Environmental factors controlling the phytoplankton blooms at the

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Deep-Sea Research I

Deep-Sea Research I 55 (2008) 1150– 1166

0967-06

doi:10.1

� Cor

E-m

pollery@

dir@noc

journal homepage: www.elsevier.com/locate/dsri

Environmental factors controlling the phytoplankton blooms at thePatagonia shelf-break in spring

Virginia M.T. Garcia a,�, Carlos A.E. Garcia b, Mauricio M. Mata b, Ricardo C. Pollery c,Alberto R. Piola d,e, Sergio R. Signorini f, Charles R. McClain f, M. Debora Iglesias-Rodriguez g

a Department of Oceanography, Federal University of Rio Grande, Av. Italia, Km 8, Rio Grande, RS 96201-900, Brazilb Department of Physics, Federal University of Rio Grande, Av. Italia, Km 8, Rio Grande, RS 96201-900, Brazilc Institute of Biological and Environmental Sciences, Universidade Santa Ursula, Rua Jornalista Orlando Dantas, 59, Rio de Janeiro, RJ 22231-010, Brazild Servicio de Hidrografia Naval, Av. Montes de Oca, 2124, Buenos Aires 1271, Argentinae Universidad de Buenos Aires, Argentinaf NASA Goddard Space Flight Center, Code 614.8, Greenbelt Road, Greenbelt, MD 20771, USAg School of Ocean and Earth Science, National Oceanography Centre, University of Southampton, European Way, Southampton SO14 3ZH, UK

a r t i c l e i n f o

Article history:

Received 10 July 2007

Received in revised form

23 April 2008

Accepted 25 April 2008Available online 10 May 2008

Keywords:

Phytoplankton bloom

Nutrients

Primary production

Patagonia shelf-break

Malvinas Current

37/$ - see front matter & 2008 Elsevier Ltd

016/j.dsr.2008.04.011

responding author. Tel.: +55 53 32336510; fa

ail addresses: [email protected], docvmt

hotmail.com (R.C. Pollery), [email protected]

.soton.ac.uk (M.D. Iglesias-Rodriguez).

a b s t r a c t

The shelf-break front formed between Argentinean shelf waters and the Malvinas Current

(MC) flow shows a conspicuous band of high phytoplankton biomass throughout spring

and summer, detected by ocean color sensors. That area is the feeding and spawning

ground of several commercial species of fish and squid and is thought to play an

important role in CO2 sequestration by the ocean. Phytoplankton blooms in this area

have been attributed mainly to coccolithophorids, a group of calcite-producing

phytoplankton. Here we present the environmental factors associated with the spring

bloom at the Patagonian shelf-break (401–481S) in the austral spring 2004. A remarkable

bloom of diatoms and dinoflagellates (approximately 1200 km long) was observed

along the front, where integrated chlorophyll values ranged from 90.3 to 1074 mg m�2. It

is suggested that supply of macro-nutrients by upwelling and probably iron by

both upwelling and shelf transport contribute to maintaining the spring bloom. Strong

water column stability along the front allowed the accumulation of algal cells

mainly in the top 50 m and their maintenance in the euphotic layer. East of

the shelf-break front, macronutrient levels were high (surface nitrate ¼ 16.6 mM,

phosphate ¼ 0.35mM, silicate ¼ 4.0 mM), associated with low phytoplankton biomass

(o2 mg m�3). This was due to mixing and advection associated with the MC flow and to

grazing pressure at a transitional site between the MC and the high chlorophyll patch.

Primary production rates (determined by the 14C technique) ranged between 1.9 and

7.8 g C m�2 d�1. Primary production was highest near 421S partly because of the elevated

phytoplankton biomass, which consumed most of the nitrate and phosphate in

surface waters in this region. These high primary production rates are comparable with

maximal seasonal productivity at eastern boundary currents. The large bloom extent at

the Patagonian shelf-break (approximately 55,000 km2 patch of 42 mg m�3 chlorophyll),

the associated primary production rates and diatom dominance indicate a potentially

significant biological control of gases such as O2 and CO2 in surface layers. The main

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[email protected] (V.M.T. Garcia), [email protected] (C.A.E. Garcia), [email protected] (M.M. Mata),

v.ar (A.R. Piola), [email protected] (S.R. Signorini), [email protected] (C.R. McClain),

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V.M.T. Garcia et al. / Deep-Sea Research I 55 (2008) 1150–1166 1151

factors favoring the development and maintenance of these blooms are nutrient supply

from MC upwelling and water column stability. Other processes such as mixing or grazing

play an important role in biomass modulation in the region.

& 2008 Elsevier Ltd. All rights reserved.

1. Introduction

The Patagonian shelf off Argentina shows complexdynamic processes influenced by tides, the confluence oftwo western boundary currents (Brazil and MalvinasCurrents), and freshwater discharge from the Rio de laPlata. Several oceanographic fronts can be identified in theshelf region associated with high chlorophyll concentra-tions (Acha et al., 2004; Bianchi et al., 2005; Carreto et al.,1995). At the shelf-break, the cooler and more salinewaters of the Malvinas Current (MC), which is derivedfrom the Antarctic Circumpolar Current, meet the sub-antarctic shelf waters producing a front with mild to weakdensity gradient (Martos and Piccolo, 1988). The cross-shelf-break temperature gradient is strongest in australsummer and autumn (Saraceno et al., 2004) and is alsoassociated with enhanced chlorophyll concentration(Acha et al., 2004; Rivas et al., 2006; Romero et al.,2006). The frontal areas on the shelf and at the shelf-breakare associated with intense ocean CO2 uptake in latesummer, with estimated mean seasonal fluxes of up to�5.7 mmol CO2 m�2 d�1 (Bianchi et al., 2005). Studiesbased on a large number of surface pCO2 measurementsand NCEP/NCAR wind data suggest that this area is asignificant sink for atmospheric CO2, with an importantcontribution from biological production (Takahashi et al.,2002). The high productivity of this region sustains stocksof several species of commercial fish and squid, whichspawn and feed along the Patagonian shelf-break front,including the Argentine hake Merlucius hubbsi (Podesta,1990), anchovy Engraulis anchoita (Berlotti et al., 1996),and the shortfin squid Illex argentinus (Berlotti et al.,1996). The intense fishing activities in this area have beendepicted through remote sensing of global light-fishing(Rodhouse et al., 2001).

Recent studies based on both past (CZCS) and recent(SeaWiFS) ocean color sensors suggest that phytoplanktonproduction has increased significantly over the past twodecades in the southwestern Atlantic ocean, particularlyin the Patagonian shelf region (Gregg et al., 2005). Thistrend has also been detected in 6 years of SeaWiFS data(Rivas et al., 2006). However, there is no published reportof in situ data collected simultaneously with satelliterecords to validate ocean color algorithms for this region.

Along the Patagonian shelf-break front, consistentstreaks of high chlorophyll (seen in Fig. 1) are observedduring austral spring and summer, often being more than1000 km long (Romero et al., 2006; Saraceno et al., 2005;Rivas, 2006). High phytoplankton biomass associated withthe shelf-break front at 38–391S was attributed to nutrientrenewal by mixing on the slope, where the subantarcticwaters of the MC are a source of macronutrients, especiallynitrate (Carreto et al., 1995). Measurements of primaryproduction during a dinoflagellate bloom near the shelf-

break (at 391S) showed values of 0.1–2.7 g C m�2 d�1 (Negriet al., 1992).

In satellite ocean color images, the chlorophyll patchesassociated with the shelf-break front show high bluereflectance, especially in mid summer, characteristic ofcoccolithophorid blooms (Brown and Podesta, 1997;Brown and Yoder, 1994). The seasonal variation of thishigh chlorophyll band (from �37 to 511S) has recentlybeen studied with a series of ocean color SeaWiFS images(Garcia et al., 2004; Rivas, 2006; Rivas et al., 2006;Romero et al., 2006; Saraceno et al., 2005). Apparently,this thermal front between the stratified subantarcticshelf waters and the cooler and vertically mixed water ofthe MC provides both light (on the stratified side) andnutrients (on the turbulent side) to sustain high phyto-plankton biomass levels at the front during the warmseason (spring and summer). However, both the phyto-plankton biomass and community composition may differsubstantially between the two seasons. The blooms beginin austral spring, probably dominated by diatoms, whenchlorophyll-a concentration is maximum (Signorini et al.,2006), but in early austral summer (December, January),there is indication of a shift in the phytoplanktoncommunity, with dominance of calcite-producing phyto-plankton and moderate chlorophyll concentration (Brownand Podesta, 1997; Brown and Yoder, 1994; Signorini et al.,2006).

Despite the ecological and biogeochemical relevance ofthe shelf-break front, to date there are only scarce in situ

measurements of the phytoplankton community structureand primary production along the shelf-break front toconfirm these seasonal patterns. Moreover, the possiblephysical and chemical mechanisms that drive and sustainthe phytoplankton blooms are not fully understood.

Here we present results of a cruise carried out alongthe Patagonian shelf-break in November 2004, during thefirst field campaign of the PATagonian EXperiment(PATEX). The experiment was designed to determine thephytoplankton taxonomic composition, primary produc-tion rates and the main oceanographic, optical andbiogeochemical features associated with shelf-breakblooms in spring and summer. The main goals of thepresent work are to determine the phytoplankton com-munity, biomass and primary production levels along thePatagonian shelf-break front in spring and to explore theassociated physical, chemical and biological mechanisms.

2. Methods

2.1. Sampling

Nineteen oceanographic stations were sampled during3–6 November 2004 in the vicinity of the Patagonia

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Fig. 1. Right panel: MODIS Aqua Chlorophyll image composite from 31 October to 07 November 2004, showing the sampling stations during the PATEX I

cruise (3–6 November) along the high chlorophyll band at the Patagonian shelf-break. Four stations with a circle (Stns. 1, 6, 12 and 16) indicate the four

sites where primary production was measured. The upper left side inset shows the study region on a monthly SeaWiFS chlorophyll composite (01–30

November 2004). The lower inset shows bathymetric lines and station numbers.

V.M.T. Garcia et al. / Deep-Sea Research I 55 (2008) 1150–11661152

shelf-break (Fig. 1). Sampling was conducted duringdaytime, in groups of four or five stations, with theship sailing southwards at night. Three transects weresampled along the shelf-break front (regions 1, 2 and 4),and one transect was sampled across the front, at 441S(region 3).

Vertical profiles of temperature, salinity, dissolvedoxygen and chlorophyll fluorescence (Seapoints chloro-phyll fluorometer) were taken with a SeaBirds 911+Carrousel system. Water samples were collectedfrom several depths using 5-l Niskin bottles for labora-tory analysis of plankton and nutrients. Several watersamples were stored and analyzed for salinity witha Guildlines 8400B Salinometer at the laboratory afterthe end of the cruise. The samples showed no significantdrift in the temperature and conductivity from thesensors.

Vertical profiles of the photosynthetically active radia-tion (PAR) were taken at most stations by a LICORs

spherical quantum sensor. A LICORs flat quantum sensorwas placed on the ship’s mast for monitoring of theincident PAR radiation, which was recorded on a datalogger (LI-1400 model).

2.2. Phytoplankton identification

Samples for phytoplankton counting and identification,collected from the surface, were fixed with alkaline lugol’ssolution (Utermohl, 1958) for later microscope examina-tion. At the laboratory, 2–10 ml sub-samples were settledin Uthermohl chambers and analyzed using a Zeisss

Axiovert inverted microscope, at 200� , 400� and1000� magnifications. For coccolithophorid identifica-tion, samples were gently filtered through Isopore filtersmounted on top of Whatmans GF/C filters. Cell examina-tion was made on a LEO 1450VP scanning electronmicroscope (SEM) at the National Oceanography Centre,Southampton.

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2.3. Phytoplankton pigment analysis

Discrete samples for chlorophyll-a determination werecollected from the surface and selected depths based onthe fluorescence profile and filtered onto Whatmans GF/Ffilters, which were kept frozen in liquid nitrogen untilanalyzed. At the laboratory, the pigment was extracted in90% acetone and fluorescence determined in a TurnerDesigns TD-700 fluorometer (previously calibrated withSigmas chlorophyll-a standards), following the non-acidification method of Welschmeyer (1994). Watercolumn integrated chlorophyll (mg m�2) was calculatedby fitting a Gauss curve to the discrete chlorophyllmeasurements (Platt et al., 1994) and integrating overdepth to the 0.1% surface irradiance level.

2.4. Primary production measurements

Simulated in situ primary production measurementswere carried out at four stations along the shelf-break bythe 14C technique (Steemann, 1952). Water samples werecollected from 5 m depth (representing the mixed layer)and from chlorophyll subsurface peaks for P� I experi-ments at six irradiance levels (in triplicate). Sub-samplesof 50 ml were dispensed in polystyrene flasks andinoculated with 10 mCi of 14C-sodium bicarbonate. Duringincubation (4–6 h) irradiances in the sample flasks wereequivalent to 100% (no mesh), 75%, 47%, 28%, 14%, 5.5%(and one dark treatment) of incident light. After incuba-tion, samples were filtered through 25 mm WhatmanGF/F filters and washed with the same volume of filteredseawater and these were kept frozen until laboratoryanalysis. Small (200 ml) sub-samples were taken fromthe sample flasks after inoculation to check for theadded radioactivity. Sub-samples and filters were thenprocessed following the procedure described by Parsonset al. (1984).

Photosynthetic parameters (Pmax, alpha, beta) wereestimated from the P� I measurements by fitting a modelto the data (Platt et al., 1980). Water column production(mg C m�2 h�1) was estimated by applying the photosyn-thetic parameters to irradiance values in the watercolumn, based on PAR incident irradiance and attenuationcoefficient. Daily primary productivity (mg C m�2 day�1)was then calculated by integrating hourly production overthe daylight hours, based on the surface incident PARmeasurements.

2.5. Nutrient analyses

Water samples for dissolved inorganic nutrients (ni-trate, nitrite, ammonium, phosphate and silicate) werecollected at all stations from the surface and selecteddepths using Niskin bottles and filtered through celluloseacetate membrane filters. Nutrients were analyzed onboard ship, following the processing recommendations inStrickland and Parsons (1972). Ammonium was measuredby the method of Koroleff (1969) following modificationsin Grasshoff et al. (1983) and absorbance readings at630 nm. Nitrite and nitrate concentrations were measured

according to Strickland and Parsons (1972). Orthopho-sphate was measured by reaction with ammoniummolybdate and absorption reading at 885 nm. Silicate inthe form of reactive Si was measured according toStrickland and Parsons (1972) and correction for sea saltinterference made following Aminot and Chaussepied(1983). Absorbance values for all nutrients were measuredin a FEMTOs spectrophotometer.

2.6. Physical parameter calculations

The potential temperature and salinity data obtainedfrom the CTD measurements were used to calculatepotential density and the stability parameter (E). Thelatter, a measure of water column stability, is proportionalto the buoyancy (or Brunt-Vaisala) frequency (N2) anddefined by:

N2¼ �

g

rqrqz

rad2 s�2� �

leading to E ¼N2

g10�8rad2 m�1� �

,

where g is gravity and r is the water density. In this study,E was used to determine the vertical profile of watercolumn stratification.

3. Results

3.1. Physical setting

The T/S diagram for all stations occupied during thecruise (Fig. 2A) shows the presence of subantarctic shelfwaters (marked as shallow stations) and MC waters(mainly at Stn. 10). Stn. 11 represents a transition betweenthose two water types. Temperature and salinity variedfrom 2.75 to 8.87 1C and from 32.13 to 34.39, respectively,in the sampled region. Apparently, bottom waters on thePatagonia outer shelf originate from the MC (see dashedcircle in Fig. 2A). The upper column of MC subantarcticwaters (Stn. 10) is colder (and more saline) thanPatagonian shelf-break waters (Fig. 2A). The cross-shelfsection collected in region 3 (Stns. 10–14; Fig. 2B) revealsthe offshore isotherm shoaling associated with the MCaxis. Note that the temperature profile at Stn. 10 (offshore)is distinct from the other stations in that transect,suggesting intense mixing and weaker vertical stratifica-tion in the upper 30 m of the water column.

3.2. Nutrient distribution at the shelf-break front

The distributions of dissolved inorganic nitrogen (DIN,comprising nitrate, nitrite and ammonium) and phos-phate in the four sampling regions are shown in Fig. 3A.Surface nutrient values can be seen in Table 1. High valuesof DIN were observed below 50 m (415mM), decreasingsharply towards the surface (Fig. 3A). Exceptions wereStns. 10 and 11 (region 3), where the large stocks ofnutrients in surface layers suggest they are not consumedby phytoplankton. Ammonium constituted an importantfraction of dissolved inorganic nitrogen, indicating

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Fig. 2. (A) T/S diagrams (temperature, 1C, and salinity) of all the cruise

stations. T/S of Stns. 10 and 11 (eastern most stations at Region 3) are

marked on the graph. (B) Upper layer vertical profiles of temperature at

Stns. 14 (shelf) through 10 (offshore), of Region 3 (cross-shelf). Station

numbers are marked on respective profiles.


significant recycling at the shelf-break front. Averagesurface ammonium fraction at the front (excluding Stns.10, 11 and 14) was 13.5% and considering the upper 50 mdecreased to 8.2%. However, overall ammonium concen-tration in the upper 50 m was not large (from 0.08 mM atsurface, Stn. 19 to 0.87mM at surface, Stn. 13). Phosphate inthe upper 25 m was very low, with values o0.2mM insurface waters (Fig. 3A). Distributions of silicate anddensity (sigma–y) are shown in Fig. 3B. Si values at thesurface varied from 0.9 mM (Stn. 13) to 3.9 mM (Stn. 10),increasing with depth, in a similar pattern as density.

The relationships between macronutrients and tem-perature are shown in Fig. 4. The close associations with

temperature indicate that cold deep waters are a source ofnutrients to the frontal system. Silicate was better relatedwith temperature through an exponential function,indicating a steeper decrease of this nutrient towardsthe surface. This may reflect differences in uptake orrecycling dynamics between nitrogen and silica in thewater column. Ratios of Si:N were highly variable in the0–50 m water column (mean 0.870.93) but wereconsistently o0.5 between 50 and 500 m, confirming thatthe Subantarctic Water source is relatively Si-depleted,as has been shown for the ACC waters north of thePolar Front (e.g. Brzezinski et al., 2001; Pondaven et al.,1999).

High N:P ratios were observed in most samples (meansurface N:P ¼ 44), away from the ‘‘Redfield ratio’’ of 16:1(Redfield et al., 1963). These high N:P ratios, coupled withlow observed phosphate levels, suggest that phosphoruscould have limited phytoplankton growth at some sites.However, recent studies (Klausmeier et al., 2004; Arrigo,2005) have shown that higher N:P ratios (430) can beadequate to phytoplankton species that are able to sustaingrowth under resource limitation.

3.3. Chlorophyll-a, phytoplankton groups and

primary production

Chlorophyll-a (equivalent to phytoplankton biomass)was particularly high in the upper 50 m (Fig. 5), withsurface values ranging from 1.8 mg m�3 (Stn. 11) to19.9 mg m�3 (Stn. 19). The lowest values (o2 mg m�3)were measured at both Stns. 10 and 11, located at thecross-shelf-break transect in region 3. Chlorophyll dis-tribution at this location shows a marked lateral gradientfrom Stn. 11 to Stn. 13, where the high biomass (412 mgm�3) is associated with the shelf-break front.

Chlorophyll concentration was positively correlatedwith dissolved oxygen saturation (Fig. 6A; po0.001),suggesting that the biological processes are important ingas exchange dynamics in the region. This correlationis also illustrated in Fig. 6B, where vertical profilesof fluorescence, dissolved oxygen and chlorophyll areplotted.

Fig. 7A shows the abundance of the main phytoplank-ton groups along the high chlorophyll band (excludingStns. 10, 11 and 14). Total cell abundance closely followedchlorophyll concentration (thick black line in Fig. 7A). Thephytoplankton community was numerically mainly com-prised of small-size diatoms (2–10 mm), followed by nano-phyto-flagellates (o20 mm) and a small contribution oflarge dinoflagellates. Although the abundance of dino-flagellates was very small, their calculated carbon biomassexceeded that of the other groups (Souza and Garcia, inpreparation). The diatom community was dominated byspecies of the genus Thallasiosira. Only a few cells of thecoccolithophorid Emiliania huxleyi were detected amongthe phytoplankton community (Fig. 7B). The distributionof the main phytoplankton groups in region 3 is shown inFig. 8. While diatoms were most abundant in thephytoplankton community associated with the shelf andshelf-break front, at Stn. 10, east of the front, thecommunity was dominated by very small (2–5mm)

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Fig. 3. (A) Left panels: Positions of stations in each sampling region at the Patagonian shelf-break. Middle and right panels: Water column distribution of

dissolved inorganic nitrogen (nitrate+nitrite+ammonium), mM, and phosphate (mM), respectively, in the corresponding regions. Station numbers are

marked on top of each graph. (B) Left panels: Positions of stations in each sampling region at the Patagonian shelf-break. Middle and right panels: Water

column distribution of silicate (mM) and density (kg m�3), respectively, in the corresponding regions. Station numbers are marked on top of each graph.


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Fig. 3. (Continued)


phyto-flagellates, represented mainly by Phaeocystis cf.antarctica. Unfortunately, samples for phytoplanktoncounting were not collected at Stn. 11.

Primary production rates determined by the 14Ctechnique at four stations along the Patagonian shelf-break(see Fig. 1) are shown in Table 1, together with surface

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Table 1Values of water column integrated chlorophyll-a and primary production (at four stations) and surface water chemical properties at all stations along the

Patagonian shelf-break in November 2004

Stn. Day in

November

Position Surface NO3

(mM)

Surface PO4

(mM)

Surface SiO4

(mM)

Surface Chla

(mg m�3)

Integrated Chla

(mg m�2)

Integrated primary production

(g C m�2 d�1)

01 03 40.0971S,

56.2001W

6.08 0.30 3.37 3.23 335 3.24

02 03 40.3581S,

56.3701W

3.82 UDL 2.62 6.43 306 –

03 03 40.5671S,

56.5821W

3.70 UDL 2.20 11.29 597 –

04 03 40.8871S,

57.0531W

1.01 UDL 1.93 11.28 672 –

05 04 41.8401S,

57.7771W

0.82 0.12 3.16 12.40 1074 –

06 04 42.0151S,

57.9901W

0.65 0.02 1.50 13.63 893 7.79

07 04 42.2721S,

58.2721W

3.50 0.25 1.87 9.11 767 –

08 04 42.4181S,

58.5431W

4.68 0.07 1.61 8.57 681 –

09 04 42.7121S,

58.7871W

1.05 UDL 1.34 4.71 829 –

10 05 44.5401S,

59.3171W

16.22 0.35 3.96 2.00 90.4 –

11 05 44.5581S,

59.7731W

12.90 0.40 1.29 1.81 108 –

12 05 44.5381S,

59.9001W

3.87 0.07 1.07 10.67 358 1.96

13 05 44.5201S,

59.9371W

2.55 0.07 0.91 12.99 754 –

14 05 44.5171S,

60.0981W

0.80 0.15 3.21 7.94 614 –

15 06 46.8581S,

60.5371W

2.57 0.02 3.00 8.10 961 –

16 06 47.2431S,

60.6231W

4.21 0.12 3.27 5.93 378 2.08

17 06 47.4131S,

60.7781W

1.44 0.02 2.57 12.53 955 –

18 06 47.7921S,

60.8381W

0.70 0.10 2.95 16.49 727 –

19 06 48.0301S,

60.8271W

0.75 0.07 2.57 19.93 815 –

Average 3.75 0.11 2.34 9.49 627 3.77

Mean surface incident irradiance over the period of primary production experiments were 1323, 1407, 1255 and 1760mmol m�2 s�1 at Stns. 01, 06, 12 and

16, respectively (UDL: under detection limit).


nutrient levels. Integrated primary production rates variedfrom 1.96 g C m�2 d�1 at Stn. 12 to 7.79 g C m�2 d�1 at Stn. 6.At the latter station, production was particularly high,partly because of the elevated phytoplankton biomass(893 mg chla m�2, as compared to 358 mg chla m�2 at Stn.12). Phytoplankton growth at this location must haveconsumed most nutrients in surface waters, resulting in thelowest nitrate levels (0.65mM) (Table 1).

4. Discussion

Several recent studies have described the seasonalcycle of phytoplankton concentration at the Patagonianshelf-break from analysis of ocean color sensors (Garciaet al., 2004; Rivas, 2006; Rivas et al., 2006; Romero et al.,2006; Saraceno et al., 2005; Signorini et al., 2006).Although the high chlorophyll band presents important

interannual variability in the bloom intensity (meanchlorophyll concentration) (Signorini et al., 2006),its location is stable (Romero et al., 2006) because theshelf-break front is bottom trapped (Saraceno et al.,2004). Due to the high latitudinal range of the frontalregion, there is a marked difference in timing of the springbloom initiation (Rivas et al., 2006), mainly following thenorth–south progression of water column stabilizationtriggered by changes in the surface heat fluxes. On average,while in the northern area (39–401S) the blooms start inmid August (Rivas et al., 2006; Saraceno et al., 2005)further south (50–551S) the blooms begin in September(Rivas et al., 2006). According to these investigations,peaks in chlorophyll over the shelf-break appear inOctober–November. Therefore, the timing of our cruise(beginning of November) likely represents the peak inphytoplankton biomass in the region, especially in thesouthern area.

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Fig. 4. Relationship between water temperature and macronutrients at

the Patagonian shelf-break: dissolved inorganic nitrogen, DIN (nitrate+

nitrite+ammonium) (top), phosphate (middle), and silicate (bottom).


4.1. Role of macro- and micro-nutrients during the shelf-

break spring bloom

Nutrient supply at the shelf-break front is probablyassociated with the convergence flow and bottom friction,generating a pressure gradient along the shelf, resulting inupwelling along the front (Matano and Palma, 2008).Upwelling processes associated with shelf-break frontsare also observed in the North Atlantic (e.g. Loder et al.,1998; Allen et al., 2005), although the mechanismsleading to upwelling along the front can be different(Matano and Palma, 2008). It has also been suggested thatthe topography of the Patagonian shelf-break promotesmesoscale activity and generation of eddies which, inturn, supply nutrients to maintain the phytoplanktonblooms (Longhurst, 1998). In this work, the arrangementof density isolines in region 3 (Fig. 3B) does suggest

upwelling occurred during our field sampling. In addition,the nutrient distributions at that transect (Fig. 3A and B)and the strong relationship between temperature andnutrients (Fig. 4) are also an indication of upwellingassociated with MC subsurface waters. Similar cross-shelf-break structures at other latitudes have beenreported by Piola and Gordon (1989), Peterson andWhitworth (1989) and Romero et al. (2006).

In surface waters, nutrient levels closely respondedto phytoplankton biomass concentration, as seen inthe inverse relationship between dissolved inorganicnitrogen (DIN) and chlorophyll-a (Fig. 9). The highestnutrient levels (Stns. 10 and 11) are associated with thelowest chlorophyll concentration. The inverse chlorophyll-a versus nutrient relationship leads to the stronghorizontal gradient in near-surface DIN, observed inregion 3, varying from 16.6 mM at Stn. 10 (offshore) to0.99 mM at Stn. 14 (shelf). A similar nitrate gradient fromcoastal waters (o2 mM) to the shelf-break (420mM) wasfound by Carreto et al. (1995) at �391S in October/November 1987 and 1988. Macronutrients are apparentlysupplied by upwelling, while phytoplankton growthtightly controls the nutrient levels at the Patagonianshelf-break front. Processes associated with the lowchlorophyll at both Stns. 10 and 11 will be addressed inthe next sections.

In addition to macronutrients, iron availability mayalso play an important role in determining phytoplanktongrowth at the shelf-break. The surface waters of the MCare probably Fe-depleted, since the upper layers of theAntarctic Circumpolar Current are known to be ironpoor (Loscher et al., 1997). Although there have beenindications of an enhanced supply of trace metals byatmospheric dust input along the Patagonian coast(Erickson et al., 2003; Gaiero et al., 2003; Gasso andStein, 2007), bio-availability of iron has not yet beendetermined in waters of the shelf-break front, whichis located approximately 200–400 km from shore.Therefore, metal upwelling along the front cannot beruled out as an important iron source to the bloom, whichwould sharply decrease towards the open ocean. Inaddition, shelf waters might also be an important sourceof iron in this region. For instance, further south, at ashallow shelf site, east of Malvinas Island, enhancediron concentrations (up to 6 nM) were found both insurface waters and near the sediments (Bowie et al.,2002). Strong tidal mixing described for the region(Palma et al., 2004) and sediment ressuspension probablyenhance Fe concentration in the shelf waters, providing anadditional supply of this element to the shelf-breakregion. In this work, an indication of this process isshown by the distribution of silicate in the cross-shelf transect (Fig. 10), where higher levels of Si areassociated with lower salinity, mid-shelf waters. Thisfeature has been consistently observed during two otherspring cruises to the region (R. Pollery, personal commu-nication). Therefore, it is reasonable to suggest that shelfwaters can also be an important source of metals to theshelf-break.

Recent field studies along the Patos-Mirim lagoonsystem (30.5–32.51S) (Windom et al., 2006) have

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Fig. 5. Vertical distribution of chlorophyll-a (mg m�3) in the four regions at the shelf-break front, shown on the left panels (3–6 November 2004).


suggested that submarine ground water discharge can bean important source of dissolved iron to the South AtlanticOcean. It is suggested that the iron flux from these lagoonscould be transported by the Brazil Current and reach the

waters of the Brazil-Malvinas Confluence, including theshelf-break region south of 381S.

In summary, we propose that nutrient supply formaintaining phytoplankton blooms in the study region,

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Fig. 6. (A) Relationship between oxygen saturation (%) and chlorophyll-a (N ¼ 79). (B) Vertical profiles of dissolved oxygen, mg l�1 (squares), fluorescence,

relative units (dots) and measured chlorophyll-a, mg m�3 (triangles) at Stn. 2 (left) and Stn. 3 (right). The fluorometer readings were scaled (internal

calibration) to approximately match chlorophyll units.


particularly in spring, is provided by a combination ofmacronutrient availability from the rich MC, enhanced byupwelling along the front, and micronutrient (mainly

iron), potentially supplied from four sources: upwelling,shallow shelf water, dust deposition and ground waterfrom remote regions.

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Fig. 7. (A) Surface chlorophyll-a (thick line) and abundance (106 organisms l�1) of main phytoplankton groups (diatoms, nanoflagellates and

dinoflagellates) along the high chlorophyll band. (B) Photomicrographs of diatoms (1–3, light microscopy), dinoflagellates (4–6, light microscopy)

diatoms (7, scanning electron microscope—SEM) and Emiliania huxleyi (8 and 9, SEM). 1: Thallasiosira sp.; 2: Thallasiosira cf. weissflogii; 3: Eucampia sp.; 4:

Gymnodinium sp.; 5: Gyrodinium sp.; 6: Ceratium sp.; 7: Thallasiosira cf. australis; 8 and 9: Emiliania huxleyi. Scale bars are 10mm (1–6) and 1 mm (7–9).


4.2. Water column stability

Physical factors, such as water column stability, prob-ably play an important role in sustaining the phytoplank-ton cells in the euphotic layer along the shelf-break front,as previously suggested (Podesta, 1990). The onset ofvertical stability is important for triggering spring bloomsin temperate latitudes, when nutrients are available from

the previous winter, but light is limiting by deep mixedlayers (Sverdrup, 1953). However, strong and persistentstability, especially in summer, has a negative impact onphytoplankton growth because it acts as a barrier forupward nutrient input from below the nutricline tothe nutrient-exhausted surface layers. At almost allstations sampled in this study, the water column waswell stratified (mean stability index between 0 and 50 m

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Fig. 8. Relative abundance in terms of cell numbers of phytoplankton groups in Region 3. Diat: diatoms; Dinof: dinoflagellates; Flag: nano-flagellates.

Note the dominance of nano flagellates (mainly Phaeocystis sp.) at Stn. 10, associated with low chlorophyll values. NA: data not available at Stn. 11.

Fig. 9. Relationship between surface dissolved inorganic nitrogen (mM) and chlorophyll-a (mg m�3) at all stations in the study region.


was from 220�10�8 to 740�10�8 rad2 m�1). An exceptionwas Stn. 10 (most offshore station) with a value ofo100 rad2 m�1

�10�8. This could partially explain thelow chlorophyll found at this site. Fig. 11 shows thestability index and surface chlorophyll-a along the cross-shelf transect (region 3). Surface chlorophyll is highest overmore stable waters (Stns. 12 and 13), implying that lightcould have been a limiting factor within the more turbulentMC waters (Stn. 10). This is in agreement with thedominance of the genus Phaeocystis at this station, whichhas been suggested to have a competitive advantage overdiatoms under high-nutrient, low-light and deep-mixingconditions (Cota et al., 1994; Hegarty and Villareal, 1998;Moisan and Mitchell, 1999).

Another factor associated with the transport dynamicsof the western boundary current is loss of phytoplanktoncells by advection, particularly at Stns. 10 and 11. Duringsampling of those two stations, the vessel drifted north-eastward at 43 knots (�150 cm s�1), which indicates ahigh-velocity jet, capable of ‘‘washing-away’’ phytoplank-ton cells downstream.

4.3. Possible grazing control on biomass levels

Apart from chemical and physical forcing onphytoplankton biomass and production, biological pro-cesses such as grazing pressure can play an importantrole in controlling biomass accumulations. Therefore, an

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Fig. 10. Surface salinity (dashed line) and silicate concentration (mM) at the surface (circles), 5 m (filled square) and 15 m (triangle) in region 3

(Stns. 10–14).

Fig. 11. Surface chlorophyll-a (circle+line) and mean water stability (E) in the top 50 m (10�8 rad2 m�1) (triangle+dashed line) across the shelf-break

(region 3).


alternative explanation for the low phytoplankton bio-mass found particularly at Stn. 11, where macronutrientsare available in a stratified water column, is grazingpressure. This hypothesis is supported by the verticaldistributions of macronutrients at this site (Fig. 12). Anindication of strong grazing pressure at Stn. 11 is thedistinctly higher concentrations of ammonium (Fig. 12A),a common excretion product of zooplankton. In addition,silicate concentrations at Stn. 11 are not distinct fromthose at the other stations along the shelf-break (Fig. 12B),indicating a similar level of utilization of this nutrient, andimplying previous diatom growth. Unfortunately, confir-mation of the phytoplankton assemblage could not bemade at this particular station, as no samples wereavailable. The low Si concentration at Stn. 11 is in contrast

with that at Stn. 10, which stands out with the highest Silevels. Therefore, both Stns. 10 and 11 presented relativelylow phytoplankton biomass (o2 mg m�3), but Stn. 11showed an apparent previous Si utilization. These lowsilicate concentrations at Stn. 11 (1.3mM at surface) werein contrast with high nitrate levels (surface DIN ¼ 14.4mM), a condition similar to that described for silicatecontrolled environments (Dugdale et al., 1995). This ‘‘silicapump’’ condition is driven by both a faster sinking and aslower recycling rate of Si (particularly in cold waters) ascompared to nitrogen. This process is particularly en-hanced by grazing, whereby Si-enriched zooplankton fecalpellets increase silicon sinking rates, resulting in rapidloss of silicate from the euphotic layer, while nitrogen isregenerated faster in the grazing cycle (Dugdale et al.,

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Fig. 12. Vertical profiles of ammonium (A) and silicate (B) at all cruise

stations. Profiles of Stn. 10 (line+circles) and 11 (line+triangles) are

highlighted. The insets show vertical profiles of the respective nutrients

in region 3 (cross-shelf).


1995; Pondaven et al., 1999). The higher levels ofammonium generated in the process are a knownpreferable nitrogen source for phytoplankton, leading toaccumulation of nitrate in the euphotic zone, as observedin this study. Therefore, at least some areas of the studyregion (and based on the generally low Si:N ratios) seemto function as a ‘‘silica pump’’, as observed at Stn. 11.

4.4. The phytoplankton community and primary

production rates

The seasonal dynamics of phytoplankton groups in theregion have been studied based on a time-series ofSeaWiFS chlorophyll (OC4v4) and calcite concentrations(Signorini et al., 2006). The study suggests that inDecember coccolithophorids begin to dominate the waterspectral signature at the shelf-break, after the springdiatom blooms. Data from the present work confirm theimportant role of diatoms in the phytoplankton commu-nity at the Patagonian shelf-break in spring, associatedwith high chlorophyll-a concentrations (2–20 mg m�3 atsurface). However, as stated above, dinoflagellates werealso important components of the biomass because oftheir generally greater size. Although the dynamics of

phytoplankton succession cannot be depicted from thiswork, the presence of fast growing small-size diatoms, therelative importance of large dinoflagellates and the lownutrient levels in the surface layers indicate an early tointermediate stage in succession (Margalef, 1962). Lowcell densities of the coccolithophorid E. huxleyi were foundamong the dominating centric diatoms and flagellates.This small E. huxleyi population likely represents theinoculum for the subsequent coccolithophorid bloomdevelopment, as suggested in ocean color studies (e.g.Brown and Podesta, 1997; Signorini et al., 2006). In fact,the presence of coccolithophorids in early summer hasrecently been confirmed by in situ surveys carried out inJanuary 2008 over a large patch of high reflectance locatedover the mid shelf (Garcia, VMT, in preparation).

These two types of communities (diatoms and cocco-lithophorids) represent different key functional groups ofphytoplankton (Doney, 1999; Moore et al., 2002) andtherefore play different roles in the food web structureand in the air–sea CO2 exchange dynamics. While diatomsare normally associated with high production rates andelevated organic matter export flux (Buesseler, 1998;Sarthou et al., 2005), coccolithophorids can have animpact on CO2 partial pressure in surface waters, byincreasing this gas during CaCO3 platelet formation(Holligan et al., 1993; Rost and Riebesell, 2004). Therefore,the alternation of dominance between the two groups indifferent seasons may result in significant changes in theCO2 exchange dynamics in the region.

Primary production rates measured in this work variedfrom approximately 2–8 g C m�2 d�1. The high magnitudesof photosynthesis caused dissolved oxygen to vary closelywith phytoplankton biomass, as seen in Fig. 6. Rates ofprimary production during a dinoflagellate bloom in thevicinity of the shelf-break at 391S were in the range0.1–2.7 g C m�2 d�1 (Negri et al., 1992), somewhat lowerthan the values found in the present work. The highprimary production rates in the present work arecomparable with maximal seasonal productivity ateastern boundary current systems such as California,Peru-Chile (Humboldt), Canary and Benguela Currents.Large-scale primary production in those systems has beenestimated between 2 and 6 g C m�2 d�1 (Carr and Kearns,2003), similar to those found in this work.

The large bloom extent at the Patagonian shelf-break(approximately 55,000 km2 patch of 42 mg m�3 chloro-phyll patch in November 2004) and the associatedprimary production rates may significantly impact oceancarbon uptake in the region. In fact, high sea–air partialpressure differences (Dp CO2) into the ocean (maximum�110 matm) have been found for this region in latesummer (Bianchi et al., 2005). Recent Dp CO2 estimatesat the shelf-break between 39 and 501S based on severalcruises conducted in spring range between �40 and�200 matm (Bianchi et al., 2008). Similarly, measurementsof CO2 fluxes along the same cruise track as the presentwork, in spring 2006, have also shown a conspicuousnegative Dp CO2 flux (�56.2 to �150 matm) associatedwith the shelf-break bloom (Ito et al., in preparation).Furthermore, CO2 fluxes on the Patagonian shelf werefound to be well related to chlorophyll levels when the

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phytoplankton community is dominated by diatoms(Schloss et al., 2007), as opposed to dominance by nano-flagellates. Therefore, data on biomass, primary produc-tion and community composition (dominance by diatoms)in the present study suggest that biological activity play asignificant role in CO2 dynamics in the region.

Results of the present work have shown that the springphytoplankton blooms at the Patagonia shelf-break areassociated with high primary production rates, compar-able with very productive areas of the world oceans. Theblooms are sustained by nutrient supply from the MCupwelling and are maintained in the upper layers (mainlyabove 50 m) by vertical stability. The elevated biomasslevels (2–17 mg m�3 surface chlorophyll) are associatedmainly with diatoms and dinoflagellates and apparentlycontrolled by mixing and grazing pressure.

Acknowledgments

The Patagonian Experiment (PATEX) is a multidisci-plinary project as part of GOAL (Group of High LatitudeOceanography) activities in the Brazilian Antarctic Pro-gram. We thank the crew of the Brazilian Navy researchship ‘‘Ary Rongel’’ for their assistance during the fieldsampling. The project was sponsored through thefunding resources of CNPq (Brazilian National Councilon Research and Development) and MMA (Ministryof Environment) to the Brazilian Antarctic Program(PROANTAR) through grant 550370/02-1. Ocean colorimages were provided by and processed at the GSFC(Goddard Space Flight Center). A.R.P. acknowledges thesupport of the Inter-American Institute for Global ChangeResearch (Grant CRN2076), which is financed by theUS National Science Foundation (Grant GEO-0452325).We are thankful for the constructive criticism ofthree anonymous reviewers, which greatly improved themanuscript.

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