I. Concepts

ICE S mar. Sei. S ym p ., 197: 3 -8 . 1993

Fundamental issues in measurement of primary production

Trevor Platt and Shubha Sathyendranath

Platt, T . , and Sathyendranath , S. 1993. Fu ndam en ta l issues in m easurem en t o f

primary production. - ICE S mar. Sei. S ym p ., 197: 3 -8 .

G iven the goal to m easure daily, w ater-column primary product ion, the various

im ped im ents to an unam biguous result are rev iew ed. T h e se include the problem o f

definit ion o f primary product ion , in both the fundam ental and o perational senses; the

extrapolation o f the results o f short-term incubations to daily rates; the problem o f

respiration; and the problem o f heterotrophic activity. T h e intrinsic tim e scales

associated with dif ferent m eth ods o f m easuring primary production are discussed, leading to an exam inat ion o f the issue o f com paring the results o f bulk-property

m eth ods with those o f in vitro m ethods. T he question o f extrapolation o f results from

local m easurem en ts to values representative o f larger spatial scales is introduced. Finally, the utility o f m athematical results as com plem entary tools to field m easure ­m ents is addressed. W h e n e v e r possible the points discussed are related to chapters

presented by other contributors to this vo lum e.

T revor Platt: B io log ica l O cea n o g ra p h y D iv ision , B e d fo rd Institute o f O cean ograph y ,

B ox 1006, D artm ou th , N o v a Scotia , C anada B 2 Y 4 A 2 ; S h ubha Sathyendranath: D e p a rtm en t o f O cean ograph y , D a lh ou sie University , Halifax, N o va Scotia , C anada

B 3 H 4 J 1 .

Introduction

Contemporary interest in the planetary carbon cycle has put measurement of marine primary production, a glo­bal flux of some 50 gigatonnes carbon per annum, back in the foreground of biological oceanographic research. This is an arena where the questions are framed at regional and seasonal scales, a perspective facilitated by the advent of satellite images of ocean colour. But many of the techniques that we use to measure primary pro­duction are applied at far smaller scales. The gap be­tween the questions we ask and what we actually do in fieldwork gives rise to a number of issues that form the principal focus of this introductory chapter. Where pos­sible, connections are made with the more detailed expositions given in the chapters that follow. The total range of scales that we must be concerned with is almost as broad as that implied by the title of this symposium. The utility of methods operating at the molecular level remains an open question: it is treated in the contri­butions by Laroche et al. (this volume) and by Raven (this volume).

Matters o f definition

A detailed commentary on the definitions of primary production is given by Williams (this volume).

Primary production is a rate: it tells us the speed of a particular process. The process of interest is the fixation of inorganic carbon in photosynthesis. As such, the rate of primary production is equivalent, let us say, to the turnover rate of the dark reactions of photosynthesis, and this may provide the basis of a fundamental defi­nition of primary production. In absolute terms, primary production can then be expressed as moles of carbon fixed per cell (or per unit volume of medium containing cells) per unit time.

As soon as we try to apply such a fundamental defi­nition in the field, we realize that it must be amplified before an operational definition can be made (Platt et al., 1984). First, consider that the fundamental defi­nition refers to an instantaneous rate. But implied in any measurement procedure for a rate is a time scale on which the result is expected to be valid. Typically, the appropriate time scale is the duration of the measure-

4 T. Platt and S. Sathyendranath

ment procedure itself. Explicitly, we say that the pro­cedure gives a result that is an average value of the rate over the time taken to do the measurement.

We should now enquire, for any particular procedure, whether its intrinsic time scale is a favourable one for the questions we wish to ask. The fundamental definition refers to a process with a characteristic time scale of order 10 ms. Clearly, this time scale is of little ecological or biogeochemical interest, even if we could observe at that scale in the field. For analysis of ecological or biogeochemical issues, the minimum time scale of inter­est is probably one day. For measurement procedures with shorter characteristic time scales, the results will have to be adjusted to at least the daily scale.

Lest we leave the impression that understanding the high frequency processes of algal photo-physiology have no relevance to the measurement of primary pro­duction, note that one of the most promising new ave­nues to estimation of photosynthesis in the field is with methods based on pigment fluorescence. These include the passive fluorescence of chlorophyll at 685 nm under solar stimulation (Kiefer et al., 1989), a signature that can usually be identified in the spectra of upwelling submarine irradiance (Topliss, 1985), addressed in the contribution of Doerffer (this volume); and the double­flash-induced fluorescence used to probe the reaction centres of photosystem II (Falkowski and Kolber, 1990), discussed in the contribution of Falkowski and Kolber (this volume).

Similar questions of scale arise with respect to the basic number of cells, mass of cells or volume of medium containing cells that the carbon fixation rate represents. The fluorescence of individual cells is at the heart of the method of flow cytometry, which has many relevant applications, discussed in the contribution of Li (this volume). Rates of fixation per cell are of little biogeo­chemical interest (although the moments of distribution of cellular rates and properties may be of intense eco­logical interest). Also of limited interest are rates per unit volume at a discrete depth. The most useful index of primary production for ecological application is one referred to unit area of ocean surface. Again, measure­ment procedures that do not yield results expressed in this form oblige us to adjust the results to make them useful for ecological or biogeochemical purposes.

In some circumstances we may be interested to evalu­ate the contribution to primary production of the broad taxonomic groups that comprise the autotrophic com­munity. Here, the best indicators we have of taxonomic status are pigment complement and size. The proven tools available are pigment separation by high perform­ance liquid chromatography, or by fluorometry, and size characterization by light scattering. These approaches are covered by the contributions of Gieskes (this vol­ume) and Li (this volume).

IC E S m ar . Sei. S y m p . . 197 (1993)

M ethods o f m easurem ent

Methods for measuring primary production are tabu­lated in Table 1, together with their nominal time scales. There are two principal, established groups of tech­niques. In vitro methods refer to measurements made on samples enclosed in glass or other containers. M etab­olism is usually indexed by uptake of isotopic tracers or, less commonly, by changes in the chemical composition of the medium. The size of the container is typically in the range from a few millilitres to a few litres, the incubation time from less than one to a few hours. Interpretation of tracer measurements of primary pro­duction is addressed in the contributions to this volume by LeBouteiller. Richardson, and Williams.

Bulk property methods are based on changes in the chemical composition of the free medium, induced by the activity of the organisms, in a certain time interval. Often, the concentration ratios of mother and daughter isotopes are used to establish the time scale over which the chemical change has occurred. The characteristic time scale for these methods is from one day to several years. The measurements may be referred to a particular depth, but because they are usually of extended dur­ation , a certain integration over depth is implied through diffusion. Application of bulk-property methods is covered in the contributions of Emerson and Quay, Minas and Robertson, in this volume.

A third group of methods, optical methods, is of growing importance. These methods, which may be active or passive, depend on the known physiological relations between absorption of radiation, fluorescence, and photosynthesis. They are dealt with in this volume in the contributions by Falkowski and Kolber, Doerffer, Sathyendranath and Platt, and Tilzer.

M etabolic interference

One of the principal problems with measurements of primary production in the field is that the (autotrophic) organisms of interest overlap in size with heterotrophic organisms in the same assemblage. It is extremely diffi­cult to distinguish the metabolism of the one group from that of the other. Further, the catabolism of the auto­trophs themselves often interferes (depending on the measurement procedure) with their anabolism that we are trying to measure. With the recent discovery of the autotrophic prochlorophyte community (Chisholm et al., 1988; Li and Wood, 1988), we now know that there is an autotrophic element corresponding to every size class of heterotrophic bacteria in the ocean.

These problems can affect both in vitro and bulk- property methods for measurement of primary pro­duction. They are dealt with in the contributions to this

IC E S m ar . Sei. S y m p . . 197 (1993) Measurement o f primary production 5

Table 1. M eth od s for est imating primary production in the ocean and the nom inal tim e scales on which the results apply . The

com p on en ts Pg (gross primary produ ct ion), P„ (net primary product ion), and Pc (net com m u nity production) o f primary

production refer to a sch em e based on carbon; PT (total primary product ion), P r (regenerated product ion), and P new (new product ion) to o n e based on n itroge n . Sedim entation rate refers to the gravitational flux o f organic particles leaving the photic z on e

( = export product ion), not the (m uch smaller) flux arriving at the sed im ent surface. Based on Platt et al. (1989) and Platt et al. (1992).

M ethodN om in al c o m p o n en t o f

production N om inal time scale

In vitro PT ( - P n ) Hours to 1 d (duration o f incubation)14C assim ilationt Pt Hours to 1 d (duration o f incubation)0 2 evolution P1 new Hours to 1 d (duration o f incubation)15N 0 3 assimilation P r Hours to 1 d (duration o f incubation)15N H 4 assim ilation Pnew ( '= P c) Hours to 1 d (duration o f incubation)

ls0 2 e vo lu t ion + f

Bulk property P1 new Hours to daysNO;, flux to photic z o n e | P* new Seasonal to annual

O 2 ut ilization rate O U R below photic z on e P1 new Seasonal to annual

N et O-. accum ulat ion in photic zone P1 new 1 d to 300 d238u/234Th§ P1 new Seasonal and longer3H /3H e§§

Optical Pt < 1 s

Double-flash fluorescence* Pt < 1 sPassive f lu o r e s c e n c e ^ Pt . Pnewll D ays to w eighted annualR e m o te s e n s i n g f l

U p p e r and low er limits Pncw ( s P c)- (low er limit) D ays to m on ths (duration o f trapSedim entation rate be low photic zone PT (upper limit) dep loym en t)

Optim al energy conversion o f p h otons absorbed!] Pnew ( low er limit) Instantaneous to annualD e p le t ion o f winter accumulation o f N 0 3 Seasonal

t H ere and e lse w h e r e , P new can be calculated from PT if there is an ind ep en dent m easurem en t or est imate o f the / -ratio , f t B en der e ta l . (1987).t A ltab et and D e u se r (1985); Lewis e t al. (1986); Jenkins (1988).§ C oale and Bruland (1987). I sotopic disequil ibrium in photic z o n e used to est im ate export o f particles from it.

S§ Jenkins (1982). I sotopic data used to establish a tim e scale for calculation o f O U R .* Falkowski and Kolber (1990).

± t Kiefer e t al. (1989).HU P t from physio logical m od el (Platt and Sathyendranath , 1988; Platt e t a!., 1990).II /-ratio from tem perature-n itrate correlations (Sathyendranath et a l ., 1991).11 P l a t t e / al. (1989).

volume by Banse, Harrison, Jackson, Langdon, and Sakshaug.

N ew production

Given the wide variety of methods, the broad range in their characteristic time scales, and their different sus­ceptibilities to metabolic interference, it should be clear that the various techniques do not all share either the same fundamental or operational definitions of primary production. Three main quantities are identified (Platt et al. , 1984). When expressed in terms of carbon fluxes, they are the gross primary production Pg, unaffected either by the respiratory metabolism of the autotrophs or by the metabolism of any other component of the pelagic community; the net primary production, Pn,

corrected for the metabolism of the autotrophic commu­nity; and the net community production, Pc, corrected for the metabolism of the entire pelagic community. Operationally, it is extremely difficult to obtain a figure for Pn unaffected by the activity of the microhetero- trophs.

There is a parallel set of terms for the fluxes expressed in terms of nitrogen (Dugdale and Goering, 1967). These are the total primary production, PT, the regener­ated production, Pr, supported by nutrients made avail­able locally through the products of metabolism; and the new production, P new, supported by nutrients supplied from sources external to the photic zone (reviewed by Platt et al., 1989). Conventionally, results from bulk- property methods are reported in the nitrogen-based scheme. Results from in vitro and optical methods may be reported in either the carbon-based or nitrogen-

6 T. Platt and S. Sathyendranath

based scheme, depending on the orientation of the work. Conventionally again, biogeochemical work is usually presented in the nitrogen-based scheme, whereas ecological work is reported in the carbon-based scheme.

The point of connection between the two schemes is that, under the assumption of biogeochemical steady state, Pnew is identified with Pc. The nominal com­ponents of primary production addressed by the princi­pal methods are shown in Table 1.

Comparing results from different

m ethods

It should be clear from the foregoing that serious diffi­culties arise whenever it is required to compare esti­mates of primary production obtained using different techniques. One of the principal problems is the conver­sion of the results of in vitro tracer methods, typically incubated for less than one day, into daily rates (the ecological goal). Even for the light period alone this is not a trivial task. For a full 24-h day it is a problem of great difficulty, and one that, historically, has not received its due attention. The integration of such re­sults over depth to give a figure for the water column is usually a less severe problem, particularly if detailed information is available on the biomass profile.

Bulk-property methods give results with implied inte­gration over depth, but the range of integration varies depending on the characteristic time scale of the method and on the details of the measurement design. More­over, these methods are usually aimed at Pnf!W, whereas in vitro tracer methods are aimed at Pg or Pn. Extreme caution must be exercised before coming to the con­clusion that the different methods do not agree with each other (Platt et al., 1989). The relationship between primary production and growth is addressed in the contribution of Geider (this volume).

Fluxes or parameters

The classical way to assess primary production in the field is through in situ incubations using the 14C method. Properly applied, this technique will give a vertical profile of primary production through the photic zone. The profile can be integrated over depth, and perhaps adjusted for incubation time, to give an estimate of daily, water-column production. To the extent that this was the goal to be met, the technique will have served us well. However, one seeks also to understand the seasonal and regional variations in daily production in terms of variations in environmental covariables, and

I C E S m ar . Sei. S y m p . , 197 (1993)

also to predict daily production given information on these covariables.

Predictive modelling requires that we are able to parameterize the process in question, that the para­meters are in fact observables of the pelagic ecosystem, and that we have access to a suitable parameter archive built up from fieldwork. Thus, another imposition is placed on field programs: to acquire data, not just on the photosynthesis flux, but also on the parameters that control it. Estimation of the parameters of the photosynthesis-light curve can be done routinely in the field. One area for which considerable data have been taken is in the Sargasso Sea region of the Northwest Atlantic Ocean.

In a study conducted there over several years, Platt et al. (1992) found that the photosynthesis parameters were remarkably constant, a result that would have been difficult, or impossible, to obtain using only information on the vertical profile of in situ primary production. Further, during spring bloom conditions, photosyn­thesis parameters were substantially higher. Their de­cline, after the bloom, to the quasi-constant values observed during most of the year, corresponded with the decline in the available nitrate. The assimilation number P® and the initial slope a B of the photosynthesis-light curve did not vary independently of each other: their magnitudes were correlated such that their ratio, Ik, the photoadaptation parameter, tended to be stabilized. Results like these can be applied immediately, both in numerical modelling of primary production and in its estimation from remotely sensed data. It would be much more difficult to assimilate into models the results of vertical profiles of primary production, although the profiles do provide the raw material for testing the models. The conclusion from this work is that as much, or more, effort should be directed in the field at measuring the parameters that control important eco­logical fluxes, in this case primary production, as at the fluxes themselves.

The calculation of primary production given infor­mation on photosynthesis parameters and biomass will be considered in the contributions of Tilzer (this vol­ume) and of Sathyendranath and Platt (this volume).

Problems arising from spectral effects

One of the most serious, and least-studied, of the poten­tial errors in measurement of primary production is that due to the wavelength of the incident light. It is well known that the action spectrum of photosynthesis is far from flat. Nor are the other critical spectra flat: the spectrum of solar radiation at the sea surface and the spectrum of attenuation of light as it transmits through the water. The picture is further complicated because

IC E S m ar . Sei. S y m p . . 197 ( I W ) Measurement o f primary production 7

the spectral effects are accentuated as the pigment biomass increases. The result is that the irradiance at depth changes both in magnitude and quality in a man­ner that it difficult to anticipate without independent knowledge of at least the shape of the distribution of pigment biomass with depth. The problem for measure­ment of primary production is the difficulty of matching either the magnitude or spectral quality of irradiance seen by the sample to the irradiance at depth. The problem is less acute for in situ incubations, addressed in the contribution of Dandonneau (this volume), than for incubations carried out on the ship, dealt with by the contributions of Lohrenz (this volume) and Tilzer (this volume).

Various approaches have been used to estimate the error involved in ignoring spectral effects in the esti­mation of primary production. For a uniformly mixed water column, Platt and Sathyendranath (1991) calcu­lated that the error was variable, ranging from negligible to greater than 30%, depending on biomass and mixed- layer depth, even using an exact, independent value for the attenuation coefficient. For non-uniform biomass profiles, Sathyendranath et al. (1989) calculated that spectral errors could be as high as 60%, depending on the shape of the profile. Systematic study of the influ­ence of the shape of the pigment profile was facilitated by construction of a generalized profile whose para­meters could be determined in specific cases.

The potential error has also been checked by direct measurement. Kyewalyanga et al. (1992) showed that, in oligotrophic waters, a fully-spectral model, using local values for the photosynthesis parameters, gave an esti­mate of water-column production in excellent agree­ment with that obtained by in situ measurement. A broad-band model, however, gave a result some 50% lower than the in situ value. If the broad-band model of primary production was implemented using a spectral model for the light transmission, the error was reduced to about 20%. If an exact value was used for the average attenuation coefficient over the photic depth, the esti­mate of water-column primary production was close to the in situ value, in agreement with the theoretical results of Platt and Sathyendranath (1991). The effect of spectral response on the estimation of primary pro­duction using remotely sensed data is considered in Platt et al. ( 1991 ). One of the principal results of this study was that the estimates from the non-spectral models could be made to match those of the fully-spectral models by adjusting the magnitude of the vertical attenuation coef­ficient. Hence the utility of the non-spectral models depends on the method used to parameterize the vertical attenuation coefficient.

The influence of spectral effects on the computation of primary production will be considered in the contri­butions of Tilzer (this volume).

Extrapolation in space

One of the recurring problems in fieldwork with ships at sea is the gross undersampling that we are obliged to accept, a simple consequence of the speed of ships and the size of the ocean. Thus, we are faced continually with the task of extrapolation of sparse data sets if we wish to produce conclusions at the regional and larger scales. Within the last ten years, a tool of enormous power has been introduced that simplifies (but does not eliminate) the task of extrapolation: remote sensing of ocean colour (Esaias e ta l., 1986). With this tool we can see, for the first time, the synoptic distribution of a biologically important quantity (surface-layer chlorophyll concen­tration) at the regional scale of the ocean. The images obtained by remote sensing of ocean colour have sensit­ized biological oceanographers to the enormity of the extrapolation problem, even while facilitating its solu­tion.

It is in dealing with the issue of extrapolation that we see the value of measuring the parameters of the photosynthesis-light response as well as the photosyn­thesis flux itself. One protocol that has been proposed to effect the extrapolation of data obtained by ship to regional ocean scale is to partition the ocean into a suite of provinces within which the critical parameters, in­cluding the photosynthesis parameters and the para­meters of the biomass profile, could be regarded as quasi-constant for a given season (Platt and Sathyendra­nath, 1988). Delineation of the provinces would be according to a variety of criteria, physical, chemical, and biological. Identifying the exact boundaries at any time would be aided by inspection of the ocean colour im­ages. This is an approach that remains to be fully tested, but in the North Atlantic, where most is known about the relevant parameters, the preliminary results are encouraging.

Proceeding by partition into provinces does not imply that one is uninterested in understanding the causal mechanisms by which the parameters are changed in time and space. Indeed, the ultimate goal would be to explain the large-scale distribution of parameters in terms of environmental properties, ideally of those properties that could be measured by remote sensing. At present, we are far from this, and we must make do with less satisfying methods.

A cknow ledgem ents

The work presented in this paper was supported by the Department of Fisheries and Oceans, Canada, the Office of Naval Research (USA), the National Aero­nautics and Space Administration (USA) and the Euro­pean Space Agency. Additional support was provided

8 T. Plait and S. Sathyendranath IC E S m ar . Sei. S y m p . , 197 (1993)

by the Natural Sciences and Engineering Research Council through Operating Grants to SS and TP.

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