. The temptation to extrapolation may be is synonymous with P,. irresistible, but the results will not be robust unless all the processes linking the 2 scales of event are under- stood in detail, which they are clearly not in this case. SCALES OF MEASUREMENT FOR PRIMARY Of course, comparisons have been, and will continue PRODUCTION to be, made between the various indices of primary production. Inconsistencies have been reported: they We may distinguish 2 kinds of index for primary may be classified into 2 groups (Platt & Harrison 1986). production (Table 1). Incubation in vitro ( In the first, which we may call Hypothesis I, indices of samples containing natural phytoplankton assem- P,,, (Table 1) are held to exceed in vitro measurements blages at natural concentrations, contained in bottles) of PT. This is a serious claim, and if supported would provides one such index of photosynthetic rate. For subsun~ethe weaker, Hypothesis I1 that bulk estimates example, the assimilation of carbon may be measured of P,,, (Table l), when extrapolated to PT, exceed in by uptake of the tracer 14C; the evolution of oxygen by vitro measures of PT. Given that PT is usually measured 80 Mar Ecol. Prog. Ser. 52: 77-88, 1989

by assimilation of 14C02, the hypotheses are often The f-ratio and Hypothesis I1 stated, ~mplicitly or explicitly, in terms of the 14C method versus methods based on changes in bulk Invoklng Hypothesis I1 requires application of the properties. We now examine the hypotheses, but do not identity PT = (f)-l P,,,,, to extrapolate estimates of P,,,, discuss the technicalities of the I4C method itself, which to PT.The f-ratio is thus cast in a role of central impor- are outside the scope of this review (Peterson 1980). In tance. Conventionally, f is measured by assimilation of testing the hypotheses we do not regard either side of "N, in the form of nltrate or ammonia, during incuba- the comparisons as an absolute standard: we look for tion in vitro (Eppley & Peterson 1979). So measured, f agreement or otherwise within the errors ofboth. has an intrinsic timescale of hours: it is inappropriate as a divisor for bulk property estimates of P,,,,, (time-scale of weeks to years) unless it can be shown that f is Hypothesis I uniform everywhere within the spatial domain defined by the characteristic timescale of P,,,, and constant Shulenberger & Reid (1981) supported Hypothesis I over the same time-scale. Because f depends on the for the central North Pacific. Increase in the O2 super- local nitrate supply and also responds to changes in the saturation (roughly 8.5 %) just below the seasonal structure and dynamics of the local food web, the thermocline between spring and summer was used as probability of its being a universal constant is remote. an estimate of P,. The primary production that would We are therefore led to define a similar ratio, ,with be required to generate this much oxygen appeared to a longer characteristic time-scale: be higher than indicated by the in vitro measurements. = Jl P,,, dz df/JJ PT dz dt Platt (1984) considered that the excess oxygen due to photosynthesis had been overestimated. Reid & where the integrals are taken through the photic zone Shulenberger (1986) disputed this view. Subsequently, and over the seasonal or longer time period. Eq. (2) can using an independent method, it was shown (Craig & be evaluated from a time series for f,provided that the Hayward 1987) that air injection would contribute covariance of PT and fis taken into account (Platt &

1.5 O/O to the oversaturation and thermodynamic correc- Harrison 1985, Vezina & Platt 1987). tions a further 1.5 '10. The mean oversaturation due to The value = 0.1 for the oligotrophic ocean, biological processes (Craig & Hayward 1987) was (6.0 suggested in the seminal paper by Eppley & Peterson k 0.62)%, close to the value (5.5%) used by Platt (1979),has sometimes been used uncritically by subse- (1984) to show that the oxygen results were not signifi- quent authors. In fact, in no oligotrophic ocean do time cantly higher than the 14C results within the resolution series exist for f,measured directly in vitro, that would of the data. Moreover, given that the O2 excess repre- allow calculation of at the seasonal or annual sents P,, it should be converted to carbon (Platt & time-scale. However, it may be possible under certain Harrison 1986) through a photosynthetic quotient of 1.8 circumstances to estimate ffrom ambient nitrate, or rather than the conservative 1.0 used in Platt (1984), nitrate and ammonia, concentrations (Platt & Harrison further increasing the carbon-based rates relative to 1985, Harrison et al. 1987), and time series data do exist the oxygen-based ones. Thus, although unexpectedly for at least one open ocean location, Station S in the high new production is implied, the evidence of the Sargasso Sea. Analysis of these data suggests that, central North Pacific is not sufficient to support instantaneously, fmay take values in the range from 0 Hypothesis I. to 0.8, and that = 0.3 at the annual scale. In extrapolation of in vitro estimates for comparison The algorithm to estimate f from ambient nitrate with bulk property estimates, it is usually assumed that concentration (Platt & Harrison 1985) was established the fluxes are constant in time and uniform over very originally using data from coastal and large areas of the ocean. The bulk property estimates waters, and can be criticized for this reason in its for a particular location are often compared, unjustifi- application to the open ocean (Le Bouteiller 1986) or in ably, with in vitro estimates averaged over entire ocean ocean regions where primary production may not be basins. Hypothesis I was supported for a region of the limited by nitrogen (Dugdale 1986). However, the subtropical North Atlantic (Jenkins 1982a) for which no annual range of nitrate values in the Station S data set is local 14C data were cited. The standard of comparison similar to that observed in coastal waters. Furthermore, used was the global mean production rate for the oligo- new data from the oligotrophic North Atlantic, west of trophic oceans (Koblentz-Mishke et al. 1970, as cited in the Azores, lead to the same general conclusions (Lewis Menzel 1974): the value of P, was inappropriate as a et al. 1986, Harrison et al. 1987).Direct measurements of yardstick for P,,,*. No evidence has been produced for fby 'W uptake at this open-ocean station were shown to the North Atlantic that compels us to support depend on ambient nitrate in a similar way as at sta- Hypothesis I. tions close to shore. The magnitude of f was consistent Platt et al. Biological production of the oceans 81

with simultaneous estimates of the vertically-diffusive (Wyrtlu et al. 1976).More importantly, the distribution of nitrate flux made from measurements of the local, verti- potential energy in the ocean is variable at the same cal gradient of nitrate and highly-resolved measure- scales (Dantzler 1977, Emery 1983). Potential energy is ments of velocity shear (Oakey 1982). associated with vertical displacement of , and Because nitrogen-limited systems are usually hence of nutrient distributions. Variance in wind stress responsive to local increases in nitrate supply, one on scales of a few days should also contribute to vertical should look to instances where these may occur for displacements of scalar fields as well as to cross-isopyc- direct evidence of temporal fluctuations in f (as meas- nal mixing. Jenkins (1988) has emphasised the intermit- ured by ''N) and their correlation with PT. For example, tency of nitrate supply to the euphotic zone in the North in the warm-core rings of the , Sargasso Atlantic near Bermuda. Entrainment of nitrate into the Sea water is carried north into the cooler Slope Water. surface layer by wind, and its subsequent utilisation by Recent work on the ageing of such rings (McCarthy & phytoplankton, has been observed directly at sea in the Nevins 1986) shows that the typical value of f at the Southern California Bight (Eppley & Renger 1988). An time of separation of the ring from the Gulf Stream is instance of episodic nitrate input leading to a phyto- 0.13, rising to 0.32 in a ring 3 mo old, presumably due to bloom in the Sargasso Sea has been observed increased vertical nitrate flux associated with convec- by ship (Glover et al. 1988). A similar incident has been tive mixing. The phytoplankton response to frictional observed by remote sensing in the decay of a warm-core ring has been modelled (Franks (Lohrenz et al. 1988). We can therefore expect that et al. 1986): it is found that relaxation of the ring causes locally-enhanced nitrate flux will not be an uncommon upward motion of nutrient-rich water leading to a value feature of the pelagic ocean. It is worthwhile, then, to of 0.2 for fat the ring center. Following the passage of a anticipate how the ecosystem might respond. storm, it was observed (McCarthy & Nevins 1986) that Compartmental analysis of the pelagic food web (Vez- deepening of the thermocline inside a ring raised f from ina & Platt 1987) is a useful technique to explore the 0.32 to 0.52. The effect of storm passage would not be consequences of transients in nitrate supply. A strictly confined to the waters inside the ring, but would be a linear model, where fluxes are directly proportional to general phenomenon within the area affected by the the mass of material in the compartments, leads to the storm (Iverson 1977). Further evidence exists for 'atypi- conclusion that ratio properties of the food web are cally' high fvalues in the Sargasso Sea. From changes uncorrelated with nitrate supply, because all fluxes are over 5 d durlng June in the nitrate content of the upper intensified by the same factor. In such a model, f would 30 m of the water column at the center of a warm-core be independent of PT. But when nonlinear dynamics ring (Garside 1985), the nitrate-based production was are admitted, in particular that the sedimentation flux calculated to be about 0.5 g C mP2 d-l. Comparison increases faster than phytoplankton biomass (Vezina & with PT measured by 14C uptake implied f> 0.5. Platt 198?), it can be shown that f depends on nitrate It could be argued that citing data from ring and eddy supply in a manner that resembles the empirical result studies distorts the true picture, an argument that would (Platt & Harrison 1985). Observational support for this be tenable if eddies were few and far between, and if f formulation comes from numerical analysis of sediment and PT did not covary. In , how- trap data from the open ocean (Betzer et al. 1984). It is ever, a picture ls emerging in which the ocean is replete more plausible than the linear one in that it does not with mesoscale eddies (Kerr 1985).Their significance for assume that the structure of the plankton community is the oceanography of the Mediterranean and other constant in time nor uniform in space. An explicit and oceans has recently been emphasized (Robinson et expression for f can be derived in terms of the flow al. 1987). An intense cold-core eddy, analogue of the structure of the pelagic food web (M. J. R. Fasham cold-core Gulf Stream rings known in the Northwest unpubl.). Atlantic, has been observed in the Northeast Atlantic Thenaturalabundance of I5Nin particles sinkingin the (Kupferman et al. 1986). Over the North Atlantic, the ocean covaries with the magnitude of the flux, distribution of eddy-scale kinetic energy indicates varia- and provides a monitor for the nitrate flux into the photic bility associated with features of characteristic size of zone during their formation (Altabet & Deuser 1985), order 100 km, such as warm-core rings and meanders in strengthening the argument that nitrate flux can be western boundary currents. Maps of eddy kinetic energy equated with sediment flux. In a 6 yr time series of derived from SEASAT altimeter data show high variance sediment trapping in the Sargasso Sea, Deuser (1986)has in a band from Cape Hatteras to the Grand Banks, and confirmed the close coupling of sedimentation to primary extending halfway across the ocean (Cheney et al. 1983, production, extending results obtained earlier at the Menard 1983). Similar features are found in the North seasonal timescale in the North Atlantic (Deuser et al. Pacific and in the western South Atlantic: they corre- 1981),Panama Basin (Honjo 1982), (Izdar et al. spond to patterns already inferred from ships' drift 1984) and North Pacific (Honjo 1984). The inverse 82 Mar Ecol. Prog. Ser. 52: 77-88, 1989

correlation between sediment flux and surface tempera- within the limits of error. They were also within the ture 1 mo earlier is taken as evidence that the amount of range of independent estimates of new production cal- material sinking is a response to vertical transport of culated from summer nitrate depletion. Further, there nitrate (accompanied by surface cooling). Moreover, the was a 3-fold variation in the summer oxygen excess, organic carbon content of the sinking material is highest and corresponding new production estimate, during when the flux is highest. The implication is that recycling the period 1969 to 1978, the variation being larger than of carbon in the pelagic is less efficient at times of high the yearly standard deviation. These results, as do production, in other words that f and PT have positive those from the Atlantic (Jenkins 1982b), suggest that covariance (Platt & Hanison 1985). Food web analysis interannual variance may be appreciable, with implica- (Vezina & Platt 1987) reproduces this result, and supports tions for the concept of the pelagic ocean as a steady the empirical result of Eppley & Peterson (1979)relating f state system at the annual time-scale. and PT. The nonlinear dynamics reveal very clearly that Because the dominant flux of new nitrogen in the the unweighted time average for fcan seriously underes- open ocean has a preferred direction, we expect that the timate . Thus, a simple mechanismin which changes water column will be vertically structured with respect in nutrient supply lead to significant changes in food web to the f-ratio, decreasing from the base of the photic zone structure subsumes both the local and regional variabil- towards the surface. Intuitively, one expects that this ity in the open ocean. decrease should be gradual, but evidence has been The evidence is accumulating, then, for local fluctua- provided from the North Pacific for the photic zone's tions in f, driven by intermittency in the physical for- being partitioned into 2 layers (Knauer et al. 1984). The cing, leading to a value of higher than previously lower layer, being closer to the nutrient source, is more supposed for the open ocean. After analyzing data on representative of eutrophic conditions, while the upper OUR from Station S and finding a figure for P,,, higher layer has a higher recycling efficiency. This picture has than anticipated, Jenkins & Goldman (1985) noted that received further support from measurements of the a conventional extrapolation of P,,, to PT, through a residence time of dissolved 234That various depths in the low and constant f, might lead to a value of PT favour- photic zone (Coale & Bruland 1987). The implication is ing support of Hypothesis 11. They also remarked that that variation of P,,,,, stated explicitly in Eq. (2), should intermittency in the nitrate supply could render this not be overlooked in the calculation of average . procedure invalid. Platt & Hanison (1985) shared the The degree of vertical structuring will depend on the same point of view: using the figure for derived local density profile: clearly, such a biological separa- from the time series of nitrate at Station S, they showed tion of layers can only be maintained if the photic zone is that the 14C and OUR data could indeed be reconciled, deeper than the mixed layer. such that Hypothesis I1 could be rejected in this test. These results are consistent with those in the later publication by Jenkins (1988), based on the relative ECOLOGICAL ENERGETICS concentration of 3He in the mixed layer. In a long-term study (VERTEX) of the Estimates of primary production must respect known Northeast Pacific (Pace et al. 1987), was found to limits on the efficiency of photosynthesis, setting an vary in the range from 0.13 to 0.25, with new produc- upper bound to the value of PT that can be extrapolated tion being higher than previously believed, but only from a given P,,, (Platt et al. 1984). The calorific value one third of that recently reported for the oligotrophic ET of total production corresponding to a new produc- Atlantic (Jenluns & Goldman 1985). In the discussion of tion P,,,, is the VERTEX data, it has also been pointed out (Martin et al. 1987) that the OUR decreases more rapidly with depth in the North Pacific than in the Sargasso Sea, implying that transport of organic carbon along iso- where the factor 12 is the atomic weight of carbon; pycnals into the area, below the photic zone, is not a 11.4 cal (mg C)-' is the caloric content of phytoplank- negligible term in the carbon budget for the Sargasso ton (Platt & Irwin 1973); and 1.8 and 1.25 are the Sea. Correcting for this advective term, new primary photosynthetic quotients for new and regenerated pro- production in the oligotrophic North Atlantic would be duction respectively (Williams et al. 1979, Raine 1983, more nearly equal to that in the North Pacific. Platt et al. 1987). Note that 1 cal = 4.1868 J. In a direct comparison of in vitro measures of new To compute the efficiency of energy conversion, we production against new production estimated from the should first recognize that in the ocean much of the biological component of oxygen oversaturation at available light is absorbed by the water itself and is Ocean Weather Station P in the subarctic Pacific, it was unavailable for photosynthesis. If the biomass is distri- found (Ernerson 1987) that the 2 sets of figures agreed buted evenly in the water column, it can be shown Platt et al.: Biological product~onof the oceans 83

(Platt et al. 1984) that the fraction q absorbed by photo- ciency is a steep function of for values of less synthetic pigments is given by than 0.35. For comparison, we note that the highest short-tern1 yields recorded in sugarcane fields are < 5%, with average field-crop yields 10 times less where k, = the specific absorption coefficient for (Radmer & Kok 1977). Efficiencies much higher than chlorophyll in m' (mg ch1)-'; B = pigment biomass in about OS%,averaged over the year, for optically- mg chl m-3; and kW = the absorption coefficient of the dilute suspensions of phytoplankton in a nutrient- water itself in m-'. For the open ocean, k,, = 0.03 in the limited ocean do not seem plausible. Considerations of visible region (Jerlov & Steemann Nielsen 1974). An ecological energetics therefore favour a value of = average value (More1 & Bricaud 1981) for k, is 0.04. It 0.4 or higher for the Sargasso Sea north of Bermuda, remains to estimate B. using a figure (Jenkins & Coldman 1985) of 5 m01 m-2 As an example, we calculate for the Sargasso Sea. yrpl for P,,,,.. This calculation should be treated as a The Station S data record shows that the average first approximation only: it can be refined as the data pigment concentration in the photic zone varies from on which it is based are improved. about 0.08 to 0.8 mg chl m-! The unweighted mean for The magnitude of can also be related to empiri- the data is 0.28 mg chl m-3, corresponding to q = 0.27 cal data for the Redfield ratio connecting biologically- (dimensionless). The total incident radiation at Ber- mediated changes in oxygen and carbon in the ocean. muda averages 1.3 X 10' cal mP2 yr-' of which roughly If the respiratory quotient in the is equal half, or 6.5 X 108 cal m-2 yr-', will be in the photosyn- and opposite to the photosynthetic quotient (PQ)in the thetically-active part of the spectrum (Sterrer et al. photic zone, they should both estimate the Redfield 1981).Multiplying this figure by q we find 1.8 X 108 cal ratio. PQ should be weighted according to the pro- m-2 yr-' absorbed by phytoplankton and available for portion of PT that is new production: photosynthesis. It is an absolute upper bound (minimiz- ing the implied efficiency) in that no allowance is made for absorption by detrital suspensoids, nor for the where the factor 1.8 is characteristic for nitrate intense absorption of the red wavelengths near the metabolism and 1.25 for ammonia metabolism (Wil- surface; that it represents all wavelengths in the visible liams et al. 1979, Raine 1983). When t£> = 0.3, spectrum, not just the energy-efficient ones (Lewis et will be equal to 1.42, a figure consistent with the al. 1985a, b); that absorption by phaeopigments (Tilzer revised (Takahashi et al. 1985) Redfield ratio for oxy- 1983) has not been discounted; and that only in the gen to carbon of 1.42. This calculation is not acutely linear, or low light, region of the photosynthesis-light sensitive to the magnitude of , however, and it curve is maximum efficiency attained. does depend on the value chosen for the PQ of nitrate Fig. 2, calculated using Eq. (3), shows how the metabolism. But if we take the revised Redfield ratio as implied conversion efficiency depends on <£> when a given and recast Eq. (5),it does seem to exclude very 5 m01 O2 m-2 yr-l. Note that conversion effi- P,,,, = low values of :

Decreasing PQnilmt,for any reason implies that has to increase in compensation, such that Eq. (6) could not be satisfied for a very low value of . A corollary of the difference in PQ for new and regenerated produc- tion is that the expected OUR calculated for a given nitrate flux will be at least 1.8/1.42 times higher than would be deduced from the standard Redfield ratio for carbon to nitrogen of 6.6.

INTERMITTENCY AND SAMPLING

Chronic undersampling is a fact of life in oceanogra- phy. Nevertheless, conclusions are often drawn on the implied premise that the ocean, and the plankton in it, Fig. 2. Implied photosynthetic conversion efficiency as a func- tion of annually averaged f-ratio at Station S in the Sargasso are uniform over large regions and constant in time. In Sea, assuming that new production is 5 m01 O2 m-2 yr-' retrospect, we can see that undersampling was at the 84 Mar. Ecol. Prog. Ser 52: 73-88, 1989

root of difficulties of interpretation in the past, as can be I4c ASSIMILATION rng C rn-'d-' illustrated by re-examination of the problems experi- 1.0 2.0 3.0 4.0 5.0 6.0 7.0 enced by kley (1953) and Steemann Nielsen (1952, 1953) in reconciling their data on primary production in the Sargasso Sea. Steemann Nielsen's argument was based on only 3 stations, none of which were north of Bermuda. Oceanographic conditions change immedi- ately south of this latitude (the subtropical front), winter conditions being characterized on the south side by mixing to no more than 150 m and on the north side to 400 m with proportionally higher nutrient content (Menzel & Ryther 1960). Moreover, Steemann Niel- sen's measurements were made in June, which we know to be the least productive month of the year (Platt & Harrison 1985). The final irony is that the detailed criticism of Riley's Sargasso Sea data was based on Steemann Nielsen's Indian Ocean data. Riley (1953) and Menzel & Ryther (1960) have drawn IN SlTU PROOUCTION SARGASSO SEA attention to the extreme temporal variability of the APRIL 1983 Sargasso Sea. Thus Riley: 'It is becoming increasingly clear that large variations occur in subtropical and even in tropical waters, so that we must study oceanic waters as closely as we examine our temperate coastal regions in order to arrive at an accurate estimate of their pro- ductivity.' Menzel & Ryther (1960), in a study of the seasonal cycle north of Bermuda found primary pro- duction rates agreeing with the observations of both Fig. 3. Varlation between days of In situ primary production at Riley and Steemann Nielsen, depending on the time of the same nominal stalon in the north Sargasso Sea, April the year. They concluded that 'The results of this study 1983. Water column isothermal over depth range shown. cannot be taken as 'typical' of the Sargasso Sea or the Unpubl. data from Biological Oceanography Division, Bedford open ocean in general, since probably neither is as Institute of Oceanography, Canada uniform as is generally implied'. This view is supported by remote sensing surveys of phytoplankton blooms off eddies and other intermittent forcing processes are the eastern seaboard of the USA (Brown et al. 1985), characteristic features of ocean circulation (Robinson and by satellite images of ocean colour for the North 1983, Sandstrom & Elliot 1984, Holligan et al. 1985).We Atlantic basin (Esaias et al. 1986). In our own work, we have shown that fluctuations in the physical forcing have found considerable variation between days in the propagate into the biological dynamics in a way that primary production of the Sargasso Sea (Fig. 3). The increases the importance of the averaging procedures mistake made by both kley and Steemann Nielsen was (Platt & Harrison 1985). Seasonal fluctuations in oxygen to express their results as annual rates when neither consumption have been found even in the sediment had covered the seasonal cycle. community of the central gyre of the North Pacific at It is against this background of spatial variability and 5900 m depth (Smith & Baldwin 1984),and highly inter- temporal intermittency that we should examine pro- mittent sedimentation has been documented at 2000 m cedures for collection and interpretation of data and in the North Atlantic (Billet et al. 1983). Thus. the criteria for assessing consistency. We should also con- underlying hypothesis of a dynamic steady state for the sider under what circumstances (space and time scales) biogeochernistry of the pelagic region of the ocean is to we can reasonably expect the flux divergences of car- be considered as no more than an idealisation of a bon and oxygen to be equal (Platt & Harrison 1985), or system that, in reality, is perturbed intermittently such the steady state assumption to be justified. The answers that the condition of instantaneous equlibrium is rarely, are by no means clear. For the time scale, it seems that if ever, attained. nothing less than the annual scale is plausible. In the It may be that in the end we shall be defeated by our vertical, the photic zone fixes the depth scale, but its inability to resolve sufficiently well the distribution of definition is problematic (Sathyendranath & Platt 1988, relevant properties in space and time. It may be better Sathyendranath et al. in press). In the horizontal, the to modify the question. Rather than ask, for example, problem is no less acute. We know that mesoscale 'What is the rate of oxygen consumption at depth in the Platt et al.: Biological production of the oceans 85

ocean?', we might ask 'What is the maximum or uptake. Rather than interpret the outcome (estimate of minimum OUR that is consistent with the distribution of P,,, exceeds that of PT) as a failing of the 14C method, properties that we are able to observe?' (cf. Emerson they concluded that the sampling had been insufficient 1987). This question would demand that we estimate to resolve the seasonal signal. Implicitly. Hypothesis I OUR from explicit box models that would reflect our was not supported. observational limitations. We would then be able to assign some index of precision to estimates of OUR (cf. Wunsch 1984),essential for a fair test of the hypotheses FUTURE WORK stated above. Such questions may be addressed through the application of inverse methods to food-web The overriding influence of spatial heterogeneity and models (Vezina & Platt 1988). temporal intermittency for the dynamics of b~ological Bulk property measurements with large, intrinsic properties in the ocean dictates the sampling strategies space-time scales (Jenkins 1982a) have the advantage that should be striven for in future work. We have that much of the averaging difficulty is removed even emphasized that reliable averages for the long term before the data are collected. No such bulk property cannot be calculated if data are lacking on the short- method exists for PT. But it is P,,, that has been shown term variances and covariances. Clearly, synopticity is in recent studies to be higher than anticipated, and for desirable. One is led inevitably to the conclusion that many applications, P,,, is a far more interesting quan- remote sensing techniques should be employed. How- tity than PT, in that it represents the exportable compo- ever, remote sensing gives direct information only on nent of primary production. For discussions of the pos- the pigment biomass. To compute primary production, sible role of the ocean biota in absorbing part of the additional information must be supplied: the irradiance increasing COz in the atmosphere, the most relevant field (Sathyendranath & Platt 1988), the vertical profile component of the carbon fixation is P,,,,. New produc- of the pigment biomass (Platt et al. 1988) and the tion represents the so-called '' that parameters of the photosynthesis-light curve (Sathyen- transports part of the CO2 absorbed from the atmo- dranath & Platt in press). One possible approach (Platt & sphere to the sediments (Gammon 1986). Similarly, the Sathyendranath 1988) is to combine the remotely- new production sets the upper limit to the carbon that sensed surface pigment fields with a dynamic biogeog- can be extracted from the ocean in the form of protein. raphy of vertical structure and physiological parame- Far better, in principle, to estimate P,,, directly ters. Because the computations use photosynthesis through OUR or sediment traps rather than from parameters determined by the I4C method, remote sens- and PT, both of which impose much more demanding ing can contribute nothing to the question of the accu- sampling requirements. At present, no con~pilation racy of local 14C data. Moreover, the error of estimation exists of data on the magnitude and global distribution by remote sensing will always be greater (lower preci- of new production. On the basis of the (admittedly sion) than can be achieved by direct measurement, limited) VERTEX data set, Martin et al. (1987) have tending to limit the power of hypothesis testing at the calculated a figure of 7.4 X 10' t C yr-' for the new local scale. On the other hand, at the regional scale, production of the world ocean, using values of estimates of primary production should be superior to 0.14 (open ocean); 0.17 (coastal zone); and 0.20 (up- those scaled up from a limited number of shipboard welling areas). The f-ratios chosen for coastal and up- observations at discrete stations, given the lich informa- welling areas seem too low, but it is instructive to note tion on the horizontal structure of the biomass field (Platt that even doubling them would have relatively small & Herman 1983, Platt & Sathyendranath 1988). effect (<30 %) on the estimate of global new produc- The question 'What is the primary production in the tion: the open ocean accounts for 90 % of the total open ocean?' has no simple answer. Primary production surface area and is therefore weighted strongly in the varies in space and time even in the open ocean, and final answer. Hence the interest in knowing for may, at particular times and places, be surprisingly the open ocean as well as possible, and in understand- high. Considerable work will be required to develop a ing the processes that conspire to make it so. reliable global average. Remote sensing has potential to It is to be regretted that the significance of P,,,, itself give information only about PT. No electromagnetic has been under-emphasized in favour of inappropriate principle is known that could be exploited to measure extrapolations for unjustified comparison with poorly P,,,,. Where the interest is in P,,,, a weighted integral resolved estimates of P,. In this respect, the conclusion for (f. PT)has to be evaluated. There is some possibility of Jennings et al. (1984) is significant. They measured that f may be estimated in a semi-quantitative manner the seasonal consumption of nutrients in the water from the rate of change of chlorophyll in serial remote column (an estimate of P,,,,,) in the Weddell Sea, and sensing images (Lohrenz et al. 1988). Sudden, local compared the results with those for P, measured by 14C increases in biomass would provide circumstantial evi- 86 Mar. Ecol. Prog. Ser. 52: 77-88, 1989

dence of additions of new nitrogen, and therefore of dynamics of the food web, that future work should be locally-elevated f-ratio. Similarly, comparing ocean col- directed. Above all, it will require an integrated study our images with thermal images should reveal local, by physical and biological oceanographers. negative, temperature anomalies and provide evidence of enhanced vertical mixing, and therefore of locally- Acknowledgements. We thank Prof. K. Banse. Dr A. R. Long- increased f-ratio. hurst and Prof. P. J. leB. Williams for helpful comments. On the basis of tests made so far, no compelling case has been made for support of either Hypothesis I or 11, but we should continue to keep an open mind to both LITERATURE CITED possibilities. Future tests should be made with far more rigour than in the past, given the importance of the Altabet, M. A., Deuser, W. G. (1985). Seasonal variations in answer (Platt & Harrison 1986). 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Th~sreview was submitted to the editor Manuscr~ptreceived: July 9, 1988 Revised version accepted: November 23, 1988