ICES mar. Sei. Symp., 197: 215-235. 1993
Estimation of primary production by observation of changes in the mesoscale nitrate field
Hans Joachim Minas and Louis A. Codispoti
Minas, H. J. and Codispoti, L. A. 1993. Estimation of primary production by observation of changes in the mesoscale nitrate field. - ICES mar. Sei. Symp., 197: 215-235.
Measuring decreases in the nutrient concentration of water masses is a long- established method for obtaining a quantitative insight into planktonic productivity. Application of this methodology is being revitalized within the J-GOFS program. In addition to nitrate consumption, which basically represents New Production (NP), attention is focused on biologically induced changes of oxygen and C 0 2. From these changes, estimates can be made of the so-called "Net Community Production" (NCP), which is similar to NP over some time and space scales. In oceanic zones of temperate and high latitudes, NCP determinations carried out with carcful consideration given to hydrological conditions have been successfully applied to the spring bloom, which constitutes the main nutrient depletion period. Typical examples are presented from the Mediterranean Sea and the North Atlantic, Arctic, and Antarctic Oceans. In tropical upwelling systems, nutrient consumption values (-A N ) and their correspond ing time-lags (At) are determined by diagram analysis of chemical and hydrological parameters. A theoretical study of the auto-heterotrophic interactions within the planktonic community permits establishment of relationships between the "nutrient depletion” property of the water and the observed chlorophyll content. Three types of temperature-nutrient relationships can be identified as indicators of slow, normal, and high apparent nutrient uptake systems. Recognizing the usefulness of these relations for NP approaches by remote sensing leads to the following conclusion: NCP methodology should be improved in order to obtain a better insight into “in vitro incubation” rates, which in some areas still show discrepancies with NCP estimates.
Hans Joachim Minas: Centre d'Océanologie de Marseille. Campus de Luminy. Case 901, 13288 Marseille cedex 09, France. Louis A. Codispoti: Monterey Bay Aquarium Research Institute, 160 Central Ave, Pacific Grove CA 93950, USA.
Introduction the substances measured clearly took place via the respiration of the plankton (Cooper 1933; Harvey 1928). A decrease in the nitrate content by photosynthetic Cooper called it ‘net production’ ”, The term “Net uptake within the euphotic zone means “new pro Community Production” (NCP) used by one of us in a duction” (NP) according to the basic definition given by study of productivity derived from nutrient distribution Dugdale and Goering (1967). Nitrate-based NP is often fields in upwelling areas (Minas et al., 1986) has been closely related to export production, as formulated by introduced earlier under almost the same expression, Eppley and Peterson (1979) and discussed in Berger et i.e. “net community organic carbon production” (Codis al. (1989). A historical review shows that pioneers poti et al., 1982b) and "net euphotic community pro working in planktology studied the seasonal nutrient duction” (Platt et al., 1982). There is general consensus depletion in order to quantify primary production. that NCP might be similar to “new production" (Eppley, Eppley (1989), in his considerations of “new pro 1989; Platt et al., 1989) over phytoplankton bloom time duction” problems, mentions the early work done by scales. Atkins and Cooper in the years 1920 to 1930. Eppley The observed decrease in the nitrate concentration wrote: “It was recognized early that this method would during periods of moderate to rapid phytoplankton underestimate primary production since regeneration of growth, ANOj = [NO^],, — [NOs],2, during the time 216 H. J. Minas and L. A. Codispoti IC ESm ar. Sei. Symp.. 197(1993)
(Smith et a l . (1991) (Codispoti et al. (1991) Goyet & Brewer (1992)— >, Weichart (1980)
Minas (1970) Minas & Bonin (1988)
-Codispoti et al. (1982 Codispoti et a l . (1986 Whitledge et al. (1986
(Broenkow (1965 (Wyrtki (1964) PERU
Minas et al. (1986) Minas & Minas (1992)
ANTARCTIC — Simon ,inoc\ (1986) Karl et al. (1991) ^ 180* 90* \ 0* Jennings et al. (1984) Figure 1. Locations and references concerning the NCP estimates presented and discussed in this paper. interval At = tl — t2 is not significantly diminished by corresponding At values measure the residence time, regeneration of nitrogen because the regenerated form beginning with the arrival in the euphotic zone of these is NH 4 and not N O 3. Not the same is true for phosphate, ascending waters. We consider also some typical NCP but since NH 4 is continuously and immediately assimi determinations based on apparent oxygen productions lated by phytoplankton (nitrification is considered as (+A O 2) or even — 2C 0 2 consumptions, because they negligible) NH 4 does not accumulate, suggesting that mostly confirm AN-based NCP rates, and because they the same is true for phosphate, because a corresponding are formed under the same hydrological control of water amount of phosphate is assimilated together with NH4. properties, which constitutes a sine qua non for all of Over phytoplankton bloom time scales, therefore, the these NCP approaches. By "hydrological control" we concentrations of these regenerated nutrients are negli mean a simultaneous study of water masses, of their gible compared to the important amount of nutrients hydrological properties and circulation, in order to used for new production. Consequently, AP0 4 as well as make sure that the nutrient changes are not significantly ANO3 can measure new production. The same consider affected by any advection of waters with different nutri ations used for AP0 4 can be made for the oxygen ent properties. increase +A 0 2 (or the C 0 2 decrease - A 2 C 0 2), which is the result of the net balance of photosynthesis vs. respiration of the whole auto-heterotrophic community. NCP based on seasonal nutrient We evaluate two systems for NCP (Fig. 1). In mid and high latitudes the reduction of nutrients (—AN) corre consumption sponds to a time-lag (At) of from several weeks to one Mid-latitude case studies season. It starts at the end of winter, is centred on the spring bloom, and extends to the early summer period. Mediterranean Sea In low latitude areas, i.e. in subtropical and tropical We begin with NCP determinations in the Northwestern regimes, nutrient consumption and/or oxygen pro Mediterranean Sea, which constitutes an interesting duction are evaluated in upwelled water bodies, and area because of its strong winter mixing in the deep- ICES mar. Sei. Symp.. 197 (1993) Primary production and changes in the mesoscale nitrate field 217
water formation zone off the French coast. Figure 2 is a position (in Fig. 3: BL). Hydrological observations were schematic representation of the seasonal nutrient de carried out down to 300 m; measurements were also pletion during the spring bloom and the periods of made of nutrients (PO 4), oxygen (Fig. 4), and daily in transition from the preceding winter to summer con situ l4C uptake. Summer conditions showed a sub ditions. It is interesting to note that a completely mixed- surface 0 2 maximum reaching an oversaturation near water column with a deep-water concentration of about 120%. Figure 5 compares in terms of oxygen the results 8 /(M N O 3 contains a potential NP of 800 mmol N m ~ 2 of different approaches: AO2 derived from 14C uptake, yr~' (i.e. 63.6 gC m ~ 2 yr_ l) in a 100-m water column. A 0 2 derived from nutrient consumption (-APO 4), and Such a high NP can in fact only be expected in limited the observed net oxygen accumulation A 02obs, which areas, only after extremely strong winter conditions. has positive values only below the thermocline. It must The studies focused on two NCP determinations: be mentioned that the A02obs, and the —APO4 vari ations have been corrected for effects of mixing of water 1st experiment: During 1964, a year starting with mild masses, especially in the deep part of the euphotic zone winter conditions, a complete seasonal study was under (for details, see Minas, 1968,1970). As can be seen from taken on the basis of four 1 0 -day observation periods, the figure, the /-ratio (= N C P:T .P. (I4C)) is very low in March, June, September, December, at an offshore the upper warm layer where, according to the concept of
WINTER SPRING SUMMER
nutrient bloom oligotrophy
input - A N /A t
thermocline
50 m nutricline
100 m
Figure 2. Schematic presentation of the seasonal nutrient depletion and associated events, from end of winter to summer (Northwest Mediterranean situation). 1 - End of winter status of homogeneous nutrient distribution due to vertical mixing. 2 -O nset of the spring bloom nutrient depletion starting with the first temperature stratification. 3 - Discontinuities in NP by nutrient inputs produced by the deepening of the thermocline due to strong wind events, according to Klein and Coste’s (1984) model. The most favourable period of such events is the end of spring and the early summer, as long as the nutricline is associated with the thermocline. 4 - Nutrient regeneration starting below the compensation depth and occurring within the 200-m layer below the euphotic system, as can be concluded from long-term observations in the similar system of the Sargasso Sea (Jenkins and Goldman. 1985). The fraction of newly regenerated nutrients (even nitrate) returning to the euphotic zone by ascending diffusion is not well known. This fact creates ambiguities in the new vs. regenerated production definition, and discrepancies between NCP estimates and those derived from asccnding fluxes and 1?N uptake measurements. 5 - Summer situation with the nutricline finishing far below the thermocline. Conditions for NCP estimates are becoming crucial, especially at the end of summer. Results of vertical diffusion calculations are given in the text. 218 H. J. Minas and L. A. Codispoti IC E S m ar. Sei. Symp., 197(1993)
Eppley and Peterson (1979), productivity is almost ex clusively based on regenerative processes. The /-ratio for the whole euphotic water column is about 0.3 (see legend in Fig. 4). Unfortunately, at the time of the observations not enough attention was paid to the l4C uptake at the bottom of the euphotic zone during the oligotrophic summer period. Evidently, present-day problems not yet solved were largely ignored at that time 3--f (measurements at depths greater than 75 m, clean tech niques, significance of dark fixation, 24-h incubations, etc.). We agree with most of the critical arguments formulated against intercomparison of an oxygen accumulation rate and l4C uptake rate (Platter«/., 1982; Platt and Harrison, 1986), especially if sporadic data at only one discrete level are compared (Shulenberger and Reid, 1981). -T’C t-P .P O , The complete four-season study leads us to a T.P. (I4C) of 78 gC m - 2 yr" 1 and an average /-ratio of 0.25. This /-ratio is not very far from that of an entirely different approach based on a relationship between the SX. /-ratio and ambient N 0 3 concentration, i.e. / = 0.31, evaluated by Platt and Harrison ( 1986) in the northern sector of the Sargasso Sea. The latter is indeed very MARCH similar to our Mediterranean system, especially during a 300 year with moderate winter conditions.
P-PO4
03
Nice
LIGURIAN ■T*C BL o S E A '' GOLFE frontal zone . 36S—' ^ 100 ...... "•••/ "/Calvi ■P-PO , DU
— main 200 deep water LION formation zone 250 JUNE Mediprod I 300
Figure 3. Chart of the Northwest Mediterranean Sea showing Figure 4. Average profiles of hydrographic and chemical the Mediprod I station grid in the deep-water formation area. properties at an open-sea station in the Northwest Mediterra Nice-Calvi transect through the central divergence and cutting nean: Cousteau’s Bouée Laboratoire (BL in Fig. 3) between the Ligurian frontal zone twice. BL is Cousteau's Bouée Labor the Côte d'Azur and Corsica. Average values correspond to atoire at its first position in 1964, when seasonal time series two hydrocasts a day, during 10-day time series in March and were made on primary production. June. From Minas (1970). ICES mar. Sei. Symp.. 197(1993) Primary production and changes in the mesoscale nitrate field 219
-A02 +A02 mil-1 0.6 0:4 0.2 0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1fl
thermocline ____ 20 - O 30 ___ o —
50. A 0 2 (eq.from 14C)
75
A02 ( AO = -276 AP 00.
Figure 5. Results of NCP estimates and 14C-uptake measurements obtained by seasonal time series in 1964 at the Bouée- Laboratoire station (BL in Fig. 3). A 0 2ohs üne indicates the changes of observed oxygen concentrations between March and June. + A 02 line represents the net change of 0 2 calculated from the phosphate depletion (AP04). + A02 derived from l4C-uptakc data was calculated with a photosynthetic quotient PQ = 1.25. From Minas (1970).
As shown in Figure 2, nutricline formation is associ dN/dz the nitrate gradient, and Rw the ascending nitro ated with establishment of the thermocline in spring and gen flux due to vertical advection (R is the nutrient early summer. For a short time during the year, deepen concentration in the nutrient gradient below the eupho ing of the thermocline by a strong wind event produces tic zone and w is the ascending velocity). Large vari an input of nutrients in the upper shallow mixed layer. ations in the computed fluxes seem due to uncertainties The model of Klein and Coste (1984) applied to such a in Kv: Kv = 104 m - 2 s -1 (Platt et al., 1982) and Kv = situation leads to a NP rate which has been somewhat 3.7 • 10 5 m ~2 s-1 (Lewis et al., 1986). Applied to the overemphasized and generalized in discussions concern P 0 4 gradient (=3.6 /itnol m~4) during the lowest sum ing the productivity controversy in the Sargasso Sea mer productivity (September), the highest Kv leads to (Jenkins and Goldman, 1985; Duce, 1986). In the Medi 31.2,amol mT2 d_ l, equivalent to 0.5 mmol m ~ 2 d -1 in terranean, the nutricline is located in summer far below terms of NO 3. This value is not too far from the 0.69 the thermocline, and wind storms, rare during summer mmol m - 2 d~' for the North Pacific gyre (Platt et al., months, cannot significantly induce NP enhancements 1982). The lowest Kv leads to 0.13 mmol m~ 2 d~' (N 0 3), (Minas etal., 1988). A new modelling effort also leads to which is practically the value given by Lewis etal. (1986) this conclusion for the Sargasso Sea (Bigg et al., 1989). for the extremely and permanently oligotrophic con Other mechanisms, such as internal waves, may play a ditions at the low latitude station in the tropical Atlantic. role at the bottom of the euphotic zone (McGowan and The NCP evaluation for the lowest productivity in Sep Hayward, 1978). tember is, on the basis of the average summer/-ratio of The most critical period of the AN evaluation occurs 0.5 (Minas, 1970), about 55 mg C m ~ 2 d” 1, which during the summer two-layer system, from which dy represents 0.69 mmol N m ~ 2 d "1, and corresponds to a namic aspects and their complex influence on the phyto flux calculated with the highest Kv value. In fact, the plankton physiology have been discussed by Goldman average NCP for the summer season (June to Sep (1988). In the 1964 experiment, the investigators con tember) is 90 mgC m ~ 2 d “ 1, i.e. 1.13 mmol m 2 d ~ l, tinued the AN vs. A 0 2 and PP ( 14C) study through the which is a high value. Interestingly, this is the latest summer period, from June to September (results are not value calculated for the upward transport for nitrate in given here). It is interesting to compare these results the Sargasso Sea (Sarmiento et al.. 1990). It is fun to with those based on vertical diffusion calculations. Cal establish and to compare all these different fluxes from culations for oligotrophic subtropical gyres gave a large the literature. We believe that the principle of the crude range of N 0 3 flux data, as shown by Duce (1986), who evaluation from nearly 30 years ago is still useful and can calculates, according to a flux equation already pro be improved by the application of modern methods such posed by McCarthy and Carpenter (1983), F = Kv • dN/ as the nanomethods for nitrate and ammonia determi dz + Rw ■ Kv is the vertical eddy diffusion coefficient, nations published recently (Raimbault et al., 1990 and 220 H. J. Minas and L. A. Codispoti 1CES mar. Sei. Symp.. 197 (1993) references therein; Jones, 1991). However, a good gration both times, and the nutrient depletion has been knowledge of the uncertainties involved in using these compared to the average results of 14C uptake measure methods to evaluate oligotrophic productivity is still ments performed at each station. The deduced/-ratio = lacking. 0.72 (Coste et al., 1972; Jacques, 1988) can no longer be Our conclusion from this first experiment is that the accepted, because the nutrient consumption was NCP results for the oligotrophic summer season are strongly overestimated. This was the consequence of an relatively high. The high/-ratio in the deeper part of the invasion of nutrient-poor surface waters into the area of euphotic zone can probably be interpreted as a failing of the grid during the time interval. As explained in the the 14C method under the circumstances of its appli revision (Minas and Bonin, 1988), the invasion of these cation at the time of our study. waters from the periphery of the deep-water formation zone is due to downwelling (spreading) of the high- 2nd experiment: A second NCP determination (Minas density water after the cooling period (Médoc Group, and Bonin, 1988) is in fact a revision of an earlier NCP 1970). Minas and Bonin therefore undertook a second and /-ratio evaluation during the spring bloom experi NCP evaluation on the “Médiprod F’ data, on the Nice- ment carried out in the Northwest Mediterranean Sea Calvi section between Côte d’Azur and Corsica, where during the “Médiprod I” cruise in 1969. The deep-water not such a massive invasion took place. In addition, the formation area was covered by a station grid carried out strategy was changed by using the diagram analysis twice (March-April) with a time interval of one month utilized in upwelling studies, as we shall see later (Minas (Fig. 3). The phosphate inventory of this area (16,000 et al., 1982b, 1986). The principle of this analysis is to km2) in the 1 0 0 -m upper layer was calculated by inte- determine, from a mixing line between two water masses (A and B), the biological variations (AN or A 02) rep resented by the deviation from the line (Fig. 6 ). In the /N case of oxygen, the A 0 2obs is the sum of photosynthetic and atmospheric oxygen (A0 2biO + A0 2atm) when the sea surface is undersaturated. The biological fraction of oxygen is calculated from the nutrient consumption according to the model of Redfield et al. (1963) after correcting for air-sea exchange of oxygen and for water mixing (Broenkow, 1965). Water masses involved in the mixing are the Levantine Intermediate Water (LIW) . / Û0 2obs = A 02 bio + Û 0 2 atm and the Winter Surface Water (WSW). The innovation in this investigation is that the diagram analysis is ap plied to the two situations (March-April); therefore the nutrient consumption is in fact the difference, i.e. the increase in two states of nutrient consumption, at the /N beginning and at the end of the one-month interval. The NO. results of the two AN distributions expressed as + A0 2biO along the transect are shown in Figure 7 (A and C). The first distribution, A (March), displays the active frontal zones which are well known for increased productivity during winter (Prieur, 1981; Estrada and Margalef, -ß NO 1988; Minas and Minas, 1989; Sournia et al., 1990). The second one, C (April), shows the effect of the spring bloom depletion invading the central area. To illustrate the atmospheric input of oxygen to be greatest in the most undersaturated area, we show the distribution of A 0 2atm in Figure 7B (March). Taking the difference of Figure 6. Schematic illustration of diagram analysis of con the two AN states avoids interferences from nutrient servative (salinity) vs. non-conservative parameters (0 2 or nutrient). The biological nitrate consumption is measured consumption effects of preceding years, especially at taking the vertical distance from the data point to the theoreti greater depths of the section near the coastal zones. The cal mixing line for a given salinity. The observed A02obs overall consumption (increase in consumption) calcu represents the sum of the biological increment A 02W„ and of lated by integration over the whole transect represents a the atmospheric increment A 02;llm under undersaturated sea- NCP of 0.247 gC m - 2 d~'. The general value of T.P. surface conditions. In the case of a three-component mixing system, the data points can fall outside the conservative mixing ( 14C) is 0.685 gC irT 2 d -1, i.e. the average of 0.387 gC triangle, as shown by Minas et al. (1991). m “ 2 d _l (March) and 0.982 gC m ~ 2 d -1 (April). The/- ICES mar. Sei. Symp.. 197(1993) Primary production and changes in the mesoscale nitrate field 221
NICE CALVI 44 43 42 41 40 39 38 37 36
200- .
10 -
30 -
5 0 -
75-
1 0 0 -
150-
200 -
250-
Figure 7. NCP study in the Northwest Mediterranean. A shows the distribution of the + A 02hio fraction along the Nice-Calvi transect during Mediprod 1 (first leg, in March). +A 02bio is calculated from the nutrient consumption (-A P 0 4). The diagram analysis method illustrates the higher productivity in the frontal zones. B shows the atmospheric oxygen A 02atm input in March when the whole area is undersaturated, especially the central area. The knowledge of A 02atm is an interesting “by-product” of the diagram method. C shows the + A 0 2bio distribution in April (second leg). In this case the diagram method demonstrates clearly the high spring bloom activity in the central divergence area, where the nutrients were mixed up into the euphotic zone. From Minas and Bonin (1988). 222 H. J. Minas and L. A. Codispoti ICES mar. Sei. Symp.. 197 (1993) ratio is / = 0.247/0.685 = 0.36. The relatively low value distribution of incubation experiments and a reawaken is believed to be due to the activity of zooplankton, ing of interest in estimating new production from the which are already present during winter in the frontal distribution of chemical variables.” The Arctic as a sink zone (Boucher et al., 1987; Minas and Bonin, 1988). region has been analysed by Walsh (1989) and polar phytoplankton physiology by Sakshaug (1989) and North Sea Smith and Sakshaug (1990). An interesting NCP deter mination has been made along a ~300-km-long transect An interesting mid-latitude study in the northern North near 78°30’N between Spitzbergen and Greenland. The Sea (Fladen Ground) describes nutrient depletion first and last transects were made on 10-12 April and 15- associated with the SC 0 2 decrease in a spring bloom 17 May, corresponding to a time interval of ~35 days experiment carried out from 8 April to 4 May in 1976 (Codispoti et al., 1991; Smith et al., 1991). From the (Weichart, 1980). Atomic ratios calculated from the removal of nitrate within the upper 150 m a NP of —40 regression lines of the nutrient concentrations measured gC m “ 2 has been calculated, giving 1.2 gC m ~ 2 d _1, with 10 m below the sea surface are AC:AN:ASi.AP = C:N (by atoms) = 6 .6 . The integration of AN extended 120:19:9:1. Phosphate consumption (A P04) agrees well to a 150-m depth, but, surprisingly, nutrient depletion with the NCP deduced from the XC0 2 change, i.e. 1.9 seems to reach greater depths. Considering our Mediter gC m “ 2 d”1, corresponding to the bloom observed ranean experience, we argue that perhaps some change during 12 days (19 April to 1 May). SCO? changes were in the watermass properties may be possible through calculated from the change of pH and alkalinity determi advection; but, according to Codispoti et al. (1991), the nations. It must be mentioned that alkalinity remained average temporal change in N 0 3 (integrated between 0 constant, as observed by Goyet and Brewer (1992), in and 150 m) for all stations in their study area (from Strait the North Atlantic Experiment. There was no correction between 78°30' and 80°N) with nitrate profiles to 150 m for C 0 2 exchange with the atmosphere (C 0 2 invasion) leads to virtually the same productivity figures. Com which, in the experiment that we describe below, was parison with l4C uptake measurements (mean of 25 very low. determinations is 2.1 gC irT 2 d“ 1) leads to a /-ratio of 0.57. Curiously, Smith et al. (1991) indicate 15N uptake North Atlantic rates of 48 mmol N m 'z d _1, which surpass the 15 mmol During NABE (North Atlantic Spring Bloom Experi N itT 2 d " 1 representing 1.2 gC m ~ 2 d“ \ deriving from ment), Goyet and Brewer (1992 and personal communi the N 0 3 depletion calculation. Codispoti et al. (1991) cation) reported SC 0 2 and p C 0 2 decreases near 47°N observed that during this spring bloom, silicon was 20°W. They compared progressive evolution of the almost not taken up, since the bloom was dominated by 2 C 0 2 profile from 25 April to 31 May 1989 to the initial Phaeocystis, a phytoplankton species that does not re end of winter 1 C 0 2 concentration in the mixed layer. quire dissolved silicon. Most profiles of silicon main This initial concentration was observed at 300 m during tained almost a winter pattern with respect to N 0 3 the time of their observations. Since there is no change profiles showing nitrate utilization. in the alkalinity, the 2 C 0 2 change represents biological Another interesting high-latitude productivity study uptake, i.e. NCP may be calculated directly in terms of based on 2 C 0 2 change and nutrient distributions arose carbon. The calculated correction due to CO? invasion from the PROBES (Processes and Resources of the from the atmosphere (surface water pC0 2 is always Bering Sea Shelf) experiment. Codispoti et al. (1982b) under 350 /
6
5
5 =L, 4 n O •a
3 • tm
2
1
0 10 20
A S i 0 3 jjM
Figure 8. Plot of ANO^ vs. ASiOi for the Antarctic north-south transect carried out during Antiprod I. From Minas and Minas (1992). ICES mar. Sei. Symp.. 197 (1993) Primary production and changes in the mesoscale nitrate field 225
O2 ~ 1 0 0 % >.1 0 0 % 0 2 = 1 0 0 % < 1 0 0 % I heat
warm cold -coast high production-*
OLIGO - AN 20 LN
60 euphotic regeneration / zone mainly NH4+ 80
1 0 0
150
Figure 9. Coastal upwelling circulation pattern and associated physical, chemical, and biological processes. Cold and high nutrient (HN) source water freshly upwelled, moving offshore and losing its nutrients through the main high productivity area. Regenerated nutrients (mainly ammonia) are mostly returned to the euphotic zone by the ascending water flux. Close to the coast, atmospheric oxygen invades the undersaturated area; further offshore, oxygen escapes from the sea into the atmosphere. In tropical areas, an important heat input increases the sea-surface temperature in the cold near coastal zone.
iron hypothesis for Antarctic waters. According to Mar can give reasonably good /-ratios, without having to tin, after winter mixing iron is available for the first measure absolute nitrogen assimilation rates. nearly 2 0 % of the nutrients and then becomes limiting; this suggestion would be consistent with extremely low uptake rates measured at the end of the Antarctic light Low latitude systems period (Slawyk, 1979; Jacques and Minas, 1981; and other papers cited previously for low instantaneous Methodology uptake rates). Thermal stability in the tropical ocean is only interrup The mean atomic ratios of the preceding open Antarc ted by ascending currents in coastal upwelling areas or in tic Ocean area nutrient depletion estimates are open-ocean divergences, such as along the equator or in ASi:AN:AP = 55.9:12.3:1. They show a high ASi:AN the cyclonic eddies associated with domes. A simple ratio of 4.55, similar to that deduced from correlation schematic representation of a biogeochemical structure plots in Figure 8 . In our opinion, not enough attention and circulation pattern under steady-state conditions of has been given to this high ratio as an indicator of new vs. coastal upwelling is given in Figure 9. Nutrient consump regenerated production. Since particulate silicon experi tion (—AN) estimates are relatively easy to obtain but ences little redissolution in the euphotic zone, regener estimating corresponding time-frames (At) is more diffi ated nitrogen production takes up “new”, i.e. “non cult because there is no way to evaluate it directly. regenerated” silicon, as does new nitrogen production. Current speeds and directions of water bodies moving The Si:N atomic ratio in particulate matter in this area is, away from the upwelling centres are extremely complex according to Copin-Montégut and Copin-Montégut because of the existence of meanders, gyres, filaments, (1978), approximately 2/1, i.e. nearly half as great as the etc., as shown by remote sensing. To deduce At from uptake ratio (Le Corre and Minas, 1983). This fact current speeds becomes extremely difficult. To over confirms a /-ratio near 0.5, as shown by earlier I5N- come the difficulty one can use the indirect way of uptake studies (Olson. 1980; Glibert et al., 1982). This residence time determination proposed by Bowden shows that instantaneous l5N incubation uptake rates (1977) in a heat budget study of the Northwest African 226 H. J. Minas and L. A. Codispoti ICES mar. Sei. Sym p.. 197 (1993)
264
263
0 m Dune Point 15 - st. 207 - 262
260 14 - O C m
St. 204 116 m 13 259
163 m
104 m
12- 35.11 source water 23Cm O 11 .8 °C
10-1
Y. i______i______i______I______'______i------1------>------*------1— .80 .90 35.00 .10 .20 .30
Figure 10. T-S plot from the Southwest Africa upwelling region. Deviation of the data from the SACW (South Atlantic Central Water) mixing line has allowed us to determine the net heat input and the residence time of the upwelled water, according to the model of Bowden (1977). From Minas et al. (1986). ICES mar. Sei. Symp.. 197 (1993) Primary production and changes in the mesoscale nitrate field 227 coastal upwelling. Residence time At, i.e. the time The advantage of this time determination is that the elapsed from the arising of water in the surface layer, is nature of analysis does not change, i.e. diagram analysis. deduced from the net heat gain occurring while the The details of this methodology and the results are given water is moving offshore. According to Bowden (1977), in Minas et al. (1982b, 1986). In Figure 11 we present a the heat increase is determined by T-S diagram analysis 0 2-S scatter plot of the data for an entire upwelling in which the temperature increase is indicated by the cruise. We chose in this rather complex diagram a low- departure from the mixing line. As an example, we show wind period corresponding to a simple upwelling circu in Figure 10 the T-S diagram of the Southwest African lation, with very low atmospheric oxygen input. upwelling near21°S. The procedure is the same as that of Detailed discussions concerning air-sea exchanges of the nutrient-salinity and 0 2-salinity diagrams (Fig. 6 ). oxygen with regard to the biological oxygen flux are
max. biol. ” v4 envelope B
a envelope A
CO 100% sat. (16' CM 100% sat. (19'
ro
O 1 i LU O >- X o »*■ 4 » Sd =36,10
0 35.20 35.60 3600 36.40 36.80 SALINITY
Figure 11. 0 2-S scatter plot of all data from an entire upwelling cruise off Northwest Africa. Envelope A corresponds to a low wind-speed period when atmospheric oxygen input (A02.„m) becomes negligible in relation to the great amount of biological oxygen produced. The theoretical mixing line connects the upwelling source water point (Sd = 36.1, [0 2]j = 3.40) with the point representing the warm offshore water (S„ = 36.6, [ 0 2] = 5.21) saturated in oxygen. The general treatment required for the diagram analysts is carried out as explained in Figure 6. From Minas et al. (1982b). 228 H. J. Minas and L. A. Codispoti ICES mar. Sei. Symp.. 197 (1993) presented in earlier publications (Minas et al., 1982a, normal to the upwelling coastlines. The average time 1986). (At) has been obtained in the same way by dividing the general heat input by the daily net heat gain, which is a characteristic of each upwelling area. Very different Results NCP rates were found (Minas et al., 1986): 2.5 gC m ~2 As an example, we present in Figure 12 the profiles of d_l (Northwest Africa), 1.1 gC i t T 2 d _l (Southwest AN and A 0 2obs 'n the Northwest African upwelling off Africa), 0.59 gC i t T 2 d“' (Peru), 0.14 gC m “ 2 d “ 1 Cape Corveiro (CINECA-V cruise of the RV “Jean (Costa Rica Dome). Charcot” ; for data see Groupe Médiprod, 1976). The NCP analysis displays different growth kinetics in Although the profiles are similar to instantaneous pro different upwelling areas. Figure 13 allows us to com duction profiles, they are actually different, because pare the rate of increase of the autotrophic standing they are cumulative curves of the consumption property stocks (2Chlobs m 2) off Northwest Africa and off Peru. or of the net accumulation of oxygen. In addition, the Referring to Walsh (1976) and Voituriez et al. (1982), shape of the profiles is influenced also by the mixing of Minas et al. (1986) explained the slow increase off Peru the waters during their transport offshore. Results from in relation to Northwest Africa by grazing, but since the several upwelling systems in the tropical Atlantic and iron limitation hypothesis arose, Minas and Minas Pacific have been studied. In order to obtain average (1992) have tried to demonstrate the grazing hypothesis values of NCP from different upwelling systems, nutri with the help of a simple model (zig-zag model), which ent consumption (-AN ) has been integrated for sections they presented in detail. The latter is inspired by day-
UJ ■L
30
30
40 -
Figure 12. A 02 and ANtota| (ANOs + ANH4) profiles at several stations off Northwest Africa (Cape Corveiro-Cape Blanc area). Stations with alow + A 0 2 and - AN inventory are coastal stations in the freshly upwelled source water. The A values arc calculatcd from a diagram analysis, as shown by Figure 6. From Minas et al. (1982b). ICES mar. Sei. Symp.. 197 (1993) Primary production and changes in the mesoscale nitrate field 229 night rhythms of planktonic activities observed in time compared to the V for the observed standing stock series: Le Bouteiller and Herbland (1982) for chloro increase (2Chlobs). The final result of the model appli phyll, Oudot (1989) for C 0 2 and 0 2, Weichart (1980) cation is that the daily specific growth rate off Peru is in for C 0 2 and nutrients. The model is based on an in fact high (1.05 d “ 1) and not much lower than the daily V terpretation of a diagram (Fig. 13) which compares off Northwest Africa (V = 1.5 d_I). In the typical increasing chlorophyll standing stocks from different HNLC waters of the Costa Rica Dome, V is as high as off upwelling zones (2Chlobs curves) as published by Minas Peru (0.98 d ^ 1). These data confirm the “fairly high et al. (1986). In the same diagram are the 2ChINCp specific growth rates” from experimental results pub curves which represent the cumulative chlorophyll pro lished recently by Cullen et al. (1992) for HNLC con duction calculated from the nutrient consumption. ditions observed almost permanently along the equa Increased kinetics are very different in the different torial Pacific. In addition, these authors conclude from upwelling systems. For instance, the Costa Rica Dome direct in situ observations that “diel variability of beam upwelling (with typical HNLC conditions) displays no attenuation also indicated high specific growth rates and increase of chlorophyll, but this does not mean that a strong coupling of production with the grazing. It there is no chlorophyll production (see the difference appears that grazing is the proximate control on the between SChlNCP(CRD) and 2Chlobs(CRD)). On the standing crop of phytoplankton”. In a recent study, contrary, off Northwest Africa, 2Chlobs increases very Minas and Minas (1992) also confirm the “grazing” quickly. explanation for a more moderate but existing HNLC In the model, daily exponential growth curves are situation in the equatorial Atlantic upwelling in the Gulf constructed in such a way that they satisfy geometrically of Guinea, which has been studied in full detail by the cumulative SChlNCP curve. This allows calculation Voituriez et al. (1982), especially in relation to zoo of the daily specific increase rate (V) and enables it to be plankton activities. In some way,/-ratio estimates seem
\M\ NW AFRICA
Ref PERU
250 NCP NCP CRD .OBS OBS
■ 200 NCP
150
100
50 HNLC
CRD OBS
0 10 20 30 4050 60 70 80
Time days
Figure 13. Time course of the observed standing crop (2Chlobs curves) off Peru and off Northwest Africa (respective equations arc: 2Chlobs = 16.11 x io" 0I54T and 2Chlobs = 26.3 x io,l 0867T). Corresponding 2ChlNCp curves (equations: SChlNCP = 29.79 x jq0.0I98T an[j v q 1incp = 47 23 x 10" 111121 ) represent the increase of total chlorophyll production deduced from the nutrient consumption. The much slower evolution of the Peru curves displays HNLC tendencies of this upwelling system during the time of the observations. From Minas et al. (1986) and Minas and Minas (1992). 230 H. J. Minas and L. A. Codispoti ICES mar. Sei. Symp., 197 (1993)
to be linked to the more or less heterotrophic activities in 26.3)1 1672 for Northwest Africa. These equations are the different tropical upwelling systems: almost linear relationships, sm c zp V p l is nearly equal to 1. In the model for a HNLC paper (Minas and Minas, /-ratio 1992), several equations were given in order to test the Northwest Africa 0.64 (Minas et al., 1986) effect of different values of grazing and specific growth Southwest Africa 0 .2 (P robyn,1988) rates. If we take the equations given in the case of Peru 0 .2 (Minas et al., 1986) exponentially increasing grazing, i.e. Y obs = 1Q0.301T and Costa Rica Dome 0.5 (Minas et al., 1986, re- Y ncp = Y obs x 10° 30,T + 10 x io° 30'(t-2) _ 5> where y evaluation and confirm = 2Chl, the relationship independent of T becomes ing earlier results of SChlNCp = 1.5 2Chlobs — 5. Only when grazing remains Wyrtki (1964) and constant does the relationship become non-linear; for Broenkow (1965)) instance, when Gr = 9, Yobs = 9 + 1 0°-3<)1T and Y NCP = (Murray etal., 1989) Pacific equator 0.1 to 0.3 9(T-1) + 10" 30IT, the relation is 2ChlNCP = 2Chlobs + Pacific equator 0.17 (Dugdale et al., 1992) 29.9 log (2Chlobs — 9). Since 2ChlNCP represents the Atlantic equator 0.3 (Minas and Minas, integrated nutrient consumption (see legend in Fig. 13), 1992) the relationships given above may be useful for new production approaches from satellite-derived chloro The low value off Peru applies to the observed situ phyll data, especially when relationships between sea ation as described in Minas et al. (1986). Mainly during surface chlorophyll and water column contents in the weaker upwelling season off Peru, high chlorophyll chlorophyll can be established (Eppley et al., 1985; concentrations are normally observed and high /-ratios Sathyendranath and Platt, 1989). Minas et al. (1982a, b) resulting from lsN-uptake measurements are found in were able to calculate such a linear regression between the literature. In a review of nutrient regimes in different surface chlorophyll data and the biological oxygen pro upwelling systems, Codispoti et al. (1982a) indicate duction deduced from diagram analysis: values in a range of 0.52 to 0.78. Ten years ago, upwell
ing systems, especially coastal systems, were considered Chi a (jug r ') = 2.59 A0 2 (ml T 1) + 0.36; r = 0.73 as normally associated with high/-ratios (Eppley et al., 1979). Probyn (1988) was the first to show HNLC Nutrient-temperature relationships tendencies associated with low/-ratios obtained by 15N measurements in the coastal upwelling system off South Attention has already been drawn to nutrient- west Africa. temperature relationships in remote-sensing studies of Possible interferences from possible iron limitation upwelling areas (Traganza et al., 1983; Dugdale et al., displayed by global charts of atmospheric dust and iron 1989). inputs in the ocean (Duce et al., 1991; and others) have In a NCP study of HNLC waters, Minas et al. (1986) been discussed in a recent analysis reviewing HNLC and Minas and Minas (1992) distinguished between conditions (Minas and Minas, 1992). three types of nutrient relationships (Fig. 14). Accord ing to the theoretical diagram shown in A, there can be a straight line relation between the nutrient properties New production and remote sensing and temperature, even with nutrient uptake. This is because, due to the heat input in cold upwelled waters, NCP production relationships temperature is strongly non-conservative. In order to A major objective at the present time is to estimate maintain a straight line, the temperature increase must primary production (T.P.) from surface chlorophyll dis be compensated by nutrient uptake, which apparently tribution available by CZCS (Coastal Zone Color Scan occurs in the data of Figure 14C. If all the conditions ner) imagery, and advances have been accomplished in necessary to establish a heat budget for a given tropical recent years (Platt et al., 1991 and references therein; upwelling area are known, nutrient fluxes can be calcu Morel and André, 1991 and references therein). A more lated from the diagram properties. When the nutrient crucial problem is to introduce NP approaches (Platt and uptake surpasses temperature increase, data points in Sathyendranath, 1988; Dugdale et al., 1989; Sathyen- the diagram fall below the straight line (Fig. 14B). The dranath et al., 1991). From equations given in Figure 13 contrary takes place when the nutrient uptake is low in for XChlNCp and 2Chlobs, can be derived the relation regard to warming of the water. This type of diagram ship SChlNCP = IC hloNCp(XChlohs/2Chloobs)"1/,"2; tak seems well associated with HNLC conditions, as de ing the values of n and SChlo, the relations for the two scribed for the Costa Rica Dome (Fig. 14D). upwellings become SChlNCP = 29.79 (2Chlobs/ Sea-surface nitrate-temperature relationships have 16.11)' 2857 for Peru and SChlNCP = 47.23 (2Chlobs/ already been successfully applied in new production ICES mar. Sei. Symp., 197 (1993) Primary production and changes in the mesoscale nitrate field 231 © 17
rich HN LC »AT ^
[N] O z intermediate status •y* * * or.;’: . depleted •%?:
cold w arm 15 20 T*C
20
2.5 5 2.0
1.0
0.5 0.5
0 15 16 17 18 19 20 14 16 18 20 22 24 26 T‘C T°C
Figure 14. Temperature-nutrient diagrams. The schematic diagram (A) displays three possible features of a temperature- nutrient diagram. 1 - Curvilinear scattering of the data points below the line AB; existing when the nutrient uptake occurs fast in accordance with the warming of the water. Example: B represents a fast-growing phytoplankton system off Peru. 2 - A straight line relationship exists when the nutrient uptake is compensated by the increase of temperature: shown as an example is the NOj-T diagram of the equatorial upwelling, according to Voituriez and Flerbland (1984). 3 - The data points are above the AB line, indicating very slow uptake rates, under HNLC conditions. Example: D, average data points of the Costa Rica dome upwelling. From Minas and Minas (1992).
approaches and modelling (Dugdale et al., 1989; Sath duction (even with NH4). In strong oligotrophic areas, yendranath et al., 1991; Morin et al., 1993). We believe or during oligotrophic summer periods, these contri that such relationships combined with the above- butions may not be negligible (Duce, 1986; Loÿe-Pilot et mentioned chlorophyll-nutrient consumption equation al., 1990). In eutrophic systems, the atmospheric signa may help to introduce new aspects for remote-sensing ture cannot be detected in the water body by normal approaches to new production. With the patchiness of NCP methodology, but corrections can be made when one single upwelling system, areas of fast and/or slow the input is known. Atmospheric enrichments have HNLC-like increasing standing stocks may be detected. received much attention since iron has been considered as a limiting factor in HNLC waters (Duce and Tindale, 1991). Enhanced primary production detected by fre Atmospheric nutrient inputs and new production quent l4C measurements has been attributed to iron Atmospheric inputs obviously contribute to new pro (Young et al., 1991). 232 H. J. Minas and L. A. Codispoti ICES mar. Sei. Symp.. 197 (1993)
Conclusions (At), since the water upwelled into the euphotic zone. Complementary isotopic methods of water-age esti 1. Nitrate depletion evaluations (—AN03) lead to New mates should help to determine At in the future, perhaps Production (NP) estimates when the corresponding time more precisely . scale (At) is known. On phytoplankton bloom time 6 . NCP rates suggest that herbivore grazing appears scales, and when NCP is calculated for the euphotic to be the most important factor limiting the increase of zone, this NP approximates also the so-called "Net phytoplankton in several upwelling systems, particularly Community Production” (NCP), which more generally in tropical HNLC waters. can also be calculated from the change of phosphate 7. Relationships between observed chlorophyll (-APO 4), oxygen (+A 02), and total C 0 2 (—AXC02). inventory per square metre (2Chlobs m 2) and the status Numerous nitrate-based NP determinations with the of nutrient depletion (—SAN m~2) can be established l5N method have been carried out in various oceanic for upwelling zones; together with different types of provinces but simultaneous comparisons of NCP vs. temperature-nutrient relationships they may help NP 15N-NP are extremely rare and possible discrepancies approaches by remote sensing. cannot be judged. Future work should focus on such 8 . Success of NCP determinations requires the ability comparisons. to define the general hydrodynamic conditions and pre 2. In temperate and high latitude areas all examples cise chemical descriptions of the waters under investi of NCP determinations concern spring bloom events. In gation. the Mediterranean Sea, two different NCP determi 9. Regenerated production according to the classical nations and their comparison with 14C-uptake rates lead definition is based on regeneration processes limited to to comparable/-ratios for the spring bloom ( f = 0.3 and the euphotic zone. In all NCP determination definitions, 0.36). The depletion evaluation procedure becomes ambiguities arise because of an active return of recently questionable towards and during the oligotrophic sum generated nutrients from below into the euphotic zone. mer conditions, but we concluded that the method is still This return occurs by diffusive vertical transport or by applicable, especially in areas with important winter direct ascending advection in upwelling systems. “New” nutrient enrichment. vs. “regenerated” terminology should be revised by 3. A review of NCP determinations in the literature attempting to distinguish the subphotic fraction of re shows that most of them belong to high latitude systems. cently recycled nitrogen (even as nitrate) able to fuel Simultaneous —AXC02 and —ANO^-based NCP rates actual regenerated production. This last point will be seem to imply extremely high C:N assimilation ratios important in new production considerations dealing (Codispoti et al., 1986; Karl et al., 1991 ; Sambrotto et al., with oceanic carbon sink systems of atmospheric C 0 2. 1993); therefore high /-ratios ( / a 1) may lead to more justified “underestimation” declarations concerning the 14C method. The authors produce the argument of unmeasured production of dissolved organic carbon. Acknowledgements Sambrotto et al. (1993, and personal communication) We thank Dr Dugdale for his critical comments and underline this important point in a statistical way on the suggestions. One of us (HJM) had the opportunity to basis of more recent data. discuss C 0 2 problems with Catherine Goyet (Woods 4. The Antarctic open-sea NCP estimates display Hole) who allowed us to present results that are in press. much lower rates than those of the high latitudes in the Marie-Claude Bonin's technical assistance in preparing northern hemisphere. A handicap is the lack of obser the manuscript has been greatly appreciated. This re vations describing Antarctic end of winter and early view was done within the context of French J-GOFS spring situations. Our open-ocean NCP rates drastically programs supported by CNRS contracts: URA-41, exceed 14C-uptake rates measured at the end of the GDR P4, FRONTAL and. with respect to the Mediter yearly productivity period. In addition to the failing of ranean results. EROS 2000/CEE. L. A. Codispoti the incubation methods, other arguments may be pro received support from the Office of Naval Research, the duced: iron (if the iron hypothesis holds), which is Monterey Bay Aquarium Research Institute, and from available after winter mixing, may start to become the National Science Foundation. limiting at the end of the productivity period; an enhanced grazing pressure may also keep productivity at a very low level during the time of our observations. 5. In tropical upwelling systems nutrient depletion References (—AN) is evaluated by diagram analysis, and heat bud Banse, K. 1974. On the interpretation of data for the carbon-to- get studies allow an indirect determination of the corre nitrogen ratio of phytoplankton. Limnol. Oceanogr., 19: sponding time-frame which represents residence time 695-699. ICES mar. Sd. Symp.. 197 (1993) Primary production and changes in the mesoscale nitrate field 233
Berger, W. H., Smetacek, V. S., and Wefer, G. (eds) 1989. problems, pp. 85-97. In Productivity of the ocean: present Productivity of the ocean: Present and past. John Wiley, New and past. Ed. by W. H. Berger, V. S. Smetacek, and G. York. 471 pp. Wefer. John Wiley, New York. 471 pp. Bigg, G. R., Jickells. T. D., Knap, A. H., and Sherriff-Dow, R. Eppley, R. W., and Peterson, B. J. 1979. Particulate organic 1989. The significance of short-term wind-induced mixing matter flux and planktonic new production in the deep events for “new” primary production in sub-tropical gyres. ocean. Nature, 282: 677-680. Oceanol. Acta, 12: 437^142. Eppley, R. W., Renger, E. H., and Harrison, W. G. 1979. Boucher, J., Ibanez, F., and Prieur, L. 1987. Daily and Nitrate and phytoplankton production in southern California seasonal variations in the spatial distribution of zooplankton coastal waters. Limnol. Oceanogr., 24: 483^194. populations in relation to the physical structure in the Eppley, R. W., Stewart, E., Abbott, M. R., and Heyman, U. Ligurian Sea front. J. mar. Res., 45: 133-173. 1985. Estimating ocean primary production from satellite Bowden, K. F. 1977. Heat budget considerations in the study of chlorophyll. Introduction to regional differences and stat upwelling, pp. 277-290. In A voyage of discovery. Ed. by M. istics for the Southern California Bight. J. Plankt. Res., 7: Angel. Pergamon Press, Oxford. 696 pp. 57-70. Broenkow, W. W. 1965. The distribution of nutrients in the Estrada, M., and Margalef, R. 1988. Supply of nutrients to the Costa Rica Dome in the eastern tropical Pacific Ocean. Mediterranean photic zone along a persistent front, pp. 133— Limnol. Oceanogr., 10: 40-52. 142. In Océanographie pélagique méditerranéenne. Ed. by Codispoti, L. A ., Dugdale, R. C., and Minas, H. J. 1982a. A H. J. Minas and P. Nival. Oceanol. Acta, No. SP9. 250 pp. comparison of the nutrient regimes off Northwest Africa, Glibert, P. M., Biggs, D. C., and McCarthy, J. J. 1982. Peru, and Baja California. Rapp. P.-v. Rcun. Cons. int. Utilization of ammonium and nitrate during austral summer Explor. Mer, 180: 184-201. in the Scotia Sea. Deep-Sea Res., 29: 837-850. Codispoti, L. A., Friederich, G. E., and Hood. D. W. 1986. Goldman, J. C. 1988. Spatial and temporal discontinuities of Variability in the inorganic carbon system over the south biological processes in pelagic surface waters, pp. 273-296. eastern Bering Sea shelf during spring 1980 and spring- In Toward a theory on biological-physical interactions in the summer 1981. Cont. Shelf Res., 5: 133-160. world ocean. Ed. by B. J. Rothschild. Kluwer. Codispoti, L. A., Friederich, G. E., Iverson, R. L., and Hood Goyet, C., and Brewer, P. G. 1992. Seasonal carbon fluxes D. W. 1982b. Temporal changes in the inorganic carbon within the upper layers of the ocean. ASLO Aquatic Sciences system of the southeastern Bering Sea during spring 1980. Meeting, Santa Fe, New Mexico, 9-14 Feb. 1992. Nature, 296: 242-245. Groupe Médiprod 1976. Résultats de la campagne CINECA 5 - Codispoti, L. A., Friederich, G. E., Sakamoto, C. M., and Jean Charcot - Capricorne 7403 (1er mars au 20 avril 1974). Gordon, L. I. 1991. Nutrient cycling and primary production Publ. CNEXO, Résultats des campagnes à la mer, 10. in the marine systems of the Arctic and Antarctic. J. mar. Holm-Hansen, O., and Mitchell, B. G. 1991. Spatial and Sys.,2: 359-384. temporal distribution of phytoplankton and primary pro Copin-Montégut, C., and Copin-Montégut, G. 1978. The duction in the western Bransfield Strait region, pp. 961-980. chemistry of particulate matter from the South Indian and In RACER: Research on Antarctic Coastal Ecosystem Antarctic oceans. Deep-Sea Res., 25: 911-931. Rates. Ed. by D. M. Karl. Deep-Sea Res., 38 (8/9). Coste, B., Gostan, J., and Minas, H. J. 1972. Influence des Jacques, G. 1988. Flux de carbone en milieu péiagique de conditions hivernales sur les productions phyto- et zooplanc- Méditerranée occidentale lors de la floraison printanière, toniques en Méditerranée nord-occidentale. I. Structures pp. 143-148. In Océanographie pélagique méditerranéenne. hydrologiques et distribution des sels nutritifs. Mar. Biol., Ed. by H. J. Minas and P. Nival. Oceanol. Acta, No. SP 9. 16: 320-348. 250 pp. Cullen, J. J., Lewis, M. R., Davis, C. O., and Barber, R. T. Jacques, G., and Minas, M. 1981. Production primaire dans le 1992. Photosynthetic characteristics and estimated growth secteur indien de l’Océan Antarctique en fin d’été. Oceanol. rates indicate grazing is the proximate control of primary Acta, 4: 33—41. production in the Equatorial Pacific. J. Geophys. Res., 97 Jenkins, W. J., and Goldman, J. C. 1985. Seasonal oxygen (Cl): 663-668. cycling and primary production in the Sargasso Sea. J. mar. Duce, R. A. 1986. The impact of atmospheric nitrogen, phos Res., 43: 465^191. phorus, and iron species on marine biological productivity, Jennings, J. C. Jr., Gordon, L. I., and Nelson, D. M. 1984. pp. 497-530. In The role of sea-air exchange in geochemical Nutrient depletion indicates high primary productivity in the cycling. Ed. by P. Buat-Ménard. D. Reidel, Dordrecht. Weddell Sea. Nature, 309: 51-54. Duce, R. A., and Tindale, N. W. 1991. Atmospheric transport Jones, R. D. 1991. An improved fluorescence method for the of iron and its deposition in the ocean. Limnol. Oceanogr., determination of nanomolar concentrations of ammonium in 36: 1715-1726. natural waters. Limnol. Oceanogr., 36: 814-819. Duce, R. A., and others. 1991. The atmospheric input of trace Karl, D. M. 1991. RACER: Research on Antarctic Coastal species to the world ocean. Global biogeochem. Cycles, 5: Ecosystem Rates. Preface. Deep-Sea Res., 38 (8/9): v-vii. 193-259. Karl, D. M., Tilbrook, B. D., and Tien, G. 1991. Seasonal Dugdale, R. C., and Goering, J. J. 1967. Uptake of new and coupling of organic matter production and particle flux in the regenerated forms of nitrogen in primary productivity. Lim western Bransfield Strait, Antarctica. Deep-Sea Res., 38 nol. Oceanogr., 12: 196-206. (8/9): 1097-1126. Dugdale, R. C., Morel, A., Bricaud, A., and Wilkerson, F. P. Klein, P., and Coste, B. 1984. Effects of wind-stress variability 1989. Modeling new production in upwelling centers: case on nutrient transport into the mixed layer. Deep-Sea Res., study of modeling new production from remotely sensed 31: 21-37. temperature and color. J. Geophys. Res., 94: 18119-18132. Le Bouteiller, A., and Herbland. A. 1982. Diel variation of Dugdale, R. C., Wilkerson, F. P., Barber, R. T., and Chavez, chlorophyll a as evidence from a 13-day station in the equa F. P. 1992. Estimating new production in the equatorial torial Atlantic Ocean. Oceanol. Acta, 5: 433-441. Pacific Ocean at 150°W. J. Geophys. Res.. 97 (Cl): 681-686. Le Corre, P., and Minas, H. J. 1983. Distribution et évolution Eppley, R. W. 1989. New production: History, methods, des éléments nutritifs dans le secteur indien de l’océan 234 H. J. Minas and L. A. Codispoti ICES mar. Sei. Symp.. 197 (1993)
Antarctique en fin de période estivale. Oceanol. Acta, 6: Murray, J. W., Downs, J. N., Strom, S., Wei, C.-L, and 365-381. Jannasch, H. W. 1989. Nutrient assimilation, export pro Lewis, M. R.. Harrison, W. G., Oakey, N. S., Hebert, D., and duction and 234Th scavenging in the eastern equatorial Platt, T. 1986. Vertical nitrate fluxes in the oligotrophic Pacific. Deep-Sea Res., 36: 1471-1489. ocean. Science, 234: 870-873. Olson, R. J. 1980. Nitrate and ammonium uptake in Antarctic Loÿc-Pilot, M. D., Martin, J. M., and Morclli, J. 1990. Atmos waters. Limnol.Oceanogr., 25: 1064-1074. pheric input of inorganic nitrogen to the Western Mediterra Oudot, C. 1989. 0 2 and CO 2 balances approach for estimating nean. Biogeochemistry, 9: 117-134. biological production in the mixed layer of the tropical Martin, J. H. 1990. Glacial-interglacial CO: change: the iron Atlantic Ocean (Guinea Dome area). J. mar. Res., 47: 385- hypothesis. Paleoccanography, 5: 1-13. 409. McCarthy, J. J., and Carpenter, E. J. 1983. Nitrogen cycling in Platt, T., Caverhill, C., and Sathyendranath, S. 1991. Basin- near-surface waters of the open ocean, pp. 487-512. In scale estimates of oceanic primary production by remote Nitrogen in the marine environment. Ed. by E. J. Carpenter sensing: the North Atlantic. J. Geophys. Res., 96 (C8): and D. G. Capone. Academic Press, New York, 900 pp. 15147-15159. McGowan, J. A., and Hayward, T. L. 1978. Mixing and Platt, T., and Harrison, W. G. 1986. Reconciliation of carbon oceanic productivity. Deep-Sea Res., 25: 771-793. and oxygen fluxes in the upper ocean. Deep-Sea Res., 33: Médoc Group. 1970. Observation of formation of Deep Water 273-276. in the Mediterranean Sea, 1969. Nature, 227: 1037-1040. Platt, T., Harrison, W. G., Lewis, M. R., Li, W. K. W., Minas, H. J. 1968. Recherches sur la production organique Sathyendranath, S., Smith, R. E., and Vezina, A. F. 1989. primaire dans le bassin méditerranéen nord-occidental. Biological production of the oceans: the case for a consensus. Rapports avec les phénomènes hydrologiques. Thèse Doct. Mar. Ecol. Prog. Ser., 52: 77-88. ès Sei.. Univ. Aix-Marseillc. 250 pp. Platt, T., Lewis, M., and Gcider, R. 1982. Thermodynamics of Minas, H . J . 1970. La distribution de l’oxygène en relation avec the pelagic ecosystem: elementary closure conditions for la production primaire en Méditerranée nord-occidentale. biological production in the open ocean, pp. 49-84. In Flows Mar. Biol.,7: 181-204. of energy and materials in marine ecosystems. Theory and Minas, H. J., and Bonin, M. C. 1988. Oxygénation physique et practice. Ed. by M. J. R. Fasham. Plenum Press. New York. biologique de la Méditerranée nord-occidentale en hiver et 733 pp. au printemps. Oceanol. Acta, No. SP 9: 123-132. Platt, T., and Sathyendranath, S. 1988. Oceanic primary pro Minas, H. J., Codispoti, L. A., and Dugdale, R. C. 1982a. duction: estimation by remote sensing at local and regional Nutrients and primary production in the upwelling region off scales. Science, 241: 1613-1620. Northwest Africa. Rapp. P.-v. Réun. Cons. int. Explor. Prieur, L. 1981. Hétérogénéité spatio-temporelle dans le bassin M er, 180: 148-183. liguro-provençal. Rapp. Comm. int. Mer Médit., 27: 177— Minas, H. J., Coste, B., Le Corre, P., Minas, M., and Raim- 179. bault, P. 1991. Biological and geochemical signatures associ Probyn, T.A. 1988. Nitrogen utilization by phytoplankton in ated with the water circulation through the Strait of Gibraltar the Namibian upwelling region during an austral spring. and in the western Alboran Sea. J. Geophys. Res., 96 (C5): Deep-Sea Res., 35: 1387-1404. 8755-8771. Raimbault, P., Slawyk, G., Coste, B., and Fry, F. 1990. Minas, H. J., and Minas, M. 1989. Primary production in the Feasibility of using an automated colorimetric procedure for Gulf of Lions with considerations to the Rhone River inputs, the determination of seawater nitrate in the 0 to 100 nM pp. 112-125. In EROS 2000. W ater Pollution Research range: examples from field and culture. Mar. Biol., 104: 347- Report 13. Ed. by J. M. Martin and H. Barth. CEE - MST 351. Paris. 453 pp. Redfield, A. C., Ketchum, B. H., and Richards, F. A. 1963. Minas, H. J., and Minas, M. 1992. Net community production The influence of organisms on the composition of sea water, in “High Nutrient-Low Chlorophyll” waters of the Tropical pp. 26-77. In The sea. ideas and observations on progress in and Antarctic oceans: grazing vs iron hypothesis. Oceanol. the study of the seas. Vol. 2. Ed. by M. N. Hill. Interscience, Acta, 15: 145-162. New York. 554 pp. Minas, H. J., Minas, M., Coste. B., Gostan, J.. Nival. P., and Sakshaug, E. 1989. The physiological ecology of polar phyto Bonin, M. C. 1988. Production de base et de recyclage; une plankton, pp. 61-89. In Proceedings of the sixth conference revue de la problématique en Méditerranée nord- of the Comité arctique international. Ed. by L. Rey and V. occidentale, pp. 155-162. In Océanographie pélagique médi Alexander. E. J. Brill. Leiden. terranéenne. Ed. by H. J. Minas and P. Nival. Oceanol. Acta Sambrotto, R. N., Savidge, G., Robinson, C., Boyd, P., No. SP 9. 250 pp. Takahashi, T., Karl, D. M., Langdon, C., Chipman, D., Minas, H. J., Minas, M., and Packard, T. T. 1986. Productivity M arra, J., and Codispoti, L. 1993. Elevated consumption of in upwelling areas deduced from hydrographic and chemical carbon relative to nitrogen in the surface ocean. Nature, 363: fields. Limnol. Oceanogr., 31: 1182-1206. 248-250. Minas, H. J., Packard, T. T., Minas, M., and Coste, B. 1982b. Sarmiento, J. L., Thiele, G., Key, R. M., and Moore, W. S. An analysis of the production regeneration system in the 1990. Oxygen and nitrate new production and remineraliza coastal upwelling area off N.W. Africa based on oxygen, tion in the North Atlantic subtropical gyre. J. Geophys. Res., nitrate and ammonium distribution. J. mar. Res., 40: 615— 95 (CIO): 18303-18315. 641. Sathyendranath, S., and Platt T. 1989. Remote sensing of Morel. A., and André, J. M. 1991. Pigment distribution and ocean chlorophyll: consequences of nonuniform pigment primary production in the western Mediterranean as derived profile. Appl. Optics, 28: 490-495. and modeled from Coastal Zone Color Scanner obser Sathyendranath, S., Platt, T., Horne, E. P. W., Harrison, vations. J. Geophys. Res., 96 (C7): 12685-12698. W. G., Ulloa, W. G., Outerbridge, R., and Hoepffner, N. Morin, P., Wafar, M. V. M., and Le Corre, P. 1993. Estimation 1991. Estimation of new production in the ocean by com of nitrate flux in a tidal front from satellite-derived tempera pound remote sensing. Nature, 353: 129-133. ture data. J. Geophys. Res., 98(C3): 4689^1695. Shulenberger, E., and Reid, J. L. 1981. The Pacific shallow ICES mar. Sei. Symp., 197 (1993) Primary production and changes in the mesoscale nitrate field 235
oxygen maximum, deep chlorophyll maximum, and primary Voituriez, B., and Herbland, A. 1984. Signification de la productivity reconsidered. Deep-Sea Res,, 28: 901-919, relation nitrate/température dans l’upwclling équatorial du Simon, V. 1986. Le système assimilation-régénération des sels golfe de Guinée. Oceanol. Acta, 7: 169-174. nutritifs dans les eaux superficielles de l’océan austral. Mar. Voituriez, B., Herbland, A., and Le Borgne, R. 1982. L’up- Biol., 92: 431-442. welling équatorial de l’Atlantiquc Est pendant l’Expérience Slawyk, G. 1979. L1C and l5N uptake by phytoplankton in the Météorologique Mondiale (PEMG). Oceanol. Acta, 5: 301— Antarctic upwelling area: results from the Antiprod I cruise 314. in the Indian Ocean sector. Austr. J. mar. Freshw. Res., 30: Walsh, J. J. 1976. Herbivory as a factor in patterns of nutrient 413-448. utilization in the sea. Limnol. Oceanogr., 21: 1-13. Smith, W. O. Jr., Codispoti, L. A., Nelson, D .M ., Manley, T., Walsh, J. J. 1989, Arctic carbon sinks: present and future. Buskey, E. J., Niebauer, H. J., and Cota, G. F. 1991. Global biogeochem. Cycles, 3: 393^111. Importance of Phaeocystis blooms in the high-latitude ocean Wcichart, G. 1980. Chemical changes and primary production carbon cycle. Nature, 352: 514-516. in the Fladen Ground area (North Sea) during the first phase Smith, W. O. Jr., and Sakshaug, E. 1990. Polar phytoplankton, of a spring phytoplankton bloom. "Meteor" Forsch-Ergebn., pp. 477-525. In Polar oceanography, Part B: Chemistry, 22 (A): 79-86. biology, and geology. Academic Press, New York. Whitledge, T. E., Reeburgh, W. S., and Walsh, J. J. 1986. Sournia, A., Brylinski, J. M., Dallot, S., Le Corre, P., Leveau, Seasonal inorganic nitrogen distributions and dynamics in M., Prieur, L., and Frogct, C. 1990. Fronts hydrologiques au the southeastern Bering Sea. Cont. Shelf Res., 5: 109-132. large des côtes françaises: Les sites-ateliers du programme Wyrtki, K. 1964. Upwelling in the Costa Rica Dome. Fish. Frontal. Oceanol. Acta, 13: 413^438. Bull., 63: 355-372. Traganza, E. D., Silva, V. M., Austin, D. M., Hansson, W. L., Young, R. W., Carder, K. L., Betzer, P. R., Costello, D. K., and Bronsink, S.H. 1983. Nutrient mapping and recurrence Duce, R. A., DiTullio, G. R., Tindale, N. W., Laws, E. A., of coastal upwelling centers by satellite remote sensing: its Ucmatsu, M., Merril, J. T., and Feely, R. A. 1991. Atmos implication to primary production and the sediment record, pheric iron inputs and primary productivity: phytoplankton pp. 61-83. In Coastal upwelling. Its sediment record. Part A. responses in the North Pacific. Global biogeochem. Cycles, Ed. by E. Suess and J. Thicde. Plenum Press, New York. 5: 119-134.