OCEANOLOGICA ACTA- VOL 15- N°2

Nutrients Net community production New production Grazing in "High Nutrient-Low Chlorophyll" waters Tropical Ocean Antarctic of the tropical and Antarctic Oceans: Nutriments Production nouvelle grazing vs iron hypothesis Broutage Océan tropical Antarctique

Hans Joachim Minas and Monique Minas Centre d'Océanologie de Marseille, Faculté des Sciences de Luminy, case 901, 13288 Marseille Cedex 9, France.

Received 13/01192, in revised form 13/02/92, accepted 20/02/92.

ABSTRACT An analysis of tropical upwelling systems shows a great range in the rate of increase of the standing stock expressed in tenns of the water column chlorophyll content. Grazing appears to be the main factor responsible for lowering the rate of increa­ se, especially in moderate and strong High Nutrient-Low Chlorophyll (HNLC) waters. A simple model comparing Net Community Production (NCP) rates with observed chlorophyll increase rates, leads us to conclude that phytoplankton population must present high specifie growth rates on a daily rhythm in order to overcome grazing. Maximum specifie growth rates (V max) calculated for daily total production (TP) are, in the two main upwelling areas, 1.57 d-1 offNW Africa and 1.04 d-1 off Peru. For extreme HNLC conditions in the Costa Rica Dome, V max remains high, 0.98 d-1. The Atlantic equatorial upwelling in the Gulf of Guinea is characterized by mode­ rate HNLC conditions. From an analysis of a nutrient-temperature diagram and beat fluxes, we deduce a nitrate-based new production (NP) rate of 0.368 g C m-2 d-1, corresponding to af-ratio of 0.3. The Peruvian coastal upwelling, during the strongest upwelling period in austral winter, shows HNLC conditions extending far offshore and reaching the Galapagos Islands. NCP could not be determined in the se waters. Antarctic nutrient consumption diagrams are also presented. An overall consumption evaluation along a 1,550 km North-South section leads to atomic assimilation ratios of âSi/.:\N/âP =55.9/12.3/1. From the end of winter to end of summer, the average nitrate consumption is 0.38 mol m-2. For this five month per­ iod, the calculated NP is 0.2 g C m-2 d-1. From the silicon-nitrogen ratios during nutrient consumption and those in the particulate material, we deduce af-ratio slightly lower than 0.5. Thisfvalue confmns earlier data derived from 15N uptake studies. The model application leads to a V max (TP) value of 0.54 d-1, which does not seem excessively low in the low temperature regime of the Southem Ocean. We discuss an Antarctic scenario starting with "grazing" limitation and finishing with iron limitation. Despite evidence in favour of the grazing hypothesis which allows us to classify regions geographically into "high and low" speed areas of phytoplankton deve-

0399-1784/92102 145 18/$ 3.80/© Gauthier-Villars 145 H.J. MINAS, M. MINAS

lopment, a global chart of dust inputs into the ocean strongly supports the iron limitation hypothesis. This observation constitutes a challenge to the "grazing only" hypothesis and militates in favour of more detailed future studies. Oceanologica Acta, 1992.15, 2, 145-162.

RÉSUMÉ Production communautaire nette des eaux «Riches en Nutriments­ Pauvres en Chlorophylle» dans les océans tropical et antarctique : le broutage face à la limitation par le fer L'analyse des systèmes tropicaux de remontées d'eaux met en évidence l'existen­ ce de toute une gamme de taux d'accroissement de la biomasse autotrophe expri­ mée par le contenu en chlorophylle dans la colonne d'eau. Le broutage s'avère être le principal facteur responsable du ralentissement du taux d'accroissement, ceci particulièrement dans les conditions «Riches en Nutriments -Pauvres en Chlorophylle» (RNPC). La construction d'un modèle simple prenant en compte les effets réciproques phyto-zooplancton au cours du cycle nycthéméral, permet de comparer les taux de Production Communautaire Nette (PCN) à ceux des accroissements observés de chlorophylle, et conduit à la conclusion que le phytoplancton, face à la pression de broutage, possède nécessairement des vitesses de croissance spécifique élevées. Les taux maximaux de croissance spécifique (Vmax) calculés pour la production totale (PT) journalière dans les deux principales zones de remontée sont de 1 ,57 r 1 devant les côtes NW-africaines et de 1,04 r 1 devant celles du Pérou. Dans la situation extrême de grande richesse nutritive associée à des biomasses faibles caractérisant le dôme de Costa-Rica, V max garde une valeur élevée de 0,98 r 1• L'upwelling équatorial atlantique dansle golfe de Guinée est marqué par des conditions RNPC. A partir de diagrammes éléments nutritifs-température, et des flux d'apport de chaleur, on déduit une consommation de nitrate qui, en termes de carbone, représente une production nouvelle (PN) de 0,368 gC m·2 r 1 et corres­ pond à un facteur f de 0,3. L'upwelling côtier péruvien, observé pendant la période principale de remontée en hiver austral, a des propriétés RNPC qui s'étendent très au large des côtes et atteignent les abords des îles Galapagos. La PCN n'a pu être déterminée dans ces eaux. Des diagrammes de consommation nutritive sont également présentés. Une éva­ luation générale de l'utilisation nutritive tout au long des 1550 km d'une section nord-sud, conduit à des valeurs de rapports atomiques de àSi/àN/àP = 55,9/12,3/1. Entre la fin de l'hiver et celle de l'été suivant, la consommation moyenne de nitrate est de 0,38 mol m·2. Pour une période de cinq mois, la PN est de 0,2 gC m·2 rt. A partir des rapports de consommation silicium-azote et de ceux du matériel particulaire, on peut déduire un facteur/légèrement inférieur à 0,5. Cette valeur confirme d'anciennes estimations de f obtenues à partir de mesures d'assimilation d'azote-15. L'application de notre modèle aux conditions antarctiques conduit à un V max (PT) de 0,54 rt. Cette valeur ne semble pas exagérément faible compte tenu des basses températures du régime antarctique. La discussion évoque un «scénario antarc­ tique» dans lequel la limitation débute par les effets de broutage, mais finit par la limitation par le fer. En dépit de l'évidence de l'hypothèse du broutage, qui nous permet de classer les régions selon une gamme de régimes de développements phytoplanctoniques lents ou rapides, une carte de l'océan mondial présentant les apports d'aérosols plaide également en faveur de l'hypothèse du fer. Cette observation constitue un avertis­ sement sérieux face à la théorie du «broutage seul» et implique la nécessité de futurs travaux plus détaillés. Oceanologica Acta, 1992.15, 2, 145-162.

146 PRODUCTIVITY IN HNLC WATERS

INTRODUCTION (1990) writes: "Meeting biological Fe requirements is rela­ tively easy in neritic waters, where resuspended bottom sediments and associated Fe-rich oxides, colloids, etc., ----- Historical considerations------occur together with elevated concentrations of Fe: Hence ----­ excess N03 is never observed in coastal upwelling envi- The iron limitation hypothesis presented recently by ronments such as those off the west coasts of Africa and Martin (1990) and Martin et al. (1990 a; 1990 b) bas bad a North and South America". considerable impact on the oceanographie community, insofar as the idea leads to the exciting possibility of In Antarctic waters, the "biological conditioning" has been conducting experiments and human interventions at large taken into account in our discussions of possible control­ scales in the open ocean. This will be "un tournant dans ling factors, such as light, temperature, turbulence (Jacques l'histoire" (as we say in French) for oceanography. Despite and Minas, 1981) and grazing (Le Corre and Minas, 1983). numerous recent critical comments (Banse, 1990; 1991 a; The "grazing" hypothesis, formulated by Walsh (1976), has 1991 b; Broecker, 1990; Dugdale and Wilkerson, 1990), become increasingly accepted as the principal explanation. the iron limitation hypothesis bas enough merit to induce a In the tropical Pacifie, the most important contribution des­ critical reevaluation of the so-called "grazing hypothesis". cribing the problem of the HNLC anomaly was made by We must ask ourselves to what extent grazing by the hete­ Thomas (1979), after his earlier observations of nutrient rotrophic community keeps the autotrophic standing stock inversions (Thomas, 1972), due to massive advection of low, and whether this can be the only factor explaining nutrient-rich waters from the Peruvian coast. We shall long residence times of unused nutrients in the euphotic show here how our French colleagues (e. g., Voituriez et zone. There seems no a priori reason to consider that iron al., 1982; Herbland et al., 1983) also considered grazing as limitation, in addition to grazing, might contribute to the the main explanation of the relatively low productivity control of slow nutrient evolution. But one may expect that during the principal upwelling season along and in the vici­ this control occurs at the end of the residence time period nity of the equator in the Gulf of Guinea. of the water body, i. e. at a time before other events are able Minas et al. (1986), in a comparative study of tropical to change the properties of the water. According to Martin, upwelling systems, came to the conclusion that grazing iron in small quantities is available at an early stage in the could explain the existence of different rates in the develop­ surface waters, mainly in the Antarctic after winter mixing. ment of the autotrophic standing stock. HNLC situations, We ali believe that the mechanisms of planktonic dynamics mainly characteristic of the equatorial Pacifie, appear ulti­ in polar waters will probably be different from those in the mately to be nothing other than repressed standing stock warmer waters of the tropical ocean. One major difference development under conditions of high heterotrophic activity. between the two systems is that tropical nutrients, unlike Warm HNLC waters at the sea surface in the tropical ocean antarctic nutrients, are not lost to the deep sea after their are an obvious indicator of longer residence time in the stay in the euphotic zone. In the tropics nutrients are only euphotic zone, because at their origin the waters ascending removed by photosynthesis, however it has not been very into the euphotic zone were cold. We shall endeavour to weil established where and under which conditions this show here in greater detail how Net Community photosynthesis occurs. Production (NCP) studies provide arguments supporting Historically, sorne of the earliest observations and conside­ the grazing hypothesis. We should remember that NCP rations dealing with the paradox of High Nutrient-Low determinations are mostly based on nutrient consumption Chlorophyll (HNLC) were made when Strickland et al. evaluations deduced from field observations. Oxygen pro­ (1969) described two types of nutrient regimes in the duction or C02 consumption can also be used (Codispoti et Peruvian coastal zone and explained nutrient-rich, transpa­ al., 1986).1t bas been recognized that NCP is almost equi­ rent waters by grazing. Barber and Ryther's (1969) investi­ valent to the New Production (NP) (Minas et al., 1986; gations led to the "biological conditioning" hypothesis for Eppley, 1989; Platt et al., 1989). Our statement is that des­ upwelling zones (Barber et al., 1971). The "Barber effect" pite a slow, very slow, or even zero, specifie increase in the was, for ali of us in the French upwelling research team, rate of the autotrophic standing stock in the water, phyto­ the possible explanation for the slow increase of producti­ plankton growth at itself actually takes place at a fast rate. vity in nutrient-rich upwelling systems. During the Cineca­ The main objective is to demonstrate that the phytoplank­ program off the NW African coast, we described once rela­ ton specifie growth is normal or even high. The determina­ tively High Nutrient-Low Chlorophyll waters associated tion of nutrient consumption permits calculation of the with relatively high surface temperatures (t > 18°C) in a total amount of chlorophyll produced by new production. limited area off Nouakchott (Groupe Médiprod, 1974; The difference to the observed chlorophyll content in the Minas et al., 1974). But, as we shall see later, HNLC water gives an indication of the part removed by grazing.lt conditions seem to be rare off NW Africa. lt is important to has been shown that in coastal upwelling zones, more than point out here, that the slow increase in productivity obser­ 60 % of the chlorophyll produced disappeared from the ved and discussed at that time was for processes observed water (Minas etal., 1982 b; 1986). The fate of the removed in NW African coastal waters, while the frrst Barber and planktonic biomass is to fuel the integration of organic Ryther (1969) observations were at the equator. Therefore, matter in the higher trophic levels, the dissolved organic the retarded planktonic bloom in the NW African coastal pool, and the exportation by fecal pellet sedimentation and upwelling was probably not due to a lack of iron. Martin other large sinking particles.

147 H.J. MINAS, M. MINAS

THE GRAZING HYPOTHESIS IN THE TROPICAL 55/1 (given by Ketchum and Corwin, 1965, and often used OCEAN by other authors; see Minas et al., 1986; 1990; Marra et al., 1990). Table 1 contains ali numerical information such as equations, growth constants, specifie growth rates, etc. The Growth kinetics in tropical upwelling systems: cao difference between the two types of curves shows how grazing explain different rates of increasing autotro­ much of the chlorophyll originally produced bas been phic standing stock ? removed by sorne process. First of ali, it can be seen that the Pero curves display a dis­ A detailed diagram analysis (Minas et al., 1982 b; 1986) tinctly Iower growth kinetics than those for NW Africa. As has permitted us to determine photosynthetic nutrient given in Table the specifie rates of increase (Vi) of the consomption (and oxygen production) in upwelled water 1, chlorophyll stock (l:Chlobs) are 0.221 d-1 for NW-Africa, bodies during their advection from an upwelling source i. area. In addition, an analysis of T-S diagrams can lead to e. six times greater, and 0.036 d-1 for Pero. For purposes of residence time evaluations according to a beat budget comparison, a reference curve (dashed) is shown in Figure 1 for a 1 d-1 , one doubling per day (equation y= y • mode! established by Bowden (1977). A combination of V~= i.e. 0 100.301 , with y • = 16.11, which is the initiall:Chlo value the two methods (Minas et al., 1986) allows NCP determi­ 0 nations for steady state upwelling systems with these for Pero).lt is important to remark that the specifie rate of results. lt is possible to study the growth kinetics of the increase is called Vi, i.e. V-integrated, because it concems autotrophic standing stock. the increase of standing stock in the whole water column, which at least contains the euphotic zone. This problem will Two types of growth curves for coastal upwelling off both be discussed later in more detail. The comparison of the NW Africa and Pero are shown in Figure 1. The thin curves three curves (Pero, NW Africa, Reference) suggests that show the observed increase in the phytoplankton standing stronger grazing off Pero is probably the reason for the slo­ stock (l:Chl0 b5), expressed as integrated chlorophyll per wer observed increase of the amount of chlorophyll. As we square meter (l:Chl mg m·2). The thick curves show the explained more fully in Minas et al. (1986), the bloom off increase in l:ChlNCP• i.e. the amount of chlorophyll dedu­ Africa can initially start over the continental shelf, and by ced from the nutrient consomption (or biological 02 pro­ the time larger animais (Euphausiids) at the shelf break duction). This quantity bas been calculated using the begin their grazing pressure, it is too late, because the phy­ Redfield conversion ratio and a carbon/chlorophyll ratio of toplankton biomass is already overwhelming and its rapid

Table 1

Summary of data shawn in Figure 1. Numerical characteristics concerning the observed increase rate of chlorophyll standing stock and that deduced from NCP rates. Specifie increase rates are given on an integrated basis (V;). and at the depth of the photosynthetic maximum, like classical assimilation numbers of the production curve. Principal attention should be paid to the characteristics of the Chlobs curve showing the "apparent" increase controlled by grazing. Corresponding NCP curve constants have also been calculated, but they have not the same significance because, as we shall see later in the theoretical paragraph, the NCP curve is a cumulative curve demonstrating nutrient consumption.

PERU NW-AFRICA REFERENCE obs NCP obs NCP 9 301 Equation IChJ.,bs = 16.11 .10°.0lS4T IChiNCP = 29.79 ,100.0I 8T ICbl0bs = 26.30 • 100.o861f IChiNcP = 47.23 .100.101ZT IChl = 16.11 • 10° T (see Fig.1) derived from derived from or IA02bio = 3.98 • 100.0198T IA02bio = 6.31 .100.1012T IChl = 16.11 e0.693T

V; (d-1) 0.036 0.047 0.221 0.262 1.0 Specifie increase rate (integrated)

AN; (mgC mgCbl-1 d-1) 0.20 0.26 1.22 1.44 55 C/Cbl=55/1 Assimilation number (integrated)

ANmax = 1.86 AN; 0.37 0.48 2.27 2.68 10.23

ANmax(TP) for f*=0.5 0.74 0.96 for f*=0.2 1.85 2.40 forf*= 0.64 355 4.19

Vmax (d-1) (TP) forf=05 0.135 0.175 forf=0.2 0.336 0.436 forf=0.64 0.646 0.762

• from Minas et al. ( 1986).

148 PRODUCTIVITY IN HNLC WATERS

increase can no longer be brought under control. Off Peru, 1 zooplankton are more abundant in the euphotic zone, becau­ 1 1 -hlgh se of the anoxie water just below. This results in more inten- ,1 - eutotroph se grazing pressure at the begiiirung of the- blooiri~ keeping ------specifie lncrease rate------­ 250 1 the phytoplankton growth under control from the outset. f,' grezlng ~ 1 low 1 Another possibility is that during the weak upwelling sea- 1 , son off Peru, relaxation periods of upwelling create zoo- ysp1 plankton excess, which is conserved near the coast by the 0 200 nlght day flow pattern of water masses (subsurface onshore flow). photoperlod In Figure 1, we also compare the shapes of the IChlNcP and IChlobs curves. The (NCP) curve increases slightly ft faster than the (obs) curve for both Peru and NW Africa. It . 150 10121 E YNCP •47.23-10 is also interesting to compare the values of the productivity Dl °' index (mgC mg Chl-1 h- 1), here called the assimilation E number (AN). The values of AN given in the literature are ~ the best inter-comparison term, representing a specifie () w 100 uptake rate. Since ANi constitutes the integrated value, we can estimate ANmax (light saturation value) by multiplying ANi by the factor 1.86. This value was statistically establi- shed by Minas et al. (1982 a). Almost the same value (1.89) resulted from a similar evaluation by Cullen et al. (1992). Considering the Peru data, the values of AN for both curves (NCP and obs) are low. This is not surprising, as ANmaxNCP can be considered as an approximation of the new production value. But the values still remain relatively 0 2 3 "' 5 8 7 8 9 low when the /-ratios are applied (see ANmax (TP) in Tab. tlme days 1). This demonstrates that the values of Vio as well as AN, are only apparent characteristics of the grazing controlled FigureZ slow speed curve. In fact, the real physiological specifie Application of the zz madel to the ChlNcP and the Chlobs curves in the growth rate must be higher. In order to show this, we case of the NW African upwelling. The principle of the model is to address the problem in the following paragraph. construct a daily exponential curve (Yzz = Yzzo·1 0 fLZZT) which, during the photoperiod (Fig. B), reaches the Ybrw curve. The latter is obtained by subtracting from the NCP curve the cumulative day-to-day difference fln lHCl = Ao + d1 + dz + ... dn• as shown by Figure A. Daily curve is presented NW AFRICA at the 5th day. The objective is to evaluate the flzz value for each day and ,., PI!RU to derive from this the co"esponding Vzznuu value. Equations and data are given in Table 2. The figure for the Peruvian system is not shown but, ClfiJ · for purposes of comparison and better understanding, the reader may .... construct the Peruvian curve and verify the data of Table 2. ~ 200 NCP ~ The day-night "zigzag model'' (zz model)

As a possible explanation for the retarded growth curves of the standing stock shown in Figure 1, we propose that the day-night rhythm of the activity of the autotrophic vs hete­ IHNLCI rotrophic community leads to a zigzag movement of the CRDD'èas autotrophic standing stock. Circadian periodicities in natu­ 0 10 20 30 40 110 110 70 80 Tlme diiY• ral populations of marine phytoplankton are a well known fact (see review done by Sournia, 1974). We are inspired Figure 1 by severa! studies in recent literature dealing with day­ night effects on the water properties of planktonic activity. Kinetic characteristics of the increasing standing stock of chlorophyll from two coastal upwellings off NW-Ajrica and Peru (redrafted from Oudot (1989) was able to detect during time series diel Minas et al., 1986). The exponential equations and specifie increase rates changes in the concentration of Oz and COz. A zigzag are given in Table 1. Curve IChloba represents the increase in water variation displays biological oxygen production and COz column chlorophyll vs time. Curve IChlNcP represents the total amount consumption during the day, and the contrary during the of chlorophyll produced as calculated from the nutrient consumption. In our interpretation, the slower evolution of Peru is due to grazing. NW­ night, due to respiration. Le Bouteiller and Herbland Africa, less controlled by grazing, grows faster. For comparison, a (1982) observed during similar studies such day-night reference curve displaying a higher specifie growth rate ( 1.0 a-I) is shown variations in chlorophyll concentration. Grazing by diel (see data on Tab.1). The points representing the Costa Rica dome (CRD) migrant zooplankton and necton and associated nitrogen upwelling are typical for HNLC conditions, and contrast with the fast­ growing high chlorophyll (HC) system off Peru. The CRD points fluxes below the euphotic zone received rouch attention in correspond to average values resulting from a model established by two papers by Longhurst and Harrison (1988) and Broenkow ( 1965) and discussed by Minas et al. ( 1974; 1986). Longhurst et al. (1989). Cullen et al. (1992) summarize:

149 H.J. MINAS, M. MINAS

Table 2

The day-night "zigzag model": equations and results of calculations leading to assimilation numbers and jinally to the highest specifie increase rates, in the areas offPeru and NW-Africa.

PERU NW-AFRICA

Equations y btw =16.876 .100.0157ST Ybtw =31.32 .100.D9tBT (see also Tab. 1)

The daily NCP-eurve equation is Yzz =Y zzo.lOI=T

n=T=1 n=T=30 n=T=60 n = T = 1 n = T = 5 n = T = 10

0.0359 0.0460 0.0566 0.188 Ybtwn- Dn 0.168 0214 JA.zz= 1og -Y-o-bs-n--1 -

v zzi (d-1) 0.086 0.139 0.471 0.635 specifie inerease rate (integrated)

ANzzi (mgC mgChl-1 b-1) 0.473 0.616 0.765 259 2.98 3.49 assimilation number (NP) (integrated)

ANzzmax= 1.86 ANzzi (NP) 0.880 1.146 1.423 4.817 5543 6.491

ANzzmax (TP) forf*=05 1.760 2.292 2.846 forf*=02 4.400 5.730 7.115 forf*=0.64 7.527 8.610 10.142

V zzmax (d-1) (TP) specifie increase rate forf=0.5 0.32 0.42 0.52 for f= 0.2 0.80 lM 1.29 forf=0.64 137 1.844

*from Minas et al. ( 1986); see also Eppley ( 1989).

"Diel variability of bearn attenuation also indicated high origin bas already the value (ChlNcP)o = 47 .23, which specifie growth rates of phytoplankton and a strong cou­ means that at the beginning there is a signature of nutrient pling of production with grazing". consomption in the water. The ftrst day curve bas to reach a point below the NCP curve at a vertical distance of !J.o = In our following demonstration, the amplitude of the day­ (ChlNCP)0 - (Chlobs)0 =20.93. For the following equation night oscillation is controlled by the intensities of algal and lzz calculation (2nd day), the first night grazing diffe­ growth vs herbivorous grazing (Fig. 2B). By means of the rence dl is cumulated with the initial !J.0 • The third day, d2 following simple model, which we call the day-night "zig­ is added to lJ.o + d 1, etc. The caption of Figure 2 de scribes zag" model, we propose to extract from the position in the in greater detail the operations for day T =5. All points diagram of the ChlNcP curve relative to the position of the reached by the daily Y zz curves can be connected by a line Chlobs curve, a specifie increase rate of the standing stock which will be called the Y btw curve because of its position during the daily photoperiod. The extracted value will between (btw) the (NCP) and the (obs) curves (equations become nearer to, or even represent the true specifie algal for ail curves are given in Table 2). The two Ybtw relations growth rate. As demonstrated by Figures 2A and 2B, the concerning Peru and NW Africa are obtained by approxi­ principle of the model is to determine for each day, the mation because, as analysed in the following theoretical exponential growth function necessary to satisfy a geome­ paragraph, the (btw) line cannot correspond to a purely trical position dictated by the ChlNcP curve. The growth exponential curve. This approximation bas almost no coefficient J.t of this daily equation will be called J.l.zz, and influence on the second decimal of the V zz values. Results the deriving assimilation numbers and specifie increase of the zz model are contained in Table 2. As for Figure 1 rates will be designed also with the zz index. Figures 2A and Table 1, we also calculated the assimilation indexes and 2B show the treatment of the ChlNCP and Chlobs curves which we then used to calculate values of V by taking into in the case of the NW African upwelling system. The same account the /-ratios. As announced before, we conclude treatment bas been applied to the Peru curves. The results that the model allows us to extract and to define from res­ for the two upwellings regimes are given in Table 2. The pective positions of the (NCP) and (obs) curves a second treatment procedure is the following: the NCP curve at the specifie increase rate V zz• in addition to the apparent

150 PRODUCTIVITY IN HNLC WATERS

increase rate given in Figure 1 and Table 1. Let us call (i.e. the V zz value) for high values ofT. This demonstrates these apparent rates (A)V and compare them to the V zz· At that a constant grazing leads very rapidly to negligible gra- the integrated level, and concerning "new production", we zing effects. In case 2, we choose a relatively low initial ---have on average the following values [V zzi forT =5 (NW--- grazing but allowed it to increase exponentially. We choose ---- . Africa) and T = 30 (Peru) in Table 2) compared with the 1-lzz to correspond to a high specifie rate of increase (V = data in Table 1: 1.5 d-1). In this case Yobs remains a simple exponential NW Africa: Vzzi = 0.54 d-1 >(A) Vi= 0.26 d-1, function resulting in a constant (Vobs = 1 d-1). The Ybtw is i.e. 2.1 times greater. also reduced to a simple exponential form, but the Y NeP Peru : Vzzi = 0.11 d-1 >(A) Vi= 0.047 d-1, equation becomes more complex. The specifie rate of i.e. 2.4 times greater. increase changes with time, starting from an initial value of 1 1 In order to obtain highest V values concerning total pro­ V NCP of 1.5 d- (frrst day) and decreasing towards 1 d- for duction (TP) at light saturation, we transformed frrst V zzi longer time values. into assimilation numbers and then back to V zzmax(TP) as Returning to the functions given in Figure 2, we can now done for the calculation in Table 1. We fmally obtain: mention that grazing increases exponentially (Gr= 6.581 . V zzmax (TP) - NW Africa = 1.57 d-1 > V zzmax (TP) - Peru 1Q0.112T). We can also state that IJ.zz bas an exponential = 1.04 d-1. function (IJ.zz = 0.1677 . }()kT, with k = 0.012).The upwards shift of 1-lzz and V zz with time is probably not a mathemati­ These values show that the specifie growth rate evaluated cal artifact because it is known from the literature that the by the model reaches a high value off Peru and therefore is specifie growth rates of phytoplankton increase with tem­ not fundamentally different from the value for NW Africa. perature. According to Eppley (1972), V= doubling d-1 = The slightly lower value in the tropical Pacifie is perhaps a 0.851 . 100.02758 (equation given under this form by Frost, signal of sorne iron limitation as we shaH see later in Figure 1987). As given in Table 2, our increase of V (from 1.4 to 6C. The difference could be due to a greater activity of 1.8, i.e. AV= 0.4 for NW Africa, and for Peru from 0.8 to microzooplankton keeping the value of V at a lower level. 13, i. e. AV = 0 .5) is of the same order of magnitude as that The grazing mechanism of microheterotrophs is still poorly calculated from Eppley's formula. A temperature change understood. In regard to migrant macrobiota, their influen­ from 15 to 19°C (the increase of e is about the same in the ce is permanent, day and night, because they are inti­ i.e. two upwelling zones) leads to an increment AV of0.6 d-1. mately associated with the algae. On the other band, Martin We are at present conducting a theoretical study of this (1990) argues that coastal upwelling systems are not lac­ model, which will be supplemented by additional observa­ king in iron because the sediments provide a sufficient sup­ tions from upwelling systems. ply. As a global conclusion resulting from our model appli­ cation, we believe that grazing is mainly responsible for the much lower apparent increase rate of· the phytoplankton The HNLC conditions of the Costa Rica dome standing stock observed off Peru. The diagram in Figure 1 shows values of ~ChiNcP and ~Chlobs from the Costa Rica dome (CRD) upwelling. Some theoretical remarks concerning the zz model These are average values, for a steady-state system corres­ ponding to the observations of Wyrtki (1964) and Instead of analysing the system, let us now build up and simulate the phenomena by establishing from the daily Table 3 basic function, i.e. Yzz = Yzzo.lO!J.ZZT, the three other func­ Equations of V vs time curves for several values of grazing (Gr) and tions, i.e. Yobs• Ybtw and YNCP· It is useful to show how daily growth coefficients (!lu). Figures of the different curves are not different levels of grazing (Gr) and specifie increase rates presented, but they can easily be constructed. (Vzz) lead to the main characteristics of the different curves as defmed in Figure 2. In Table 3 we present the equations Casel Equations for sorne simple values of the model parameters (we do not present the figures of the curves, which can easily be Grazing is constant constructed). In the first case (case 1), grazing is kept Example: Gr= 9 Yzz = 10 .100301T constant at a relatively high value in regard to the initial l1zz = 0301 Yobs = 10. 100.301T + 9 (i.e. Vzz= 1 d-1) Ybtw = 100301T + 18 chlorophyll content, i.e. 90% ofYzzo; the daily IJ.zz is cho­ Yzzo= 10 y NCP = 9 (T + 1) + 1Q0.301T sen at a constant value of 0.301, corresponding to one dou­ bling per day (V= 1 d-1). It is interesting to note that the Case2 Equations equation concerning the apparent increase of chlorophyll Grazing increases standing stock bas the form of Yobs = a.lO~tT + b. The same exponentially is true for the equation Ybtw· Ail the equations contain the

same value of 1-l (i.e. 0.301), but on the other band the Example: Gr= Gr0 .10ilT Yzz = 10 . 100.39794T addition in the equation of the constant grazing term is res­ with Gr0 = 5 and 11 = 0.301 ponsible for a shift up of the specifie increase rates (V) 301 l1zz = 039794 Y0bs = 10. 100 T with time. For example, for the Yobs curve, Vobs is initially (i.e. Vzz = 1.5 d-1) ybtw = Yoobs.l()0.301T + GroJ()0.301 T-1 0.1 d-1 (frrst day) and then steadily increases towards 1 d-1 Yzzo= 10 YNCP = YObtw.l00301T + 10 . 100.301T-2_ 5

151 H.J. MINAS, M. MINAS

Broenkow (1965). These values are considered to be repre­ sentative of typical HNLC conditions (Minas et al., 1986). In the dome, where nutrients are high, the chlorophyll concentration stays at a permanently low level near 10 mg Chi m·2 during the upwelling period. The NCP point in Figure 1 corresponds to a value of 218 mg Chl m·2 with a residence time of 83 days. The ratio of :I:Chlobsfl:ChlNCP is 0.046 which is a low value, but appears to be typical of HNLC waters. As we shalllater show, similar values are observed in the Antarctic section of our study. The "zz model" described earlier can be used for evalua­ tion of the specifie increase in the rate of daily production (i. e. V zz). If the grazing rate compensates the daily auto­ trophic chlorophyll production, 218/83 = 2.63 mg Chi are involved in the day-night oscillation. The daily growth constant according to the model is J.lzz =log 12.63/10 = 0.1014 and the corresponding value ofVzzi is 0.263 d- 1• Following the same mode of calculation as before and using a /-ratio of 0.5, the final specifie rate of increase at optimallight conditions reaches a relatively high value of V zzmax = 0.98 d- 1• This is almost the same value as pre­ viously calculated for Pern. In HNLC waters with a higher background of chlorophyll, Cullen et al. (1991) concluded that high (about 15 d-l) to extremely high (>15 d-1) speci­ fie growth rates of phytoplankton suggest vigorous growth of phytoplankton, effectively controlled by grazing. We . •. m. shaH retum to same question in our final paragraph devoted to the NCP study in the Antarctic waters. Our observations of high specifie rates of increase, which are perhaps stilllower than the true physiological phyto­ ,··, ..' ' .1 plankton growth rates, could be discussed in detail within ' ·. ,,... ' .·. 1 •• . .·. the context of an analysis done recently by Banse (1991 lOO... a;1991 b). We agree with Banse's arguments and his conclusion that shipboard culture work on natural popula­ tions suffers from incubation artifacts by modifying the Figure3 natural open-water grazing environment. North-South equator section along 4°W, showing the distribution of temperature (°C), nitrate (Jl.M) and chlorophyll (1!8 [-1) during the main upwelling season (August 1978), draftedfrom Voituriez and Herbland NCP and grazing in the Atlantic equatorial upwelling (1984) and Voituriez et al. (1982). In the Gulf of Guinea, upwelling is covering a large band reaching 5°S. The Atlantic equatorial upwelling has been studied during a several-year programme in the Gulf of Guinea and sur­ conservative properties cannot be determined easily. Minas rounding oligotrophic areas. One of the principal conclu­ .et al. (1991), encountered such difficulties in analysing a sions was that planktonic productivity does not increase three-component mixing system. during the main upwelling season at the equator, despite a We propose, therefore, an approach inspired by a study of significant input of nutrients into the photic zone (Voituriez temperature-nutrient diagrams (Voituriez and Herbland, et al., 1982; Herbland et al., 1983). Zooplankton grazing 1984) of the equatorial divergence. Such diagrams can be was considered as the principal factor for keeping primary used to indicate the intensity of nutrient uptake in upwel­ production at moderate levels. A North-South section of ling zones. temperature, nitrate and chlorophyll crossing the equator in Figure 4 contains a simple scheme showing how three the Gulf of Guinea, south of Abidjan (4°W) is shown in types of diagrams can be formed as a consequence of diffe­ Figure 3. The centre of the upwelling is situated slightly rent intensities of simultaneous surface heating and south of the equator. Cold water with a temperature of 21 to nutrient assimilation. When nutrient uptake is very fast 22°C occupies a large area and has a southem boundary relative to heating, the data points fall below the theoretical near 5°S. Upwelled waters result in surface nutrient levels straight line of mixing, connecting here the end members A between 3 and 6 J.lM N03, but chlorophyll concentrations and B of non-conservative properties. A rapid assimilation never reach high values and are generally less than 1 J.lg t·l. system, as described in Figure 4B, shows such a distribu­ We are at present conducting an evaluation of nutrient tion. If the opposite situation occurs, data points fall above consumption by diagram analysis. Since complex mixing the AB line. Such diagrams characterize strong HNLC occurs in this area, this is a difficult process because non- conditions. As examples, we show diagrams for the Costa

152 PRODUCTIVITY IN HNLC WATERS

Rica dome (Fig. 4C) and equatorial Pacifie (Fig. 4D) with a higher nitrate assimilation, thus maintaining the during HNLC conditions. straight line relationship. The following simple approach Linear temperatu~e-nutrient relationships are encountered can lead to a nitrate flux evaluation, and therefore to a new ---·-in thesuiface water of upwe111ng zones more frequently-- product~on · (~~) · ?ete~inati~n:- ~astenrath ·and· L~mb ---- than deviations from the straight line. This suggests that (1978), m the~2 ~limatlc Atl~s 'mdtcate a net heat gru~ of surface heating and nu trient uptake occur at similar rates 1~ ± 20 W m .rn the u?welhng ~e~ of the Gu~ of Gu~ea or, rather at rates compensating each other, in order to keep d~nng Aug~st,.z. e ..dunng the pn~ctpal u?welhng penod. straight the AB line. It is evident that in this case, mixing St.nc~ there ts m thts area a relatlv~ly mtxed wat~r body which normally occurs in all these systems does not produ- ~~thi~ the upper ~0 ~· one can constder that the druly heat ce any change in the straight line relationship. With a few mput ts absorbed m this upper layer. An average heat flux of 2 2 1 noteworthy exceptions (e. g. Traganza et al., 1983; 100 W m- (i.e. 207 cal cm- d- ), is sufficjent to increa~e Dugdale et al., 1989), these relationships have not received t?e temperature of the upper_ 30 ~ by. 0.07 C pe~ d~y. T e enough attention in remote sensing studies. Ail surface lmear N03-temperature relattonship gtven by Vmtunez and temperature-nutrient relationships in our coastal upwelling Herbland is described by N03 =- 1.88T + 45.5;! = 0.95** studies (Minas et al. 1986) show linear relationships des- (n = 540). Thus a temperature change of 0.07 C corres- cribed by: ' ponds to a change in N03 of 0.1316 (.lM N03. The daily change in a 30-m water column would therefore be 3.948 x T= -0.16 [N03] + 17.53; r=0.96** (n=48) forNW Mrica 10-3 mol N, i.e. -4 x w-3 mol N m-2 d-1. 14C productivity T = - 2.26 [P04] + 21.30; r = 0.97** (n = 48) for Peru curves from the same area show that most of the production T =- 2.40 [P04] + 17 .48; r = 0.87** (n = 63) for SW Mrica. takes place in the upper 30 metres (Voituriez et al., 1982). Voituriez and Herbland (1984) observed that there is no Lewis et al. (1990) have shown that in the equatorial change in the temperature-nitrate relationship between the Pacifie, most of the net heat fluxes reach the deeper part of upwelling and the non-upwelling seasons at, and near the the euphotic zone below the upper mixed layer. In a system equator (see diagram of Fig. 4E). They concluded that there of constant linear temperature-nu trient relationship, this is no increase in the nitrate uptake during the upwelling sea- would mean a more intense nitrogen uptake in the deeper son (July-August-September). We do not full y agree with part of the euphotic zone. Such deeper thermal effects may this statement. The principal reason is that a higher heat also occur along the Atlantic equator. In fact, they do not input should occur during the upwelling regime, coinciding change the average estimation of nitrate consumption on

, ric:ft A @

[N1

Figure4 depfeted

Nutrient-temperature diagram properties in upwelling cotd T warm zones. A) Theoretical explanation: three cases can be · observed: 1) Nutrient assimilation moves the data points below the AB straight line, and simultaneous ® heating is not sufficient to bring the points back to the AB line (·MV > +!:J.T). This type of diagram depictsfast­ .1.6 growing production systems, leading to high .... chlorophyll (HC) concentrations. An example is given ...o• in Figure 4B; 2) Nutrient consumption is small or 1.0 negligible in regard to heating. Such a diagram indicates HNLC conditions (Fig. 4C and 4D); 3) 0.6 0.5 Heating on the average compensates nutrient 0 consumption. The straight line relationship is conserved 14._.... 16~ .... 18-20=--=2~2 ~:u:----=28:--­ (Fig.4E). T•c B) P04 vs T diagram showing fast·growing autotrophs

(from Minas et al., 1986) in the Peruvian coastal Zl upwelling. C) N03 vs T diagram belonging to the equatorial 17 Pacifie upwelling (from Barber et al., 1983), showing HNLC conditions. •.... D: P04 vs T plot, indicating HNLC and corresponding ..13 to the average data of the Broenkow (1965) mode/, 0z drafted from Data Report Scripps Institution of • Oceanography ( 1960). E) General scatter diagram combining ail data collected along 4°W.from 0 to 5°S [Gulf of Guinea (from Voituriez and Herbland,J984)]. The equation given by the authors ~~~-~~-~~~-~m~~e~ is: N03 = -1.88T + 45.49; r = 0.95 (n = 540). T•C

153 H.J. MINAS, M. MINAS the square metre basis. Special attention bas to be paid to 47 46 46 44 43 42 41 40 this problem in future more detailed studies. In terms of carbon, the calculated NP represents 318 mg C m-2 d-1. Voituriez et al. indicate an average value of 14c production (total production) of 1069 mg m-2 d-1. The corresponding /-ratio expressed in terms of carbon is 318/1069 =0.3. This is a first approach which seems reasonable. Since zoo­ plankton are active, a regenerated production of 70 % appears realistic. Modem trace metal clean methods would probably result in a lower /-ratio, since 14C uptake measu­ rements were somewhat underestimated in the past (Martin et al., 1989). This daily NP represents a yearly rate of 9.67 mol C m-2 yi"' 1 (yearly rates are often used by geo­ chemists). Garçon et al. (1989) have recently conducted a theoretical evaluation of NP for this region. Mathematical box model calculations, using the kinematics of co2 fluxes along the equatorial Atlantic divergence, lead to a nitrate based NP of near 17 mol C rn-2 yi"' 1. They indicate a /-ratio of 0.3 for the Gulf of Guinea. Thisfvalue is in fact largely underesti­ mated because total production was overestimated by fac­ tor 2 to 2.4 (hourly 14C uptake rates have been erroneously converted into daily rates). One may argue that the biologi­ cal part of the model does not take into account "grazing", which seems to become a key problem for equatorial zones. We can conclude that because of the relative! y low 5' 10'S chlorophyll content of the waters associated with relatively GALAPAGOS PERU high nutrients, the Atlantic equatorial upwelling may be considered as a moderate HNLC system. lt seems to tum FigureS out that such systems have low /-ratio tendencies, suppor­ Temperature, nitrate (IJM) and chlorophyll (~tg z-1) on the connection ting the idea of more regenerated production due to a domi­ section between the coast of Peru ( 15° S) and the Galapagos Islands. The nant heterotrophic activity. Similar low /-ratios 0.1 to 0.3 section shows a great extension offshore, with high nitrate and low 1 were observed by Murray et al. (1989), who compared and chlorophyll ( < 1 1!8 z- ), with one exception at a coastal station (T and N03 distributions from Minas et al., 1990). discussed the results of severa! NP approaches in the east­ ern equatorial Pacifie. et al. (1989) measured primary productivity with the 14C method in June of the same year at sorne stations south of HNLC in the Peruvian coastal upwelling the equator, between Ecuador (2°S) and the Galapagos. They judged this productivity (0.3 to 0.4 gC m-2 d-l) "ano­ malously low, especially considering the nutrient concen­ The Peruvian coastal upwelling, which during austral win­ tration available". In our first approach (Minas et al., ter appears to belong to the HNLC conditions, bas been 1990), we were cautious with "grazing" arguments, since studied for pelagie productivity mostly during the weak other important factors such as turbulence, light and per­ upwelling season (Barber and Smith, 1981; Codispoti et haps now iron limitation may play a role, especially in the al., 1982). During this weak upwelling season, a great offshore waters. A NCP analysis, as done by Minas et al. variability in the chlorophyll vs nutrient regime exists, sho­ (1986), appears to be very difficult or even impossible for wing aspects of HNLC tendencies as explained above and this season (Minas et al., 1990). also very high chlorophyll concentrations associated with high production rates (Ryther et al., 1971; Simpson and Zirino, 1980; Boyd and Smith, 1983). Only a few descrip­ Some thoughts and concluding remarks dealing with tions are available when strongest winds induce the main large scale features in the tropical Atlantic and Pacifie upwelling during the austral winter (Ju~e to September) (Guillén et al., 1973; Walsh et al., 1980). Long sections Global productivity charts displaying total and export pro­ were carried out during the French Paciprod cruise of R.V. duction (Berger et al., 1987), as weil as satellite images of Jean-Charcot in 1986 [August 8 to September 18 (Coste et sea surface chlorophyll distribution, are frequently exhibi­ al., 1989; Minas et al., 1990)]. High nutrients are observed ted within the framework of Global Change Programs. in the surface water (N03 > 10 ~-tM) along a section bet­ From our review of the main upwelling systems and the ween the Galapagos Islands and the Peruvian coast near kinetics of growth characteristics, we conclude that the 15°S (Fig. 5). Chlorophyll is very low, mostly between 0.5 NW-African coastal upwelling, which is one of the best and 1 1-1g I-1, with sorne higher values near the coast. 14C known area of the world ocean through the Cineca pro­ productivity is in general below 0.5 g C m-2 d-1. These cha­ gramme, appears to be a rapidly growing, and therefore racteristics classify these waters as HNLC waters. Murray highly productive zone with high chlorophyll concentra-

154 PRODUCTIVITY IN HNLC WATERS tions as a permanent characteristic. Export to the offshore oligotrophic regime seems to occur by transport of particulate and dissolved organic matter. On the other band, in the Pacifie South American upwelling (mainly Peru), growth appears to be more controlled by grazing. During austral winter, the HNLC conditions, associated with very low productivity, allow an extension of nutrient-rich water towards the open ocean, following the general circulation pattern (Peru and South Equatorial Current). During the weak upwelling season off Peru , pro­ ductivity, as shown by many observations, also frequentl y exhibits a high chlorophyll pattern, like NW Africa. The upwelling along the equa­ torial Pacifie is the most expressive emanation of HNLC characteristics, with al most the same properties as the Costa Rica dome upwelling (Fig. 6B and Tab. 3). Global CZCS sea surface chlorophyll charts generally clearly demonstrate the different patterns between the tropical Atlantic and Pacifie Oceans (Fig. 6A). The more extensive chlorophyll, particularly off NW Africa, contrasts with less chlorophyll-produ­ cing Peruvian and equatorial zones in the Pacifie Ocean. Unfortunately, global charts often give average situations, obliterating seasonal events. . ' ' One of the greatest unsolved questions for ocea­ ----< nographers concerned with biological producti­ c_ y- vity is to know and understand the fate of nutrients transported away from Peru during ~ austral winter, and ali those nutrients upwelling along the equator. Where and how are they consumed (Minas and Minas, 1990)? Almost nothing is known about the dynamics of the tao· 120° w 60" o· nu trient utilization far from the upwelling source areas. This large-scale problem, existing since the work of Thomas (1972; 1979), will be adres­ sed by the US-J-GOFS EqPac Process Study. The most important contribution, more clearly elaborated by observation than by nutrient dyna­ rnic explanation, is due to Feldman et al. (1984) and Feldman (1986 a; 1986 b). There are blooms observed off Peru, and even far SW of the Galapagos islands. Sorne blooms have been studied already in greater detail (Bender and McPhaden, 1990). Pisias and Lyle (1988) noted, on the basis of Eastropac Atlas, that "the Costa Rica dome is the locus of the highest surface Figure 6 productivity of any open ocean region in the A) CZCS images of tropical upwelling systems (Feldman, 1989) disclose equatorial Pacifie". This demonstrates that the generally a greater development and extension of near-surface Costa Rica dome can switch from a HNLC site chlorophyll, especially off NW Africa. This fact agrees with our geographical classification of fast- ta slow-growing systems under the to a normal situation. The remaining question influence of more or less grazing pressure (see Tab . 3 and Fig. 68 ). concems the reason of such phytoplankton out­ B) Location of HNLC zones weiL developed along the equatorial Pacifie, bursts . The washout effect of the great dilution and seasonally in the Costa Rica da me and off Peru. Th e tropical during an upwelling event allows the autotrophs Atlantic displays only moderate HNLC situations, especially during the equatorial upwelling. NW Africa is showing a/most permanent/y high to outgrow their grazers. Are atmospheric iron chlorophyll situations , inputs, or simply iron availability increased by C) Global fluxes of mineral aerosol ta the ocean in mg m-2 yr-1, dilution with old oligotrophic surface waters, the according ta Duce et aL (1991). Th is chart supports great/y the iron key elements for launching these events? The limitation hypothesis, and therefore constitutes a challenge ta the "only grazing" explanation.

155 H.J. MINAS, M. MINAS

Table4 residence times in the photic zone. Great attention will have to be paid to these aspects in the future. Studies Classification of tropical upwelling systems between extreme HC and HNLC conditions. Seasonal characteristics are very important; the should focus also on the regional dynamics of the herbi­ same upwelling, like that off Peru, can belong to ali types between HC vores. Dominant grazing pressure should result from andHNLC. excess zooplankton. It is tempting to suggest that transport of zooplankton by surface circulation (Peru Current, South HC fast-growing standing stock with high chlorophyll Equatorial Current), from the coastal upwelling areas towards the equator, induces grazing pressure in the water - NW-Africa, mostly permanent situation, with upwelling along the equator. Charts of zooplankton ahun­ possible local exceptions dance (Reid, 1962; 1977) seem to support this idea. - Peru, coasta! upwelling, frequent during the weak upwelling season - SW-Mrica, coasta! upwelling, frequent during the weak upwelling season THE ANTARCTIC OCEAN - Peru, coasta! upwelling during the weak upwelling season NCP in the Antarctic HNLC waters - SW-Mrica, coasta! upwelling during the main upwelling season (Probyn, 1988) During the Antiprod 1 croise, carried out by the Médiprod - Atlantic Equatorial Upwelling (Gulf of Guinea), with Group on R.V. Marion-Dufresne at the end of austral sum­ moderate HNLC conditions during the main upwelling period (July-August-September) mer in 1977, a section was made from 40°S to 62°S in the lndian Ocean (Fig. 7). Nutrient distribution has been stu­ died along this section, and primary production has been - Peru, coasta! upwelling, HNLC situation during the measured with the 14C method at each station. Nutrients in main upwelling season (austral winter) the surface waters decrease from south to north. Nutrient - Pacifie Equatorial Upwelling with extreme HNLC consumption has been evaluated from the concentration conditions difference between the subsurface thermal minimum water - Costa Rica dome and the surface waters (Le Corre and Minas, 1983). The HNLC very low or stationary chlorophyll standing stock nutrient concentration in the temperature minimum water represents the concentration of the mixed layer and, there­ fore, the concentration of the surface and near-surface global chart of dust inputs to the ocean published by Duce waters at the end of winter. The following relationship bet­ et al. (1991) is a welcome addition to this discussion (Fig. ween nitrate and silicate consumption has been established: 6C). At first glanee, this seems, from a geographical point AN03 =0.25 ASi (OH)4- 0.55. This relationship concems of view, to provide strong support for the iron limitation only the sea surface consumption data. In order to use the hypothesis. This is true not only for the Antarctic Ocean, but also for the tropical Atlantic and Pacifie features, parti­ cularly if one considers NW Africa vs the eastern equato­ 70" E rial Pacifie and its HNLC zones. This constitutes a challen­ ge to the "grazing only hypothesis" and suggests that we need to be cautious. Even the Atlantic equatorial upwel­ • z ling, which we earlier called "moderate HNLC" might be :: ., • 27 partiy influenced by a greater iron availability. The most • • 28 recent publication (Young et al., 1991; Betzer, pers. eltOtt'Tia 5 • •... ~ : K!:JrG\t!LP 1. comm.) shows that even oligotrophic zones may respond by sporadic productivity increases to atmospheric iron inputs in the North Pacifie. lll:oiiiO 1. '4 At present, arguments in favour of "grazing" seem more convincing, mainly due to the fact that in iron-rich freshly upwelled coastal water, production can start slowly. In very ... slow growing regimes, there is evidence that high specifie uptake rates must be inferred or even directly observed (Cullen et al., 1992). In our view, the strongest argument supporting the grazing explanation is that, in a Chl vs time diagram, the whole spectrum of growth velocities cao be observed, from very fast to extremely slow (see classifica­ tion of Tab. 4). Iron limitation should not allow such a variety of intermediate status. Despite these arguments, it is clear that iron, and other metals which play such an impor­ tant role in algal physiology (Martin and Gordon, 1988; Morel, 1991), may also exercise their limitation or fertili­ Figure7 zation effects, especially during the final stage of longer Station chart of the Antiprod-1 cruise.

156 PRODUCTIVITY IN HNLC WATERS

N NCP approach and the zz model, we have also calculated 0 the integrated nutrient consumption in the water column at each station. To illustrate our calculation, we show fust, in ___ Figure 8, the thermal structure of the upper 200 rn, from ____ 50 which the depths of the temperature minimum have been determined. The nutrient content of this temperature mini- 100 mum water is remarkably constant from south to north ([N03] = 29.1 ± 0.6).The lapse of time corresponding to the nutrient consumption (delta) is roughly six months, the 150 primary productivity period in the Southem Ocean (Martin, 1990). The profiles of the âN03 at the different 200 stations are shown in Figure 9. Profiles of âP04 and âSi (OH)4 (not shown) have almost the same shape. Regression calculations allow the establishment of the fol- 250 lowing relations between the changes in the consumption of the different nutrients. 300 Figure 10 shows the relationship between the integrated m values of water column âSi03 and âN03. The best fit equa- Figure 8 tion is: âN03 =0.23 âSi03- 11.38; r =0.95 (n = 17). The Distribution of temperature along the section of Figure 7, in the upper scatter diagram in Figure 11 contains ali the individual data 300-metre layer, showing the thermal minimum (o). points, and regression calculation leads to the equation:

Figure 9

Nitrate consumption (l1N03 in !JM) profiles at the Antiprod- 1 cruise stations.l1N03 is obtained by subtractingfrom the nitrate concentration at the thermal minimum the end-of­ summer concentration observed at each depth. Water column integrated values ('1:.!!1N03 in mmol m-2) are indicatedfor each station: [!1N03 = (NOJJrmin-(NOJ)obsl·

1000 •

C'l 1 E • 'à E 1500 • ' e • • 1'1 z0 • •

0 1000 2000 3000 4000 .15103 mmol. m-2 6 ..

Figure 10 15 2 Water column integrated consumption of nitrate ('1:.!1N03 in mmol m- ) 2 vs silicate ('J:.J!Si03 in mmol m- ), see Figure 9. 6' z <1 3

2

Figure 11

All-data diagram of consumption of nitrate (!!.NO 3 in ~tM) vs con~umption t?f silicate (l!.Si03 in JtM) at stations 7 to 23 of the 0 20 Antlprod-1 CrUISe.

157 H.J. MINAS, M. MINAS

âN03 = 0.21 ASi03 + 0.18; r = 0.94 (n = 116). Integrated is similar to the value observed in the HNLC waters of the âN03 vs AP04 (diagram not shown) gives the relationship : Costa Rica dome. âN03 = 13.32 AP04-17.54;r=0.87 (n = 17). In order to obtain an overall average of the nutrient Grazing and thef-ratio problem consumption, we have integrated the whole nutrient consumption along the 1 553 km long North-South section Silicon and nitrogen analyses of particulate matter from the (stations 7 to 23). The total annual consumption below a same region of the Indian Ocean have been undertaken 1m-wide band having the same length is 594 kgmol for (Copin-Montégut and Copin-Montégut, 1978). Figure 12, nitrate, 48 kgmol for phosphate and 2,712 kgmol for silica­ as published by Le Corre and Minas (1983), shows the te. The overall average of the nutrient consumption per consumption values of silicate and nitrate along the North­ square metre is therefore: South section (deltas of the surface waters). The values of for nitrate nitrogen :I:âN-N03 = 0.380 mol m·2; particulate silicon and nitrogen are low in comparison with the consumption values of both elements. This demons­ for mineral phosphorus :I:AP-P04 0.031 mol m·2; = trates also that most of the elements assimilated by particu­ for silicate silicium :I:ASi (OH)4 = 1.750 mol m·2. late matter are removed from the water column. Particulate The average molar uptake ratios are: silicon leaves the surface waters by sedimentation of fecal :I:âNŒAP = 12.3 pellets or direct sedimentation of large diatoms. :I:âNŒASi =0.22. An intriguing aspect of the consumption results is the high ASi03/AN03 ratio. The very strong correlation would sug­ or by taking phosphorus as the reference: gest tight coupling between nitrogen assimilation and parti­ ASi/âN/AP =55.9/12.3/1. culate silicon formation, probably by Antarctic diatoms, weil The average amount of nitrate-nitrogen removed from known for their heavy skeleton. Particulate matter, on the these waters (0.380 mol. m·2) leads, according to Redfield ratios, to a nitrate based new production (NP), in terms of • carbon, equal to 2.52 mol C m·2, or 30.2 g C m·2, which • • • • • • • have been produced within the time interval from the end :Il.... 20 •• • of winter (August-September) to the time of observation, at • ~ :Il the end of summer (February-March). The time interval of :1: • • .... 9 • the removal is not easy to determine; thus we have estima­ • 5 ... éii :a ted the daily average NP using following time intervals: <3 10 • 4 "" ~ 3 éii 5 months =0.20 g C m·2 d-1 0 0 " 0 0 0 • 2 ~ o"' 0 0 0 0 0 0 0 0 6 months =0.17 g C m·2 d-1 z 0 0 1 z" <3 0 7 months 0.14 g C m·2 d-L • = 22 •23 4 The mean value of the I c uptake measurements carried 45° so• ss• 80" out at each station is 0.14 g C m·2 d-1. This represents the new production which corresponds to a 7-month interval. Figure 12 4 Besides underestimation by the 1 C method, one may argue North-South distribution of surface nitrate and silicate consumption that the period of high production may have existed during values (AN03 in fJM and t.si(OH)4 in JAM),for the Antiprod-1 cruise. the preceding time period. In fact, it is obvious that this 0 : AN03 values; .6.: â.Si(OH)4 values; ---: concentration level of new production is fairly low if one considers the luxurious particulate silicium; e : concentration of particulate nitrogen (from Le abundance of nutrients available in the waters. A recent Corre and Minas,l983). estimation of new production in the more productive mar­ ginal ice zone gives 49 g C m·2 yr·l (Smith and Nelson, other band, has a much lower Si/N ratio, with values near 2. 1990). ln comparison with oligotrophic waters of the tropi­ This observation suggests that recycled nitrogen assimilation cal ocean, our NP rate, which is practically the yearly value can make the difference. The high uptake ratio, i.e. 4.5 times for these Antarctic waters (with nearly 6 months without more silicate than nitrate, suggests that more than half of the production), is relatively higher. Martin et al.'s (1989 ) total productivity is regenerated production. This is also mean value of NP (sediment trap results in tropical Pacifie) consistent with /-ratio values deduced from 15NH4 and in the Vertex Program was 18.4 g C m·2 yr·l while our NP 15N03 uptake measurements by Oison (1980) and Glibert et in the Mediterranean Sea was 19.5 g C m·2 yr·l (Minas, al. (1982) who respectively calculatedfvalues slightly higher 1970; Minas et al., 1988). and lower than 0.5.1f we choose a photosynthetically active If we couvert the NP of carbon to equivalent amounts of period of about five months, the total production deduced chlorophyll using a C/Chl =55, we obtain a chlorophyll from the nutrient consumption study is therefore TP =2 x 0.2 production rate of 549 mg Chi m·2 yr·l. Since we have =0.4 g C m·2 d-1. This value is 2.9 times greater than the 14C summarized the total amount of chlorophyll in the area in uptake rate of 0.14 g C m·2 d-1. Simon (1986) in a similar the same way as the nutrient consumption, we found an study in a western area of the Indian Antarctic sector came to average content of 0.025 g m·2. The ratio observed vs that almost the same result. Without reopening the old 14C­ actually produced is theo 25/549 =0.045, i.e. 4.5 %. This controversy, a main argument for the Antarctic region is to

158 PRODUCTIVITY IN HNLC WATERS

imagine a scenario with the assumption of an initial producti- stock in tropical upwelled waters during their transport away ve episode during late winter-spring. Indeed, a higher N03 from the source area show that two kinds of specifie increase uptake was found by Oison (1980) and Glibert et al. (1982) rates (V) can be defined:a) the apparent V of the increasing ---during that period. Wheeler and Kokkinakis (1990) came to __ standing stock which varies from high tovery low_yalues, or ______the same conclusion for the subantarctic Pacifie. even to zero in HNLC waters; b) the actual V, which is dedu­ Our principal objective here, the application of the "zigzag ced as being high everywhere in the tropical ocean. model" to Antarctic conditions, leads to the following cal­ Grazing by herbivores appears to be the principal factor culations: on the basis of the average water column chloro­ responsible for the reduced apparent velocity. phyll content, remaining at a constant level of 25 mg Chl 2) NCP determinations should receive more attention, m-Z, for a 5-month time interval, the daily increase (or because they are the best indicator of the average past new decrease) of chlorophyll is 549/150 = 3.66 mg, !lzz is production which remains as a signature of N03 consump­ 0.0593 and Vzzi =0.15 d-1. tion in the water body. NCP determinations are comple­ According to the same method of calculation as was used mentary to other new production (NP) methods (Eppley, before and assuming aj-ratio of0.5 for Antarctic waters, the 1989). In the Pacifie HNLC waters along the equator, the fmal specifie increase rate for total production is V (TP) =0.54. application ofWyrtki's (1964) NP calculation (Chavez and This value, consistent with the grazing hypothesis, appears to Barber, 1987) depends on the ascending water fluxes, be reasonable within the low temperature regime of the which are highly variable (see Minas et al., 1990). The Southem Ocean. Eppley's formula for a temperature of 3°C weakest feature of this method is that nutrient dilution by leads to a value for V of 1 d-1. Smith and Nelson (1990) esti­ mixing with oligotrophic waters is not taken into account. mated doubling rates for Antarctic phytoplankton and found a We hope to propose soon our own NCP method for more mean doubling time of 0.3 d- 1 with several values higher than complex mixing processes near the equator. 0.5 d-1. Results of laboratory cultures of Antarctic species lead 3) An important open question concems the fate of nutrients to values of0.7 d- 1 (Raimbault, 1984 and pers. comm.). in HNLC waters, since they do not downwell as in the Despite satisfying results obtained from our NCP concept Antarctic Ocean. The CZCS data base can help to discover and model, it cannot be completely excluded that iron limi­ phytoplankton outbursts away from the upwelling source tation may be involved, especially at the end of the time area (see ali Feldman references), or within the source area, course, in the grazing scenario.lf most of the N03 assimi­ for instance the Costa Rica dome (Pisias and Lyle, 1988). lation takes place in the upper 50 rn, nearly 20 % of the ori­ Why sudden outbursts? Iron input by dust, or cessation of ginal 29 !lM N03 were consumed (= 17 % for an average grazing? We believe that short-time surface and near-surfa­ consumption of 5 !lM). According to Martin (1990), iron ce stability under daily heat input favours the departure of limitation starts at that point leaving the remaining 80 % of autotrophs, overpowering the microheterotrophs because nutrients unused.lt is possible that our low 14C-uptake esti­ more light becomes available. mations have been undertaken under such limitation condi­ 4) A principal consequence of HNLC situations is a fertili­ tions. A slightly different scenario could be imagined as zation of large-scale areas in the open ocean, because dis­ follows: since frequent measurements are lacking in this solved nutrients are transported more easily than particula­ region, sorne unobserved sporadic phytoplankton blooms te matter. may occur at an earlier period (springtime) quickly exhaus­ HNLC zones are also large COz source areas, because bio­ ting nutrients, down to the 20% limit, where iron limitation logical COz uptake favours COz escape from the upwelled begins. Such a scenario acts against the Wheeler and water to the atmosphere. In addition, COz outgassing is Kokkinakis' concept founded basically on McCarthy's accelerated by surface warming (Minas and Minas, 1990). N03 uptake repression by ammonia and refuting the iron limitation. In the subantarctic waters, total N uptake (84- 5) HNLC conditions in the coastal Peruvian upwelling pro­ 732 !lM d-1) seems to fall in the order of magnitude of our vide perhaps less food to higher trophic levels (for instan­ data. Unfortunately, there are no estimates ofN uptake on a ce, Anchoveta) than El Niiio waters, as was shown by square metre basis, and thus comparison becomes difficult. Feldman's (1986 a and b) observations. We do not have enough experience to analyse grazing 6) If both the grazing and iron hypotheses are valid in the conditions as a function of algal population, size, and gra­ Antarctic Ocean, the iron limitation starts late, when most zing capacities of micro- or macroheterotrophs (Banse, of the yearly photosynthesis period is over. 1990; 1991 a and b; Frost, 1987; 1991). We have the fee­ 7) Attention has to be paid to the origin of the excess zoo­ ling that turbulence is the greatest handicap for microalgae plankton. This excess has not to be necessary great, but intimately associated with the microheterotrophs. Near the great enough to maintain a permanent grazing pressure on a surface, stability is the best chance for the algae to win the low biomass. We assume this excess is autochthonous in the battle of auto vs heterotrophy. Antarctic Ocean, but great! y allochthonous along the Pacifie equator, especially in the area of its eastern boundaries. 8) The idea of iron fertilization of more or less greater zones CONCLUSIONS of the open ocean seems excellent to us, but any interven­ tion in the laboratory and at sea should also focus on the 1) Our Net Community Production (NCP) analysis and study heterotrophic activity and its elimination ("Killing zoo­ of the in situ development of the phytoplankton standing plankton since one cannot tell it togo on hunger-strike").

·159 H.J. MINAS, M. MINAS

HNLC waters are perhaps nothing other than waters with general CUBA Pro gram, which was under the leadership an excess of animais; the principal question is becoming : of Prof. R.T. Barber. We thank also Dr S. Weiler and Dr Wh y? J. Cullen for in vi ting one of us to attend the meeting devoted to a study of factors controlling productivity in HNLC regimes. Dr. Murray's criticism, suggestions and Acknowledgements corrections on the manuscript were extremely useful for writing the final version. Helpful discussions were held This work could not have been accomplished without with and comments received from our French colleagues the benefit of collaboration with our American col­ Drs J.-P. Béthoux, Y. Dandonneau and A. Sournia. We leagues, Drs Dugdale, Codispoti and Packard, for many are grateful to M.-C. Bonin for her assistance in prepar­ years. They invited HJM to Pacifie croises within the ing the manuscript.

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