Silicon limitation of biogenic silica production in the Equatorial Pacific

Deep-Sea Research I 48 (2001) 639}660

Silicon limitation of biogenic silica productionin the Equatorial Paci"c

A. Leynaert!,*, P. TreH guer!, Christiane Lancelot", Martine Rodier#

!Laboratoire **Flux de matie% re et re&ponses du vivant++, Institut Universitaire Europe&en de la Mer,TechnopoL le Brest-Iroise. Place N. Copernic, 29 280 Plouzane, France

"Groupe de Microbiologie des Milieux Aquatiques, Campus de la Plaine, CP 221, Boulevard du Triomphe,1050 Bruxelles, Belgium

#Institut de Recherche pour le De& veloppement, Station Marine d'Endoume, Chemin de la batterie des lions,13007 Marseille, France

Received 4 August 1999; received in revised form 14 February 2000; accepted 6 March 2000

Abstract

During the EBENE cruise (November 1996), distributions of biogenic silica concentration and productionrates were investigated in the surface waters of the equatorial Paci"c (1803W, from 83S to 83N), withparticular emphasis on the limitation of the biogenic silica production by ambient silicic acid concentrations.Integrated over the depth of the euphotic layer, concentrations of biogenic silica and production rates weremaximum at the Equator (8.0 and 2.6 mmol m~2 d~1) and decreased more or less symmetrically polewards.Contribution of diatoms to the new production was estimated indirectly, comparing biogenic silica produc-tion rates and available data of new and export production in the same area. This comparison shows thatnew production in the equatorial area could mostly be sustained by diatoms, accounting for the major part ofthe exported #ux of organic carbon. Kinetics experiments of silicic acid enrichment were performed. Halfsaturation constants were 1.57 lM at 33S and 2.42 lm at the Equator close to the ambient concentrations.The corresponding <

.!9values for Si uptake were 0.028 h~1 at 33S and 0.052 h~1 at the equator.

Experiments also show that in situ rates were restricted to 13}78% of<.!9

, depending on ambient silicic acidconcentrations. This work provides the "rst direct evidence that the rate of Si uptake by diatom populationsof the equatorial Paci"c is limited by the ambient concentration of silicic acid. However, such Si limitationmight not be su$cient in itself to explain the low diatom growth rates observed, and additional limitation issuggested. One hypothesis that is consistent with the results of Fe limitation studies is that Fe and Silimitations may interact, rather than just being a mutually exclusive explanation for the HNLC character ofthe system. ( 2000 Elsevier Science Ltd. All rights reserved.

Keywords: Silicon cycle; Diatoms; Limiting factor; Equatorial Paci"c

*Corresponding author. Tel.: 33-2-98-49-86-57; fax: 33-98-49-86-95.E-mail address: [email protected] (A. Leynaert).

0967-0637/01/$ - see front matter ( 2000 Elsevier Science Ltd. All rights reserved.PII: S 0 9 6 7 - 0 6 3 7 ( 0 0 ) 0 0 0 4 4 - 3

1. Introduction

The carbon biologically "xed in the surface layer and exported to the deep sea (the biologicalpump of CO2) is one of the major factors controlling CO2 partial pressure in the atmosphere(Sarmiento and Siegenthaler, 1992). Accurate determination of this #ux and of its controllingfactors are therefore critically important for understanding global carbon cycling and itsresponse to climate change. It has been estimated that about half of the export #ux of organiccarbon to the deep ocean is synthesized by diatoms (Nelson et al., 1995). Consequently, it isessential to consider the factors in#uencing the relative contribution of diatoms to total primaryand export production, to better understand the processes that determine the e$ciency of thebiological pump.

Most studies of biogenic silica production reported to date have emphasized areas of known orpresumed high primary productivity, relatively high diatom abundance, and active accumulationof diatomaceous sediments. The equatorial Paci"c is one of the main areas for opal sedimentaccumulation from which few measurements of silica production from overlying waters are yetavailable.

The central equatorial Paci"c is known as a `high nutrient low chlorophylla (HNLC) region. Ifphytoplankton biomass and production rates remain low, diatoms have been implicated to play animportant role (Chavez et al., 1990). Among other factors that have been put forth to unravel theprocesses that maintain the relatively constant HNLC conditions, grazing pressure and ironlimitation have been argued (Coale et al., 1996a; Landry et al., 1997), but neither has provensu$cient in itself to explain the characteristics of HNLC regions (Price et al., 1994).

Recently, Ku et al. (1995) suggested the availability of `newa silicic acid as a limiting factorcontrolling production in the upper equatorial Paci"c. This hypothesis, based upon studies ofnutrient budgets and 228Ra distributions, received support from Dugdale et al. (1995) andDugdale and Wilkerson (1998), who also showed from a simple silicon-cycle model that silicic acidwould play a key role in the regulation of new production in the equatorial Paci"c upwelling.However, no direct experimental evidence of silicic acid limitation has yet ever been obtained inthis area.

As part of a more global investigation of biogenic silica concentration and production rates, thispaper reports the "rst experimental evidence of silicic acid limitation of diatom silica production inthe equatorial Paci"c. Experiments were conducted during the IRD (ex-ORSTOM) EBENE cruise(1996) in the equatorial Paci"c, as part of the French contribution to the international JGOFSprogram. It was in continuity with the FLUPAC cruise (1994). Since data on the silica cycle werealso collected along the equator (between 1703E and 1553W) during FLUPAC, we will frequentlyrefer to the FLUPAC cruise in this paper.

2. Methods

Experiments were conducted during the EBENE cruise, in the equatorial Paci"c (Octo-ber}November 1996), aboard the French R.V. Atalante. The cruise plan consisted of one transectalong the date line, from 83S to 83N, with a station at each degree and two time-series stations, at33S and at the Equator.

640 A. Leynaert et al. / Deep-Sea Research I 48 (2001) 639}660

Chemical measurements (nitrate, nitrite, ammonium, phosphate and silicic acid) were carried outby standard automated colorimetric methods (Strickland and Parsons, 1972). Data sets andanalytical details are reported in Le Borgne et al. (1998).

2.1. Biogenic silica concentration

Biogenic silica (BSi) was determined on particulate matter collected by "ltration of 2 l of seawater through 0.6 lm polycarbonate membrane "lter. The "lter was folded in quarters, placed ina petri dish, dried at 603C for 12 h and stored at ambient temperature. Later analysis wasperformed using the alkaline digestion method (Paasche, 1973) modi"ed by Ragueneau andTreH guer (1994). The blank was 6 nmol l~1 (SD"3 nmol l~1).

2.2. Biogenic silica production rates

Biogenic silica production rates (PBSi) were measured at six depths in the euphotic zone.Incubations were generally conducted under simulated in situ conditions, except at the time seriesstations, where incubations were performed in situ from dawn to dusk (total duration of about12 h), using a drifting array, and followed by deck incubations for the night, to complete the 24 h.The general procedure was the following: 250 ml samples, in polycarbonate bottles, were spikedwith 50 000 dpm (830 Bq) of 32Si tracer (52 000 Bq/lg Si, Los Alamos National Laboratory). At theend of the incubation period (24 h), each sample was gently vacuum-"ltered through a 0.6 lmpolycarbonate membrane "lter (Nuclepore) and rinsed with 10 ml of "ltered seawater. The "lterwas then immediately placed in the bottom of a 20 ml plastic vial. 2 ml of 2.9 M HF was added todissolve biogenic silica. The reaction was complete after 30 minutes, and 10 ml of scintillationcocktail (Ultima Gold XR) was then added to each vial. After shaking, samples were counted ona Tri-carb 1500 TR instrument (Packard) for 60 minutes, or when a counting precision of 0.5% wasachieved for cpm in each counting window. An equilibrated 32Si solution and 32P standards wereused to deconvolve the energy spectra, as described in Leynaert et al. (1996). The biogenic silicaproduction rate (PBSi, in nmol l~1 h~1) is the fraction between the initially dissolved 32Si activityadded to the sample, and the 32Si taken up by phytoplankton and counted on the "lter at the end ofthe incubation, divided by the incubation time.

To control for the non-biological uptake of 32Si, sodium azide and HgCl2 have been usedessentially on seawater samples from turbid environments (North Sea and Black Sea coastalwaters). Evidence of adsorption has never been observed, "nal counts being always at thebackground level. However, because of the extremely high cost of the radionucleide 32Si, thesecontrol experiments are not run each time.

The speci"c production rate (<, time~1) is the molar ratio of the biogenic silica production rateto the initial biogenic silica standing stock. < represents a minimum estimate of the speci"cproduction rate by living cells, due to the presence of non-living biogenic silica (empty frustules,shell fragments, etc.).

The growth rate (k) is the rate of increase of a cell substance per unit of that cell substance(Eppley, 1972; Schlegel, 1987). In mathematical terms:

k"1N

]dNd¹

, (1.1)

A. Leynaert et al. / Deep-Sea Research I 48 (2001) 639}660 641

which upon integration becomes

k"ln N!ln N0t

, (1.2)

N could be any cellular constituent (carbon, chlorophyll, biogenic silica, cells number, etc.). In ourcase, N and N0 denote the biogenic silica at time t0 and at time t, respectively. The biogenic silica attime t is predicted from the initial biogenic silica concentration and the uptake rate. However, atsteady state, <"k (Eppley, 1972; Schlegel, 1987).

The mean doubling time (t$) is de"ned as the time required for the cellular component to increase

by a factor 2. The relationship between t$

and k is derived from Eq. (1.2):

t$"

ln 2k .

Its reciprocal, the number of doublings per unit of time (1/t$), is also commonly used.

When comparing the growth rate and the cell division rate, one must bear in mind that mass percell is not necessarily constant and can change during growth. However, at steady state, a doublingof biomass is accompanied by a doubling of all other measurable constituents of the population.

2.3. Si-limitation experiments

The concentration dependence of diatom silicic acid uptake rates was investigated at 33S and atthe Equator by conducting 32Si tracer kinetic experiments at di!erent silicic acid concentrations.For each kinetic experiment, a set of 10 (at 33S) or eight (at the Equator) 250 ml sub-samples werepoured into polycarbonate incubation bottles and enriched with Si(OH)4 , at concentrationsranging from 0 to 10 lM above ambient. A 50 ml subsample was collected for nutrient analysis andimmediately processed. Then 200000 dpm (3300 Bq) of 32Si tracer (52 000 Bq/lg Si) at 33S, or125 000 dpm (2100 Bq) at the Equator, was added to each bottle. Incubations were conducted atsunrise for 6 h, at full light and under in situ simulated conditions. After incubation, samples wereprocessed as described above for biogenic silica production experiments.

Additional experiments on silicic acid limitation were conducted at two depths (surface and chla maximum) at each station, according to Glibert and McCarthy (1984) and Brzezinski et al. (1997).Basically, these experiments compare 32Si incubation performed at ambient concentration withthose enriched to 10 lM Si(OH)4 . Considering the K

4of 1 lM reported for eastern tropical Paci"c

diatoms (Thomas and Dodson, 1975) and assuming that silicic acid uptake obeys the Michaelis-Menten equation, more than 90% of <

.!9is reached at 10 lM Si(OH)4 enrichments (10 times

the K4). The ratio between in situ and enriched samples gives an indication of the degree to which

silicic acid uptake by phytoplankton is limited by ambient silicic acid concentrations.

3. Results

3.1. Climatic regime during EBENE, in October}November 1996

The climate system of the equatorial Paci"c is subject to intermittent variabilities that lead tolarge sea surface temperature anomalies. Oscillations between unusually warm (El Nin8 o) and cold


Fig. 1. TAO (Tropical Atmosphere Ocean) monthly mean sea surface temperature (3C) and winds (m s~1), andtemperature anomalies of the studied area (printed from http://www.pmel.noaa.gov/tao-bin/tao/cover), in November1994 (FLUPAC cruise) and in November 1996 (EBENE cruise).

(La Nin8 a) conditions have now been well documented. Along the Equator, in November 1996,EBENE took place during a `neutral scenarioa between El Nin8 o and La Nin8 a, as shown by the plotof sea surface temperature anomalies (Fig. 1). The cruise track crossed the Equator at 1803W.Although fairly to the west, the tongue of cool upwelled water was still perceptible at that longitude(sea surface temperature was close to 28.53C).

3.2. Nutrient distributions

Fig. 2 shows section plots of silicic acid and inorganic nitrogen (nitrate#nitrite#ammonium)concentrations along the transect in the upper 400 m, from 83S to 83N. Silicic acid concentrations


Fig. 2. Vertical nutrient distributions: (a) N505!-

in lmol l~1, (b) Si(OH)4

in lmol l~1, (c) Si/N505!-

molar ratio, from 83S to83N, at 1803W.


Fig. 3. Vertical section of biogenic silica concentrations (nmol-Si l~1) along 1803W (negative latitudes are south).

were relatively constant at the surface, ranging from 1.0 to 2.3 lM. Inorganic nitrogen concentra-tions were more variable, ranging from complete depletion to 3.5 lM. Contours shoal inresponse to strong vertical advection in the equatorial upwelling zone. They decrease polewardsat the surface. In the water column, silicic acid and nitrate concentrations increased sharply belowthe 0.1% light depth (150 m) to reach about 25 and 32 lM, respectively, at 400 m. The lack ofcoupling between nitrate and silicic acid regeneration is evidenced by the vertical distribution of theSi/N molar ratio, considering the value of 1 as typical for diatom growth requirement (Fig. 2c).Values slightly below, but close to 1, are observed in the surface upwelled waters at the equator,whereas the ratio decreases to values lower than 0.5 at the base of the euphotic zone (150 m).At the surface, the ratio increases polewards dramatically to values exceeding 50, resulting fromnitrate depletion.

3.3. Biogenic silica distribution across the Equator (83S}83N) along the date line

Biogenic silica concentrations were very low (7}80 nmol l~1) all along the transect (Fig. 3). Themaximum was encountered at the Equator. A two-fold increase of the concentrations was observedin the euphotic zone for stations of the equatorial area (13S}13N), as compared to stationspolewards. Vertical distribution of biogenic silica evidenced a maximum at the surface, and often inthe subsurface, close to the nitracline, for stations outside the direct in#uence of the upwelling(south of 13S and north of 13N). A slight maximum in biogenic silica concentration was also noticedaround 300 m depth (Fig. 3).

During the long-term stations at the equator and at 33S, vertical pro"les of BSi were obtainedduring three successive days. Integrated in the euphotic layer (150 m), BSi concentrations were 6.9,7.4 and 9.5 mmol m~2 at the Equator and 3.4, 4.8, and 3.7 mmol m~2, at 33S, giving averages of 8.0($1.4) and 4.0 ($0.7) mmol m~2. No noticeable variations can be evidenced during the timecourse of each station, as the maximum standard deviation between the successive experiments(1.4 mmol m~2) is close to the detection limit.


Fig. 4. Time course of biogenic silica production (nmol-Si l~1) determined from surface water in situ incubations of 6, 12and 24 h, in triplicate, (a) at the Equator, and (b) at 33S.

3.4. Biogenic silica production rates

Time course experiments of silicic acid uptake were conducted for 24 h at two stations (33S andthe Equator). Sub-samples were taken after 6, 12 and 24 h incubation, and the silicic acid uptakewas measured. Results (Fig. 4) clearly show that silicic acid uptake did not proceed at the same rateduring day and night. A signi"cant decrease of Si uptake of about 30% was observed during thedark period for both investigated communities. Although we cannot rule out a possible bottleartifact, these results suggest some energy dependence of Si uptake by diatoms. Accordingly,samples collected at 0.1% light depth did not show any Si uptake. Other studies have reported(Brzezinski and Nelson, 1989; Nelson and Brzezinski, 1997) little evidence of systematic day/nightdi!erences among pro"les of the biogenic silica speci"c production rates for natural phytoplanktonpopulation. However diel periodicity in Si uptake was observed by Goering et al. (1973), with


Fig. 5. Vertical section of biogenic silica production rates (PBSi, in nmol-Si l~1 h~1), along 1803W (negative latitudes aresouth).

Fig. 6. Latitudinal (from 83S to 73N) pro"le of daily biogenic silica production, integrated in the photic layer(mmol m~2 d~1), along 1803W.

maximum rates occurring at noon. It implies that diatom speci"c uptake rate derived fromshort-term incubations might be over-estimated or under-estimated, depending on whether theincubation has been conducted around noon or not.

Daily rates of biogenic silica production (Fig. 5) in surface waters were generally very low,ranging from less than 0.2 to about 36 nmol l~1 d~1. Vertical pro"les of biogenic silica productionshow maximum rates in surface or subsurface waters, and a general decrease with depth.

Integrated in the upper layer, daily rates of biogenic silica production (Fig. 6) were maximal atthe Equator (2.58$0.40 mmol m~2 d~1) and decreased more or less symmetrically polewards, to0.3 mmol m~2 d~1 at 73N and less than 0.1 mmol m~2 d~1 at 83S. During the long-term station at


Fig. 7. Biogenic silica biomass (lmol l~1) and production (nmol l~1 h~1) pro"les performed during three successive daysat the equator (03S, 1803W).

the Equator, biogenic silica production measurements, carried out during three successive days,showed little daily #uctuation (Fig. 7). When integrated in the euphotic layer, they varied from 2.14to 2.91 and 2.70 mmol m~2 d~1, suggesting steady state.

It is interesting to note that there is one order of magnitude di!erence between the productionrate of surface waters at the Equator and the most northern and southern stations, whereas there isonly a two-fold increase in biogenic silica concentrations. As a result, diatom communities at theequator are characterized by signi"cantly higher speci"c production rates (<, d~1). Indeed, theaverage daily rates in surface waters are 0.43 ($0.23) d~1 for stations in the equatorial band(13N}13S), and 0.21 ($0.21) d~1 for stations polewards. In the same way, the mean estimateddoubling time of the silica biomass (t

$) varied from 2.4 ($1.1) days to 6.2 ($5.6) days in the two

areas de"ned above.The vertical pro"les of < (not shown) generally paralleled those of PBSi, displaying a sharp

decrease with depth in the upper 100 m and very low values below. The speci"c production rate (<),when averaged over the euphotic layer, varied by one order of magnitude during the whole cruise:from 0.03 to 0.29 d~1. In the area between 13N and 13S, < averaged 0.24 d~1, consistent withtypical values reported for coastal upwelling (0.3 d~1 o! Baja California, Nelson and Goering,1978). The mean for stations situated polewards was 0.13 d~1, exceeding mean speci"c productionrates reported for HNLC polar waters (generally below 0.1 d~1, Nelson and Smith, 1986, 1991;Banahan and Goering, 1986), but in the same range as values reported for oligotrophic mid-oceangyres (Nelson and Brzezinski, 1997).

3.5. Kinetic studies of silicic acid uptake

The silicic acid concentration dependence of Si uptake was investigated at two stations (33S andthe Equator). Speci"c uptake rates (<, h~1) were plotted as a function of the ambient silicic acid


Fig. 8. Concentration dependence of silicic uptake rate by natural diatom assemblages (a) at 33S and (b) at the Equator,at 1803W. Data points show the measured values of<; the curve represents the Michaelis}Menten hyperbola "tted to thedata by the non-linear regression method of Wilkinson (1961).

concentrations (Fig. 8). The dependence of < upon (Si(OH)4) was determined by "tting theMichaelis}Menten equation to the data

<"<

.!9][Si(OH)4]

K4#[Si(OH)4]

,

in which< is the speci"c uptake rate,<.!9

the speci"c uptake rate at in"nite [Si(OH)4], and K4the

half-saturation constant (the silicic acid concentration at which <"<.!9

/2). These two constantsare determined by "tting the data with the non-linear method of Wilkinson (1961).

At 33S, the ambient (Si(OH)4 ) was 1.45 lM. The Si-enrichment experiment gives some evidenceof an hyperbolic response of < to increased silicic acid concentration (Fig. 8a), although the "t tothe Michaelis}Menten function is only approximate. K

4and<

.!9values are 1.57 ($1.32) lM and

0.028 ($0.006) h~1. As diatoms were taking up silicic acid quite rapidly, as indicated by therelatively high <

.!9value, the scatter in the data may be attributed to the very low phytoplankton

biomass, and particularly the very low biogenic concentrations (30 nmol l~1).


Fig. 9. Ratio of biogenic silica production rates at ambient silicic acid concentrations to biogenic silica production ratesat 10 lM of silicic acid concentration above ambient, versus in situ silicic acid concentrations. Experiments wereconducted at each station, at the surface and/or at the chl a maximum.

At the Equator (Fig. 8b), ambient (Si(OH)4 ) was 2.00 lM, and the biogenic silica standing stockwas higher (70 nmol l~1). Accordingly, the Si-enrichment experiment was more conclusive, provid-ing a much better description of the dependence of < upon silicic acid concentrations. CalculatedK

4and <

.!9values are higher, reaching 2.42 ($0.53) lM and 0.052 ($0.004) h~1.

Finally, systematic indications of the degree to which Si uptake was limited by ambient silicicacid concentrations were provided by comparing Si uptake rate at ambient concentration and afteraddition of 10 lM silicic acid, at each station, at the surface or at the depth of the chlorophyllmaximum (Fig. 9). Considering that the K

4determined experimentally at 33S and at the Equator

(1.57 and 2.42 lM) are representative for diatom assemblages of the equatorial area, <.!9

couldtheoretically be reached by adding 10 times the K

4concentration (i.e. 15 to 24 lM of Si(OH)4 ). The

addition of 10 lM of silicic acid, as applied in our experiments, would thus only enhance Si uptakerate up to approximately 85% of <

.!9. Therefore, the <(!."*%/5)/<(10 lM !"07% !."*%/5) ratio, experi-

mentally determined at all stations (Fig. 9), probably underestimates the degree to which Si uptakeby the diatoms is limited by ambient silicic acid concentration. However, a signi"cant increase of Siuptake was observed at all stations after addition of 10 lM Si(OH)4 . In situ production rates wererestricted to between 13 and 76% of <(10 lM !"07% !."*%/5) . A stronger Si limitation was observed forlower ambient concentrations (Fig. 9).

4. Discussion

4.1. Production and export

4.1.1. Biogenic silica stocks and production ratesAt the Equator (03N, 1803E). The geographical limits of the area in#uenced by the equatorial

upwelling vary more or less longitudinally depending upon the oscillation of the system from warm(El Nin8 o) to cold conditions (La Nin8 a). Chemical and physical conditions encountered during theEBENE cruise at the Equator (1803W) show a very similar pattern to those recorded during theFLUPAC cruise (Le Borgne et al., 1995; Eldin et al., 1997), at 1633W (station 76). Although ourcruise track crossed the Equator more to the west, situations are highly comparable because


FLUPAC occurred during a warming event (El Nin8 o), and the warm pool was displaced eastward(Fig. 1). The two sampling areas were situated at the edge of the cool tongue, with a sea surfacetemperature close to 28.53C. Silicic acid and nitrate concentrations were about 2 lM, thus witha Si/N ratio close to 1. For both cruises, surface biogenic silica concentration and production rateswere highly comparable, with values close to 80 nmol l~1 and 2 mmol m~2 d~1 (Blain et al., 1997).Accordingly, similar speci"c rates of biogenic production were 0.5 d~1 for surface waters. Althoughexceptional situations can occur and have been met in frontal structures (Yoder, 1994), our resultsindicate comparable biogenic silica concentrations and production rates for similar physical andchemical conditions. This low variability reinforces the idea that, because of the quasi stationaryequatorial upwelling (driven by trades winds) associated with the surface divergence, the equatorialupwelling area works like a chemostat (Frost and Franzen, 1992).

Interesting comparison can also be made with recent estimates calculated indirectly from silicicacid supply rate to the euphotic zone (Dugdale and Wilkerson, 1998). The authors estimated a Siuptake rate of 2.36 mmol m~2 d~1, i.e. similar to the rates measured directly. However, thereported biogenic silica concentration (43 nmol l~1) was substantially lower, which led to higherspeci"c uptake rates (0.8 d~1) compared to our results. This disagreement could be explained bythe uncertainties resulting from their indirect estimate of the silica biomass. Dugdale and Wilker-son (1998) evaluated the biogenic silica biomass from an estimate of diatom chlorophyll contribu-tion to total chl a (12%) by converting the diatom}chlorophyll to biogenic silica, considering that1 lg l~1 Chl-a"1 mmol m~3 PON, and then using a 1 : 1 molar ratio for diatom N/Si. This wasa stopgap measure in the absence of available data, but it is not surprising to get a two-folddi!erence given the variations that can be observed in Chl-a/PON or N/Si ratios. Hutchins andBruland (1998), for example, found diatom N/Si ratios two to three times lower in Fe-limitedmedium than in Fe-enriched incubations.

Stations poleward (north of 13N and south of 13S). At stations away from the direct in#uence of theequatorial upwelling, conditions encountered were typical of oligotrophic ecosystems. Integratedproduction rates were very low (range 0.1}0.7 mmol-Si m~2 d~1), averaging 0.4 mmol-Si m~2 d~1.These values are close to the lowest rates reported to date from other low silicic acid environments,like the western Sargasso Sea (range 0.2}1.5 mmol-Si m~2 d~1, Brzezinski and Nelson, 1996), theBATS site (range 0.1}0.9 mmol-Si m~2 d~1, Nelson and Brzezinski, 1997) or the western equato-rial Paci"c (mean 1.5 mmol-Si m~2 d~1, Blain et al., 1997). These low silica production rates maypartly be the result of the low availability of the major nutrients, as compared to silicic acid, and asshown by the Si/N ratios '1.

4.1.2. Contribution of diatoms to the new production of the equatorial PacixcThe contribution of diatoms to the new production was estimated indirectly from the compari-

son of biogenic silica production rates to new production measurements reported in the same area(Table 1). In the equatorial area (13S}13N), biogenic silica production rates range between 0.61 and2.91 mmol-Si m~2 d~1 (average: 1.78 mmol-Si m~2 d~1) and can be compared with direct estima-tion of total new production based upon 15NO3 uptake rate measurements. Such a comparison isconsistent as, owing to the low ambient ammonium concentration ((0.1 lM), N requirements ofdiatoms were probably fully met by NO3 uptake (Dortch, 1990). Furthermore, a strong correlationbetween NO3 uptake rates and diatom chlorophyll biomass was found by Landry et al. (1997) on


Tab

le1

Sum

mar

yofre

por

ted

rate

sofne

wpr

oduc

tion

and

expor

ted#ux

oforg

anic

mat

ter

from

the

surfac

ela

yer

ofth

eeq

uato

rial

Pac

i"c

Loc

atio

nPer

iod

Met

hod

New

pro

duct

ion

(mm

ol-C

m~2

d~1)

Exp

ort#ux

(mm

ol-C

m~2

d~1)

Ref

.

903W}18

03103N}103S

14C

]fra

tio

(0.5

)15

Chav

ezan

dBar

ber

(198

7)14

03W

02}03

/199

222

8Ra/

nitr

ate

dist

ribu

tion

17K

uet

al.(

1995

)903W}18

0353

N}53

S-1

992

13C

and

upw

elle

dnitra

te13

.5}20

Chav

ezet

al.(1

996)

1403

W,

53N}53

S02}03

/199

215

Nupt

ake,

die

lpe

riodic

ity

ElN

ino

4.8

McC

arth

yet

al.

(199

6)23

N}23

S08}09

/199

2Pos

tElN

ino

18.5

1503

W13

S}13

N2D

adve

ctiv

eba

lanc

ebe

twee

nupw

and

mer

idio

naldiv

erge

nce

ofN

O3

28C

arr

etal

.(1

995)

234T

h/s

cave

ngin

gm

ode

l4}

5(1

00m

)Bue

ssel

eret

al.(

1995

)14

03W

02}03

/199

223

0Th/2

28Th

0.6}

1.3

(100

m)/0.

14}0.

5(8

50m

)Luo

etal

.(1

995)

93N}123S

08}09

/199

21.

5}5.

0(1

00m

)/0.

5}1.

1(8

50m

)14

03W

02}03

/199

223

4Th/s

ed.tr

ap8.

24.

6}8.

3(1

50m

)M

urra

yet

al.(1

996)

123N

-123

S08}09

/199

214

03W

03}04

/199

223

4Th,on

e-D

model

1.9

(120

m)/0.

54(2

00m

)Bac

on

etal

.(19

96)

10/1

992

2.4

(120

m)/0.

71(2

00m

)13

53W

23N

-63S

04/8

815

N16

.6Pen

8aet

al.(1

992)

!

1503

W,03

10/9

414

C,15

N,se

d.tr

ap19

.112

.1(1

55m

)/3.

7(3

20m

)R

odie

ret

al.(

1997

)18

03W

03S,

1803

W10}11

/199

632

Si9}

20T

his

study

!Aco

nst

antm

ola

rR

ed"el

dra

tio

of6.

6w

asuse

dto

conve

rtnitro

gen

upta

kedat

ain

toca

rbon

upta

ke.


Fig. 10. Evolution of salinity and temperature at 20 m depth, at a station located at 03N, 1803E, during three successivedays.

EqPac cruises during El Nin8 o (January}February 1992), and during normal upwelling conditions(August}September 1992). Our results based upon Si-uptake are consistent with rates of newproduction reported by McCarthy et al. (1996) and Pen8 a et al. (1992) from NO3 uptake(0.72}2.51 mmol-N m~2 d~1) in the same area. This comparison gives a mean Si/N ratio of 1.1,which is consistent with existing Si/N data for diatoms in culture. These ratios were shown to varybetween 0.7 and 2, depending on ambient Fe concentrations (Takeda, 1998).

The primary production due to diatoms in the equatorial area (13N}13S) can be estimated fromthe biogenic silica production and a Si/C diatom stoichiometry ranging from 0.13 (Brzezinski,1985) to 0.29 (Takeda, 1998). Such a range is used to take into account a possible variation of thedegree of silici"cation in response to a potential iron de"ciency (Hutchins and Bruland, 1998).Results of these calculations give a primary production due to diatoms that ranged between 2.10and 22.38 mmol-C m~2 d~1 (average: 12.2 mmol-C m~2 day~1). These values compare well withcarbon new production estimates reported from the same area (Table 1), ranging from 4.8 to28 mmol-C m~2 d~1.

Altogether, these calculations based on direct measurement of Si uptake suggest that newproduction in the equatorial region (13N}13S) could mostly be sustained by diatoms.

4.1.3. Biogenic silica export yuxes (03S, 1803W)It is generally admitted that the diatom-based production is exported to deeper layers (Dugdale

and Goering, 1967; Eppley and Peterson, 1979), either directly (aggregation, sedimentation) orindirectly (after mesozooplankton grazing).

An indirect estimate of biogenic silica loss in the surface layer can be derived from biogenic silicaproduction rates measured during three successive days at the equator (Fig. 7), where steady-stateconditions were met. Steady state was deduced from the stability of physical (Fig. 10), chemical andbiological parameters (Le Borgne et al., 1998). Under such conditions, the biogenic silica producedin the euphotic layer (the gross production, equal to 2.6 mmol m~2 d~1) is balanced by thebiogenic silica loss (i.e. export#recycled production) of the system.

An indirect estimate of the contribution of diatom export production to the total carbon exportproduction can be derived from the comparison between the diatom-C loss and carbon exportproduction #uxes reported by others (Table 1) for the same area. The former was estimated fromthe mean biogenic silica production rate measured at steady state, during the 3-days station at theequator (03S, 1803W), and converted to carbon using Si/C ratios. It ranges between 9 and20 mmol-C m~2 d~1. Carbon export production from the euphotic zone was estimated either from


Th isotopes distribution or from particles interceptor traps (PIT). If we consider C export #uxesfrom the upper layer (100}150 m), they range altogether between 0.6 and 12.1 mmol-C m~2 d~1,with most of the data in the lower range (Table 1).

This comparison shows that the minimum value calculated for the diatom-C loss is close to orhigher than the maximum value of particulate organic carbon exported #ux. This suggests, on theone hand, that diatoms are a major contributor to the export #ux of organic matter from thesurface to deeper layers, and, on the other hand, that a signi"cant fraction of the diatom biogenicsilica is redissolved in the euphotic layer.

4.1.4. Dissolution of biogenic silica in the surface layerDirect measurements of biogenic silica dissolution rates are seldom made in low chlorophyll

environment because of the lack of su$ciently sensitive methods. However, the few existing data(Nelson and Goering, 1977; Nelson et al., 1981; Nelson and Gordon, 1982; Brzezinski and Nelson,1989) cover a fairly wide range of marine systems. The overall mean resulting from thesestudies indicates that, in surface waters, dissolution represents 58% of the biogenic silicaproduction (Nelson et al., 1995). Temperature, physiological state of diatom cells (Kamatani, 1982),and bacterial activity (Bidle and Azam, 1999) have been shown to enhance the processes ofbiogenic silica dissolution. The speci"c value of 0.006 h~1 or 0.14 d~1 reported by Brzezinski andNelson (1989) from the relatively warm waters (203C) of a Gulf Stream core ring is the one thatcould best compare with expected values for the equatorial Paci"c. On this basis, we calculatethat biogenic silica dissolution could represent, in the upper 150 m, 33% (0.006 h~1/0.018 h~1)of the average speci"c production in the 13N}13S area, and 75% for stations polewards(0.006 h~1/0.008 h~1).

In the equatorial Paci"c, biogenic silica dissolution rate can also be estimated from the budgetbetween production rate and downward #ux of biogenic silica measured at 300 m depth withdrifting sediment traps (Blain et al., 1997) in October 1994 (FLUPAC cruise). This percentagereaches 84%. It is very high compared to rates calculated above for the upper layer (150 m), but wemust note that it is measured at 300 m depth, and dissolution at intervening depths might be high,as evidenced by Bacon et al. (1996).

These results suggest strongly that, as in oligotrophic gyres, biogenic silica dissolution is ofquantitative signi"cance and must be taken into account in the silicic acid cycle of the equatorialPaci"c.

4.2. Diatom limitation

4.2.1. In situ diatom growth limitationAt steady state, the diatom growth rate, calculated from the measurement of Si uptake rate, is

equal to the division rate of the diatom assemblage. Steady-state uptake rate is measured when theinstantaneous conditions (nutrient concentration, temperature, salinity, light, etc.) are the same asthe preconditioning one (Morel, 1987). The equatorial Paci"c has many non-steady-state charac-teristics. Westward propagating tropical instability waves, and eastward propagating Kelvinwaves, are able to induce variability in biogeochemical processes on time scales of days. Theirsignatures can be seen in modi"cations of sea surface characteristics. However, no such events wereobserved at the equator over the course of the study (5}7 November 96), as shown by the


temperature and salinity evolution (Fig. 10) or as described in more detail in the cruise report (LeBorgne et al., 1998). In this context, the Si uptake rate was measured at steady state, and thededuced diatom growth rate (k

*/ 4*56) should be equal to the division rate of the diatom assemblage.

In the equatorial zone (13S}13N), mean uptake rates measured under simulated in situ condi-tions at the surface imply a mean growth rate (k

*/ 4*56) of 0.35 d~1, yielding 0.5 doubling of biogenic

silica per day. These growth rates are substantially lower than the 2.5 doublings of biomass per daypredicted by the temperature-dependent equation of Eppley (1972), i.e., in non-limiting light andnutrient conditions, and suggest that diatom growth is limited.

4.2.2. Direct evidence of Si limitationThe positive response of Si uptake rates by natural diatom communities of the central equatorial

Paci"c after silicic acid enrichments, provides the "rst direct evidence of a widespread silicic acidlimitation of biogenic silica production rates in this area.

In both areas, half saturation constants of the diatom population are close to the ambient silicicacid concentration. At 33S, the measured K

4is 1.57 ($1.32) lM when ambient concentration is

1.45 lM, whereas at the Equator, the K4

is 2.42 ($0.53) lM in ambient concentration of 2 lM.These half saturation constants of Si uptake are in the range of values reported for other naturaldiatoms assemblages. Previously measured K

4values for silicic acid uptake vary widely, at least by

one order of magnitude, from 0.53 lM (in a Gulf Stream warm-core ring, where ambient silicic acidconcentration was below the detection limit, Nelson and Brzezinski, 1990) to 5.3 lM (in theMississippi river plume, Nelson and Dortch, 1996). Higher K

4values are generally characteristic of

silicic-acid-enriched environments. One example is the Ross Sea, where a K4

of 4.6 lM has beenmeasured by Nelson and TreH guer (1992), in waters where silicic acid concentration seldom decreasebelow 5 lM. In situ measured K

4do not refer to a speci"c species, but rather to an assemblage of

di!erent diatoms and could re#ect some adaptation of the diatom assemblage to in situ conditions.These results are in good agreement and support the Dugdale and Wilkerson (1998) modi"edSi(OH)4 pump model, which states that the diatom population is regulating at about half themaximal uptake, with a substrate concentration near the half saturation constant, K

4.

The<.!9

values reported from the two Si uptake kinetic studies (0.028 h~1 at 33S and 0.052 h~1at the Equator) are comparable to those previously reported for natural population of theoligotrophic waters of the Sargasso Sea and the Gulf Stream warm-core ring (Brzezinski andNelson, 1996; Nelson and Brzezinski, 1990), but lower than in the Peru upwelling region, whereGoering et al. (1973) reported a <

.!9as high as 0.075 h~1.

Furthermore, the ratio <*/ 4*56

/<.!9

provides an indication of the degree to which the diatom Siuptake is limited by ambient silicic acid concentrations. That limitation is evaluated at 54% of themaximal speci"c uptake rate at 33S and 42% at the Equator. This direct evidence of Si uptake ratelimitation does not necessarily imply that diatom growth rate is limited by Si. It is known thatdiatoms can maintain division rates close to k

.!9, even when the rate of Si uptake is signi"cantly

less than <.!9

, by decreasing the Si content of the frustule. Conversely, physiological adaptationcan take place in response to nutrient abundance (increase in cellular quota), in the course of theexperiment, while division rate remains approximately constant. In other words, diatoms are ableto maintain a growth rate signi"cantly lower than k

.!9, even when the rate of Si uptake is close to

<.!9

, by increasing the Si content of their frustule. Then the diatom division rate (0.8 d~1, or 1.15doubling of the biomass per day) that we can predict from <

.!9is certainly an over-estimation of


the maximal growth rate that diatoms could reach in their environment if ambient silicic acid wasnot limiting.

However, this predicted and over-estimated daily growth is still signi"cantly lower thanthe 2.5 doublings of biomass per day predicted by the temperature-dependent equation ofEppley (1972), i.e., under non-limiting light and nutrient conditions. Comparing doublingtimes reported for equatorial Paci"c diatoms and those expected from temperature (Eppley, 1972)could appear bold. Eppley's curve is the upper limit of a scatter plot that has tremendousvariations, and it does not exclude the possibility that many phytoplankton assemblagesmay not be physiologically capable of reaching this maximum. Nevertheless, Latasa et al. (1997)have measured, from dilution experiments in the central equatorial Paci"c, diatom growth rates of1.7 d~1. This result implies 2.4 doublings per day of the diatom population. Even if Latasa et al.(1997) did not rule out a possible containment or contamination artifact in their experiments toexplain such high growth rates, this result shows that some diatom assemblages of the centralequatorial Paci"c are physiologically capable of reaching the maximum predicted by Eppley'sequation.

As far as silicic acid limitation in the central equatorial Paci"c is concerned, we can conclude thatambient silicic acid is limiting biogenic silica production, but the silicic acid limitation of diatomgrowth is an hypothesis that remains to be tested. However, even if diatom growth was limited byambient silicic acid, such Si limitation would certainly not be su$cient in itself to explain the lowdiatom growth rates observed in situ.

4.2.3. Co-limitationThese results suggest that diatoms in the central equatorial Paci"c might be co-limited simulta-

neously by some other resource than silicic acid. In this area of the Paci"c, when looking foradditional potentially co-limiting factor, we evidently think about iron, because iron limitation hasbeen extensively reported as a controlling factor of phytoplankton growth. For instance, the IronexII experiment (Coale et al., 1996b) resulted in a 85-fold increase in diatom biomass within a 10 km2patch of surface water over 10 days, corresponding to a growth rate of about 1 db d~1 (Coale et al.,1996a), which is also signi"cantly lower than the maximum expected from Eppley's formula (i.e.2.5 db d~1).

If, with Fe addition alone, or Si addition alone, diatom growth does not even approach the upperlimit imposed by the temperature dependence relation, then one explanation could be that Fe andSi limitations interact, rather than just being opposing explanations for the HNLC character of thesystem. Although little is known on the synergy between iron and silicic acid limitation, process-level experiments performed at non-limiting silicic acid concentrations (Hutchins and Bruland,1998; Takeda, 1998) have shown that Fe de"ciency could induce increases in cellular silica ora decrease in the cellular N content of diatoms. It is not clear, however, what the relationshipbetween Fe limitation and cellular Si content would be once silicic acid is depleted to levels thatlimit the rate of Si uptake. All experiments to date that show increases in cellular Si under Felimitation have been preformed at non-limiting silicic acid concentrations, and once Si uptake islimited by silicic acid, it would probably be more di$cult for diatom cells to produce frustules withelevated Si content. We could envision, as suggested in Ragueneau et al. (in press), that when bothSi and Fe are depleted, diatom Si uptake rate is limited by silicic acid concentrations, but NO3uptake rate or photosynthesis are limited by Fe.


Additional data on those interactions would be of great value. But already existing models andstudies of nutrient limitation should be reconsidered. They generally assume a single-controllingnutrient (Hecky and Kilham, 1988; Lancelot et al., 1997; Dugdale and Wilkerson, 1998), which isdetermined as the most limiting nutrient. The latter is "xed by the comparison between the ambientconcentrations and the Michaelis}Menten kinetic parameters, characterizing the uptake of eachnutrient. All nutrient uptake rates are then set proportional to that nutrient (Liebig model).

O'Neill et al. (1989) show that although the Liebig model remains useful when one nutrientlimitation predominates, it fails to converge to reasonable numbers when several nutrients arereaching sub-optimal concentrations. He studied and compared the behaviour of di!erent models:additive, multiplicative, and others. Among them, the additive model appears to have the bestproperties to serve as a general description for multiple nutrient limitation. In the equatorialPaci"c, conditions might be those reported by O'Neill et al. (1989) as ambient silicic acid and ironconcentrations have both been reported as being at sub-optimal levels.

Future studies should take into account simultaneous limitation by di!erent nutrients reachingsub-optimal concentrations, and new models (such the one proposed by O'Neill et al., 1989) shouldbe tested. The development of a high sensitivity method to measure in situ silica dissolution ratesand process-level studies to better understand the links between the silica and carbon cycles arenecessary.

Acknowledgements

We especially thank Robert Le Borgne for his leadership as chief scientist, the captain and crewof the R.V. Atalante, and Annick Masson for technical assistance in sample analysis. This researchwas supported by CNRS-INSU and ORSTOM.

References

Bacon, M.P., Cochran, J.K., Hirschberg, D., Hammar, T.R., Fleer, A.P., 1996. Export #ux of carbon at the Equatorduring the Eqpac time-series cruises estimated from 234Th measurments. Deep-Sea Research II 43 (4}6), 1133}1154.

Banahan, S., Goering, J.J., 1986. The production of biogenic silica and its accumulation on the southeastern Bering Seashelf. Continental Shelf Research 5, 199}213.

Bidle, K.D., Azam, F., 1999. Accelerated dissolution of diatom silica by marine bacterial assemblages. Nature 397,508}512.

Blain, S., Leynaert, A., TreH guer, P., ChreH tiennot-Dinet, M.J., Rodier, M., 1997. Biomass, growth rates and limitation ofequatorial Paci"c diatoms. Deep-Sea Research I 44, 1255}1275.

Brzezinski, A.M., 1985. The Si : C : N ratio of marine diatoms: interspeci"c variability and the e!ect of some environ-mental variables. Journal of Phycology 21, 347}357.

Brzezinski, M.A., Nelson, D.M., 1989. Seasonal changes in the silicon cycle within a Gulf Strean warm-core ring.Deep-Sea Research I 36, 1009}1030.

Brzezinski, M.A., Nelson, D.M., 1996. Chronic substrate limitation of silicic acid uptake rates in the western SargassoSea. Deep-Sea Research II 43, 437}453.

Brzezinski, M.A., Phillips, D.R., Chavez, F.P., Friederich, G.E., Dugdale, R.C., 1997. Silica production in the Monterey,California, upwelling system. Limnology and Oceanography 42 (8), 1694}1705.

Buesseler, K.O., Andrews, J.A., Hartman, M.C., Belastock, R., Chai, F., 1995. Regional estimates of the export #ux ofparticulate organic carbon derived from thorium-234 during the JGOFS Eqpac program. Deep-Sea Research II 42(2}3), 777}804.


Carr, M., Lewis, M.R., Kelley, D., Jones, B., 1995. A physical estimate of new production in the equatorial Paci"c along1503W. Limnology and Oceanography 40 (1), 138}147.

Chavez, F.P., Buck, K.R., Service, S.K., Newton, J., Barber, R.T., 1996. Phytoplankton variability in the central andeastern tropical Paci"c. Deep-Sea Research II 43 (4}6), 835}870.

Chavez, F.P., Barber, R.T., 1987. An estimate of new production in the equatorial Paci"c. Deep Sea Research 34,1229}1243.

Chavez, F.P., Buck, K.R., Barber, R.T., 1990. Phytoplankton taxa in relation to primary production in the equatiorialPaci"c. Deep-Sea Research 37, 1733}1752.

Coale, K.H., Fitzwater, S.E., Gordon, R.M., Johnson, K.S., Barber, R.T., 1996a. Control of community growth andexport production by upwelled iron in the equatorial Paci"c Ocean. Nature 379, 621}624.

Coale, K.H., Johnson, K.S., Fitzwater, S.E., Gordon, R.M., Tanner, S., Chavez, F.P., Ferioli, L., Sakamoto, C., Rogers, P.,Millero, F., Steinberg, P., Nightingale, P., Cooper, D., Cochlan, W.P., Landry, M.R., Constantinou, J., Rollwagen, G.,Trasvina, A., Kudela, R., 1996b. A massive phytoplankton bloom induced by an ecosystem-scale iron fertilizationexperiment in the equatorial Paci"c Ocean. Nature 383, 495}501.

Dortch, Q., 1990. The interaction between ammonium and nitrate uptake in phytoplankton. Marine Ecology ProgressSeries 61, 183}201.

Dugdale, R.C., Goering, J.J., 1967. Uptake of new and regenerated form of nitrogen in primary productivity. Limnologyand Oceanography 12, 196}206.

Dugdale, R.C., Wilkerson, F.P., Minas, H.J., 1995. The role of silicate pump in driving new production. Deep-SeaResearch I 42, 697}719.

Dugdale, R.C., Wilkerson, F.P., 1998. Silicate regulation of new production in the equatorial Paci"c upwelling. Nature391, 270}273.

Eldin, G., Rodier, M., Radenac, M.-H., 1997. Physical and nutrient variability in the upper equatorialPaci"c associated with westerly wind forcing and wave activity in October 1994. Deep-Sea Research II 44,1783}1800.

Eppley, R.W., 1972. Temperature and phytoplankton growth in the sea. Fisheries Bulletin 70, 1063}1085.Eppley, R.W., Peterson, B.J., 1979. Particulate organic matter #ux and planktonic new production in the deep ocean.

Nature 282, 677}680.Frost, B.W., Franzen, N.C., 1992. Grazing and iron limitation in the control of phytoplankton stock and nutrient

concentration: a chemostat analogue of the Paci"c equatorial upwelling zone. Marine Ecology Progress Series 83,291}303.

Glibert, P.M., McCarthy, J.J., 1984. Uptake and assimilation of ammonium and nitrate by phytoplankton: indices ofnutritional status for natural assemblages. Journal of Plankton Research 6, 677}697.

Goering, J.J., Nelson, D.M., Carter, J.A., 1973. Silicic acid uptake by natural population of marine phytoplankton.Deep-Sea Research I 20, 777}789.

Hecky, R.E., Kilham, P., 1988. Nutrient limitations of phytoplankton in freshwater and marine environments; a review ofrecent evidence on the e!ects of enrichment. Limnology and Oceanography 33, 796}822.

Hutchins, D.A., Bruland, K.W., 1998. Iron-limited diatom growth and Si : N uptake ratios in a coastal upwelling regime.Nature 393, 561}564.

Kamatani, A., 1982. Dissolution rates of silica from diatoms decomposing at various temperatures. Marine Biology 68,91}96.

Ku, T.L., Luo, S., Kusakabe, M., Bishop, J.K.B., 1995. 228Ra-derived nutrient budgets in the upper equatorial Paci"c andthe role of `newa silicate in limiting productivity. Deep-Sea Research II 42 (2}3), 479}498.

Lancelot, C., Rousseau, V., Billen, G., Van Eeckhout, D., 1997. Coastal eutrophication of the Southern Bight of NorthSea: assessment and modeling. In: Ozsoy, E., Mikaelyan, A. (Eds.), Sensitivity to Change: Black Sea, Baltic Sea andNorth Sea. NATO-ASI Series, Vol. 2, pp. 439}454.

Landry, M.R., Barber, R.T., Bidigare, R.R., Chai, F., Coale, K.H., Dam, H.G., Lewis, M.R., Lindley, S.T., McCarthy, J.J.,Roman, M.R., Stoecker, D.K., Verity, P.G., White, J.R., 1997. Iron and grazing constraints on primary production inthe central equatorial Paci"c: an Eqpac synthesis. Limnology and Oceanography 42, 405}418.

Latasa, M., Landry, M.R., SchluK ter, L., Bidigare, R.R., 1997. Pigment-speci"c growth and grazing rates of phytoplanktonin the central equatorial Paci"c. Limnology and Oceanography 42 (2), 289}298.


Le Borgne, R., Brunet, C., Eldin, G., Radenac, M.H., Rodier, M., 1995. Campagne oceH anographique FLUPAC a bord duN.O. l'Atalante. Du 23 septembre au 29 octobre 1994. Recueil des donneH es, Tome 1. ORSTOM, NoumeH a, ArchivesSciences de la Mer, oceH anographie, No. 1.

Le Borgne, R., Langlade, M.J., Polidori, P., Rodier, M., 1998. Campagne oceH anographique EBENE a bord du N.O.l'Atalante. Du 21 octobre au 20 novembre 1996. Recueil des donneH es, Tome 1. ORSTOM, NoumeH a, Archives Sciencesde la Mer, oceH anographie, No. 3.

Leynaert, A., TreH guer, P., Nelson, D.M., Del Amo, Y., 1996. 32Si as a tracer of biogenic silica production: methodologicalimprovements. In: Baeyens, J., Dehairs, F., Goeyens, L. (Eds), Integrated Marine System Analysis, Minute of the FirstWorkshop Meeting. VUB, Brussels, Belgium, pp. 29}35.

Luo, S., Ku, T.L., Kusakabe, M., Bishop, J.K.B., Yang, Y.L., 1995. Tracing particle cycling in the upper ocean with 230Thand 228Th: An investigation in the equatorial Paci"c along 1403W. Deep-Sea Research II 42 (2}3), 805}830.

McCarthy, J.J., Garside, C., Nevins, J.L., Barber, R.T., 1996. New production along 1403W in th equatorial Paci"c duringand following the 1992 El Nino event. Deep-Sea Research II 43 (4}6), 1065}1094.

Morel, F.M.M., 1987. Kinetics of nutrient uptake and growth in phytoplankton. Journal of Phycology 23, 137}150.Murray, J.W., Young, J., Newton, J., Dunne, J., Chapin, T., Paul, B., McCarthy, J.J., 1996. Export #ux of particulate

organic carbon from the central equatorial Paci"c determined using a combined drifting trap - 234Th approach.Deep-Sea Research II 43 (4-6), 1095}1132.

Nelson, D.M., Brzezinski, M.A., 1990. Kinetics of silicic acid uptake by natural diatom assemblages in two Gulf Streamwarm-core rings. Marine Ecology Progress Series 62, 283}292.

Nelson, D.M., Brzezinski, M.A., 1997. Diatom growth and productivity in an oligotrophic midocean gyre: a 3-yr recordfrom the Sargasso Sea near Bermuda. Limnology and Oceanography 42, 473}486.

Nelson, D.M., Dortch, Q., 1996. Silicic acid depletion and silicon limitation in the plume of the Mississippi river: evidencefrom kinetics studies in spring and summer. Marine Ecology Progress Series 136, 163}178.

Nelson, D.M., Goering, J.J., 1977. Near-surface silica dissolution in the upwelling region o! northwest Africa. Deep-SeaResearch I 24, 65}73.

Nelson, D.M., Goering, J.J., 1978. Assimilation of silicic acid by phytoplankton in the Baja California and northwestAfrica. Limnology and Oceanography 23 (3), 508}517.

Nelson, D.M., Goering, J.J., Boisseau, D.W., 1981. Consumption and regeneration of silicic acid in three coastalupwelling systems. In: Richards, F.A. (Ed.), Coastal Upwelling, Vol. 1. AGU, Washington DC, pp. 242}256.

Nelson, D.M., Gordon, L.I., 1982. Production and pelagic dissolution of biogenic silica in the southern Ocean.Geochimica et Cosmochimica Acta 46, 491}501.

Nelson, D.M., Smith, W.O., 1986. Phytoplankton bloom dynamics of the western Ross Sea ice-edge. II. Mesoscale cyclingof nitrogen and silicon. Deep-Sea Research I 33, 1389}1412.

Nelson, D.M., Smith, W.O., 1991. Sverdrup revisited: critical depths, maximum chlorophyll levels, and controlof Southern Ocean productivity by the irradiance-mixing regime. Limnology and Oceanography 36 (8),1650}1661.

Nelson, D.M., TreH guer, P., 1992. Role of silicon as a limiting nutrient to Antarctic diatoms: evidence from kinetic studiesin the Ross Sea ice-edge zone. Marine Ecology Progress Series 80, 255}264.

Nelson, D.M., TreH guer, P., Brzezinski, M.A., Leynaert, A., QueH guiner, B., 1995. Production and dissolution of biogenicsilica in the ocean: revised estimates, comparison with regional data and relationship to biogenic silica sedimentation.Global Biogeochemical Cycle 9, 359}372.

O'Neill, R.V., DeAngelis, D.L., Pastor, J.J., Post, W.M., 1989. Multiple nutrient limitation in ecological models.Ecological Modelling 46, 147}163.

Paasche, E., 1973. Silicon and the ecology of marine plankton diatoms. 1. Thalassiosira pseudonana (Cyclotella nana)grown in a chemostat with silicate as a limiting nutrient. Marine Biology 19, 117}126.

Pen8 a, M.A., Harrison, W.G., Lewis, M.R., 1992. New production in the central equatorial Paci"c. Marine EcologyProgress Series 80, 265}274.

Price, N.M., Ahner, B.A., Morel, F.M.M., 1994. The equatorial Paci"c ocean: grazer-controlled phytoplankton popula-tion in an iron-limited ecosystem. Limnology and Oceanography 39, 520}534.

Ragueneau, O., TreH guer, P., 1994. Determination of biogenic silica in coastal waters: applicability and limits of thealkaline digestion method. Marine Chemistry 45, 43}51.


Ragueneau, O., TreH guer, P., Leynaert, A., et al., in press. A review of the Si cycle in the modern ocean: recent progress andmissing gaps in the application of biogenic opal as a paleoproductivity proxy. Global and Planetary Change.

Sarmiento, J.L., Siegenthaler, U., 1992. In: Falkowski, P.G., Woodhead, A.D. (Eds.), Primary productivity and Bio-geochemical Cycles in the Sea. Plenum, New York.

Schlegel, H.G., 1987. In: General Microbiology. Cambridge University Press, Great Britain, 587 p.Strickland, J.D.H., Parsons, T.R., 1972. A practical handbook of seawater analysis. Bulletin Fishery Research Canada

167, 310.Takeda, S., 1998. In#uence of iron availability on nutrient consumption ratio of diatoms in oceanic waters. Nature 393,

774}777.Thomas, W.H., Dodson, A.N., 1975. On silicic acid limitation of diatoms in near-surface waters of the eastern tropical

Paci"c Ocean. Deep-Sea Research I 22, 671}677.Wilkinson, G.N., 1961. Statistical estimations in enzyme kinetics. Biochemical Journal 890, 1375}1387.Yoder, J.A., 1994. A line in the sea. Nature 371, 689}692.


Documents

Silicon limitation of biogenic silica production in the Equatorial Pacific